Insights into the key roles of proteoglycans in breast cancer biology and translational medicine

Biochimica et Biophysica Acta - Reviews on Cancer

Volumn 1855, Issue 2, 2015, Pages 276-300

  Theocharis, Achilleas D ^a   Skandalis, Spyros S ^a   Neill, Thomas ^b   Multhaupt, Hinke A B ^c   Hubo, Mario ^d   Frey, Helena ^d   Gopal, Sandeep ^c   Gomes, Angélica ^c   Afratis, Nikos ^c   Lim, Hooi Ching ^c   Couchman, John R ^c   Filmus, Jorge ^e   Ralph D S , Sanderson ^f   Schaefer, Liliana ^d   Iozzo, Renato V ^b   Karamanos, Nikos K ^a  

^a UNIVERSITY OF PATRAS   (Greece)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d GOETHE UNIVERSITY   (Germany)

^e Sunnybrook Health Sciences Centre   (Canada)

^f University of Alabama at Birmingham   (United States)

Author keywords

Breast cancer; Decorin; Glypicans; Proteoglycans; Serglycin; Syndecans

Indexed keywords

ANTINEOPLASTIC AGENT; BIGLYCAN; BISPHOSPHONIC ACID DERIVATIVE; DECORIN; GLYPICAN; HEPARANASE; IMATINIB; ONCOPROTEIN; PG 545; PROTEOGLYCAN; RONEPARSTAT; SERGLYCIN; SYNDECAN; UNCLASSIFIED DRUG; VERSICAN; ZOLEDRONIC ACID;

AUTOPHAGY; BINDING AFFINITY; BREAST CANCER; CANCER CELL; CANCER PROGNOSIS; CANCER RADIOTHERAPY; CANCER SURVIVAL; CARCINOGENESIS; CELL ADHESION; CELL GROWTH; CELL MIGRATION; CELL SURVIVAL; DRUG EFFICACY; DRUG MECHANISM; ENDOTHELIUM CELL; EXOSOME; EXTRACELLULAR MATRIX; GLYCOSYLATION; HUMAN; METASTASIS; MITOPHAGY; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN METABOLISM; PROTEIN PHOSPHORYLATION; PROTEIN SECRETION; PROTEIN STRUCTURE; PROTEIN TARGETING; REVIEW; TUMOR MICROENVIRONMENT; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; BREAST TUMOR; FEMALE; GENE EXPRESSION REGULATION; GENETICS; MOLECULARLY TARGETED THERAPY; NEOVASCULARIZATION, PATHOLOGIC; PATHOLOGY; SIGNAL TRANSDUCTION; TRANSLATIONAL RESEARCH;

BREAST NEOPLASMS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MOLECULAR TARGETED THERAPY; NEOVASCULARIZATION, PATHOLOGIC; PROTEOGLYCANS; SIGNAL TRANSDUCTION; TRANSLATIONAL MEDICAL RESEARCH; TUMOR MICROENVIRONMENT;

EID: 84927546643     PISSN: 0304419X     EISSN: 18792561     Source Type: Journal    
DOI: 10.1016/j.bbcan.2015.03.006     Document Type: Review

References (372)

1. Allred D.C. Issues and updates: evaluating estrogen receptor-alpha, progesterone receptor, and HER2 in breast cancer. Mod. Pathol. 2010, 23(Suppl. 2):S52-S59.
2. Theocharis A.D., Gialeli C., Hascall V.C., Karamanos N.K. Extracellular matrix: a functional scaffold. Extracellular Matrix: Pathobiology and Signaling 2012, 3-19. Walter de Gruyter GmbH & Co. KG, Berlin/Boston. N.K. Karamanos (Ed.).
3. Theocharis A.D., Skandalis S.S., Tzanakakis G.N., Karamanos N.K. Proteoglycans in health and disease: novel roles for proteoglycans in malignancy and their pharmacological targeting. FEBS J. 2010, 277:3904-3923.
4. Vigetti D., Viola M., Karousou E., De Luca G., Passi A. Metabolic control of hyaluronan synthases. Matrix Biol. 2014, 35:8-13.
5. Afratis N., Gialeli C., Nikitovic D., Tsegenidis T., Karousou E., Theocharis A.D., Pavao M.S., Tzanakakis G.N., Karamanos N.K. Glycosaminoglycans: key players in cancer cell biology and treatment. FEBS J. 2012, 279:1177-1197.
6. Iozzo R.V. Matrix proteoglycans: from molecular design to cellular function. Annu. Rev. Biochem. 1998, 67:609-652.
7. Schaefer L., Schaefer R.M. Proteoglycans: from structural compounds to signaling molecules. Cell Tissue Res. 2010, 339:237-246.
8. Theocharis A.D., Gialeli C., Bouris P., Giannopoulou E., Skandalis S.S., Aletras A.J., Iozzo R.V., Karamanos N.K. Cell-matrix interactions: focus on proteoglycan-proteinase interplay and pharmacological targeting in cancer. FEBS J. 2014, 281:5023-5042.
9. Yan D., Lin X. Shaping morphogen gradients by proteoglycans. Cold Spring Harb. Perspect. Biol. 2009, 1:a002493.
10. Ferguson J.E., Schor A.M., Howell A., Ferguson M.W. Changes in the extracellular matrix of the normal human breast during the menstrual cycle. Cell Tissue Res. 1992, 268:167-177.
11. de Lima C.R., de Arimatea dos Santos Junior J., Nazario A.C., Michelacci Y.M. Changes in glycosaminoglycans and proteoglycans of normal breast and fibroadenoma during the menstrual cycle. Biochim. Biophys. Acta 2012, 1820:1009-1019.
12. Skandalis S.S., Kletsas D., Kyriakopoulou D., Stavropoulos M., Theocharis D.A. The greatly increased amounts of accumulated versican and decorin with specific post-translational modifications may be closely associated with the malignant phenotype of pancreatic cancer. Biochim. Biophys. Acta 2006, 1760:1217-1225.
13. Theocharis A.D., Vynios D.H., Papageorgakopoulou N., Skandalis S.S., Theocharis D.A. Altered content composition and structure of glycosaminoglycans and proteoglycans in gastric carcinoma. Int. J. Biochem. Cell Biol. 2003, 35:376-390.
14. Ricciardelli C., Brooks J.H., Suwiwat S., Sakko A.J., Mayne K., Raymond W.A., Seshadri R., LeBaron R.G., Horsfall D.J. Regulation of stromal versican expression by breast cancer cells and importance to relapse-free survival in patients with node-negative primary breast cancer. Clin. Cancer Res. Off. J. Am. Assoc. Cancer Res. 2002, 8:1054-1060.
15. Troup S., Njue C., Kliewer E.V., Parisien M., Roskelley C., Chakravarti S., Roughley P.J., Murphy L.C., Watson P.H. Reduced expression of the small leucine-rich proteoglycans, lumican, and decorin is associated with poor outcome in node-negative invasive breast cancer. Clin. Cancer Res. Off. J. Am. Assoc. Cancer Res. 2003, 9:207-214.
16. Skandalis S.S., Labropoulou V.T., Ravazoula P., Likaki-Karatza E., Dobra K., Kalofonos H.P., Karamanos N.K., Theocharis A.D. Versican but not decorin accumulation is related to malignancy in mammographically detected high density and malignant-appearing microcalcifications in non-palpable breast carcinomas. BMC Cancer 2011, 11:314.
17. Suwiwat S., Ricciardelli C., Tammi R., Tammi M., Auvinen P., Kosma V.M., LeBaron R.G., Raymond W.A., Tilley W.D., Horsfall D.J. Expression of extracellular matrix components versican, chondroitin sulfate, tenascin, and hyaluronan, and their association with disease outcome in node-negative breast cancer. Clin. Cancer Res. Off. J. Am. Assoc. Cancer Res. 2004, 10:2491-2498.
18. Prinz R.D., Willis C.M., Viloria-Petit A., Kluppel M. Elimination of breast tumor-associated chondroitin sulfate promotes metastasis. Genet. Mol. Res. 2011, 10:3901-3913.
19. Neill T., Painter H., Buraschi S., Owens R.T., Lisanti M.P., Schaefer L., Iozzo R.V. Decorin antagonizes the angiogenic network: concurrent inhibition of Met, hypoxia inducible factor 1alpha, vascular endothelial growth factor A, and induction of thrombospondin-1 and TIMP3. J. Biol. Chem. 2012, 287:5492-5506.
20. Neill T., Torres A., Buraschi S., Owens R.T., Hoek J.B., Baffa R., Iozzo R.V. Decorin induces mitophagy in breast carcinoma cells via peroxisome proliferator-activated receptor gamma coactivator-1alpha (PGC-1alpha) and mitostatin. J. Biol. Chem. 2014, 289:4952-4968.
21. Frey H., Schroeder N., Manon-Jensen T., Iozzo R.V., Schaefer L. Biological interplay between proteoglycans and their innate immune receptors in inflammation. FEBS J. 2013, 280:2165-2179.
22. Hsieh L.T., Nastase M.V., Zeng-Brouwers J., Iozzo R.V., Schaefer L. Soluble biglycan as a biomarker of inflammatory renal diseases. Int. J. Biochem. Cell Biol. 2014, 54:223-235.
23. Moreth K., Frey H., Hubo M., Zeng-Brouwers J., Nastase M.V., Hsieh L.T., Haceni R., Pfeilschifter J., Iozzo R.V., Schaefer L. Biglycan-triggered TLR-2- and TLR-4-signaling exacerbates the pathophysiology of ischemic acute kidney injury. Matrix Biol. 2014, 35:143-151.
24. Fernandez-Vega I., Garcia O., Crespo A., Castanon S., Menendez P., Astudillo A., Quiros L.M. Specific genes involved in synthesis and editing of heparan sulfate proteoglycans show altered expression patterns in breast cancer. BMC Cancer 2013, 13:24.
25. Iozzo R.V., Sanderson R.D. Proteoglycans in cancer biology, tumour microenvironment and angiogenesis. J. Cell. Mol. Med. 2011, 15:1013-1031.
26. Kousidou O., Berdiaki A., Kletsas D., Zafiropoulos A., Theocharis A.D., Tzanakakis G.N., Karamanos N.K. Estradiol-estrogen receptor: a key interplay of the expression of syndecan-2 and metalloproteinase-9 in breast cancer cells. Mol. Oncol. 2008, 2:223-232.
27. Skandalis S.S., Afratis N., Smirlaki G., Nikitovic D., Theocharis A.D., Tzanakakis G.N., Karamanos N.K. Cross-talk between estradiol receptor and EGFR/IGF-IR signaling pathways in estrogen-responsive breast cancers: focus on the role and impact of proteoglycans. Matrix Biol. 2014, 35:182-193.
28. Tsonis A.I., Afratis N., Gialeli C., Ellina M.I., Piperigkou Z., Skandalis S.S., Theocharis A.D., Tzanakakis G.N., Karamanos N.K. Evaluation of the coordinated actions of estrogen receptors with epidermal growth factor receptor and insulin-like growth factor receptor in the expression of cell surface heparan sulfate proteoglycans and cell motility in breast cancer cells. FEBS J. 2013, 280:2248-2259.
29. Lendorf M.E., Manon-Jensen T., Kronqvist P., Multhaupt H.A., Couchman J.R. Syndecan-1 and syndecan-4 are independent indicators in breast carcinoma. J. Histochem. Cytochem. 2011, 59:615-629.
30. Lim H.C., Couchman J.R. Syndecan-2 regulation of morphology in breast carcinoma cells is dependent on RhoGTPases. Biochim. Biophys. Acta 2014, 1840:2482-2490.
31. Ramani V.C., Purushothaman A., Stewart M.D., Thompson C.A., Vlodavsky I., Au J.L., Sanderson R.D. The heparanase/syndecan-1 axis in cancer: mechanisms and therapies. FEBS J. 2013, 280:2294-2306.
32. Sanderson R.D., Couchman J.R. Targeting syndecan shedding in cancer. Extracellular Matrix: Pathobiology and Signaling 2012, 802-812. de Gruyter GmbH. N.K. Karamanos (Ed.).
33. Korpetinou A., Skandalis S.S., Moustakas A., Happonen K.E., Tveit H., Prydz K., Labropoulou V.T., Giannopoulou E., Kalofonos H.P., Blom A.M., Karamanos N.K., Theocharis A.D. Serglycin is implicated in the promotion of aggressive phenotype of breast cancer cells. PLoS One 2013, 8:e78157.
34. Theocharis A.D. Versican in health and disease. Connect. Tissue Res. 2008, 49:230-234.
35. Labropoulou V.T., Theocharis A.D., Ravazoula P., Perimenis P., Hjerpe A., Karamanos N.K., Kalofonos H.P. Versican but not decorin accumulation is related to metastatic potential and neovascularization in testicular germ cell tumours. Histopathology 2006, 49:582-593.
36. Kischel P., Waltregny D., Dumont B., Turtoi A., Greffe Y., Kirsch S., De Pauw E., Castronovo V. Versican overexpression in human breast cancer lesions: known and new isoforms for stromal tumor targeting. Int. J. Cancer 2010, 126:640-650.
37. Skandalis S.S., Theocharis A.D., Papageorgakopoulou N., Vynios D.H., Theocharis D.A. The increased accumulation of structurally modified versican and decorin is related with the progression of laryngeal cancer. Biochimie 2006, 88:1135-1143.
38. Theocharis A.D. Human colon adenocarcinoma is associated with specific post-translational modifications of versican and decorin. Biochim. Biophys. Acta 2002, 1588:165-172.
39. Tsara M.E., Theocharis A.D., Theocharis D.A. Compositional and structural alterations of proteoglycans in human rectum carcinoma with special reference to versican and decorin. Anticancer Res 2002, 22:2893-2898.
40. Tian Y., Esteva F.J., Song J., Zhang H. Altered expression of sialylated glycoproteins in breast cancer using hydrazide chemistry and mass spectrometry. Mol. Cell. Proteomics 2012, 11. (M111 011403).
41. Nikitovic D., Zafiropoulos A., Katonis P., Tsatsakis A., Theocharis A.D., Karamanos N.K., Tzanakakis G.N. Transforming growth factor-beta as a key molecule triggering the expression of versican isoforms v0 and v1, hyaluronan synthase-2 and synthesis of hyaluronan in malignant osteosarcoma cells. IUBMB Life 2006, 58:47-53.
42. Yeung T.L., Leung C.S., Wong K.K., Samimi G., Thompson M.S., Liu J., Zaid T.M., Ghosh S., Birrer M.J., Mok S.C. TGF-beta modulates ovarian cancer invasion by upregulating CAF-derived versican in the tumor microenvironment. Cancer Res. 2013, 73:5016-5028.
43. Dondeti V.R., Wubbenhorst B., Lal P., Gordan J.D., D'Andrea K., Attiyeh E.F., Simon M.C., Nathanson K.L. Integrative genomic analyses of sporadic clear cell renal cell carcinoma define disease subtypes and potential new therapeutic targets. Cancer Res. 2012, 72:112-121.
44. Keire P.A., Bressler S.L., Lemire J.M., Edris B., Rubin B.P., Rahmani M., McManus B.M., van de Rijn M., Wight T.N. A role for versican in the development of leiomyosarcoma. J. Biol. Chem. 2014, 289:34089-34103.
45. Wasa J., Nishida Y., Shinomura T., Isogai Z., Futamura N., Urakawa H., Arai E., Kozawa E., Tsukushi S., Ishiguro N. Versican V1 isoform regulates cell-associated matrix formation and cell behavior differentially from aggrecan in Swarm rat chondrosarcoma cells. Int. J. Cancer 2012, 130:2271-2281.
46. Havre P.A., Dang L.H., Ohnuma K., Iwata S., Morimoto C., Dang N.H. CD26 expression on T-anaplastic large cell lymphoma (ALCL) line Karpas 299 is associated with increased expression of versican and MT1-MMP and enhanced adhesion. BMC Cancer 2013, 13:517.
47. Gao D., Joshi N., Choi H., Ryu S., Hahn M., Catena R., Sadik H., Argani P., Wagner P., Vahdat L.T., Port J.L., Stiles B., Sukumar S., Altorki N.K., Rafii S., Mittal V. Myeloid progenitor cells in the premetastatic lung promote metastases by inducing mesenchymal to epithelial transition. Cancer Res. 2012, 72:1384-1394.
48. Kim S., Takahashi H., Lin W.W., Descargues P., Grivennikov S., Kim Y., Luo J.L., Karin M. Carcinoma-produced factors activate myeloid cells through TLR2 to stimulate metastasis. Nature 2009, 457:102-106.
49. Li D., Wang X., Wu J.L., Quan W.Q., Ma L., Yang F., Wu K.Y., Wan H.Y. Tumor-produced versican V1 enhances hCAP18/LL-37 expression in macrophages through activation of TLR2 and vitamin D3 signaling to promote ovarian cancer progression in vitro. PLoS One 2013, 8:e56616.
50. Scheeren F.A., Kuo A.H., van Weele L.J., Cai S., Glykofridis I., Sikandar S.S., Zabala M., Qian D., Lam J.S., Johnston D., Volkmer J.P., Sahoo D., van de Rijn M., Dirbas F.M., Somlo G., Kalisky T., Rothenberg M.E., Quake S.R., Clarke M.F. A cell-intrinsic role for TLR2-MYD88 in intestinal and breast epithelia and oncogenesis. Nat. Cell Biol. 2014, 16:1238-1248.
51. Xia L., Huang W., Tian D., Zhang L., Qi X., Chen Z., Shang X., Nie Y., Wu K. Forkhead box Q1 promotes hepatocellular carcinoma metastasis by transactivating ZEB2 and VersicanV1 expression. Hepatology 2014, 59:958-973.
52. Takahashi Y., Kuwabara H., Yoneda M., Isogai Z., Tanigawa N., Shibayama Y. Versican G1 and G3 domains are upregulated and latent transforming growth factor-beta binding protein-4 is downregulated in breast cancer stroma. Breast Cancer 2012, 19:46-53.
53. Du W.W., Fang L., Yang W., Sheng W., Zhang Y., Seth A., Yang B.B., Yee A.J. The role of versican G3 domain in regulating breast cancer cell motility including effects on osteoblast cell growth and differentiation in vitro-evaluation towards understanding breast cancer cell bone metastasis. BMC Cancer 2012, 12:341.
54. Du W.W., Yang B.B., Shatseva T.A., Yang B.L., Deng Z., Shan S.W., Lee D.Y., Seth A., Yee A.J. Versican G3 promotes mouse mammary tumor cell growth, migration, and metastasis by influencing EGF receptor signaling. PLoS One 2010, 5:e13828.
55. Du W.W., Yang B.B., Yang B.L., Deng Z., Fang L., Shan S.W., Jeyapalan Z., Zhang Y., Seth A., Yee A.J. Versican G3 domain modulates breast cancer cell apoptosis: a mechanism for breast cancer cell response to chemotherapy and EGFR therapy. PLoS One 2011, 6:e26396.
56. Du W.W., Fang L., Yang X., Sheng W., Yang B.L., Seth A., Zhang Y., Yang B.B., Yee A.J. The role of versican in modulating breast cancer cell self-renewal. Mol. Cancer Res. 2013, 11:443-455.
57. Arslan F., Bosserhoff A.K., Nickl-Jockschat T., Doerfelt A., Bogdahn U., Hau P. The role of versican isoforms V0/V1 in glioma migration mediated by transforming growth factor-beta2. Br. J. Cancer 2007, 96:1560-1568.
58. Morrione A., Neill T., Iozzo R.V. Dichotomy of decorin activity on the insulin-like growth factor-I system. FEBS J. 2013, 280:2138-2149.
59. Neill T., Schaefer L., Iozzo R.V. Decorin, a guardian from the matrix. Am. J. Pathol. 2012, 181:380-387.
60. Morcavallo A., Buraschi S., Xu S.-Q., Belfiore A., Schaefer L., Iozzo R.V., Morrione A. Decorin differentially modulates the activity of insulin receptor isoform A ligands. Matrix Biol. 2014, 35:82-90.
61. Goldoni S., Seidler D.G., Heath J., Fassan M., Baffa R., Thakur M.L., Owens R.T., McQuillan D.J., Iozzo R.V. An antimetastatic role for decorin in breast cancer. Am. J. Pathol. 2008, 173:844-855.
62. Hu Y., Sun H., Owens R.T., Wu J., Chen Y.Q., Berquin I.M., Perry D., O'Flaherty J.T., Edwards I.J. Decorin suppresses prostate tumor growth through inhibition of epidermal growth factor and androgen receptor pathways. Neoplasia 2009, 11:1042-1053.
63. Reed C.C., Gauldie J., Iozzo R.V. Suppression of tumorigenicity by adenovirus-mediated gene transfer of decorin. Oncogene 2002, 21:3688-3695.
64. Reed C.C., Waterhouse A., Kirby S., Kay P., Owens R.T., McQuillan D.J., Iozzo R.V. Decorin prevents metastatic spreading of breast cancer. Oncogene 2005, 24:1104-1110.
65. Seidler D.G., Goldoni S., Agnew C., Cardi C., Thakur M.L., Owens R.A., McQuillan D.J., Iozzo R.V. Decorin protein core inhibits in vivo cancer growth and metabolism by hindering epidermal growth factor receptor function and triggering apoptosis via caspase-3 activation. J. Biol. Chem. 2006, 281:26408-26418.
66. Bi X., Pohl N.M., Qian Z., Yang G.R., Gou Y., Guzman G., Kajdacsy-Balla A., Iozzo R.V., Yang W. Decorin-mediated inhibition of colorectal cancer growth and migration is associated with E-cadherin in vitro and in mice. Carcinogenesis 2012, 33:326-330.
67. Bi X., Tong C., Dockendorff A., Bancroft L., Gallagher L., Guzman G., Iozzo R.V., Augenlicht L.H., Yang W. Genetic deficiency of decorin causes intestinal tumor formation through disruption of intestinal cell maturation. Carcinogenesis 2008, 29:1435-1440.
68. Iozzo R.V., Chakrani F., Perrotti D., McQuillan D.J., Skorski T., Calabretta B., Eichstetter I. Cooperative action of germline mutations in decorin and p53 accelerates lymphoma tumorigenesis. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:3092-3097.
69. Horvath Z., Kovalszky I., Fullar A., Kiss K., Schaff Z., Iozzo R.V., Baghy K. Decorin deficiency promotes hepatic carcinogenesis. Matrix Biol. 2014, 35:194-205.
70. Cawthorn T.R., Moreno J.C., Dharsee M., Tran-Thanh D., Ackloo S., Zhu P.H., Sardana G., Chen J., Kupchak P., Jacks L.M., Miller N.A., Youngson B.J., Iakovlev V., Guidos C.J., Vallis K.A., Evans K.R., McCready D., Leong W.L., Done S.J. Proteomic analyses reveal high expression of decorin and endoplasmin (HSP90B1) are associated with breast cancer metastasis and decreased survival. PLoS One 2012, 7:e30992.
71. Robinson P.S., Huang T.F., Kazam E., Iozzo R.V., Birk D.E., Soslowsky L.J. Influence of decorin and biglycan on mechanical properties of multiple tendons in knockout mice. J. Biomech. Eng. 2005, 127:181-185.
72. Dunkman A.A., Buckley M.R., Mienaltowski M.J., Adams S.M., Thomas S.J., Satchell L., Kumar A., Pathmanathan L., Beason D.P., Iozzo R.V., Birk D.E., Soslowsky L.J. Decorin expression is important for age-related changes in tendon structure and mechanical properties. Matrix Biol. 2013, 32:3-13.
73. Reese S.P., Underwood C.J., Weiss J.A. Effects of decorin proteoglycan on fibrillogenesis, ultrastructure, and mechanics of type I collagen gels. Matrix Biol. 2013, 32:414-423.
74. Chen S., Young M.F., Chakravarti S., Birk D.E. Interclass small leucine-rich repeat proteoglycan interactions regulate collagen fibrillogenesis and corneal stromal assembly. Matrix Biol. 2014, 35:103-111.
75. Brown E.L., Wooten R.M., Johnson B.J., Iozzo R.V., Smith A., Dolan M.C., Guo B.P., Weis J.J., Hook M. Resistance to Lyme disease in decorin-deficient mice. J. Clin. Invest. 2001, 107:845-852.
76. Brandan E., Gutierrez J. Role of skeletal muscle proteoglycans during myogenesis. Matrix Biol. 2013, 32:289-297.
77. Duncan M.B. Extracellular matrix transcriptome dynamics in hepatocellular carcinoma. Matrix Biol. 2013, 32:393-398.
78. Nikolovska K., Renke J.K., Jungmann O., Grobe K., Iozzo R.V., Zamfir A.D., Seidler D.G. A decorin-deficient matrix affects skin chondroitin/dermatan sulfate levels and keratinocyte function. Matrix Biol. 2014, 35:91-102.
79. Wu Z., Horgan C.E., Carr O., Owens R.T., Iozzo R.V., Lechner B.E. Biglycan and decorin differentially regulate signaling in the fetal membranes. Matrix Biol. 2014, 35:266-275.
80. Zoeller J.J., Pimtong W., Corby H., Goldoni S., Iozzo A.E., Owens R.T., Ho S.-Y., Iozzo R.V. A central role for decorin during vertebrate convergent extension. J. Biol. Chem. 2009, 284:11728-11737.
81. Ichii M., Frank M.B., Iozzo R.V., Kincade P.W. The canonical Wnt pathway shapes niches supportive of hematopoietic stem/progenitor cells. Blood 2012, 119:1683-1692.
82. Zeng-Brouwers J., Beckmann J., Nastase M.V., Iozzo R.V., Schaefer L. De novo expression of circulating biglycan evokes an innate inflammatory tissue response via MyD88/TRIF pathways. Matrix Biol. 2014, 35:132-142.
83. Merline R., Moreth K., Beckmann J., Nastase M.V., Zeng-Brouwers J., Tralhao J.G., Lemarchand P., Pfeilschifter J., Schaefer R.M., Iozzo R.V., Schaefer L. Signaling by the matrix proteoglycan decorin controls inflammation and cancer through PDCD4 and MicroRNA-21. Sci. Signal. 2011, 4:ra75.
84. Neill T., Schaefer L., Iozzo R.V. Instructive roles of extracellular matrix on autophagy. Am. J. Pathol. 2014, 184:2146-2153.
85. Wang K., Klionsky D.J. Mitochondria removal by autophagy. Autophagy 2011, 7:297-300.
86. Yang Z., Klionsky D.J. Mammalian autophagy: core molecular machinery and signaling regulation. Curr. Opin. Cell Biol. 2010, 22:124-131.
87. Koren I., Kimchi A. Promoting tumorigenesis by suppressing autophagy. Science 2012, 338:889-890.
88. Chen P., Cescon M., Bonaldo P. Collagen VI in cancer and its biological mechanisms. Trends Mol. Med. 2013, 19:410-417.
89. Bonaldo P., Sandri M. Cellular and molecular mechanisms of muscle atrophy. Dis. Model. Mech. 2013, 6:25-39.
90. Goyal A., Pal N., Concannon M., Paulk M., Doran M., Poluzzi C., Sekiguchi K., Whitelock J.M., Neill T., Iozzo R.V. Endorepellin, the angiostatic module of perlecan, interacts with both the α2β1 integrin and vascular endothelial growth factor receptor 2 (VEGFR2). J. Biol. Chem. 2011, 286:25947-25962.
91. Goyal A., Poluzzi C., Willis A.C., Smythies J., Shellard A., Neill T., Iozzo R.V. Endorepellin affects angiogenesis by antagonizing diverse VEGFR2-evoked signaling pathways: transcriptional repression of HIF-1α and VEGFA and concurrent inhibition of NFAT1 activation. J. Biol. Chem. 2012, 287:43543-43556.
92. Hood B.L., Lucas D.A., Kim G., Chan K.C., Blonder J., Issaq H.J., Veenstra T.D., Conrads T.P., Pollet I., Karsan A. Quantitative analysis of the low molecular weight serum proteome using (18)O stable isotope labeling in a lung tumor xenograft mouse model. J. Am. Soc. Mass Spectrom. 2005, 16:1221-1230.
93. Morselli E., Galluzzi L., Kepp O., Marino G., Michaud M., Vitale I., Maiuri M.C., Kroemer G. Oncosuppressive functions of autophagy. Antioxid. Redox Signal. 2011, 14:2251-2269.
94. Michaud M., Martins I., Sukkurwala A.Q., Adjemian S., Ma Y., Pellegatti P., Kepp O., Scoazec M., Mignot G., Rello-Varona S., Tailler M., Menger L., Vacchelli E., Galluzzi L., Ghiringhelli F., diVirgilio F., Zitvogel L., Kroemer G. Autophagy-dependent anticancer immune responses induced by chemotherapeutic agents in mice. Science 2011, 334:1573-1577.
95. Buraschi S., Neill T., Goyal A., Poluzzi C., Smythies J., Owens R.T., Schaefer L., Torres A., Iozzo R.V. Decorin causes autophagy in endothelial cells via Peg3. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:E2582-E2591.
96. Buraschi S., Neill T., Owens R.T., Iniguez L.A., Purkins G., Vadigepalli R., Evans B., Schaefer L., Peiper S.C., Wang Z.X., Iozzo R.V. Decorin protein core affects the global gene expression profile of the tumor microenvironment in a triple-negative orthotopic breast carcinoma xenograft model. PLoS One 2012, 7:e45559.
97. Poluzzi C., Casulli J., Goyal A., Mercer T.J., Neill T., Iozzo R.V. Endorepellin evokes autophagy in endothelial cells. J. Biol. Chem. 2014, 289:16114-16128.
98. Willis C.D., Poluzzi C., Mongiat M., Iozzo R.V. Endorepellin laminin-like globular repeat 1/2 domains bind Ig3-5 of vascular endothelial growth factor(VEGF) receptor 2 and block pro-angiogenic signaling by VEGFA in endothelial cells. FEBS J. 2013, 280:2271-2294.
99. Nguyen T.M.B., Subramanian I.V., Xiao X., Ghosh G., Nguyen P., Kelekar A., Ramakrishnan S. Endostatin induces autophagy in endothelial cells by modulating Beclin 1 and β-catenin levels. J. Cell. Mol. Med. 2009, 13:3687-3698.
100. Nguygen T.M.B., Subramanian I.V., Kelekar A., Ramakrishnan S. Kringle 5 of human plasminogen, an angiogenesis inhibitor, induces both autophagy and apoptotic death in endothelial cells. Blood 2007, 109:4793-4802.
101. Urciuolo A., Quarta A., Morbidoni V., Gattazzo F., Molon S., Grumati P., Montemurro F., Tedesco F.S., Blaauw B., Cossu G., Vozzi G., Rando T.A., Bonaldo P. Collagen VI regulates satellite cell self-renewal and muscle regeneration. Nat. Commun. 2013, 4:1964.
102. Irwin W.A., Bergamin N., Sabatelli P., Reggiani C., Megighian A., Merlini L., Braghetta P., Columbaro M., Volpin D., Bressan G.M., Bernardi P., Bonaldo P. Mitochondrial dysfunction and apoptosis in myopathic mice with collagen VI deficiency. Nat. Genet. 2003, 35:367-371.
103. Grumati P., Coletto L., Sabatelli P., Cescon M., Angelin A., Bertaggia E., Blaauw B., Urciuolo A., Tiepolo T., Merlini L., Maraldi N.M., Bernardi P., Sandri M., Bonaldo P. Autophagy is defective in collagen VI muscular dystrophies, and its reactivation rescues myofiber degeneration. Nat. Med. 2011, 16:1313-1320.
104. Grumati P., Bonaldo P. Autophagy in skeletal muscle homeostasis and in muscular dystrophies. Cells 2012, 1:325-345.
105. Carmignac V., Svensson M., Krner Z., Elowsson L., Matsumura C., Gawlik K.I., Allamand V., Durbeej M. Autophagy is increased in laminin α2 chain-deficient muscle and its inhibition improves muscle morphology in a mouse model of MDC1A. Hum. Mol. Genet. 2011, 20:4891-4902.
106. Buraschi S., Neill T., Owens R.T., Iniguez L.A., Purkins G., Vadigepalli R., Evans B., Schaefer L., Peiper S.C., Wang Z., Iozzo R.V. Decorin protein core affects the global gene expression profile of the tumor microenvironment in a triple-negative orthotopic breast carcinoma xenograft model. PLoS One 2012, 7:e45559.
107. Kuroiwa Y., Kaneko-Ishino T., Kagitani F., Kohda T., Li L.-L., Tada M., Suzuki R., Yokoyama M., Shiroishi T., Wakana S., Barton S.C., Ishino F., Surani M.A. Peg3 imprinted gene on proximal chromosome 7 encodes for a zinc finger protein. Nat. Genet. 1996, 12:186-190.
108. Yamaguchi A., Taniguchi M., Hori O., Ogawa S., Tojo N., Matsuoka N., Miyake S.-i., Kasai K., Sugimoto H., Tamatani M., Yamashita T., Yamashita T., Tohyama M. Peg3/Pw1 is involved in p53-mediated cell death pathway in brain ischemia/hypoxia. J. Biol. Chem. 2002, 277:623-629.
109. Kohda T., Asai A., Kuroiwa Y., Kobayashi S., Aisaka K., Nagashima G., Yoshida M.C., Kondo Y., Kagiyama N., Kirino T., Kaneko-Ishino T., Ishino F. Tumour suppressor activity of human imprinted gene PEG3 in a glioma cell line. Genes Cells 2001, 6:237-247.
110. Dowdy S.C., Gostout B.S., Shridhar V., Wu X., Smith D.I., Podratz K.C., Jiang S.-W. Biallelic methylation and silencing of paternally expressed gene 3 (PEG3) in gynecologic cancer cell lines. Gynecol. Oncol. 2005, 99:126-134.
111. Jiang X., Yu Y., Yang H.W., Agar N.Y.R., Frado L., Johnson M.D. The imprinted gene PEG3 inhibits Wnt signaling and regulates glioma growth. J. Biol. Chem. 2010, 285:8472-8480.
112. Buraschi S., Neill T., Goyal A., Poluzzi C., Smythies J., Owens R.T., Schaefer L., Torres A.T., Iozzo R.V. Decorin causes autophagy in endothelial cells via Peg3. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:E2582-E2591.
113. Neill T., Torres A.T., Buraschi S., Iozzo R.V. Decorin has an appetite for endothelial cell autophagy. Autophagy 2013, 9:1626-1628.
114. Iozzo R.V., Goldoni S., Berendsen A., Young M.F. Small leucine-rich proteoglycans. Extracellular Matrix: An overview 2011, 197-231. Springer. R.P. Mecham (Ed.).
115. Merline R., Nastase M.V., Iozzo R.V., Schaefer L. Small leucine-rich proteoglycans: multifunctional signaling effectors. Extracellular Matrix: Pathobiology and signaling 2012, 185-196. Walter de Gruytier Gmbh and Co., Berlin. N. Karamanos (Ed.).
116. Schaefer L., Iozzo R.V. Small leucine-rich proteoglycans, at the crossroad of cancer growth and inflammation. Curr. Opin. Genet. Dev. 2012, 22:56-57.
117. Goyal A., Neill T., Owens R.T., Schaefer L., Iozzo R.V. Decorin activates AMPK, an energy sensor kinase, to induce autophagy in endothelial cells. Matrix Biol. 2014, 34:46-54.
118. Funderburk S.F., Wang Q.J., Yue Z. The Beclin 1-VPS34 complex-at the crossroads of autophagy and beyond. Trends Cell Biol. 2010, 20:355-362.
119. Wang R.C., Wei Y., An Z., Zou Z., Xiao G., Bhagat G., White M., Reichelt J., Levine B. Akt-mediated regulation of autophagy and tumorigenesis through Beclin 1 phosphorylation. Science 2012, 338:956-959.
120. Kim J., Kundu M., Viollet B., Guan K.-L. AMPK and mTOR regulate autophagy through direct phopshorylation of Ulk1. Nat. Cell Biol. 2011, 13:132-141.
121. Lee J.W., Park S., Takahashi Y., Wang H.-G. The association of AMPK with ULK1 regulates autophagy. PLoS One 2010, 5:e15394.
122. Levine B., Kroemer G. Autophagy in the pathogenesis of disease. Cell 2008, 132:27-42.
123. Choi A.M.K., Ryter S.W., Levine B. Autophagy in human health and disease. N. Engl. J. Med. 2013, 368:651-662.
124. Settembre C., Di Malta C., Polito V.A., Arencibia M.G., Vetrini F., Erdin S., Huynh T., Medina D., Colella P., Sardiello M., Rubinsztein D.C., Ballabio A. TFEB links autophagy to lysosomal biogenesis. Science 2011, 332:1429-1433.
125. Settembre C., Zoncu R., Medina D.L., Vetrini F., Erdin S., Erdin S., Huynh T., Ferron M., Karsenty G., Vellard M.C., Facchinetti V., Sabatini D.M., Ballabio A. A lysosome-to-lysosome signaling mechanism senses and regulates the lysosome via mTOR and TFEB. EMBO J. 2012, 31:1095-1108.
126. Roczniak-Ferguson A., Petit C.S., Froehlich F., Qian S., Ky J., Angarola B., Walther T.C., Ferguson S.M. The transcription factor TFEB links mTORC1 signaling to transcriptional control of lysosome homeostasis. Sci. Signal. 2012, 5:ra42.
127. Buraschi S., Pal N., Tyler-Rubinstein N., Owens R.T., Neill T., Iozzo R.V. Decorin antagonizes Met receptor activity and downregulates β-catenin and Myc levels. J. Biol. Chem. 2010, 285:42075-42085.
128. Goldoni S., Humphries A., Nystrom A., Sattar S., Owens R.T., McQuillan D.J., Ireton K., Iozzo R.V. Decorin is a novel antagonistic ligand of the Met receptor. J. Cell Biol. 2009, 185:743-754.
129. Goldoni S., Iozzo R.V. Tumor microenvironment: modulation by decorin and related molecules harboring leucine-rich tandem motifs. Int. J. Cancer 2008, 123:2473-2479.
130. Neill T., Jones H.R., Crane-Smith Z., Owens R.T., Schaefer L., Iozzo R.V. Decorin induces rapid secretion of thrombospondin-1 in basal breast carcinoma cells via inhibition of Ras homolog gene family, member A/Rho-associated coiled-coil containing protein kinase 1. FEBS J. 2013, 280:2353-2368.
131. Xu W., Neill T., Yang Y., Hu Z., Cleveland E., Wu Y., Hutten R., Xiao X., Stock S.R., Shevrin D., Kaul K., Brendler C., Iozzo R.V., Seth P. The systemic delivery of an oncolytic adenovirus expressing decorin inhibits bone metastasis in a mouse model of human prostate cancer. Gene Ther. 2015, 23:31-40.
132. Araki K., Wakabayashi H., Shintani K., Morikawa J., Matsumine A., Kusuzaki K., Sudo A., Uchida A. Decorin suppresses bone metastasis in a breast cancer cell line. Oncology 2009, 77:92-99.
133. Fassan M., D'Arca D., Letko J., Vecchione A., Gardiman M.P., McCue P., Wildemore B., Rugge M., Shupp-Byrne D., Gomella L.G., Morrione A., Iozzo R.V., Baffa R. Mitostatin is down-regulated in human prostate cancer and suppresses the invasive phenotype of prostate cancer cells. PLoS One 2011, 6:e19771.
134. Vecchione A., Fassan M., Anesti V., Morrione A., Goldoni S., Baldassarre G., Byrne D., D'Arca D., Palazzo J.P., Lloyd J., Scorrano L., Gomella L.G., Iozzo R.V., Baffa R. MITOSTATIN, a putative tumor suppressor on chromosome 12q24.1, is downregulated in human bladder and breast cancer. Oncogene 2009, 28:257-269.
135. Cerqua C., Anesti V., Pyakurel A., Liu D., Naon D., Wiche G., Baffa R., Dimmer K.S., Scorrano L. Trichoplein/mitostatin regulates endoplasmic reticulum-mitochondria juxtaposition. EMBO Rep. 2010, 11:854-860.
136. Ventura-Clapier R., Garnier A., Veksler W. Transcriptional control of mitochondrial biogenesis: the central role of PGC-1α. Cardiovasc. Res. 2008, 79:208-217.
137. Vazquez F., Lim J.-H., Chim H., Bhalla K., Girnun G., Pierce K., Clish C.B., Granter S.R., Widlund H.R., Spiegelman B.M., Puigserver P. PGC1α expression defines a subset of human melanoma tumors with increased mitochondrial capacity and resistance to oxidative stress. Cancer Cell 2013, 23:287-301.
138. Kroemer G., Pouyssegur J. Tumor cell metabolism: cancer's Achilles' heel. Cancer Cell 2008, 13:472-482.
139. Galluzzi L., Kepp O., Kroemer G. Mitochondria: master regulators of danger signalling. Nat. Rev. Mol. Cell Biol. 2012, 13:780-788.
140. Dagda R., Cherra S.J.I., Kulich S.M., Tandon A., Park D., Chu C.T. Loss of PINK1 function promotes mitophagy through effects on oxidative stress and mitochondrial fission. J. Biol. Chem. 2009, 284:13843-13855.
141. Maiuri M.C., Zalckvar E., Kimchi A., Kroemer G. Self-eating and self-killing: crosstalk between autophagy and apoptosis. Nat. Rev. Mol. Cell Biol. 2007, 8:741-752.
142. Narendra D., Walker J.E., Youle R. Mitochondrial quality control mediated by PINK1 and Parkin: links to parkinsonism. Cold Spring Harb. Perspect. Biol. 2012, 4.
143. Csordas G., Santra M., Reed C.C., Eichstetter I., McQuillan D.J., Gross D., Nugent M.A., Hajnoczky G., Iozzo R.V. Sustained down-regulation of the epidermal growth factor receptor by decorin. A mechanism for controlling tumor growth in vivo. J. Biol. Chem. 2000, 275:32879-32887.
144. Geisler S., Holmstrom K.M., Skujat D., Fiesel F.C., Rothfuss O.C., Kahle P.J., Springer W. PINK1/Parkin-mediated mitophagy is dependent on VDAC1 and p62/SQSTM1. Nat. Cell Biol. 2010, 12:119-131.
145. Vincow E.S., Merrihew G., Thomas R.E., Shulman N.J., Beyer R.P., MacCoss M.J., Pallanck L.J. The PINK1-Parkin pathway promotes both mitophagy and selective respiratory chain turnover in vivo. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:6400-6405.
146. Narendra D., Kane L.A., Hauser D.N., Fearnley I.M., Youle R.J. p62/SQSTM1 is required for Parkin-induced mitochondrial clustering but not mitophagy; VDAC1 is dispensable for both. Autophagy 2010, 6:1090-1106.
147. Ward P.S., Thompson C.B. Metabolic reprogramming: a cancer hallmark even Warburg did not appreciate. Cancer Cell 2012, 21:297-308.
148. Cenki B., Sephton C.F., Cenik B.K., Herz J., Yu G. Progranulin: a proteolytically processed protein at the crossroads of inflammation and neurodegeneration. J. Biol. Chem. 2012, 287:32298-32306.
149. Staropoli J.F., McDermott C., Martinat C., Schulman B., Demireva E., Abeliovich A. Parkin is a component of an SCF-like ubiquitin ligase complex and protects postmitotic neurons from kainate excitotoxicity. Neuron 2003, 37:735-749.
150. Flugel D., Gorlach A., Kietzmann T. GSK-3β regulates cell growth, migration, and angiogenesis via Fbw7 and USP28-dependent degradation of HIF-1α. Blood 2012, 119:1292-1301.
151. Welcker M., Orian A., Grim J.E., Eisenman R.N., Clurman B.E. A nucleolar isoform of the Fbw7 ubiquitin ligase regulates c-Myc and cell size. Curr. Biol. 2004, 14:1852-1857.
152. Nastase M.V., Young M.F., Schaefer L. Biglycan: a multivalent proteoglycan providing structure and signals. J. Histochem. Cytochem. 2012, 60:963-975.
153. Xu T., Bianco P., Fisher L.W., Longenecker G., Smith E., Goldstein S., Bonadio J., Boskey A., Heegaard A.M., Sommer B., Satomura K., Dominguez P., Zhao C., Kulkarni A.B., Robey P.G., Young M.F. Targeted disruption of the biglycan gene leads to an osteoporosis-like phenotype in mice. Nat. Genet. 1998, 20:78-82.
154. Schaefer L., Babelova A., Kiss E., Hausser H.J., Baliova M., Krzyzankova M., Marsche G., Young M.F., Mihalik D., Gotte M., Malle E., Schaefer R.M., Grone H.J. The matrix component biglycan is proinflammatory and signals through Toll-like receptors 4 and 2 in macrophages. J. Clin. Invest. 2005, 115:2223-2233.
155. Schaefer L. Complexity of danger: the diverse nature of damage-associated molecular patterns. J. Biol. Chem. 2014, 289:35237-35245.
156. Moreth K., Brodbeck R., Babelova A., Gretz N., Spieker T., Zeng-Brouwers J., Pfeilschifter J., Young M.F., Schaefer R.M., Schaefer L. The proteoglycan biglycan regulates expression of the B cell chemoattractant CXCL13 and aggravates murine lupus nephritis. J. Clin. Invest. 2010, 120:4251-4272.
157. Zhu Y.H., Yang F., Zhang S.S., Zeng T.T., Xie X., Guan X.Y. High expression of biglycan is associated with poor prognosis in patients with esophageal squamous cell carcinoma. Int. J. Clin. Exp. Pathol. 2013, 6:2497-2505.
158. Nishino R., Honda M., Yamashita T., Takatori H., Minato H., Zen Y., Sasaki M., Takamura H., Horimoto K., Ohta T., Nakanuma Y., Kaneko S. Identification of novel candidate tumour marker genes for intrahepatic cholangiocarcinoma. J. Hepatol. 2008, 49:207-216.
159. Modolo F., Biz M.T., Martins M.T., Machado de Sousa S.O., de Araujo N.S. Expression of extracellular matrix proteins in adenomatoid odontogenic tumor. J. Oral Pathol. Med. 2010, 39:230-235.
160. Jaeger J., Koczan D., Thiesen H.J., Ibrahim S.M., Gross G., Spang R., Kunz M. Gene expression signatures for tumor progression, tumor subtype, and tumor thickness in laser-microdissected melanoma tissues. Clin. Cancer Res. Off. J. Am. Assoc. Cancer Res. 2007, 13:806-815.
161. Galamb O., Sipos F., Spisak S., Galamb B., Krenacs T., Valcz G., Tulassay Z., Molnar B. Potential biomarkers of colorectal adenoma-dysplasia-carcinoma progression: mRNA expression profiling and in situ protein detection on TMAs reveal 15 sequentially upregulated and 2 downregulated genes. Cell. Oncol. 2009, 31:19-29.
162. Gu X., Ma Y., Xiao J., Zheng H., Song C., Gong Y., Xing X. Up-regulated biglycan expression correlates with the malignancy in human colorectal cancers. Clin. Exp. Med. 2012, 12:195-199.
163. Mikula M., Rubel T., Karczmarski J., Goryca K., Dadlez M., Ostrowski J. Integrating proteomic and transcriptomic high-throughput surveys for search of new biomarkers of colon tumors. Funct. Integr. Genomics 2011, 11:215-224.
164. Liu Y., Li W., Li X., Tai Y., Lu Q., Yang N., Jiang J. Expression and significance of biglycan in endometrial cancer. Arch. Gynecol. Obstet. 2014, 289:649-655.
165. Wang B., Li G.X., Zhang S.G., Wang Q., Wen Y.G., Tang H.M., Zhou C.Z., Xing A.Y., Fan J.W., Yan D.W., Qiu G.Q., Yu Z.H., Peng Z.H. Biglycan expression correlates with aggressiveness and poor prognosis of gastric cancer. Exp. Biol. Med. (Maywood) 2011, 236:1247-1253.
166. Fang D.D., Kim Y.J., Lee C.N., Aggarwal S., McKinnon K., Mesmer D., Norton J., Birse C.E., He T., Ruben S.M., Moore P.A. Expansion of CD133(+) colon cancer cultures retaining stem cell properties to enable cancer stem cell target discovery. Br. J. Cancer 2010, 102:1265-1275.
167. Aprile G., Avellini C., Reni M., Mazzer M., Foltran L., Rossi D., Cereda S., Iaiza E., Fasola G., Piga A. Biglycan expression and clinical outcome in patients with pancreatic adenocarcinoma. Tumour Biol. J. Int. Soc. Oncodev. Biol. Med. 2013, 34:131-137.
168. Niedworok C., Rock K., Kretschmer I., Freudenberger T., Nagy N., Szarvas T., Vom Dorp F., Reis H., Rubben H., Fischer J.W. Inhibitory role of the small leucine-rich proteoglycan biglycan in bladder cancer. PLoS One 2013, 8:e80084.
169. Rydstrom K., Joost P., Ehinger M., Eden P., Jerkeman M., Cavallin-Stahl E., Linderoth J. Gene expression profiling indicates that immunohistochemical expression of CD40 is a marker of an inflammatory reaction in the tumor stroma of diffuse large B-cell lymphoma. Leuk. Lymphoma 2012, 53:1764-1768.
170. Weber C.K., Sommer G., Michl P., Fensterer H., Weimer M., Gansauge F., Leder G., Adler G., Gress T.M. Biglycan is overexpressed in pancreatic cancer and induces G1-arrest in pancreatic cancer cell lines. Gastroenterology 2001, 121:657-667.
171. Takekawa M., Tatebayashi K., Itoh F., Adachi M., Imai K., Saito H. Smad-dependent GADD45beta expression mediates delayed activation of p38 MAP kinase by TGF-beta. EMBO J. 2002, 21:6473-6482.
172. Yamamoto K., Ohga N., Hida Y., Maishi N., Kawamoto T., Kitayama K., Akiyama K., Osawa T., Kondoh M., Matsuda K., Onodera Y., Fujie M., Kaga K., Hirano S., Shinohara N., Shindoh M., Hida K. Biglycan is a specific marker and an autocrine angiogenic factor of tumour endothelial cells. Br. J. Cancer 2012, 106:1214-1223.
173. Liu T., Du X., Sheng X. Gene expression changes after ionizing radiation in endothelial cells derived from human endometrial cancer-preliminary outcomes. Arch. Gynecol. Obstet. 2014, 289:1315-1323.
174. Berendsen A.D., Pinnow E.L., Maeda A., Brown A.C., McCartney-Francis N., Kram V., Owens R.T., Robey P.G., Holmbeck K., de Castro L.F., Kilts T.M., Young M.F. Biglycan modulates angiogenesis and bone formation during fracture healing. Matrix Biol. 2014, 35:223-231.
175. Xing X., Gu X., Ma T., Ye H. Biglycan up-regulated vascular endothelial growth factor (VEGF) expression and promoted angiogenesis in colon cancer. Tumour Biol. 2015, 36:1773-1780.
176. West X.Z., Malinin N.L., Merkulova A.A., Tischenko M., Kerr B.A., Borden E.C., Podrez E.A., Salomon R.G., Byzova T.V. Oxidative stress induces angiogenesis by activating TLR2 with novel endogenous ligands. Nature 2010, 467:972-976.
177. Babelova A., Moreth K., Tsalastra-Greul W., Zeng-Brouwers J., Eickelberg O., Young M.F., Bruckner P., Pfeilschifter J., Schaefer R.M., Grone H.J., Schaefer L. Biglycan, a danger signal that activates the NLRP3 inflammasome via toll-like and P2X receptors. J. Biol. Chem. 2009, 284:24035-24048.
178. Recktenwald C.V., Leisz S., Steven A., Mimura K., Muller A., Wulfanger J., Kiessling R., Seliger B. HER-2/neu-mediated down-regulation of biglycan associated with altered growth properties. J. Biol. Chem. 2012, 287:24320-24329.
179. Schaefer L., Beck K.F., Raslik I., Walpen S., Mihalik D., Micegova M., Macakova K., Schonherr E., Seidler D.G., Varga G., Schaefer R.M., Kresse H., Pfeilschifter J. Biglycan, a nitric oxide-regulated gene, affects adhesion, growth, and survival of mesangial cells. J. Biol. Chem. 2003, 278:26227-26237.
180. Shimizu-Hirota R., Sasamura H., Kuroda M., Kobayashi E., Hayashi M., Saruta T. Extracellular matrix glycoprotein biglycan enhances vascular smooth muscle cell proliferation and migration. Circ. Res. 2004, 94:1067-1074.
181. Berendsen A.D., Fisher L.W., Kilts T.M., Owens R.T., Robey P.G., Gutkind J.S., Young M.F. Modulation of canonical Wnt signaling by the extracellular matrix component biglycan. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:17022-17027.
182. Ward M., Ajuwon K.M. Regulation of pre-adipocyte proliferation and apoptosis by the small leucine-rich proteoglycans, biglycan and decorin. Cell Prolif. 2011, 44:343-351.
183. Hu L., Duan Y.T., Li J.F., Su L.P., Yan M., Zhu Z.G., Liu B.Y., Yang Q.M. Biglycan enhances gastric cancer invasion by activating FAK signaling pathway. Oncotarget 2014, 5:1885-1896.
184. Bischof A.G., Yuksel D., Mammoto T., Mammoto A., Krause S., Ingber D.E. Breast cancer normalization induced by embryonic mesenchyme is mediated by extracellular matrix biglycan. Integr. Biol. Quant. Biosci. Nano Macro 2013, 5:1045-1056.
185. Tufvesson E., Westergren-Thorsson G. Biglycan and decorin induce morphological and cytoskeletal changes involving signalling by the small GTPases RhoA and Rac1 resulting in lung fibroblast migration. J. Cell Sci. 2003, 116:4857-4864.
186. Datsis G.A., Berdiaki A., Nikitovic D., Mytilineou M., Katonis P., Karamanos N.K., Tzanakakis G.N. Parathyroid hormone affects the fibroblast growth factor-proteoglycan signaling axis to regulate osteosarcoma cell migration. FEBS J. 2011, 278:3782-3792.
187. Mintz M.B., Sowers R., Brown K.M., Hilmer S.C., Mazza B., Huvos A.G., Meyers P.A., Lafleur B., McDonough W.S., Henry M.M., Ramsey K.E., Antonescu C.R., Chen W., Healey J.H., Daluski A., Berens M.E., Macdonald T.J., Gorlick R., Stephan D.A. An expression signature classifies chemotherapy-resistant pediatric osteosarcoma. Cancer Res. 2005, 65:1748-1754.
188. Pan S., Cheng L., White J.T., Lu W., Utleg A.G., Yan X., Urban N.D., Drescher C.W., Hood L., Lin B. Quantitative proteomics analysis integrated with microarray data reveals that extracellular matrix proteins, catenins, and p53 binding protein 1 are important for chemotherapy response in ovarian cancers. OMICS 2009, 13:345-354.
189. Couchman J.R. Transmembrane signaling proteoglycans. Annu. Rev. Cell Dev. Biol. 2010, 26:89-114.
190. Xian X., Gopal S., Couchman J.R. Syndecans as receptors and organizers of the extracellular matrix. Cell Tissue Res. 2010, 339:31-46.
191. Xu D., Esko J.D. Demystifying heparan sulfate-protein interactions. Annu. Rev. Biochem. 2014, 83:129-157.
192. Kreuger J., Kjellen L. Heparan sulfate biosynthesis: regulation and variability. J. Histochem. Cytochem. 2012, 60:898-907.
193. Lee D., Oh E.S., Woods A., Couchman J.R., Lee W. Solution structure of a syndecan-4 cytoplasmic domain and its interaction with phosphatidylinositol 4,5-bisphosphate. J. Biol. Chem. 1998, 273:13022-13029.
194. Choi S., Lee E., Kwon S., Park H., Yi J.Y., Kim S., Han I.O., Yun Y., Oh E.S. Transmembrane domain-induced oligomerization is crucial for the functions of syndecan-2 and syndecan-4. J. Biol. Chem. 2005, 280:42573-42579.
195. Oh E.S., Woods A., Couchman J.R. Syndecan-4 proteoglycan regulates the distribution and activity of protein kinase C. J. Biol. Chem. 1997, 272:8133-8136.
196. Baietti M.F., Zhang Z., Mortier E., Melchior A., Degeest G., Geeraerts A., Ivarsson Y., Depoortere F., Coomans C., Vermeiren E., Zimmermann P., David G. Syndecan-syntenin-ALIX regulates the biogenesis of exosomes. Nat. Cell Biol. 2012, 14:677-685.
197. Morgan M.R., Hamidi H., Bass M.D., Warwood S., Ballestrem C., Humphries M.J. Syndecan-4 phosphorylation is a control point for integrin recycling. Dev. Cell 2013, 24:472-485.
198. Chen K., Williams K.J. Molecular mediators for raft-dependent endocytosis of syndecan-1, a highly conserved, multifunctional receptor. J. Biol. Chem. 2013, 288:13988-13999.
199. Morgan M.R., Humphries M.J., Bass M.D. Synergistic control of cell adhesion by integrins and syndecans. Nat. Rev. Mol. Cell Biol. 2007, 8:957-969.
200. Greene D.K., Tumova S., Couchman J.R., Woods A. Syndecan-4 associates with alpha-actinin. J. Biol. Chem. 2003, 278:7617-7623.
201. Lambaerts K., Wilcox-Adelman S.A., Zimmermann P. The signaling mechanisms of syndecan heparan sulfate proteoglycans. Curr. Opin. Cell Biol. 2009, 21:662-669.
202. Liu B.Y., Kim Y.C., Leatherberry V., Cowin P., Alexander C.M. Mammary gland development requires syndecan-1 to create a beta-catenin/TCF-responsive mammary epithelial subpopulation. Oncogene 2003, 22:9243-9253.
203. Alexander C.M., Reichsman F., Hinkes M.T., Lincecum J., Becker K.A., Cumberledge S., Bernfield M. Syndecan-1 is required for Wnt-1-induced mammary tumorigenesis in mice. Nat. Genet. 2000, 25:329-332.
204. Ishiguro K., Kadomatsu K., Kojima T., Muramatsu H., Tsuzuki S., Nakamura E., Kusugami K., Saito H., Muramatsu T. Syndecan-4 deficiency impairs focal adhesion formation only under restricted conditions. J. Biol. Chem. 2000, 275:5249-5252.
205. Echtermeyer F., Streit M., Wilcox-Adelman S., Saoncella S., Denhez F., Detmar M., Goetinck P. Delayed wound repair and impaired angiogenesis in mice lacking syndecan-4. J. Clin. Invest. 2001, 107:R9-R14.
206. Beck J.C., Lekutis C., Couchman J., Parry G. Stage-specific remodeling of the mammary gland basement membrane during lactogenic development. Biochem. Biophys. Res. Commun. 1993, 190:616-623.
207. Hinkes M.T., Goldberger O.A., Neumann P.E., Kokenyesi R., Bernfield M. Organization and promoter activity of the mouse syndecan-1 gene. J. Biol. Chem. 1993, 268:11440-11448.
208. Vihinen T., Maatta A., Jaakkola P., Auvinen P., Jalkanen M. Functional characterization of mouse syndecan-1 promoter. J. Biol. Chem. 1996, 271:12532-12541.
209. Iguchi-Ishiguro H., Ouchi Y., Watanabe S., Numabe Y. Analysis of syndecan-1 gene promoter during mouse tooth development. Arch. Oral Biol. 2012, 57:531-538.
210. Cook D.M., Hinkes M.T., Bernfield M., Rauscher F.J. Transcriptional activation of the syndecan-1 promoter by the Wilms' tumor protein WT1. Oncogene 1996, 13:1789-1799.
211. Okuyama E., Suzuki A., Murata M., Ando Y., Kato I., Takagi Y., Takagi A., Murate T., Saito H., Kojima T. Molecular mechanisms of syndecan-4 upregulation by TNF-alpha in the endothelium-like EAhy926 cells. J. Biochem. 2013, 154:41-50.
212. Fujita N., Hirose Y., Tran C.M., Chiba K., Miyamoto T., Toyama Y., Shapiro I.M., Risbud M.V. HIF-1-PHD2 axis controls expression of syndecan 4 in nucleus pulposus cells. FASEB J. 2014, 28:2455-2465.
213. Dedes P.G., Gialeli C., Tsonis A.I., Kanakis I., Theocharis A.D., Kletsas D., Tzanakakis G.N., Karamanos N.K. Expression of matrix macromolecules and functional properties of breast cancer cells are modulated by the bisphosphonate zoledronic acid. Biochim. Biophys. Acta 2012, 1820:1926-1939.
214. Ma L., Teruya-Feldstein J., Weinberg R.A. Tumour invasion and metastasis initiated by microRNA-10b in breast cancer. Nature 2007, 449:682-688.
215. Ibrahim S.A., Yip G.W., Stock C., Pan J.W., Neubauer C., Poeter M., Pupjalis D., Koo C.Y., Kelsch R., Schule R., Rescher U., Kiesel L., Gotte M. Targeting of syndecan-1 by microRNA miR-10b promotes breast cancer cell motility and invasiveness via a Rho-GTPase- and E-cadherin-dependent mechanism. Int. J. Cancer 2012, 131:E884-E896.
216. Sun H., Berquin I.M., Edwards I.J. Omega-3 polyunsaturated fatty acids regulate syndecan-1 expression in human breast cancer cells. Cancer Res. 2005, 65:4442-4447.
217. Yang Y., Macleod V., Miao H.Q., Theus A., Zhan F., Shaughnessy J.D., Sawyer J., Li J.P., Zcharia E., Vlodavsky I., Sanderson R.D. Heparanase enhances syndecan-1 shedding: a novel mechanism for stimulation of tumor growth and metastasis. J. Biol. Chem. 2007, 282:13326-13333.
218. Okolicsanyi R.K., Buffiere A., Jacinto J.M., Chacon-Cortes D., Chambers S.K., Youl P.H., Haupt L.M., Griffiths L.R. Association of heparan sulfate proteoglycans SDC1 and SDC4 polymorphisms with breast cancer in an Australian Caucasian population. Tumour Biol. 2015, 36:1731-1738.
219. Menashe I., Maeder D., Garcia-Closas M., Figueroa J.D., Bhattacharjee S., Rotunno M., Kraft P., Hunter D.J., Chanock S.J., Rosenberg P.S., Chatterjee N. Pathway analysis of breast cancer genome-wide association study highlights three pathways and one canonical signaling cascade. Cancer Res. 2010, 70:4453-4459.
220. Barbareschi M., Maisonneuve P., Aldovini D., Cangi M.G., Pecciarini L., Angelo Mauri F., Veronese S., Caffo O., Lucenti A., Palma P.D., Galligioni E., Doglioni C. High syndecan-1 expression in breast carcinoma is related to an aggressive phenotype and to poorer prognosis. Cancer 2003, 98:474-483.
221. Lofgren L., Sahlin L., Jiang S., Von Schoultz B., Fernstad R., Skoog L., Von Schoultz E. Expression of syndecan-1 in paired samples of normal and malignant breast tissue from postmenopausal women. Anticancer Res 2007, 27:3045-3050.
222. Tsanou E., Ioachim E., Briasoulis E., Charchanti A., Damala K., Karavasilis V., Pavlidis N., Agnantis N.J. Clinicopathological study of the expression of syndecan-1 in invasive breast carcinomas. correlation with extracellular matrix components. J. Exp. Clin. Cancer Res. 2004, 23:641-650.
223. Leivonen M., Lundin J., Nordling S., von Boguslawski K., Haglund C. Prognostic value of syndecan-1 expression in breast cancer. Oncology 2004, 67:11-18.
224. Mundhenke C., Meyer K., Drew S., Friedl A. Heparan sulfate proteoglycans as regulators of fibroblast growth factor-2 receptor binding in breast carcinomas. Am. J. Pathol. 2002, 160:185-194.
225. Loussouarn D., Campion L., Sagan C., Frenel J.S., Dravet F., Classe J.M., Pioud-Martigny R., Berton-Rigaud D., Bourbouloux E., Mosnier J.F., Bataille F.R., Campone M. Prognostic impact of syndecan-1 expression in invasive ductal breast carcinomas. Br. J. Cancer 2008, 98:1993-1998.
226. Su G., Blaine S.A., Qiao D., Friedl A. Membrane type 1 matrix metalloproteinase-mediated stromal syndecan-1 shedding stimulates breast carcinoma cell proliferation. Cancer Res. 2008, 68:9558-9565.
227. Mennerich D., Vogel A., Klaman I., Dahl E., Lichtner R.B., Rosenthal A., Pohlenz H.D., Thierauch K.H., Sommer A. Shift of syndecan-1 expression from epithelial to stromal cells during progression of solid tumours. Eur. J. Cancer 2004, 40:1373-1382.
228. Stanley M.J., Stanley M.W., Sanderson R.D., Zera R. Syndecan-1 expression is induced in the stroma of infiltrating breast carcinoma. Am. J. Clin. Pathol. 1999, 112:377-383.
229. Nikolova V., Koo C.Y., Ibrahim S.A., Wang Z., Spillmann D., Dreier R., Kelsch R., Fischgrabe J., Smollich M., Rossi L.H., Sibrowski W., Wulfing P., Kiesel L., Yip G.W., Gotte M. Differential roles for membrane-bound and soluble syndecan-1 (CD138) in breast cancer progression. Carcinogenesis 2009, 30:397-407.
230. Beauvais D.M., Rapraeger A.C. Syndecan-1-mediated cell spreading requires signaling by alphavbeta3 integrins in human breast carcinoma cells. Exp. Cell Res. 2003, 286:219-232.
231. Maeda T., Alexander C.M., Friedl A. Induction of syndecan-1 expression in stromal fibroblasts promotes proliferation of human breast cancer cells. Cancer Res. 2004, 64:612-621.
232. Maeda T., Desouky J., Friedl A. Syndecan-1 expression by stromal fibroblasts promotes breast carcinoma growth in vivo and stimulates tumor angiogenesis. Oncogene 2006, 25:1408-1412.
233. Burbach B.J., Ji Y., Rapraeger A.C. Syndecan-1 ectodomain regulates matrix-dependent signaling in human breast carcinoma cells. Exp. Cell Res. 2004, 300:234-247.
234. Ibrahim S.A., Hassan H., Vilardo L., Kumar S.K., Kumar A.V., Kelsch R., Schneider C., Kiesel L., Eich H.T., Zucchi I., Reinbold R., Greve B., Gotte M. Syndecan-1 (CD138) modulates triple-negative breast cancer stem cell properties via regulation of LRP-6 and IL-6-mediated STAT3 signaling. PLoS One 2013, 8:e85737.
235. Tokes A.M., Szasz A.M., Farkas A., Toth A.I., Dank M., Harsanyi L., Molnar B.A., Molnar I.A., Laszlo Z., Rusz Z., Kulka J. Stromal matrix protein expression following preoperative systemic therapy in breast cancer. Clin. Cancer Res. Off. J. Am. Assoc. Cancer Res. 2009, 15:731-739.
236. Gotte M., Kersting C., Ruggiero M., Tio J., Tulusan A.H., Kiesel L., Wulfing P. Predictive value of syndecan-1 expression for the response to neoadjuvant chemotherapy of primary breast cancer. Anticancer Res 2006, 26:621-627.
237. Baba F., Swartz K., van Buren R., Eickhoff J., Zhang Y., Wolberg W., Friedl A. Syndecan-1 and syndecan-4 are overexpressed in an estrogen receptor-negative, highly proliferative breast carcinoma subtype. Breast Cancer Res. Treat. 2006, 98:91-98.
238. Lim H., Multhaupt H., Couchman J.R. Cell surface heparan sulfate proteoglycans control adhesion and invasion of breast carcinoma cells. Mol. Cancer 2015, 14:15.
239. Wu Z.S., Pandey V., Wu W.Y., Ye S., Zhu T., Lobie P.E. Prognostic significance of the expression of GFRalpha1, GFRalpha3 and syndecan-3, proteins binding ARTEMIN, in mammary carcinoma. BMC Cancer 2013, 13:34.
240. Allinen M., Beroukhim R., Cai L., Brennan C., Lahti-Domenici J., Huang H., Porter D., Hu M., Chin L., Richardson A., Schnitt S., Sellers W.R., Polyak K. Molecular characterization of the tumor microenvironment in breast cancer. Cancer Cell 2004, 6:17-32.
241. Polyak K. Heterogeneity in breast cancer. J. Clin. Invest. 2011, 121:3786-3788.
242. Bissell M.J., Hall H.G., Parry G. How does the extracellular matrix direct gene expression?. J. Theor. Biol. 1982, 99:31-68.
243. Beauvais D.M., Burbach B.J., Rapraeger A.C. The syndecan-1 ectodomain regulates alphavbeta3 integrin activity in human mammary carcinoma cells. J. Cell Biol. 2004, 167:171-181.
244. Beauvais D.M., Ell B.J., McWhorter A.R., Rapraeger A.C. Syndecan-1 regulates alphavbeta3 and alphavbeta5 integrin activation during angiogenesis and is blocked by synstatin, a novel peptide inhibitor. J. Exp. Med. 2009, 206:691-705.
245. Beauvais D.M., Rapraeger A.C. Syndecan-1 couples the insulin-like growth factor-1 receptor to inside-out integrin activation. J. Cell Sci. 2010, 123:3796-3807.
246. Leppä S., Mali M., Miettinen H.M., Jalkanen M. Syndecan expression regulates cell morphology and growth of mouse mammary epithelial tumor cells. Proc. Natl. Acad. Sci. U. S. A. 1992, 89:932-936.
247. Yang N., Mosher R., Seo S., Beebe D., Friedl A. Syndecan-1 in breast cancer stroma fibroblasts regulates extracellular matrix fiber organization and carcinoma cell motility. Am. J. Pathol. 2011, 178:325-335.
248. Conklin M.W., Eickhoff J.C., Riching K.M., Pehlke C.A., Eliceiri K.W., Provenzano P.P., Friedl A., Keely P.J. Aligned collagen is a prognostic signature for survival in human breast carcinoma. Am. J. Pathol. 2011, 178:1221-1232.
249. Oh E.S., Couchman J.R. Syndecans-2 and -4; close cousins, but not identical twins. Mol. Cells 2004, 17:181-187.
250. Barash U., Cohen-Kaplan V., Dowek I., Sanderson R.D., Ilan N., Vlodavsky I. Proteoglycans in health and disease: new concepts for heparanase function in tumor progression and metastasis. FEBS J. 2010, 277:3890-3903.
251. Arvatz G., Shafat I., Levy-Adam F., Ilan N., Vlodavsky I. The heparanase system and tumor metastasis: is heparanase the seed and soil?. Cancer Metastasis Rev. 2011, 30:253-268.
252. Hammond E., Khurana A., Shridhar V., Dredge K. The role of heparanase and sulfatases in the modification of heparan sulfate proteoglycans within the tumor microenvironment and opportunities for novel cancer therapeutics. Front Oncol 2014, 4:195.
253. Gotte M., Yip G.W. Heparanase, hyaluronan, and CD44 in cancers: a breast carcinoma perspective. Cancer Res. 2006, 66:10233-10237.
254. Gomes A.M., Stelling M.P., Pavao M.S. Heparan sulfate and heparanase as modulators of breast cancer progression. Biomed. Res. Int. 2013, 2013:852093.
255. Peterson S.B., Liu J. Multi-faceted substrate specificity of heparanase. Matrix Biol. 2013, 32:223-227.
256. Gingis-Velitski S., Zetser A., Flugelman M.Y., Vlodavsky I., Ilan N. Heparanase induces endothelial cell migration via protein kinase B/Akt activation. J. Biol. Chem. 2004, 279:23536-23541.
257. Sotnikov I., Hershkoviz R., Grabovsky V., Ilan N., Cahalon L., Vlodavsky I., Alon R., Lider O. Enzymatically quiescent heparanase augments T cell interactions with VCAM-1 and extracellular matrix components under versatile dynamic contexts. J. Immunol. 2004, 172:5185-5193.
258. Ramani V.C., Yang Y., Ren Y., Nan L., Sanderson R.D. Heparanase plays a dual role in driving hepatocyte growth factor (HGF) signaling by enhancing HGF expression and activity. J. Biol. Chem. 2011, 286:6490-6499.
259. Nadir Y., Brenner B., Gingis-Velitski S., Levy-Adam F., Ilan N., Zcharia E., Nadir E., Vlodavsky I. Heparanase induces tissue factor pathway inhibitor expression and extracellular accumulation in endothelial and tumor cells. Thromb. Haemost. 2008, 99:133-141.
260. Maxhimer J.B., Quiros R.M., Stewart R., Dowlatshahi K., Gattuso P., Fan M., Prinz R.A., Xu X. Heparanase-1 expression is associated with the metastatic potential of breast cancer. Surgery 2002, 132:326-333.
261. Gawthorpe S., Brown J.E., Arif M., Nightingale P., Nevill A., Carmichael A.R. Heparanase and COX-2 expression as predictors of lymph node metastasis in large, high-grade breast tumors. Anticancer Res 2014, 34:2797-2800.
262. Maxhimer J.B., Pesce C.E., Stewart R.A., Gattuso P., Prinz R.A., Xu X. Ductal carcinoma in situ of the breast and heparanase-1 expression: a molecular explanation for more aggressive subtypes. J. Am. Coll. Surg. 2005, 200:328-335.
263. Tang D., Zhang Q., Zhao S., Wang J., Lu K., Song Y., Zhao L., Kang X., Wang J., Xu S., Tian L. The expression and clinical significance of microRNA-1258 and heparanase in human breast cancer. Clin. Biochem. 2013, 46:926-932.
264. Cohen I., Pappo O., Elkin M., San T., Bar-Shavit R., Hazan R., Peretz T., Vlodavsky I., Abramovitch R. Heparanase promotes growth, angiogenesis and survival of primary breast tumors. Int. J. Cancer 2006, 118:1609-1617.
265. Zetser A., Bashenko Y., Edovitsky E., Levy-Adam F., Vlodavsky I., Ilan N. Heparanase induces vascular endothelial growth factor expression: correlation with p38 phosphorylation levels and Src activation. Cancer Res. 2006, 66:1455-1463.
266. Edovitsky E., Elkin M., Zcharia E., Peretz T., Vlodavsky I. Heparanase gene silencing, tumor invasiveness, angiogenesis, and metastasis. J. Natl. Cancer Inst. 2004, 96:1219-1230.
267. Zhang Z.H., Chen Y., Zhao H.J., Xie C.Y., Ding J., Hou Y.T. Silencing of heparanase by siRNA inhibits tumor metastasis and angiogenesis of human breast cancer in vitro and in vivo. Cancer Biol. Ther. 2007, 6:587-595.
268. Ridgway L.D., Wetzel M.D., Ngo J.A., Erdreich-Epstein A., Marchetti D. Heparanase-induced GEF-H1 signaling regulates the cytoskeletal dynamics of brain metastatic breast cancer cells. Mol. Cancer Res. 2012, 10:689-702.
269. Zhang L., Sullivan P.S., Goodman J.C., Gunaratne P.H., Marchetti D. MicroRNA-1258 suppresses breast cancer brain metastasis by targeting heparanase. Cancer Res. 2011, 71:645-654.
270. Zhang L., Ridgway L.D., Wetzel M.D., Ngo J., Yin W., Kumar D., Goodman J.C., Groves M.D., Marchetti D. The identification and characterization of breast cancer CTCs competent for brain metastasis. Sci. Transl. Med. 2013, 5:180ra148.
271. Manon-Jensen T., Itoh Y., Couchman J.R. Proteoglycans in health and disease: the multiple roles of syndecan shedding. FEBS J. 2010, 277:3876-3889.
272. Su G., Blaine S.A., Qiao D., Friedl A. Shedding of syndecan-1 by stromal fibroblasts stimulates human breast cancer cell proliferation via FGF2 activation. J. Biol. Chem. 2007, 282:14906-14915.
273. Manon-Jensen T., Multhaupt H.A., Couchman J.R. Mapping of matrix metalloproteinase cleavage sites on syndecan-1 and syndecan-4 ectodomains. FEBS J. 2013, 280:2320-2331.
274. Teng Y.H., Aquino R.S., Park P.W. Molecular functions of syndecan-1 in disease. Matrix Biol. 2012, 31:3-16.
275. Purushothaman A., Chen L., Yang Y., Sanderson R.D. Heparanase stimulation of protease expression implicates it as a master regulator of the aggressive tumor phenotype in myeloma. J. Biol. Chem. 2008, 283:32628-32636.
276. Purushothaman A., Uyama T., Kobayashi F., Yamada S., Sugahara K., Rapraeger A.C., Sanderson R.D. Heparanase-enhanced shedding of syndecan-1 by myeloma cells promotes endothelial invasion and angiogenesis. Blood 2010, 115:2449-2457.
277. Ding K., Lopez-Burks M., Sanchez-Duran J.A., Korc M., Lander A.D. Growth factor-induced shedding of syndecan-1 confers glypican-1 dependence on mitogenic responses of cancer cells. J. Cell Biol. 2005, 171:729-738.
278. Kelly T., Suva L.J., Huang Y., Macleod V., Miao H.Q., Walker R.C., Sanderson R.D. Expression of heparanase by primary breast tumors promotes bone resorption in the absence of detectable bone metastases. Cancer Res. 2005, 65:5778-5784.
279. Kelly T., Suva L.J., Nicks K.M., MacLeod V., Sanderson R.D. Tumor-derived syndecan-1 mediates distal cross-talk with bone that enhances osteoclastogenesis. J. Bone Miner. Res. 2010, 25:1295-1304.
280. Yang C., Robbins P.D. The roles of tumor-derived exosomes in cancer pathogenesis. Clin. Dev. Immunol. 2011, 2011:842849.
281. Record M., Subra C., Silvente-Poirot S., Poirot M. Exosomes as intercellular signalosomes and pharmacological effectors. Biochem. Pharmacol. 2011, 81:1171-1182.
282. Zhang H.G., Grizzle W.E. Exosomes: a novel pathway of local and distant intercellular communication that facilitates the growth and metastasis of neoplastic lesions. Am. J. Pathol. 2014, 184:28-41.
283. Peinado H., Aleckovic M., Lavotshkin S., Matei I., Costa-Silva B., Moreno-Bueno G., Hergueta-Redondo M., Williams C., Garcia-Santos G., Ghajar C.M., Nitadori-Hoshino A., Hoffman C., Badal K., Garcia B.A., Callahan M.K., Yuan J., Martins V.R., Skog J., Kaplan R.N., Brady M.S., Wolchok J.D., Chapman P.B., Kang Y., Bromberg J., Lyden D. Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. Nat. Med. 2012, 18:883-891.
284. Luga V., Zhang L., Viloria-Petit A.M., Ogunjimi A.A., Inanlou M.R., Chiu E., Buchanan M., Hosein A.N., Basik M., Wrana J.L. Exosomes mediate stromal mobilization of autocrine Wnt-PCP signaling in breast cancer cell migration. Cell 2012, 151:1542-1556.
285. Zhou W., Fong M.Y., Min Y., Somlo G., Liu L., Palomares M.R., Yu Y., Chow A., O'Connor S.T., Chin A.R., Yen Y., Wang Y., Marcusson E.G., Chu P., Wu J., Wu X., Li A.X., Li Z., Gao H., Ren X., Boldin M.P., Lin P.C., Wang S.E. Cancer-secreted miR-105 destroys vascular endothelial barriers to promote metastasis. Cancer Cell 2014, 25:501-515.
286. Chen W.X., Liu X.M., Lv M.M., Chen L., Zhao J.H., Zhong S.L., Ji M.H., Hu Q., Luo Z., Wu J.Z., Tang J.H. Exosomes from drug-resistant breast cancer cells transmit chemoresistance by a horizontal transfer of microRNAs. PLoS One 2014, 9:e95240.
287. Wei Y., Lai X., Yu S., Chen S., Ma Y., Zhang Y., Li H., Zhu X., Yao L., Zhang J. Exosomal miR-221/222 enhances tamoxifen resistance in recipient ER-positive breast cancer cells. Breast Cancer Res. Treat. 2014, 147:423-431.
288. Chen W.X., Cai Y.Q., Lv M.M., Chen L., Zhong S.L., Ma T.F., Zhao J.H., Tang J.H. Exosomes from docetaxel-resistant breast cancer cells alter chemosensitivity by delivering microRNAs. Tumour Biol. J. Int. Soc. Oncodev. Biol. Med. 2014, 35:9649-9659.
289. Lim P.K., Bliss S.A., Patel S.A., Taborga M., Dave M.A., Gregory L.A., Greco S.J., Bryan M., Patel P.S., Rameshwar P. Gap junction-mediated import of microRNA from bone marrow stromal cells can elicit cell cycle quiescence in breast cancer cells. Cancer Res. 2011, 71:1550-1560.
290. Muralidharan-Chari V., Clancy J.W., Sedgwick A., D'Souza-Schorey C. Microvesicles: mediators of extracellular communication during cancer progression. J. Cell Sci. 2010, 123:1603-1611.
291. Harding C.V., Heuser J.E., Stahl P.D. Exosomes: looking back three decades and into the future. J. Cell Biol. 2013, 200:367-371.
292. Henne W.M., Buchkovich N.J., Emr S.D. The ESCRT pathway. Dev. Cell 2011, 21:77-91.
293. Ostrowski M., Carmo N.B., Krumeich S., Fanget I., Raposo G., Savina A., Moita C.F., Schauer K., Hume A.N., Freitas R.P., Goud B., Benaroch P., Hacohen N., Fukuda M., Desnos C., Seabra M.C., Darchen F., Amigorena S., Moita L.F., Thery C. Rab27a and Rab27b control different steps of the exosome secretion pathway. Nat. Cell Biol. 2010, 12:19-30.
294. Thompson C.A., Purushothaman A., Ramani V.C., Vlodavsky I., Sanderson R.D. Heparanase regulates secretion, composition, and function of tumor cell-derived exosomes. J. Biol. Chem. 2013, 288:10093-10099.
295. Filmus J., Capurro M., Rast J. Glypicans. Genome Biol. 2008, 9:224.
296. Traister A., Shi W., Filmus J. Mammalian notum induces the release of glypicans and other GPI-anchored proteins from the cell surface. Biochem. J. 2008, 410:503-511.
297. De Cat B., Muyldermans S.Y., Coomans C., Degeest G., Vanderschueren B., Creemers J., Biemar F., Peers B., David G. Processing by proprotein convertases is required for glypican-3 modulation of cell survival, Wnt signaling, and gastrulation movements. J. Cell Biol. 2003, 163:625-635.
298. Svensson G., Awad W., Hakansson M., Mani K., Logan D.T. Crystal structure of N-glycosylated human glypican-1 core protein: structure of two loops evolutionary conserved in vertebrate glypican-1. J. Biol. Chem. 2012, 287:14040-14051.
299. Fico A., de Chevigny A., Egea J., Bosl M.R., Cremer H., Maina F., Dono R. Modulating Glypican4 suppresses tumorigenicity of embryonic stem cells while preserving self-renewal and pluripotency. Stem Cells 2012, 30:1863-1874.
300. Gao W., Kim H., Feng M., Phung Y., Xavier C.P., Rubin J.S., Ho M. Inactivation of Wnt signaling by a human antibody that recognizes the heparan sulfate chains of glypican-3 for liver cancer therapy. Hepatology 2014, 60:576-587.
301. Shiba K., Hu N., Bronner-Fraser M. Altering glypican-1 levels modulates canonical Wnt signaling during trigeminal placode development. Dev. Biol. 2010, 348:107-118.
302. Song H.H., Shi W., Xiang Y., Filmus J. The loss of Glypican-3 induces alterations in Wnt signaling. J. Biol. Chem. 2005, 280:2116-2125.
303. Topczewsky J., Sepich D.S., Myers D.C., Walker C., Amores A., Lele Z., Hammerschmidt M., Postlethwait J., Solnica-Krezel L. The zebrafish glypican knypek controls cell polarity during gastrulation movements of convergent extension. Dev. Cell 2001, 1:251-264.
304. Tsuda M., Kamimura K., Nakato H., Archer M., Staatz W., Fox B., Humphrey M., Olson S., Futch T., Kaluza V., Siegfried E., Stam L., Selleck S.B. The cell-surface proteoglycan Dally regulates Wingless signaling in Drosophila. Nature 1999, 400:276-280.
305. Yan D., Wu Y., Feng Y., Lin S.C., Lin X. The core protein of glypican Dally-like determines its biphasic activity in wingless morphogen signaling. Dev. Cell 2009, 17:470-481.
306. Capurro M.I., Xu P., Shi W., Li F., Jia A., Filmus J. Glypican-3 inhibits hedgehog signaling during development by competing with patched for hedgehog binding. Dev. Cell 2008, 14:700-711.
307. Desbordes S.C., Sanson B. The glypican Dally-like is required for hedgehog signalling in the embryonic epidermis of Drosophila. Development 2003, 130:6245-6255.
308. Li F., Shi W., Capurro M., Filmus J. Glypican-5 stimulates rhabdomyosarcoma cell proliferation by activating Hedgehog signaling. J. Cell Biol. 2011, 192:691-704.
309. Lum L., Yao S., Mozer B., Rovescalli A., Von Kessler D., Nirenberg M., Beachy P.A. Identification of hedgehog pathway components by RNAi in Drosophila cultured cells. Science 2003, 299:2039-2045.
310. Rawson J.M., Dimitroff B., Johnson K.G., Rawson J.M., Ge X., Van Vactor D., Selleck S.B. The heparan sulfate proteoglycans Dally-like and Syndecan have distinct functions in axon guidance and visual-system assembly in Drosophila. Curr. Biol. 2005, 15:833-838.
311. Belenkaya T.Y., Han C., Yan D., Opoka R.J., Khodoun M., Liu H., Lin X. Drosophila Dpp morphogen movement is independent of dynamin-mediated endocytosis but regulated by the glypican members of heparan sulfate proteoglycans. Cell 2004, 119:231-244.
312. Fujise M., Takeo S., Kamimura K., Matsuo T., Aigaki T., Izumi S., Nakato H. Dally regulates Dpp morphogen gradient formation in the Drosophila wing. Development 2003, 130:1515-1522.
313. Kuo W.J., Digman M.A., Lander A.D. Heparan sulfate acts as a bone morphogenetic protein coreceptor by facilitating ligand-induced receptor hetero-oligomerization. Mol. Biol. Cell 2010, 21:4028-4041.
314. Taneja-Bageshwar S., Gumienny T.L. Two functional domains in C. elegans glypican LON-2 can indepepndently inhibit BMP-like signaling. Dev. Biol. 2012, 371:66-76.
315. Gutierrez J., Brandan E. A novel mechanism of sequestering FGF-2 by glypican in lipid rafts, allowing skeletal muscle differentiation. Mol. Cell. Biol. 2010, 30:1634-1649.
316. Okamoto K., Tokunaga K., Doi K., Fujita T., Suzuki H., Katoh T., Watanabe T., Nishida N., Mabuchi A., Takahashi A., Kubo M., Maeda S., Nakamura Y., Noiri E. Common variation in GPC5 is associated with acquired nephrotic syndrome. Nat. Genet. 2011, 43:459-463.
317. Ayers K.L., Gallet A., Staccini-Lavenant L., Therond P.P. The long-range activity of hedgehog is regulated in the apical extracellular space by the glypican Dally and the hydrolase Notum. Dev. Cell 2010, 18:605-620.
318. Eugster C., Panakova D., Mahmoud A., Eaton S. Lipoprotein-heparan sulfate interactions in the Hh pathway. Dev. Cell 2007, 13:57-71.
319. Vyas N., Goswami D., Manonmani A., Sharma P., Ranganath H.A., VijayRaghavan K., Shashidhara L.S., Sowdhamini R., Mayor S. Nanoscale organization of hedgehog is essential for long-range signaling. Cell 2008, 133:1214-1227.
320. Yan D., Wu Y., Yang Y., Belenkaya T.Y., Tang X., Lin X. The cell-surface proteins Dally-like and Ihog differentially regulate Hedgehog signaling strength and range during development. Development 2010, 137:2033-2044.
321. Franch-Marro X., Marchand O., Piddini E., Ricardo S., Alexandre C., Vincent J.P. Glypicans shunt the wingless signal between local signalling and further transport. Development 2005, 132:659-666.
322. Gallet A., Staccini-Lavenant L., Therond P.P. Cellular trafficking of the glypican Dally-like is required for full-strength hedgehog signaling and wingless transcytosis. Dev. Cell 2008, 14:712-725.
323. Kreuger J., Perez L., Giraldez A.J., Cohen S.M. Opposing activities of Dally-like glypican at high and low levels of Wingless morphogen activity. Dev. Cell 2004, 7:503-512.
324. Smart A.D., Course M.M., Rawson J., Selleck S.B., Van Vactor D., Johnson K.G. Heparan sulfate proteoglycan specificity during axon pathway formation in Drosophila embryo. Dev. Neurobiol. 2011, 71:608-618.
325. Allen N.J., Bennett M.L., Foo L.C., Wang G.X., Chakraborty C., Smith S.J., Barres B.A. Astrocyte glypicans 4 and 6 promote formation of excitatory synapses via GluA1 AMPA receptors. Nature 2012, 486:410-414.
326. de Wit J., O'sullivan M.L., Savas J.N., Condomitti G., Caccese M.C., Vennekens K.M., Yates J.R., Ghosh A. Unbiased discovery of glypican as a receptor for LRRTM4 in regulating excitatory synapse development. Neuron 2013, 79:1-16.
327. Capurro M., Xiang Y.Y., Lobe C., Filmus J. Glypican-3 promotes the growth of hepatocellular carcinoma by stimulating canonical Wnt signaling. Cancer Res. 2005, 65:6245-6254.
328. Murthy S.S., Shen T., De Rienzo A., Lee W.C., Ferriola P.C., Jhanwar S.C., Mossman B.T., Filmus J., Testa J.R. Expression of GPC3, an X-linked recessive overgrowth gene, is silenced in malignant mesothelioma. Oncogene 2000, 19:410-416.
329. Xiang Y.Y., Ladeda V., Filmus J. Glypican-3 expression is silenced in human breast cancer. Oncogene 2001, 20:7408-7412.
330. Matsuda K., Maruyama H., Guo F., Kleeff J., Itakura J., Matsumoto Y., Lander A.D., Korc M. Glypican-1 is overexpressed in human breast cancer and modulates the mitogenic effects of multiple heparin-binding growth factors in breast cancer cells. Cancer Res. 2001, 61:5562-5569.
331. Yan P.S., Chen C.M., Shi H., Rahmatpanah F., Wei S.H., Caldwell C.W., Huang T.H.M. Dissecting complex epigenetic alterations in breast cancer using CpG island microarrays. Cancer Res. 2001, 61:8375-8380.
332. Peters M.G., Farias E., Colombo L., Filmus J., Puricelli L., Bal de Kier Joffe E. Inhibition of invasion and metastasis by glypican-3 in a syngeneic breast cancer model. Breast Cancer Res. Treat. 2003, 80:221-232.
333. Yiu G.K., Kaunisto A., Chin R., Toker A. NFAT promotes carcinoma invasive migration through glypican-6. Biochem. J. 2011, 440:157-166.
334. Korpetinou A., Skandalis S.S., Labropoulou V.T., Smirlaki G., Noulas A., Karamanos N.K., Theocharis A.D. Serglycin: at the crossroad of inflammation and malignancy. Front Oncol 2014, 3:327.
335. Meen A.J., Oynebraten I., Reine T.M., Duelli A., Svennevig K., Pejler G., Jenssen T., Kolset S.O. Serglycin is a major proteoglycan in polarized human endothelial cells and is implicated in the secretion of the chemokine GROalpha/CXCL1. J. Biol. Chem. 2011, 286:2636-2647.
336. Tyan S.W., Hsu C.H., Peng K.L., Chen C.C., Kuo W.H., Lee E.Y., Shew J.Y., Chang K.J., Juan L.J., Lee W.H. Breast cancer cells induce stromal fibroblasts to secrete ADAMTS1 for cancer invasion through an epigenetic change. PLoS One 2012, 7:e35128.
337. Pejler G., Sadler J.E. Mechanism by which heparin proteoglycan modulates mast cell chymase activity. Biochemistry 1999, 38:12187-12195.
338. Lindstedt L., Lee M., Kovanen P.T. Chymase bound to heparin is resistant to its natural inhibitors and capable of proteolyzing high density lipoproteins in aortic intimal fluid. Atherosclerosis 2001, 155:87-97.
339. Pejler G., Berg L. Regulation of rat mast cell protease 1 activity. Protease inhibition is prevented by heparin proteoglycan. Eur. J. Biochem. 1995, 233:192-199.
340. Hallgren J., Spillmann D., Pejler G. Structural requirements and mechanism for heparin-induced activation of a recombinant mouse mast cell tryptase, mouse mast cell protease-6: formation of active tryptase monomers in the presence of low molecular weight heparin. J. Biol. Chem. 2001, 276:42774-42781.
341. Sakai K., Ren S., Schwartz L.B. A novel heparin-dependent processing pathway for human tryptase. Autocatalysis followed by activation with dipeptidyl peptidase I. J. Clin. Invest. 1996, 97:988-995.
342. Zhang L., Yang M., Yang D., Cavey G., Davidson P., Gibson G. Molecular interactions of MMP-13 C-terminal domain with chondrocyte proteins. Connect. Tissue Res. 2010, 51:230-239.
343. Malla N., Berg E., Theocharis A.D., Svineng G., Uhlin-Hansen L., Winberg J.O. In vitro reconstitution of complexes between pro-matrix metalloproteinase-9 and the proteoglycans serglycin and versican. FEBS J. 2013, 280:2870-2887.
344. Winberg J.O., Kolset S.O., Berg E., Uhlin-Hansen L. Macrophages secrete matrix metalloproteinase 9 covalently linked to the core protein of chondroitin sulphate proteoglycans. J. Mol. Biol. 2000, 304:669-680.
345. Winberg J.O., Berg E., Kolset S.O., Uhlin-Hansen L. Calcium-induced activation and truncation of promatrix metalloproteinase-9 linked to the core protein of chondroitin sulfate proteoglycans. Eur. J. Biochem. 2003, 270:3996-4007.
346. Labropoulou V.T., Theocharis A.D., Symeonidis A., Skandalis S.S., Karamanos N.K., Kalofonos H.P. Pathophysiology and pharmacological targeting of tumor-induced bone disease: current status and emerging therapeutic interventions. Curr. Med. Chem. 2011, 18:1584-1598.
347. Theocharis A.D., Seidel C., Borset M., Dobra K., Baykov V., Labropoulou V., Kanakis I., Dalas E., Karamanos N.K., Sundan A., Hjerpe A. Serglycin constitutively secreted by myeloma plasma cells is a potent inhibitor of bone mineralization in vitro. J. Biol. Chem. 2006, 281:35116-35128.
348. Purushothaman A., Toole B.P. Serglycin proteoglycan is required for multiple myeloma cell adhesion, in vivo growth, and vascularization. J. Biol. Chem. 2014, 289:5499-5509.
349. Skliris A., Labropoulou V.T., Papachristou D.J., Aletras A., Karamanos N.K., Theocharis A.D. Cell-surface serglycin promotes adhesion of myeloma cells to collagen type I and affects the expression of matrix metalloproteinases. FEBS J. 2013, 280:2342-2352.
350. He L., Zhou X., Qu C., Tang Y., Zhang Q., Hong J. Serglycin (SRGN) overexpression predicts poor prognosis in hepatocellular carcinoma patients. Med. Oncol. 2013, 30:707.
351. Li X.J., Ong C.K., Cao Y., Xiang Y.Q., Shao J.Y., Ooi A., Peng L.X., Lu W.H., Zhang Z., Petillo D., Qin L., Bao Y.N., Zheng F.J., Chia C.S., Iyer N.G., Kang T.B., Zeng Y.X., Soo K.C., Trent J.M., Teh B.T., Qian C.N. Serglycin is a theranostic target in nasopharyngeal carcinoma that promotes metastasis. Cancer Res. 2011, 71:3162-3172.
352. Cooney C.A., Jousheghany F., Yao-Borengasser A., Phanavanh B., Gomes T., Kieber-Emmons A.M., Siegel E.R., Suva L.J., Ferrone S., Kieber-Emmons T., Monzavi-Karbassi B. Chondroitin sulfates play a major role in breast cancer metastasis: a role for CSPG4 and CHST11 gene expression in forming surface P-selectin ligands in aggressive breast cancer cells. Breast Cancer Res. 2011, 13:R58.
353. Skliris A., Happonen K.E., Terpos E., Labropoulou V., Borset M., Heinegard D., Blom A.M., Theocharis A.D. Serglycin inhibits the classical and lectin pathways of complement via its glycosaminoglycan chains: implications for multiple myeloma. Eur. J. Immunol. 2011, 41:437-449.
354. Raman K., Kuberan B. Chemical tumor biology of heparan sulfate proteoglycans. Curr. Chem. Biol. 2010, 4:20-31.
355. Casu B., Naggi A., Torri G. Heparin-derived heparan sulfate mimics to modulate heparan sulfate-protein interaction in inflammation and cancer. Matrix Biol. 2010, 29:442-452.
356. Kuberan B., Ethirajan M., Victor X.V., Tran V., Nguyen K., Do A. "Click" xylosides initiate glycosaminoglycan biosynthesis in a mammalian cell line. Chembiochem 2008, 9:198-200.
357. Garud D.R., Tran V.M., Victor X.V., Koketsu M., Kuberan B. Inhibition of heparan sulfate and chondroitin sulfate proteoglycan biosynthesis. J. Biol. Chem. 2008, 283:28881-28887.
358. Gingis-Velitski S., Zetser A., Kaplan V., Ben-Zaken O., Cohen E., Levy-Adam F., Bashenko Y., Flugelman M.Y., Vlodavsky I., Ilan N. Heparanase uptake is mediated by cell membrane heparan sulfate proteoglycans. J. Biol. Chem. 2004, 279:44084-44092.
359. Christianson H.C., Svensson K.J., van Kuppevelt T.H., Li J.P., Belting M. Cancer cell exosomes depend on cell-surface heparan sulfate proteoglycans for their internalization and functional activity. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:17380-17385.
360. Ritchie J.P., Ramani V.C., Ren Y., Naggi A., Torri G., Casu B., Penco S., Pisano C., Carminati P., Tortoreto M., Zunino F., Vlodavsky I., Sanderson R.D., Yang Y. SST0001, a chemically modified heparin, inhibits myeloma growth and angiogenesis via disruption of the heparanase/syndecan-1 axis. Clin. Cancer Res. Off. J. Am. Assoc. Cancer Res. 2011, 17:1382-1393.
361. Zhou H., Roy S., Cochran E., Zouaoui R., Chu C.L., Duffner J., Zhao G., Smith S., Galcheva-Gargova Z., Karlgren J., Dussault N., Kwan R.Y., Moy E., Barnes M., Long A., Honan C., Qi Y.W., Shriver Z., Ganguly T., Schultes B., Venkataraman G., Kishimoto T.K. M402, a novel heparan sulfate mimetic, targets multiple pathways implicated in tumor progression and metastasis. PLoS One 2011, 6:e21106.
362. Dredge K., Hammond E., Handley P., Gonda T.J., Smith M.T., Vincent C., Brandt R., Ferro V., Bytheway I. PG545, a dual heparanase and angiogenesis inhibitor, induces potent anti-tumour and anti-metastatic efficacy in preclinical models. Br. J. Cancer 2011, 104:635-642.
363. Hammond E., Brandt R., Dredge K. PG545, a heparan sulfate mimetic, reduces heparanase expression in vivo, blocks spontaneous metastases and enhances overall survival in the 4T1 breast carcinoma model. PLoS One 2012, 7:e52175.
364. Barbouri D., Afratis N., Gialeli C., Vynios D.H., Theocharis A.D., Karamanos N.K. Syndecans as modulators and potential pharmacological targets in cancer progression. Front. Oncol. 2014, 4:4.
365. Choi S., Kang D.H., Oh E.S. Targeting syndecans: a promising strategy for the treatment of cancer. Expert Opin. Ther. Targets 2013, 17:695-705.
366. Malavaki C.J., Roussidis A.E., Gialeli C., Kletsas D., Tsegenidis T., Theocharis A.D., Tzanakakis G.N., Karamanos N.K. Imatinib as a key inhibitor of the platelet-derived growth factor receptor mediated expression of cell surface heparan sulfate proteoglycans and functional properties of breast cancer cells. FEBS J. 2013, 280:2477-2489.
367. Rousseau C., Ferrer L., Supiot S., Bardies M., Davodeau F., Faivre-Chauvet A., Baumgartner P., Wijdenes J., Lacombe M., Barbet J., Guillaume T., Moreau P., Harousseau J.L., Kraeber-Bodere F., Cherel M. Dosimetry results suggest feasibility of radioimmunotherapy using anti-CD138 (B-B4) antibody in multiple myeloma patients. Tumour Biol. J. Int. Soc. Oncodev. Biol. Med. 2012, 33:679-688.
368. Rousseau C., Ruellan A.L., Bernardeau K., Kraeber-Bodere F., Gouard S., Loussouarn D., Sai-Maurel C., Faivre-Chauvet A., Wijdenes J., Barbet J., Gaschet J., Cherel M., Davodeau F. Syndecan-1 antigen, a promising new target for triple-negative breast cancer immuno-PET and radioimmunotherapy. A preclinical study on MDA-MB-468 xenograft tumors. EJNMMI Res. 2011, 1:20.
369. Rapraeger A.C. Synstatin: a selective inhibitor of the syndecan-1-coupled IGF1R-alphavbeta3 integrin complex in tumorigenesis and angiogenesis. FEBS J. 2013, 280:2207-2215.
370. Ween M.P., Hummitzsch K., Rodgers R.J., Oehler M.K., Ricciardelli C. Versican induces a pro-metastatic ovarian cancer cell behavior which can be inhibited by small hyaluronan oligosaccharides. Clin. Exp. Metastasis 2011, 28:113-125.
371. Nastase M.V., Iozzo R.V., Schaefer L. Key roles for the small leucine-rich proteoglycans in renal and pulmonary pathophysiology. Biochim. Biophys. Acta 2014, 1840:2460-2470.
372. Tralhao J.G., Schaefer L., Micegova M., Evaristo C., Schonherr E., Kayal S., Veiga-Fernandes H., Danel C., Iozzo R.V., Kresse H., Lemarchand P. In vivo selective and distant killing of cancer cells using adenovirus-mediated decorin gene transfer. FASEB J. 2003, 17:464-466.