Roles of versican in cancer biology - Tumorigenesis, progression and metastasis

Histology and Histopathology

Volumn 28, Issue 6, 2013, Pages 701-713

  Du, William Weidong ^a,b   Yang, Weining ^a,b   Yee, Albert J ^a,b  

^a Sunnybrook Health Sciences Centre   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

Apoptosis; Invasion; Metastasis; Tumorigenesis; Versican

Indexed keywords

VCAN PROTEIN, HUMAN; VERSICAN;

CELL TRANSFORMATION; CELLULAR, SUBCELLULAR AND MOLECULAR BIOLOGICAL PHENOMENA AND FUNCTIONS; DISEASE COURSE; FEMALE; GENE EXPRESSION REGULATION; GENETICS; HUMAN; MALE; METABOLISM; MOLECULARLY TARGETED THERAPY; NEOPLASM; PATHOLOGY; REVIEW;

CELL PHYSIOLOGICAL PROCESSES; CELL TRANSFORMATION, NEOPLASTIC; DISEASE PROGRESSION; FEMALE; GENE EXPRESSION REGULATION; HUMANS; MALE; MOLECULAR TARGETED THERAPY; NEOPLASMS; VERSICANS;

EID: 84878973564     PISSN: 02133911     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (139)

1. Almholt K., Juncker-Jensen A., Laerum O.D., Dano K., Johnsen M., Lund L.R. and Romer J. (2008). Metastasis is strongly reduced by the matrix metalloproteinase inhibitor Galardin in the MMTV-PymT transgenic breast cancer model. Mol. Cancer Ther. 7, 2758-2767.
2. Ang L.C., Zhang Y., Cao L., Yang B.L., Young B., Kiani C., Lee V., Allan K. and Yang B.B. (1999). Versican enhances locomotion of astrocytoma cells and reduces cell adhesion through its G1 domain. J. Neuropathol. Exp. Neurol. 58, 597-605.
3. Arslan F., Bosserhoff A.K., Nickl-Jockschat T., Doerfelt A., Bogdahn U. and Hau P. (2007). The role of versican isoforms V0/V1 in glioma migration mediated by transforming growth factor-beta2. Br. J. Cancer 96, 1560-1568.
4. Asimakopoulou A.P., Theocharis A.D., Tzanakakis G.N. and Karamanos N.K. (2008). The biological role of chondroitin sulfate in cancer and chondroitin-based anticancer agents. In Vivo 22, 385-389.
5. Aspberg A., Binkert C. and Ruoslahti E. (1995). The versican C-type lectin domain recognizes the adhesion protein tenascin-R. Proc. Natl. Acad. Sci. USA 92, 10590-10594.
6. Aspberg A., Adam S., Kostka G., Timpl R. and Heinegard D. (1999). Fibulin-1 is a ligand for the C-type lectin domains of aggrecan and versican. J. Biol. Chem. 274, 20444-20449.
7. Bensadoun E.S., Burke A.K., Hogg J.C. and Roberts C.R. (1997). Proteoglycans in granulomatous lung diseases. Eur. Respir. J. 10, 2731-2737.
8. Berdiaki A., Zafiropoulos A., Fthenou E., Katonis P., Tsatsakis A., Karamanos N.K. and Tzanakakis G.N. (2008). Regulation of hyaluronan and versican deposition by growth factors in fibrosarcoma cell lines. Biochim. Biophys. Acta 1780, 194-202.
9. Burgess J.K., Oliver B.G., Poniris M.H., Ge Q., Boustany S., Cox N., Moir L.M., Johnson P.R. and Black J.L. (2006). A phosphodiesterase 4 inhibitor inhibits matrix protein deposition in airways in vitro. J. Allergy Clin. Immunol. 118, 649-657.
10. Casey R.C., Koch K.A., Oegema T.R., Skubitz K.M., Pambuccian S.E., Grindle S.M. and Skubitz A.P. (2003). Establishment of an in vitro assay to measure the invasion of ovarian carcinoma cells through mesothelial cell monolayers. Clin. Exp. Metastasis 20, 343-356.
11. Cattaruzza S., Schiappacassi M., Kimata K., Colombatti A. and Perris R. (2004). The globular domains of PG-M/versican modulate the proliferation-apoptosis equilibrium and invasive capabilities of tumor cells. FASEB J. 18, 779-781.
12. Cross N.A., Chandrasekharan S., Jokonya N., Fowles A., Hamdy F.C., Buttle D.J. and Eaton C.L. (2005). The expression and regulation of ADAMTS-1,-4,-5,-9, and-15, and TIMP-3 by TGFbeta1 in prostate cells: relevance to the accumulation of versican. Prostate 63, 269-275.
13. Domenzain C., Docampo M.J., Serra M., Miquel L. and Bassols, A. (2003). Differential expression of versican isoforms is a component of the human melanoma cell differentiation process. Biochim. Biophys. Acta. 1642, 107-114.
14. Domenzain-Reyna C., Hernandez D., Miquel-Serra L., Docampo M.J., Badenas C., Fabra A. and Bassols A. (2009). Structure and regulation of the versican promoter: the versican promoter is regulated by AP-1 and TCF transcription factors in invasive human melanoma cells. J. Biol. Chem. 284, 12306-12317.
15. Dondeti V.R., Wubbenhorst B., Lal P., Gordan J.D., D'Andrea K., Attiyeh E.F., Simon M.C. and Nathanson K.L. (2012). Integrative genomic analyses of sporadic clear cell renal cell carcinoma define disease subtypes and potential new therapeutic targets. Cancer Res. 72, 112-121.
16. Dours-Zimmermann M.T. and Zimmermann D.R. (1994). A novel glycosaminoglycan attachment domain identified in two alternative splice variants of human versican. J. Biol. Chem. 269, 32992-32998.
17. Draffin J.E., McFarlane S., Hill A., Johnston P.G. and Waugh D.J. (2004). CD44 potentiates the adherence of metastatic prostate and breast cancer cells to bone marrow endothelial cells. Cancer Res. 64, 5702-5711.
18. Du W.W., Yang B.B., Shatseva T.A., Yang B.L., Deng Z., Shan S.W., Lee D.Y., Seth A. and Yee A.J. (2010). Versican G3 promotes mouse mammary tumor cell growth, migration, and metastasis by influencing EGF receptor signaling. PLoS One 5, e13828.
19. Du W.W., Yang B.B., Yang B.L., Deng Z., Fang L., Shan S.W., Jeyapalan Z., Zhang Y., Seth A. and Yee, A.J. (2011). Versican G3 domain modulates breast cancer cell apoptosis: a mechanism for breast cancer cell response to chemotherapy and EGFR therapy. PLoS One 6, e26396.
20. Du W.W., Fang L., Yang W., Sheng W., Zhang Y., Seth A., Yang B. and Yee A. (2012). The role of versican G3 domain in regulating breast cancer cell motility including effects on osteoblast cell growth and differentiation in vitro inverted question mark evaluation towards understanding breast cancer cell bone metastasis. BMC Cancer 12, 341.
21. Erdelyi I., van Asten A.J., van Dijk J.E. and Nederbragt H. (2005). Expression of versican in relation to chondrogenesis-related extracellular matrix components in canine mammary tumors. Histochem. Cell. Biol. 124, 139-149.
22. Evanko S.P., Angello J.C. and Wight T.N. (1999). Formation of hyaluronan-and versican-rich pericellular matrix is required for proliferation and migration of vascular smooth muscle cells. Arterioscler. Thromb. Vasc. Biol. 19, 1004-1013.
23. Evanko S.P., Johnson P.Y., Braun K.R., Underhill C.B., Dudhia J. and Wight T.N. (2001). Platelet-derived growth factor stimulates the formation of versican-hyaluronan aggregates and pericellular matrix expansion in arterial smooth muscle cells. Arch. Biochem. Biophys. 394, 29-38.
24. Fu Y., Nagy J.A., Brown L.F., Shih S.C., Johnson P.Y., Chan C.K., Dvorak H.F. and Wight, T.N. (2012). Proteolytic cleavage of versican and involvement of ADAMTS-1 in VEGF-A/VPF-induced pathological angiogenesis. J. Histochem. Cytochem. 59, 463-473.
25. Ghosh S., Albitar L., LeBaron R., Welch W.R., Samimi G., Birrer M.J., Berkowitz R.S. and Mok S.C. (2012). Up-regulation of stromal versican expression in advanced stage serous ovarian cancer. Gynecol. Oncol. 119, 114-120.
26. Gorter A., Zijlmans H.J., van Gent H., Trimbos J.B., Fleuren G.J. and Jordanova E.S. (2012). Versican expression is associated with tumor-infiltrating CD8-positive T cells and infiltration depth in cervical cancer. Mod. Pathol. 23, 1605-1615.
27. Gulyas M. and Hjerpe A. (2003). Proteoglycans and WT1 as markers for distinguishing adenocarcinoma, epithelioid mesothelioma, and benign mesothelium. J. Pathol. 199, 479-487.
28. Haase H.R., Clarkson R.W., Waters M.J. and Bartold P.M. (1998). Growth factor modulation of mitogenic responses and proteoglycan synthesis by human periodontal fibroblasts. J. Cell Physiol. 174, 353-361.
29. Halpert I., Sires U.I., Roby J.D., Potter-Perigo S., Wight T.N., Shapiro S.D., Welgus H.G., Wickline S.A. and Parks W.C. (1996). Matrilysin is expressed by lipid-laden macrophages at sites of potential rupture in atherosclerotic lesions and localizes to areas of versican deposition, a proteoglycan substrate for the enzyme. Proc. Natl. Acad. Sci. USA 93, 9748-9753.
30. Hamamura K., Zhang P. and Yokota H. (2008). IGF2-driven PI3 kinase and TGFbeta signaling pathways in chondrogenesis. Cell. Biol. Int. 32, 1238-1246.
31. Hanahan D and Weinberg R.A. (2000). The hallmarks of cancer. Cell 100, 57-70.
32. Hanekamp E.E., Gielen S.C., Smid-Koopman E., Kuhne L.C., de Ruiter P.E., Chadha-Ajwani S., Brinkmann A.O., Grootegoed J.A., Burger C.W., Huikeshoven F.J. and Blok L.J. (2003). Consequences of loss of progesterone receptor expression in development of invasive endometrial cancer. Clin. Cancer Res. 9, 4190-4199.
33. Hernandez D., Miquel-Serra L., Docampo M.J., Marco-Ramell A. and Bassols A. (2012). Role of versican V0/V1 and CD44 in the regulation of human melanoma cell behavior. Int. J. Mol. Med. 27, 269-275.
34. Huang J., Olivenstein R., Taha R., Hamid Q. and Ludwig M. (1999). Enhanced proteoglycan deposition in the airway wall of atopic asthmatics. Am. J. Respir. Crit. Care. Med. 160, 725-729.
35. Igney F.H. and Krammer P.H. (2002). Death and anti-death: tumour resistance to apoptosis. Nat. Rev. Cancer 2, 277-288.
36. Isogai Z., Aspberg A., Keene D.R., Ono R.N., Reinhardt D.P. and Sakai, L.Y. (2002). Versican interacts with fibrillin-1 and links extracellular microfibrils to other connective tissue networks. J. Biol. Chem. 277, 4565-4572.
37. Ito K., Shinomura T., Zako M., Ujita M. and Kimata K. (1995). Multiple forms of mouse PG-M, a large chondroitin sulfate proteoglycan generated by alternative splicing. J. Biol. Chem. 270, 958-965.
38. Ito Y., Abiko Y., Tanaka Y., Rahemtulla F., and Kaku T. (2002). Immunohistochemical localization of large chondroitin sulfate proteoglycan in odontogenic tumor. Med. Electron Microsc. 35, 173-177.
39. Kawashima H., Hirose M., Hirose J., Nagakubo D., Plaas A.H. and Miyasaka M. (2000). Binding of a large chondroitin sulfate/dermatan sulfate proteoglycan, versican, to L-selectin, P-selectin, and CD44. J. Biol. Chem. 275, 35448-35456.
40. Kenagy R.D., Plaas A.H. and Wight T.N. (2006). Versican degradation and vascular disease. Trends Cardiovasc. Med. 16, 209-215.
41. Kern C.B., Twal W.O., Mjaatvedt C.H., Fairey S.E., Toole B.P., Iruela-Arispe M.L. and Argraves W.S. (2006). Proteolytic cleavage of versican during cardiac cushion morphogenesis. Dev. Dyn. 235, 2238-2247.
42. Kim S., Takahashi H., Lin W.W., Descargues P., Grivennikov S., Kim Y., Luo J.L. and Karin M. (2009). Carcinoma-produced factors activate myeloid cells through TLR2 to stimulate metastasis. Nature 457, 102-106.
43. Kishimoto J., Ehama R., Wu L., Jiang S., Jiang N. and Burgeson R.E. (1999). Selective activation of the versican promoter by epithelialmesenchymal interactions during hair follicle development. Proc. Natl. Acad. Sci. USA 96, 7336-7341.
44. Kodama J., Hasengaowa Kusumoto T., Seki N., Matsuo T., Nakamura K., Hongo A. and Hiramatsu Y. (2007a). Versican expression in human cervical cancer. Eur. J. Cancer 43, 1460-1466.
45. Kodama J., Hasengaowa Kusumoto T., Seki N., Matsuo T., Ojima Y., Nakamura K., Hongo A. and Hiramatsu Y. (2007b). Prognostic significance of stromal versican expression in human endometrial cancer. Ann. Oncol. 18, 269-274.
46. Koyama H., Hibi T., Isogai Z., Yoneda M., Fujimori M., Amano J., Kawakubo M., Kannagi R., Kimata K., Taniguchi S. and Itano N. (2007). Hyperproduction of hyaluronan in neu-induced mammary tumor accelerates angiogenesis through stromal cell recruitment: possible involvement of versican/PG-M. Am. J. Pathol. 170, 1086-1099.
47. Kreutziger K.L., Muskheli V., Johnson P., Braun K., Wight T.N. and Murry C.E. (2012). Developing vasculature and stroma in engineered human myocardium. Tissue Eng. Part A 17, 1219-1228.
48. Kunisada M., Yogianti F., Sakumi K., Ono R., Nakabeppu Y. and Nishigori C,. (2012). Increased expression of versican in the inflammatory response to UVB-and reactive oxygen speciesinduced skin tumorigenesis. Am. J. Pathol. 179, 3056-3065.
49. Kusumoto T., Kodama J., Seki N., Nakamura K., Hongo A. and Hiramatsu Y. (2012). Clinical significance of syndecan-1 and versican expression in human epithelial ovarian cancer. Oncol. Rep. 23, 917-925.
50. Labropoulou V.T., Theocharis A.D., Ravazoula P., Perimenis P., Hjerpe A., Karamanos N.K. and Kalofonos H.P. (2006). Versican but not decorin accumulation is related to metastatic potential and neovascularization in testicular germ cell tumours. Histopathology 49, 582-593.
51. Lancaster J.M., Dressman H.K., Clarke, J.P., Sayer R.A., Martino M.A., Cragun J.M., Henriott A.H., Gray J., Sutphen R., Elahi A., Whitaker R.S., West M., Marks J.R., Nevins J.R. and Berchuck A. (2006). Identification of genes associated with ovarian cancer metastasis using microarray expression analysis. Int. J. Gynecol. Cancer 16, 1733-1745.
52. LaPierre D.P., Lee D.Y., Li S.Z., Xie Y.Z., Zhong L., Sheng W., Deng Z. and Yang B.B. (2007). The ability of versican to simultaneously cause apoptotic resistance and sensitivity. Cancer Res. 67, 4742-4750.
53. Lebaron R.G. (1996). Versican. Perspect. Dev. Neurobiol. 3, 261-271.
54. Lee G.M., Johnstone B., Jacobson K. and Caterson B. (1993). The dynamic structure of the pericellular matrix on living cells. J. Cell Biol. 123, 1899-1907.
55. Lee C.M., Tanaka T., Murai T., Kondo M., Kimura J., Su W., Kitagawa T., Ito T., Matsuda H. and Miyasaka M. (2002). Novel chondroitin sulfate-binding cationic liposomes loaded with cisplatin efficiently suppress the local growth and liver metastasis of tumor cells in vivo. Cancer Res. 62, 4282-4288.
56. Lee D.Y., Shatseva T., Jeyapalan Z., Du W.W., Deng Z. and Yang B.B. (2009). A 3'-untranslated region (3'UTR) induces organ adhesion by regulating miR-199a* functions. PLoS One 4, e4527.
57. Lee D.Y., Jeyapalan Z., Fang L., Zhang Y., Yee A.Y., Li M., Du W.W., Shatseva T. and Yang B.B. (2010). Expression of versican 3'-untranslated region modulates endogenous microRNA functions. Plos One 5, e13599.
58. Lemire J.M., Chan C.K., Bressler S., Miller J., LeBaron R.G. and Wight T.N. (2007). Interleukin-1beta selectively decreases the synthesis of versican by arterial smooth muscle cells. J. Cell Biochem. 101, 753-766.
59. Luo J., Kato M., Wang H., Bernfield M. and Bischoff J. (2001). Heparan sulfate and chondroitin sulfate proteoglycans inhibit E-selectin binding to endothelial cells. J. Cell Biochem. 80, 522-531.
60. Makatsori E., Lamari F.N., Theocharis A.D., Anagnostides S., Hjerpe A., Tsegenidis T. and Karamanos N.K. (2003). Large matrix proteoglycans, versican and perlecan, are expressed and secreted by human leukemic monocytes. Anticancer Res. 23, 3303-3309.
61. Mantovani A. (2009). Cancer: Inflaming metastasis. Nature 457, 36-37.
62. Matsumoto K., Shionyu M., Go M., Shimizu K., Shinomura T., Kimata K. and Watanabe H. (2003). Distinct interaction of versican/PG-M with hyaluronan and link protein. J. Biol. Chem. 278, 41205-41212.
63. Mauri P., Scarpa A., Nascimbeni A.C., Benazzi L., Parmagnani E., Mafficini A., Della Peruta M., Bassi C., Miyazaki K. and Sorio C. (2005). Identification of proteins released by pancreatic cancer cells by multidimensional protein identification technology: a strategy for identification of novel cancer markers. FASEB J. 19, 1125-1127.
64. Migliore C., Petrelli A., Ghiso E., Corso S., Capparuccia L., Eramo A., Comoglio P.M. and Giordano S. (2008). MicroRNAs impair METmediated invasive growth. Cancer Res. 68, 10128-10136.
65. Monzavi-Karbassi B., Stanley J.S., Hennings L., Jousheghany F., Artaud C., Shaaf S. and Kieber-Emmons T. (2007). Chondroitin sulfate glycosaminoglycans as major P-selectin ligands on metastatic breast cancer cell lines. Int. J. Cancer 120, 1179-1191.
66. Morton S.U., Scherz P.J., Cordes K.R., Ivey K.N., Stainier D.Y. and Srivastava D. (2008). microRNA-138 modulates cardiac patterning during embryonic development. Proc Natl Acad Sci. USA 105, 17830-17835.
67. Mukaratirwa S., van Ederen A.M., Gruys E. and Nederbragt H. (2004). Versican and hyaluronan expression in canine colonic adenomas and carcinomas: relation to malignancy and depth of tumour invasion. J. Comp. Pathol. 131, 259-270.
68. Nakamura J.L., Haas-Kogan D.A. and Pieper R.O. (2007). Glioma invasiveness responds variably to irradiation in a co-culture model. Int. J. Radiat. Oncol. Biol. Phys. 69, 880-886.
69. Nara Y., Kato Y., Torii Y., Tsuji Y., Nakagaki S., Goto S., Isobe H., Nakashima N. and Takeuchi J. (1997). Immunohistochemical localization of extracellular matrix components in human breast tumours with special reference to PG-M/versican. Histochem. J. 29, 21-30.
70. Naso M.F., Zimmermann D.R. and Iozzo R.V. (1994). Characterization of the complete genomic structure of the human versican gene and functional analysis of its promoter. J. Biol. Chem. 269, 32999-33008.
71. Nikitovic D., Zafiropoulos A., Katonis P., Tsatsakis A., Theocharis A.D., Karamanos N.K. and Tzanakakis G.N. (2006). 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 58, 47-53.
72. Passi A., Negrini D., Albertini R., Miserocchi G. and De Luca G. (1999). The sensitivity of versican from rabbit lung to gelatinase A (MMP-2) and B (MMP-9) and its involvement in the development of hydraulic lung edema. FEBS Lett. 456, 93-96.
73. Paulus W., Baur I., Dours-Zimmermann M.T. and Zimmermann D.R. (1996). Differential expression of versican isoforms in brain tumors. J. Neuropathol. Exp. Neurol. 55, 528-533.
74. Perides G., Asher R.A., Lark M.W., Lane W.S., Robinson R.A. and Bignami A. (1995). Glial hyaluronate-binding protein: a product of metalloproteinase digestion of versican? Biochem. J. 312 (Pt 2), 377-384.
75. Pirinen R., Leinonen T., Bohm J., Johansson R., Ropponen K., Kumpulainen E. and Kosma V.M. (2005). Versican in nonsmall cell lung cancer: relation to hyaluronan, clinicopathologic factors, and prognosis. Hum. Pathol. 36, 44-50.
76. Potter-Perigo S., Baker C., Tsoi C., Braun K.R., Isenhath S., Altman G.M., Altman L.C. and Wight T.N. (2004). Regulation of proteoglycan synthesis by leukotriene d4 and epidermal growth factor in bronchial smooth muscle cells. Am. J. Respir. Cell Mol. Biol. 30, 101-108.
77. Pukkila M.J., Kosunen A.S., Virtaniemi J.A., Kumpulainen E.J., Johansson R.T., Kellokoski J.K., Nuutinen J. and Kosma V.M. (2004). Versican expression in pharyngeal squamous cell carcinoma: an immunohistochemical study. J. Clin. Pathol. 57, 735-739.
78. Pukkila M., Kosunen A., Ropponen K., Virtaniemi J., Kellokoski J., Kumpulainen E., Pirinen R., Nuutinen J., Johansson R. and Kosma V.M. (2007). High stromal versican expression predicts unfavourable outcome in oral squamous cell carcinoma. J. Clin. Pathol. 60, 267-272.
79. Pumphrey C.Y., Theus A.M., Li S., Parrish R.S. and Sanderson R.D. (2002). Neoglycans, carbodiimide-modified glycosaminoglycans: a new class of anticancer agents that inhibit cancer cell proliferation and induce apoptosis. Cancer Res. 62, 3722-3728.
80. Rahmani M., Read J.T., Carthy J.M., McDonald P.C., Wong B.W., Esfandiarei M., Si X., Luo Z., Luo H., Rennie P.S. and McManus B.M. (2005). Regulation of the versican promoter by the betacatenin-T-cell factor complex in vascular smooth muscle cells. J. Biol. Chem. 280, 13019-13028.
81. Read J.T., Rahmani M., Boroomand S., Allahverdian S., McManus B.M. and Rennie P.S. (2007). Androgen receptor regulation of the versican gene through an androgen response element in the proximal promoter. J. Biol. Chem. 282, 31954-31963.
82. Ricciardelli C., Mayne K., Sykes P.J., Raymond W.A., McCaul K., Marshall V.R. and Horsfall D.J. (1998). Elevated levels of versican but not decorin predict disease progression in early-stage prostate cancer. Clin. Cancer Res. 4, 963-971.
83. Ricciardelli C., Brooks J.H., Suwiwat S., Sakko A.J., Mayne K., Raymond W.A., Seshadri R., LeBaron R.G. and Horsfall D.J. (2002). Regulation of stromal versican expression by breast cancer cells and importance to relapse-free survival in patients with nodenegative primary breast cancer. Clin. Cancer Res. 8, 1054-1060.
84. Ricciardelli C., Russell D.L., Ween M.P., Mayne K., Suwiwat S., Byers S., Marshall V.R., Tilley W.D. and Horsfall D.J. (2007). Formation of hyaluronan-and versican-rich pericellular matrix by prostate cancer cells promotes cell motility. J. Biol. Chem. 282, 10814-10825.
85. Ricciardelli C., Sakko A.J., Ween M.P., Russell D.L. and Horsfall D.J. (2009). The biological role and regulation of versican levels in cancer. Cancer Metastasis Rev. 28, 233-245.
86. Rivera C.G., Bader J.S. and Popel A.S. (2012). Angiogenesisassociated crosstalk between collagens, CXC chemokines, and thrombospondin domain-containing proteins. Ann. Biomed. Eng. 39, 2213-2222.
87. Rottiers P., Verfaillie T., Contreras R., Revets H., Desmedt M., Dooms H., Fiers W. and Grooten J. (1998). Differentiation of EL4 lymphoma cells by tumoral environment is associated with inappropriate expression of the large chondroitin sulfate proteoglycan PG-M and the tumor-associated antigen HTgp-175. Int. J. Cancer 78, 503-510.
88. Russell D.L., Doyle K.M., Ochsner S.A., Sandy J.D. and Richards J.S. (2003). Processing and localization of ADAMTS-1 and proteolytic cleavage of versican during cumulus matrix expansion and ovulation. J. Biol. Chem. 278, 42330-42339.
89. Sakko A.J., Ricciardelli C., Mayne K., Suwiwat S., LeBaron R.G., Marshall V.R., Tilley W.D. and Horsfall D.J. (2003). Modulation of prostate cancer cell attachment to matrix by versican. Cancer Res. 63, 4786-4791.
90. Sandy J.D., Westling J., Kenagy R.D., Iruela-Arispe M.L., Verscharen C., Rodriguez-Mazaneque J.C., Zimmermann D.R., Lemire J.M., Fischer J.W., Wight T.N. and Clowes A.W. (2001). Versican V1 proteolysis in human aorta in vivo occurs at the Glu441-Ala442 bond, a site that is cleaved by recombinant ADAMTS-1 and ADAMTS-4. J. Biol. Chem. 276, 13372-13378.
91. Schonherr E., Jarvelainen H.T., Sandell L.J. and Wight T.N. (1991). Effects of platelet-derived growth factor and transforming growth factor-beta 1 on the synthesis of a large versican-like chondroitin sulfate proteoglycan by arterial smooth muscle cells. J. Biol. Chem. 266, 17640-17647.
92. Schonherr E., Kinsella M.G. and Wight T.N. (1997). Genistein selectively inhibits platelet-derived growth factor-stimulated versican biosynthesis in monkey arterial smooth muscle cells. Arch. Biochem. Biophys. 339, 353-361.
93. Serra M., Miquel L., Domenzain C., Docampo M.J., Fabra A., Wight T.N. and Bassols A. (2005). V3 versican isoform expression alters the phenotype of melanoma cells and their tumorigenic potential. Int. J. Cancer. 114, 879-886.
94. Sheng W., Wang G., Wang Y., Liang J., Wen J., Zheng P.S., Wu Y., Lee V., Slingerland J., Dumont D. and Yang B.B. (2005). The roles of versican V1 and V2 isoforms in cell proliferation and apoptosis. Mol. Biol. Cell 16, 1330-1340.
95. Sheng W., Wang G., La Pierre D.P., Wen J., Deng Z., Wong C.K., Lee D.Y. and Yang B.B. (2006). Versican mediates mesenchymalepithelial transition. Mol. Biol. Cell 17, 2009-2020.
96. Sheng W., Dong H.H., Lee D.Y., Lu W.Y., Yang B.B. (2007). Versican modulates gap junction intercellular communication, J. Cell. Physiol. 211, 213-219.
97. Shimizu-Hirota R., Sasamura H., Mifune M., Nakaya H., Kuroda M., Hayashi M. and Saruta T. (2001). Regulation of vascular proteoglycan synthesis by angiotensin II type 1 and type 2 receptors. J. Am. Soc. Nephrol. 12, 2609-2615.
98. Shukla S., Nair R., Rolle M.W., Braun K.R., Chan C.K., Johnson P.Y., Wight T.N. and McDevitt T.C. (2012). Synthesis and organization of hyaluronan and versican by embryonic stem cells undergoing embryoid body differentiation. J. Histochem. Cytochem. 58, 345-358.
99. Simpson M.A., Reiland J., Burger S.R., Furcht L.T., Spicer A.P., Oegema T.R. Jr and McCarthy J.B. (2001). Hyaluronan synthase elevation in metastatic prostate carcinoma cells correlates with hyaluronan surface retention, a prerequisite for rapid adhesion to bone marrow endothelial cells. J. Biol. Chem. 276, 17949-17957.
100. Skandalis S.S., Labropoulou V.T., Ravazoula P., Likaki-Karatza E., Dobra K., Kalofonos H.P., Karamanos N.K. and Theocharis A.D. (2004a). 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 11, 314.
101. Skandalis S.S., Theocharis A.D., Theocharis D.A., Papadas T., Vynios D.H. and Papageorgakopoulou N. (2004b). Matrix proteoglycans are markedly affected in advanced laryngeal squamous cell carcinoma. Biochim. Biophys. Acta 1689, 152-161.
102. Skandalis S.S., Kletsas D., Kyriakopoulou D., Stavropoulos M. and Theocharis D.A. (2006). 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 1760, 1217-1225.
103. Soltermann A., Tischler V., Arbogast S., Braun J., Probst-Hensch N., Weder W., Moch H. and Kristiansen G. (2008). Prognostic significance of epithelial-mesenchymal and mesenchymal-epithelial transition protein expression in non-small cell lung cancer. Clin Cancer Res. 14, 7430-7437.
104. Somerville R.P., Longpre J.M., Jungers K.A., Engle J.M., Ross M., Evanko S., Wight T.N., Leduc R. and Apte S.S. (2003). Characterization of ADAMTS-9 and ADAMTS-20 as a distinct ADAMTS subfamily related to Caenorhabditis elegans GON-1. J. Biol. Chem. 278, 9503-9513.
105. Suwiwat S., Ricciardelli C., Tammi R., Tammi M., Auvinen P., Kosma V.M., LeBaron R.G., Raymond W.A., Tilley W.D. and Horsfall D.J. (2004). 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. 10, 2491-2498.
106. Syrokou A., Tzanakakis G.N., Hjerp A. and Karamanos N.K. (1999). Proteoglycans in human malignant mesothelioma. Stimulation of their synthesis induced by epidermal, insulin and platelet-derived growth factors involves receptors with tyrosine kinase activity. Biochimie 81, 733-744.
107. Takahashi Y., Kuwabara H., Yoneda M., Isogai Z., Tanigawa N. and Shibayama Y. (2012). Versican G1 and G3 domains are upregulated and latent transforming growth factor-beta binding protein-4 is downregulated in breast cancer stroma. Breast Cancer 19, 46-53.
108. Theocharis, A.D. (2008). Versican in health and disease. Connect Tissue Res 49, 230-234.
109. Touab M., Villena J., Barranco C., Arumi-Uria M. and Bassols A. (2002). Versican is differentially expressed in human melanoma and may play a role in tumor development. Am. J. Pathol. 160, 549-557.
110. Tufvesson E. and Westergren-Thorsson G. (2000). Alteration of proteoglycan synthesis in human lung fibroblasts induced by interleukin-1beta and tumor necrosis factor-alpha. J. Cell Biochem. 77, 298-309.
111. Vankemmelbeke M.N., Jones G.C., Fowles C., Ilic M.Z., Handley C.J., Day A.J., Knight C.G., Mort J.S. and Buttle D.J. (2003). Selective inhibition of ADAMTS-1,-4 and-5 by catechin gallate esters. Eur. J. Biochem. 270, 2394-2403.
112. Voutilainen K., Anttila M., Sillanpaa S., Tammi R., Tammi M., Saarikoski S and Kosma, V.M. (2003). Versican in epithelial ovarian cancer: relation to hyaluronan, clinicopathologic factors and prognosis. Int. J. Cancer 107, 359-364.
113. Wang W., Xu G.L., Jia W.D., Ma J.L., Li J.S., Ge Y.S., Ren W.H., Yu J.H. and Liu W.B. (2009). Ligation of TLR2 by versican: a link between inflammation and metastasis. Arch. Med. Res. 40, 321-323.
114. Wang X., Hu G. and Zhou J. (2010). Repression of versican expression by microRNA-143. J. Biol. Chem. 285, 23241-23250.
115. Wasa J., Nishida Y., Shinomura T., Isogai Z., Futamura N., Urakawa H., Arai E., Kozawa E., Tsukushi S. and Ishiguro N. (2012). Versican V1 isoform regulates cell-associated matrix formation and cell behavior differentially from aggrecan in Swarm rat chondrosarcoma cells. Int. J. Cancer 130, 2271-2281.
116. Ween M.P., Hummitzsch K., Rodgers R.J., Oehler M.K. and Ricciardelli C. (2012). Versican induces a pro-metastatic ovarian cancer cell behavior which can be inhibited by small hyaluronan oligosaccharides. Clin. Exp. Metastasis 28, 113-125.
117. Wight T.N. (2002). Versican: a versatile extracellular matrix proteoglycan in cell biology. Curr. Opin. Cell. Biol. 14, 617-623.
118. Wight T.N. and Merrilees M.J. (2004). Proteoglycans in atherosclerosis and restenosis: key roles for versican. Circ. Res. 94, 1158-1167.
119. Willert J., Epping M., Pollack J.R., Brown P.O. and Nusse R. (2002). A transcriptional response to Wnt protein in human embryonic carcinoma cells. BMC Dev. Biol. 2, 8.
120. Wu Y. Chen L. Zheng P.S. and Yang B.B. (2002). beta 1-Integrinmediated glioma cell adhesion and free radical-induced apoptosis are regulated by binding to a C-terminal domain of PG-M/versican. J. Biol. Chem. 277, 12294-12301.
121. Wu Y., Chen L., Cao L., Sheng W. and Yang B.B. (2004). Overexpression of the C-terminal PG-M/versican domain impairs growth of tumor cells by intervening in the interaction between epidermal growth factor receptor and beta1-integrin. J. Cell Sci. 117, 2227-2237.
122. Wu Y., W, J., Lee D.Y., Yee A., Cao L., Zhang Y., Kiani C. and Yang B.B. (2005a). Versican protects cells from oxidative stress-induced apoptosis. Matrix Biol. 24, 3-13.
123. Wu Y.J., La Pierre D.P., Wu J., Yee A.J. and Yang B.B. (2005b). The interaction of versican with its binding partners. Cell. Res. 15, 483-494.
124. Wu Y., Sheng W., Dong H., Lapierre D., Wan Y., Lu W.Y. and Yang B.B. (2009). Versican isoforms modulate expression and function of nicotinic acetylcholine receptors. Intl. J. Physiol. Pathophysiol. Pharmacol. 1, 64-75.
125. Xiang Y.Y., Dong H., Wan Y., Li J., Yee A., Yang B.B. and Lu W.Y. (2006). Versican G3 domain regulates neurite growth and synaptic transmission of hippocampal neurons by activation of epidermal growth factor receptor, J. Biol. Chem. 281, 19358-19368.
126. Yamagata M., Yamada K.M., Yoneda M., Suzuki S. and Kimata K. (1986). Chondroitin sulfate proteoglycan (PG-M-like proteoglycan) is involved in the binding of hyaluronic acid to cellular fibronectin. J. Biol. Chem. 261, 13526-13535.
127. Yang B.L., Zhang Y., Cao L. and Yang B.B. (1999). Cell adhesion and proliferation mediated through the G1 domain of versican. J. Cell. Biochem. 72, 210-220.
128. Yang B.L., Cao L., Kiani C., Lee V., Zhang Y., Adams M.E. and Yang B.B. (2000). Tandem repeats are involved in G1 domain inhibition of versican expression and secretion and the G3 domain enhances glycosaminoglycan modification and secretion via the complementbinding protein motif. J. Biol. Chem. 275, 21255-21261.
129. Yang J. and Weinberg, R.A. (2008). Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Dev. Cell. 14, 818-829.
130. Yee A.J., Akens M., Yang B.L., Finkelstein J., Zheng P.S., Deng Z. and Yang B. (2007). The effect of versican G3 domain on local breast cancer invasiveness and bony metastasis. Breast Cancer Res. 9, R47.
131. Yoon H., Liyanarachchi S., Wright F.A., Davuluri R., Lockman J.C., de la Chapelle A. and Pellegata N.S. (2002). Gene expression profiling of isogenic cells with different TP53 gene dosage reveals numerous genes that are affected by TP53 dosage and identifies CSPG2 as a direct target of p53. Proc. Natl. Acad. Sci. USA 99, 15632-15637.
132. Zeng C., Toole B.P., Kinney S.D., Kuo J.W. and Stamenkovic I. (1998). Inhibition of tumor growth in vivo by hyaluronan oligomers. Int. J. Cancer 77, 396-401.
133. Zhang Y., Cao L., Yang B.L. and Yang B.B. (1998a). The G3 Domain of versican enhances cell proliferation via epidermal growth factor-like motifs. J. Biol. Chem. 273, 21342-21352.
134. Zhang Y., Cao L., Kiani C., Yang B.L. and Yang B.B. (1998b). The G3 domain of versican inhibits mesenchymal chondrogenesis via the epidermal growth factor-like motifs. J. Biol. Chem. 273, 33054-33063.
135. Zhang Y., Cao L., Kiani C., Yang B.L., Hu W. and Yang B.B. (1999). Promotion of chondrocyte proliferation by versican mediated by the G1 domain and EGF-like motifs. J. Cell Biochem. 73, 445-457.
136. Zhang Y., Wu Y., Cao L., Lee V., Chen L., Lin Z., Kiani C., Adams M.E. and Yang B.B. (2001). Versican modulates embryonic chondrocyte morphology via the epidermal growth factor-like motifs in G3. Exp. Cell Res. 263, 33-42.
137. Zheng P.S., Vais D., La Pierre D., Liang Y.Y., Yang B.L. and Yang B.B. (2004a). PG-M/versican binds to P-Selectin glycoprotein ligand-1 and mediates leukocyte aggregation. J. Cell Sci. 117, 5887-5895.
138. Zheng P.S., Wen J., Ang L.C., Sheng W., Viloria-Petit A., Wang Y., Wu Y., Kerbel R.S. and Yang B.B. (2004b). Versican/PG-M G3 domain promotes tumor growth and angiogenesis. FASEB J. 18, 754-756.
139. Zheng P.S., Reis M., Sparling C., Lee D.Y., La Pierre D.P., Wong C.K.A., Deng Z., Kahai S., Wen J. and Yang B.B. (2006). Versican G3 domain promotes blood coagulation through suppressing the activity of tissue factor pathway inhibitor-1. J. Biol. Chem. 281, 8175-8182.