Versatile role of heparanase in inflammation

Matrix Biology

Volumn 32, Issue 5, 2013, Pages 234-240

  Goldberg, Rachel ^a   Meirovitz, Amichay ^a   Hirshoren, Nir ^a   Bulvik, Raanan ^a   Binder, Adi ^a   Rubinstein, Ariel M ^a   Elkin, Michael ^a  

^a HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

Author keywords

Cancer; Extracellular matrix; Heparan sulfate; Heparanase; Inflammation; Macrophages; Tumor microenvironment

Indexed keywords

CYCLOOXYGENASE 2; GLYCOSAMINOGLYCAN; HEPARAN SULFATE; HEPARANASE; I KAPPA B; INTERLEUKIN 1; INTERLEUKIN 12; INTERLEUKIN 6; PROTEIN P53; STAT3 PROTEIN; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA;

BARRETT ESOPHAGUS; CANCER SURVIVAL; CARCINOGENESIS; CHRONIC INFLAMMATION; COLITIS; COLORECTAL CANCER; CROHN DISEASE; CYTOKINE RELEASE; ENDOTHELIUM; ENTERITIS; ENZYME ACTIVITY; ENZYME DEGRADATION; ENZYME SUBSTRATE; ESOPHAGEAL ADENOCARCINOMA; EXTRACELLULAR MATRIX; GLYCOCALYX; HEPATITIS C; HUMAN; IMMUNE RESPONSE; INFLAMMATION; LIVER CELL CARCINOMA; LUNG INJURY; MACROPHAGE; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PANCREAS ADENOCARCINOMA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROCESSING; REVIEW; SEPSIS; SIGNAL TRANSDUCTION; STOMACH CARCINOMA; TUMOR GROWTH; ULCERATIVE COLITIS;

CARCINOGENESIS; EXTRACELLULAR MATRIX; GENE EXPRESSION REGULATION; GLUCURONIDASE; HEPARITIN SULFATE; HUMANS; INFLAMMATORY BOWEL DISEASES; MACROPHAGES; NEOPLASMS; PNEUMONIA; SIGNAL TRANSDUCTION;

MAMMALIA;

EID: 84879602314     PISSN: 0945053X     EISSN: 15691802     Source Type: Journal    
DOI: 10.1016/j.matbio.2013.02.008     Document Type: Review

References (128)

1. Abboud-Jarrous G., Rangini-Guetta Z., Aingorn H., Atzmon R., Elgavish S., Peretz T., Vlodavsky I. Site-directed mutagenesis, proteolytic cleavage, and activation of human proheparanase. J. Biol. Chem. 2005, 280:13568-13575.
2. Abboud-Jarrous G., Atzmon R., Peretz T., Palermo C., Gadea B.B., Joyce J.A., Vlodavsky I. Cathepsin L is responsible for processing and activation of proheparanase through multiple cleavages of a linker segment. J. Biol. Chem. 2008, 283:18167-18176.
3. Akbarshahi H., Axelsson J.B., Said K., Malmstrom A., Fischer H., Andersson R. TLR4 dependent heparan sulphate-induced pancreatic inflammatory response is IRF3-mediated. J. Transl. Med. 2011, 9:219.
4. Allen B.L., Filla M.S., Rapraeger A.C. Role of heparan sulfate as a tissue-specific regulator of FGF-4 and FGF receptor recognition. J. Cell Biol. 2001, 155:845-858.
5. Ateeq B., Unterberger A., Szyf M., Rabbani S.A. Pharmacological inhibition of DNA methylation induces proinvasive and prometastatic genes in vitro and in vivo. Neoplasia 2008, 10:266-278.
6. Axelsson J., Xu D., Kang B.N., Nussbacher J.K., Handel T.M., Ley K., Sriramarao P., Esko J.D. Inactivation of heparan sulfate 2-O-sulfotransferase accentuates neutrophil infiltration during acute inflammation in mice. Blood 2012, 120:1742-1751.
7. Baker A.B., Groothuis A., Jonas M., Ettenson D.S., Shazly T., Zcharia E., Vlodavsky I., Seifert P., Edelman E.R. Heparanase alters arterial structure, mechanics, and repair following endovascular stenting in mice. Circ. Res. 2009, 104:380-387.
8. Baraz L., Haupt Y., Elkin M., Peretz T., Vlodavsky I. Tumor suppressor p53 regulates heparanase gene expression. Oncogene 2006, 25:3939-3947.
9. Belmiro C.L., Souza H.S., Elia C.C., Castelo-Branco M.T., Silva F.R., Machado R.L., Pavao M.S. Biochemical and immunohistochemical analysis of glycosaminoglycans in inflamed and non-inflamed intestinal mucosa of patients with Crohn's disease. Int. J. Colorectal Dis. 2005, 20:295-304.
10. Belting M. Heparan sulfate proteoglycan as a plasma membrane carrier. Trends Biochem. Sci. 2003, 28:145-151.
11. Benhamron S., Nechushtan H., Verbovetski I., Krispin A., Abboud-Jarrous G., Zcharia E., Edovitsky E., Nahari E., Peretz T., Vlodavsky I., Mevorach D. Translocation of active heparanase to cell surface regulates degradation of extracellular matrix heparan sulfate upon transmigration of mature monocyte-derived dendritic cells. J. Immunol. 2006, 176:6417-6424.
12. Benhamron S., Reiner I., Zcharia E., Atallah M., Grau A., Vlodavsky I., Mevorach D. Dissociation between mature phenotype and impaired transmigration in dendritic cells from heparanase-deficient mice. PLoS One 2012, 7:e35602.
13. Bernfield M., Gotte M., Park P.W., Reizes O., Fitzgerald M.L., Lincecum J., Zako M. Functions of cell surface heparan sulfate proteoglycans. Annu. Rev. Biochem. 1999, 68:729-777.
14. Bishop J.R., Schuksz M., Esko J.D. Heparan sulphate proteoglycans fine-tune mammalian physiology. Nature 2007, 446:1030-1037.
15. Blich M., Golan A., Arvatz G., Sebbag A., Shafat I., Sabo E., Cohen-Kaplan V., Petcherski S., Avniel-Polak S., Eitan A., Hammerman H., Aronson D., Axelman E., Ilan N., Nussbaum G., Vlodavsky I. Macrophage activation by heparanase is mediated by TLR-2 and TLR-4 and associates with plaque progression. Arterioscler. Thromb. Vasc. Biol. 2012, 33:56-65.
16. Bode L., Salvestrini C., Park P.W., Li J.P., Esko J.D., Yamaguchi Y., Murch S., Freeze H.H. Heparan sulfate and syndecan-1 are essential in maintaining murine and human intestinal epithelial barrier function. J. Clin. Invest. 2008, 118:229-238.
17. Brun R., Naroditsky I., Waterman M., Ben-Izhak O., Groisman G., Ilan N., Vlodavsky I. Heparanase expression by Barrett's epithelium and during esophageal carcinoma progression. Mod. Pathol. 2009, 22:1548-1554.
18. Brunn G.J., Bungum M.K., Johnson G.B., Platt J.L. Conditional signaling by Toll-like receptor 4. FASEB J. 2005, 19:872-874.
19. Chen G., Wang D., Vikramadithyan R., Yagyu H., Saxena U., Pillarisetti S., Goldberg I.J. Inflammatory cytokines and fatty acids regulate endothelial cell heparanase expression. Biochemistry 2004, 43:4971-4977.
20. Chiba T., Marusawa H., Ushijima T. Inflammation-associated cancer development in digestive organs: mechanisms and roles for genetic and epigenetic modulation. Gastroenterology 2012, 143:550-563.
21. Clayburgh D.R., Shen L., Turner J.R. A porous defense: the leaky epithelial barrier in intestinal disease. Lab. Invest. 2004, 84:282-291.
22. 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.
23. Cohen I., Maly B., Simon I., Meirovitz A., Pikarsky E., Zcharia E., Peretz T., Vlodavsky I., Elkin M. Tamoxifen induces heparanase expression in estrogen receptor-positive breast cancer. Clin. Cancer Res. 2007, 13:4069-4077.
24. Cohen-Kaplan V., Doweck I., Naroditsky I., Vlodavsky I., Ilan N. Heparanase augments epidermal growth factor receptor phosphorylation: correlation with head and neck tumor progression. Cancer Res. 2008, 68:10077-10085.
25. Constantinescu A.A., Vink H., Spaan J.A. Endothelial cell glycocalyx modulates immobilization of leukocytes at the endothelial surface. Arterioscler. Thromb. Vasc. Biol. 2003, 23:1541-1547.
26. Day R., Forbes A. Heparin, cell adhesion, and pathogenesis of inflammatory bowel disease. Lancet 1999, 354:62-65.
27. Day R., Ilyas M., Daszak P., Talbot I., Forbes A. Expression of syndecan-1 in inflammatory bowel disease and a possible mechanism of heparin therapy. Dig. Dis. Sci. 1999, 44:2508-2515.
28. de Mestre A.M., Khachigian L.M., Santiago F.S., Staykova M.A., Hulett M.D. Regulation of inducible heparanase gene transcription in activated T cells by early growth response 1. J. Biol. Chem. 2003, 278:50377-50385.
29. de Mestre A.M., Rao S., Hornby J.R., Soe-Htwe T., Khachigian L.M., Hulett M.D. Early growth response gene 1 (EGR1) regulates heparanase gene transcription in tumor cells. J. Biol. Chem. 2005, 280:35136-35147.
30. Doviner V., Maly B., Kaplan V., Gingis-Velitski S., Ilan N., Vlodavsky I., Sherman Y. Spatial and temporal heparanase expression in colon mucosa throughout the adenoma-carcinoma sequence. Mod. Pathol. 2006, 19:878-888.
31. 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.
32. 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.
33. Edovitsky E., Lerner I., Zcharia E., Peretz T., Vlodavsky I., Elkin M. Role of endothelial heparanase in delayed-type hypersensitivity. Blood 2006, 107:3609-3616.
34. El-Assal O.N., Yamanoi A., Ono T., Kohno H., Nagasue N. The clinicopathological significance of heparanase and basic fibroblast growth factor expressions in hepatocellular carcinoma. Clin. Cancer Res. 2001, 7:1299-1305.
35. Elkin M., Ilan N., Ishai-Michaeli R., Friedmann Y., Papo O., Pecker I., Vlodavsky I. Heparanase as mediator of angiogenesis: mode of action. FASEB J. 2001, 15:1661-1663.
36. Elkin M., Cohen I., Zcharia E., Orgel A., Guatta-Rangini Z., Peretz T., Vlodavsky I., Kleinman H.K. Regulation of heparanase gene expression by estrogen in breast cancer. Cancer Res. 2003, 63:8821-8826.
37. Escobar Galvis M.L., Jia J., Zhang X., Jastrebova N., Spillmann D., Gottfridsson E., van Kuppevelt T.H., Zcharia E., Vlodavsky I., Lindahl U., Li J.P. Transgenic or tumor-induced expression of heparanase upregulates sulfation of heparan sulfate. Nat. Chem. Biol. 2007, 3:773-778.
38. Ferro V., Hammond E., Fairweather J.K. The development of inhibitors of heparanase, a key enzyme involved in tumour metastasis, angiogenesis and inflammation. Mini-Rev. Med. Chem. 2004, 4:693-702.
39. Floer M., Gotte M., Wild M.K., Heidemann J., Gassar E.S., Domschke W., Kiesel L., Luegering A., Kucharzik T. Enoxaparin improves the course of dextran sodium sulfate-induced colitis in syndecan-1-deficient mice. Am. J. Pathol. 2010, 176:146-157.
40. Fridman R., Lider O., Naparstek Y., Fuks Z., Vlodavsky I., Cohen I.R. Soluble antigen induces T lymphocytes to secrete an endoglycosidase that degrades the heparan sulfate moiety of subendothelial extracellular matrix. J. Cell. Physiol. 1987, 130:85-92.
41. 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.
42. Goldshmidt O., Zcharia E., Cohen M., Aingorn H., Cohen I., Nadav L., Katz B.Z., Geiger B., Vlodavsky I. Heparanase mediates cell adhesion independent of its enzymatic activity. FASEB J. 2003, 17:1015-1025.
43. Gotte M. Syndecans in inflammation. FASEB J. 2003, 17:575-591.
44. Grivennikov S.I., Karin M. Inflammation and oncogenesis: a vicious connection. Curr. Opin. Genet. Dev. 2010, 20:65-71.
45. Guo C.H., Koo C.Y., Bay B.H., Tan P.H., Yip G.W. Comparison of the effects of differentially sulphated bovine kidney- and porcine intestine-derived heparan sulphate on breast carcinoma cellular behaviour. Int. J. Oncol. 2007, 31:1415-1423.
46. Gupta R.B., Harpaz N., Itzkowitz S., Hossain S., Matula S., Kornbluth A., Bodian C., Ullman T. Histologic inflammation is a risk factor for progression to colorectal neoplasia in ulcerative colitis: a cohort study. Gastroenterology 2007, 133:1099-1105. (quiz 1340-1091).
47. Hanahan D., Weinberg R.A. Hallmarks of cancer: the next generation. Cell 2011, 144:646-674.
48. He Y.Q., Sutcliffe E.L., Bunting K.L., Li J., Goodall K.J., Poon I.K., Hulett M.D., Freeman C., Zafar A., McInnes R.L., Taya T., Parish C.R., Rao S. The endoglycosidase heparanase enters the nucleus of T lymphocytes and modulates H3 methylation at actively transcribed genes via the interplay with key chromatin modifying enzymes. Transcription 2012, 3:130-145.
49. Hershkoviz R., Mor F., Miao H.Q., Vlodavsky I., Lider O. Differential effects of polysulfated polysaccharide on experimental encephalomyelitis, proliferation of autoimmune T cells, and inhibition of heparanase activity. J. Autoimmun. 1995, 8:741-750.
50. Hoffmann A.C., Mori R., Vallbohmer D., Brabender J., Drebber U., Baldus S.E., Klein E., Azuma M., Metzger R., Hoffmann C., Hoelscher A.H., Danenberg K.D., Prenzel K.L., Danenberg P.V. High expression of heparanase is significantly associated with dedifferentiation and lymph node metastasis in patients with pancreatic ductal adenocarcinomas and correlated to PDGFA and via HIF1a to HB-EGF and bFGF. J. Gastrointest. Surg. 2008, 12:1674-1681. (discussion 1681-1672).
51. Ilan N., Elkin M., Vlodavsky I. Regulation, function and clinical significance of heparanase in cancer metastasis and angiogenesis. Int. J. Biochem. Cell Biol. 2006, 38:2018-2039.
52. Iozzo R.V., Sanderson R.D. Proteoglycans in cancer biology, tumour microenvironment and angiogenesis. J. Cell. Mol. Med. 2011, 15:1013-1031.
53. Irony-Tur-Sinai M., Vlodavsky I., Ben-Sasson S.A., Pinto F., Sicsic C., Brenner T. A synthetic heparin-mimicking polyanionic compound inhibits central nervous system inflammation. J. Neurol. Sci. 2003, 206:49-57.
54. Jiang G., Zheng L., Pu J., Mei H., Zhao J., Huang K., Zeng F., Tong Q. Small RNAs targeting transcription start site induce heparanase silencing through interference with transcription initiation in human cancer cells. PLoS One 2012, 7:e31379.
55. Johnson G.B., Brunn G.J., Kodaira Y., Platt J.L. Receptor-mediated monitoring of tissue well-being via detection of soluble heparan sulfate by Toll-like receptor 4. J. Immunol. 2002, 168:5233-5239.
56. Joyce J.A., Freeman C., Meyer-Morse N., Parish C.R., Hanahan D. A functional heparan sulfate mimetic implicates both heparanase and heparan sulfate in tumor angiogenesis and invasion in a mouse model of multistage cancer. Oncogene 2005, 24:4037-4051.
57. Kato M., Wang H., Kainulainen V., Fitzgerald M.L., Ledbetter S., Ornitz D.M., Bernfield M. Physiological degradation converts the soluble syndecan-1 ectodomain from an inhibitor to a potent activator of FGF-2. Nat. Med. 1998, 4:691-697.
58. Koliopanos A., Friess H., Kleeff J., Shi X., Liao Q., Pecker I., Vlodavsky I., Zimmermann A., Buchler M.W. Heparanase expression in primary and metastatic pancreatic cancer. Cancer Res. 2001, 61:4655-4659.
59. Kramer K.L., Yost H.J. Heparan sulfate core proteins in cell-cell signaling. Annu. Rev. Genet. 2003, 37:461-484.
60. Ledin J., Staatz W., Li J.P., Gotte M., Selleck S., Kjellen L., Spillmann D. Heparan sulfate structure in mice with genetically modified heparan sulfate production. J. Biol. Chem. 2004, 279:42732-42741.
61. Lerner I., Baraz L., Pikarsky E., Meirovitz A., Edovitsky E., Peretz T., Vlodavsky I., Elkin M. Function of heparanase in prostate tumorigenesis: potential for therapy. Clin. Cancer Res. 2008, 14:668-676.
62. Lerner I., Hermano E., Zcharia E., Rodkin D., Bulvik R., Doviner V., Rubinstein A.M., Ishai-Michaeli R., Atzmon R., Sherman Y., Meirovitz A., Peretz T., Vlodavsky I., Elkin M. Heparanase powers a chronic inflammatory circuit that promotes colitis-associated tumorigenesis in mice. J. Clin. Invest. 2011, 121:1709-1721.
63. Levy-Adam F., Miao H.Q., Heinrikson R.L., Vlodavsky I., Ilan N. Heterodimer formation is essential for heparanase enzymatic activity. Biochem. Biophys. Res. Commun. 2003, 308:885-891.
64. Li J.P., Vlodavsky I. Heparin, heparan sulfate and heparanase in inflammatory reactions. Thromb. Haemost. 2009, 102:823-828.
65. Li R.W., Freeman C., Yu D., Hindmarsh E.J., Tymms K.E., Parish C.R., Smith P.N. Dramatic regulation of heparanase activity and angiogenesis gene expression in synovium from patients with rheumatoid arthritis. Arthritis Rheum. 2008, 58:1590-1600.
66. Li L., Wang B., Gao T., Zhang X., Hao J.X., Vlodavsky I., Wiesenfeld-Hallin Z., Xu X.J., Li J.P. Heparanase overexpression reduces carrageenan-induced mechanical and cold hypersensitivity in mice. Neurosci. Lett. 2012, 511:4-7.
67. Lider O., Baharav E., Mekori Y.A., Miller T., Naparstek Y., Vlodavsky I., Cohen I.R. Suppression of experimental autoimmune diseases and prolongation of allograft survival by treatment of animals with low doses of heparins. J. Clin. Invest. 1989, 83:752-756.
68. Lider O., Mekori Y.A., Miller T., Bar-Tana R., Vlodavsky I., Baharav E., Cohen I.R., Naparstek Y. Inhibition of T lymphocyte heparanase by heparin prevents T cell migration and T cell-mediated immunity. Eur. J. Immunol. 1990, 20:493-499.
69. Lowenfels A.B., Maisonneuve P., Cavallini G., Ammann R.W., Lankisch P.G., Andersen J.R., Dimagno E.P., Andren-Sandberg A., Domellof L. Pancreatitis and the risk of pancreatic cancer. International Pancreatitis Study Group. N. Engl. J. Med. 1993, 328:1433-1437.
70. Mahtouk K., Hose D., Raynaud P., Hundemer M., Jourdan M., Jourdan E., Pantesco V., Baudard M., De Vos J., Larroque M., Moehler T., Rossi J.F., Reme T., Goldschmidt H., Klein B. Heparanase influences expression and shedding of syndecan-1, and its expression by the bone marrow environment is a bad prognostic factor in multiple myeloma. Blood 2007, 109:4914-4923.
71. Mantovani A., Allavena P., Sica A., Balkwill F. Cancer-related inflammation. Nature 2008, 454:436-444.
72. Massena S., Christoffersson G., Hjertstrom E., Zcharia E., Vlodavsky I., Ausmees N., Rolny C., Li J.P., Phillipson M. A chemotactic gradient sequestered on endothelial heparan sulfate induces directional intraluminal crawling of neutrophils. Blood 2010, 116:1924-1931.
73. Matzner Y., Bar-Ner M., Yahalom J., Ishai-Michaeli R., Fuks Z., Vlodavsky I. Degradation of heparan sulfate in the subendothelial extracellular matrix by a readily released heparanase from human neutrophils. Possible role in invasion through basement membranes. J. Clin. Invest. 1985, 76:1306-1313.
74. 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.
75. McKenzie E.A. Heparanase: a target for drug discovery in cancer and inflammation. Br. J. Pharmacol. 2007, 151:1-14.
76. McKenzie E., Tyson K., Stamps A., Smith P., Turner P., Barry R., Hircock M., Patel S., Barry E., Stubberfield C., Terrett J., Page M. Cloning and expression profiling of Hpa2, a novel mammalian heparanase family member. Biochem. Biophys. Res. Commun. 2000, 276:1170-1177.
77. McKenzie E., Young K., Hircock M., Bennett J., Bhaman M., Felix R., Turner P., Stamps A., McMillan D., Saville G., Ng S., Mason S., Snell D., Schofield D., Gong H., Townsend R., Gallagher J., Page M., Parekh R., Stubberfield C. Biochemical characterization of the active heterodimer form of human heparanase (Hpa1) protein expressed in insect cells. Biochem. J. 2003, 373:423-435.
78. Murch S.H., MacDonald T.T., Walker-Smith J.A., Levin M., Lionetti P., Klein N.J. Disruption of sulphated glycosaminoglycans in intestinal inflammation. Lancet 1993, 341:711-714.
79. Naggi A., Casu B., Perez M., Torri G., Cassinelli G., Penco S., Pisano C., Giannini G., Ishai-Michaeli R., Vlodavsky I. Modulation of the heparanase-inhibiting activity of heparin through selective desulfation, graded N-acetylation, and glycol splitting. J. Biol. Chem. 2005, 280:12103-12113.
80. Nakajima M., Irimura T., Di Ferrante N., Nicolson G.L. Metastatic melanoma cell heparanase. Characterization of heparan sulfate degradation fragments produced by B16 melanoma endoglucuronidase. J. Biol. Chem. 1984, 259:2283-2290.
81. Naomoto Y., Takaoka M., Okawa T., Nobuhisa T., Gunduz M., Tanaka N. The role of heparanase in gastrointestinal cancer (review). Oncol. Rep. 2005, 14:3-8.
82. Naparstek Y., Cohen I.R., Fuks Z., Vlodavsky I. Activated T lymphocytes produce a matrix-degrading heparan sulphate endoglycosidase. Nature 1984, 310:241-244.
83. Nardella C., Lahm A., Pallaoro M., Brunetti M., Vannini A., Steinkuhler C. Mechanism of activation of human heparanase investigated by protein engineering. Biochemistry 2004, 43:1862-1873.
84. Nobuhisa T., Naomoto Y., Ohkawa T., Takaoka M., Ono R., Murata T., Gunduz M., Shirakawa Y., Yamatsuji T., Haisa M., Matsuoka J., Tsujigiwa H., Nagatsuka H., Nakajima M., Tanaka N. Heparanase expression correlates with malignant potential in human colon cancer. J. Cancer Res. Clin. Oncol. 2005, 131:229-237.
85. Ogishima T., Shiina H., Breault J.E., Tabatabai L., Bassett W.W., Enokida H., Li L.C., Kawakami T., Urakami S., Ribeiro-Filho L.A., Terashima M., Fujime M., Igawa M., Dahiya R. Increased heparanase expression is caused by promoter hypomethylation and up-regulation of transcriptional factor early growth response-1 in human prostate cancer. Clin. Cancer Res. 2005, 11:1028-1036.
86. Ogishima T., Shiina H., Breault J.E., Terashima M., Honda S., Enokida H., Urakami S., Tokizane T., Kawakami T., Ribeiro-Filho L.A., Fujime M., Kane C.J., Carroll P.R., Igawa M., Dahiya R. Promoter CpG hypomethylation and transcription factor EGR1 hyperactivate heparanase expression in bladder cancer. Oncogene 2005, 24:6765-6772.
87. Osterholm C., Folkersen L., Lengquist M., Ponten F., Renne T., Li J., Hedin U. Increased expression of heparanase in symptomatic carotid atherosclerosis. Atherosclerosis 2013, 226:67-73.
88. Pan W., Miao H.Q., Xu Y.J., Navarro E.C., Tonra J.R., Corcoran E., Lahiji A., Kussie P., Kiselyov A.S., Wong W.C., Liu H. 1-[4-(1H-Benzoimidazol-2-yl)-phenyl]-3-[4-(1H-benzoimidazol-2-yl)-phenyl]-urea derivatives as small molecule heparanase inhibitors. Bioorg. Med. Chem. Lett. 2006, 16:409-412.
89. Parish C.R. The role of heparan sulphate in inflammation. Nat. Rev. Immunol. 2006, 6:633-643.
90. Parish C.R., Hindmarsh E.J., Bartlett M.R., Staykova M.A., Cowden W.B., Willenborg D.O. Treatment of central nervous system inflammation with inhibitors of basement membrane degradation. Immunol. Cell Biol. 1998, 76:104-113.
91. Parish C.R., Freeman C., Hulett M.D. Heparanase: a key enzyme involved in cell invasion. Biochim. Biophys. Acta 2001, 1471:M99-M108.
92. Picardo S.L., Maher S.G., O'Sullivan J.N., Reynolds J.V. Barrett's to oesophageal cancer sequence: a model of inflammatory-driven upper gastrointestinal cancer. Dig. Surg. 2012, 29:251-260.
93. Pikas D.S., Li J.P., Vlodavsky I., Lindahl U. Substrate specificity of heparanases from human hepatoma and platelets. J. Biol. Chem. 1998, 273:18770-18777.
94. 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.
95. Purushothaman A., Babitz S.K., Sanderson R.D. Heparanase enhances the insulin receptor signaling pathway to activate ERK in multiple myeloma. J. Biol. Chem. 2012, 287:41288-41296.
96. Qian B.Z., Pollard J.W. Macrophage diversity enhances tumor progression and metastasis. Cell 2010, 141:39-51.
97. 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.
98. Rao G., Ding H.G., Huang W., Le D., Maxhimer J.B., Oosterhof A., van Kuppevelt T., Lum H., Lewis E.J., Reddy V., Prinz R.A., Xu X. Reactive oxygen species mediate high glucose-induced heparanase-1 production and heparan sulphate proteoglycan degradation in human and rat endothelial cells: a potential role in the pathogenesis of atherosclerosis. Diabetologia 2011, 54:1527-1538.
99. 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. 2011, 17:1382-1393.
100. Roy M., Reiland J., Murry B.P., Chouljenko V., Kousoulas K.G., Marchetti D. Antisense-mediated suppression of heparanase gene inhibits melanoma cell invasion. Neoplasia 2005, 7:253-262.
101. Sanderson R.D. Heparan sulfate proteoglycans in invasion and metastasis. Semin. Cell Dev. Biol. 2001, 12:89-98.
102. Sasisekharan R., Shriver Z., Venkataraman G., Narayanasami U. Roles of heparan-sulphate glycosaminoglycans in cancer. Nat. Rev. Cancer 2002, 2:521-528.
103. Schmidt E.P., Yang Y., Janssen W.J., Gandjeva A., Perez M.J., Barthel L., Zemans R.L., Bowman J.C., Koyanagi D.E., Yunt Z.X., Smith L.P., Cheng S.S., Overdier K.H., Thompson K.R., Geraci M.W., Douglas I.S., Pearse D.B., Tuder R.M. The pulmonary endothelial glycocalyx regulates neutrophil adhesion and lung injury during experimental sepsis. Nat. Med. 2012, 18:1217-1223.
104. Shteper P.J., Zcharia E., Ashhab Y., Peretz T., Vlodavsky I., Ben-Yehuda D. Role of promoter methylation in regulation of the mammalian heparanase gene. Oncogene 2003, 22:7737-7749.
105. Simizu S., Ishida K., Osada H. Heparanase as a molecular target of cancer chemotherapy. Cancer Sci. 2004, 95:553-558.
106. Sonoda R., Naomoto Y., Shirakawa Y., Fujiwara Y., Yamatsuji T., Noma K., Tanabe S., Takaoka M., Gunduz M., Tsujigiwa H., Nagatsuka H., Ohara N., Yoshino T., Takubo K., Vieth M., Tanaka N. Preferential up-regulation of heparanase and cyclooxygenase-2 in carcinogenesis of Barrett's oesophagus and intestinal-type gastric carcinoma. Histopathology 2010, 57:90-100.
107. Taylor K.R., Gallo R.L. Glycosaminoglycans and their proteoglycans: host-associated molecular patterns for initiation and modulation of inflammation. FASEB J. 2006, 20:9-22.
108. 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.
109. Timar J., Lapis K., Dudas J., Sebestyen A., Kopper L., Kovalszky I. Proteoglycans and tumor progression: Janus-faced molecules with contradictory functions in cancer. Semin. Cancer Biol. 2002, 12:173-186.
110. Vlodavsky I., Fuks Z., Bar-Ner M., Ariav Y., Schirrmacher V. Lymphoma cell-mediated degradation of sulfated proteoglycans in the subendothelial extracellular matrix: relationship to tumor cell metastasis. Cancer Res. 1983, 43:2704-2711.
111. Vlodavsky I., Eldor A., Haimovitz-Friedman A., Matzner Y., Ishai-Michaeli R., Lider O., Naparstek Y., Cohen I.R., Fuks Z. Expression of heparanase by platelets and circulating cells of the immune system: possible involvement in diapedesis and extravasation. Invasion Metastasis 1992, 12:112-127.
112. Vlodavsky I., Miao H.Q., Medalion B., Danagher P., Ron D. Involvement of heparan sulfate and related molecules in sequestration and growth promoting activity of fibroblast growth factor. Cancer Metastasis Rev. 1996, 15:177-186.
113. Vlodavsky I., Friedmann Y., Elkin M., Aingorn H., Atzmon R., Ishai-Michaeli R., Bitan M., Pappo O., Peretz T., Michal I., Spector L., Pecker I. Mammalian heparanase: gene cloning, expression and function in tumor progression and metastasis. Nat. Med. 1999, 5:793-802.
114. Vreys V., David G. Mammalian heparanase: what is the message?. J. Cell. Mol. Med. 2007, 11:427-452.
115. Wang L., Fuster M., Sriramarao P., Esko J.D. Endothelial heparan sulfate deficiency impairs L-selectin- and chemokine-mediated neutrophil trafficking during inflammatory responses. Nat. Immunol. 2005, 6:902-910.
116. Wang B., Jia J., Zhang X., Zcharia E., Vlodavsky I., Pejler G., Li J.P. Heparanase affects secretory granule homeostasis of murine mast cells through degrading heparin. J. Allergy Clin. Immunol. 2011, 128(1310-1317):e1318.
117. Wang F., Wang Y., Zhang D., Puthanveetil P., Johnson J.D., Rodrigues B. Fatty acid-induced nuclear translocation of heparanase uncouples glucose metabolism in endothelial cells. Arterioscler. Thromb. Vasc. Biol. 2012, 32:406-414.
118. Waterman M., Ben-Izhak O., Eliakim R., Groisman G., Vlodavsky I., Ilan N. Heparanase upregulation by colonic epithelium in inflammatory bowel disease. Mod. Pathol. 2007, 20:8-14.
119. Weinbaum S., Tarbell J.M., Damiano E.R. The structure and function of the endothelial glycocalyx layer. Annu. Rev. Biomed. Eng. 2007, 9:121-167.
120. Xavier R.J., Podolsky D.K. Unravelling the pathogenesis of inflammatory bowel disease. Nature 2007, 448:427-434.
121. Xiong Z., Lu M.H., Fan Y.H., Cao Y.L., Hu C.J., Wu Y.Y., Wang S.M., Luo G., Fang D.C., Li C., Yang S.M. Downregulation of heparanase by RNA interference inhibits invasion and tumorigenesis of hepatocellular cancer cells in vitro and in vivo. Int. J. Oncol. 2012, 40:1601-1609.
122. Xu X., Ding J., Rao G., Shen J., Prinz R.A., Rana N., Dmowski W.P. Estradiol induces heparanase-1 expression and heparan sulphate proteoglycan degradation in human endometrium. Hum. Reprod. 2007, 22:927-937.
123. Yang Y., Macleod V., Bendre M., Huang Y., Theus A.M., Miao H.Q., Kussie P., Yaccoby S., Epstein J., Suva L.J., Kelly T., Sanderson R.D. Heparanase promotes the spontaneous metastasis of myeloma cells to bone. Blood 2005, 105:1303-1309.
124. Young E. The anti-inflammatory effects of heparin and related compounds. Thromb. Res. 2008, 122:743-752.
125. Zetser A., Bashenko Y., Miao H.Q., Vlodavsky I., Ilan N. Heparanase affects adhesive and tumorigenic potential of human glioma cells. Cancer Res. 2003, 63:7733-7741.
126. 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.
127. Zhang Y., Li L., Wang Y., Zhang J., Wei G., Sun Y., Shen F. Downregulating the expression of heparanase inhibits the invasion, angiogenesis and metastasis of human hepatocellular carcinoma. Biochem. Biophys. Res. Commun. 2007, 358:124-129.
128. Zhang X., Wang B., O'Callaghan P., Hjertstrom E., Jia J., Gong F., Zcharia E., Nilsson L.N., Lannfelt L., Vlodavsky I., Lindahl U., Li J.P. Heparanase overexpression impairs inflammatory response and macrophage-mediated clearance of amyloid-beta in murine brain. Acta Neuropathol. 2012, 124:465-478.