Heparanase powers a chronic inflammatory circuit that promotes colitis-associated tumorigenesis in mice

Journal of Clinical Investigation

Volumn 121, Issue 5, 2011, Pages 1709-1721

  Lerner, Immanuel ^a   Hermano, Esther ^a   Zcharia, Eyal ^b   Rodkin, Dina ^a   Bulvik, Raanan ^a   Doviner, Victoria ^a   Rubinstein, Ariel M ^a   Ishai Michaeli, Rivka ^a   Atzmon, Ruth ^a   Sherman, Yoav ^a   Meirovitz, Amichay ^a   Peretz, Tamar ^a   Vlodavsky, Israel ^b   Elkin, Michael ^a  

^a HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

^b TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

CATHEPSIN L; DEXTRAN SULFATE; HEPARANASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; STAT3 PROTEIN; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER INCIDENCE; CHRONIC INFLAMMATION; COLON CANCER; COLON CARCINOGENESIS; COLON MUCOSA; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE SEVERITY; ENZYME ACTIVATION; ENZYME SYNTHESIS; HUMAN; HUMAN CELL; INTESTINE FLORA; MACROPHAGE ACTIVATION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; TRANSGENIC MOUSE; ULCERATIVE COLITIS;

ANIMALS; BIOPSY; CELL LINE, TUMOR; COLITIS; ENZYME ACTIVATION; GENE EXPRESSION REGULATION, NEOPLASTIC; GLUCURONIDASE; HUMANS; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MACROPHAGES; MALE; MICE; MICE, INBRED BALB C; PHENOTYPE; POLYSACCHARIDES; RECOMBINANT PROTEINS;

EID: 79955509614     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI43792     Document Type: Article

References (72)

1. Iozzo RV. Heparan sulfate proteoglycans: intricate molecules with intriguing functions. J Clin Invest. 2001;108(2):165-167. (Pubitemid 32656237)
2. Vlodavsky I, Bar-Shavit R, Ishai-Michaeli R, Bashkin P, Fuks Z. Extracellular sequestration and release of fibroblast growth factor: a regulatory mechanism? Trends Biochem Sci. 1991;16(7):268-271. (Pubitemid 121004450)
3. Vlodavsky I, et al. Heparanase: one molecule with multiple functions in cancer progression. Connect Tissue Res. 2008;49(3):207-210.
4. Elkin M, et al. Heparanase as mediator of angiogenesis: mode of action. FASEB J. 2001;15(9):1661-1663.
5. Kato M, et al. Physiological degradation converts the soluble syndecan-1 ectodomain from an inhibitor to a potent activator of FGF-2. Nat Med. 1998;4(6):691-697. (Pubitemid 28274669)
6. Edovitsky E, Elkin M, Zcharia E, Peretz T, Vlodavsky I. Heparanase gene silencing, tumor invasiveness, angiogenesis, and metastasis. J Natl Cancer Inst. 2004; 96(16):1219-1230. (Pubitemid 39232713)
7. Vlodavsky I, et al. Mammalian heparanase: gene cloning, expression and function in tumor progression and metastasis. Nat Med. 1999;5(7):793-802. (Pubitemid 29318614)
8. Parish CR, Freeman C, Hulett MD. Heparanase: a key enzyme involved in cell invasion. Biochim Biophys Acta. 2001;1471(3):M99-M108. (Pubitemid 32206686)
9. Yang Y, et al. Heparanase enhances syndecan-1 shedding: a novel mechanism for stimulation of tumor growth and metastasis. J Biol Chem. 2007; 282(18):13326-13333. (Pubitemid 47100527)
10. Abboud-Jarrous G, et al. Cathepsin L is responsible for processing and activation of proheparanase through multiple cleavages of a linker segment. J Biol Chem. 2008;283(26):18167-18176.
11. Doviner V, et al. Spatial and temporal heparanase expression in colon mucosa throughout the adenoma-carcinoma sequence. Mod Pathol. 2006; 19(6):878-888. (Pubitemid 43780459)
12. Friedmann Y, et al. Expression of heparanase in normal, dysplastic, and neoplastic human colonic mucosa and stroma: evidence for its role in colonic tumorigenesis. Am J Pathol. 2000;157(4):1167-1175.
13. Naomoto Y, Takaoka M, Okawa T, Nobuhisa T, Gunduz M, Tanaka N. The role of heparanase in gastrointestinal cancer (Review). Oncol Rep. 2005;14(1):3-8.
14. Nobuhisa T, et al. Heparanase expression correlates with malignant potential in human colon cancer. J Cancer Res Clin Oncol. 2005;131(4):229-237. (Pubitemid 40238939)
15. Vlodavsky I, et al. Expression of heparanase by platelets and circulating cells of the immune system: possible involvement in diapedesis and extravasation. Invasion Metastasis. 1992;12(2):112-127.
16. 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(1):8-14. (Pubitemid 44967944)
17. Clevers H. Colon cancer--understanding how NSAIDs work. N Engl J Med. 2006;354(7):761-763. (Pubitemid 43247150)
18. Karin M, Greten FR. NF-kappaB: linking inflammation and immunity to cancer development and progression. Nat Rev Immunol. 2005;5(10):749-759. (Pubitemid 41400849)
19. Okayasu I, Ohkusa T, Kajiura K, Kanno J, Sakamoto S. Promotion of colorectal neoplasia in experimental murine ulcerative colitis. Gut. 1996;39(1):87-92. (Pubitemid 26239112)
20. Greten FR, et al. IKKbeta links inflammation and tumorigenesis in a mouse model of colitis-associated cancer. Cell. 2004;118(3):285-296. (Pubitemid 39061110)
21. Agoff SN, et al. The role of cyclooxygenase 2 in ulcerative colitis-associated neoplasia. Am J Pathol. 2000;157(3):737-745. (Pubitemid 32109366)
22. Yu H, Pardoll D, Jove R. STATs in cancer inflammation and immunity: a leading role for STAT3. Nat Rev Cancer. 2009;9(11):798-809.
23. Sato T, et al. Heparanase expression in human colorectal cancer and its relationship to tumor angiogenesis, hematogenous metastasis, and prognosis. J Surg Oncol. 2004;87(4):174-181. (Pubitemid 39167384)
24. Okayasu I, Hatakeyama S, Yamada M, Ohkusa T, Inagaki Y, Nakaya R. A novel method in the induction of reliable experimental acute and chronic ulcerative colitis in mice. Gastroenterology. 1990;98(3):694-702. (Pubitemid 20069706)
25. Okayasu I, Yamada M, Mikami T, Yoshida T, Kanno J, Ohkusa T. Dysplasia and carcinoma development in a repeated dextran sulfate sodium-induced colitis model. J Gastroenterol Hepatol. 2002;17(10):1078-1083. (Pubitemid 35013962)
26. Zcharia E, et al. Transgenic expression of mammalian heparanase uncovers physiological functions of heparan sulfate in tissue morphogenesis, vascularization, and feeding behavior. FASEB J. 2004;18(2):252-263. (Pubitemid 38186244)
27. Zcharia E, et al. Heparanase accelerates wound angiogenesis and wound healing in mouse and rat models. FASEB J. 2005;19(2):211-221. (Pubitemid 40192578)
28. Kram V, et al. Heparanase is expressed in osteoblastic cells and stimulates bone formation and bone mass. J Cell Physiol. 2006;207(3):784-792. (Pubitemid 43668243)
29. van den Hoven MJ, et al. Increased expression of heparanase in overt diabetic nephropathy. Kidney Int. 2006;70(12):2100-2108.
30. Baker AB, et al. Heparanase alters arterial structure, mechanics, and repair following endovascular stenting in mice. Circ Res. 2009;104(3):380-387.
31. Li JP, et al. In vivo fragmentation of heparan sulfate by heparanase overexpression renders mice resistant to amyloid protein A amyloidosis. Proc Natl Acad Sci U S A. 2005;102(18):6473-6477.
32. Kumar V, Abbas A, Fausto N, eds. Robbins and Cotran Pathologic Basis of Disease. 7th ed. Burlington, Massachusetts, USA: Elsevier Saunders; 2005.
33. Coussens LM, Werb Z. Inflammation and cancer. Nature. 2002;420(6917):860-867. (Pubitemid 36019639)
34. Danese S, et al. Angiogenesis as a novel component of inflammatory bowel disease pathogenesis. Gastroenterology. 2006;130(7):2060-2073. (Pubitemid 43816964)
35. Danese S, et al. Angiogenesis blockade as a new therapeutic approach to experimental colitis. Gut. 2007;56(6):855-862. (Pubitemid 46854204)
36. Pahl HL. Activators and target genes of Rel/NF-kappaB transcription factors. Oncogene. 1999;18(49):6853-6866.
37. Wang D, Dubois RN. The role of COX-2 in intestinal inflammation and colorectal cancer. Oncogene. 2010;29(6):781-788.
38. Danese S, Mantovani A. Inflammatory bowel disease and intestinal cancer: a paradigm of the Yin-Yang interplay between inflammation and cancer. Oncogene. 2010;29(23):3313-3323.
39. Becker C, et al. IL-6 signaling promotes tumor growth in colorectal cancer. Cell Cycle. 2005;4(2):217-220. (Pubitemid 41365319)
40. Banks C, Bateman A, Payne R, Johnson P, Sheron N. Chemokine expression in IBD. Mucosal chemokine expression is unselectively increased in both ulcerative colitis and Crohn's disease. J Pathol. 2003; 199(1):28-35. (Pubitemid 36054726)
41. Vainer B, Nielsen OH, Horn T. Expression of E-selectin, sialyl Lewis X, and macrophage inflammatory protein-1alpha by colonic epithelial cells in ulcerative colitis. Dig Dis Sci. 1998;43(3):596-608. (Pubitemid 28155583)
42. Bollrath J, et al. gp130-mediated Stat3 activation in enterocytes regulates cell survival and cell-cycle progression during colitis-associated tumorigenesis. Cancer Cell. 2009;15(2):91-102.
43. Grivennikov S, et al. IL-6 and Stat3 are required for survival of intestinal epithelial cells and development of colitis-associated cancer. Cancer Cell. 2009; 15(2):103-113.
44. Bollrath J, Greten FR. IKK/NF-kappaB and STAT3 pathways: central signalling hubs in inflammation-mediated tumour promotion and metastasis. EMBO Rep. 2009;10(12):1314-1319.
45. Jarnicki A, Putoczki T, Ernst M. Stat3: linking inflammation to epithelial cancer - more than a αgutα feeling? Cell Div. 2010;5:14.
46. Mahida YR. The key role of macrophages in the immunopathogenesis of inflammatory bowel disease. Inflamm Bowel Dis. 2000;6(1):21-33.
47. Elson CO, Sartor RB, Tennyson GS, Riddell RH. Experimental models of inflammatory bowel disease. Gastroenterology. 1995;109(4):1344-1367.
48. Krieglstein CF, et al. Collagen-binding integrin alpha- 1beta1 regulates intestinal inflammation in experimental colitis. J Clin Invest. 2002;110(12):1773-1782. (Pubitemid 36076484)
49. Pollard JW. Tumour-educated macrophages promote tumour progression and metastasis. Nat Rev Cancer. 2004;4(1):71-78. (Pubitemid 38082155)
50. Starkey PM, Turley L, Gordon S. The mouse macrophage- specific glycoprotein defined by monoclonal antibody F4/80: characterization, biosynthesis and demonstration of a rat analogue. Immunology. 1987;60(1):117-122. (Pubitemid 17230149)
51. Poltorak A, et al. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science. 1998;282(5396):2085-2088. (Pubitemid 29001265)
52. Fukata M, et al. Toll-like receptor-4 promotes the development of colitis-associated colorectal tumors. Gastroenterology. 2007;133(6):1869-1881.
53. Fukata M, et al. Innate immune signaling by Toll-like receptor-4 (TLR4) shapes the inflammatory microenvironment in colitis-associated tumors. Inflamm Bowel Dis. 2009;15(7):997-1006.
54. Sanchez-Munoz F, Dominguez-Lopez A, Yamamoto- Furusho JK. Role of cytokines in inflammatory bowel disease. World J Gastroenterol. 2008;14(27):4280-4288.
55. Brunn GJ, Bungum MK, Johnson GB, Platt JL. Conditional signaling by Toll-like receptor 4. FASEB J. 2005;19(7):872-874. (Pubitemid 40617413)
56. Miao HQ, Ornitz DM, Aingorn E, Ben-Sasson SA, Vlodavsky I. Modulation of fibroblast growth factor- 2 receptor binding, dimerization, signaling, and angiogenic activity by a synthetic heparin-mimicking polyanionic compound. J Clin Invest. 1997; 99(7):1565-1575. (Pubitemid 27163807)
57. Arbibe L, et al. Toll-like receptor 2-mediated NF-kappa B activation requires a Rac1-dependent pathway. Nat Immunol. 2000;1(6):533-540.
58. Guha M, Mackman N. The phosphatidylinositol 3-kinase-Akt pathway limits lipopolysaccharide activation of signaling pathways and expression of inflammatory mediators in human monocytic cells. J Biol Chem. 2002;277(35):32124-32132. (Pubitemid 34969025)
59. Liu H, Perlman H, Pagliari LJ, Pope RM. Constitutively activated Akt-1 is vital for the survival of human monocyte-differentiated macrophages. Role of Mcl-1, independent of nuclear factor (NF)-kappaB, Bad, or caspase activation. J Exp Med. 2001;194(2):113-126.
60. Chen G, et al. Inflammatory cytokines and fatty acids regulate endothelial cell heparanase expression. Biochemistry. 2004;43(17):4971-4977. (Pubitemid 38544450)
61. Popivanova BK, et al. Blocking TNF-alpha in mice reduces colorectal carcinogenesis associated with chronic colitis. J Clin Invest. 2008;118(2):560-570. (Pubitemid 351206546)
62. Menzel K, et al. Cathepsins B, L and D in inflammatory bowel disease macrophages and potential therapeutic effects of cathepsin inhibition in vivo. Clin Exp Immunol. 2006;146(1):169-180. (Pubitemid 44393851)
63. Fiebiger E, et al. Invariant chain controls the activity of extracellular cathepsin L. J Exp Med. 2002;196(9):1263-1269. (Pubitemid 35304191)
64. Gupta RB, et al. Histologic inflammation is a risk factor for progression to colorectal neoplasia in ulcerative colitis: a cohort study. Gastroenterology. 2007;133(4):1099-1105. (Pubitemid 47494461)
65. Rutter M, et al. Severity of inflammation is a risk factor for colorectal neoplasia in ulcerative colitis. Gastroenterology. 2004;126(2):451-459. (Pubitemid 38182302)
66. Subbaramaiah K, et al. Microsomal prostaglandin E synthase-1 is overexpressed in inflammatory bowel disease. Evidence for involvement of the transcription factor Egr-1. J Biol Chem. 2004;279(13):12647-12658. (Pubitemid 38445836)
67. de Mestre AM, Rao S, Hornby JR, Soe-Htwe T, Khachigian LM, Hulett MD. Early growth response gene 1 (EGR1) regulates heparanase gene transcription in tumor cells. J Biol Chem. 2005;280(42):35136-35147. (Pubitemid 41532700)
68. Bouma G, Strober W. The immunological and genetic basis of inflammatory bowel disease. Nat Rev Immunol. 2003;3(7):521-533. (Pubitemid 37328672)
69. Munitz A, Seidu L, Cole ET, Ahrens R, Hogan SP, Rothenberg ME. Resistin-like molecule alpha decreases glucose tolerance during intestinal inflammation. J Immunol. 2009;182(4):2357-2363.
70. Edelblum KL, Goettel JA, Koyama T, McElroy SJ, Yan F, Polk DB. TNFR1 promotes tumor necrosis factor-mediated mouse colon epithelial cell survival through RAF activation of NF-kappaB. J Biol Chem. 2008;283(43):29485-29494.
71. Kelly T, et al. High heparanase activity in multiple myeloma is associated with elevated microvessel density. Cancer Res. 2003;63(24):8749-8756. (Pubitemid 38064053)
72. 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(6):2704-2711. (Pubitemid 13100536)