Heparanase enhances myeloma progression via CXCL10 downregulation

Leukemia

Volumn 28, Issue 11, 2014, Pages 2178-2187

  Barash, U ^a   Zohar, Y ^a   Wildbaum, G ^a   Beider, K ^b   Nagler, A ^b   Karin, N ^a   Ilan, N ^a   Vlodavsky, I ^a  

^a TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^b TEL AVIV UNIVERSITY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIINFECTIVE AGENT; BETA GLUCURONIDASE; CXCL10 PROTEIN, HUMAN; CXCL10 PROTEIN, MOUSE; DOXYCYCLINE; GAMMA INTERFERON INDUCIBLE PROTEIN 10; HEPARANASE;

ANIMAL; CELL PROLIFERATION; DISEASE COURSE; DOWN REGULATION; DRUG EFFECTS; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; MOUSE; MULTIPLE MYELOMA; PATHOLOGY; PHYSIOLOGY; TUMOR CELL CULTURE;

ANIMALS; ANTI-BACTERIAL AGENTS; CELL PROLIFERATION; CHEMOKINE CXCL10; DISEASE PROGRESSION; DOWN-REGULATION; DOXYCYCLINE; GENE EXPRESSION; GENE EXPRESSION REGULATION, NEOPLASTIC; GLUCURONIDASE; HUMANS; MICE; MULTIPLE MYELOMA; TUMOR CELLS, CULTURED;

EID: 84922329456     PISSN: 08876924     EISSN: 14765551     Source Type: Journal    
DOI: 10.1038/leu.2014.121     Document Type: Article

References (55)

1. 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. DOI: 10.1007/s10555-011-9288-x
2. Barash U, Cohen-Kaplan V, Dowek I, Sanderson RD, 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. DOI: 10.1111/j.1742-4658.2010.07799.x
3. Ilan N, Elkin M, Vlodavsky I. Regulation, function and clinical significance of heparanase in cancer metastasis and angiogenesis. Intl J Biochem Cell Biol 2006; 38: 2018–2039. DOI: 10.1016/j.biocel.2006.06.004
4. Vlodavsky I, Ilan N, Naggi A, Casu B. Heparanase: structure, biological functions, and inhibition by heparin-derived mimetics of heparan sulfate. Curr Pharm Des 2007; 13: 2057–2073. DOI: 10.2174/138161207781039742
5. Vreys V, David G. Mammalian heparanase: what is the message? J Cell Mol Med 2007; 11: 427–452. DOI: 10.1111/j.1582-4934.2007.00039.x
6. Cohen I, Pappo O, Elkin M, San T, Bar-Shavit R, Hazan R et al. Heparanase promotes growth, angiogenesis and survival of primary breast tumors. Intl J Cancer 2006; 118: 1609–1617. DOI: 10.1002/ijc.21552
7. Fux L, Ilan N, Sanderson RD, Vlodavsky I. Heparanase: busy at the cell surface. Trends Biochem Sci 2009; 34: 511–519. DOI: 10.1016/j.tibs.2009.06.005
8. Lerner I, Baraz L, Pikarsky E, Meirovitz A, Edovitsky E, Peretz T et al. Function of heparanase in prostate tumorigenesis: potential for therapy. Clin Cancer Res 2008; 14: 668–676. DOI: 10.1158/1078-0432.CCR-07-1866
9. Cassinelli G, Lanzi C, Tortoreto M, Cominetti D, Petrangolini G, Favini E et al. Antitumor efficacy of the heparanase inhibitor SST0001 alone and in combination with antiangiogenic agents in the treatment of human pediatric sarcoma models. Biochemical Pharmacol 2013; 85: 1424–1432. DOI: 10.1016/j.bcp.2013.02.023
10. Dredge K, Hammond E, Handley P, Gonda TJ, Smith MT, Vincent C et al. 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. DOI: 10.1038/bjc.2011.11
11. Ritchie JP, Ramani VC, Ren Y, Naggi A, Torri G, Casu B et al. 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. DOI: 10.1158/1078-0432.CCR-10-2476
12. Shafat I, Ben-Arush MW, Issakov J, Meller I, Naroditsky I, Tortoreto M et al. Pre-clinical and clinical significance of heparanase in Ewing’s sarcoma. J Cell Mol Med 2011; 15: 1857–1864. DOI: 10.1111/j.1582-4934.2010.01190.x
13. Elkin M, Ilan N, Ishai-Michaeli R, Friedmann Y, Papo O, Pecker I et al. Heparanase as mediator of angiogenesis: mode of action. FASEB J 2001; 15: 1661–1663. DOI: 10.1096/fj.00-0895fje
14. Folkman J, Klagsbrun M, Sasse J, Wadzinski M, Ingber D, Vlodavsky I. A heparin-binding angiogenic protein—basic fibroblast growth factor—is stored within basement membrane. Am J Pathol 1988; 130: 393–400.
15. Barash U, Cohen-Kaplan V, Arvatz G, Gingis-Velitski S, Levy-Adam F, Nativ O et al. A novel human heparanase splice variant, T5, endowed with protumorigenic characteristics. FASEB J 2010; 24: 1239–1248. DOI: 10.1096/fj.09-147074
16. Fux L, Feibish N, Cohen-Kaplan V, Gingis-Velitski S, Feld S, Geffen C et al. Structure-function approach identifies a COOH-terminal domain that mediates heparanase signaling. Cancer Res 2009; 69: 1758–1767. DOI: 10.1158/0008-5472.CAN-08-1837
17. 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. DOI: 10.1158/0008-5472.CAN-08-2910
18. Cohen-Kaplan V, Jrbashyan J, Yanir Y, Naroditsky I, Ben-Izhak O, Ilan N et al. Heparanase induces signal transducer and activator of transcription (STAT) protein phosphorylation: preclinical and clinical significance in head and neck cancer. J Biol Chem 2012; 287: 6668–6678. DOI: 10.1074/jbc.M111.271346
19. Riaz A, Ilan N, Vlodavsky I, Li JP, Johansson S. Characterization of heparanase-induced phosphatidylinositol 3-kinase-AKT activation and its integrin dependence. J Biol Chem 2013; 288: 12366–12375. DOI: 10.1074/jbc.M112.435172
20. Cohen-Kaplan V, Naroditsky I, Zetser A, Ilan N, Vlodavsky I, Doweck I. Heparanase induces VEGF C and facilitates tumor lymphangiogenesis. Intl J Cancer 2008; 123: 2566–2573. DOI: 10.1002/ijc.23898
21. Nadir Y, Brenner B, Zetser A, Ilan N, Shafat I, Zcharia E et al. Heparanase induces tissue factor expression in vascular endothelial and cancer cells. J Thromb Haemost 2006; 4: 2443–2451. DOI: 10.1111/j.1538-7836.2006.02212.x
22. Yang Y, Ren Y, Ramani VC, Nan L, Suva LJ, Sanderson RD. Heparanase enhances local and systemic osteolysis in multiple myeloma by upregulating the expression and secretion of RANKL. Cancer Res 2010; 70: 8329–8338. DOI: 10.1158/0008-5472.CAN-10-2179
23. Okawa T, Naomoto Y, Nobuhisa T, Takaoka M, Motoki T, Shirakawa Y et al. Heparanase is involved in angiogenesis in esophageal cancer through induction of cyclooxygenase-2. Clin Cancer Res 2005; 11: 7995–8005. DOI: 10.1158/1078-0432.CCR-05-1103
24. Ramani VC, Yang Y, Ren Y, Nan L, Sanderson RD. 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. DOI: 10.1074/jbc.M110.183277
25. Nadav L, Katz BZ, Baron S, Cohen N, Naparstek E, Geiger B. The generation and regulation of functional diversity of malignant plasma cells. Cancer Res 2006; 66: 8608–8616. DOI: 10.1158/0008-5472.CAN-06-1301
26. Purushothaman A, Uyama T, Kobayashi F, Yamada S, Sugahara K, Rapraeger AC et al. Heparanase-enhanced shedding of syndecan-1 by myeloma cells promotes endothelial invasion and angiogenesis. Blood 2010; 115: 2449–2457. DOI: 10.1182/blood-2009-07-234757
27. Gingis-Velitski S, Zetser A, Flugelman MY, Vlodavsky I, Ilan N. Heparanase induces endothelial cell migration via protein kinase B/Akt activation. J Biol Chem 2004; 279: 23536–23541. DOI: 10.1074/jbc.M400554200
28. Beider K, Begin M, Abraham M, Wald H, Weiss ID, Wald O et al. CXCR4 antagonist 4F-benzoyl-TN14003 inhibits leukemia and multiple myeloma tumor growth. Exp Hematol 2011; 39: 282–292. DOI: 10.1016/j.exphem.2010.11.010
29. 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. DOI: 10.1158/0008-5472.CAN-05-1811
30. Meiron M, Zohar Y, Anunu R, Wildbaum G, Karin N. CXCL12 (SDF-1alpha) suppresses ongoing experimental autoimmune encephalomyelitis by selecting antigen-specific regulatory T cells. J Exp Med 2008; 205: 2643–2655. DOI: 10.1084/jem.20080730
31. Vlodavsky I. Preparation of extracellular matrices produced by cultured corneal endothelial and PF-HR9 endodermal cells. In: Bonifacino MD JS, Hartford JB, Lippincott-Schwartz J, Yamada KM, (eds) Protocols in Cell Biology vol. 1. John Wiley & Sons: New York, pp 10.14.11–10.14.14 1999.
32. Barash U, Arvatz G, Farfara R, Naroditsky I, Doweck I, Feld S et al. Clinical significance of heparanase splice variant (t5) in renal cell carcinoma: evaluation by a novel t5-specific monoclonal antibody. PLoS One 2012; 7: e51494. DOI: 10.1371/journal.pone.0051494
33. Sanderson RD, Yang Y, Kelly T, Macleod V, Dai Y, Theus A. Enzymatic remodeling of heparan sulfate proteoglycans within the tumor microenvironment: growth regulation and the prospect of new cancer therapies. J Cell Biochem 2005; 96: 897–905. DOI: 10.1002/jcb.20602
34. Arvatz G, Barash U, Nativ O, Ilan N, Vlodavsky I. Post-transcriptional regulation of heparanase gene expression by a 3′ AU-rich element. FASEB J 2011; 24: 4969–4976. DOI: 10.1096/fj.10-156372
35. Miao HQ, Liu H, Navarro E, Kussie P, Zhu Z. Development of heparanase inhibitors for anti-cancer therapy. Curr Med Chem 2006; 13: 2101–2111. DOI: 10.2174/092986706777935230
36. Purushothaman A, Babitz SK, Sanderson RD. Heparanase enhances the insulin receptor signaling pathway to activate extracellular signal-regulated kinase in multiple myeloma. J Biol Chem 2012; 287: 41288–41296. DOI: 10.1074/jbc.M112.391417
37. Purushothaman A, Chen L, Yang Y, Sanderson RD. 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. DOI: 10.1074/jbc.M806266200
38. Ramani VC, Purushothaman A, Stewart MD, Thompson CA, Vlodavsky I, Au JL et al. The heparanase/syndecan-1 axis in cancer: mechanisms and therapies. FEBS J 2013; 280: 2294–2306. DOI: 10.1111/febs.12168
39. Sanderson RD, Iozzo RV. Targeting heparanase for cancer therapy at the tumor-matrix interface. Matrix Biol 2012; 31: 283–284. DOI: 10.1016/j.matbio.2012.05.001
40. Sanderson RD, Yang Y. Syndecan-1: a dynamic regulator of the myeloma microenvironment. Clin Exp Metastasis 2008; 25: 149–159. DOI: 10.1007/s10585-007-9125-3
41. He YQ, Sutcliffe EL, Bunting KL, Li J, Goodall KJ, Poon IK et al. 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. DOI: 10.4161/trns.19998
42. Li RW, Freeman C, Yu D, Hindmarsh EJ, Tymms KE, Parish CR et al. Dramatic regulation of heparanase activity and angiogenesis gene expression in synovium from patients with rheumatoid arthritis. Arthritis Rheum 2008; 58: 1590–1600. DOI: 10.1002/art.23489
43. Giuliani N, Bonomini S, Romagnani P, Lazzaretti M, Morandi F, Colla S et al. CXCR3 and its binding chemokines in myeloma cells: expression of isoforms and potential relationships with myeloma cell proliferation and survival. Haematologica 2006; 91: 1489–1497.
44. Liu M, Guo S, Stiles JK. The emerging role of CXCL10 in cancer (Review). Oncol Lett 2011; 2: 583–589. DOI: 10.3892/ol.2011.300
45. Rosenkilde MM, Schwartz TW. The chemokine system - a major regulator of angiogenesis in health and disease. APMIS 2004; 112: 481–495. DOI: 10.1111/j.1600-0463.2004.apm11207-0808.x
46. Bodnar RJ, Yates CC, Rodgers ME, Du X, Wells A. IP-10 induces dissociation of newly formed blood vessels. J Cell Sci 2009; 122: 2064–2077. DOI: 10.1242/jcs.048793
47. Luster AD, Greenberg SM, Leder P. The IP-10 chemokine binds to a specific cell surface heparan sulfate site shared with platelet factor 4 and inhibits endothelial cell proliferation. J Exp Med 1995; 182: 219–231. DOI: 10.1084/jem.182.1.219
48. Feldman AL, Friedl J, Lans TE, Libutti SK, Lorang D, Miller MS et al. Retroviral gene transfer of interferon-inducible protein 10 inhibits growth of human melanoma xenografts. Intl J Cancer 2002; 99: 149–153. DOI: 10.1002/ijc.10292
49. Man K, Ng KT, Xu A, Cheng Q, Lo CM, Xiao JW et al. Suppression of liver tumor growth and metastasis by adiponectin in nude mice through inhibition of tumor angiogenesis and downregulation of Rho kinase/IFN-inducible protein 10/matrix metalloproteinase 9 signaling. Clin Cancer Res 2010; 16: 967–977. DOI: 10.1158/1078-0432.CCR-09-1487
50. Sun Y, Finger C, Alvarez-Vallina L, Cichutek K, Buchholz CJ. Chronic gene delivery of interferon-inducible protein 10 through replication-competent retrovirus vectors suppresses tumor growth. Cancer Gene Ther 2005; 12: 900–912. DOI: 10.1038/sj.cgt.7700854
51. Tannenbaum CS, Tubbs R, Armstrong D, Finke JH, Bukowski RM, Hamilton TA. The CXC chemokines IP-10 and Mig are necessary for IL-12-mediated regression of the mouse RENCA tumor. J Immunol 1998; 161: 927–932.
52. Sgadari C, Angiolillo AL, Cherney BW, Pike SE, Farber JM, Koniaris LG et al. Interferon-inducible protein-10 identified as a mediator of tumor necrosis in vivo. Proc Natl Acad Sci USA 1996; 93: 13791–13796. DOI: 10.1073/pnas.93.24.13791
53. Arenberg DA, White ES, Burdick MD, Strom SR, Strieter RM. Improved survival in tumor-bearing SCID mice treated with interferon-gamma-inducible protein 10 (IP-10/CXCL10). Cancer Immunol Immunother 2001; 50: 533–538. DOI: 10.1007/s00262-001-0231-9
54. Lamy L, Ngo VN, Emre NC, Shaffer AL 3rd, Yang Y, Tian E et al. Control of autophagic cell death by caspase-10 in multiple myeloma. Cancer Cell 2013; 23: 435–449. DOI: 10.1016/j.ccr.2013.02.017
55. Veitonmaki N, Hansson M, Zhan F, Sundberg A, Lofstedt T, Ljungars A et al. A human ICAM-1 antibody isolated by a function-first approach has potent macrophage-dependent antimyeloma activity in vivo. Cancer Cell 2013; 23: 502–515. DOI: 10.1016/j.ccr.2013.02.026