Heparanase: Multiple functions in inflammation, diabetes and atherosclerosis

Matrix Biology

Volumn 32, Issue 5, 2013, Pages 220-222

  Vlodavsky, Israel ^a   Iozzo, Renato V ^b   Sanderson, Ralph D ^c  

^a TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

^c University of Alabama at Birmingham   (United States)

Author keywords

Atherosclerosis; Diabetes; Extracellular matrix; Heparan sulfate; Heparanase; Inflammation; Tumor microenvironment

Indexed keywords

AMINO ACID; CATHEPSIN L; GELATINASE B; GLYCOSIDASE; HEPARAN SULFATE; HEPARANASE; MESSENGER RNA; MONOCLONAL ANTIBODY; PROTEIN KINASE B; SCATTER FACTOR; VASCULOTROPIN;

ATHEROSCLEROSIS; BLADDER DYSFUNCTION; BLOOD VESSEL INJURY; CANCER GROWTH; CELL MIGRATION; DIABETES MELLITUS; ENDOTHELIUM CELL; ENZYME ACTIVE SITE; ENZYME SPECIFICITY; ENZYME STRUCTURE; EXTRACELLULAR MATRIX; HUMAN; INFLAMMATION; INNATE IMMUNITY; INSULIN DEPENDENT DIABETES MELLITUS; LYMPHOCYTE DIFFERENTIATION; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; TUMOR MICROENVIRONMENT;

ATHEROSCLEROSIS; CELL ADHESION; CELL MOVEMENT; DIABETES MELLITUS; EXTRACELLULAR MATRIX; GENE EXPRESSION REGULATION; GLUCURONIDASE; HEPARITIN SULFATE; HUMANS; INFLAMMATION; MODELS, MOLECULAR; PROTEIN MULTIMERIZATION; SIGNAL TRANSDUCTION; SUBSTRATE SPECIFICITY;

EID: 84879607285     PISSN: 0945053X     EISSN: 15691802     Source Type: Journal    
DOI: 10.1016/j.matbio.2013.03.001     Document Type: Review

References (36)

1. 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.
2. Baker A.B., Gibson W.J., Kolachalama V.B., Golomb M., Indolfi L., Spruell C., Zcharia E., Vlodavsky I., Edelman E.R. Heparanase regulates thrombosis in vascular injury and stent-induced flow disturbance. J. Am. Coll. Cardiol. 2012, 59:1551-1560.
3. Blich M., Golan A., Arvatz G., Sebbag A., Shafat I., Sabo E., Cohen-Kaplan V., Petcherski 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. 2013, 33:e56-65.
4. Daly S.B., Urquhart J.E., Hilton E., McKenzie E.A., Kammerer R.A., Lewis M., Kerr B., Stuart H., Donnai D., Long D.A., Burgu B., Aydogdu O., Derbent M., Garcia-Minaur S., Reardon W., Gener B., Shalev S., Smith R., Woolf A.S., Black G.C., Newman W.G. Mutations in HPSE2 cause urofacial syndrome. Am. J. Hum. Genet. 2010, 86:963-969.
5. 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.
6. 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.
7. Freeman C., Parish C.R. Human platelet heparanase: purification, characterization and catalytic activity. Biochem. J. 1998, 330:1341-1350.
8. Fux L., Ilan N., Sanderson R.D., Vlodavsky I. Heparanase: busy at the cell surface. Trends Biochem. Sci. 2009, 34:511-519.
9. Gil N., Goldberg R., Neuman T., Garsen M., Zcharia E., Rubinstein A., van Kuppevelt T., Meirovitz A., Pisano C., Li J.-P., van der Vlag J., Vlodavsky I., Elkin M. Heparanase is essential for the development of diabetic nephropathy in mice. Diabetes 2012, 61:208-216.
10. 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.
11. Hermano E., Lerner I., Elkin M. Heparanase enzyme in chronic inflammatory bowel disease and colon cancer. Cell. Mol. Life Sci. 2012, 69:2501-2513.
12. Hulett M.D., Freeman C., Hamdorf B.J., Baker R.T., Harris M.J., Parish C.R. Cloning of mammalian heparanase, an important enzyme in tumor invasion and metastasis. Nat. Med. 1999, 5:803-809.
13. Hulett M.D., Hornby J.R., Ohms S.J., Zuegg J., Freeman C., Gready J.E., Parish C.R. Identification of active-site residues of the pro-metastatic endoglycosidase heparanase. Biochemistry 2000, 39:15659-15667.
14. 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.
15. Kussie P.H., Hulmes J.D., Ludwig D.L., Patel S., Navarro E.C., Seddon A.P., Giorgio N.A., Bohlen P. Cloning and functional expression of a human heparanase gene. Biochem. Biophys. Res. Commun. 1999, 261:183-187.
16. 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.
17. Levy-Adam F., Feld S., Cohen-Kaplan V., Shteingauz A., Gross M., Arvatz G., Naroditsky I., Ilan N., Doweck I., Vlodavsky I. Heparanase 2 interacts with heparan sulfate with high affinity and inhibits heparanase activity. J. Biol. Chem. 2010, 285:28010-28019.
18. Levy-Adam F., Feld S., Suss-Toby E., Vlodavsky I., Ilan N. Heparanase facilitates cell adhesion and spreading by clustering of cell surface heparan sulfate proteoglycans. PLoS One 2008, 3:e2319.
19. 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.
20. Nadir Y., Brenner B., Zetser A., Ilan N., Shafat I., Zcharia E., Goldshmidt O., Vlodavsky I. Heparanase induces tissue factor expression in vascular endothelial and cancer cells. J. Thromb. Haemost. 2006, 4:2443-2451.
21. Osterholm C., Folkersen L., Lengquist M., Ponten F., Renne T., Li J., Hedin U. Increased expression of heparanase in symptomatic carotid atherosclerosis. Atherosclerosis Oct. 23 2012.
22. Pang J., Zhang S., Yang P., Hawkins-Lee B., Zhong J., Zhang Y., Ochoa B., Agundez J.A., Voelckel M.A., Fisher R.B., Gu W., Xiong W.C., Mei L., She J.X., Wang C.Y. Loss-of-function mutations in HPSE2 cause the autosomal recessive urofacial syndrome. Am. J. Hum. Genet. 2010, 86:957-962.
23. Parish C.R., Freeman C., Hulett M.D. Heparanase: a key enzyme involved in cell invasion. Biochim. Biophys. Acta 2001, 1471:M99-108.
24. 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.
25. 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.
26. 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. Feb 4 2013.
27. 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.
28. 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.
29. Sanderson R.D., Iozzo R.V. Targeting heparanase for cancer therapy at the tumor-matrix interface. Matrix Biol. 2012, 31:283-284.
30. 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. July 22 2012.
31. Toyoshima M., Nakajima M. Human heparanase. Purification, characterization, cloning, and expression. J. Biol. Chem. 1999, 274:24153-24160.
32. Vlodavsky I., Beckhove P., Lerner I., Pisano C., Meirovitz A., Ilan N., Elkin M. Significance of heparanase in cancer and inflammation. Cancer Microenviron. 2012, 5:115-132.
33. 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.
34. Vreys V., David G. Mammalian heparanase: what is the message?. J. Cell. Mol. Med. 2007, 11:427-452.
35. 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.
36. Ziolkowski A.F., Popp S.K., Freeman C., Parish C.R., Simeonovic C.J. Heparan sulfate and heparanase play key roles in mouse beta cell survival and autoimmune diabetes. J. Clin. Invest. 2012, 122:132-141.