Structure-function approach identifies a COOH-terminal domain mediates heparanase signaling

Cancer Research

Volumn 69, Issue 5, 2009, Pages 1758-1767

  Fux, Liat ^a   Feibish, Nir ^a   Cohen Kaplan, Victoria ^a   Gingis Velitski, Svetlana ^a   Feld, Sari ^a   Geffen, Chen ^a   Vlodavsky, Israel ^a   Neta, Ilan ^a  

^a TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

HEPARANASE; PROTEIN KINASE; BETA GLUCURONIDASE; PROTEIN KINASE B;

ANGIOGENESIS; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; FEMALE; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; METASTASIS; PRIORITY JOURNAL; PROTEIN DOMAIN; TUMOR GROWTH; TUMOR XENOGRAFT; ANIMAL; BAGG ALBINO MOUSE; CHEMICAL STRUCTURE; CHEMISTRY; CONFOCAL MICROSCOPY; DRUG ANTAGONISM; EXPERIMENTAL NEOPLASM; METABOLISM; MOUSE; PHOSPHORYLATION; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE; SIGNAL TRANSDUCTION; STRUCTURE ACTIVITY RELATION; TUMOR CELL LINE;

ANIMALS; CELL LINE, TUMOR; CELL PROLIFERATION; FEMALE; GLUCURONIDASE; HUMANS; MICE; MICE, INBRED BALB C; MICROSCOPY, CONFOCAL; MODELS, MOLECULAR; NEOPLASMS, EXPERIMENTAL; PHOSPHORYLATION; PROTEIN STRUCTURE, TERTIARY; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 62449097111     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-08-1837     Document Type: Article

References (41)

1. Parish CR, Freeman C, Hulett MD. Heparanase: a key enzyme involved in cell invasion. Biochim Biophys Acta 2001:1471 199-208.
2. Vlodavsky I, Friedmann Y. Molecular properties and involvement of heparanase in cancer metastasis and angiogenesis. J Clin Invest 2001;108:341-7.
3. Nakajima M, Irimura T, DiFerrante D, DiFerrante N, Nicolson GL. Heparan, sulfate degradation: relation to tumor invasive and metastatic properties of mouse B 16 melanoma sublines. Science 1983;220:611-3.
4. Vlodavsky I, Fuks Z, Bar-Ner M, Ariav Y, Schirrmacher V. Lymphoma cells mediated degradation of sulfated proteoglycans in the subendothelial extracellular matrix: relation to tumor cell metastasis. Cancer Res 1983:43: 2704-11.
5. Edovitsky E, EIkIn M, Zcharia E,Peretz T, Vlodavsky I. Heparanase gene silencing, tumor invasiveness, angio-genesis, and metastasis. J Natl Cancer Inst 2004:96: 121.9-30.
6. 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: 2018-39.
7. Vlodavsky I, Abboud-Jarrous G, Elkin M, et al. The impact of heparanese and heparin on cancer metastasis and angiogenesis. Pathophysiol Haemost Thromb 2006; 35:116-27.
8. Vlodavsky I, Ban N, Naggi A, Casu B. Heparanase: structure, biological functions, and Inhibition, by hepa-rin-derived mimetics of heparan sulfate. Curr Pharm Des 2007;13:2057-73.
9. Fairbanks MB, Mlldner AM, Leone JW, et al. Processing of the human heparanase precursor and evidence that the active enzyme is a heterodimer. J Biol Chem 1.999; 274:29587-90.
10. Levy-Adam F, Miao HQ, Heinrikson RL, Vlodavsky I, Ilan N. Heterodimer formation is essential for hepar-anase enzymatic activity. Biochem Biophys Res Commun 2003;308:885-91.
11. McKenzie E, Young K, Hircock M, et al. Biochemical characterization of the active heterodimer form, of human heparanase (Hpal) protein, expressed in Insect cells. Biochem J 2003;373:423-35.
12. Ben-Zaken O, Shafat I, Gingis-Velltski S, et al. Low and high affinity receptors mediate cellular uptake of heparanase. Int J Biochem Cell Biol 2008;40:530-42.
13. Gingis-Velitski S, Zetser A, Kaplan V, et al. Heparanase uptake is mediated by cell membrane heparan sulfate proteoglycans. J Biol Chem. 2004;279:44084-92.
14. Vreys V, Delande N, Zhang Z, et al. Cellular uptake of mammalian heparanase precursor involves low density lipoprotein receptor-related proteins, mannose 6-phos-phate receptors, and heparan, sulfate proteoglycans. J Biol Chem 2005;280:33141-8.
15. Goldshmidt O, Nadav L, Alngorn H, et al. Human heparanase is localized within lysosomes in a stable form. Exp Cell Res 2002;281:50-62.
16. Nadav L, Eldor A, Yacoby-Zeevi O, et al. Activation, processing and trafficking of extracellular heparanase by primary human, fibroblasts. J Cell Sci 2002:115: 2179-87.
17. Zetser A, Levy-Adam F, Kaplan V et al. Processing and activation of latent heparanase occurs in lysosomes. J Cell Sci 2004;117:2249-58.
18. Abboud-Jarrous G, Atzmon R, Peretz T, et al. Cathepsin L is responsible for processing and activation ofproheparanase through multiple cleavages of a linker segment. J Biol Chem. 2008;283:18167-76.
19. Abboud-Jarrous G, Ranglni-Guetta Z, Alngorn H, et al. Site-directed mutagenesis, proteolytic cleavage, and activation of human proheparanase. J Biol Chem 2005; 280:13568-75.
20. Levy-Adam F, Abboud-Jarrous G, Guerrini M, Beccati D, Vlodavsky I, Ban N. Identification and characterization of heparin/heparan sulfate binding domains of the endoglycosidase heparanase. J Biol Chem 2005:280: 20457-66.
21. Nardella C, Lahm A, Pallaoro M, Brunetti M, Vannini A, Steinkuhler C. Mechanism, of activation of human heparanase investigated by protein engineering. Bio-chemistry 2004;43:1862-73.
22. Goldshmidt O, Zcharia E, Cohen. M, et al. Heparanase mediates cell adhesion independent of its enzymatic activity. FASEB J 2003;17:1015-25.
23. Sotnikov I, Hershkoviz R, Grabovsky V, et al. Enzymatically quiescent heparanase augments T cell interactions with VCAM-I and extracellular matrix components under versatile dynamic contexts. J Immunol 2004;172:5185-93.
24. Zetser A, Bashenko Y, Miao H-Q, Vlodavsky I Ilan N. Heparanase affects adhesive and tumorigenic potential of human glioma cells. Cancer Res 2003;63:7733-41.
25. 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;66:1455-63.
26. Nadir Y, Brenner B, Zetser A, et al. Heparanase induces tissue factor expression in vascular endothelial and cancer cells. J Thromb Haemost 2006;4:2443-51.
27. Gingis-Velitski S, Zetser A, Flugelman MY, Vlodavsky I, Ilan N. Heparanase induces endothelial cell migration via protein, kinase B/A.kt activation. J Biol Chem 2004; 279:23536-41.
28. Cohen I, Pappo O, Elkin M, et al. Heparanase promotes growth, angiogenesis and survival of primary breast tumors. Int J Cancer 2006;118:1609-17.
29. Hulett MD, Hornby JR, Ohms SJ, et al. Identification of active-site residues of the prometastatic endoglycosidase heparanase. Biochemistry 2000;39:15659-67.
30. Kim DE, Chivian D, Baker D. Protein structure prediction and analysis using the Robetta server. Nucleic Acids Res 2004;32:W526-31.
31. Hovel K, Shallom D, Niefind K, et al. Crystal structure and snapshots along the reaction pathway of a family 51 a-i-arabinofuranosidase. EMBO J 2003;22:4922-32.
32. Rosenthal EL, Kulbersh BD, Duncan RD, et al. In vivo detection of head and neck cancer orthotopic xeno-grafts by immunofluorescence. Laryngoscope 2006:1.16: 1636-41.
33. Ben-Zaken O, Gingls-Velltski S, Vlodavsky I, Ilan N. Heparanase induces Akt phosphorylation via a lipid raft receptor. Biochem Biophys Res Commun 2007:361: 829-34.
34. 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.
35. Elkin M, Ilan N, Ishai-Michaeli R, et al. Heparanase as mediator of angiogenesis: mode of action. FASEB J 2001; 15:1661-3.
36. Zcharia E, Zilka R, Yaar A, et al. Heparanase accelerates wound angiogenesis and wound healing in mouse and rat models. FASEB J 2005;19:211-21.
37. Wood RJ, Hulett MD. CeU surface-expressed cation-independent mannose 6-phosphate receptor (CD222) binds enzymaticaUy active heparanase independently of mannose 6-phosphate to promote extracellular matrix degradation. J Biol Chem 2008;283:4165-76.
38. Bar-Ner M, Eldor A, Wasserman L, et al. Inhibition of heparanase-mediated degradation, of extracellular matrix heparan sulfate by non-anticoagulant heparin species. Blood 1987;70:551-7.
39. Lewis KD, Robinson WA, Millward MJ, et al. A phase II study of the heparanase inhibitor PI-88 in patients with advanced melanoma. Invest New Drugs 2008;26: 89-94.
40. Lai NS, Simizu S, Morisaki D, Muroi M, Osada H. Requirement of conserved, hydrophobic C-terminus region for the activation of heparanase. Exp Cell Res 2008;314:2834-45.
41. Stern R, Jedrzejas MJ. Hyaluronidases: their genomics, structures, and mechanisms of action. Chem Rev 2006;.106:818-39.