Processing of VEGF-A by matrix metalloproteinases regulates bioavailability and vascular patterning in tumors

Journal of Cell Biology

Volumn 169, Issue 4, 2005, Pages 681-691

  Lee, Sunyoung ^a   Jilan, Shahla M ^a   Nikolova, Ganka V ^a   Carpizo, Darren ^a   Luisa Iruela Arispe, M ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ISOPROTEIN; MATRIX METALLOPROTEINASE; RECOMBINANT PROTEIN; VASCULOTROPIN A; VASCULOTROPIN RECEPTOR 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOAVAILABILITY; CANCER CELL CULTURE; CAPILLARY; CELL STRAIN HEK293; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN CELL; MOUSE; NEOVASCULARIZATION (PATHOLOGY); NONHUMAN; PEPTIDE MAPPING; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; REGULATORY MECHANISM; SOLUBILITY; SWINE; TUMOR; TUMOR VASCULARIZATION; VASODILATATION;

ANIMALS; BLOOD VESSELS; CELL LINE; CELL LINE, TUMOR; ENDOTHELIAL CELLS; EXTRACELLULAR MATRIX; FEMALE; HUMANS; MATRIX METALLOPROTEINASES; MICE; MICE, NUDE; NEOPLASM INVASIVENESS; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; PEPTIDE FRAGMENTS; PHOSPHORYLATION; PROTEIN ISOFORMS; RECEPTORS, VASCULAR ENDOTHELIAL GROWTH FACTOR; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASODILATION;

EID: 22344437713     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200409115     Document Type: Article

References (51)

1. Balbin, M., A. Fueyo, A.M. Tester, A.M. Pendas, A.S. Pitiot, A. Astudillo, C.M. Overall, S.D. Shapiro, and C. Lopez-Otin. 2003. Loss of collagenase-2 confers increased skin tumor susceptibility to male mice. Nat. Genet. 35:252-257.
2. Bergers, G., R. Brekken, G. McMahon, T.H. Vu, T. Itoh, K. Tamaki, K. Tanzawa, P. Thorpe, S. Itohara, Z. Werb, and D. Hanahan. 2000. Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis. Nat. Cell Biol. 2:737-744.
3. Bergsten, E., M. Uutela, X. Li, K. Pietras, A. Ostman, C.H. Heldin, K. Alitalo, and U. Eriksson. 2001. PDGF-D is a specific, protease-activated ligand for the PDGF beta-receptor. Nat. Cell Biol. 3:512-516.
4. Borrell-Pages, M., F. Rojo, J. Albanell, J. Baselga, and J. Arribas. 2003. TACE is required for the activation of the EGFR by TGF-alpha in tumors. EMBO J. 22:1114-1124.
5. Carmeliet, P., and R.K. Jain. 2000. Angiogenesis in cancer and other diseases. Nature. 407:249-257.
6. Carmeliet, P., V. Ferreira, G. Breier, S. Pollefeyt, L. Kieckens, M. Gertsenstein, M. Fahrig, A. Vandenhoeck, K. Harpal, C. Eberhardt, et al. 1996. Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature. 380:435-439.
7. Coussens, L.M., and Z. Werb. 2002. Inflammation and cancer. Nature. 420: 860-867.
8. Damert, A., L. Miquerol, M. Gertsenstein, W. Risau, and A. Nagy. 2002. Insufficient VEGFA activity in yolk sac endoderm compromises haematopoietic and endothelial differentiation. Development. 129:1881-1892.
9. Darland, D.C., and P.A. D'Amore. 2001. Cell-cell interactions in vascular development. Curr. Top. Dev. Biol. 52:107-149.
10. Dvorak, H.F. 2002. Vascular permeability factor/vascular endothelial growth factor: a critical cytokine in tumor angiogenesis and a potential target for diagnosis and therapy. J. Clin. Oncol. 20:4368-4380.
11. Ferrara, N. 2000. VEGF: an update on biological and therapeutic aspects. Curr. Opin. Biotechnol. 11:617-624.
12. Ferrara, N. 2002. VEGF and the quest for tumour angiogenesis factors. Nat. Rev. Cancer. 2:795-803.
13. Ferrara, N., K. Carver-Moore, H. Chen, M. Dowd, L. Lu, K.S. O'Shea, L. Powell-Braxton, K.J. Hillan, and M.W. Moore. 1996. Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature. 380:439-442.
14. Ferrara, N., H.P. Gerber, and J. LeCouter. 2003. The biology of VEGF and its receptors. Nat. Med. 9:669-676.
15. Ferrara, N., K.J. Hillan, H.P. Gerber, and W. Novotny. 2004. Discovery and development of bevacizumab, an anti-VEGF antibody for treating cancer. Nat. Rev. Drug Discov. 3:391-400.
16. Fuentes-Prior, P., Y. Iwanaga, R. Huber, R. Pagila, G. Rumennik, M. Seto, J. Morser, D.R. Light, and W. Bode. 2000. Structural basis for the anticoagulant activity of the thrombin-thrombomodulin complex. Nature. 404:518-525.
17. Gerber, H.P., K.J. Hillan, A.M. Ryan, J. Kowalski, G.A. Keller, L. Rangell, B.D. Wright, F. Radtke, M. Aguet, and N. Ferrara. 1999. VEGF is required for growth and survival in neonatal mice. Development. 126:1149-1159.
18. Gerber, H.P., A.K. Malik, G.P. Solar, D. Sherman, X.H. Liang, G. Meng, K. Hong, J.C. Marsters, and N. Ferrara. 2002. VEGF regulates haematopoietic stem cell survival by an internal autocrine loop mechanism. Nature. 417:954-958.
19. Grunstein, J., J.J. Masbad, R. Hickey, F. Giordano, and R.S. Johnson. 2000. Isoforms of vascular endothelial growth factor act in a coordinate fashion To recruit and expand tumor vasculature. Mol. Cell. Biol. 20:7282-7291.
20. Hamano, Y., M. Zeisberg, H. Sugimoto, J.C. Lively, Y. Maeshima, C. Yang, R.O. Hynes, Z. Werb, A. Sudhakar, and R. Kalluri. 2003. Physiological levels of tumstatin, a fragment of collagen IV alpha3 chain, are generated by MMP-9 proteolysis and suppress angiogenesis via alphaV beta3 integrin. Cancer Cell. 3:589-601.
21. Heissig, B., K. Hattori, M. Friedrich, S. Rafii, and Z. Werb. 2003. Angiogenesis: vascular remodeling of the extracellular matrix involves metalloproteinases. Curr. Opin. Hematol. 10:136-141.
22. Helmlinger, G., M. Endo, N. Ferrara, L. Hlatky, and R.K. Jain. 2000. Formation of endothelial cell networks. Nature. 405:139-141.
23. Houck, K.A., N. Ferrara, J. Winer, G. Cachianes, B. Li, and D.W. Leung. 1991. The vascular endothelial growth factor family: identification of a fourth molecular species and characterization of alternative splicing of RNA. Mol. Endocrinol. 5:1806-1814.
24. Houck, K.A., D.W. Leung, A.M. Rowland, J. Winer, and N. Ferrara. 1992. Dual regulation of vascular endothelial growth factor bioavailability by genetic and proteolytic mechanisms. J. Biol. Chem. 267:26031-26037.
25. Hutchings, H., N. Ortega, and J. Plouet. 2003. Extracellular matrix-bound vascular endothelial growth factor promotes endothelial cell adhesion, migration, and survival through integrin ligation. FASEB J. 17:1520-1522.
26. Inoue, M., J.H. Hager, N. Ferrara, H.P. Gerber, and D. Hanahan. 2002. VEGF-A has a critical, nonredundant role in angiogenic switching and pancreatic beta cell carcinogenesis. Cancer Cell. 1:193-202.
27. Junttila, T.T., M. Sundvall, J.A. Maatta, and K. Elenius. 2000. Erbb4 and its isoforms: selective regulation of growth factor responses by naturally occurring receptor variants. Trends Cardiovasc. Med. 10:304-310.
28. Keck, R.G., L. Berleau, R. Harris, and B.A. Keyt. 1997. Disulfide structure of the heparin binding domain in vascular endothelial growth factor: characterization of posttranslational modifications in VEGF. Arch. Biochem. Biophys. 344:103-113.
29. Kim, K.J., B. Li, J. Winer, M. Armanini, N. Gillett, H.S. Phillips, and N. Ferrara. 1993. Inhibition of vascular endothelial growth factor-induced angiogenesis suppresses tumour growth in vivo. Nature. 362:841-844.
30. Luque, A., D.R. Carpizo, and M.L. Iruela-Arispe. 2003. ADAMTS1/METH1 inhibits endothelial cell proliferation by direct binding and sequestration of VEGF165. J. Biol. Chem. 278:23656-23665.
31. McColl, B.K., M.E. Baldwin, S. Roufail, C. Freeman, R.L. Moritz, R.J. Simpson, K. Alitalo, S.A. Stacker, and M.G. Achen. 2003. Plasmin activates the lymphangiogenic growth factors VEGF-C and VEGF-D. J. Exp. Med. 198:863-868.
32. McDonald, D.M., and P.L. Choyke. 2003. Imaging of angiogenesis: from microscope to clinic. Nat. Med. 9:713-725.
33. McQuibban, G.A., J.H. Gong, E.M. Tam, C.A. McCulloch, I. Clark-Lewis, and C.M. Overall. 2000. Inflammation dampened by gelatinase A cleavage of monocyte chemoattractant protein-3. Science. 289:1202-1206.
34. McQuibban, G.A., J.H. Gong, J.P. Wong, J.L. Wallace, I. Clark-Lewis, and C.M. Overall. 2002. Matrix metalloproteinase processing of monocyte chemoattractant proteins generates CC chemokine receptor antagonists with anti-inflammatory properties in vivo. Blood. 100:1160-1167.
35. Miquerol, L., B.L. Langille, and A. Nagy. 2000. Embryonic development is disrupted by modest increases in vascular endothelial growth factor gene expression. Development. 127:3941-3946.
36. Nanba, D., A. Mammoto, K. Hashimoto, and S. Higashiyama. 2003. Proteolytic release of the carboxy-terminal fragment of proHB-EGF causes nuclear export of PLZF. J. Cell Biol. 163:489-502.
37. O'Reilly, M.S., D. Wiederschain, W.G. Stetler-Stevenson, J. Folkman, and M.A. Moses. 1999. Regulation of angiostatin production by matrix metalloproteinase-2 in a model of concomitant resistance. J. Biol. Chem. 274:29568-29571.
38. Overall, C.M., and C. Lopez-Otin. 2002. Strategies for MMP inhibition in cancer: innovations for the post-trial era. Nat. Rev. Cancer. 2:657-672.
39. Park, J.E., G.A. Keller, and N. Ferrara. 1993. The vascular endothelial growth factor (VEGF) isoforms: differential deposition into the subepithelial extracellular matrix and bioactivity of extracellular matrix-bound VEGF. Mol. Biol. Cell. 4:1317-1326.
40. Pettersson, A., J.A. Nagy, L.F. Brown, C. Sundberg, E. Morgan, S. Jungles, R. Carter, J.E. Krieger, E.J. Manseau, V.S. Harvey, et al. 2000. Heterogeneity of the angiogenic response induced in different normal adult tissues by vascular permeability factor/vascular endothelial growth factor. Lab. Invest. 80:99-115.
41. Plouet, J., F. Moro, S. Bertagnolli, N. Coldeboeuf, H. Mazarguil, S. Clamens, and F. Bayard. 1997. Extracellular cleavage of the vascular endothelial growth factor 189-amino acid form by urokinase is required for its mitogenic effect. J. Biol. Chem. 272:13390-13396.
42. Poltorak, Z., T. Cohen, R. Sivan, Y. Kandelis, G. Spira, I. Vlodavsky, E. Keshet, and G. Neufeld. 1997. VEGF145, a secreted vascular endothelial growth factor isoform that binds to extracellular matrix. J. Biol. Chem. 272:7151-7158.
43. Pozzi, A., P.E. Moberg, L.A. Miles, S. Wagner, P. Soloway, and H.A. Gardner. 2000. Elevated matrix metalloprotease and angiostatin levels in integrin alpha 1 knockout mice cause reduced tumor vascularization. Proc. Natl. Acad. Sci. USA. 97:2202-2207.
44. Robinson, C.J., and S.E. Stringer. 2001. The splice variants of vascular endothelial growth factor (VEGF) and their receptors. J. Cell Sci. 114:853-865.
45. Rodriguez-Manzaneque, J.C., T.F. Lane, M.A. Ortega, R.O. Hynes, J. Lawler, and M.L. Iruela-Arispe. 2001. Thrombospondin-1 suppresses spontaneous tumor growth and inhibits activation of matrix metalloproteinase-9 and mobilization of vascular endothelial growth factor. Proc. Natl. Acad. Sci. USA. 98:12485-12490.
46. Rossant, J., and M. Hirashima. 2003. Vascular development and patterning: making the right choices. Curr. Opin. Genet. Dev. 13:408-412.
47. Ruhrberg, C., H. Gerhardt, M. Golding, R. Watson, S. Ioannidou, H. Fujisawa, C. Betsholtz, and D.T. Shima. 2002. Spatially restricted patterning cues provided by heparin-binding VEGF-A control blood vessel branching morphogenesis. Genes Dev. 16:2684-2698.
48. Sioussat, T.M., H.F. Dvorak, T.A. Brock, and D.R. Senger. 1993. Inhibition of vascular permeability factor (vascular endothelial growth factor) with antipeptide antibodies. Arch. Biochem. Biophys. 301:15-20.
49. Tischer, E., R. Mitchell, T. Hartman, M. Silva, D. Gospodarowicz, J.C. Fiddes, and J.A. Abraham. 1991. The human gene for vascular endothelial growth factor. Multiple protein forms are encoded through alternative exon splicing. J. Biol. Chem. 266:11947-11954.
50. Vazquez, F., J.C. Rodriguez-Manzaneque, J.P. Lydon, D.P. Edwards, B.W. O'Malley, and M.L. Iruela-Arispe. 1999. Progesterone regulates proliferation of endothelial cells. J. Biol. Chem. 274:2185-2192.
51. Vincenti, V., C. Cassano, M. Rocchi, and G. Persico. 1996. Assignment of the vascular endothelial growth factor gene to human chromosome 6p21.3. Circulation. 93:1493-1495.