MT1-MMP-dependent neovessel formation within the confines of the three-dimensional extracellular matrix

Journal of Cell Biology

Volumn 167, Issue 4, 2004, Pages 757-767

  Chun, Tae Hwa ^a   Sabeh, Farideh ^a   Ota, Ichiro ^a   Murphy, Hedwig ^b   McDonagh, Kevin T ^b   Holmbeck, Kenn ^c   Birkedal Hansen, Henning ^c   Allen, Edward D ^a   Weiss, Stephen J ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA3 INTEGRIN; CELL SURFACE RECEPTOR; COLLAGEN TYPE 1; GELATINASE A; GELATINASE B; HERMES ANTIGEN; MATRIX METALLOPROTEINASE 14; PLASMINOGEN;

ANGIOGENESIS; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL INVASION; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME ACTIVITY; ENZYME ANALYSIS; EX VIVO STUDY; EXPLANT; EXTRACELLULAR MATRIX; GENE TARGETING; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION;

ANIMALS; ANTIGENS, CD44; BLOOD VESSELS; CELL MEMBRANE; CELLS, CULTURED; CHICK EMBRYO; COLLAGEN TYPE I; ENDOTHELIAL CELLS; EXTRACELLULAR MATRIX; GENE TARGETING; HUMANS; INTEGRIN BETA3; MALE; MATRIX METALLOPROTEINASE 14; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; MATRIX METALLOPROTEINASES, MEMBRANE-ASSOCIATED; METALLOENDOPEPTIDASES; MICE; MICE, KNOCKOUT; MODELS, BIOLOGICAL; NEOVASCULARIZATION, PHYSIOLOGIC; PHENOTYPE; PLASMINOGEN; RECEPTORS, CELL SURFACE;

ANIMALIA;

EID: 9444274032     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200405001     Document Type: Article

References (65)

1. Andrews, K.L., T. Betsuyaku, S. Rogers, J.M. Shipley, R.M. Senior, and J.H. Miner. 2000. Gelatinase B (MMP-9) is not essential in the normal kidney and does not influence progression of renal disease in a mouse model of Alport Syndrome. Am. J. Pathol. 157:303-311.
2. Atkinson, S.J., M.L. Patterson, M.J. Butler, and G. Murphy. 2001. Membrane type 1 matrix metalloproteinase and gelatinase A synergistically degrade type 1 collagen in a cell model. FEBS Lett. 491:222-226.
3. Baluk, P., W.W. Raymond, E. Ator, L.M. Coussens, D.M. McDonald, and G.H. Caughey. 2004. Matrix metalloproteinase-2 and -9 expression increases in Mycoplasma-infected airways but is not required for microvascular remodeling. Am. J. Physiol. Lung Cell. Mol. Physiol. 287:L307-L317.
4. 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.
5. Berglin, L., S. Sarman, I. van der Ploeg, B. Steen, Y. Ming, S. Itohara, S. Seregard, and A. Kvanta. 2003. Reduced choroidal neovascular membrane formation in matrix metalloproteinase-2-deficient mice. Invest. Ophthalmol. Vis. Sci. 44:403-408.
6. Brodsky, S., J. Chen, A. Lee, K. Akassoglou, J. Norman, and M.S. Goligorsky. 2001. Plasmin-dependent and -independent effects of plasminogen activators and inhibitor-1 on ex vivo angiogenesis. Am. J. Physiol. Heart Circ. Physiol. 281:H1784-H1792.
7. 3. Cell. 85:683-693.
8. Brooks, P.C., S. Silletti, T.L. von Schlascha, M. Friedlander, and D.A. Cheresh. 1998. Disruption of angiogenesis by PEX, a noncatalytic metalloproteinase fragment with integrin binding activity. Cell. 92:391-400.
9. Cameron, M.D., E.E. Schmidt, N. Kerkvliet, K.V. Nadkarni, V.L. Morris, A.C. Groom, A.F. Chambers, and I.C. MacDonald. 2000. Temporal progression of metastasis in lung: cell survival, dormancy, and location dependence of metastatic inefficiency. Cancer Res. 60:2541-2546.
10. Canham, P.B., H.M. Finlay, J.A. Kiernan, and G.G. Ferguson. 1999. Layered structure of saccular aneurysms assessed by collagen birefringence. Neurol. Res. 21:618-626.
11. Carmeliet, P., and R.K. Jain. 2000. Angiogenesis in cancer and other diseases. Nature. 407:249-257.
12. Carver, W., L. Terracio, and T.K. Borg. 1993. Expression and accumulation of interstitial collagen in the neonatal rat heart. Anat. Rec. 236:511-520.
13. Collen, A., R. Hanemaaijer, F. Lupu, P.A. Quax, N. van Lent, J. Grimbergene, E. Peters, P. Koolwijk, and V.W. van Hinsbergh. 2003. Membrane-type matrix metalloproteinase-mediated angiogenesis in a fibrin-collagen matrix. Blood. 101:1810-1817.
14. Creemers, L.B., D.C. Jansen, A. van Veen-Reurings, T. van den Bos, and V. Everts. 1997. Microassay for the assessment of low levels of hydroxyproline. Biotechniques. 22:656-658.
15. Davis, G.E., K.A. Pintar Allen, R. Salazar, and S.A. Maxwell. 2001. Matrix metalloproteinase-1 and -9 activation by plasmin regulates a novel endothelial cell-mediated mechanism of collagen gel contraction and capillary tube regression in three-dimensional collagen matrices. J. Cell Sci. 114:917-930.
16. Davis, G.E., K.J. Bayless, and A. Mavila. 2002. Molecular basis of endothelial cell morphogenesis in three-dimensional extracellular matrices. Anat. Rec. 268:252-275.
17. 3 in tumor cells expressing membrane-type 1 matrix metalloproteinase. Int. J. Cancer. 86:15-23.
18. Egeblad, M., and Z. Werb. 2002. New functions for the matrix metalloproteinases in cancer progression. Nat. Rev. Cancer. 2:161-174.
19. Engsig, M.T., Q.-J. Chen, T.H. Vu, A.-C. Pedersen, B. Therrkidsen, L.R. Lund, K. Henriksen, T. Lenhard, N.T. Foged, Z. Werb, and J.-M. Delaisse. 2000. Matrix metalloproteinase 9 and vascular endothelial growth factor are essential for osteoclast recruitment into developing long bones. J. Cell Biol. 151:879-889.
20. Fisher, C., S. Gilbertson-Beadling, E.A. Powers, G. Petzold, R. Poorman, and M.A. Mitchell. 1994. Interstitial collagenase is required for angiogenesis in vitro. Dev. Biol. 162:499-510.
21. 3 integrins at distinct cell compartments modulating its internalization and activity on human endothelial cells. J. Cell Biol. 159:509-521.
22. Guedez, L., A.M. Rivera, R. Salloum, M.L. Miller, J.J. Diegmueller, P.M. Bungam, and W.G. Stetler-Stevenson. 2003. Quantitative assessment of angiogenic responses by the directed in vivo angiogenesis assay. Am. J. Pathol. 162:1431-1439.
23. Haas, T.L., S.J. Davis, and J.A. Madri. 1998. Three-dimensional type I collagen lattices induce coordinate expression of matrix metalloproteinases MT1-MMP and MMP-2 in microvascular endothelial cells. J. Biol. Chem. 273:3604-3610.
24. 3 integrin. Cancer Cell. 3:589-601.
25. Hay, E.D. 1991. Cell Biology of Extracellular Matrix. Plenum Press, New York. 417 pp.
26. 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.
27. Hiraoka, N., E. Allen, I.J. Apel, M.R. Gyetko, and S.J. Weiss. 1998. Matrix metalloproteinases regulate neovascularization by acting as pericellular fibrinolysins. Cell. 95:365-377.
28. Holmbeck, K., P. Bianco, J. Caterina, S. Yamada, M. Kromer, S.A. Kuznetsov, M. Mankani, P.O. Robey, A.R. Poole, I. Pidoux, et al. 1999. MT1-MMP-deficient mice develop dwarfism, osteopenia, arthritis, and connective tissue disease due to inadequate collagen turnover. Cell. 99:81-92.
29. Hotary, K., E. Allen, A. Punturieri, I. Yana, and S.J. Weiss. 2000. Regulation of cell invasion and morphogenesis in a three-dimensional type I collagen matrix by membrane-type matrix metalloproteinases 1, 2, and 3. J. Cell Biol. 149:1309-1323.
30. Hotary, K.B., I. Yana, F. Sabeh, X.-Y. Li, K. Holmbeck, H. Birkedal-Hansen, E.D. Allen, N. Hiraoka, and S.J. Weiss. 2002. Matrix metalloproteinases (MMPs) regulate fibrin-invasive activity via MT1-MMP-dependent and -independent processes. J. Exp. Med. 195:295-308.
31. Hotary, K.B., E.D. Allen, P.C. Brooks, N.S. Datta, M.W. Long, and S.J. Weiss. 2003. Membrane type I matrix metalloproteinase usurps tumor growth control imposed by the three-dimensional extracellular matrix. Cell. 114:33-45.
32. Itoh, T., M. Tanioka, H. Yoshida, T. Yoshioka, H. Nishimoto, and S. Itohara. 1998. Reduced angiogenesis and tumor progression in gelatinase A-deficient mice. Cancer Res. 58:1048-1051.
33. Kajita, M., Y. Itoh, T. Chiba, H. Mori, A. Okada, H. Kinoh, and M. Seiki. 2001. Membrane-type 1 matrix metalloproteinase cleaves CD44 and promotes cell migration. J. Cell Biol. 153:893-904.
34. Kheradmand, F., K. Rishi, and Z. Werb. 2002. Signaling through the EGF receptor controls lung morphogenesis in part by regulating MT1-MMP-mediated activation of gelatinase A/MMP2. J. Cell Sci. 115:839-848.
35. Koivunen, E., W. Arap, H. Valtanen, A. Rainisalo, O.P. Medina, P. Heikkila, C. Kantor, C.G. Gahmberg, T. Salo, Y.T. Konttinen, et al. 1999. Tumor targeting with a selective gelatinase inhibitor. Nat. Biotechnol. 17:768-774.
36. Lafleur, M.A., M.M. Handsley, V. Knauper, G. Murphy, and D.R. Edwards. 2002. Endothelial tubulogenesis within fibrin gels specifically requires the activity of membrane-type-matrix metalloproteinases (MT-MMPs). J. Cell Sci. 115:3427-3438.
37. Lelongt, B., G. Trugnan, G. Murphy, and P.M. Ronco. 1997. Matrix metalloproteinases MMP2 and MMP9 are produced in early stages of kidney morphogenesis but only MMP9 is required for renal organogenesis in vitro. J. Cell Biol. 136:1363-1373.
38. Lubarsky, B., and M.A. Krasnow. 2003. Tube morphogenesis: making and shaping biological tubes. Cell. 112:19-28.
39. Lyden, D., A.Z. Young, D. Zagzag, W. Yan, W. Gerald, R. O'Reilly, B.L. Bader, R.O. Hynes, Y. Zhuang, K. Manova, and R. Benezra. 1999. Id1 and Id3 are required for neurogenesis, angiogenesis and vascularization of tumour xenografts. Nature. 401:670-677.
40. Miralles, F., T. Battelino, P. Czernichow, and R. Scharfmann. 1998. TGF-β plays a key role in morphogenesis of the pancreatic islets of Langerhans by controlling the activity of the matrix metalloproteinase MMP-2. J. Cell Biol. 143:827-836.
41. Mori, H., T. Tomari, N. Koshikawa, M. Kajita, Y. Itoh, H. Sato, H. Tojo, I. Yana, and M. Seiki. 2002. CD44 directs membrane-type 1 matrix metalloproteinase to lamellipodia by associating with its hemopexin-like domain. EMBO J. 21:3949-3959.
42. Morita, Y., J. Yang, R. Gupta, K. Shimizu, E.A. Shelden, J. Endres, J.J. Mule, K.T. McDonagh, and D.A. Fox. 2001. Dendritic cells genetically engineered to express IL-4 inhibit murine collagen-induced arthritis. J. Clin. Invest. 107:1275-1284.
43. Murphy, H.S., N. Bakopoulos, M.K. Dame, J. Varani, and P.A. Ward. 1998. Heterogeneity of vascular endothelial cells: differences in susceptibility to neutrophil-mediated injury. Microvasc. Res. 56:203-211.
44. Nicosia, R.F., and J.A. Madri. 1987. The microvascular extracellular matrix. Developmental changes during angiogenesis in the aortic ring-plasma clot model. Am. J. Pathol. 128:78-90.
45. Oh, J., R. Takahashi, E. Adachi, S. Kondo, S. Kuratomi, A. Noma, D.B. Alexander, H. Motoda, A. Okada, M. Seiki, et al. 2004. Mutations in two matrix metalloproteinase genes, MMP-2 and MT1-MMP, are synthetic lethal in mice. Oncogene. 23:5041-5048.
46. Ohuchi, E., K. Imai, Y. Fujii, H. Sato, M. Seiki, and Y. Okada. 1997. Membrane type 1 matrix metalloproteinase digests interstitial collagens and other extracellular matrix macromolecules. J. Biol. Chem. 272:2446-2451.
47. Pepper, M.S. 2001. Role of the matrix metalloproteinase and plasminogen activator-plasmin systems in angiogenesis. Arterioscler. Thromb. Vasc. Biol. 21:1104-1117.
48. 5 integrins. Nat. Med. 8:27-34.
49. 3 cooperates with metalloproteinase MMP-9 in regulating migration of metastatic breast cancer cells. Proc. Natl. Acad. Sci. USA. 100:9482-9487.
50. Romer, J., T.H. Bugge, C. Pyke, L.R. Lund, M.J. Flick, J.L. Degen, and K. Dano. 1996. Impaired wound healing in mice with a disrupted plasminogen gene. Nat. Med. 2:287-292.
51. Seandel, M., K. Noack-Kunnmann, D. Zhu, R.T. Aimes, and J.P. Quigley. 2001. Growth factor-induced angiogenesis in vivo requires specific cleavage of fibrillar type I collagen. Blood. 97:2323-2332.
52. Seiki, M. 2002. The cell surface: the stage for matrix metalloproteinase regulation of migration. Curr. Opin. Cell Biol. 14:624-632.
53. Seo, D.-W., H. Li, L. Guedez, P.T. Wingfield, T. Diaz, R. Salloum, B.-Y. Wei, and W.G. Stetler-Stevenson. 2003. TIMP-2 mediated inhibition of angiogenesis: an MMP-independent mechanism. Cell. 114:171-180.
54. Shi, G.-P., G.K. Sukhova, M. Kuzuya, Q. Ye, J. Du, Y. Zhang, J.-H. Pan, M.L. Lu, X.W. Cheng, A. Iguchi, et al. 2003. Deficiency of the cysteine protease cathepsin S impairs microvessel growth. Circ. Res. 92:493-500.
55. 3 by an organic molecule inhibits angiogenesis and tumor growth in vivo. Proc. Natl. Acad. Sci. USA. 98:119-124.
56. Tournier, J.-M., M. Polette, J. Hinnrasky, J. Beck, Z. Werb, and C. Basbaum. 1994. Expression of gelatinase A, a mediator of extracellular matrix remodeling, by tracheal gland serous cells in culture and in vivo. J. Biol. Chem. 269:25454-25464.
57. Toth, M., I. Chvyrkova, M.M. Bernardo, S. Hernandez-Barrantes, and R. Fridman. 2003. Pro-MMP-9 activation by the MT1-MMP/MMP-2 axis and MMP-3: role of TIMP-2 and plasma membranes. Biochem. Biophys. Res. Commun. 308:386-395.
58. Van Exan, R.J., and M.H. Hardy. 1984. The differentiation of the dermis in the laboratory mouse. Am. J. Anat. 169:149-164.
59. Wang, Q., P. Teder, N.P. Judd, P.W. Noble, and C.M. Doerschuk. 2002. CD44 deficiency leads to enhanced neutrophil migration and lung injury in Escherichia coli pneumonia in mice. Am. J. Pathol. 161:2219-2228.
60. Wiseman, B.S., M.D. Sternlicht, L.R. Lund, C.M. Alexander, J. Mott, M.J. Bissell, P. Soloway, S. Itohara, and Z. Werb. 2003. Site-specific inductive and inhibitory activities of MMP-2 and MMP-3 orchestrate mammary gland branching morphogenesis. J. Cell Biol. 162:1123-1133.
61. Xu, J., E. Petitclerc, J.J. Kim, M. Hangai, S.M. Yuen, G.E. Davis, and P.C. Brooks. 2001. Proteolytic exposure of a cryptic site within collagen type IV is required for angiogenesis and tumor growth in vivo. J. Cell Biol. 154:1069-1079.
62. Yana, I., and S.J. Weiss. 2000. Regulation of membrane type-1 matrix metalloproteinase activation by proprotein convertases. Mol. Biol. Cell. 11:2387-2401.
63. Yu, Q., and I. Stamenkovic. 1999. Localization of matrix metalloproteinase 9 to the cell surface provides a mechanism for CD44-mediated tumor invasion. Genes Dev. 13:35-48.
64. Zhou, Z., S.S. Apte, R. Soininen, R. Cao, G.Y. Baaklini, R.W. Rauser, J. Wang, Y. Cao, and K. Tryggvason. 2000. Impaired endothondral ossification and angiogenesis in mice deficient in membrane-type matrix metalloproteinase I. Proc. Natl. Acad. Sci. USA. 97:4052-4057.
65. Zhu, W.-H., X. Guo, S. Villaschi, and R.F. Nicosia. 2000. Regulation of vascular growth and regression by matrix metalloproteinases in the rat aorta model of angiogenesis. Lab. Invest. 80:545-555.