Regulation of matrix metalloproteinase (MMP) activity by the low-density lipoprotein receptor-related protein (LRP). A new function for an "old friend"

Biochimie

Volumn 87, Issue 3-4 SPEC. ISS., 2005, Pages 369-376

  Emonard, Hervé ^a,b   Bellon, Georges ^a   De Diesbach, Philippe ^b   Mettlen, Marcel ^b   Hornebeck, William ^a   Courtoy, Pierre J ^b  

^a CNRS   (France)

^b DE DUVE INSTITUTE   (Belgium)

Author keywords

Endocytosis; Low density lipoprotein receptor related protein; Matrix metalloproteinase; Regulation

Indexed keywords

LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN; MATRIX METALLOPROTEINASE; TISSUE INHIBITOR OF METALLOPROTEINASE; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TISSUE INHIBITOR OF METALLOPROTEINASE 2;

CANCER CELL; CELL COMPARTMENTALIZATION; CELL HETEROGENEITY; DOWN REGULATION; ENDOCYTOSIS; ENZYME ACTIVITY; EXTRACELLULAR MATRIX; FIBROSARCOMA; HUMAN; LIPOPROTEIN METABOLISM; NONHUMAN; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS REGULATION; REVIEW; STRUCTURE ANALYSIS; WESTERN BLOTTING;

EID: 15244352841     PISSN: 03009084     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biochi.2004.11.013     Document Type: Article

References (72)

1. M. Egeblad, and Z. Werb New functions for the matrix metalloproteinases in cancer progression Nat. Rev. Cancer 2 2002 161 174
2. M.D. Sternlicht, and Z. Werb How matrix metalloproteinases regulate cell behavior Annu. Rev. Cell Dev. Biol. 17 2001 463 516
3. W.G. Stetler-Stevenson Type IV collagenases in tumor invasion and metastasis Cancer Metast. Rev. 9 1990 283 303
4. T. Itoh, M. Tanioka, H. Yoshida, T. Yoshioka, H. Nishimoto, and S. Itohara Reduced angiogenesis and tumor progression in gelatinase A-deficient mice Cancer Res. 58 1998 1048 1051
5. G. Bergers, R. Brekken, G. McMahon, T.H. Vu, T. Itoh, K. Tamaki, K. Tanzawa, P. Thorpe, S. Itohara, Z. Werb, and D. Hanahan Matrix- metalloproteinase-9 triggers the angiogenic switch during carcinogenesis Nat. Cell Biol. 2 2000 737 744
6. C.F. Chantrain, H. Shimada, S. Jodele, S. Groshen, W. Ye, D.R. Shalinsky, Z. Werb, L.M. Coussens, and Y.A. DeClerck Stromal matrix metalloproteinase-9 regulates the vascular architecture in neuroblastoma by promoting pericyte recruitment Cancer Res. 64 2004 1675 1686
7. J.M.P. Freije, I. Díez-Itza, M. Balbín, L.M. Sánchez, R. Blasco, and J. Tolivia Molecular cloning and expression of collagenase-3, a novel human matrix metalloproteinase produced by breast carcinomas J. Biol. Chem. 269 1994 16766 16773
8. M. Balbín, A.M. Pendás, J.A. Uría, M.G. Jiḿnez, J.P. Freije, and C. López-Otín Expression and regulation of collagenase-3 (MMP-13) in human malignant tumors APMIS 107 1999 45 53
9. M.E. Fini, J.R. Cook, R. Mohan, and C.E. Brinckerhoff Regulation of matrix metalloproteinase gene expression W.C. Parks R.P. Mecham Matrix Metalloproteinases 1998 Academic Press San Diego 299 356
10. W. Hornebeck, H. Emonard, J.-C. Monboisse, and G. Bellon Matrix-directed regulation of pericellular proteolysis and tumor progression Semin. Cancer Biol. 12 2002 231 241
11. B.P. Toole EMMPRIN (CD147), a cell surface regulator of matrix metalloproteinase production and function Curr. Top. Dev. Biol. 54 2003 371 389
12. Y. Eeckhout, and P. Henriet Matrix metalloproteinases T.E. Creighton Wiley Encyclopedia of Molecular Medicine 2002 John Wiley & Sons Inc New York 2022 2026
13. S. Hernandez-Barrantes, M. Bernardo, M. Toth, and R. Fridman Regulation of membrane type-matrix metalloproteinases Semin. Cancer Biol. 12 2002 131 138
14. J.-S. Rhee, and L.M. Coussens RECKing MMP function: implications for cancer development Trends Cell Biol. 12 2002 209 211
15. C. Takahashi, Z. Sheng, T.P. Horan, H. Kitayama, M. Maki, K. Hitomi, Y. Kitaura, S. Takai, R.M. Sasahara, A. Horimoto, Y. Ikawa, B.J. Ratzkin, T. Arakawa, and M. Noda Regulation of matrix metalloproteinase-9 and inhibition of tumor invasion by the membrane-anchored glycoprotein RECK Proc. Natl. Acad. Sci. USA 95 1998 13221 13226
16. K. Brew, D. Dinakarpandian, and H. Nagase Tissue inhibitors of metalloproteinases: evolution, structure and function Biochim. Biophys. Acta 1477 2000 267 283
17. T. Kinoshita, H. Sato, A. Okada, E. Ohuchi, K. Imai, Y. Okada, and M. Seiki TIMP-2 promotes activation of progelatinase A by membrane-type 1 matrix metalloproteinase immobilized on agarose beads J. Biol. Chem. 273 1998 16098 16103
18. N.C. Partridge, J.J. Jeffrey, L.S. Ehlich, S.L. Teitelbaum, C. Fliszar, H.G. Welgus, and A.J. Kahn Hormonal regulation of the production of collagenase and a collagenase inhibitor activity by rat osteogenic sarcoma cells Endocrinology 120 1987 1956 1962
19. T.H. Omura, A. Noguchi, C.A. Johanns, J.J. Jeffrey, and N.C. Partridge Identification of a specific receptor for interstitial collagenase on osteoblastic cells J. Biol. Chem. 269 1994 24994 24998
20. J. Herz, and D.K. Strickland LRP: a multifunctional scavenger and signaling receptor J. Clin. Invest. 108 2001 779 784
21. J. Lawler The functions of thrombospondin-1 and -2 Curr. Opin. Cell Biol. 12 2000 634 640
22. 2-macroglobulin receptor mediates the cellular internalization and degradation of thrombospondin. A process facilitated by cell-surface proteoglycans J. Biol. Chem. 270 1995 9543 9549
23. H. Chen, D.K. Strickland, and D.F. Mosher Metabolism of thrombospondin 2. Binding and degradation by 3T3 cells and glycosaminoglycan-variant chinese hamster ovary cells J. Biol. Chem. 271 1996 15993 15999
24. A.M. Salicioni, K.S. Mizelle, E. Loukinova, I. Mikhailenko, D.K. Strickland, and S.L. Gonias The low density lipoprotein receptor-related protein mediates fibronectin catabolism and inhibits fibronectin accumulation on cell surfaces J. Biol. Chem. 277 2002 16160 16166
25. 2-macroglobulin receptor is an hepatic receptor for tissue-type plasminogen activator Proc. Natl. Acad. Sci. USA 89 1992 7427 7431
26. 2-macroglobulin receptor Proc. Natl. Acad. Sci. USA 89 1992 7422 7426
27. A. Nykjaer, L. Kjoller, R.L. Cohen, D.A. Lawrence, J. Gliemann, and P.A. Andreasen Both pro-uPA and uPA:PAI-1 complex bind to alpha 2-macroglobulin/LDL receptor-related protein. Evidence for multiple independent contacts between the ligands and receptor Ann. N. Y. Acad. Sci. 737 1994 483 485
28. K. Bajou, V. Masson, R.D. Gerard, P.M. Schmitt, V. Albert, M. Praus, L.R. Lund, T.L. Frandsen, N. Brunner, K. Dano, N.E. Fusenig, U. Weidle, G. Carmeliet, D. Loskutoff, D. Collen, P. Carmeliet, J.M. Foidart, and A. Noel The plasminogen activator inhibitor PAI-1 controls in vivo tumor vascularization by interaction with proteases, not vitronectin. Implications for antiangiogenic strategies J. Cell Biol. 152 2001 777 784
29. Z. Yang, D.K. Strickland, and P. Bornstein Extracellular matrix metalloproteinase 2 levels are regulated by the low density lipoprotein-related scavenger receptor and thrombospondin 2 J. Biol. Chem. 276 2001 8403 8408
30. E. Hahn-Dantona, J.F. Ruiz, P. Bornstein, and D.K. Strickland The low density lipoprotein receptor-related protein modulates levels of matrix metalloproteinase 9 (MMP-9) by mediating its cellular catabolism J. Biol. Chem. 276 2001 15498 15503
31. O.J. Barmina, H.W. Walling, G.J. Fiacco, J.M.P. Freije, C. Lopez-Otin, J.J. Jeffrey, and M.C. Partridge Collagenase-3 binds to a specific receptor and requires the low density lipoprotein receptor-related protein for internalization J. Biol. Chem. 274 1999 30087 30093
32. 2-macroglobulin receptor-associated protein. Human homologue of a Heymann nephritis antigen J. Biol. Chem. 266 1991 13364 13369
33. G. Bu, and A.L. Schwartz RAP, a novel type of ER chaperone Trends Cell Biol. 8 1998 272 276
34. B.J. Bacskai, M.Q. Xia, D.K. Strickland, G.W. Rebeck, and B.T. Hyman The endocytic receptor protein LRP also mediates neuronal calcium signaling via N-methyl-d-aspartate receptors Proc. Natl. Acad. Sci. USA 97 2000 11551 11556
35. Y. Zhu, and D.Y. Hui Apolipoprotein E binding to low density lipoprotein receptor-related protein-1 inhibits cell migration via activation of cAMP-dependent protein kinase A J. Biol. Chem. 278 2003 36257 36263
36. B. Degryse, J.G. Neels, R.-P. Czekay, K. Aertgeerts, Y.-I. Kamikubo, and D.J. Loskutoff The low density lipoprotein receptor-related protein is a motogenic receptor for plasminogen activator inhibitor-1 J. Biol. Chem. 279 2004 22595 22604
37. E. Loukinova, S. Ranganathan, S. Kuznetsov, N. Gorlatova, M.M. Migliorini, D. Loukinov, P.G. Ulery, I. Mikhailenko, D.A. Lawrence, and D.K. Strickland Platelet-derived growth factor (PDGF)-induced tyrosine phosphorylation of the low density lipoprotein receptor-related protein (LRP). Evidence for integrated co-receptor function between LRP and the PDGF J. Biol. Chem. 277 2002 15499 15506
38. D.E. Gomez, D.F. Alonso, H. Yoshiji, and U.P. Thorgeirsson Tissue inhibitors of metalloproteinases: structure, regulation and biological functions Eur. J. Cell Biol. 74 1997 111 122
39. S.M. Wilhelm, I.E. Collier, B.L. Marmer, A.Z. Eizen, G.A. Grant, and G.I. Goldberg SV40-transformed human lung fibroblasts secrete a 92-kDa type IV collagenase which is identical to that secreted by normal human macrophages J. Biol. Chem. 264 1989 17213 17221
40. L. Bailey, D. Wienke, M. Howard, V. Knäuper, C.M. Isacke, and G. Murphy Investigation of the role of Endo180/urokinase-type plasminogen activator receptor-associated protein as a collagenase 3 (matrix metalloproteinase 13) receptor Biochem. J. 363 2002 67 72
41. R.-P. Czekay, T.A. Kuemmel, R.A. Orlando, and M.G. Farquhar Direct binding of occupied urokinase receptor (uPAR) to LDL receptor-related protein is required for endocytosis of uPAR and regulation of cell surface urokinase activity Mol. Biol. Cell 12 2001 1467 1479
42. Z. Yang, T.R. Kyriakides, and P. Bornstein Matricellular proteins as modulators of cell-matrix interactions: adhesive defect in thrombospondin 2-null fibroblasts is a consequence of increased levels of matrix metalloproteinase-2 Mol. Biol. Cell 11 2000 3353 3364
43. K. Bein, and M. Simons Thrombospondin type 1 repeats interact with matrix metalloproteinase 2. Regulation of metalloproteinase activity J. Biol. Chem. 275 2000 32167 32173
44. G.I. Goldberg, B.L. Marmer, G.A. Grant, A.Z. Eizen, S. Wilhelm, and C. He Human 72-kilodalton type collagenase forms a complex with a tissue inhibitor of metalloproteases designated TIMP-2 Proc. Natl. Acad. Sci. USA 86 1989 8207 8211
45. H. Emonard, G. Bellon, L. Troeberg, A. Berton, A. Robinet, P. Henriet, E. Marbaix, K. Kirkegaard, L. Patthy, Y. Eeckhart, H. Magase, W. Hornebeck, and P.J. Courtoy The low density lipoprotein receptor-related protein mediates endocytic clearance of proMMP-2:TIMP-2 complex through a thrombospondin- independent pathway J. Biol. Chem. 279 2004 54944 54951
46. H.P. Emonard, A.G. Remacle, A.C. Noël, J.-A. Grimaud, W.G. Stetler-Stevenson, and J.-M. Foidart Tumor cell surface-associated binding site for the Mr 72,000 type IV collagenase Cancer Res. 52 1992 5845 5848
47. W.L. Monsky, T. Kelly, C.-Y. Lin, Y. Yeh, W.G. Stetler-Stevenson, and S.C. Mueller Binding and localization of Mr 72,000 matrix metalloproteinase at cell surface invadopodia Cancer Res. 53 1993 3159 3164
48. H. Nakahara, L. Howard, E.W. Thompson, H. Sato, M. Seiki, Y. Yeh, and W.-T. Chen Transmembrane/cytoplasmic domain-mediated membrane type 1-matrix metalloprotease docking to invadopodia is required for cell invasion Proc. Natl. Acad. Sci. USA 94 1997 7959 7964
49. K. Simons, and D. Toomre Lipid rafts and signal transduction Nat. Rev. Mol. Cell. Biol. 1 2000 31 39
50. S. Mañes, G. Del Real, and C.-A. Martínez Pathogens: raft hijackers Nat. Rev. Immunol. 3 2003 557 568
51. L. Pelkmans, and A. Helenius Endocytosis via caveolae Traffic 3 2002 311 320
52. A. Sorkin, and C.M. Waters Endocytosis of growth factor receptors Bioessays 15 1993 375 382
53. B. Annabi, M.-P. Lachambre, N. Bousquet-Gagnon, M. Paǵ, D. Gingras, and R. B́liveau Localization of membrane-type 1 matrix metalloproteinase in caveolae membrane domains Biochem. J. 353 2001 547 553
54. A. Puyraimond, R. Fridman, M. Lemesle, B. Arbeille, and S. Menashi MMP-2 colocalizes with caveolae on the surface of endothelial cells Exp. Cell Res. 262 2001 28 36
55. A. Remacle, G. Murphy, and C. Roghi Membrane type 1-matrix metalloproteinase (MT1-MMP- is internalized by two different pathways and is recycled to the cell surface J. Cell Sci. 116 2003 3905 3916
56. B.G. Gálvez, S. Matías-Román, M. Yáñez-Mó, M. Vicente-Manzanares, F. Sánchez-Madrid, and A.G. Arroyo Caveolae are a novel pathway for membrane-type 1 matrix metalloproteinase traffic in human endothelial cells Mol. Biol. Cell 15 2004 678 687
57. Y. Itoh, M. Kajita, H. Kinoh, H. Mori, A. Okada, and M. Seiki Membrane type 4 matrix metalloproteinase (MT4-MMP, MMP-17) is a glycosylphosphatidylinositol-anchored proteinase J. Biol. Chem. 274 1999 34260 34266
58. P. Boucher, P. Liu, M. Gotthard, T. Hiesberger, R.G.W. Anderson, and J. Herz Platelet-derived growth factor mediates tyrosine phosphorylation of the cytoplasmic domain of the low density lipoprotein receptor-related protein in caveolae J. Biol. Chem. 277 2002 15507 15513
59. P. Drevot, C. Langlet, X.-J. Guo, A.-M. Bernard, O. Colard, J.-P. Chauvin, R. Lasserre, and H.-T. He TCR signal initiation machinery is pre-assembled and activated in a subset of membrane rafts EMBO J 21 2002 1899 1908
60. B. Casslen, J. Nordengren, B. Gustavsson, M. Nilbert, and L.R.J. Lund Progesterone stimulates degradation of urokinase plasminogen activator (u-PA) in endometrial stromal cells by increasing its inhibitor and surface expression of the u-PA receptor J. Clin. Endocrinol. Metab. 80 1995 2776 2784
61. P. Henriet, P.B. Cornet, P. Lemoine, C. Galant, C.F. Singer, P.J. Courtoy, Y. Eeckhout, and E. Marbaix Circulating ovarian steroids and endometrial matrix metalloproteinases (MMPs) Ann. N.Y. Acad. Sci. 955 2002 119 138
62. C. Foca, E.K. Moses, M.A. Quinn, and G.E. Rice Differential expression of the α2-macroglobulin receptor and the receptor associated protein in normal human endometrium and endometrial carcinoma Mol. Hum. Reprod. 6 2000 921 927
63. 2- macroglobulin receptor in invasive cell clones derived from human prostate and breast tumor cells Oncol. Res. 6 1994 365 372
64. 2-macroglobulin receptor and its receptor-associated protein in lates stages of cutaneous melanocytic tumor progression Cancer Res. 56 1996 1432 1439
65. A.M. Weaver, I.M. Hussaini, A. Mazar, J. Henkin, and S.L. Gonias Embryonic fibroblasts that are genetically deficient in low density lipoprotein receptor-related protein demonstrate increased activity of the urokinase receptor system and accelerated migration on vitronectin J. Biol. Chem. 272 1997 14372 14379
66. D.J. Webb, D.H.D. Nguyen, and S.L. Gonias Extracellular signal-regulated kinase functions in the urokinase receptor-dependent pathway by which neutralization of low density lipoprotein receptor-related protein promotes fibrosarcoma cell migration and matrigel invasion J. Cell Sci. 113 2000 123 134
67. M. Seiki Membrane-type 1 matrix metalloproteinase: a key enzyme for tumor invasion Cancer Lett. 194 2003 1 11
68. D.V. Rozanov, E. Hahn-Dantona, D.K. Strickland, and A.Y. Strongin The low density lipoprotein receptor-related protein LRP is regulated by membrane type-1 matrix metalloproteinase (MT1-MMP) proteolysis in malignant cells J. Biol. Chem. 279 2004 4260 4268
69. P.L. Tran, J.P. Vigneron, D. Pericat, S. Dubois, D. Cazals, M. Hervy, Y.A. DeClerck, C. Degott, and C. Auclair Gene therapy for hepatocellular carcinoma using non-viral vectors composed of bis guanidinium-tren-cholesterol and plasmids encoding the tissue inhibitors of metalloproteinases TIMP-2 and TIMP-3 Cancer Gene Ther. 10 2003 435 444
70. Y. Jiang, I.D. Goldberg, and Y.E. Shi Complex roles of tissue inhibitors of metalloproteinases in cancer Oncogene 21 2002 2245 2252
71. D.J. Grignon, W. Sakr, M. Toth, V. Ravery, J. Angulo, F. Shamsa, J.E. Pontes, J.C. Crissman, and R. Fridman High levels of tissue inhibitor of metalloproteinase-2 (TIMP-2) expression are asociated with poor outcome in invasive bladder cancer Cancer Res. 56 1996 1654 1659
72. H. Gakiopoulou, L. Nakopoulou, A. Siatelis, I. Mavrommatis, E.G. Panayotopoulou, I. Tsirmpa, C. Stravodimos, and A. Giannopoulos Tissue inhibitor of metalloproteinase-2 as a multifunctional molecule of which the expression is associated with adverse prognosis of patients with urothelial bladder carcinomas Clin. Cancer Res. 15 2003 5573 5581