Matrix metalloproteinases in inflammation

Biochimica et Biophysica Acta - General Subjects

Volumn 1840, Issue 8, 2014, Pages 2571-2580

  Nissinen, Liisa ^a   Kähäri, Veli Matti ^a  

^a UNIVERSITY OF TURKU   (Finland)

Author keywords

Cancer; Inflammation; Matrix; Proteinase; Signaling

Indexed keywords

CHEMOKINE; COLLAGENASE 3; GELATINASE A; GELATINASE B; GROWTH FACTOR; INTERSTITIAL COLLAGENASE; MACROPHAGE ELASTASE; MATRILYSIN; MATRIX METALLOPROTEINASE; MATRIX METALLOPROTEINASE 14; MATRIX METALLOPROTEINASE 16; MATRIX METALLOPROTEINASE 17; MATRIX METALLOPROTEINASE 19; MATRIX METALLOPROTEINASE 24; MATRIX METALLOPROTEINASE 26; MATRIX METALLOPROTEINASE 28; NEUTROPHIL COLLAGENASE; STROMELYSIN; STROMELYSIN 2; STROMELYSIN 3; UNCLASSIFIED DRUG;

ARTICLE; BIOAVAILABILITY; CANCER GROWTH; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME STRUCTURE; ENZYME SUBSTRATE COMPLEX; HUMAN; INFLAMMATION; NONHUMAN; PERMEABILITY BARRIER; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; TISSUE INJURY; TUMOR ESCAPE; TUMOR MICROENVIRONMENT;

EID: 84942818262     PISSN: 03044165     EISSN: 18728006     Source Type: Journal    
DOI: 10.1016/j.bbagen.2014.03.007Review     Document Type: Article

References (136)

1. M.D. Sternlicht, and Z. Werb How matrix metalloproteinases regulate cell behavior Annu. Rev. Cell Dev. Biol. 17 2001 463 516
2. M. Toriseva, and V.M. Kähäri Proteinases in cutaneous wound healing Cell. Mol. Life Sci. 66 2009 203 224
3. P.S. Burrage, K.S. Mix, and C.E. Brinckerhoff Matrix metalloproteinases: role in arthritis Front. Biosci. 11 2006 529 543
4. K. Kessenbrock, V. Plaks, and Z. Werb Matrix metalloproteinases: regulators of the tumor microenvironment Cell 141 2010 52 67
5. W.C. Parks, C.W. Wilson, and Y.S. Lopez-Boado Matrix metalloproteinases as modulators of inflammation and innate immunity Nat. Rev. Immunol. 4 2004 617 629
6. G.S. Butler, and C.M. Overall Matrix metalloproteinase processing of signaling molecules to regulate inflammation Periodontol. 2000 63 2013 123 148
7. F.X. Gomis-Rüth Structural aspects of the metzincin clan of metalloendopeptidases Mol. Biotechnol. 24 2003 157 202
8. T. Klein, and R. Bischoff Physiology and pathophysiology of matrix metalloproteases Amino Acids 41 2011 271 290
9. K.A. Hasty, T.F. Pourmotabbed, G.I. Goldberg, J.P. Thompson, D.G. Spinella, R.M. Stevens, and C.L. Mainardi Human neutrophil collagenase. A distinct gene product with homology to other matrix metalloproteinases J. Biol. Chem. 265 1990 11421 11424
10. N.D. Marchenko, G.N. Marchenko, and A.Y. Strongin Unconventional activation mechanisms of MMP-26, a human matrix metalloproteinase with a unique PHCGXXD cysteine-switch motif J. Biol. Chem. 277 2002 18967 18972
11. R. Lang, M. Braun, N.E. Sounni, A. Noel, F. Frankenne, J.M. Foidart, W. Bode, and K. Maskos Crystal structure of the catalytic domain of MMP-16/MT3-MMP: characterization of MT-MMP specific features J. Mol. Biol. 336 2004 213 225
12. A. Sohail, Q. Sun, H. Zhao, M.M. Bernardo, J.A. Cho, and R. Fridman MT4-(MMP17) and MT6-MMP (MMP25), a unique set of membrane-anchored matrix metalloproteinases: properties and expression in cancer Cancer Metastasis Rev. 27 2008 289 302
13. U. Benbow, and C.E. Brinckerhoff The AP-1 site and MMP gene regulation: what is all the fuss about? Matrix Biol. 15 1997 519 526
14. R. Ala-aho, and V.M. Kähäri Collagenases in cancer Biochimie 87 2005 273 286
15. N. Reunanen, S.P. Li, M. Ahonen, M. Foschi, J. Han, and V.M. Kähäri Activation of p38α MAPK enhances collagenase-1 (matrix metalloproteinase (MMP)-1) and stromelysin-1 (MMP-3) expression by mRNA stabilization J. Biol. Chem. 277 2002 32360 32368
16. C.M. Overall, J.L. Wrana, and J. Sodek Transcriptional and post-transcriptional regulation of 72-kDa gelatinase/type IV collagenase by transforming growth factor-β1 in human fibroblasts. Comparisons with collagenase and tissue inhibitor of matrix metalloproteinase gene expression J. Biol. Chem. 266 1991 14064 14071
17. A.V. Chernov, and A.Y. Strongin Epigenetic regulation of matrix metalloproteinases and their collagen substrates in cancer Biomol. Concepts 2 2011 135 147
18. X. Fu, S.Y. Kassim, W.C. Parks, and J.W. Heinecke Hypochlorous acid generated by myeloperoxidase modifies adjacent tryptophan and glycine residues in the catalytic domain of matrix metalloproteinase-7 (matrilysin): an oxidative mechanism for restraining proteolytic activity during inflammation J. Biol. Chem. 278 2003 28403 28409
19. I. Yana, and S.J. Weiss Regulation of membrane type-1 matrix metalloproteinase activation by proprotein convertases Mol. Biol. Cell 11 2000 2387 2401
20. A.H. Baker, D.R. Edwards, and G. Murphy Metalloproteinase inhibitors: biological actions and therapeutic opportunities J. Cell Sci. 115 2002 3719 3727
21. T. Shimada, H. Nakamura, E. Ohuchi, Y. Fujii, Y. Murakami, H. Sato, M. Seiki, and Y. Okada Characterization of a truncated recombinant form of human membrane type 3 matrix metalloproteinase Eur. J. Biochem. 262 1999 907 914
22. H. Will, S.J. Atkinson, G.S. Butler, B. Smith, and G. Murphy The soluble catalytic domain of membrane type 1 matrix metalloproteinase cleaves the propeptide of progelatinase A and initiates autoproteolytic activation. Regulation by TIMP-2 and TIMP-3 J. Biol. Chem. 271 1996 17119 17123
23. K. Holmbeck, P. Bianco, J. Caterina, S. Yamada, M. Kromer, S.A. Kuznetsov, M. Mankani, P.G. Robey, A.R. Poole, I. Pidoux, J.M. Ward, and H. Birkedal-Hansen MT1-MMP-deficient mice develop dwarfism, osteopenia, arthritis, and connective tissue disease due to inadequate collagen turnover Cell 99 1999 81 92
24. A. Ducharme, S. Frantz, M. Aikawa, E. Rabkin, M. Lindsey, L.E. Rohde, F.J. Schoen, R.A. Kelly, Z. Werb, P. Libby, and R.T. Lee Targeted deletion of matrix metalloproteinase-9 attenuates left ventricular enlargement and collagen accumulation after experimental myocardial infarction J. Clin. Invest. 106 2000 55 62
25. M. Asahi, X. Wang, T. Mori, T. Sumii, J.C. Jung, M.A. Moskowitz, M.E. Fini, and E.H. Lo Effects of matrix metalloproteinase-9 gene knock-out on the proteolysis of blood-brain barrier and white matter components after cerebral ischemia J. Neurosci. 21 2001 7724 7732
26. K.Y. Vermaelen, D. Cataldo, K. Tournoy, T. Maes, A. Dhulst, R. Louis, J.M. Foidart, A. Noël, and R. Pauwels Matrix metalloproteinase-9-mediated dendritic cell recruitment into the airways is a critical step in a mouse model of asthma J. Immunol. 171 2003 1016 1022
27. B. Dubois, S. Masure, U. Hurtenbach, L. Paemen, H. Heremans, J. van den Oord, R. Sciot, T. Meinhardt, G. Hämmerling, G. Opdenakker, and B. Arnold Resistance of young gelatinase B-deficient mice to experimental autoimmune encephalomyelitis and necrotizing tail lesions J. Clin. Invest. 104 1999 1507 1515
28. D. Graesser, S. Mahooti, and J.A. Madri Distinct roles for matrix metalloproteinase-2 and α4 integrin in autoimmune T cell extravasation and residency in brain parenchyma during experimental autoimmune encephalomyelitis J. Neuroimmunol. 109 2000 121 131
29. B.C. Kieseier, R. Kiefer, J.M. Clements, K. Miller, G.M. Wells, T. Schweitzer, A.J. Gearing, and H.P. Hartung Matrix metalloproteinase-9 and -7 are regulated in experimental autoimmune encephalomyelitis Brain 121 Pt 1 1998 159 166
30. P.T. Nygårdas, and A.E. Hinkkanen Up-regulation of MMP-8 and MMP-9 activity in the BALB/c mouse spinal cord correlates with the severity of experimental autoimmune encephalomyelitis Clin. Exp. Immunol. 128 2002 245 254
31. D.G. Morris, X. Huang, N. Kaminski, Y. Wang, S.D. Shapiro, G. Dolganov, A. Glick, and D. Sheppard Loss of integrin αvβ6-mediated TGF-β activation causes MMP12-dependent emphysema Nature 422 2003 169 173
32. M. Wang, X. Qin, J.S. Mudgett, T.A. Ferguson, R.M. Senior, and H.G. Welgus Matrix metalloproteinase deficiencies affect contact hypersensitivity: stromelysin-1 deficiency prevents the response and gelatinase B deficiency prolongs the response Proc. Natl. Acad. Sci. U. S. A. 96 1999 6885 6889
33. B. Lelongt, S. Bengatta, M. Delauche, L.R. Lund, Z. Werb, and P.M. Ronco Matrix metalloproteinase 9 protects mice from anti-glomerular basement membrane nephritis through its fibrinolytic activity J. Exp. Med. 193 2001 793 802
34. M. Balbín, A. Fueyo, A.M. Tester, A.M. Pendás, A.S. Pitiot, A. Astudillo, C.M. Overall, S.D. Shapiro, and C. López-Otín Loss of collagenase-2 confers increased skin tumor susceptibility to male mice Nat. Genet. 35 2003 252 257
35. C.A. Owen, Z. Hu, C. Lopez-Otin, and S.D. Shapiro Membrane-bound matrix metalloproteinase-8 on activated polymorphonuclear cells is a potent, tissue inhibitor of metalloproteinase-resistant collagenase and serpinase J. Immunol. 172 2004 7791 7803
36. Y. Yoshihara, H. Nakamura, K. Obata, H. Yamada, T. Hayakawa, K. Fujikawa, and Y. Okada Matrix metalloproteinases and tissue inhibitors of metalloproteinases in synovial fluids from patients with rheumatoid arthritis or osteoarthritis Ann. Rheum. Dis. 59 2000 455 461
37. K. Joronen, R. Ala-aho, M.L. Majuri, H. Alenius, V.M. Kähäri, and E. Vuorio Adenovirus mediated intra-articular expression of collagenase-3 (MMP-13) induces inflammatory arthritis in mice Ann. Rheum. Dis. 63 2004 656 664
38. K. Joronen, V.M. Kähäri, and E. Vuorio Temporospatial expression of matrix metalloproteinases and tissue inhibitors of matrix metalloproteinases in mouse antigen-induced arthritis Histochem. Cell Biol. 124 2005 535 545
39. R.E. Vandenbroucke, E. Dejonckheere, F. Van Hauwermeiren, S. Lodens, R. De Rycke, E. Van Wonterghem, A. Staes, K. Gevaert, C. López-Otin, and C. Libert Matrix metalloproteinase 13 modulates intestinal epithelial barrier integrity in inflammatory diseases by activating TNF EMBO Mol. Med. 5 2013 932 948
40. M. Vaalamo, M.L. Karjalainen-Lindsberg, P. Puolakkainen, J. Kere, and U. Saarialho-Kere Distinct expression profiles of stromelysin-2 (MMP-10), collagenase-3 (MMP-13), macrophage metalloelastase (MMP-12), and tissue inhibitor of metalloproteinases-3 (TIMP-3) in intestinal ulcerations Am. J. Pathol. 152 1998 1005 1014
41. J.K. McGuire, Q. Li, and W.C. Parks Matrilysin (matrix metalloproteinase-7) mediates E-cadherin ectodomain shedding in injured lung epithelium Am. J. Pathol. 162 2003 1831 1843
42. S.E. Dunsmore, U.K. Saarialho-Kere, J.D. Roby, C.L. Wilson, L.M. Matrisian, H.G. Welgus, and W.C. Parks Matrilysin expression and function in airway epithelium J. Clin. Invest. 102 1998 1321 1331
43. B.K. Pilcher, J.A. Dumin, B.D. Sudbeck, S.M. Krane, H.G. Welgus, and W.C. Parks The activity of collagenase-1 is required for keratinocyte migration on a type I collagen matrix J. Cell Biol. 137 1997 1445 1457
44. K.M. Bullard, L. Lund, J.S. Mudgett, T.N. Mellin, T.K. Hunt, B. Murphy, J. Ronan, Z. Werb, and M.J. Banda Impaired wound contraction in stromelysin-1-deficient mice Ann. Surg. 230 1999 260 265
45. M. Toriseva, M. Laato, O. Carpén, S.T. Ruohonen, E. Savontaus, M. Inada, S.M. Krane, and V.M. Kähäri MMP-13 regulates growth of wound granulation tissue and modulates gene expression signatures involved in inflammation, proteolysis, and cell viability PLoS One 7 2012 e42596
46. S.A. Eming, T. Krieg, and J.M. Davidson Inflammation in wound repair: molecular and cellular mechanisms J. Invest. Dermatol. 127 2007 514 525
47. A. Gutiérrez-Fernández, M. Inada, M. Balbín, A. Fueyo, A.S. Pitiot, A. Astudillo, K. Hirose, M. Hirata, S.D. Shapiro, A. Noël, Z. Werb, S.M. Krane, C. López-Otín, and X.S. Puente Increased inflammation delays wound healing in mice deficient in collagenase-2 (MMP-8) FASEB J. 21 2007 2580 2591
48. M. Vaalamo, L. Mattila, N. Johansson, A.L. Kariniemi, M.L. Karjalainen-Lindsberg, V.M. Kähäri, and U. Saarialho-Kere Distinct populations of stromal cells express collagenase-3 (MMP-13) and collagenase-1 (MMP-1) in chronic ulcers but not in normally healing wounds J. Invest. Dermatol. 109 1997 96 101
49. A. Reijerkerk, G. Kooij, S.M. van der Pol, S. Khazen, C.D. Dijkstra, and H.E. de Vries Diapedesis of monocytes is associated with MMP-mediated occludin disappearance in brain endothelial cells FASEB J. 20 2006 2550 2552
50. D.Y. Lu, W.H. Yu, W.L. Yeh, C.H. Tang, Y.M. Leung, K.L. Wong, Y.F. Chen, C.H. Lai, and W.M. Fu Hypoxia-induced matrix metalloproteinase-13 expression in astrocytes enhances permeability of brain endothelial cells J. Cell. Physiol. 220 2009 163 173
51. Y. Ichikawa, T. Ishikawa, N. Momiyama, M. Kamiyama, H. Sakurada, R. Matsuyama, S. Hasegawa, T. Chishima, Y. Hamaguchi, S. Fujii, S. Saito, K. Kubota, H. Ike, S. Oki, and H. Shimada Matrilysin (MMP-7) degrades VE-cadherin and accelerates accumulation of β-catenin in the nucleus of human umbilical vein endothelial cells Oncol. Rep. 15 2006 311 315
52. Z. Liu, X. Zhou, S.D. Shapiro, J.M. Shipley, S.S. Twining, L.A. Diaz, R.M. Senior, and Z. Werb The serpin α1-proteinase inhibitor is a critical substrate for gelatinase B/MMP-9 in vivo Cell 102 2000 647 655
53. Z. Liu, N. Li, L.A. Diaz, M. Shipley, R.M. Senior, and Z. Werb Synergy between a plasminogen cascade and MMP-9 in autoimmune disease J. Clin. Invest. 115 2005 879 887
54. P.E. Van Den Steen, A. Wuyts, S.J. Husson, P. Proost, J. Van Damme, and G. Opdenakker Gelatinase B/MMP-9 and neutrophil collagenase/MMP-8 process the chemokines human GCP-2/CXCL6, ENA-78/CXCL5 and mouse GCP-2/LIX and modulate their physiological activities Eur. J. Biochem. 270 2003 3739 3749
55. U. Schönbeck, F. Mach, and P. Libby Generation of biologically active IL-1β by matrix metalloproteinases: a novel caspase-1-independent pathway of IL-1β processing J. Immunol. 161 1998 3340 3346
56. G.A. McQuibban, J.H. Gong, E.M. Tam, C.A. McCulloch, I. Clark-Lewis, and C.M. Overall Inflammation dampened by gelatinase A cleavage of monocyte chemoattractant protein-3 Science 289 2000 1202 1206
57. G.A. McQuibban, G.S. Butler, J.H. Gong, L. Bendall, C. Power, I. Clark-Lewis, and C.M. Overall Matrix metalloproteinase activity inactivates the CXC chemokine stromal cell-derived factor-1 J. Biol. Chem. 276 2001 43503 43508
58. G.A. McQuibban, J.H. Gong, J.P. Wong, J.L. Wallace, I. Clark-Lewis, and C.M. Overall Matrix metalloproteinase processing of monocyte chemoattractant proteins generates CC chemokine receptor antagonists with anti-inflammatory properties in vivo Blood 100 2002 1160 1167
59. H. Haro, H.C. Crawford, B. Fingleton, K. Shinomiya, D.M. Spengler, and L.M. Matrisian Matrix metalloproteinase-7-dependent release of tumor necrosis factor-α in a model of herniated disc resorption J. Clin. Invest. 105 2000 143 150
60. L.J. McCawley, and L.M. Matrisian Matrix metalloproteinases: they're not just for matrix anymore! Curr. Opin. Cell Biol. 13 2001 534 540
61. A. Ito, A. Mukaiyama, Y. Itoh, H. Nagase, I.B. Thogersen, J.J. Enghild, Y. Sasaguri, and Y. Mori Degradation of interleukin 1β by matrix metalloproteinases J. Biol. Chem. 271 1996 14657 14660
62. Q. Li, P.W. Park, C.L. Wilson, and W.C. Parks Matrilysin shedding of syndecan-1 regulates chemokine mobilization and transepithelial efflux of neutrophils in acute lung injury Cell 111 2002 635 646
63. D.B. Corry, A. Kiss, L.Z. Song, L. Song, J. Xu, S.H. Lee, Z. Werb, and F. Kheradmand Overlapping and independent contributions of MMP2 and MMP9 to lung allergic inflammatory cell egression through decreased CC chemokines FASEB J. 18 2004 995 997
64. D.B. Corry, K. Rishi, J. Kanellis, A. Kiss, L.Z. Song Lz, J. Xu, L. Feng, Z. Werb, and F. Kheradmand Decreased allergic lung inflammatory cell egression and increased susceptibility to asphyxiation in MMP2-deficiency Nat. Immunol. 3 2002 347 353
65. P.E. Van den Steen, P. Proost, A. Wuyts, J. Van Damme, and G. Opdenakker Neutrophil gelatinase B potentiates interleukin-8 tenfold by aminoterminal processing, whereas it degrades CTAP-III, PF-4, and GRO-α and leaves RANTES and MCP-2 intact Blood 96 2000 2673 2681
66. P. Van Lint, B. Wielockx, L. Puimège, A. Noël, C. López-Otin, and C. Libert Resistance of collagenase-2 (matrix metalloproteinase-8)-deficient mice to TNF-induced lethal hepatitis J. Immunol. 175 2005 7642 7649
67. L.M. Coussens, and Z. Werb Inflammatory cells and cancer: think different! J. Exp. Med. 193 2001 F23 F26
68. A. Mantovani, P. Allavena, A. Sica, and F. Balkwill Cancer-related inflammation Nature 454 2008 436 444
69. R. Masson, O. Lefebvre, A. Noël, M.E. Fahime, M.P. Chenard, C. Wendling, F. Kebers, M. LeMeur, A. Dierich, J.M. Foidart, P. Basset, and M.C. Rio In vivo evidence that the stromelysin-3 metalloproteinase contributes in a paracrine manner to epithelial cell malignancy J. Cell Biol. 140 1998 1535 1541
70. L.M. Coussens, C.L. Tinkle, D. Hanahan, and Z. Werb MMP-9 supplied by bone marrow-derived cells contributes to skin carcinogenesis Cell 103 2000 481 490
71. P. Allavena, C. Garlanda, M.G. Borrello, A. Sica, and A. Mantovani Pathways connecting inflammation and cancer Curr. Opin. Genet. Dev. 18 2008 3 10
72. J.L. Luo, S. Maeda, L.C. Hsu, H. Yagita, and M. Karin Inhibition of NF-kappaB in cancer cells converts inflammation- induced tumor growth mediated by TNFα to TRAIL-mediated tumor regression Cancer Cell 6 2004 297 305
73. A.M. Manicone, and J.K. McGuire Matrix metalloproteinases as modulators of inflammation Semin. Cell Dev. Biol. 19 2008 34 41
74. J.M. Burns, B.C. Summers, Y. Wang, A. Melikian, R. Berahovich, Z. Miao, M.E. Penfold, M.J. Sunshine, D.R. Littman, C.J. Kuo, K. Wei, B.E. McMaster, K. Wright, M.C. Howard, and T.J. Schall A novel chemokine receptor for SDF-1 and I-TAC involved in cell survival, cell adhesion, and tumor development J. Exp. Med. 203 2006 2201 2213
75. S. Struyf, P. Proost, J. Vandercappellen, S. Dempe, B. Noyens, S. Nelissen, M. Gouwy, M. Locati, G. Opdenakker, C. Dinsart, and J. Van Damme Synergistic up-regulation of MCP-2/CCL8 activity is counteracted by chemokine cleavage, limiting its inflammatory and anti-tumoral effects Eur. J. Immunol. 39 2009 843 857
76. A. Müller, B. Homey, H. Soto, N. Ge, D. Catron, M.E. Buchanan, T. McClanahan, E. Murphy, W. Yuan, S.N. Wagner, J.L. Barrera, A. Mohar, E. Verástegui, and A. Zlotnik Involvement of chemokine receptors in breast cancer metastasis Nature 410 2001 50 56
77. M. Egeblad, and Z. Werb New functions for the matrix metalloproteinases in cancer progression Nat. Rev. Cancer 2 2002 161 174
78. N.M. Weathington, A.H. van Houwelingen, B.D. Noerager, P.L. Jackson, A.D. Kraneveld, F.S. Galin, G. Folkerts, F.P. Nijkamp, and J.E. Blalock A novel peptide CXCR ligand derived from extracellular matrix degradation during airway inflammation Nat. Med. 12 2006 317 323
79. A.M. Houghton, P.A. Quintero, D.L. Perkins, D.K. Kobayashi, D.G. Kelley, L.A. Marconcini, R.P. Mecham, R.M. Senior, and S.D. Shapiro Elastin fragments drive disease progression in a murine model of emphysema J. Clin. Invest. 116 2006 753 759
80. B.C. Sheu, S.M. Hsu, H.N. Ho, H.C. Lien, S.C. Huang, and R.H. Lin A novel role of metalloproteinase in cancer-mediated immunosuppression Cancer Res. 61 2001 237 242
81. H. Kataoka, H. Uchino, T. Iwamura, M. Seiki, K. Nabeshima, and M. Koono Enhanced tumor growth and invasiveness in vivo by a carboxyl-terminal fragment of α1-proteinase inhibitor generated by matrix metalloproteinases: a possible modulatory role in natural killer cytotoxicity Am. J. Pathol. 154 1999 457 468
82. K.E. de Visser, A. Eichten, and L.M. Coussens Paradoxical roles of the immune system during cancer development Nat. Rev. Cancer 6 2006 24 37
83. R. Ala-aho, M. Ahonen, S.J. George, J. Heikkilä, R. Grénman, M. Kallajoki, and V.M. Kähäri Targeted inhibition of human collagenase-3 (MMP-13) expression inhibits squamous cell carcinoma growth in vivo Oncogene 23 2004 5111 5123
84. A. Dufour, and C.M. Overall Missing the target: matrix metalloproteinase antitargets in inflammation and cancer Trends Pharmacol. Sci. 34 2013 233 242
85. P. Vihinen, R. Ala-aho, and V.M. Kähäri Matrix metalloproteinases as therapeutic targets in cancer Curr. Cancer Drug Targets 5 2005 203 220
86. U. auf dem Keller, A. Prudova, U. Eckhard, B. Fingleton, and C.M. Overall Systems-level analysis of proteolytic events in increased vascular permeability and complement activation in skin inflammation Sci. Signal. 6 258 2013 rs2 10.1126/scisignal.2003512
87. R. Rajah, R.V. Nachajon, M.H. Collins, H. Hakonarson, M.M. Grunstein, and P. Cohen Elevated levels of the IGF-binding protein protease MMP-1 in asthmatic airway smooth muscle Am. J. Respir. Cell Mol. Biol. 20 1999 199 208
88. J.L. Fowlkes, J.J. Enghild, K. Suzuki, and H. Nagase Matrix metalloproteinases degrade insulin-like growth factor-binding protein-3 in dermal fibroblast cultures J. Biol. Chem. 269 1994 25742 25746
89. S. Lee, S.M. Jilani, G.V. Nikolova, D. Carpizo, and M.L. Iruela-Arispe Processing of VEGF-A by matrix metalloproteinases regulates bioavailability and vascular patterning in tumors J. Cell Biol. 169 2005 681 691
90. Q. Yu, and I. Stamenkovic Cell surface-localized matrix metalloproteinase-9 proteolytically activates TGF-β and promotes tumor invasion and angiogenesis Genes Dev. 14 2000 163 176
91. E. Levi, R. Fridman, H.Q. Miao, Y.S. Ma, A. Yayon, and I. Vlodavsky Matrix metalloproteinase 2 releases active soluble ectodomain of fibroblast growth factor receptor 1 Proc. Natl. Acad. Sci. U. S. A. 93 1996 7069 7074
92. R.A. Dean, G.S. Butler, Y. Hamma-Kourbali, J. Delbé, D.R. Brigstock, J. Courty, and C.M. Overall Identification of candidate angiogenic inhibitors processed by matrix metalloproteinase 2 (MMP-2) in cell-based proteomic screens: disruption of vascular endothelial growth factor (VEGF)/heparin affin regulatory peptide (pleiotrophin) and VEGF/Connective tissue growth factor angiogenic inhibitory complexes by MMP-2 proteolysis Mol. Cell. Biol. 27 2007 8454 8465
93. Z. Zhang, P.G. Winyard, K. Chidwick, G. Murphy, M. Wardell, R.W. Carrell, and D.R. Blake Proteolysis of human native and oxidised α1-proteinase inhibitor by matrilysin and stromelysin Biochim. Biophys. Acta 1199 1994 224 228
94. H.A. Coppock, A. White, J.D. Aplin, and M. Westwood Matrix metalloprotease-3 and -9 proteolyze insulin-like growth factor-binding protein-1 Biol. Reprod. 71 2004 438 443
95. S. Maeda, D.D. Dean, I. Gay, Z. Schwartz, and B.D. Boyan Activation of latent transforming growth factor β1 by stromelysin 1 in extracts of growth plate chondrocyte-derived matrix vesicles J. Bone Miner. Res. 16 2001 1281 1290
96. M. Suzuki, G. Raab, M.A. Moses, C.A. Fernandez, and M. Klagsbrun Matrix metalloproteinase-3 releases active heparin-binding EGF-like growth factor by cleavage at a specific juxtamembrane site J. Biol. Chem. 272 1997 31730 31737
97. R. Agnihotri, H.C. Crawford, H. Haro, L.M. Matrisian, M.C. Havrda, and L. Liaw Osteopontin, a novel substrate for matrix metalloproteinase-3 (stromelysin-1) and matrix metalloproteinase-7 (matrilysin) J. Biol. Chem. 276 2001 28261 28267
98. W.H. Yu, J.F. Woessner, J.D. McNeish, and I. Stamenkovic CD44 anchors the assembly of matrilysin/MMP-7 with heparin-binding epidermal growth factor precursor and ErbB4 and regulates female reproductive organ remodeling Genes Dev. 16 2002 307 323
99. A.K. Kivisaari, M. Kallajoki, R. Ala-aho, J.A. McGrath, J.W. Bauer, R. Königová, M. Medvecz, W. Beckert, R. Grénman, and V.M. Kähäri Matrix metalloproteinase-7 activates heparin-binding epidermal growth factor-like growth factor in cutaneous squamous cell carcinoma Br. J. Dermatol. 163 2010 726 735
100. W.C. Powell, B. Fingleton, C.L. Wilson, M. Boothby, and L.M. Matrisian The metalloproteinase matrilysin proteolytically generates active soluble Fas ligand and potentiates epithelial cell apoptosis Curr. Biol. 9 1999 1441 1447
101. N. Mitsiades, W.H. Yu, V. Poulaki, M. Tsokos, and I. Stamenkovic Matrix metalloproteinase-7-mediated cleavage of Fas ligand protects tumor cells from chemotherapeutic drug cytotoxicity Cancer Res. 61 2001 577 581
102. C.K. Li, S.L. Pender, K.M. Pickard, V. Chance, J.A. Holloway, A. Huett, N.S. Gonçalves, J.S. Mudgett, G. Dougan, G. Frankel, and T.T. MacDonald Impaired immunity to intestinal bacterial infection in stromelysin-1 (matrix metalloproteinase-3)-deficient mice J. Immunol. 173 2004 5171 5179
103. B. Holtz, P. Cuniasse, A. Boulay, R. Kannan, A. Mucha, F. Beau, P. Basset, and V. Dive Role of the S1′ subsite glutamine 215 in activity and specificity of stromelysin-3 by site-directed mutagenesis Biochemistry 38 1999 12174 12179
104. A. Churg, R.D. Wang, H. Tai, X. Wang, C. Xie, J. Dai, S.D. Shapiro, and J.L. Wright Macrophage metalloelastase mediates acute cigarette smoke-induced inflammation via tumor necrosis factor-α release Am. J. Respir. Crit. Care Med. 167 2003 1083 1089
105. M. D'Angelo, P.C. Billings, M. Pacifici, P.S. Leboy, and T. Kirsch Authentic matrix vesicles contain active metalloproteases (MMP). A role for matrix vesicle-associated MMP-13 in activation of transforming growth factor-β J. Biol. Chem. 276 2001 11347 11353
106. H.I. Park, B.E. Turk, F.E. Gerkema, L.C. Cantley, and Q.X. Sang Peptide substrate specificities and protein cleavage sites of human endometase/ matrilysin-2/matrix metalloproteinase-26 J. Biol. Chem. 277 2002 35168 35175
107. T. Itoh, H. Matsuda, M. Tanioka, K. Kuwabara, S. Itohara, and R. Suzuki The role of matrix metalloproteinase-2 and matrix metalloproteinase-9 in antibody-induced arthritis J. Immunol. 169 2002 2643 2647
108. J. Esparza, M. Kruse, J. Lee, M. Michaud, and J.A. Madri MMP-2 null mice exhibit an early onset and severe experimental autoimmune encephalomyelitis due to an increase in MMP-9 expression and activity FASEB J. 18 2004 1682 1691
109. P. Garg, M. Rojas, A. Ravi, K. Bockbrader, S. Epstein, M. Vijay-Kumar, A.T. Gewirtz, D. Merlin, and S.V. Sitaraman Selective ablation of matrix metalloproteinase-2 exacerbates experimental colitis: contrasting role of gelatinases in the pathogenesis of colitis J. Immunol. 177 2006 4103 4112
110. H. Matsusaka, M. Ikeuchi, S. Matsushima, T. Ide, T. Kubota, A.M. Feldman, A. Takeshita, K. Sunagawa, and H. Tsutsui Selective disruption of MMP-2 gene exacerbates myocardial inflammation and dysfunction in mice with cytokine-induced cardiomyopathy Am. J. Physiol. Heart Circ. Physiol. 289 2005 H1858 H1864
111. K.B. Deatrick, C.E. Luke, M.A. Elfline, V. Sood, J. Baldwin, G.R. Upchurch, F.A. Jaffer, T.W. Wakefield, and P.K. Henke The effect of matrix metalloproteinase 2 and matrix metalloproteinase 2/9 deletion in experimental post-thrombotic vein wall remodeling J. Vasc. Surg. 58 2013 1375 1384.e1372
112. J.S. Mudgett, N.I. Hutchinson, N.A. Chartrain, A.J. Forsyth, J. McDonnell, I.I. Singer, E.K. Bayne, J. Flanagan, D. Kawka, C.F. Shen, K. Stevens, H. Chen, M. Trumbauer, and D.M. Visco Susceptibility of stromelysin 1-deficient mice to collagen-induced arthritis and cartilage destruction Arthritis Rheum. 41 1998 110 121
113. R.L. Warner, L. Beltran, E.M. Younkin, C.S. Lewis, S.J. Weiss, J. Varani, and K.J. Johnson Role of stromelysin 1 and gelatinase B in experimental acute lung injury Am. J. Respir. Cell Mol. Biol. 24 2001 537 544
114. K.J. Gurney, E.Y. Estrada, and G.A. Rosenberg Blood-brain barrier disruption by stromelysin-1 facilitates neutrophil infiltration in neuroinflammation Neurobiol. Dis. 23 2006 87 96
115. C.M. Yamashita, L. Dolgonos, R.L. Zemans, S.K. Young, J. Robertson, N. Briones, T. Suzuki, M.N. Campbell, J. Gauldie, D.C. Radisky, D.W. Riches, G. Yu, N. Kaminski, C.A. McCulloch, and G.P. Downey Matrix metalloproteinase 3 is a mediator of pulmonary fibrosis Am. J. Pathol. 179 2011 1733 1745
116. S.A. Gharib, W.A. Altemeier, L.S. Van Winkle, C.G. Plopper, S.Y. Schlesinger, C.A. Buell, R. Brauer, V. Lee, W.C. Parks, and P. Chen Matrix metalloproteinase-7 coordinates airway epithelial injury response and differentiation of ciliated cells Am. J. Respir. Cell Mol. Biol. 48 2013 390 396
117. A.M. Tester, J.H. Cox, A.R. Connor, A.E. Starr, R.A. Dean, X.S. Puente, C. López-Otín, and C.M. Overall LPS responsiveness and neutrophil chemotaxis in vivo require PMN MMP-8 activity PLoS One 2 2007 e312
118. E. García-Prieto, A. González-López, S. Cabrera, A. Astudillo, A. Gutiérrez-Fernández, M. Fanjul-Fernandez, E. Batalla-Solís, X.S. Puente, A. Fueyo, C. López-Otín, and G.M. Albaiceta Resistance to bleomycin-induced lung fibrosis in MMP-8 deficient mice is mediated by interleukin-10 PLoS One 5 2010 e13242
119. S. García, J. Forteza, C. López-Otin, J.J. Gómez-Reino, A. González, and C. Conde Matrix metalloproteinase-8 deficiency increases joint inflammation and bone erosion in the K/BxN serum-transfer arthritis model Arthritis Res. Ther. 12 2010 R224
120. F.E. Castaneda, B. Walia, M. Vijay-Kumar, N.R. Patel, S. Roser, V.L. Kolachala, M. Rojas, L. Wang, G. Oprea, P. Garg, A.T. Gewirtz, J. Roman, D. Merlin, and S.V. Sitaraman Targeted deletion of metalloproteinase 9 attenuates experimental colitis in mice: central role of epithelial-derived MMP Gastroenterology 129 2005 1991 2008
121. A. Luttun, E. Lutgens, A. Manderveld, K. Maris, D. Collen, P. Carmeliet, and L. Moons Loss of matrix metalloproteinase-9 or matrix metalloproteinase-12 protects apolipoprotein E-deficient mice against atherosclerotic media destruction but differentially affects plaque growth Circulation 109 2004 1408 1414
122. Z. Liu, J.M. Shipley, T.H. Vu, X. Zhou, L.A. Diaz, Z. Werb, and R.M. Senior Gelatinase B-deficient mice are resistant to experimental bullous pemphigoid J. Exp. Med. 188 1998 475 482
123. S.J. McMillan, J. Kearley, J.D. Campbell, X.W. Zhu, K.Y. Larbi, J.M. Shipley, R.M. Senior, S. Nourshargh, and C.M. Lloyd Matrix metalloproteinase-9 deficiency results in enhanced allergen-induced airway inflammation J. Immunol. 172 2004 2586 2594
124. D.D. Cataldo, K.G. Tournoy, K. Vermaelen, C. Munaut, J.M. Foidart, R. Louis, A. Noël, and R.A. Pauwels Matrix metalloproteinase-9 deficiency impairs cellular infiltration and bronchial hyperresponsiveness during allergen-induced airway inflammation Am. J. Pathol. 161 2002 491 498
125. S. Lanone, T. Zheng, Z. Zhu, W. Liu, C.G. Lee, B. Ma, Q. Chen, R.J. Homer, J. Wang, L.A. Rabach, M.E. Rabach, J.M. Shipley, S.D. Shapiro, R.M. Senior, and J.A. Elias Overlapping and enzyme-specific contributions of matrix metalloproteinases-9 and -12 in IL-13-induced inflammation and remodeling J. Clin. Invest. 110 2002 463 474
126. H. Lukkarinen, A. Hogmalm, U. Lappalainen, and K. Bry Matrix metalloproteinase-9 deficiency worsens lung injury in a model of bronchopulmonary dysplasia Am. J. Respir. Cell Mol. Biol. 41 2009 59 68
127. W. Tian, and T.R. Kyriakides Matrix metalloproteinase-9 deficiency leads to prolonged foreign body response in the brain associated with increased IL-1β levels and leakage of the blood-brain barrier Matrix Biol. 28 2009 148 159
128. F.L. Koller, E.A. Dozier, K.T. Nam, M. Swee, T.P. Birkland, W.C. Parks, and B. Fingleton Lack of MMP10 exacerbates experimental colitis and promotes development of inflammation-associated colonic dysplasia Lab. Invest. 92 2012 1749 1759
129. R.L. Warner, C.S. Lewis, L. Beltran, E.M. Younkin, J. Varani, and K.J. Johnson The role of metalloelastase in immune complex-induced acute lung injury Am. J. Pathol. 158 2001 2139 2144
130. R.D. Hautamaki, D.K. Kobayashi, R.M. Senior, and S.D. Shapiro Requirement for macrophage elastase for cigarette smoke-induced emphysema in mice Science 277 1997 2002 2004
131. H. Uchinami, E. Seki, D.A. Brenner, and J. D'Armiento Loss of MMP 13 attenuates murine hepatic injury and fibrosis during cholestasis Hepatology 44 2006 420 429
132. W. Xiong, R. Knispel, J. MacTaggart, T.C. Greiner, S.J. Weiss, and B.T. Baxter Membrane-type 1 matrix metalloproteinase regulates macrophage-dependent elastolytic activity and aneurysm formation in vivo J. Biol. Chem. 284 2009 1765 1771
133. M.M. Gueders, S.J. Hirst, F. Quesada-Calvo, G. Paulissen, J. Hacha, C. Gilles, P. Gosset, R. Louis, J.M. Foidart, C. Lopez-Otin, A. Noël, and D.D. Cataldo Matrix metalloproteinase-19 deficiency promotes tenascin-C accumulation and allergen-induced airway inflammation Am. J. Respir. Cell Mol. Biol. 43 2010 286 295
134. A.R. Folgueras, T. Valdés-Sánchez, E. Llano, L. Menéndez, A. Baamonde, B.L. Denlinger, C. Belmonte, L. Juárez, A. Lastra, O. García-Suárez, A. Astudillo, M. Kirstein, A.M. Pendás, I. Fariñas, and C. López-Otín Metalloproteinase MT5-MMP is an essential modulator of neuro-immune interactions in thermal pain stimulation Proc. Natl. Acad. Sci. U. S. A. 106 2009 16451 16456
135. Y. Ma, G.V. Halade, J. Zhang, T.A. Ramirez, D. Levin, A. Voorhees, Y.F. Jin, H.C. Han, A.M. Manicone, and M.L. Lindsey Matrix metalloproteinase-28 deletion exacerbates cardiac dysfunction and rupture after myocardial infarction in mice by inhibiting M2 macrophage activation Circ. Res. 112 2013 675 688
136. A.M. Manicone, T.P. Birkland, M. Lin, T. Betsuyaku, N. van Rooijen, J. Lohi, J. Keski-Oja, Y. Wang, S.J. Skerrett, and W.C. Parks Epilysin (MMP-28) restrains early macrophage recruitment in Pseudomonas aeruginosa pneumonia J. Immunol. 182 2009 3866 3876