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(The FASEB Journal. 1998;12:1075-1095.)
© 1998 FASEB

Matrix metalloproteinases: structures, evolution, and diversification

Irina Massova1,a,1, Lakshmi P. Kotraa, Rafael Fridmanb and Shahriar Mobasherya,1

a Department of Chemistry, Wayne State University, Detroit, Michigan 48202–3489, USA
b Department of Pathology and Karmanos Cancer Institute, Wayne State University, Detroit, Michigan 48202–3489, USA

A comprehensive sequence alignment of 64 members of the family of matrix metalloproteinases (MMPs) for the entire sequences, and subsequently the catalytic and the hemopexin-like domains, have been performed. The 64 MMPs were selected from plants, invertebrates, and vertebrates. The analyses disclosed that as many as 23 distinct subfamilies of these proteins are known to exist. Information from the sequence alignments was correlated with structures, both crystallographic as well as computational, of the catalytic domains for the 23 representative members of the MMP family. A survey of the metal binding sites and two loops containing variable sequences of amino acids, which are important for substrate interactions, are discussed. The collective data support the proposal that the assembly of the domains into multidomain enzymes was likely to be an early evolutionary event. This was followed by diversification, perhaps in parallel among the MMPs, in a subsequent evolutionary time scale. Analysis indicates that a retrograde structure simplification may have accounted for the evolution of MMPs with simple domain constituents, such as matrilysin, from the larger and more elaborate enzymes.—Massova, I., Kotra, L. P., Fridman, R., Mobashery, S. Matrix metalloproteinases: structures, evolution, and diversification. FASEB J. 12, 1075–1095 (1998)


Key Words: extracellular matrix • MMP • hemopexin • tissue inhibitor of matrix metalloproteinase




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M. M. Bernardo, S. Brown, Z.-H. Li, R. Fridman, and S. Mobashery
Design, Synthesis, and Characterization of Potent, Slow-binding Inhibitors That Are Selective for Gelatinases
J. Biol. Chem., March 22, 2002; 277(13): 11201 - 11207.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
E. I. Deryugina, B. I. Ratnikov, T. I. Postnova, D. V. Rozanov, and A. Y. Strongin
Processing of Integrin alpha v Subunit by Membrane Type 1 Matrix Metalloproteinase Stimulates Migration of Breast Carcinoma Cells on Vitronectin and Enhances Tyrosine Phosphorylation of Focal Adhesion Kinase
J. Biol. Chem., March 15, 2002; 277(12): 9749 - 9756.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
D. V. Rozanov, B. Ghebrehiwet, T. I. Postnova, A. Eichinger, E. I. Deryugina, and A. Y. Strongin
The Hemopexin-like C-terminal Domain of Membrane Type 1 Matrix Metalloproteinase Regulates Proteolysis of a Multifunctional Protein, gC1qR
J. Biol. Chem., March 8, 2002; 277(11): 9318 - 9325.
[Abstract] [Full Text] [PDF]

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 J. Immunol.Home page
D. Min, A. G. Moore, M. A. Bain, S. N. Breit, and J. G. Lyons
Activation of Macrophage Promatrix Metalloproteinase-9 by Lipopolysaccharide-Associated Proteinases
J. Immunol., March 1, 2002; 168(5): 2449 - 2455.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
J. M. Mason, H.-P. Xu, S. K. Rao, A. Leask, M. Barcia, J. Shan, R. Stephenson, and S. Tabibzadeh
Lefty Contributes to the Remodeling of Extracellular Matrix by Inhibition of Connective Tissue Growth Factor and Collagen mRNA Expression and Increased Proteolytic Activity in a Fibrosarcoma Model
J. Biol. Chem., January 4, 2002; 277(1): 407 - 415.
[Abstract] [Full Text]

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 Cancer Res.Home page
S. Saad, D. J. Gottlieb, K. F. Bradstock, C. M. Overall, and L. J. Bendall
Cancer Cell-associated Fibronectin Induces Release of Matrix Metalloproteinase-2 from Normal Fibroblasts
Cancer Res., January 1, 2002; 62(1): 283 - 289.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
E. I. Deryugina, L. Soroceanu, and A. Y. Strongin
Up-Regulation of Vascular Endothelial Growth Factor by Membrane-type 1 Matrix Metalloproteinase Stimulates Human Glioma Xenograft Growth and Angiogenesis
Cancer Res., January 1, 2002; 62(2): 580 - 588.
[Abstract] [Full Text] [PDF]

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 Cell Growth Differ.Home page
H. Hayashita-Kinoh, H. Kinoh, A. Okada, K. Komori, Y. Itoh, T. Chiba, M. Kajita, I. Yana, and M. Seiki
Membrane-Type 5 Matrix Metalloproteinase Is Expressed in Differentiated Neurons and Regulates Axonal Growth
Cell Growth Differ., November 1, 2001; 12(11): 573 - 580.
[Abstract] [Full Text] [PDF]

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 FASEB J.Home page
K.-D. KRONCKE
Cysteine-Zn2+ complexes: unique molecular switches for inducible nitric oxide synthase-derived NO
FASEB J, November 1, 2001; 15(13): 2503 - 2507.
[Abstract] [Full Text] [PDF]

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 J. Immunol.Home page
Z. Ma, H. Qin, and E. N. Benveniste
Transcriptional Suppression of Matrix Metalloproteinase-9 Gene Expression by IFN-{gamma} and IFN-{beta}: Critical Role of STAT-1{alpha}
J. Immunol., November 1, 2001; 167(9): 5150 - 5159.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
A. Jiang, K. Lehti, X. Wang, S. J. Weiss, J. Keski-Oja, and D. Pei
Regulation of membrane-type matrix metalloproteinase 1 activity by dynamin-mediated endocytosis
PNAS, October 31, 2001; (2001) 241293698.
[Abstract] [Full Text] [PDF]

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 J. Pharmacol. Exp. Ther.Home page
S. Bellosta, M. Canavesi, E. Favari, L. Cominacini, G. Gaviraghi, R. Fumagalli, R. Paoletti, and F. Bernini
Lalsoacidipine Modulates the Secretion of Matrix Metalloproteinase-9 by Human Macrophages
J. Pharmacol. Exp. Ther., March 1, 2001; 296(3): 736 - 743.
[Abstract] [Full Text]

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 Am. J. Physiol. Renal Physiol.Home page
N. Obermuller, N. Morente, B. Kranzlin, N. Gretz, and R. Witzgall
A possible role for metalloproteinases in renal cyst development
Am J Physiol Renal Physiol, March 1, 2001; 280(3): F540 - F550.
[Abstract] [Full Text] [PDF]

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 FASEB J.Home page
A. FABER-ELMANN, V. GRABOVSKY, M. DAYAN, M. SELA, R. ALON, and E. MOZES
An altered peptide ligand inhibits the activities of matrix metalloproteinase-9 and phospholipase C, and inhibits T cell interactions with VCAM-1 induced in vivo by a myasthenogenic T cell epitope
FASEB J, January 1, 2001; 15(1): 187 - 194.
[Abstract] [Full Text] [PDF]

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 IOVSHome page
N. Di Girolamo, D. Wakefield, and M. T. Coroneo
Differential Expression of Matrix Metalloproteinases and Their Tissue Inhibitors at the Advancing Pterygium Head
Invest. Ophthalmol. Vis. Sci., December 1, 2000; 41(13): 4142 - 4149.
[Abstract] [Full Text]

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 Cancer Res.Home page
I. Ozaki, T. Mizuta, G. Zhao, H. Yotsumoto, T. Hara, S. Kajihara, A. Hisatomi, T. Sakai, and K. Yamamoto
Involvement of the Ets-1 Gene in Overexpression of Matrilysin in Human Hepatocellular Carcinoma
Cancer Res., November 1, 2000; 60(22): 6519 - 6525.
[Abstract] [Full Text]

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 JDRHome page
J. Catering, J. Shi, X. Sun, Q. Qian, S. Yamada, Y. Liu, S. Krakora, J.D. Bartlett, Y. Yamada, J.A. Engler, et al.
Cloning, Characterization, and Expression Analysis of Mouse Enamelysin
Journal of Dental Research, September 1, 2000; 79(9): 1697 - 1703.
[Abstract] [PDF]

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 GutHome page
B von Lampe, B Barthel, S E Coupland, E-O Riecken, and S Rosewicz
Differential expression of matrix metalloproteinases and their tissue inhibitors in colon mucosa of patients with inflammatory bowel disease
Gut, July 1, 2000; 47(1): 63 - 73.
[Abstract] [Full Text] [PDF]

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 IOVSHome page
A. Béliveau, M. Bérubé, A. Rousseau, G. Pelletier, and S. L. Guérin
Expression of Integrin {alpha}5{beta}1 and MMPs Associated with Epithelioid Morphology and Malignancy of Uveal Melanoma
Invest. Ophthalmol. Vis. Sci., July 1, 2000; 41(8): 2363 - 2372.
[Abstract] [Full Text]

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 Br. J. Ophthalmol.Home page
C S SETHI, T A BAILEY, P J LUTHERT, and N H V CHONG
Matrix metalloproteinase biology applied to vitreoretinal disorders
Br. J. Ophthalmol., June 1, 2000; 84(6): 654 - 666.
[Full Text]

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 J. Biol. Chem.Home page
S. Hernandez-Barrantes, M. Toth, M. M. Bernardo, M. Yurkova, D. C. Gervasi, Y. Raz, Q. A. Sang, and R. Fridman
Binding of Active (57 kDa) Membrane Type 1-Matrix Metalloproteinase (MT1-MMP) to Tissue Inhibitor of Metalloproteinase (TIMP)-2 Regulates MT1-MMP Processing and Pro-MMP-2 Activation
J. Biol. Chem., April 14, 2000; 275(16): 12080 - 12089.
[Abstract] [Full Text] [PDF]

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 J. Am. Soc. Nephrol.Home page
O. LENZ, S. J. ELLIOT, and W. G. STETLER-STEVENSON
Matrix Metalloproteinases in Renal Development and Disease
J. Am. Soc. Nephrol., March 1, 2000; 11(3): 574 - 581.
[Full Text] [PDF]

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 J. Biol. Chem.Home page
M. W. Olson, M. M. Bernardo, M. Pietila, D. C. Gervasi, M. Toth, L. P. Kotra, I. Massova, S. Mobashery, and R. Fridman
Characterization of the Monomeric and Dimeric Forms of Latent and Active Matrix Metalloproteinase-9. DIFFERENTIAL RATES FOR ACTIVATION BY STROMELYSIN 1
J. Biol. Chem., January 28, 2000; 275(4): 2661 - 2668.
[Abstract] [Full Text] [PDF]

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 CirculationHome page
J. Loscalzo
Vascular Matrix and Vein Graft Failure : Is the Message in the Medium?
Circulation, January 25, 2000; 101(3): 221 - 223.
[Full Text] [PDF]

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 DevelopmentHome page
A. Leontovich, J Zhang, K Shimokawa, H Nagase, and M. Sarras
A novel hydra matrix metalloproteinase (HMMP) functions in extracellular matrix degradation, morphogenesis and the maintenance of differentiated cells in the foot process
Development, January 2, 2000; 127(4): 907 - 920.
[Abstract] [PDF]

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 Cancer Res.Home page
S. Pasco, J. Han, P. Gillery, G. Bellon, F.-X. Maquart, J. P. Borel, N. A. Kefalides, and J. C. Monboisse
A Specific Sequence of the Noncollagenous Domain of the {{alpha}}3(IV) Chain of Type IV Collagen Inhibits Expression and Activation of Matrix Metalloproteinases by Tumor Cells
Cancer Res., January 1, 2000; 60(2): 467 - 473.
[Abstract] [Full Text]

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 J. Biol. Chem.Home page
J. M. Maidment, D. Moore, G. P. Murphy, G. Murphy, and I. M. Clark
Matrix Metalloproteinase Homologues from Arabidopsis thaliana. EXPRESSION AND ACTIVITY
J. Biol. Chem., December 3, 1999; 274(49): 34706 - 34710.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Renal Physiol.Home page
Y. S. Kanwar, K. Ota, Q. Yang, J. Wada, N. Kashihara, Y. Tian, and E. I. Wallner
Role of membrane-type matrix metalloproteinase 1 (MT-1-MMP), MMP-2, and its inhibitor in nephrogenesis
Am J Physiol Renal Physiol, December 1, 1999; 277(6): F934 - F947.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
Y. Wang, A. R. Johnson, Q.-Z. Ye, and R. D. Dyer
Catalytic Activities and Substrate Specificity of the Human Membrane Type 4 Matrix Metalloproteinase Catalytic Domain
J. Biol. Chem., November 12, 1999; 274(46): 33043 - 33049.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
C. M. Roberts, P. H. Tani, L. C. Bridges, Z. Laszik, and R. D. Bowditch
MDC-L, a Novel Metalloprotease Disintegrin Cysteine-rich Protein Family Member Expressed by Human Lymphocytes
J. Biol. Chem., October 8, 1999; 274(41): 29251 - 29259.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
L. L. Johnson, D. A. Bornemeier, J. A. Janowicz, J. Chen, A. G. Pavlovsky, and D. F. Ortwine
Effect of Species Differences on Stromelysin-1 (MMP-3) Inhibitor Potency. AN EXPLANATION OF INHIBITOR SELECTIVITY USING HOMOLOGY MODELING AND CHIMERIC PROTEINS
J. Biol. Chem., August 27, 1999; 274(35): 24881 - 24887.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
H. Nagase and J. F. Woessner Jr.
Matrix Metalloproteinases
J. Biol. Chem., July 30, 1999; 274(31): 21491 - 21494.
[Full Text] [PDF]

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 ScienceHome page
E. Morgunova, A. Tuuttila, U. Bergmann, M. Isupov, Y. Lindqvist, G. Schneider, and K. Tryggvason
Structure of Human Pro-Matrix Metalloproteinase-2: Activation Mechanism Revealed
Science, June 4, 1999; 284(5420): 1667 - 1670.
[Abstract] [Full Text]

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 J. Biol. Chem.Home page
D. Pei
Identification and Characterization of the Fifth Membrane-type Matrix Metalloproteinase MT5-MMP
J. Biol. Chem., March 26, 1999; 274(13): 8925 - 8932.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
Z. Zhang, J. K. Kolls, P. Oliver, D. Good, P. O. Schwarzenberger, M. S. Joshi, J. L. Ponthier, and J. R. Lancaster Jr.
Activation of Tumor Necrosis Factor-alpha -converting Enzyme-mediated Ectodomain Shedding by Nitric Oxide
J. Biol. Chem., May 19, 2000; 275(21): 15839 - 15844.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
W.-H. Yu, S.-s. C. Yu, Q. Meng, K. Brew, and J. F. Woessner Jr.
TIMP-3 Binds to Sulfated Glycosaminoglycans of the Extracellular Matrix
J. Biol. Chem., September 29, 2000; 275(40): 31226 - 31232.
[Abstract] [Full Text] [PDF]


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