Membrane type-matrix metalloproteinases and tumor progression

[en] Matrix metalloproteinases (MMPs) are a family of zinc endopeptidases that process growth factors, growth factor binding proteins, cell surface proteins, degrade extracellular matrix (ECM) components and thereby play a central role in tissue remodeling and tumor progression. Membrane-type matrix metalloproteinases (MT-MMPs) are a recently discovered subgroup of intrinsic plasma membrane proteins. Their functions have been extended from pericellular proteolysis and control of cell migration to cell signaling, control of cell proliferation and regulation of multiple stages of tumor progression including growth and angiogenesis. This review sheds light on the new functions of MT-MMPs and their inhibitors in tumor development and angiogenesis, and presents recent investigations that document their influence on various cell functions.

Disciplines :

Anatomy (cytology, histology, embryology...) & physiology

Author, co-author :

Sounni, Nor Eddine ; Université de Liège - ULiège > Département des sciences cliniques > Labo de biologie des tumeurs et du développement

Noël, Agnès ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie cellulaire et moléculaire appliquée à l'homme

Language :

English

Title :

Membrane type-matrix metalloproteinases and tumor progression

Publication date :

2005

Journal title :

Biochimie

ISSN :

0300-9084

eISSN :

1638-6183

Publisher :

Elsevier, Paris, France

Volume :

Pages :

329-342

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 21 December 2009

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163 (6 by ULiège)

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288 (2 by ULiège)

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Scopus citations^®

126

Scopus citations^®
without self-citations

112

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Bibliography

Engbring J.A., and Kleinman H.K. The basement membrane matrix in malignancy J. Pathol. 200 2003 465 470
Sternlicht M.D., and Werb Z. How matrix metalloproteinases regulate cell behavior Annu. Rev. Cell Dev. Biol. 17 2001 463 516
Zucker S., Pei D., Cao J., and Lopez-Otin C. Membrane type-matrix metalloproteinases (MT-MMP) Curr. Top. Dev. Biol. 54 2003 1 74
Egeblad M., and Werb Z. New functions for the matrix metalloproteinases in cancer progression Nat. Rev. Cancer 2 2002 161 174
Lopez-Otin C., and Overall C.M. Protease degradomics: a new challenge for proteomics Nat. Rev. Mol. Cell Biol. 3 2002 509 519
Noda M., Oh J., Takahashi R., Kondo S., Kitayama H., and Takahashi C. RECK: a novel suppressor of malignancy linking oncogenic signaling to extracellular matrix remodeling Cancer Metastasis Rev. 22 2003 167 175
Baker A.H., Edwards D.R., and Murphy G. Metalloproteinase inhibitors: biological actions and therapeutic opportunities J. Cell Sci. 115 2002 3719 3727
Bramhall S.R., Hallissey M.T., Whiting J., Scholefield J., Tierney G., Stuart R.C., Hawkins R.E., McCulloch P., Maughan T., Baillet P.D., Brown M., and Fielding J.W. Marimastat as maintenance therapy for patients with advanced gastric cancer: a randomised trial Br. J. Cancer 86 2002 1864 1870
Coussens L.M., Fingleton B., and Matrisian L.M. Matrix metalloproteinase inhibitors and cancer: trials and tribulations Science 295 2002 2387 2392
Overall C.M., and Lopez-Otin C. Strategies for MMP inhibition in cancer: innovations for the post-trial era Nat. Rev. Cancer 2 2002 657 672
Bergers G., Javaherian K., Lo K.M., Folkman J., and Hanahan D. Effects of angiogenesis inhibitors on multistage carcinogenesis in mice Science 284 1999 808 812
Black R.A. Tumor necrosis factor-alpha converting enzyme Int. J. Biochem. Cell Biol. 34 2002 1 5
Stamenkovic I. Extracellular matrix remodelling: the role of matrix metalloproteinases J. Pathol. 200 2003 448 464
Puente X.S., Sanchez L.M., Overall C.M., and Lopez-Otin C. Human and mouse proteases: a comparative genomic approach Nat. Rev. Genet. 4 2003 544 558
Bauvois B. Transmembrane proteases in cell growth and invasion: new contributors to angiogenesis? Oncogene 23 2004 317 329
Noel A., Maillard C., Rocks N., Jost M., Chabottaux V., Sounni N.E., Maquoi E., Cataldo D., and Foidart J.M. Membrane associated proteases and their inhibitors in tumour angiogenesis J. Clin. Pathol. 57 2004 577 584
Szabo R., Wu Q., Dickson R.B., Netzel-Arnett S., Antalis T.M., and Bugge T.H. Type II transmembrane serine proteases Thromb. Haemost. 90 2003 185 193
Bogenrieder T., and Herlyn M. Cell-surface proteolysis, growth factor activation and intercellular communication in the progression of melanoma Crit Rev. Oncol. Hematol. 44 2002 1 15
Keppler D., Sameni M., Moin K., Mikkelsen T., Diglio C.A., and Sloane B.F. Tumor progression and angiogenesis: cathepsin B & Co Biochem. Cell Biol. 74 1996 799 810
Kondoh K., Tsuji N., Kamagata C., Sasaki M., Kobayashi D., Yagihashi A., and Watanabe N. A novel aspartic protease gene, ALP56, is up-regulated in human breast cancer independently from the cathepsin D gene Breast Cancer Res. Treat. 78 2003 37 44
Sato H., Takino T., Okada Y., Cao J., Shinagawa A., Yamamoto E., and Seiki M. A matrix metalloproteinase expressed on the surface of invasive tumour cells Nature 370 1994 61 65 (see comments)
Pavlaki M., Cao J., Hymowitz M., Chen W.T., Bahou W., and Zucker S. A conserved sequence within the propeptide domain of membrane type 1:matrix metalloproteinase is critical for function as an intramolecular chaperone J. Biol. Chem. 277 2002 2740 2749
Pei D., and Weiss S.J. Transmembrane-deletion mutants of the membrane-type matrix metalloproteinase-1 process progelatinase A and express intrinsic matrix-degrading activity J. Biol. Chem. 271 1996 9135 9140
Hotary K., Allen E., Punturieri A., Yana I., and Weiss S.J. 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 2000 1309 1323
Yana I., and Weiss S.J. Regulation of membrane type-1 matrix metalloproteinase activation by proprotein convertases Mol. Biol. Cell 11 2000 2387 2401
Rozanov D.V., Deryugina E.I., Ratnikov B.I., Monosov E.Z., Marchenko G.N., Quigley J.P., and Strongin A.Y. Mutation analysis of membrane type-1 matrix metalloproteinase (MT1-MMP). The role of the cytoplasmic tail Cys(574), the active site Glu(240), and furin cleavage motifs in oligomerization, processing, and self-proteolysis of MT1-MMP expressed in breast carcinoma cells J. Biol. Chem. 276 2001 25705 25714
Sato H., Kinoshita T., Takino T., Nakayama K., and Seiki M. Activation of a recombinant membrane type 1-matrix metalloproteinase (MT1-MMP) by furin and its interaction with tissue inhibitor of metalloproteinases (TIMP)-2 FEBS Lett. 393 1996 101 104
Yana I., and Seiki M. MT-MMPs play pivotal roles in cancer dissemination Clin. Exp. Metastasis 19 2002 209 215
Cao J., Rehemtulla A., Bahou W., and Zucker S. Membrane type matrix metalloproteinase 1:activates pro-gelatinase A without furin cleavage of the N-terminal domain J. Biol. Chem. 271 1996 30174 30180
Okumura Y., Sato H., Seiki M., and Kido H. Proteolytic activation of the precursor of membrane type 1:matrix metalloproteinase by human plasmin. A possible cell surface activator FEBS Lett. 402 1997 181 184
Fernandez-Catalan C., Bode W., Huber R., Turk D., Calvete J.J., Lichte A., Tschesche H., and Maskos K. Crystal structure of the complex formed by the membrane type 1-matrix metalloproteinase with the tissue inhibitor of metalloproteinases-2, the soluble progelatinase A receptor EMBO J. 17 1998 5238 5248
Lang R., Braun M., Sounni N.E., Noel A., Frankenne F., Foidart J.M., Bode W., and Maskos K. Crystal structure of the catalytic domain of MMP-16/MT3-MMP: Characterization of MT-MMP specific features J. Mol. Biol. 336 2004 213 225
English W.R., Holtz B., Vogt G., Knauper V., and Murphy G. Characterization of the role of the "MT-loop": an eight-amino acid insertion specific to progelatinase A (MMP2) activating membrane-type matrix metalloproteinases J. Biol. Chem. 276 2001 42018 42026
Miyamori H., Takino T., Seiki M., and Sato H. Human membrane type-2 matrix metalloproteinase is defective in cell-associated activation of progelatinase A Biochem. Biophys. Res. Commun. 267 2000 796 800
Sounni N.E., Janssen M., Foidart J.M., and Noel A. Membrane type-1 matrix metalloproteinase and TIMP-2 in tumor angiogenesis Matrix Biol. 22 2003 55 61
Cataldo D.D., Gueders M.M., Rocks N., Sounni N.E., Evrard B., Bartsch P., Louis R., Noel A., and Foidart J.M. Pathogenic role of matrix metalloproteases and their inhibitors in asthma and chronic obstructive pulmonary disease and therapeutic relevance of matrix metalloproteases inhibitors Cell Mol. Biol. (Noisy. -le-grand) 49 2003 875 884
Itoh Y., Takamura A., Ito N., Maru Y., Sato H., Suenaga N., Aoki T., and Seiki M. Homophilic complex formation of MT1-MMP facilitates proMMP-2 activation on the cell surface and promotes tumor cell invasion EMBO J. 20 2001 4782 4793
Uekita T., Gotoh I., Kinoshita T., Itoh Y., Sato H., Shiomi T., Okada Y., and Seiki M. Membrane-type 1:matrix metalloproteinase cytoplasmic tail-binding protein-1 is a new member of the cupin superfamily: a possible multifunctional protein acting as an invasion suppressor down-regulated in tumors J. Biol. Chem. 279 2004 12734 12743
Wang X., Ma D., Keski-Oja J., and Pei D. Co-recycling of MT1-MMP and MT3-MMP through the trans-Golgi network. Identification of DKV582 as a recycling signal J. Biol. Chem. 279 2004 9331 9336
Sounni N.E., Roghi C., Chabottaux V., Janssen M., Munaut C., Maquoi E., Galvez B.G., Gilles C., Frankenne F., Murphy G., Foidart J.M., and Noel A. Up-regulation of vascular endothelial growth factor-a by active membrane-type 1:matrix metalloproteinase through activation of src-tyrosine kinases J. Biol. Chem. 279 2004 13564 13574
Gingras D., Bousquet-Gagnon N., Langlois S., Lachambre M.P., Annabi B., and Beliveau R. Activation of the extracellular signal-regulated protein kinase (ERK) cascade by membrane-type-1 matrix metalloproteinase (MT1-MMP) FEBS Lett. 507 2001 231 236
Ohuchi E., Imai K., Fujii Y., Sato H., Seiki M., and Okada Y. Membrane type 1:matrix metalloproteinase digests interstitial collagens and other extracellular matrix macromolecules J. Biol. Chem. 272 1997 2446 2451
Holmbeck K., Bianco P., Caterina J., Yamada S., Kromer M., Kuznetsov S.A., Mankani M., Robey P.G., Poole A.R., Pidoux I., Ward J.M., and Birkedal-Hansen H. MT1-MMP-deficient mice develop dwarfism, osteopenia, arthritis, and connective tissue disease due to inadequate collagen turnover Cell 99 1999 81 92
Holmbeck K., Bianco P., Chrysovergis K., Yamada S., and Birkedal-Hansen H. MT1-MMP-dependent, apoptotic remodeling of unmineralized cartilage: a critical process in skeletal growth J. Cell Biol. 163 2003 661 671
Yoshiyama Y., Sato H., Seiki M., Shinagawa A., Takahashi M., and Yamada T. Expression of the membrane-type 3:matrix metalloproteinase (MT3-MMP) in human brain tissues Acta Neuropathol. (Berl) 96 1998 347 350
Hiraoka N., Allen E., Apel I.J., Gyetko M.R., and Weiss S.J. Matrix metalloproteinases regulate neovascularization by acting as pericellular fibrinolysins Cell 95 1998 365 377
Hotary K.B., Yana I., Sabeh F., Li X.Y., Holmbeck K., Birkedal-Hansen H., Allen E.D., Hiraoka N., and Weiss S.J. Matrix metalloproteinases (MMPs) regulate fibrin-invasive activity via MT1-MMP-dependent and -independent processes J. Exp. Med. 195 2002 295 308
d'Ortho M.P., Will H., Atkinson S., Butler G., Messent A., Gavrilovic J., Smith B., Timpl R., Zardi L., and Murphy G. Membrane-type matrix metalloproteinases 1:and 2:exhibit broad-spectrum proteolytic capacities comparable to many matrix metalloproteinases Eur. J. Biochem. 250 1997 751 757
d'Ortho M.P., Stanton H., Butler M., Atkinson S.J., Murphy G., and Hembry R.M. MT1-MMP on the cell surface causes focal degradation of gelatin films FEBS Lett. 421 1998 159 164
Kang T., Yi J., Yang W., Wang X., Jiang A., and Pei D. Functional characterization of MT3-MMP in transfected MDCK cells: progelatinase A activation and tubulogenesis in 3-D collagen lattice FASEB J. 14 2000 2559 2568
Shimada T., Nakamura H., Ohuchi E., Fujii Y., Murakami Y., Sato H., Seiki M., and Okada Y. Characterization of a truncated recombinant form of human membrane type 3:matrix metalloproteinase Eur. J. Biochem. 262 1999 907 914
Endo K., Takino T., Miyamori H., Kinsen H., Yoshizaki T., Furukawa M., and Sato H. Cleavage of syndecan-1 by membrane type matrix metalloproteinase-1 stimulates cell migration J. Biol. Chem. 278 2003 40764 40770
Wang Y., Johnson A.R., Ye Q.Z., and Dyer R.D. Catalytic activities and substrate specificity of the human membrane type 4:matrix metalloproteinase catalytic domain J. Biol. Chem. 274 1999 33043 33049
English W.R., Puente X.S., Freije J.M., Knauper V., Amour A., Merryweather A., Lopez-Otin C., and Murphy G. Membrane type 4:matrix metalloproteinase (MMP17) has tumor necrosis factor-alpha convertase activity but does not activate pro-MMP2 J. Biol. Chem. 275 2000 14046 14055
Gao G., Plaas A., Thompson V.P., Jin S., Zuo F., and Sandy J.D. ADAMTS4 (aggrecanase-1) activation on the cell surface involves C-terminal cleavage by glycosylphosphatidyl inositol-anchored membrane type 4-matrix metalloproteinase and binding of the activated proteinase to chondroitin sulfate and heparan sulfate on syndecan-1 J. Biol. Chem. 279 2004 10042 10051
Llano E., Pendas A.M., Freije J.P., Nakano A., Knauper V., Murphy G., and Lopez-Otin C. Identification and characterization of human MT5-MMP, a new membrane-bound activator of progelatinase a overexpressed in brain tumors Cancer Res. 59 1999 2570 2576
Matsuda A., Itoh Y., Koshikawa N., Akizawa T., Yana I., and Seiki M. Clusterin, an abundant serum factor, is a possible negative regulator of MT6-MMP/MMP-25 produced by neutrophils J. Biol. Chem. 278 2003 36350 36357
Strongin A.Y., Collier I., Bannikov G., Marmer B.L., Grant G.A., and Goldberg G.I. Mechanism of cell surface activation of 72-kDa type IV collagenase. Isolation of the activated form of the membrane metalloprotease J. Biol. Chem. 270 1995 5331 5338
Seiki M. Membrane-type matrix metalloproteinases APMIS 107 1999 137 143
Seiki M., Koshikawa N., and Yana I. Role of pericellular proteolysis by membrane-type 1:matrix metalloproteinase in cancer invasion and angiogenesis Cancer Metastasis Rev. 22 2003 129 143
Wu Y.I., Munshi H.G., Sen R., Snipas S.J., Salvesen G.S., Fridman R., and Stack M.S. Glycosylation broadens the substrate profile of membrane type 1:matrix metalloproteinase J. Biol. Chem. 279 2004 8278 8289
Murphy G., Stanton H., Cowell S., Butler G., Knauper V., Atkinson S., and Gavrilovic J. Mechanisms for pro matrix metalloproteinase activation APMIS 107 1999 38 44
Atkinson S.J., Crabbe T., Cowell S., Ward R.V., Butler M.J., Sato H., Seiki M., Reynolds J.J., and Murphy G. Intermolecular autolytic cleavage can contribute to the activation of progelatinase A by cell membranes J. Biol. Chem. 270 1995 30479 30485
Baramova E.N., Bajou K., Remacle A., L'Hoir C., Krell H.W., Weidle U.H., Noel A., and Foidart J.M. Involvement of PA/plasmin system in the processing of pro-MMP-9 and in the second step of pro-MMP-2 activation FEBS Lett. 405 1997 157 162
Sounni N.E., Baramova E.N., Munaut C., Maquoi E., Frankenne F., Foidart J.M., and Noel A. Expression of membrane type 1:matrix metalloproteinase (MT1-MMP) in A2058 melanoma cells is associated with MMP-2 activation and increased tumor growth and vascularization Int. J. Cancer 98 2002 23 28
Butler G.S., Hutton M., Wattam B.A., Williamson R.A., Knauper V., Willenbrock F., and Murphy G. The specificity of TIMP-2 for matrix metalloproteinases can be modified by single amino acid mutations J. Biol. Chem. 274 1999 20391 20396
Lafleur M.A., Hollenberg M.D., Atkinson S.J., Knauper V., Murphy G., and Edwards D.R. Activation of pro-(matrix metalloproteinase-2) (pro-MMP-2) by thrombin is membrane-type-MMP-dependent in human umbilical vein endothelial cells and generates a distinct 63:kDa active species Biochem. J. 357 2001 107 115
Toth M., Bernardo M.M., Gervasi D.C., Soloway P.D., Wang Z., Bigg H.F., Overall C.M., DeClerck Y.A., Tschesche H., Cher M.L., Brown S., Mobashery S., and Fridman R. Tissue inhibitor of metalloproteinase (TIMP)-2 acts synergistically with synthetic matrix metalloproteinase (MMP) inhibitors but not with TIMP-4 to enhance the (Membrane type 1)-MMP-dependent activation of pro-MMP-2 J. Biol. Chem. 275 2000 41415 41423
Hernandez-Barrantes S., Toth M., Bernardo M.M., Yurkova M., Gervasi D.C., Raz Y., Sang Q.A., and Fridman R. 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. 275 2000 12080 12089
Worley J.R., Thompkins P.B., Lee M.H., Hutton M., Soloway P., Edwards D.R., Murphy G., and Knauper V. Sequence motifs of tissue inhibitor of metalloproteinases 2 (TIMP-2) determining progelatinase A (proMMP-2) binding and activation by membrane-type metalloproteinase 1 (MT1-MMP) Biochem. J. 372 2003 799 809
Murphy G., Knauper V., Lee M.H., Amour A., Worley J.R., Hutton M., Atkinson S., Rapti M., and Williamson R. Role of TIMPs (tissue inhibitors of metalloproteinases) in pericellular proteolysis: the specificity is in the detail Biochem. Soc. Symp. 2003 65 80
Morrison C.J., Butler G.S., Bigg H.F., Roberts C.R., Soloway P.D., and Overall C.M. Cellular activation of MMP-2 (gelatinase A) by MT2-MMP occurs via a TIMP-2-independent pathway J. Biol. Chem. 276 2001 47402 47410
Hernandez-Barrantes S., Bernardo M., Toth M., and Fridman R. Regulation of membrane type-matrix metalloproteinases Semin. Cancer Biol. 12 2002 131 138
Brooks P.C., Stromblad S., Sanders L.C., von Schalscha T.L., Aimes R.T., Stetler-Stevenson W.G., Quigley J.P., and Cheresh D.A. Localization of matrix metalloproteinase MMP-2 to the surface of invasive cells by interaction with integrin alpha v beta 3 Cell 85 1996 683 693
Miyamori H., Takino T., Kobayashi Y., Tokai H., Itoh Y., Seiki M., and Sato H. Claudin promotes activation of pro-matrix metalloproteinase-2 mediated by membrane-type matrix metalloproteinases J. Biol. Chem. 276 2001 28204 28211
Zhao H., Bernardo M.M., Osenkowski P., Sohail A., Pei D., Nagase H., Kashiwagi M., Soloway P.D., DeClerck Y.A., and Fridman R. Differential Inhibition of MT3-MMP and MT1-MMP by TIMP-2 and TIMP-3 regulates Pro-MMP-2 activation J. Biol. Chem. 2003
Nie J., and Pei D. Direct activation of pro-matrix metalloproteinase-2 by leukolysin/membrane-type 6:matrix metalloproteinase/matrix metalloproteinase 25:at the asn(109)-Tyr bond Cancer Res. 63 2003 6758 6762
Knauper V., Will H., Lopez-Otin C., Smith B., Atkinson S.J., Stanton H., Hembry R.M., and Murphy G. Cellular mechanisms for human procollagenase-3 (MMP-13) activation. Evidence that MT1-MMP (MMP-14) and gelatinase a (MMP-2) are able to generate active enzyme J. Biol. Chem. 271 1996 17124 17131
Knauper V., Bailey L., Worley J.R., Soloway P., Patterson M.L., and Murphy G. Cellular activation of proMMP-13 by MT1-MMP depends on the C-terminal domain of MMP-13 FEBS Lett. 532 2002 127 130
Toth M., Chvyrkova I., Bernardo M.M., Hernandez-Barrantes S., and Fridman R. 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 2003 386 395
Mu D., Cambier S., Fjellbirkeland L., Baron J.L., Munger J.S., Kawakatsu H., Sheppard D., Broaddus V.C., and Nishimura S.L. The integrin alpha(v)beta8 mediates epithelial homeostasis through MT1-MMP-dependent activation of TGF-beta1 J. Cell Biol. 157 2002 493 507
Velasco-Loyden G., Arribas J., and Lopez-Casillas F. The shedding of betaglycan is regulated by pervanadate and mediated by membrane type matrix metalloprotease-1 J. Biol. Chem. 279 2004 7721 7733
Manes S., Mira E., Barbacid M.M., Cipres A., Fernandez-Resa P., Buesa J.M., Merida I., Aracil M., Marquez G., and Martinez A. Identification of insulin-like growth factor-binding protein-1 as a potential physiological substrate for human stromelysin-3 J. Biol. Chem. 272 1997 25706 25712
Manes S., Llorente M., Lacalle R.A., Gomez-Mouton C., Kremer L., Mira E., and Martinez A. The matrix metalloproteinase-9 regulates the insulin-like growth factor-triggered autocrine response in DU-145 carcinoma cells J. Biol. Chem. 274 1999 6935 6945
Whitelock J.M., Murdoch A.D., Iozzo R.V., and Underwood P.A. The degradation of human endothelial cell-derived perlecan and release of bound basic fibroblast growth factor by stromelysin, collagenase, plasmin, and heparanases J. Biol. Chem. 271 1996 10079 10086
Hashimoto G., Inoki I., Fujii Y., Aoki T., Ikeda E., and Okada Y. Matrix metalloproteinases cleave connective tissue growth factor and reactivate angiogenic activity of vascular endothelial growth factor 165 J. Biol. Chem. 277 2002 36288 36295
Suzuki M., Raab G., Moses M.A., Fernandez C.A., and Klagsbrun M. 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
Yu W.H., Woessner J.F. Jr, McNeish J.D., and Stamenkovic I. 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
Levi E., Fridman R., Miao H.Q., Ma Y.S., Yayon A., and Vlodavsky I. Matrix metalloproteinase 2:releases active soluble ectodomain of fibroblast growth factor receptor 1 Proc. Natl. Acad. Sci. USA 93 1996 7069 7074
Codony-Servat J., Albanell J., Lopez-Talavera J.C., Arribas J., and Baselga J. Cleavage of the HER2 ectodomain is a pervanadate-activable process that is inhibited by the tissue inhibitor of metalloproteases-1 in breast cancer cells Cancer Res. 59 1999 1196 1201
Vecchi M., Rudolph-Owen L.A., Brown C.L., Dempsey P.J., and Carpenter G. Tyrosine phosphorylation and proteolysis. Pervanadate-induced, metalloprotease-dependent cleavage of the ErbB-4 receptor and amphiregulin J. Biol. Chem. 273 1998 20589 20595
Nath D., Williamson N.J., Jarvis R., and Murphy G. Shedding of c-Met is regulated by crosstalk between a G-protein coupled receptor and the EGF receptor and is mediated by a TIMP-3 sensitive metalloproteinase J. Cell Sci. 114 2001 1213 1220
McQuibban G.A., Gong J.H., Tam E.M., McCulloch C.A., Clark-Lewis I., and Overall C.M. Inflammation dampened by gelatinase A cleavage of monocyte chemoattractant protein-3 Science 289 2000 1202 1206
McQuibban G.A., Gong J.H., Wong J.P., Wallace J.L., Clark-Lewis I., and Overall C.M. Matrix metalloproteinase processing of monocyte chemoattractant proteins generates CC chemokine receptor antagonists with anti-inflammatory properties in vivo Blood 100 2002 1160 1167
Overall C.M., McQuibban G.A., and Clark-Lewis I. Discovery of chemokine substrates for matrix metalloproteinases by exosite scanning: a new tool for degradomics Biol. Chem. 383 2002 1059 1066
McQuibban G.A., Butler G.S., Gong J.H., Bendall L., Power C., Clark-Lewis I., and Overall C.M. Matrix metalloproteinase activity inactivates the CXC chemokine stromal cell-derived factor-1 J. Biol. Chem. 276 2001 43503 43508
Tam E.M., Morrison C.J., Wu Y.I., Stack M.S., and Overall C.M. Membrane protease proteomics: Isotope-coded affinity tag MS identification of undescribed MT1-matrix metalloproteinase substrates Proc. Natl. Acad. Sci. USA 101 2004 6917 6922
Belkin A.M., Akimov S.S., Zaritskaya L.S., Ratnikov B.I., Deryugina E.I., and Strongin A.Y. Matrix-dependent proteolysis of surface transglutaminase by membrane-type metalloproteinase regulates cancer cell adhesion and locomotion J. Biol. Chem. 276 2001 18415 18422
Kajita M., Itoh Y., Chiba T., Mori H., Okada A., Kinoh H., and Seiki M. Membrane-type 1:matrix metalloproteinase cleaves CD44 and promotes cell migration J. Cell Biol. 153 2001 893 904
Deryugina E.I., Ratnikov B.I., Postnova T.I., Rozanov D.V., and Strongin A.Y. 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. 277 2002 9749 9756
Rozanov D.V., Ghebrehiwet B., Postnova T.I., Eichinger A., Deryugina E.I., and Strongin A.Y. The hemopexin-like C-terminal domain of membrane type 1:matrix metalloproteinase regulates proteolysis of a multifunctional protein, gC1qR J. Biol. Chem. 277 2002 9318 9325
Strickland D.K., Gonias S.L., and Argraves W.S. Diverse roles for the LDL receptor family Trends Endocrinol. Metab. 13 2002 66 74
Rozanov D.V., Hahn-Dantona E., Strickland D.K., and Strongin A.Y. 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
Annabi B., Lachambre M., Bousquet-Gagnon N., Page M., Gingras D., and Beliveau R. Localization of membrane-type 1:matrix metalloproteinase in caveolae membrane domains Biochem. J. 353 2001 547 553
Jiang A., Lehti K., Wang X., Weiss S.J., Keski-Oja J., and Pei D. Regulation of membrane-type matrix metalloproteinase 1:activity by dynamin-mediated endocytosis Proc. Natl. Acad. Sci. USA 98 2001 13693 13698
Remacle A., Murphy G., and Roghi C. Membrane type I-matrix metalloproteinase (MT1-MMP) is internalised by two different pathways and is recycled to the cell surface J. Cell Sci. 116 2003 3905 3916
Takino T., Miyamori H., Watanabe Y., Yoshioka K., Seiki M., and Sato H. Membrane type 1:matrix metalloproteinase regulates collagen-dependent mitogen-activated protein/extracellular signal-related kinase activation and cell migration Cancer Res. 64 2004 1044 1049
Cao J., Kozarekar P., Pavlaki M., Chiarelli C., Bahou W.F., and Zucker S. Distinct roles for the catalytic and hemopexin domains of membrane type 1-matrix metalloproteinase in substrate degradation and cell migration J. Biol. Chem. 279 2004 14129 14139
Nakamura H., Suenaga N., Taniwaki K., Matsuki H., Yonezawa K., Fujii M., Okada Y., and Seiki M. Constitutive and induced CD44 shedding by ADAM-like proteases and membrane-Type 1:matrix metalloproteinase Cancer Res. 64 2004 876 882
Yamada E., Tobe T., Yamada H., Okamoto N., Zack D.J., Werb Z., Soloway P.D., and Campochiaro P.A. TIMP-1 promotes VEGF-induced neovascularization in the retina Histol. Histopathol. 16 2001 87 97
Roelle S., Grosse R., Aigner A., Krell H.W., Czubayko F., and Gudermann T. Matrix metalloproteinases 2:and 9:mediate epidermal growth factor receptor transactivation by gonadotropin-releasing hormone J. Biol. Chem. 278 2003 47307 47318
Uchiyama-Tanaka Y., Matsubara H., Nozawa Y., Murasawa S., Mori Y., Kosaki A., Maruyama K., Masaki H., Shibasaki Y., Fujiyama S., Nose A., Iba O., Hasagawa T., Tateishi E., Higashiyama S., and Iwasaka T. Angiotensin II signaling and HB-EGF shedding via metalloproteinase in glomerular mesangial cells Kidney Int. 60 2001 2153 2163
Eguchi S., Dempsey P.J., Frank G.D., Motley E.D., and Inagami T. Activation of MAPKs by angiotensin II in vascular smooth muscle cells. Metalloprotease-dependent EGF receptor activation is required for activation of ERK and p38 MAPK but not for JNK J. Biol. Chem. 276 2001 7957 7962
Santiskulvong C., and Rozengurt E. Galardin (GM 6001), a broad-spectrum matrix metalloproteinase inhibitor, blocks bombesin- and LPA-induced EGF receptor transactivation and DNA synthesis in rat-1 cells Exp. Cell Res. 290 2003 437 446
Langlois S., Gingras D., and Beliveau R. Membrane type 1-matrix metalloproteinase (MT1-MMP) cooperates with sphingosine 1-phosphate to induce endothelial cell migration and morphogenic differentiation Blood 103 2004 3020 3028
Langlois S., Gingras D., and Beliveau R. Membrane type 1-matrix metalloproteinase (MT1-MMP) cooperates with sphingosine 1-phosphate to induce endothelial cell migration and morphogenic differentiation Blood 2003
Uekita T., Itoh Y., Yana I., Ohno H., and Seiki M. Cytoplasmic tail-dependent internalization of membrane-type 1:matrix metalloproteinase is important for its invasion-promoting activity J. Cell Biol. 155 2001 1345 1356
Langlois S., Gingras D., and Beliveau R. Membrane type 1-matrix metalloproteinase (MT1-MMP) cooperates with sphingosine 1-phosphate to induce endothelial cell migration and morphogenic differentiation Blood 2003
Rozanov D.V., Ghebrehiwet B., Ratnikov B., Monosov E.Z., Deryugina E.I., and Strongin A.Y. The cytoplasmic tail peptide sequence of membrane type-1 matrix metalloproteinase (MT1-MMP) directly binds to gC1qR, a compartment- specific chaperone-like regulatory protein FEBS Lett. 527 2002 51 57
Polette M., and Birembaut P. Membrane-type metalloproteinases in tumor invasion Int. J. Biochem. Cell Biol. 30 1998 1195 1202
Sato H., and Seiki M. Membrane-type matrix metalloproteinases (MT-MMPs) in tumor metastasis J. Biochem. 119 1996 209 215 (Tokyo)
Sakakibara M., Koizumi S., Saikawa Y., Wada H., Ichihara T., Sato H., Horita S., Mugishima H., Kaneko Y., and Koike K. Membrane-type matrix metalloproteinase-1 expression and activation of gelatinase A as prognostic markers in advanced pediatric neuroblastoma Cancer 85 1999 231 239
Michael M., Babic B., Khokha R., Tsao M., Ho J., Pintilie M., Leco K., Chamberlain D., and Shepherd F.A. Expression and prognostic significance of metalloproteinases and their tissue inhibitors in patients with small-cell lung cancer J. Clin. Oncol. 17 1999 1802 1808
Yoshizaki T., Maruyama Y., Sato H., and Furukawa M. Expression of tissue inhibitor of matrix metalloproteinase-2 correlates with activation of matrix metalloproteinase-2 and predicts poor prognosis in tongue squamous cell carcinoma Int. J. Cancer 95 2001 44 50
Yoshizaki T., Sato H., Maruyama Y., Murono S., Furukawa M., Park C.S., and Seiki M. Increased expression of membrane type 1-matrix metalloproteinase in head and neck carcinoma Cancer 79 1997 139 144
Kanayama H., Yokota K., Kurokawa Y., Murakami Y., Nishitani M., and Kagawa S. Prognostic values of matrix metalloproteinase-2 and tissue inhibitor of metalloproteinase-2 expression in bladder cancer Cancer 82 1998 1359 1366
Davidson B., Goldberg I., Gotlieb W.H., Kopolovic J., Ben Baruch G., Nesland J.M., and Reich R. The prognostic value of metalloproteinases and angiogenic factors in ovarian carcinoma Mol. Cell Endocrinol. 187 2002 39 45
Bendardaf R., Lamlum H., Vihinen P., Ristamaki R., Laine J., and Pyrhonen S. Low collagenase-1 (MMP-1) and MT1-MMP expression levels are favourable survival markers in advanced colorectal carcinoma Oncology 65 2003 337 346
Polette M., Nawrocki B., Gilles C., Sato H., Seiki M., Tournier J.M., and Birembaut P. MT-MMP expression and localisation in human lung and breast cancers Virchows Arch. 428 1996 29 35
Bisson C., Blacher S., Polette M., Blanc J.F., Kebers F., Desreux J., Tetu B., Rosenbaum J., Foidart J.M., Birembaut P., and Noel A. Restricted expression of membrane type 1-matrix metalloproteinase by myofibroblasts adjacent to human breast cancer cells Int. J. Cancer 105 2003 7 13
Okada A., Bellocq J.P., Rouyer N., Chenard M.P., Rio M.C., Chambon P., and Basset P. Membrane-type matrix metalloproteinase (MT-MMP) gene is expressed in stromal cells of human colon, breast, and head and neck carcinomas Proc. Natl. Acad. Sci. USA 92 1995 2730 2734
Gilles C., Polette M., Seiki M., Birembaut P., and Thompson E.W. Implication of collagen type I-induced membrane-type 1-matrix metalloproteinase expression and matrix metalloproteinase-2 activation in the metastatic progression of breast carcinoma Lab. Invest. 76 1997 651 660
Gilles C., Polette M., Piette J., Munaut C., Thompson E.W., Birembaut P., and Foidart J.M. High level of MT-MMP expression is associated with invasiveness of cervical cancer cells Int. J. Cancer 65 1996 209 213
Nakada M., Nakamura H., Ikeda E., Fujimoto N., Yamashita J., Sato H., Seiki M., and Okada Y. Expression and tissue localization of membrane-type 1, 2, and 3:matrix metalloproteinases in human astrocytic tumors Am. J. Pathol. 154 1999 417 428
Nuttall R.K., Pennington C.J., Taplin J., Wheal A., Yong V.W., Forsyth P.A., and Edwards D.R. Elevated membrane-type matrix metalloproteinases in gliomas revealed by profiling proteases and inhibitors in human cancer cells Mol. Cancer Res. 1 2003 333 345
Kitagawa Y., Kunimi K., Uchibayashi T., Sato H., and Namiki M. Expression of messenger RNAs for membrane-type 1, 2, and 3:matrix metalloproteinases in human renal cell carcinomas J. Urol. 162 1999 905 909
Ueno H., Nakamura H., Inoue M., Imai K., Noguchi M., Sato H., Seiki M., and Okada Y. Expression and tissue localization of membrane-types 1, 2, and 3:matrix metalloproteinases in human invasive breast carcinomas Cancer Res. 57 1997 2055 2060
Takino T., Sato H., Shinagawa A., and Seiki M. Identification of the second membrane-type matrix metalloproteinase (MT- MMP-2) gene from a human placenta cDNA library. MT-MMPs form a unique membrane-type subclass in the MMP family J. Biol. Chem. 270 1995 23013 23020
Velasco G., Cal S., Merlos-Suarez A., Ferrando A.A., Alvarez S., Nakano A., Arribas J., and Lopez-Otin C. Human MT6-matrix metalloproteinase: identification, progelatinase A activation, and expression in brain tumors Cancer Res. 60 2000 877 882
Ha H.Y., Moon H.B., Nam M.S., Lee J.W., Ryoo Z.Y., Lee T.H., Lee K.K., So B.J., Sato H., Seiki M., and Yu D.Y. Overexpression of membrane-type matrix metalloproteinase-1 gene induces mammary gland abnormalities and adenocarcinoma in transgenic mice Cancer Res. 61 2001 984 990
Itoh T., Tanioka M., Yoshida H., Yoshioka T., Nishimoto H., and Itohara S. Reduced angiogenesis and tumor progression in gelatinase A-deficient mice Cancer Res. 58 1998 1048 1051
Hajitou A., Sounni N.E., Devy L., Grignet-Debrus C., Lewalle J.M., Li H., Deroanne C.F., Lu H., Colige A., Nusgens B.V., Frankenne F., Maron A., Yeh P., Perricaudet M., Chang Y., Soria C., Calberg-Bacq C.M., Foidart J.M., and Noel A. Down-regulation of vascular endothelial growth factor by tissue inhibitor of metalloproteinase-2: effect on in vivo mammary tumor growth and angiogenesis Cancer Res. 61 2001 3450 3457
Sounni N.E., Devy L., Hajitou A., Frankenne F., Munaut C., Gilles C., Deroanne C., Thompson E.W., Foidart J.M., and Noel A. MT1-MMP expression promotes tumor growth and angiogenesis through an up- regulation of vascular endothelial growth factor expression FASEB J. 16 2002 555 564
Deryugina E.I., Soroceanu L., and Strongin A.Y. Up-regulation of vascular endothelial growth factor by membrane-type 1:matrix metalloproteinase stimulates human glioma xenograft growth and angiogenesis Cancer Res. 62 2002 580 588
Hotary K.B., Allen E.D., Brooks P.C., Datta N.S., Long M.W., and Weiss S.J. Membrane type I matrix metalloproteinase usurps tumor growth control imposed by the three-dimensional extracellular matrix Cell 114 2003 33 45
Iida J., Wilhelmson K.L., Price M.A., Wilson C.M., Pei D., Furcht L.T., and McCarthy J.B. Membrane type-1 matrix metalloproteinase promotes human melanoma invasion and growth J. Invest Dermatol. 122 2004 167 176
Tester A.M., Waltham M., Oh S.J., Bae S.N., Bills M.M., Walker E.C., Kern F.G., Stetler-Stevenson W.G., Lippman M.E., and Thompson E.W. Pro-matrix metalloproteinase-2 transfection increases orthotopic primary growth and experimental metastasis of MDA-MB-231 human breast cancer cells in nude mice Cancer Res. 64 2004 652 658
Takino T., Koshikawa N., Miyamori H., Tanaka M., Sasaki T., Okada Y., Seiki M., and Sato H. Cleavage of metastasis suppressor gene product KiSS-1 protein/metastin by matrix metalloproteinases Oncogene 22 2003 4617 4626
Gilles C., Polette M., Coraux C., Tournier J.M., Meneguzzi G., Munaut C., Volders L., Rousselle P., Birembaut P., and Foidart J.M. Contribution of MT1-MMP and of human laminin-5 gamma2 chain degradation to mammary epithelial cell migration J. Cell Sci. 114 2001 2967 2976
Tsunezuka Y., Kinoh H., Takino T., Watanabe Y., Okada Y., Shinagawa A., Sato H., and Seiki M. Expression of membrane-type matrix metalloproteinase 1 (MT1-MMP) in tumor cells enhances pulmonary metastasis in an experimental metastasis assay Cancer Res. 56 1996 5678 5683
Shimada T., Nakamura H., Yamashita K., Kawata R., Murakami Y., Fujimoto N., Sato H., Seiki M., and Okada Y. Enhanced production and activation of progelatinase A mediated by membrane-type 1:matrix metalloproteinase in human oral squamous cell carcinomas: implications for lymph node metastasis Clin. Exp. Metastasis 18 2000 179 188
Habelhah H., Okada F., Kobayashi M., Nakai K., Choi S., Hamada J., Moriuchi T., Kaya M., Yoshida K., Fujinaga K., and Hosokawa M. Increased E1AF expression in mouse fibrosarcoma promotes metastasis through induction of MT1-MMP expression Oncogene 18 1999 1771 1776
Ratnikov B.I., Rozanov D.V., Postnova T.I., Baciu P.G., Zhang H., DiScipio R.G., Chestukhina G.G., Smith J.W., Deryugina E.I., and Strongin A.Y. An alternative processing of integrin alpha(v) subunit in tumor cells by membrane type-1 matrix metalloproteinase J. Biol. Chem. 277 2002 7377 7385
Koshikawa N., Giannelli G., Cirulli V., Miyazaki K., and Quaranta V. Role of cell surface metalloprotease MT1-MMP in epithelial cell migration over laminin-5 J. Cell Biol. 148 2000 615 624
Ueda J., Kajita M., Suenaga N., Fujii K., and Seiki M. Sequence-specific silencing of MT1-MMP expression suppresses tumor cell migration and invasion: importance of MT1-MMP as a therapeutic target for invasive tumors Oncogene 22 2003 8716 8722
Lafleur M.A., Handsley M.M., Knauper V., Murphy G., and Edwards D.R. Endothelial tubulogenesis within fibrin gels specifically requires the activity of membrane-type-matrix metalloproteinases (MT-MMPs) J. Cell Sci. 115 2002 3427 3438
Kadono Y., Shibahara K., Namiki M., Watanabe Y., Seiki M., and Sato H. Membrane type 1-matrix metalloproteinase is involved in the formation of hepatocyte growth factor/scatter factor-induced branching tubules in madin-darby canine kidney epithelial cells Biochem. Biophys. Res. Commun. 251 1998 681 687
Haas T.L., Davis S.J., and Madri J.A. 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 1998 3604 3610
Zhou Z., Apte S.S., Soininen R., Cao R., Baaklini G.Y., Rauser R.W., Wang J., Cao Y., and Tryggvason K. Impaired endochondral ossification and angiogenesis in mice deficient in membrane-type matrix metalloproteinase I Proc. Natl. Acad. Sci. USA 97 2000 4052 4057
Seftor R.E., Seftor E.A., Koshikawa N., Meltzer P.S., Gardner L.M., Bilban M., Stetler-Stevenson W.G., Quaranta V., and Hendrix M.J. Cooperative interactions of laminin 5:gamma2 chain, matrix metalloproteinase-2, and membrane type-1-matrix/metalloproteinase are required for mimicry of embryonic vasculogenesis by aggressive melanoma Cancer Res. 61 2001 6322 6327
Maquoi E., Sounni N.E., Devy L., Olivier F., Frankenne F., Krell H.W., Grams F., Foidart J.M., and Noel A. Anti-invasive, antitumoral, and antiangiogenic efficacy of a pyrimidine-2,4,6-trione derivative, an orally active and selective matrix metalloproteinases inhibitor Clin. Cancer Res. 10 2004 4038 4047
Munaut C., Boniver J., Foidart J.M., and Deprez M. Macrophage migration inhibitory factor (MIF) expression in human glioblastomas correlates with vascular endothelial growth factor (VEGF) expression Neuropathol. Appl. Neurobiol. 28 2002 452 460
Sekiya I., Vuoristo J.T., Larson B.L., and Prockop D.J. In vitro cartilage formation by human adult stem cells from bone marrow stroma defines the sequence of cellular and molecular events during chondrogenesis Proc. Natl. Acad. Sci. USA 99 2002 4397 4402
Bergers G., Brekken R., McMahon G., Vu T.H., Itoh T., Tamaki K., Tanzawa K., Thorpe P., Itohara S., Werb Z., and Hanahan D. Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis Nat. Cell Biol. 2 2000 737 744
Belotti D., Paganoni P., Manenti L., Garofalo A., Marchini S., Taraboletti G., and Giavazzi R. Matrix metalloproteinases (MMP9 and MMP2) induce the release of vascular endothelial growth factor (VEGF) by ovarian carcinoma cells: implications for ascites formation Cancer Res. 63 2003 5224 5229
Arlt M., Kopitz C., Pennington C., Watson K.L., Krell H.W., Bode W., Gansbacher B., Khokha R., Edwards D.R., and Kruger A. Increase in gelatinase-specificity of matrix metalloproteinase inhibitors correlates with antimetastatic efficacy in a T-cell lymphoma model Cancer Res. 62 2002 5543 5550
Valente P., Fassina G., Melchiori A., Masiello L., Cilli M., Vacca A., Onisto M., Santi L., Stetler-Stevenson W.G., and Albini A. TIMP-2 over-expression reduces invasion and angiogenesis and protects B16F10 melanoma cells from apoptosis Int. J. Cancer 75 1998 246 253
Li H., Lindenmeyer F., Grenet C., Opolon P., Menashi S., Soria C., Yeh P., Perricaudet M., and Lu H. AdTIMP-2 inhibits tumor growth, angiogenesis, and metastasis, and prolongs survival in mice Hum. Gene Ther. 12 2001 515 526
Yoshiji H., Harris S.R., Raso E., Gomez D.E., Lindsay C.K., Shibuya M., Sinha C.C., and Thorgeirsson U.P. Mammary carcinoma cells over-expressing tissue inhibitor of metalloproteinases-1 show enhanced vascular endothelial growth factor expression Int. J. Cancer 75 1998 81 87
Spurbeck W.W., Ng C.Y., Vanin E.F., and Davidoff A.M. Retroviral vector-producer cell-mediated in vivo gene transfer of TIMP-3 restricts angiogenesis and neuroblastoma growth in mice Cancer Gene Ther. 10 2003 161 167
Spurbeck W.W., Ng C.Y., Strom T.S., Vanin E.F., and Davidoff A.M. Enforced expression of tissue inhibitor of matrix metalloproteinase-3 affects functional capillary morphogenesis and inhibits tumor growth in a murine tumor model Blood 100 2002 3361 3368
Chand H.S., Du X., Ma D., Inzunza H.D., Kamei S., Foster D., Brodie S., and Kisiel W. The effect of human tissue factor pathway inhibitor-2 on the growth and metastasis of fibrosarcoma tumors in athymic mice Blood 103 2004 1069 1077
Qi J.H., Ebrahem Q., Moore N., Murphy G., Claesson-Welsh L., Bond M., Baker A., and Anand-Apte B. A novel function for tissue inhibitor of metalloproteinases-3 (TIMP3): inhibition of angiogenesis by blockage of VEGF binding to VEGF receptor- 2 Nat. Med. 9 2003 407 415
Seo D.W., Li H., Guedez L., Wingfield P.T., Diaz T., Salloum R., Wei B.Y., and Stetler-Stevenson W.G. TIMP-2 mediated inhibition of angiogenesis: an MMP-independent mechanism Cell 114 2003 171 180
Takahashi C., Junseo O., and Noda M. The membrane-anchored metalloproteinase inhibitor RECK Tanpakushitsu Kakusan Koso 47 2002 1889 1895
Furumoto K., Arii S., Mori A., Furuyama H., Gorrin Rivas M.J., Nakao T., Isobe N., Murata T., Takahashi C., Noda M., and Imamura M. RECK gene expression in hepatocellular carcinoma: correlation with invasion-related clinicopathological factors and its clinical significance. Reverse-inducing-- cysteine-rich protein with Kazal motifs Hepatology 33 2001 189 195
Masui T., Doi R., Koshiba T., Fujimoto K., Tsuji S., Nakajima S., Koizumi M., Toyoda E., Tulachan S., Ito D., Kami K., Mori T., Wada M., Noda M., and Imamura M. RECK expression in pancreatic cancer: its correlation with lower invasiveness and better prognosis Clin. Cancer Res. 9 2003 1779 1784
Oh J., Takahashi R., Kondo S., Mizoguchi A., Adachi E., Sasahara R.M., Nishimura S., Imamura Y., Kitayama H., Alexander D.B., Ide C., Horan T.P., Arakawa T., Yoshida H., Nishikawa S., Itoh Y., Seiki M., Itohara S., Takahashi C., and Noda M. The membrane-anchored MMP inhibitor RECK is a key regulator of extracellular matrix integrity and angiogenesis Cell 107 2001 789 800