New facets of matrix metalloproteinases MMP-2 and MMP-9 as cell surface transducers: Outside-in signaling and relationship to tumor progression

Biochimica et Biophysica Acta - Reviews on Cancer

Volumn 1825, Issue 1, 2012, Pages 29-36

  Bauvois, Brigitte ^a  

^a CENTRE DE RECHERCHE DES CORDELIERS   (France)

Author keywords

Cancer; Cell surface binding; Function; Gelatinase; Inhibitor; Outside in signaling

Indexed keywords

BATIMASTAT; BISPHOSPHONIC ACID DERIVATIVE; CGS 27123A; CHEMOKINE; CYTOKINE; CYTOKINE RECEPTOR; DOXYCYCLINE; GELATINASE; GELATINASE A; GELATINASE B; GELATINASE INHIBITOR; GROWTH FACTOR; GROWTH FACTOR RECEPTOR; HERMES ANTIGEN; INCYCLINIDE; INTEGRIN; KU ANTIGEN; MARIMASTAT; MATRIX METALLOPROTEINASE INHIBITOR; MINOCYCLINE; PRINOMASTAT; REBIMASTAT; S 3304; TANOMASTAT; TETRACYCLINE DERIVATIVE; UNCLASSIFIED DRUG;

ANGIOGENESIS; BRAIN TUMOR; CANCER GROWTH; CARBOXY TERMINAL SEQUENCE; CELL GROWTH; CELL INVASION; CELL MIGRATION; CELL SURFACE; CELL SURFACE TRANSDUCER; CELL SURVIVAL; DRUG BIOAVAILABILITY; DRUG BLOOD LEVEL; DRUG DESIGN; DRUG TARGETING; ENZYME ACTIVE SITE; EXTRACELLULAR MATRIX; HUMAN; INFLAMMATION; KAPOSI SARCOMA; MALIGNANT NEOPLASTIC DISEASE; MUSCULOSKELETAL DISEASE; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DOMAIN; REVIEW; SIGNAL TRANSDUCTION; SOLID TUMOR; TRANSDUCER;

CELL MEMBRANE; DISEASE PROGRESSION; HUMANS; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; NEOPLASMS; SIGNAL TRANSDUCTION; TUMOR MARKERS, BIOLOGICAL;

EID: 80054997801     PISSN: 0304419X     EISSN: 18792561     Source Type: Journal    
DOI: 10.1016/j.bbcan.2011.10.001     Document Type: Review

References (109)

1. Kessenbrock K., Plaks V., Werb Z. Matrix metalloproteinases: regulators of the tumor microenvironment. Cell 2010, 141:52-67.
2. Klein T., Bischoff R. Physiology and pathophysiology of matrix metalloproteases. Amino Acids 2011, 41:271-290.
3. Cruz-Munoz W., Khokha R. The role of tissue inhibitors of metalloproteinases in tumorigenesis and metastasis. Crit. Rev. Clin. Lab. Sci. 2008, 45:291-338.
4. Bourboulia D., Stetler-Stevenson W.G. Matrix metalloproteinases (MMPs) and tissue inhibitors of metalloproteinases (TIMPs): positive and negative regulators in tumor cell adhesion. Semin. Cancer Biol. 2010, 20:161-168.
5. Brew K., Nagase H. The tissue inhibitors of metalloproteinases (TIMPs): an ancient family with structural and functional diversity. Biochim. Biophys. Acta 2010, 1803:55-71.
6. Devy L., Dransfield D.T. New strategies for the next generation of matrix-metalloproteinase inhibitors: selectively targeting membrane-anchored MMPs with therapeutic antibodies. Biochem. Res. Int. 2011, 10.1155/2011/191670.
7. Bjorklund M., Koivunen E. Gelatinase-mediated migration and invasion of cancer cells. Biochim. Biophys. Acta 2005, 1755:37-69.
8. Roy R., Yang J., Moses M.A. Matrix metalloproteinases as novel biomarkers and potential therapeutic targets in human cancer. J. Clin. Oncol. 2009, 27:5287-5297.
9. Hatfield K.J., Reikvam H., Bruserud O. The crosstalk between the matrix metalloprotease system and the chemokine network in acute myeloid leukemia. Curr. Med. Chem. 2010, 17:4448-4461.
10. Cauwe B., Van den Steen P.E., Opdenakker G. The biochemical, biological, and pathological kaleidoscope of cell surface substrates processed by matrix metalloproteinases. Crit. Rev. Biochem. Mol. Biol. 2007, 42:113-185.
11. Rodriguez D., Morrison C.J., Overall C.M. Matrix metalloproteinases: what do they not do? New substrates and biological roles identified by murine models and proteomics. Biochim. Biophys. Acta 2010, 1803:39-54.
12. Deryugina E.I., Quigley J.P. Pleiotropic roles of matrix metalloproteinases in tumor angiogenesis: contrasting, overlapping and compensatory functions. Biochim. Biophys. Acta 2010, 1803:103-120.
13. Gialeli C., Theocharis A.D., Karamanos N.K. Roles of matrix metalloproteinases in cancer progression and their pharmacological targeting. FEBS J. 2011, 278:16-27.
14. Lynch C.C. Matrix metalloproteinases as master regulators of the vicious cycle of bone metastasis. Bone 2011, 48:44-53.
15. Li N.G., Shi Z.H., Tang Y.P., Duan J.A. Selective matrix metalloproteinase inhibitors for cancer. Curr. Med. Chem. 2009, 16:3805-3827.
16. Dorman G., Cseh S., Hajdu I., Barna L., Konya D., Kupai K., Kovacs L., Ferdinandy P. Matrix metalloproteinase inhibitors: a critical appraisal of design principles and proposed therapeutic utility. Drugs 2010, 70:949-964.
17. Falardeau P., Champagne P., Poyet P., Hariton C., Dupont E. Neovastat, a naturally occurring multifunctional antiangiogenic drug, in phase III clinical trials. Semin. Oncol. 2001, 28:620-625.
18. Cianfrocca M., Cooley T.P., Lee J.Y., Rudek M.A., Scadden D.T., Ratner L., Pluda J.M., Figg W.D., Krown S.E., Dezube B.J. Matrix metalloproteinase inhibitor COL-3 in the treatment of AIDS-related Kaposi's sarcoma: a phase I AIDS malignancy consortium study. J. Clin. Oncol. 2002, 20:153-159.
19. Sapadin A.N., Fleischmajer R. Tetracyclines: nonantibiotic properties and their clinical implications. J. Am. Acad. Dermatol. 2006, 54:258-265.
20. Cianfrocca M., Lee S., Von Roenn J., Rudek M.A., Dezube B.J., Krown S.E., Sparano J.A. Pilot study evaluating the interaction between paclitaxel and protease inhibitors in patients with human immunodeficiency virus-associated Kaposi's sarcoma: an Eastern Cooperative Oncology Group (ECOG) and AIDS Malignancy Consortium (AMC) trial. Cancer Chemother. Pharmacol. 2011, 68:827-833.
21. Lacerna L., Hohneker J. Zoledronic acid for the treatment of bone metastases in patients with breast cancer and other solid tumors. Semin. Oncol. 2003, 30:150-160.
22. Yadav R.K., Gupta S.P., Sharma P.K., Patil V.M. Recent advances in studies on hydroxamates as matrix metalloproteinase inhibitors: a review. Curr. Med. Chem. 2011, 18:1704-1722.
23. Mant T.G., Bradford D., Amin D.M., Pisupati J., Kambayashi Y., Yano Y., Tanaka K., Yamada-Sawada T. Pharmacokinetics and safety assessments of high-dose and 4-week treatment with S-3304, a novel matrix metalloproteinase inhibitor, in healthy volunteers. Br. J. Clin. Pharmacol. 2007, 63:512-526.
24. Chiappori A.A., Eckhardt S.G., Bukowski R., Sullivan D.M., Ikeda M., Yano Y., Yamada-Sawada T., Kambayashi Y., Tanaka K., Javle M.M., Mekhail T., O'Bryant L., Creaven C.P.J. A phase I pharmacokinetic and pharmacodynamic study of s-3304, a novel matrix metalloproteinase inhibitor, in patients with advanced and refractory solid tumors. Clin. Cancer Res. 2007, 13:2091-2099.
25. Overall C.M., Kleifeld O. Towards third generation matrix metalloproteinase inhibitors for cancer therapy. Br. J. Cancer 2006, 94:941-946.
26. Lopez-Otin C., Matrisian L.M. Emerging roles of proteases in tumour suppression. Nat. Rev. Cancer 2007, 7:800-808.
27. Murphy G., Nagase H. Progress in matrix metalloproteinase research. Mol. Aspects Med. 2008, 29:290-308.
28. Overall C.M., Kleifeld O. Tumour microenvironment - opinion: validating matrix metalloproteinases as drug targets and anti-targets for cancer therapy. Nat. Rev. Cancer 2006, 6:227-239.
29. Martin M.D., Matrisian L.M. The other side of MMPs: protective roles in tumor progression. Cancer Metastasis Rev. 2007, 26:717-724.
30. Turpeenniemi-Hujanen T. Gelatinases (MMP-2 and -9) and their natural inhibitors as prognostic indicators in solid cancers. Biochimie 2005, 87:287-297.
31. Yu X.F., Han Z.C. Matrix metalloproteinases in bone marrow: roles of gelatinases in physiological hematopoiesis and hematopoietic malignancies. Histol. Histopathol. 2006, 21:519-531.
32. Rydlova M., Holubec L., Ludvikova M., Kalfert D., Franekova J., Povysil C., Ludvikova M. Biological activity and clinical implications of the matrix metalloproteinases. Anticancer. Res. 2008, 28:1389-1397.
33. Klein G., Vellenga E., Fraaije M.W., Kamps W.A., de Bont E.S. The possible role of matrix metalloproteinase (MMP)-2 and MMP-9 in cancer, e.g. acute leukemia. Crit. Rev. Oncol. Hematol. 2004, 50:87-100.
34. Toth M., Gervasi D.C., Fridman R. Phorbol ester-induced cell surface association of matrix metalloproteinase-9 in human MCF10A breast epithelial cells. Cancer Res. 1997, 57:3159-3167.
35. Paupert J., Mansat-De Mas V., Demur C., Salles B., Muller C. Cell-surface MMP-9 regulates the invasive capacity of leukemia blast cells with monocytic features. Cell Cycle 2008, 7:1047-1053.
36. Fridman R., Toth M., Chvyrkova I., Meroueh S.O., Mobashery S. Cell surface association of matrix metalloproteinase-9 (gelatinase B). Cancer Metastasis Rev. 2003, 22:153-166.
37. Bannikov G.A., Karelina T.V., Collier I.E., Marmer B.L., Goldberg G.I. Substrate binding of gelatinase B induces its enzymatic activity in the presence of intact propeptide. J. Biol. Chem. 2002, 277:16022-16027.
38. Geurts N., Martens E., Van Aelst I., Proost P., Opdenakker G., Van den Steen P.E. Beta-hematin interaction with the hemopexin domain of gelatinase B/MMP-9 provokes autocatalytic processing of the propeptide, thereby priming activation by MMP-3. Biochemistry 2008, 47:2689-2699.
39. Freise C., Erben U., Muche M., Farndale R., Zeitz M., Somasundaram R., Ruehl M. The alpha 2 chain of collagen type VI sequesters latent proforms of matrix-metalloproteinases and modulates their activation and activity. Matrix Biol. 2009, 28:480-489.
40. 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., Noda M. The membrane-anchored MMP inhibitor RECK is a key regulator of extracellular matrix integrity and angiogenesis. Cell 2001, 107:789-800.
41. Takahashi C., Sheng Z., Horan T.P., Kitayama H., Maki M., Hitomi K., Kitaura Y., Takai S., Sasahara R.M., Horimoto A., Ikawa Y., Ratzkin B.J., Arakawa T., Noda M. Regulation of matrix metalloproteinase-9 and inhibition of tumor invasion by the membrane-anchored glycoprotein RECK. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:13221-13226.
42. Egeblad M., Werb Z. New functions for the matrix metalloproteinases in cancer progression. Nat. Rev. Cancer 2002, 2:161-174.
43. Baluk P., Raymond W.W., Ator E., Coussens L.M., McDonald D.M., Caughey G.H. Matrix metalloproteinase-2 and -9 expression increases in Mycoplasma-infected airways but is not required for microvascular remodeling. Am. J. Physiol. Lung Cell Mol. Physiol. 2004, 287:L307-L317.
44. Hotary K., Li X.Y., Allen E., Stevens S.L., Weiss S.J. A cancer cell metalloprotease triad regulates the basement membrane transmigration program. Genes Dev. 2006, 20:2673-2686.
45. Sabeh F., Li X.Y., Saunders T.L., Rowe R.G., Weiss S.J. Secreted versus membrane-anchored collagenases: relative roles in fibroblast-dependent collagenolysis and invasion. J. Biol. Chem. 2009, 284:23001-23011.
46. Hangai M., Kitaya N., Xu J., Chan C.K., Kim J.J., Werb Z., Ryan S.J., Brooks P.C. Matrix metalloproteinase-9-dependent exposure of a cryptic migratory control site in collagen is required before retinal angiogenesis. Am. J. Pathol. 2002, 161:1429-1437.
47. Xu J., Rodriguez D., Petitclerc E., Kim J.J., Hangai M., Moon Y.S., Davis G.E., Brooks P.C. Proteolytic exposure of a cryptic site within collagen type IV is required for angiogenesis and tumor growth in vivo. J. Cell Biol. 2001, 154:1069-1079.
48. Giannelli G., Falk-Marzillier J., Schiraldi O., Stetler-Stevenson W.G., Quaranta V. Induction of cell migration by matrix metalloprotease-2 cleavage of laminin-5. Science 1997, 277:225-228.
49. Bergers G., Brekken R., McMahon G., Vu T.H., Itoh T., Tamaki K., Tanzawa K., Thorpe P., Itohara S., Werb Z., Hanahan D. Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis. Nat. Cell Biol. 2000, 2:737-744.
50. Yu Q., Stamenkovic I. Cell surface-localized matrix metalloproteinase-9 proteolytically activates TGF-beta and promotes tumor invasion and angiogenesis. Genes Dev. 2000, 14:163-176.
51. Yang L., DeBusk L.M., Fukuda K., Fingleton B., Green-Jarvis B., Shyr Y., Matrisian L.M., Carbone D.P., Lin P.C. Expansion of myeloid immune suppressor Gr+CD11b+ cells in tumor-bearing host directly promotes tumor angiogenesis. Cancer Cell 2004, 6:409-421.
52. Du R., Lu K.V., Petritsch C., Liu P., Ganss R., Passegue E., Song H., Vandenberg S., Johnson R.S., Werb Z., Bergers G. HIF1alpha induces the recruitment of bone marrow-derived vascular modulatory cells to regulate tumor angiogenesis and invasion. Cancer Cell 2008, 13:206-220.
53. Ardi V.C., Van den Steen P.E., Opdenakker G., Schweighofer B., Deryugina E.I., Quigley J.P. Neutrophil MMP-9 proenzyme, unencumbered by TIMP-1, undergoes efficient activation in vivo and catalytically induces angiogenesis via a basic fibroblast growth factor (FGF-2)/FGFR-2 pathway. J. Biol. Chem. 2009, 284:25854-25866.
54. Hamano Y., Zeisberg M., Sugimoto H., Lively J.C., Maeshima Y., Yang C., Hynes R.O., Werb Z., Sudhakar A., Kalluri R. Physiological levels of tumstatin, a fragment of collagen IV alpha3 chain, are generated by MMP-9 proteolysis and suppress angiogenesis via alphaV beta3 integrin. Cancer Cell 2003, 3:589-601.
55. Heljasvaara R., Nyberg P., Luostarinen J., Parikka M., Heikkila P., Rehn M., Sorsa T., Salo T., Pihlajaniemi T. Generation of biologically active endostatin fragments from human collagen XVIII by distinct matrix metalloproteases. Exp. Cell Res. 2005, 307:292-304.
56. Mantovani A., Allavena P., Sica A., Balkwill F. Cancer-related inflammation. Nature 2008, 454:436-444.
57. Tian M., Neil J.R., Schiemann W.P. Transforming growth factor-beta and the hallmarks of cancer. Cell. Signal. 2011, 23:951-962.
58. Levi E., Fridman R., Miao H.Q., Ma Y.S., Yayon A., Vlodavsky I. Matrix metalloproteinase 2 releases active soluble ectodomain of fibroblast growth factor receptor 1. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:7069-7074.
59. Nelissen I., Martens E., Van den Steen P.E., Proost P., Ronsse I., Opdenakker G. Gelatinase B/matrix metalloproteinase-9 cleaves interferon-beta and is a target for immunotherapy. Brain 2003, 126:1371-1381.
60. Fowlkes J.L., Serra D.M., Nagase H., Thrailkill K.M. MMPs are IGFBP-degrading proteinases: implications for cell proliferation and tissue growth. Ann. N. Y. Acad. Sci. 1999, 878:696-699.
61. Takino T., Koshikawa N., Miyamori H., Tanaka M., Sasaki T., Okada Y., Seiki M., Sato H. Cleavage of metastasis suppressor gene product KiSS-1 protein/metastin by matrix metalloproteinases. Oncogene 2003, 22:4617-4626.
62. Takafuji V., Forgues M., Unsworth E., Goldsmith P., Wang X.W. An osteopontin fragment is essential for tumor cell invasion in hepatocellular carcinoma. Oncogene 2007, 26:6361-6371.
63. Sheu B.C., Hsu S.M., Ho H.N., Lien H.C., Huang S.C., Lin R.H. A novel role of metalloproteinase in cancer-mediated immunosuppression. Cancer Res. 2001, 61:237-242.
64. Heissig B., Hattori K., Dias S., Friedrich M., Ferris B., Hackett N.R., Crystal R.G., Besmer P., Lyden D., Moore M.A., Werb Z., Rafii S. Recruitment of stem and progenitor cells from the bone marrow niche requires MMP-9 mediated release of kit-ligand. Cell 2002, 109:625-637.
65. Seandel M., Butler J., Lyden D., Rafii S. A catalytic role for proangiogenic marrow-derived cells in tumor neovascularization. Cancer Cell 2008, 13:181-183.
66. Fiore E., Fusco C., Romero P., Stamenkovic I. Matrix metalloproteinase 9 (MMP-9/gelatinase B) proteolytically cleaves ICAM-1 and participates in tumor cell resistance to natural killer cell-mediated cytotoxicity. Oncogene 2002, 21:5213-5223.
67. McQuibban G.A., Gong J.H., Tam E.M., McCulloch C.A., Clark-Lewis I., Overall C.M. Inflammation dampened by gelatinase A cleavage of monocyte chemoattractant protein-3. Science 2000, 289:1202-1206.
68. Van den Steen P.E., Proost P., Wuyts A., Van Damme J., Opdenakker G. Neutrophil gelatinase B potentiates interleukin-8 tenfold by aminoterminal processing, whereas it degrades CTAP-III, PF-4, and GRO-alpha and leaves RANTES and MCP-2 intact. Blood 2000, 96:2673-2681.
69. Hofmann U.B., Houben R., Brocker E.B., Becker J.C. Role of matrix metalloproteinases in melanoma cell invasion. Biochimie 2005, 87:307-314.
70. Stefanidakis M., Koivunen E. Cell-surface association between matrix metalloproteinases and integrins: role of the complexes in leukocyte migration and cancer progression. Blood 2006, 108:1441-1450.
71. Hahn-Dantona E., Ruiz J.F., Bornstein P., Strickland D.K. The low density lipoprotein receptor-related protein modulates levels of matrix metalloproteinase 9 (MMP-9) by mediating its cellular catabolism. J. Biol. Chem. 2001, 276:15498-15503.
72. Yang Z., Strickland D.K., Bornstein P. Extracellular matrix metalloproteinase 2 levels are regulated by the low density lipoprotein-related scavenger receptor and thrombospondin 2. J. Biol. Chem. 2001, 276:8403-8408.
73. Van den Steen P.E., Van Aelst I., Hvidberg V., Piccard H., Fiten P., Jacobsen C., Moestrup S.K., Fry S., Royle L., Wormald M.R., Wallis R., Rudd P.M., Dwek R.A., Opdenakker G. The hemopexin and O-glycosylated domains tune gelatinase B/MMP-9 bioavailability via inhibition and binding to cargo receptors. J. Biol. Chem. 2006, 281:18626-18637.
74. Monferran S., Paupert J., Dauvillier S., Salles B., Muller C. The membrane form of the DNA repair protein Ku interacts at the cell surface with metalloproteinase 9. EMBO J. 2004, 23:3758-3768.
75. Bourguignon L.Y., Gunja-Smith Z., Iida N., Zhu H.B., Young L.J., Muller W.J., Cardiff R.D. CD44v(3,8-10) is involved in cytoskeleton-mediated tumor cell migration and matrix metalloproteinase (MMP-9) association in metastatic breast cancer cells. J. Cell. Physiol. 1998, 176:206-215.
76. Yu Q., Stamenkovic I. Localization of matrix metalloproteinase 9 to the cell surface provides a mechanism for CD44-mediated tumor invasion. Genes Dev. 1999, 13:35-48.
77. Hu Y., Ivashkiv L.B. Costimulation of chemokine receptor signaling by matrix metalloproteinase-9 mediates enhanced migration of IFN-alpha dendritic cells. J. Immunol. 2006, 176:6022-6033.
78. Dufour A., Sampson N.S., Zucker S., Cao J. Role of the hemopexin domain of matrix metalloproteinases in cell migration. J. Cell. Physiol. 2008, 217:643-651.
79. Dufour A., Zucker S., Sampson N.S., Kuscu C., Cao J. Role of matrix metalloproteinase-9 dimers in cell migration: design of inhibitory peptides. J. Biol. Chem. 2010, 285:35944-35956.
80. Redondo-Munoz J., Ugarte-Berzal E., Garcia-Marco J.A., del Cerro M.H., Van den Steen P.E., Opdenakker G., Terol M.J., Garcia-Pardo A. Alpha4beta1 integrin and 190-kDa CD44v constitute a cell surface docking complex for gelatinase B/MMP-9 in chronic leukemic but not in normal B cells. Blood 2008, 112:169-178.
81. Brooks P.C., Stromblad S., Sanders L.C., von Schalscha T.L., Aimes R.T., Stetler-Stevenson W.G., Quigley J.P., Cheresh D.A. Localization of matrix metalloproteinase MMP-2 to the surface of invasive cells by interaction with integrin alpha v beta 3. Cell 1996, 85:683-693.
82. Brooks P.C., Silletti S., von Schalscha T.L., Friedlander M., Cheresh D.A. Disruption of angiogenesis by PEX, a noncatalytic metalloproteinase fragment with integrin binding activity. Cell 1998, 92:391-400.
83. Menashi S., Dehem M., Souliac I., Legrand Y., Fridman R. Density-dependent regulation of cell-surface association of matrix metalloproteinase-2 (MMP-2) in breast-carcinoma cells. Int. J. Cancer 1998, 75:259-265.
84. Hofmann U.B., Westphal J.R., Van Kraats A.A., Ruiter D.J., Van Muijen G.N. Expression of integrin alpha(v)beta(3) correlates with activation of membrane-type matrix metalloproteinase-1 (MT1-MMP) and matrix metalloproteinase-2 (MMP-2) in human melanoma cells in vitro and in vivo. Int. J. Cancer 2000, 87:12-19.
85. Silletti S., Kessler T., Goldberg J., Boger D.L., Cheresh D.A. Disruption of matrix metalloproteinase 2 binding to integrin alpha vbeta 3 by an organic molecule inhibits angiogenesis and tumor growth in vivo. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:119-124.
86. Levkau B., Kenagy R.D., Karsan A., Weitkamp B., Clowes A.W., Ross R., Raines E.W. Activation of metalloproteinases and their association with integrins: an auxiliary apoptotic pathway in human endothelial cells. Cell Death Differ. 2002, 9:1360-1367.
87. Rolli M., Fransvea E., Pilch J., Saven A., Felding-Habermann B. Activated integrin alphavbeta3 cooperates with metalloproteinase MMP-9 in regulating migration of metastatic breast cancer cells. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:9482-9487.
88. Wang X.Q., Sun P., Paller A.S. Ganglioside GM3 inhibits matrix metalloproteinase-9 activation and disrupts its association with integrin. J. Biol. Chem. 2003, 278:25591-25599.
89. Bjorklund M., Heikkila P., Koivunen E. Peptide inhibition of catalytic and noncatalytic activities of matrix metalloproteinase-9 blocks tumor cell migration and invasion. J. Biol. Chem. 2004, 279:29589-29597.
90. Stefanidakis M., Bjorklund M., Ihanus E., Gahmberg C.G., Koivunen E. Identification of a negatively charged peptide motif within the catalytic domain of progelatinases that mediates binding to leukocyte beta 2 integrins. J. Biol. Chem. 2003, 278:34674-34684.
91. Stefanidakis M., Ruohtula T., Borregaard N., Gahmberg C.G., Koivunen E. Intracellular and cell surface localization of a complex between alphaMbeta2 integrin and promatrix metalloproteinase-9 progelatinase in neutrophils. J. Immunol. 2004, 172:7060-7068.
92. Rupp P.A., Visconti R.P., Czirok A., Cheresh D.A., Little C.D. Matrix metalloproteinase 2-integrin alpha(v)beta3 binding is required for mesenchymal cell invasive activity but not epithelial locomotion: a computational time-lapse study. Mol. Biol. Cell 2008, 19:5529-5540.
93. Chetty C., Lakka S.S., Bhoopathi P., Rao J.S. MMP-2 alters VEGF expression via alphaVbeta3 integrin-mediated PI3K/AKT signaling in A549 lung cancer cells. Int. J. Cancer 2010, 127:1081-1095.
94. Nisato R.E., Hosseini G., Sirrenberg C., Butler G.S., Crabbe T., Docherty A.J., Wiesner M., Murphy G., Overall C.M., Goodman S.L., Pepper M.S. Dissecting the role of matrix metalloproteinases (MMP) and integrin alpha(v)beta3 in angiogenesis in vitro: absence of hemopexin C domain bioactivity, but membrane-Type 1-MMP and alpha(v)beta3 are critical. Cancer Res. 2005, 65:9377-9387.
95. Hofmann U.B., Westphal J.R., Waas E.T., Becker J.C., Ruiter D.J., van Muijen G.N. Coexpression of integrin alpha(v)beta3 and matrix metalloproteinase-2 (MMP-2) coincides with MMP-2 activation: correlation with melanoma progression. J. Invest. Dermatol. 2000, 115:625-632.
96. Redondo-Munoz J., Ugarte-Berzal E., Terol M.J., Van den Steen P.E., Hernandez del Cerro M., Roderfeld M., Roeb E., Opdenakker G., Garcia-Marco J.A., Garcia-Pardo A. Matrix metalloproteinase-9 promotes chronic lymphocytic leukemia b cell survival through its hemopexin domain. Cancer Cell 2010, 17:160-172.
97. Hu X., Paik P.K., Chen J., Yarilina A., Kockeritz L., Lu T.T., Woodgett J.R., Ivashkiv L.B. IFN-gamma suppresses IL-10 production and synergizes with TLR2 by regulating GSK3 and CREB/AP-1 proteins. Immunity 2006, 24:563-574.
98. Rao J.S., Bhoopathi P., Chetty C., Gujrati M., Lakka S.S. MMP-9 short interfering RNA induced senescence resulting in inhibition of medulloblastoma growth via p16(INK4a) and mitogen-activated protein kinase pathway. Cancer Res. 2007, 67:4956-4964.
99. Bhoopathi P., Chetty C., Kunigal S., Vanamala S.K., Rao J.S., Lakka S.S. Blockade of tumor growth due to matrix metalloproteinase-9 inhibition is mediated by sequential activation of beta1-integrin, ERK, and NF-kappaB. J. Biol. Chem. 2008, 283:1545-1552.
100. Bauvois B., Dumont J., Mathiot C., Kolb J.P. Production of matrix metalloproteinase-9 in early stage B-CLL: suppression by interferons. Leukemia 2002, 16:791-798.
101. Chen L.S., Balakrishnan K., Gandhi V. Inflammation and survival pathways: chronic lymphocytic leukemia as a model system. Biochem. Pharmacol. 2010, 80:1936-1945.
102. Wheeler D.L., Dunn E.F., Harari P.M. Understanding resistance to EGFR inhibitors-impact on future treatment strategies. Nat. Rev. Clin. Oncol. 2010, 7:493-507.
103. Frame M.C., Patel H., Serrels B., Lietha D., Eck M.J. The FERM domain: organizing the structure and function of FAK. Nat. Rev. Mol. Cell Biol. 2010, 11:802-814.
104. Conant K., St Hillaire C., Nagase H., Visse R., Gary D., Haughey N., Anderson C., Turchan J., Nath A. Matrix metalloproteinase 1 interacts with neuronal integrins and stimulates dephosphorylation of Akt. J. Biol. Chem. 2004, 279:8056-8062.
105. Dumin J.A., Dickeson S.K., Stricker T.P., Bhattacharyya-Pakrasi M., Roby J.D., Santoro S.A., Parks W.C. Pro-collagenase-1 (matrix metalloproteinase-1) binds the alpha(2)beta(1) integrin upon release from keratinocytes migrating on type I collagen. J. Biol. Chem. 2001, 276:29368-29374.
106. Mauch S., Kolb C., Kolb B., Sadowski T., Sedlacek R. Matrix metalloproteinase-19 is expressed in myeloid cells in an adhesion-dependent manner and associates with the cell surface. J. Immunol. 2002, 168:1244-1251.
107. Overall C.M., Lopez-Otin C. Strategies for MMP inhibition in cancer: innovations for the post-trial era. Nat. Rev. Cancer 2002, 2:657-672.
108. Sela-Passwell N., Rosenblum G., Shoham T., Sagi I. Structural and functional bases for allosteric control of MMP activities: can it pave the path for selective inhibition?. Biochim. Biophys. Acta 2010, 1803:29-38.
109. Mantuano E., Inoue G., Li X., Takahashi K., Gaultier A., Gonias S.L., Campana W.M. The hemopexin domain of matrix metalloproteinase-9 activates cell signaling and promotes migration of Schwann cells by binding to low-density lipoprotein receptor-related protein. J. Neurosci. 2008, 28:11571-11582.