Matrix Metalloproteinases: Regulators of the Tumor Microenvironment

Cell

Volumn 141, Issue 1, 2010, Pages 52-67

  Kessenbrock, Kai ^a   Plaks, Vicki ^a   Werb, Zena ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAM PROTEIN; ALPHA2 INTEGRIN ANTIBODY; BATIMASTAT; COLLAGENASE 3; CXCL1 CHEMOKINE; EPIDERMAL GROWTH FACTOR RECEPTOR; GELATINASE A; GELATINASE B; INTERLEUKIN 8; INTERSTITIAL COLLAGENASE; MATRILYSIN; MATRIX METALLOPROTEINASE; MATRIX METALLOPROTEINASE 20; MATRIX METALLOPROTEINASE INHIBITOR; METALLOPROTEINASE; STROMELYSIN; STROMELYSIN 2; TISSUE INHIBITOR OF METALLOPROTEINASE 1; UNCLASSIFIED DRUG;

ADIPOCYTE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; BREAST CANCER; CANCER CELL; CANCER GROWTH; CELL MIGRATION; COLON CANCER; DRUG PROTEIN BINDING; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; ENZYME REGULATION; ENZYME STRUCTURE; EXTRACELLULAR MATRIX; HUMAN; IMMUNOPATHOGENESIS; INFLAMMATION; LEUKOCYTE ACTIVATION; LUNG CANCER; LYMPHANGIOGENESIS; MALIGNANT TRANSFORMATION; METASTASIS; NONHUMAN; OVARY CANCER; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN DEGRADATION; REVIEW; SIGNAL TRANSDUCTION; TUMOR IMMUNITY; TUMOR MICROENVIRONMENT; TUMOR VASCULARIZATION;

EID: 77950931419     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2010.03.015     Document Type: Review

References (132)

1. Agrawal S., Anderson P., Durbeej M., van Rooijen N., Ivars F., Opdenakker G., Sorokin L.M. Dystroglycan is selectively cleaved at the parenchymal basement membrane at sites of leukocyte extravasation in experimental autoimmune encephalomyelitis. J. Exp. Med. 2006, 203:1007-1019.
2. Ahn G.O., Brown J.M. Matrix metalloproteinase-9 is required for tumor vasculogenesis but not for angiogenesis: Role of bone marrow-derived myelomonocytic cells. Cancer Cell 2008, 13:193-205.
3. Alexander C.M., Selvarajan S., Mudgett J., Werb Z. Stromelysin-1 regulates adipogenesis during mammary gland involution. J. Cell Biol. 2001, 152:693-703.
4. Ardi V.C., Kupriyanova T.A., Deryugina E.I., Quigley J.P. Human neutrophils uniquely release TIMP-free MMP-9 to provide a potent catalytic stimulator of angiogenesis. Proc. Natl. Acad. Sci. USA 2007, 104:20262-20267.
5. 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.
6. Balbin M., Fueyo A., Tester A.M., Pendas A.M., Pitiot A.S., Astudillo A., Overall C.M., Shapiro S.D., Lopez-Otin C. Loss of collagenase-2 confers increased skin tumor susceptibility to male mice. Nat. Genet. 2003, 35:252-257.
7. Balkwill F. Tumour necrosis factor and cancer. Nat. Rev. Cancer 2009, 9:361-371.
8. Bergers G., Brekken R., McMahon G., Vu T.H., Itoh T., Tamaki K., Tanzawa K., Thorpe P., Itohara S., Werb Z., et al. Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis. Nat. Cell Biol. 2000, 2:737-744.
9. Bild A.H., Yao G., Chang J.T., Wang Q., Potti A., Chasse D., Joshi M.B., Harpole D., Lancaster J.M., Berchuck A., et al. Oncogenic pathway signatures in human cancers as a guide to targeted therapies. Nature 2006, 439:353-357.
10. Boire A., Covic L., Agarwal A., Jacques S., Sherifi S., Kuliopulos A. PAR1 is a matrix metalloprotease-1 receptor that promotes invasion and tumorigenesis of breast cancer cells. Cell 2005, 120:303-313.
11. Bond M., Fabunmi R.P., Baker A.H., Newby A.C. Synergistic upregulation of metalloproteinase-9 by growth factors and inflammatory cytokines: an absolute requirement for transcription factor NF-kappa B. FEBS Lett. 1998, 435:29-34.
12. Bremer C., Tung C.H., Weissleder R. In vivo molecular target assessment of matrix metalloproteinase inhibition. Nat. Med. 2001, 7:743-748.
13. Brinkmann V., Reichard U., Goosmann C., Fauler B., Uhlemann Y., Weiss D.S., Weinrauch Y., Zychlinsky A. Neutrophil extracellular traps kill bacteria. Science 2004, 303:1532-1535.
14. Bruyere F., Melen-Lamalle L., Blacher S., Roland G., Thiry M., Moons L., Frankenne F., Carmeliet P., Alitalo K., Libert C., et al. Modeling lymphangiogenesis in a three-dimensional culture system. Nat. Methods 2008, 5:431-437.
15. Burns J.M., Summers B.C., Wang Y., Melikian A., Berahovich R., Miao Z., Penfold M.E., Sunshine M.J., Littman D.R., Kuo C.J., et al. A novel chemokine receptor for SDF-1 and I-TAC involved in cell survival, cell adhesion, and tumor development. J. Exp. Med. 2006, 203:2201-2213.
16. Butcher D.T., Alliston T., Weaver V.M. A tense situation: forcing tumour progression. Nat. Rev. Cancer 2009, 9:108-122.
17. Chun T.H., Hotary K.B., Sabeh F., Saltiel A.R., Allen E.D., Weiss S.J. A pericellular collagenase directs the 3-dimensional development of white adipose tissue. Cell 2006, 125:577-591.
18. 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.
19. Cornelius L.A., Nehring L.C., Harding E., Bolanowski M., Welgus H.G., Kobayashi D.K., Pierce R.A., Shapiro S.D. Matrix metalloproteinases generate angiostatin: effects on neovascularization. J. Immunol. 1998, 161:6845-6852.
20. Coussens L.M., Werb Z. Inflammation and cancer. Nature 2002, 420:860-867.
21. Coussens L.M., Fingleton B., Matrisian L.M. Matrix metalloproteinase inhibitors and cancer: trials and tribulations. Science 2002, 295:2387-2392.
22. Cowden Dahl K.D., Symowicz J., Ning Y., Gutierrez E., Fishman D.A., Adley B.P., Stack M.S., Hudson L.G. Matrix metalloproteinase 9 is a mediator of epidermal growth factor-dependent e-cadherin loss in ovarian carcinoma cells. Cancer Res. 2008, 68:4606-4613.
23. Cox J.H., Dean R.A., Roberts C.R., Overall C.M. Matrix metalloproteinase processing of CXCL11/I-TAC results in loss of chemoattractant activity and altered glycosaminoglycan binding. J. Biol. Chem. 2008, 283:19389-19399.
24. Crawford H.C., Scoggins C.R., Washington M.K., Matrisian L.M., Leach S.D. Matrix metalloproteinase-7 is expressed by pancreatic cancer precursors and regulates acinar-to-ductal metaplasia in exocrine pancreas. J. Clin. Invest. 2002, 109:1437-1444.
25. Cuniasse P., Dev L., Makaritis A., Beau F., Georgiadis D., Matziari M., Yiotakis A., Dive V. Future challenges facing the development of specific active-site-directed synthetic inhibitors of MMPs. Biochimie 2005, 87:393-402.
26. Dallas S.L., Rosser J.L., Mundy G.R., Bonewald L.F. Proteolysis of latent transforming growth factor-beta (TGF-beta)-binding protein-1 by osteoclasts. A cellular mechanism for release of TGF-beta from bone matrix. J. Biol. Chem. 2002, 277:21352-21360.
27. de Visser K.E., Eichten A., Coussens L.M. Paradoxical roles of the immune system during cancer development. Nat. Rev. Cancer 2006, 6:24-37.
28. Deryugina E.I., Quigley J.P. Matrix metalloproteinases and tumor metastasis. Cancer Metastasis Rev. 2006, 25:9-34.
29. Du R., Lu K.V., Petritsch C., Liu P., Ganss R., Passegue E., Song H., Vandenberg S., Johnson R.S., Werb Z., et al. HIF1alpha induces the recruitment of bone marrow-derived vascular modulatory cells to regulate tumor angiogenesis and invasion. Cancer Cell 2008, 13:206-220.
30. 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.
31. Edwards D.R., Handsley M.M., Pennington C.J. The ADAM metalloproteinases. Mol. Aspects Med. 2008, 29:258-289.
32. Egeblad M., Werb Z. New functions for the matrix metalloproteinases in cancer progression. Nat. Rev. Cancer 2002, 2:161-174.
33. Egeblad M., Ewald A.J., Askautrud H.A., Truitt M.L., Welm B.E., Bainbridge E., Peeters G., Krummel M.F., Werb Z. Visualizing stromal cell dynamics in different tumor microenvironments by spinning disk confocal microscopy. Dis. Model. Mech. 2008, 1:155-167.
34. Erler J.T., Bennewith K.L., Cox T.R., Lang G., Bird D., Koong A., Le Q.T., Giaccia A.J. Hypoxia-induced lysyl oxidase is a critical mediator of bone marrow cell recruitment to form the premetastatic niche. Cancer Cell 2009, 15:35-44.
35. Friedl P., Wolf K. Tube travel: the role of proteases in individual and collective cancer cell invasion. Cancer Res. 2008, 68:7247-7249.
36. Fu X., Kassim S.Y., Parks W.C., Heinecke J.W. 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. 2003, 278:28403-28409.
37. Furumoto S., Takashima K., Kubota K., Ido T., Iwata R., Fukuda H. Tumor detection using 18F-labeled matrix metalloproteinase-2 inhibitor. Nucl. Med. Biol. 2003, 30:119-125.
38. Galvez B.G., Matias-Roman S., Albar J.P., Sanchez-Madrid F., Arroyo A.G. Membrane type 1-matrix metalloproteinase is activated during migration of human endothelial cells and modulates endothelial motility and matrix remodeling. J. Biol. Chem. 2001, 276:37491-37500.
39. Glasheen B.M., Kabra A.T., Page-McCaw A. Distinct functions for the catalytic and hemopexin domains of a Drosophila matrix metalloproteinase. Proc. Natl. Acad. Sci. USA 2009, 106:2659-2664.
40. Gross J., Lapiere C.M. Collagenolytic activity in amphibian tissues: a tissue culture assay. Proc. Natl. Acad. Sci. USA 1962, 48:1014-1022.
41. Gutierrez-Fernandez A., Inada M., Balbin M., Fueyo A., Pitiot A.S., Astudillo A., Hirose K., Hirata M., Shapiro S.D., Noel A., et al. Increased inflammation delays wound healing in mice deficient in collagenase-2 (MMP-8). FASEB J. 2007, 21:2580-2591.
42. Gutierrez-Fernandez A., Fueyo A., Folgueras A.R., Garabaya C., Pennington C.J., Pilgrim S., Edwards D.R., Holliday D.L., Jones J.L., Span P.N., et al. Matrix metalloproteinase-8 functions as a metastasis suppressor through modulation of tumor cell adhesion and invasion. Cancer Res. 2008, 68:2755-2763.
43. 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.
44. Hanahan D., Weinberg R.A. The hallmarks of cancer. Cell 2000, 100:57-70.
45. Haro H., Crawford H.C., Fingleton B., Shinomiya K., Spengler D.M., Matrisian L.M. Matrix metalloproteinase-7-dependent release of tumor necrosis factor-alpha in a model of herniated disc resorption. J. Clin. Invest. 2000, 105:143-150.
46. Heissig B., Hattori K., Dias S., Friedrich M., Ferris B., Hackett N.R., Crystal R.G., Besmer P., Lyden D., Moore M.A., et al. Recruitment of stem and progenitor cells from the bone marrow niche requires MMP-9 mediated release of kit-ligand. Cell 2002, 109:625-637.
47. 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.
48. Hiratsuka S., Watanabe A., Aburatani H., Maru Y. Tumour-mediated upregulation of chemoattractants and recruitment of myeloid cells predetermines lung metastasis. Nat. Cell Biol. 2006, 8:1369-1375.
49. Hiratsuka S., Watanabe A., Sakurai Y., Akashi-Takamura S., Ishibashi S., Miyake K., Shibuya M., Akira S., Aburatani H., Maru Y. The S100A8-serum amyloid A3-TLR4 paracrine cascade establishes a pre-metastatic phase. Nat. Cell Biol. 2008, 10:1349-1355.
50. Houghton A.M., Grisolano J.L., Baumann M.L., Kobayashi D.K., Hautamaki R.D., Nehring L.C., Cornelius L.A., Shapiro S.D. Macrophage elastase (matrix metalloproteinase-12) suppresses growth of lung metastases. Cancer Res. 2006, 66:6149-6155.
51. Houghton A.M., Quintero P.A., Perkins D.L., Kobayashi D.K., Kelley D.G., Marconcini L.A., Mecham R.P., Senior R.M., Shapiro S.D. Elastin fragments drive disease progression in a murine model of emphysema. J. Clin. Invest. 2006, 116:753-759.
52. Houghton A.M., Hartzell W.O., Robbins C.S., Gomis-Ruth F.X., Shapiro S.D. Macrophage elastase kills bacteria within murine macrophages. Nature 2009, 460:637-641.
53. Huang Y., Song N., Ding Y., Yuan S., Li X., Cai H., Shi H., Luo Y. Pulmonary vascular destabilization in the premetastatic phase facilitates lung metastasis. Cancer Res. 2009, 69:7529-7537.
54. Hynes N.E., Lane H.A. ERBB receptors and cancer: the complexity of targeted inhibitors. Nat. Rev. Cancer 2005, 5:341-354.
55. Islekel H., Oktay G., Terzi C., Canda A.E., Fuzun M., Kupelioglu A. Matrix metalloproteinase-9,-3 and tissue inhibitor of matrix metalloproteinase-1 in colorectal cancer: relationship to clinicopathological variables. Cell Biochem. Funct. 2007, 25:433-441.
56. Jastrzebska B., Lebel R., Therriault H., McIntyre J.O., Escher E., Guerin B., Paquette B., Neugebauer W.A., Lepage M. New enzyme-activated solubility-switchable contrast agent for magnetic resonance imaging: from synthesis to in vivo imaging. J. Med. Chem. 2009, 52:1576-1581.
57. Jiang T., Olson E.S., Nguyen Q.T., Roy M., Jennings P.A., Tsien R.Y. Tumor imaging by means of proteolytic activation of cell-penetrating peptides. Proc. Natl. Acad. Sci. USA 2004, 101:17867-17872.
58. Kalluri R., Weinberg R.A. The basics of epithelial-mesenchymal transition. J. Clin. Invest. 2009, 119:1420-1428.
59. Kang Y., Siegel P.M., Shu W., Drobnjak M., Kakonen S.M., Cordon-Cardo C., Guise T.A., Massague J. A multigenic program mediating breast cancer metastasis to bone. Cancer Cell 2003, 3:537-549.
60. Kaplan R.N., Riba R.D., Zacharoulis S., Bramley A.H., Vincent L., Costa C., MacDonald D.D., Jin D.K., Shido K., Kerns S.A., et al. VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche. Nature 2005, 438:820-827.
61. Kessenbrock K., Krumbholz M., Schonermarck U., Back W., Gross W.L., Werb Z., Grone H.J., Brinkmann V., Jenne D.E. Netting neutrophils in autoimmune small-vessel vasculitis. Nat. Med. 2009, 15:623-625.
62. Langenskiold M., Holmdahl L., Falk P., Ivarsson M.L. Increased plasma MMP-2 protein expression in lymph node-positive patients with colorectal cancer. Int. J. Colorectal Dis. 2005, 20:245-252.
63. Le Maux Chansac B., Misse D., Richon C., Vergnon I., Kubin M., Soria J.C., Moretta A., Chouaib S., Mami-Chouaib F. Potentiation of NK cell-mediated cytotoxicity in human lung adenocarcinoma: role of NKG2D-dependent pathway. Int. Immunol. 2008, 20:801-810.
64. Lee S., Jilani S.M., Nikolova G.V., Carpizo D., Iruela-Arispe M.L. Processing of VEGF-A by matrix metalloproteinases regulates bioavailability and vascular patterning in tumors. J. Cell Biol. 2005, 169:681-691.
65. Levental K.R., Yu H., Kass L., Lakins J.N., Egeblad M., Erler J.T., Fong S.F., Csiszar K., Giaccia A., Weninger W., et al. Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 2009, 139:891-906.
66. Li Q., Park P.W., Wilson C.L., Parks W.C. Matrilysin shedding of syndecan-1 regulates chemokine mobilization and transepithelial efflux of neutrophils in acute lung injury. Cell 2002, 111:635-646.
67. Lijnen H.R., Van Hoef B., Collen D. Inactivation of the serpin alpha(2)-antiplasmin by stromelysin-1. Biochim. Biophys. Acta 2001, 1547:206-213.
68. Lin W.W., Karin M. A cytokine-mediated link between innate immunity, inflammation, and cancer. J. Clin. Invest. 2007, 117:1175-1183.
69. Liotta L.A., Tryggvason K., Garbisa S., Hart I., Foltz C.M., Shafie S. Metastatic potential correlates with enzymatic degradation of basement membrane collagen. Nature 1980, 284:67-68.
70. Littlepage L.E., Sternlicht M.D., Rougier N., Phillips J., Gallo E., Yu Y., Williams K., Brenot A., Gordon J.I., Werb Z. Matrix metalloproteinases contribute distinct roles in neuroendocrine prostate carcinogenesis, metastasis, and angiogenesis progression. Cancer Res. 2010, 70:2224-2234.
71. Liu H., Zhang T., Li X., Huang J., Wu B., Huang X., Zhou Y., Zhu J., Hou J. Predictive value of MMP-7 expression for response to chemotherapy and survival in patients with non-small cell lung cancer. Cancer Sci. 2008, 99:2185-2192.
72. Liu S., Wang H., Currie B.M., Molinolo A., Leung H.J., Moayeri M., Basile J.R., Alfano R.W., Gutkind J.S., Frankel A.E., et al. Matrix metalloproteinase-activated anthrax lethal toxin demonstrates high potency in targeting tumor vasculature. J. Biol. Chem. 2008, 283:529-540.
73. Liu Z., Zhou X., Shapiro S.D., Shipley J.M., Twining S.S., Diaz L.A., Senior R.M., Werb Z. The serpin alpha1-proteinase inhibitor is a critical substrate for gelatinase B/MMP-9 in vivo. Cell 2000, 102:647-655.
74. Lochter A., Galosy S., Muschler J., Freedman N., Werb Z., Bissell M.J. Matrix metalloproteinase stromelysin-1 triggers a cascade of molecular alterations that leads to stable epithelial-to-mesenchymal conversion and a premalignant phenotype in mammary epithelial cells. J. Cell Biol. 1997, 139:1861-1872.
75. Lopez-Otin C., Matrisian L.M. Emerging roles of proteases in tumour suppression. Nat. Rev. Cancer 2007, 7:800-808.
76. Lu X., Wang Q., Hu G., Van Poznak C., Fleisher M., Reiss M., Massague J., Kang Y. ADAMTS1 and MMP1 proteolytically engage EGF-like ligands in an osteolytic signaling cascade for bone metastasis. Genes Dev. 2009, 23:1882-1894.
77. Luo J.L., Maeda S., Hsu L.C., Yagita H., Karin M. Inhibition of NF-kappaB in cancer cells converts inflammation-induced tumor growth mediated by TNFalpha to TRAIL-mediated tumor regression. Cancer Cell 2004, 6:297-305.
78. Lynch C.C., Hikosaka A., Acuff H.B., Martin M.D., Kawai N., Singh R.K., Vargo-Gogola T.C., Begtrup J.L., Peterson T.E., Fingleton B., et al. MMP-7 promotes prostate cancer-induced osteolysis via the solubilization of RANKL. Cancer Cell 2005, 7:485-496.
79. Manicone A.M., McGuire J.K. Matrix metalloproteinases as modulators of inflammation. Semin. Cell Dev. Biol. 2008, 19:34-41.
80. Maretzky T., Reiss K., Ludwig A., Buchholz J., Scholz F., Proksch E., de Strooper B., Hartmann D., Saftig P. ADAM10 mediates E-cadherin shedding and regulates epithelial cell-cell adhesion, migration, and beta-catenin translocation. Proc. Natl. Acad. Sci. USA 2005, 102:9182-9187.
81. Massague J. TGFbeta in Cancer. Cell 2008, 134:215-230.
82. McQuibban G.A., Gong J.H., Wong J.P., Wallace J.L., Clark-Lewis I., Overall C.M. Matrix metalloproteinase processing of monocyte chemoattractant proteins generates CC chemokine receptor antagonists with anti-inflammatory properties in vivo. Blood 2002, 100:1160-1167.
83. Mentzel T., Brown L.F., Dvorak H.F., Kuhnen C., Stiller K.J., Katenkamp D., Fletcher C.D. The association between tumour progression and vascularity in myxofibrosarcoma and myxoid/round cell liposarcoma. Virchows Arch. 2001, 438:13-22.
84. Mitsiades N., Yu W.H., Poulaki V., Tsokos M., Stamenkovic I. Matrix metalloproteinase-7-mediated cleavage of Fas ligand protects tumor cells from chemotherapeutic drug cytotoxicity. Cancer Res. 2001, 61:577-581.
85. Motrescu E.R., Rio M.C. Cancer cells, adipocytes and matrix metalloproteinase 11: a vicious tumor progression cycle. Biol. Chem. 2008, 389:1037-1041.
86. Mu D., Cambier S., Fjellbirkeland L., Baron J.L., Munger J.S., Kawakatsu H., Sheppard D., Broaddus V.C., Nishimura S.L. The integrin alpha(v)beta8 mediates epithelial homeostasis through MT1-MMP-dependent activation of TGF-beta1. J. Cell Biol. 2002, 157:493-507.
87. Murphy G. The ADAMs: signalling scissors in the tumour microenvironment. Nat. Rev. Cancer 2008, 8:932-941.
88. Nagase H., Visse R., Murphy G. Structure and function of matrix metalloproteinases and TIMPs. Cardiovasc. Res. 2006, 69:562-573.
89. Nakamura E.S., Koizumi K., Kobayashi M., Saiki I. Inhibition of lymphangiogenesis-related properties of murine lymphatic endothelial cells and lymph node metastasis of lung cancer by the matrix metalloproteinase inhibitor MMI270. Cancer Sci. 2004, 95:25-31.
90. Nozawa H., Chiu C., Hanahan D. Infiltrating neutrophils mediate the initial angiogenic switch in a mouse model of multistage carcinogenesis. Proc. Natl. Acad. Sci. USA 2006, 103:12493-12498.
91. Olson E.S., Aguilera A.T., Jiang T., Ellies L.G., Nguyen Q.T., Wong E.H., Gross L.A., Tsien R.Y. In vivo characterization of activatable cell penetrating pepides for targeting protease activity in cancer. Integrative Biol. 2009, 1:382-393.
92. Packard B.Z., Artym V.V., Komoriya A., Yamada K.M. Direct visualization of protease activity on cells migrating in three-dimensions. Matrix Biol. 2009, 28:3-10.
93. Padera T.P., Kadambi A., di Tomaso E., Carreira C.M., Brown E.B., Boucher Y., Choi N.C., Mathisen D., Wain J., Mark E.J., et al. Lymphatic metastasis in the absence of functional intratumor lymphatics. Science 2002, 296:1883-1886.
94. Page-McCaw A., Ewald A.J., Werb Z. Matrix metalloproteinases and the regulation of tissue remodelling. Nat. Rev. Mol. Cell Biol. 2007, 8:221-233.
95. Palavalli L.H., Prickett T.D., Wunderlich J.R., Wei X., Burrell A.S., Porter-Gill P., Davis S., Wang C., Cronin J.C., Agrawal N.S., et al. Analysis of the matrix metalloproteinase family reveals that MMP8 is often mutated in melanoma. Nat. Genet. 2009, 41:518-520.
96. Parks W.C., Wilson C.L., Lopez-Boado Y.S. Matrix metalloproteinases as modulators of inflammation and innate immunity. Nat. Rev. Immunol. 2004, 4:617-629.
97. Patterson B.C., Sang Q.A. Angiostatin-converting enzyme activities of human matrilysin (MMP-7) and gelatinase B/type IV collagenase (MMP-9). J. Biol. Chem. 1997, 272:28823-28825.
98. Pinilla S., Alt E., Abdul Khalek F.J., Jotzu C., Muehlberg F., Beckmann C., Song Y.H. Tissue resident stem cells produce CCL5 under the influence of cancer cells and thereby promote breast cancer cell invasion. Cancer Lett. 2009, 284:80-85.
99. Radisky D.C., Levy D.D., Littlepage L.E., Liu H., Nelson C.M., Fata J.E., Leake D., Godden E.L., Albertson D.G., Nieto M.A., et al. Rac1b and reactive oxygen species mediate MMP-3-induced EMT and genomic instability. Nature 2005, 436:123-127.
100. 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.
101. Ribatti D. Endogenous inhibitors of angiogenesis: a historical review. Leuk. Res. 2009, 33:638-644.
102. Rocks N., Paulissen G., Quesada-Calvo F., Munaut C., Gonzalez M.L., Gueders M., Hacha J., Gilles C., Foidart J.M., Noel A., et al. ADAMTS-1 metalloproteinase promotes tumor development through the induction of a stromal reaction in vivo. Cancer Res. 2008, 68:9541-9550.
103. Rozanov D.V., Sikora S., Godzik A., Postnova T.I., Golubkov V., Savinov A., Tomlinson S., Strongin A.Y. Non-proteolytic, receptor/ligand interactions associate cellular membrane type-1 matrix metalloproteinase with the complement component C1q. J. Biol. Chem. 2004, 279:50321-50328.
104. 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.
105. Rutkowski J.M., Davis K.E., Scherer P.E. Mechanisms of obesity and related pathologies: the macro- and microcirculation of adipose tissue. FEBS J. 2009, 276:5738-5746.
106. Sabeh F., Ota I., Holmbeck K., Birkedal-Hansen H., Soloway P., Balbin M., Lopez-Otin C., Shapiro S., Inada M., Krane S., et al. Tumor cell traffic through the extracellular matrix is controlled by the membrane-anchored collagenase MT1-MMP. J. Cell Biol. 2004, 167:769-781.
107. Sabeh F., Shimizu-Hirota R., Weiss S.J. Protease-dependent versus -independent cancer cell invasion programs: three-dimensional amoeboid movement revisited. J. Cell Biol. 2009, 185:11-19.
108. Sakamoto T., Seiki M. Cytoplasmic tail of MT1-MMP regulates macrophage motility independently from its protease activity. Genes Cells 2009, 14:617-626.
109. Schafers M., Riemann B., Kopka K., Breyholz H.J., Wagner S., Schafers K.P., Law M.P., Schober O., Levkau B. Scintigraphic imaging of matrix metalloproteinase activity in the arterial wall in vivo. Circulation 2004, 109:2554-2559.
110. Scherer R.L., McIntyre J.O., Matrisian L.M. Imaging matrix metalloproteinases in cancer. Cancer Metastasis Rev. 2008, 27:679-690.
111. Scherer R.L., VanSaun M.N., McIntyre J.O., Matrisian L.M. Optical imaging of matrix metalloproteinase-7 activity in vivo using a proteolytic nanobeacon. Mol. Imaging 2008, 7:118-131.
112. Schulte M., Reiss K., Lettau M., Maretzky T., Ludwig A., Hartmann D., de Strooper B., Janssen O., Saftig P. ADAM10 regulates FasL cell surface expression and modulates FasL-induced cytotoxicity and activation-induced cell death. Cell Death Differ. 2007, 14:1040-1049.
113. Smith M.L., Gourdon D., Little W.C., Kubow K.E., Eguiluz R.A., Luna-Morris S., Vogel V. Force-induced unfolding of fibronectin in the extracellular matrix of living cells. PLoS Biol. 2007, 5:e268.
114. Sounni N.E., Dehne K., van Kempen L.L.C.L., Egeblad M., Affara N., Cuevas I., Wiesen J., Junankar J., Korets L., Lee L., et al. Stromal regulation of vessel stability by MMP9 and TGFβ. Dis. Model. Mech. 2010, Published online March 11, 2010. 10.1242/dmm.00386.3.
115. Sternlicht M.D., Werb Z. How matrix metalloproteinases regulate cell behavior. Annu. Rev. Cell Dev. Biol. 2001, 17:463-516.
116. Sternlicht M.D., Lochter A., Sympson C.J., Huey B., Rougier J.P., Gray J.W., Pinkel D., Bissell M.J., Werb Z. The stromal proteinase MMP3/stromelysin-1 promotes mammary carcinogenesis. Cell 1999, 98:137-146.
117. Strongin A.Y., Collier I., Bannikov G., Marmer B.L., Grant G.A., 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. 1995, 270:5331-5338.
118. Struyf S., Proost P., Vandercappellen J., Dempe S., Noyens B., Nelissen S., Gouwy M., Locati M., Opdenakker G., Dinsart C., et al. Synergistic up-regulation of MCP-2/CCL8 activity is counteracted by chemokine cleavage, limiting its inflammatory and anti-tumoral effects. Eur. J. Immunol. 2009, 39:843-857.
119. Tatti O., Vehvilainen P., Lehti K., Keski-Oja J. MT1-MMP releases latent TGF-beta1 from endothelial cell extracellular matrix via proteolytic processing of LTBP-1. Exp. Cell Res. 2008, 314:2501-2514.
120. Temma T., Sano K., Kuge Y., Kamihashi J., Takai N., Ogawa Y., Saji H. Development of a radiolabeled probe for detecting membrane type-1 matrix metalloproteinase on malignant tumors. Biol. Pharm. Bull. 2009, 32:1272-1277.
121. 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.
122. Waldhauer I., Goehlsdorf D., Gieseke F., Weinschenk T., Wittenbrink M., Ludwig A., Stevanovic S., Rammensee H.G., Steinle A. Tumor-associated MICA is shed by ADAM proteases. Cancer Res. 2008, 68:6368-6376.
123. Weathington N.M., van Houwelingen A.H., Noerager B.D., Jackson P.L., Kraneveld A.D., Galin F.S., Folkerts G., Nijkamp F.P., Blalock J.E. A novel peptide CXCR ligand derived from extracellular matrix degradation during airway inflammation. Nat. Med. 2006, 12:317-323.
124. Weiss S.J., Peppin G., Ortiz X., Ragsdale C., Test S.T. Oxidative autoactivation of latent collagenase by human neutrophils. Science 1985, 227:747-749.
125. Witters L., Scherle P., Friedman S., Fridman J., Caulder E., Newton R., Lipton A. Synergistic inhibition with a dual epidermal growth factor receptor/HER-2/neu tyrosine kinase inhibitor and a disintegrin and metalloprotease inhibitor. Cancer Res. 2008, 68:7083-7089.
126. Woessner J.F., Nagase H. Matrix Metalloproteinases and TIMPs 2000, Oxford University Press, New York.
127. Wolf K., Wu Y.I., Liu Y., Geiger J., Tam E., Overall C., Stack M.S., Friedl P. Multi-step pericellular proteolysis controls the transition from individual to collective cancer cell invasion. Nat. Cell Biol. 2007, 9:893-904.
128. Wu Y., Smas C.M. Wdnm1-like, a new adipokine with a role in MMP-2 activation. Am. J. Physiol. Endocrinol. Metab. 2008, 295:E205-E215.
129. Wyckoff J., Wang W., Lin E.Y., Wang Y., Pixley F., Stanley E.R., Graf T., Pollard J.W., Segall J., Condeelis J. A paracrine loop between tumor cells and macrophages is required for tumor cell migration in mammary tumors. Cancer Res. 2004, 64:7022-7029.
130. Yeh W.L., Lu D.Y., Lee M.J., Fu W.M. Leptin induces migration and invasion of glioma cells through MMP-13 production. Glia 2009, 57:454-464.
131. 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.
132. Zhang X., Halvorsen K., Zhang C.Z., Wong W.P., Springer T.A. Mechanoenzymatic cleavage of the ultralarge vascular protein von Willebrand factor. Science 2009, 324:1330-1334.