Cancer invasion and metastasis: Changing views

Journal of Pathology

Volumn 214, Issue 3, 2008, Pages 283-293

  Duffy, M J ^a,b   McGowan, P M ^a,b   Gallagher, W M ^b  

^a ST VINCENT S UNIVERSITY HOSPITAL   (Ireland)

^b UNIVERSITY COLLEGE DUBLIN   (Ireland)

Author keywords

Cancer; Invasion; Metalloproteinase; Metastasis; Progression

Indexed keywords

ANTIMETASTATIC AGENT; BEVACIZUMAB; ENDOSTATIN; FLUOROURACIL; GENE PRODUCT; MATRIX METALLOPROTEINASE; MATRIX METALLOPROTEINASE INHIBITOR; PAI 1 PROTEIN; PROTEINASE; PROTEINASE INHIBITOR; SERINE PROTEINASE INHIBITOR; SORAFENIB; SUNITINIB; TISSUE INHIBITOR OF METALLOPROTEINASE 1; UNCLASSIFIED DRUG; UROKINASE;

ANGIOGENESIS; ANTINEOPLASTIC ACTIVITY; BLEEDING; CANCER INVASION; CARCINOGENESIS; CELL MIGRATION; CELL MOTILITY; CELL PROLIFERATION; COLORECTAL CANCER; EXTRACELLULAR MATRIX; GENE ACTIVATION; GENE FUNCTION; HUMAN; HYPERTENSION; INTESTINE PERFORATION; METASTASIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; THROMBOEMBOLISM; TUMOR CELL; TUMOR GROWTH; WOUND HEALING;

EXTRACELLULAR MATRIX PROTEINS; GENE EXPRESSION REGULATION, NEOPLASTIC; GENETIC MARKERS; HUMANS; MATRIX METALLOPROTEINASES; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; SERINE PROTEINASE INHIBITORS;

EID: 38949143636     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.2282     Document Type: Review

References (117)

1. Steeg PS. Tumor metastasis: mechanistic insights and clinical challenges. Nature Med 2006;12:895-904.
2. Chambers AF, Groom AC, MacDonald IC. Dissemination and growth of cancer cells in metastatic sites. Nature Rev Cancer 2002;2:563-572.
3. Hahn WC, Weinberg RA. Rules for making human tumor cells. N Engl J Med 2002;347:1593-1603.
4. Vogelstein B, Kinzler KW. Cancer genes and the pathways they control. Nature Med 2004;10:789-799.
5. Duffy MJ. The biochemistry of metastasis. Adv Clin Chem 1996;32:135-166.
6. Poste G, Fidler IJ. The pathogenesis of cancer metastasis. Nature 1980;283:139-146.
7. Bernards R, Weinberg RA. A progression puzzle. Nature 2002;418:823.
8. Pantel K, Cote RJ, Fodstad O. Detection and clinical importance of micrometastatic disease. J Natl Cancer Inst 1999;91:1113-1124.
9. Duffy MJ, Kelly ZD, Culhane AC, O'Brien A, Gallagher WM. DNA microarray-based gene expression profiling in cancer: aiding cancer diagnosis, assessing prognosis and predicting response to therapy. Curr Pharmacogenomics 2005;3:289-304.
10. Chambers AF, Tuck AB. Ras-responsive genes and tumor metastasis. Crit Rev Oncog 1993;4:95-114.
11. Yu D, Wang SS, Dulski KM, Tsai CM, Nicolson GL, Hung MC. c-erbB-2/neu overexpression enhances metastatic potential of human lung cancer cells by induction of metastasis-associated properties. Cancer Res 1994;54:3260-3266.
12. Myoui A, Nishimura R, Williams PJ, Hiraga T, Tamura D, Michigami T, et al. C-SRC tyrosine kinase activity is associated with tumor colonization in bone and lung in an animal model of human breast cancer metastasis. Cancer Res 2003;63:5028-5033.
13. Egeblad M, Werb Z. New functions for the matrix metalloproteinases in cancer progression. Nature Rev Cancer 2002;2:161-174.
14. Duffy MJ. The urokinase plasminogen activator system: role in malignancy. Curr Pharm Des 2004;10:39-49.
15. Engel J, Eckel R, Kerr J, Schmidt M, Furstenberger G, Richter R, et al. The process of metastasisation for breast cancer. Eur J Cancer 2003;39:1794-1806.
16. Steeg PS. Metastasis suppressors alter the signal transduction of cancer cells. Nature Rev Cancer 2003;3:55-63.
17. Shevde LA, Welch DR. Metastasis suppressor pathways - an evolving paradigm. Cancer Lett 2003;198:1-20.
18. Kang Y, Siegel PM, Shu W, Drobnjak M, Kakonen SM, Cordon-Cardo C, et al. A multigenic program mediating breast cancer metastasis to bone. Cancer Cell 2003;3:537-549.
19. Minn AJ, Kang Y, Serganova I, Gupta GP, Giri DD, Doubrovin M, et al. Distinct organ-specific metastatic potential of individual breast cancer cells and primary tumors. J Clin Invest 2005;115:44-55.
20. van 't Veer LJ, Dai H, van de Vijver MJ, He YD, Hart AA, Mao M, et al. Gene expression profiling predicts clinical outcome of breast cancer. Nature 2002;415:530-536.
21. Minn AJ, Gupta GP, Siegel PM, Bos PD, Shu W, Giri DD, et al. Genes that mediate breast cancer metastasis to lung. Nature 2005;436:518-524.
22. Gupta GP, Nguyen DX, Chiang AC, Bos PD, Kim JY, Nadal C, et al. Mediators of vascular remodelling co-opted for sequential steps in lung metastasis. Nature 2007;446:765-770.
23. Chambers AF, Matrisian LM. Changing views of the role of matrix metalloproteinases in metastasis. J Natl Cancer Inst 1997;89:1260- 1270.
24. Kalluri R. Basement membranes: structure, assembly and role in tumour angiogenesis. Nature Rev Cancer 2003;3:422-433.
25. Hicklin DJ, Ellis LM. Role of the vascular endothelial growth factor pathway in tumor growth and angiogenesis. J Clin Oncol 2005;23:1011-1027.
26. Bergers G, Brekken R, McMahon G, Vu TH, Itoh T, Tamaki K, et al. Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis. Nature Cell Biol 2000;2:737-744.
27. Mandriota SJ, Jussila L, Jeltsch M, Compagni A, Baetens D, Prevo R, et al. Vascular endothelial growth factor-C-mediated lymphangiogenesis promotes tumour metastasis. EMBO J 2001;20:672-682.
28. Stacker SA, Caesar C, Baldwin ME, Thornton GE, Williams RA, Prevo R, et al. VEGF-D promotes the metastatic spread of tumor cells via the lymphatics. Nature Med 2001;7:186-191.
29. McColl BK, Baldwin ME, Roufail S, Freeman C, Moritz RL, Simpson RJ, et al. Plasmin activates the lymphangiogenic growth factors VEGF-C and VEGF-D. J Exp Med 2003;198:863-868.
30. O'Reilly MS, Boehm T, Shing Y, Fukai N, Vasios G, Lane WS, et al. Endostatin: an endogenous inhibitor of angiogenesis and tumor growth. Cell 1997;88:277-285.
31. Jin X, Bookstein R, Wills K, Avanzini J, Tsai V, LaFace D, et al. Evaluation of endostatin antiangiogenesis gene therapy in vitro and in vivo. Cancer Gene Ther 2001;8:89-982.
32. Schuch G, Heymach JV, Nomi M, Machluf M, Force J, Atala A, et al. Endostatin inhibits the vascular endothelial growth factor-induced mobilization of endothelial progenitor cells. Cancer Res 2003;63:8345-8350.
33. Parks WC, Wilson CL, Lopez-Boado YS. Matrix metalloproteinases as modulators of inflammation and innate immunity. Nature Rev Immunol 2004;4:617-629.
34. Hojilla CV, Mohammed FF, Khokha R. Matrix metalloproteinases and their tissue inhibitors direct cell fate during cancer development. Br J Cancer 2003;89:1817-1821.
35. Sahin U, Weskamp G, Kelly K, Zhou HM, Higashiyama S, Peschon J, et al. Distinct roles for ADAM10 and ADAM17 in ectodomain shedding of six EGFR ligands. J Cell Biol 2004;164:769-779.
36. Blobel CP. ADAMs: key components in EGFR signalling and development. Nature Rev Mol Cell Biol 2005;6:32-43.
37. Baselga J. Why the epidermal growth factor receptor? The rationale for cancer therapy. Oncologist 2002;7(Suppl 4):2-8.
38. Ciardiello F, Tortora G. A novel approach in the treatment of cancer: targeting the epidermal growth factor receptor. Clin Cancer Res 2001;7:70-2958.
39. Schafer B, Gschwind A. Ullrich A. Multiple G-protein-coupled receptor signals converge on the epidermal growth factor receptor to promote migration and invasion. Oncogene 2004;23:991-999.
40. Schafer B, Marg B, Gschwind A. Ullrich A. Distinct ADAM metalloproteinases regulate G protein-coupled receptor-induced cell proliferation and survival. J Biol Chem 2004;279:47929-47938.
41. Levi E, Fridman R, Miao HQ, Ma YS, 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.
42. Peschon JJ, Slack JL, Reddy P, Stocking KL, Sunnarborg SW, Lee DC, et al. An essential role for ectodomain shedding in mammalian development. Science 1998;282:1281-1284.
43. Solomon KA, Pesti N, Wu G, Newton RC. Cutting edge: a dominant negative form of TNF-alpha converting enzyme inhibits proTNF and TNFRII secretion. J Immunol 1999;163:4105-4108.
44. Liu PC, Liu X, Li Y, Covington M, Wynn R, Huber R, et al. Identification of ADAM10 as a major source of HER2 ectodomain sheddase activity in HER2 overexpressing breast cancer cells. Cancer Biol Ther 2006;5:657-664.
45. Rio C, Buxbaum JD, Peschon JJ, Corfas G. Tumor necrosis factor-alpha-converting enzyme is required for cleavage of erbB4/HER4. J Biol Chem 2000;275:10379-10387.
46. Lopez-Otin C, Overall CM. Protease degradomics: a new challenge for proteomics. Nature Rev Mol Cell Biol 2002;3:509-519.
47. Jiang Y, Goldberg ID, Shi YE. Complex roles of tissue inhibitors of metalloproteinases in cancer. Oncogene 2002;21:2245-2252.
48. Andreasen PA, Kjoller L, Christensen L, Duffy MJ. The urokinase-type plasminogen activator system in cancer metastasis: a review. Int J Cancer 1997;72:1-22.
49. Baker AH, Edwards DR, Murphy G. Metalloproteinase inhibitors: biological actions and therapeutic opportunities. J Cell Sci 2002;115:3719- 3727.
50. Porter JF, Shen S, Denhardt DT. Tissue inhibitor of metalloproteinase-1 stimulates proliferation of human cancer cells by inhibiting a metalloproteinase. Br J Cancer 2004;90:463-470.
51. Ahonen M, Baker AH, Kahari VM. Adenovirus-mediated gene delivery of tissue inhibitor of metalloproteinases-3 inhibits invasion and induces apoptosis in melanoma cells. Cancer Res 1998;58:2310-2315.
52. Baker AH, George SJ, Zaltsman AB, Murphy G, Newby AC. Inhibition of invasion and induction of apoptotic cell death of cancer cell lines by overexpression of TIMP-3. Br J Cancer 1999;79:1347-1355.
53. Liu XW, Taube ME, Jung KK, Dong Z, Lee YJ, Roshy S, et al. Tissue inhibitor of metalloproteinase-1 protects human breast epithelial cells from extrinsic cell death: a potential oncogenic activity of tissue inhibitor of metalloproteinase-1. Cancer Res 2005;65:898-906.
54. Wang Z, Juttermann R, Soloway PD. TIMP-2 is required for efficient activation of proMMP-2 in vivo. J Biol Chem 2000;275:26411-26415.
55. Itoh Y, Takamura A, Ito N, Maru Y, Sato H, Suenaga N, et al. Homophilic complex formation of MT1-MMP facilitates proMMP-2 activation on the cell surface and promotes tumor cell invasion. EMBO J 2001;20:4782-4793.
56. Lu KV, Jong KA, Rajasekaran AK, Cloughesy TF, Mischel PS. Upregulation of tissue inhibitor of metalloproteinases (TIMP)-2 promotes matrix metalloproteinase (MMP)-2 activation and cell invasion in a human glioblastoma cell line. Lab Invest 2004;84:8-20.
57. Czekay RP, Aertgeerts K, Curriden SA, Loskutoff DJ. Plasminogen activator inhibitor-1 detaches cells from extracellular matrices by inactivating imegrins. J Cell Biol 2003;160:781-791.
58. Bajou K, Maillard C, Jost M, Lijnen RH, Gils A, Declerck P, et al. Host-derived plasminogen activator inhibitor-1 (PAI-1) concentration is critical for in vivo tumoral angiogenesis and growth. Oncogene 2004;23:6986-6990.
59. Duffy MJ. Urokinase plasminogen activator and its inhibitor, PAI-1, as prognostic markers in breast cancer: from pilot to level 1 evidence studies. Clin Chem 2002;48:1194-1197.
60. McCarthy K, Maguire T, McGreal G, McDermott E, O'Higgins N, Duffy MJ. High levels of tissue inhibitor of metalloproteinase-1 predict poor outcome in patients with breast cancer. Int J Cancer 1999;84:44-48.
61. Zeng ZS, Cohen AM, Zhang ZF, Stetler-Stevenson W, Guillem JG. Elevated tissue inhibitor of metalloproteinase 1 RNA in colorectal cancer stroma correlates with lymph node and distant metastases. Clin Cancer Res 1995;1:899-906.
62. Joo YE, Seo KS, Kim HS, Rew JS, Park CS, Kim SJ. Expression of tissue inhibitors of metalloproteinases (TIMPs) in gastric cancer. Dig Dis Sci 2000;45:114-121.
63. Still K, Robson CN, Autzen P, Robinson MC, Hamdy FC. Localization and quantification of mRNA for matrix metalloproteinase-2 (MMP-2) and tissue inhibitor of matrix metalloproteinase-2 (TIMP-2) in human benign and malignant prostatic tissue. Prostate 2000;42:18-25.
64. Mueller MM, Fusenig NE. Friends or foes - bipolar effects of the tumour stroma in cancer. Nature Rev Cancer 2004;4:839-849.
65. Bhowmick NA, Neilson EG, Moses HL. Stromal fibroblasts in cancer initiation and progression. Nature 2004;432:332-337.
66. van Kempen LC, de Visser KE, Coussens LM. Inflammation, proteases and cancer. Eur J Cancer 2006;42:728-734.
67. Coussens LM, Tinkle CL, Hanahan D, Werb Z. MMP-9 supplied by bone marrow-derived cells contributes to skin carcinogenesis. Cell 2000;103:481-490.
68. Huang S, Van Arsdall M, Tedjarati S, McCarty M, Wu W, Langley R, et al. Contributions of stromal metalloproteinase-9 to angiogenesis and growth of human ovarian carcinoma in mice. J Natl Cancer Inst 2002;94:1134-1142.
69. Giraudo E, Inoue M, Hanahan D. An amino-bisphosphonate targets MMP-9-expressing macrophages and angiogenesis to impair cervical carcinogenesis. J Clin Invest 2004;114:623-633.
70. Almholt K, Lund LR, Rygaard J, Nielsen BS, Dano K, Romer J, et al. Reduced metastasis of transgenic mammary cancer in urokinase-deficient mice. Int J Cancer 2005;113:525-532.
71. Duffy MJ. Proteases as prognostic markers in cancer. Clin Cancer Res 1996;2:613-618.
72. Hewitt R, Dano K. Stromal cell expression of components of matrix-degrading protease systems in human cancer. Enzyme Protein 1996;49:163-173.
73. Basset P, Wolf C, Chambon P. Expression of the stromelysin-3 gene in fibroblastic cells of invasive carcinomas of the breast and other human tissues: a review. Breast Cancer Res Treat 1993;24:185-193.
74. Chenard MP, O'Siorain L, Shering S, Rouyer N, Lutz Y, Wolf C, et al. High levels of stromelysin-3 correlate with poor prognosis in patients with breast carcinoma. Int J Cancer 1996;69:448-451.
75. Pellikainen JM, Ropponen KM, Kataja VV, Kellokoski JK, Eskelinen MJ, Kosma VM. Expression of matrix metalloproteinase (MMP)-2 and MMP-9 in breast cancer with special reference to activator protein-2, HER2 and prognosis. Clin Cancer Res 2004;10:7621-7628.
76. Biswas C, Zhang Y, DeCastro R, Guo H, Nakamura T, Kataoka H, et al. The human tumor cell-derived collagenase stimulatory factor (renamed EMMPRIN) is a member of the immunoglobulin superfamily. Cancer Res 1995;55:434-439.
77. Kusano K, Miyaura C, Inada M, Tamura T, Ito A, Nagase H, et al. Regulation of matrix metalloproteinases (MMP-2, -3, -9, and -13) by interleukin-1 and interleukin-6 in mouse calvaria: association of MMP induction with bone resorption. Endocrinology 1998;139:1338-1345.
78. Sieuwerts AM, Klijn JG, Henzen-Logmans SC, Foekens JA. Cytokine-regulated urokinase-type-plasminogen-activator (uPA) production by human breast fibroblasts in vitro. Breast Cancer Res Treat 1999;55:9-20.
79. Allinen M, Beroukhim R, Cai L, Brennan C, Lahti-Domenici J, Huang H, et al. Molecular characterization of the tumor microenvironment in breast cancer. Cancer Cell 2004;6:17-32.
80. Bhowmick NA, Chytil A, Plieth D, Gorska AE, Dumont N, Shappell S, et al. TGF-beta signaling in fibroblasts modulates the oncogenic potential of adjacent epithelia. Science 2004;303:848-851.
81. Wyckoff JB, Jones JG, Condeelis JS, Segall JE. A critical step in metastasis: in vivo analysis of intravasation at the primary tumor. Cancer Res 2000;60:2504-2511.
82. Zijlstra A, Mellor R, Panzarella G, Aimes RT, Hooper JD, Marchenko ND, et al. A quantitative analysis of rate-limiting steps in the metastatic cascade using human-specific real-time polymerase chain reaction. Cancer Res 2002;62:7083-7092.
83. Ossowski L. Invasion of connective tissue by human carcinoma cell lines: requirement for urokinase, urokinase receptor, and interstitial collagenase. Cancer Res 1992;52:6754-6760.
84. Kim J, Yu W, Kovalski K, Ossowski L. Requirement for specific proteases in cancer cell intravasation as revealed by a novel semiquantitative PCR-based assay. Cell 1998;94:353-362.
85. Luzzi KJ, MacDonald IC, Schmidt EE, Kerkvliet N, Morris V. L, Chambers AF, et al. Multistep nature of metastatic inefficiency: dormancy of solitary cells after successful extravasation and limited survival of early micrometastases. Am J Pathol 1998;153:865-873.
86. Koop S, Khokha R, Schmidt EE, MacDonald IC, Morris VL, Chambers AF, et al. Overexpression of metalloproteinase inhibitor in B16F10 cells does not affect extravasation but reduces tumor growth. Cancer Res 1994;54:4791-4797.
87. Koop S, MacDonald IC, Luzzi K, Schmidt EE, Morris VL, Grattan M, et al. Fate of melanoma cells entering the microcirculation: over 80% survive and extravasate. Cancer Res 1995;55:2520-2523.
88. Kaplan RN, Rafii S, Lyden D. Preparing the 'soil': the premetastatic niche. Cancer Res 2006;66:11089-11093.
89. Kaplan RN, Riba RD, Zacharoulis S, Bramley AH, Vincent L, Costa C, et al. VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche. Nature 2005;438:820-827.
90. Hiratsuka S, Watanabe A, Aburatani H, Maru Y. Tumour-mediated upregulation of chemoattractants and recruitment of myeloid cells predetermines lung metastasis. Nature Cell Biol 2006;8:1369-1375.
91. Duffy MJ, O'Grady P, Devaney D, O'Siorain L, Fennelly JJ, Lijnen HJ. Urokinase-plasminogen activator, a marker for aggressive breast carcinomas. Preliminary report. Cancer 1988;62:531-533.
92. Janicke F, Prechtl A, Thomssen C, Harbeck N, Meisner C, Untch M, et al. Randomized adjuvant chemotherapy trial in high-risk, lymph node-negative breast cancer patients identified by urokinase-type plasminogen activator and plasminogen activator inhibitor type 1. J Natl Cancer Inst 2001;93:913-920.
93. Look MP, van Putten WL, Duffy MJ, Harbeck N, Christensen IJ, Thomssen C, et al. Pooled analysis of prognostic impact of urokinase-type plasminogen activator and its inhibitor PAI-1 in 8377 breast cancer patients. J Natl Cancer Inst 2002;94:116-128.
94. Hayes DF, Bast RC, Desch CE, Fritsche H Jr, Kemeny NE, Jessup JM, et al. Tumor marker utility grading system: a framework to evaluate clinical utility of tumor markers. J Natl Cancer Inst 1996;88:1456-1466.
95. Smid M, Wang Y, Klijn JG, Sieuwerts AM, Zhang Y, Atkins D, et al. Genes associated with breast cancer metastatic to bone. J Clin Oncol 2006;24:2261-2267.
96. Zucker S, Cao J, Chen WT. Critical appraisal of the use of matrix metalloproteinase inhibitors in cancer treatment. Oncogene 2000;19:6642-6650.
97. Overall CM, Kleifeld O. Tumour microenvironment - opinion: validating matrix metalloproteinases as drug targets and antitargets for cancer therapy. Nature Rev Cancer 2006;6:227-239.
98. Fingleton B, Menon R, Carter KJ, Overstreet PD, Hachey DL, Matrisian LM, et al. Proteinase activity in human and murine saliva as a biomarker for proteinase inhibitor efficacy. Clin Cancer Res 2004;10:7865-7874.
99. Presta LG, Chen H, O'Connor SJ, Chisholm V, Meng YG, Krummen L, et al. Humanization of an anti-vascular endothelial growth factor monoclonal antibody for the therapy of solid tumors and other disorders. Cancer Res 1997;57:4593-4599.
100. Hurwitz H, Fehrenbacher L, Novotny W, Cartwright T, Hainsworth J, Heim W, et al. Bevacizumab plus irinotecan, fluorouracil, and leucovorin for metastatic colorectal cancer. N Engl J Med 2004;350:2335-2342.
101. Kerbel RS. Antiangiogenic therapy: a universal chemosensitization strategy for cancer? Science 2006;312:1171-1175.
102. Ferrara N, Kerbel RS. Angiogenesis as a therapeutic target. Nature 2005;438:967-974.
103. Motzer RJ, Hutson TE, Tomczak P, Michaelson MD, Bukowski RM, Rixe O, et al. Sunitinib versus interferon alpha in metastatic renal-cell carcinoma. N Engl J Med 2007;356:115-124.
104. Escudier B, Eisen T, Stadler WM, Szczylik C, Oudard S, Siebeis M, et al. Sorafenib in advanced clear-cell renal-cell carcinoma. N Engl J Med 2007;356:125-134.
105. Wilhelm S, Carter C, Lynch M, Lowinger T, Dumas J, Smith RA, et al. Discovery and development of sorafenib: a multikinase inhibitor for treating cancer. Nature Rev Drug Discov 2006;5:835-844.
106. Bhatt RS, Seth P, Sukhatme VP. Biomarkers for monitoring antiangiogenic therapy. Clin Cancer Res 2007;13:777s-780s.
107. Elvin P, Garner AP. Tumour invasion and metastasis: challenges facing drug discovery. Curr Opin Pharmacol 2005;5:374-381.
108. Powell WC, Fingleton B, Wilson CL, Boothby M, Matrisian LM. The metalloproteinase matrilysin proteolytically generates active soluble Fas ligand and potentiates epithelial cell apoptosis. Curr Biol 1999;9:1441-1447.
109. Vargo-Gogola T, Fingleton B, Crawford HC, Matrisian LM. Matrilysin (matrix metalloproteinase-7) selects for apoptosis-resistant mammary cells in vivo. Cancer Res 2002;62:5559-5563.
110. Suzuki M, Raab G, Moses MA, Fernandez CA, Klagsbrun M. Matrix metalloproteinase-3 releases active heparin-binding EGF-like growth factor by cleavage at a specific juxtamembrane site. J Biol Chem 1997;272:31730-31737.
111. 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.
112. Manes S, Mira E, Barbacid MM, Cipres A, Fernandez-Resa P, Buesa JM, et al. Identification of insulin-like growth factor-binding protein-1 as a potential physiological substrate for human stromelysin-3. J Biol Chem 1997;272:25706-25712.
113. Vu TH, Werb Z. Matrix metalloproteinases: effectors of development and normal physiology. Genes Dev 2000;14:2123-2133.
114. Van Damme J, Struyf S, Opdenakker G. Chemokine-protease interactions in cancer. Semin Cancer Biol 2004;14:201-208.
115. Noe V, Fingleton B, Jacobs K, Crawford HC, Vermeulen S, Steelant W, et al. Release of an invasion promoter E-cadherin fragment by matrilysin and stromelysin-1. J Cell Sci 2001;114:111-118.
116. Deryugina EI, Ratnikov BI, Postnova TI, Rozanov DV, Strongin AY. 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 2002;277:9749-9756.
117. 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.