Endogenous angiogenesis inhibitor blocks tumor growth via direct and indirect effects on tumor microenvironment

American Journal of Pathology

Volumn 179, Issue 5, 2011, Pages 2589-2600

  Bourboulia, Dimitra ^a   Jensen Taubman, Sandra ^a   Rittler, Matthew R ^a   Han, Hui Ying ^a   Chatterjee, Tania ^a,b   Wei, Beiyang ^a   Stetler Stevenson, William G ^a,b  

^a NATIONAL CANCER INSTITUTE   (United States)

^b UNIVERSITY OF MARYLAND   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TISSUE INHIBITOR OF METALLOPROTEINASE 2;

ADENOCARCINOMA; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BASAL CELL; CANCER INHIBITION; CANCER INVASION; CARCINOMA CELL; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR MICROENVIRONMENT; TUMOR XENOGRAFT; ZYMOGRAPHY;

ADENOCARCINOMA; ANIMALS; APOPTOSIS; CELL MOVEMENT; CELL PROLIFERATION; FEMALE; FOCAL ADHESION PROTEIN-TYROSINE KINASES; HUMANS; LUNG NEOPLASMS; MATRIX METALLOPROTEINASE 2; MICE; MICE, NUDE; MICROVESSELS; NEOPLASM INVASIVENESS; NEOPLASM TRANSPLANTATION; NEOVASCULARIZATION, PATHOLOGIC; PROTO-ONCOGENE PROTEINS C-AKT; TISSUE INHIBITOR OF METALLOPROTEINASE-2; TRANSPLANTATION, HETEROLOGOUS; TUMOR CELLS, CULTURED; TUMOR MICROENVIRONMENT;

EID: 80055005759     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2011.07.035     Document Type: Article

References (52)

1. W.G. Stetler-Stevenson, and A.E. Yu Proteases in invasion: matrix metalloproteinases Semin Cancer Biol 11 2001 143 152
2. K. Kessenbrock, V. Plaks, and Z. Werb Matrix metalloproteinases: regulators of the tumor microenvironment Cell 141 2010 52 67
3. D.X. Nguyen, P.D. Bos, and J. Massague Metastasis: from dissemination to organ-specific colonization Nat Rev Cancer 9 2009 274 284
4. K. Brew, and H. Nagase The tissue inhibitors of metalloproteinases (TIMPs): an ancient family with structural and functional diversity Biochim Biophys Acta 1803 2010 55 71
5. A.H. Baker, D.R. Edwards, and G. Murphy Metalloproteinase inhibitors: biological actions and therapeutic opportunities J Cell Sci 115 2002 3719 3727
6. C. Fernandez-Catalan, W. Bode, R. Huber, D. Turk, J.J. Calvete, A. Lichte, H. Tschesche, and K. Maskos 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
7. K. Maskos, R. Lang, H. Tschesche, and W. Bode Flexibility and variability of TIMP binding: x-ray structure of the complex between collagenase-3/MMP-13 and TIMP-2 J Mol Biol 366 2007 1222 1231
8. S. Hernandez-Barrantes, M. Bernardo, M. Toth, and R. Fridman Regulation of membrane type-matrix metalloproteinases Semin Cancer Biol 12 2002 131 138
9. A.Y. Strongin, I. Collier, G. Bannikov, B.L. Marmer, G.A. Grant, and G.I. Goldberg 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
10. A. Albini, A. Melchiori, L. Santi, L.A. Liotta, P.D. Brown, and W.G. Stetler-Stevenson Tumor cell invasion inhibited by TIMP-2 J Natl Cancer Inst 83 1991 775 779
11. S. Imren, D.B. Kohn, H. Shimada, L. Blavier, and Y.A. DeClerck Overexpression of tissue inhibitor of metalloproteinases-2 retroviral-mediated gene transfer in vivo inhibits tumor growth and invasion Cancer Res 56 1996 2891 2895
12. D.W. Seo, H. Li, L. Guedez, P.T. Wingfield, T. Diaz, R. Salloum, B.Y. Wei, and W.G. Stetler-Stevenson TIMP-2 mediated inhibition of angiogenesis: an MMP-independent mechanism Cell 114 2003 171 180
13. E. Johansson, A. Komuro, C. Iwata, A. Hagiwara, Y. Fuse, A. Watanabe, Y. Morishita, H. Aburatani, K. Funa, M.R. Kano, and K. Miyazono Exogenous introduction of tissue inhibitor of metalloproteinase 2 reduces accelerated growth of TGF-beta-disrupted diffuse-type gastric carcinoma Cancer Sci 101 2010 2398 2403
14. S.W. Yang, J.J. Cody, A.A. Rivera, R. Waehler, M. Wang, K.J. Kimball, R.A. Alvarez, G.P. Siegal, J.T. Douglas, and S. Ponnazhagan Conditionally replicating adenovirus expressing TIMP2 for ovarian cancer therapy Clin Cancer Res 17 2011 538 549
15. N.S. Waleh, B.J. Murphy, and N.T. Zaveri Increase in tissue inhibitor of metalloproteinase-2 (TIMP-2) levels and inhibition of MMP-2 activity in a metastatic breast cancer cell line by an anti-invasive small molecule SR13179 Cancer Lett 289 2010 111 118
16. S.M. Ahn, S.J. Jeong, Y.S. Kim, Y. Sohn, and A. Moon Retroviral delivery of TIMP-2 inhibits H-ras-induced migration and invasion in MCF10A human breast epithelial cells Cancer Lett 207 2004 49 57
17. Y.K. Lee, I.S. So, S.C. Lee, J.H. Lee, C.W. Lee, W.M. Kim, M.K. Park, S.T. Lee, D.Y. Park, D.Y. Shin, C.U. Park, and Y.S. Kim Suppression of distant pulmonary metastasis of MDA-MB 435 human breast carcinoma established in mammary fat pads of nude mice by retroviral-mediated TIMP-2 gene transfer J Gene Med 7 2005 145 157
18. Y.A. DeClerck, N. Perez, H. Shimada, T.C. Boone, K.E. Langley, and S.M. Taylor Inhibition of invasion and metastasis in cells transfected with an inhibitor of metalloproteinases Cancer Res 52 1992 701 708
19. C.A. Fernandez, C. Butterfield, G. Jackson, and M.A. Moses Structural and functional uncoupling of the enzymatic and angiogenic inhibitory activities of tissue inhibitor of metalloproteinase-2 (TIMP-2): loop 6 is a novel angiogenesis inhibitor J Biol Chem 278 2003 40989 40995
20. P.T. Wingfield, J.K. Sax, S.J. Stahl, J. Kaufman, I. Palmer, V. Chung, M.L. Corcoran, D.E. Kleiner, and W.G. Stetler-Stevenson Biophysical and functional characterization of full-length, recombinant human tissue inhibitor of metalloproteinases-2 (TIMP-2) produced in Escherichia coli Comparison of wild type and amino-terminal alanine appended variant with implications for the mechanism of TIMP functions J Biol Chem 274 1999 21362 21368
21. C.A. Fernandez, R. Roy, S. Lee, J. Yang, D. Panigrahy, K.J. Van Vliet, and M.A. Moses The anti-angiogenic peptide, loop 6, binds insulin-like growth factor-1 receptor J Biol Chem 285 2010 41886 41895
22. J. Oh, D.W. Seo, T. Diaz, B. Wei, Y. Ward, J.M. Ray, Y. Morioka, S. Shi, H. Kitayama, C. Takahashi, M. Noda, and W.G. Stetler-Stevenson Tissue inhibitors of metalloproteinase 2 inhibits endothelial cell migration through increased expression of RECK Cancer Res 64 2004 9062 9069
23. L. Perez-Martinez, and D.M. Jaworski Tissue inhibitor of metalloproteinase-2 promotes neuronal differentiation by acting as an anti-mitogenic signal J Neurosci 25 2005 4917 4929
24. G. Lluri, G.D. Langlois, B. McClellan, P.D. Soloway, and D.M. Jaworski Tissue inhibitor of metalloproteinase-2 (TIMP-2) regulates neuromuscular junction development via a beta1 integrin-mediated mechanism J Neurobiol 66 2006 1365 1377
25. G. Lluri, G.D. Langlois, P.D. Soloway, and D.M. Jaworski Tissue inhibitor of metalloproteinase-2 (TIMP-2) regulates myogenesis and beta1 integrin expression in vitro Exp Cell Res 314 2008 11 24
26. J. Oh, T. Diaz, B. Wei, H. Chang, M. Noda, and W.G. Stetler-Stevenson TIMP-2 upregulates RECK expression via dephosphorylation of paxillin tyrosine residues 31 and 118 Oncogene 25 2006 4230 4234
27. D.W. Seo, H. Li, C.K. Qu, J. Oh, Y.S. Kim, T. Diaz, B. Wei, J.W. Han, and W.G. Stetler-Stevenson Shp-1 mediates the antiproliferative activity of tissue inhibitor of metalloproteinase-2 in human microvascular endothelial cells J Biol Chem 281 2006 3711 3721
28. O. Galm, H. Suzuki, Y. Akiyama, M. Esteller, M.V. Brock, R. Osieka, S.B. Baylin, and J.G. Herman Inactivation of the tissue inhibitor of metalloproteinases-2 gene by promoter hypermethylation in lymphoid malignancies Oncogene 24 2005 4799 4805
29. S.M. Pulukuri, S. Patibandla, J. Patel, N. Estes, and J.S. Rao Epigenetic inactivation of the tissue inhibitor of metalloproteinase-2 (TIMP-2) gene in human prostate tumors Oncogene 26 2007 5229 5237
30. T. Ivanova, S. Vinokurova, A. Petrenko, E. Eshilev, N. Solovyova, F. Kisseljov, and N. Kisseljova Frequent hypermethylation of 5′ flanking region of TIMP-2 gene in cervical cancer Int J Cancer 108 2004 882 886
31. M.D. Abramoff, P.J. Magelhaes, and S.J. Ram Image Processing with ImageJ Biophoton Int 11 2004 36 42
32. M. Hoyhtya, R. Fridman, D. Komarek, K. Porter-Jordan, W.G. Stetler-Stevenson, L.A. Liotta, and C.M. Liang Immunohistochemical localization of matrix metalloproteinase 2 and its specific inhibitor TIMP-2 in neoplastic tissues with monoclonal antibodies Int J Cancer 56 1994 500 505
33. D.E. Kleiner, and W.G. Stetler-Stevenson Quantitative zymography: detection of picogram quantities of gelatinases Anal Biochem 218 1994 325 329
34. G.W. Oliver, J.D. Leferson, W.G. Stetler-Stevenson, and D.E. Kleiner Quantitative reverse zymography: analysis of picogram amounts of metalloproteinase inhibitors using gelatinase A and B reverse zymograms Anal Biochem 244 1997 161 166
35. J. Folkman Angiogenesis and apoptosis Semin Cancer Biol 13 2003 159 167
36. M. Streit, L. Riccardi, P. Velasco, L.F. Brown, T. Hawighorst, P. Bornstein, and M. Detmar Thrombospondin-2: a potent endogenous inhibitor of tumor growth and angiogenesis Proc Natl Acad Sci USA 96 1999 14888 14893
37. W.G. Stetler-Stevenson Tissue inhibitors of metalloproteinases in cell signaling: metalloproteinase-independent biological activities Sci Signal 1 2008 re6
38. M.E. Taube, X.W. Liu, R. Fridman, and H.R. Kim TIMP-1 regulation of cell cycle in human breast epithelial cells via stabilization of p27(KIP1) protein Oncogene 25 2006 3041 3048
39. K.H. Kang, S.Y. Park, S.B. Rho, and J.H. Lee Tissue inhibitor of metalloproteinases-3 interacts with angiotensin II type 2 receptor and additively inhibits angiogenesis Cardiovasc Res 79 2008 150 160
40. J.H. Qi, Q. Ebrahem, N. Moore, G. Murphy, L. Claesson-Welsh, M. Bond, A. Baker, and B. Anand-Apte 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
41. A.N. Murphy, E.J. Unsworth, and W.G. Stetler-Stevenson Tissue inhibitor of metalloproteinases-2 inhibits bFGF-induced human microvascular endothelial cell proliferation J Cell Physiol 157 1993 351 358
42. S.E. Hoegy, H.R. Oh, M.L. Corcoran, and W.G. Stetler-Stevenson Tissue inhibitor of metalloproteinases-2 (TIMP-2) suppresses TKR-growth factor signaling independent of metalloproteinase inhibition J Biol Chem 276 2001 3203 3214
43. A.L. Feldman, W.G. Stetler-Stevenson, N.G. Costouros, V. Knezevic, G. Baibakov, H.R. Alexander Jr., D. Lorang, S.M. Hewitt, D.W. Seo, M.S. Miller, S. O'Connor, and S.K. Libutti Modulation of tumor-host interactions, angiogenesis, and tumor growth by tissue inhibitor of metalloproteinase 2 via a novel mechanism Cancer Res 64 2004 4481 4486
44. P. Valente, G. Fassina, A. Melchiori, L. Masiello, M. Cilli, A. Vacca, M. Onisto, L. Santi, W.G. Stetler-Stevenson, and A. Albini TIMP-2 over-expression reduces invasion and angiogenesis and protects B16F10 melanoma cells from apoptosis Int J Cancer 75 1998 246 253
45. A. Albini, G. Fontanini, L. Masiello, C. Tacchetti, D. Bigini, P. Luzzi, D.M. Noonan, and W.G. Stetler-Stevenson Angiogenic potential in vivo by Kaposi's sarcoma cell-free supernatants and HIV-1 tat product: inhibition of KS-like lesions by tissue inhibitor of metalloproteinase-2 AIDS 8 1994 1237 1244
46. A.M. Montgomery, B.M. Mueller, R.A. Reisfeld, S.M. Taylor, and Y.A. DeClerck Effect of tissue inhibitor of the matrix metalloproteinases-2 expression on the growth and spontaneous metastasis of a human melanoma cell line Cancer Res 54 1994 5467 5473
47. A. Goyal, N. Pal, M. Concannon, M. Paul, M. Doran, C. Poluzzi, K. Sekiguchi, J.M. Whitelock, T. Neill, and R.V. Iozzo Endorepellin, perlecan angiostatic module, interacts with both the α2β1 integrin and VEGFreceptor 2: A dual receptor antagonism J Biol Chem 286 2011 25947 25962
48. A. Nystrom, Z.P. Shaik, D. Gullberg, T. Krieg, B. Eckes, R. Zent, A. Pozzi, and R.V. Iozzo Role of tyrosine phosphatase SHP-1 in the mechanism of endorepellin angiostatic activity Blood 114 2009 4897 4906
49. G.W. McLean, N.O. Carragher, E. Avizienyte, J. Evans, V.G. Brunton, and M.C. Frame The role of focal-adhesion kinase in cancera new therapeutic opportunity Nat Rev Cancer 5 2005 505 515
50. J.A. Engelman Targeting PI3K signalling in cancer: opportunities, challenges and limitations Nat Rev Cancer 9 2009 550 562
51. B.D. Manning, and L.C. Cantley AKT/PKB signaling: navigating downstream Cell 129 2007 1261 1274
52. S.J. Lee, P.S. Tsang, T.M. Diaz, B.Y. Wei, and W.G. Stetler-Stevenson TIMP-2 modulates VEGFR-2 phosphorylation and enhances phosphodiesterase activity in endothelial cells Lab Invest 90 2010 374 382