Kaposi's sarcoma-associated herpesvirus infection promotes invasion of primary human umbilical vein endothelial cells by inducing matrix metalloproteinases

Journal of Virology

Volumn 81, Issue 13, 2007, Pages 7001-7010

  Qian, Li Wu ^a,b   Xie, Jianping ^a,b   Ye, Fengchun ^a,b   Gao, Shou Jiang ^a,b,c,d  

^a UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^b Mays Cancer Center at UT Health San Antonio   (United States)

^c University of Texas Health Science Center at San Antonio   (United States)

^d WUHAN INSTITUTE OF VIROLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BATIMASTAT; CIS ACTING ELEMENT; GELATINASE A; GELATINASE B; INTERSTITIAL COLLAGENASE; MATRIGEL; MATRIX METALLOPROTEINASE; MESSENGER RNA; TRANSCRIPTION FACTOR AP 1;

ARTICLE; CELL INVASION; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME INDUCTION; ENZYME RELEASE; HERPES; HUMAN; HUMAN CELL; HUMAN HERPESVIRUS 8; KAPOSI SARCOMA; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; UMBILICAL VEIN; VIRUS CARCINOGENESIS; VIRUS CELL INTERACTION; VIRUS INFECTIVITY;

AUTOCRINE COMMUNICATION; CELL TRANSFORMATION, VIRAL; CELLS, CULTURED; COLLAGENASES; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HERPESVIRUS 8, HUMAN; HUMANS; NEOPLASM INVASIVENESS; NEOVASCULARIZATION, PATHOLOGIC; PARACRINE COMMUNICATION; PHENYLALANINE; PROTEASE INHIBITORS; RESPONSE ELEMENTS; RNA, MESSENGER; RNA, NEOPLASM; SARCOMA, KAPOSI; THIOPHENES; TRANSCRIPTION FACTOR AP-1; UMBILICAL VEINS; UP-REGULATION;

HUMAN HERPESVIRUS 8;

EID: 34250811336     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00016-07     Document Type: Article

References (51)

1. Akula, S. M., N. P. Pramod, F. Z. Wang, and B. Chandran. 2002. Integrin α3β1 (CD 49c/29) is a cellular receptor for Kaposi's sarcoma-associated herpesvirus (KSHV/HHV-8) entry into the target cells. Cell 108:407-419.
2. An, J., A. K. Lichtenstein, G. Brent, and M. B. Rettig. 2002. The Kaposi's sarcoma-associated herpesvirus (KSHV) induces cellular interleukin 6 expression: role of the KSHV latency-associated nuclear antigen and the AP1 response element. Blood 99:649-654.
3. An, J., Y. Sun, R. Sun, and M. B. Rettig. 2003. Kaposi's sarcoma-associated herpesvirus encoded vFLIP induces cellular IL-6 expression: the role of the NF-κB and JNK/AP1 pathways. Oncogene 22:3371-3385.
4. Bais, C., B. Santomasso, O. Coso, L. Arvanitakis, E. G. Raaka, J. S. Gutkind, A. S. Asch, E. Cesarman, M. C. Gershengorn, and E. A. Mesri. 1998. G-protein-coupled receptor of Kaposi's sarcoma-associated herpesvirus is a viral oncogene and angiogenesis activator. Nature 391:86-89.
5. Balbin, M., A. Fueyo, A. M. Tester, A. M. Pendas, A. S. Pitiot, A. Astudillo, C. M. Overall, S. D. Shapiro, and C. Lopez-Otin. 2003. Loss of collagenase-2 confers increased skin tumor susceptibility to male mice. Nat. Genet. 35: 252-257.
6. Blankaert, D., T. Simonart, J. P. Van Vooren, D. Parent, C. Liesnard, C. M. Farber, T. Marique, and J. Werenne. 1998. Constitutive release of metalloproteinase-9 (92-kd type IV collagenase) by Kaposi's sarcoma cells. J. Acquir. Immune Defic. Syndr. Hum. Retrovirol. 18:203-209.
7. Bogenrieder, T., and M. Herlyn. 2003. Axis of evil: molecular mechanisms of cancer metastasis. Oncogene 22:6524-6536.
8. Brinkmann, M. M., M. Glenn, L. Rainbow, A. Kieser, C. Henke-Gendo, and T. F. Schulz. 2003. Activation of mitogen-activated protein kinase and NF-κB pathways by a Kaposi's sarcoma-associated herpesvirus K15 membrane protein. J. Virol. 77:9346-9358.
9. Carroll, P. A., E. Brazeau, and M. Lagunoff. 2004. Kaposi's sarcoma-associated herpesvirus infection of blood endothelial cells induces lymphatic differentiation. Virology 328:7-18.
10. Chang, Y., E. Cesarman, M. S. Pessin, F. Lee, J. Culpepper, D. M. Knowles, and P. S. Moore. 1994. Identification of herpesvirus-like DNA sequences in AIDS-associated Kaposi's sarcoma. Science 266:1865-1869.
11. Cheung, T. W. 2004. AIDS-related cancer in the era of highly active antiretroviral therapy (HAART): a model of the interplay of the immune system, virus, and cancer. On the offensive: the Trojan Horse is being destroyed. Part A: Kaposi's sarcoma. Cancer Investig. 22:774-786.
12. Cianfrocca, M., T. P. Cooley, J. Y. Lee, M. A. Rudek, D. T. Scadden, L. Ratner, J. M. Pluda, W. D. Figg, S. E. Krown, and B. J. Dezube. 2002. Matrix metalloproteinase inhibitor COL-3 in the treatment of AIDS-related Kaposi's sarcoma: a phase I AIDS malignancy consortium study. J. Clin. Oncol. 20:153-159.
13. Deryugina, E. I., and J. P. Quigley. 2006. Matrix metalloproteinases and tumor metastasis. Cancer Metastasis Rev. 25:9-34.
14. Dourmishev, L. A., A. L. Dourmishev, D. Palmeri, R. A. Schwartz, and D. M. Lukac. 2003. Molecular genetics of Kaposi's sarcoma-associated herpesvirus (human herpesvirus-8) epidemiology and pathogenesis. Microbiol. Mol. Biol. Rev. 67:175-212.
15. Fingleton, B., T. Vargo-Gogola, H. C. Crawford, and L. M. Matrisian. 2001. Matrilysin [MMP-7] expression selects for cells with reduced sensitivity to apoptosis. Neoplasia 3:459-468.
16. Gao, S. J., J. H. Deng, and F. C. Zhou. 2003. Productive lytic replication of a recombinant Kaposi's sarcoma-associated herpesvirus in efficient primary infection of primary human endothelial cells. J. Virol. 77:9738-9749.
17. Gao, S. J., L. Kingsley, D. R. Hoover, T. J. Spira, C. R. Rinaldo, A. Saah, J. Phair, R. Detels, P. Parry, Y. Chang, and P. S. Moore. 1996. Seroconversion to antibodies against Kaposi's sarcoma-associated herpesvirus-related latent nuclear antigens before the development of Kaposi's sarcoma. N. Engl. J. Med. 335:233-241.
18. Gonzalez, C. M., E. L. Wong, B. S. Bowser, G. K. Hong, S. Kenney, and B. Damania. 2006. Identification and characterization of the Orf49 protein of Kaposi's sarcoma-associated herpesvirus. J. Virol. 80:3062-3070.
19. Greene, W., K. Kuhne, F. C. Ye, J. G. Chen, F. C. Zhou, X. F. Lei, and S.-J. Gao. 2007. Molecular biology of KSHV in relation to AIDS-associated oncogenesis, p. 69-127. In C. Meyers (ed.), AIDS-associated viral oncogenesis. Springer Science Business Media, New York, NY.
20. Hamza, M. S., R. A. Reyes, Y. Izumiya, R. Wisdom, H. J. Kung, and P. A. Luciw. 2004. ORF36 protein kinase of Kaposi's sarcoma herpesvirus activates the c-Jun N-terminal kinase signaling pathway. J. Biol. Chem. 279: 38325-38330.
21. Handsley, M. M., and D. R. Edwards. 2005. Metalloproteinases and their inhibitors in tumor angiogenesis. Int. J. Cancer 115:849-860.
22. Ho, A. T., E. B. Voura, P. D. Soloway, K. L. Watson, and R. Khokha. 2001. MMP inhibitors augment fibroblast adhesion through stabilization of focal adhesion contacts and up-regulation of cadherin function. J. Biol. Chem. 276:40215-40224.
23. Impola, U., M. A. Cuccuru, M. V. Masala, L. Jeskanen, F. Cottoni, and U. Saarialho-Kere. 2003. Preliminary communication: matrix metalloproteinases in Kaposi's sarcoma. Br. J. Dermatol. 149:905-907.
24. Ishii, Y., T. Ogura, M. Tatemichi, H. Fujisawa, F. Otsuka, and H. Esumi. 2003. Induction of matrix metalloproteinase gene transcription by nitric oxide and mechanisms of MMP-1 gene induction in human melanoma cell lines. Int. J. Cancer 103:161-168.
25. 2+- or PI3K-dependent signaling pathway in a human vascular endothelial cell line. FEBS Lett. 579:6451-6458.
26. Lu, J., H. H. Chua, S. Y. Chen, J. Y. Chen, and C. H. Tsai. 2003. Regulation of matrix metalloproteinase-1 by Epstein-Barr virus proteins. Cancer Res. 63:256-262.
27. McCormick, C., and D. Ganem. 2005. The kaposin B protein of KSHV activates the p38/MK2 pathway and stabilizes cytokine mRNAs. Science 307:739-741.
28. McQuibban, G. A., J. H. Gong, E. M. Tam, C. A. McCulloch, I. Clark-Lewis, and C. M. Overall. 2000. Inflammation dampened by gelatinase A cleavage of monocyte chemoattractant protein-3. Science 289:1202-1206.
29. Meade-Tollin, L. C., D. Way, and M. H. Witte. 1999. Expression of multiple matrix metalloproteinases and urokinase type plasminogen activator in cultured Kaposi sarcoma cells. Acta Histochem. 101:305-316.
30. Naranatt, P. P., H. H. Krishnan, S. R. Svojanovsky, C. Bloomer, S. Mathur, and B. Chandran. 2004. Host gene induction and transcriptional reprogramming in Kaposi's sarcoma-associated herpesvirus (KSHV/HHV-8)-infected endothelial, fibroblast, and B cells: insights into modulation events early during infection. Cancer Res. 64:72-84.
31. Nawrocki-Raby, B., C. Gilles, M. Polette, C. Martinella-Catusse, N. Bonnet, E. Puchelle, J. M. Foidart, F. Van Roy, and P. Birembaut. 2003. E-cadherin mediates MMP down-regulation in highly invasive bronchial tumor cells. Am. J. Pathol. 163:653-661.
32. Nguyen, M., J. Arkell, and C. J. Jackson. 1998. Active and tissue inhibitor of matrix metalloproteinase-free gelatinase B accumulates within human microvascular endothelial vesicles. J. Biol. Chem. 273:5400-5404.
33. Overall, C. M., and O. Kleifeld. 2006. Tumour microenvironment. Opinion: validating matrix metalloproteinases as drug targets and anti-targets for cancer therapy. Nat. Rev. Cancer 6:227-239.
34. Pan, H., J. Xie, F. Ye, and S. J. Gao. 2006. Modulation of Kaposi's sarcoma-associated herpesvirus infection and replication by MEK/ERK, JNK, and p38 multiple mitogen-activated protein kinase pathways during primary infection. J. Virol. 80:5371-5382.
35. Parks, W. C., C. L. Wilson, and Y. S. Lopez-Boado. 2004. Matrix metalloproteinases as modulators of inflammation and innate immunity. Nat. Rev. Immunol. 4:617-629.
36. Pirila, E., A. Sharabi, T. Salo, V. Quaranta, H. Tu, R. Heljasvaara, N. Koshikawa, T. Sorsa, and P. Maisi. 2003. Matrix metalloproteinases process the laminin-5 gamma 2-chain and regulate epithelial cell migration. Biochem. Biophys. Res. Commun. 303:1012-1017.
37. Radisky, D. C., D. D. Levy, L. E. Littlepage, H. Liu, C. M. Nelson, J. E. Fata, D. Leake, E. L. Godden, D. G. Albertson, M. A. Nieto, Z. Werb, and M. J. Bissell. 2005. Rac1b and reactive oxygen species mediate MMP-3-induced EMT and genomic instability. Nature 436:123-127.
38. Schenk, S., and V. Quaranta. 2003. Tales from the crypt[ic] sites of the extracellular matrix. Trends Cell Biol. 13:366-375.
39. Steinle, J. J., C. J. Meininger, R. Forough, G. Wu, M. H. Wu, and H. J. Granger. 2002. Eph B4 receptor signaling mediates endothelial cell migration and proliferation via the phosphatidylinositol 3-kinase pathway. J. Biol. Chem. 277:43830-43835.
40. Taraboletti, G., S. D'Ascenzo, P. Borsotti, R. Giavazzi, A. Pavan, and V. Dolo. 2002. Shedding of the matrix metalloproteinases MMP-2, MMP-9, and MT1-MMP as membrane vesicle-associated components by endothelial cells. Am. J. Pathol. 160:673-680.
41. Thompson, E. W., S. Nakamura, T. B. Shima, A. Melchiori, G. R. Martin, S. Z. Salahuddin, R. C. Gallo, and A. Albini. 1991. Supernatants of acquired immunodeficiency syndrome-related Kaposi's sarcoma cells induce endothelial cell chemotaxis and invasiveness. Cancer Res. 51:2670-2676.
42. Toschi, E., G. Barillari, C. Sgadari, I. Bacigalupo, A. Cereseto, D. Carlei, C. Palladino, C. Zietz, P. Leone, M. Sturzl, S. Butto, A. Cafaro, P. Monini, and B. Ensoli. 2001. Activation of matrix-metalloproteinase-2 and membrane-type-1-matrix-metalloproteinase in endothelial cells and induction of vascular permeability in vivo by human immunodeficiency virus-1 Tat protein and basic fibroblast growth factor. Mol. Biol. Cell 12:2934-2946.
43. Vihinen, P., and V. M. Kahari. 2002. Matrix metalloproteinases in cancer: prognostic markers and therapeutic targets. Int. J. Cancer 99:157-166.
44. Visse, R., and H. Nagase. 2003. Matrix metalloproteinases and tissue inhibitors of metalloproteinases: structure, function, and biochemistry. Circ. Res. 92:827-839.
45. Wang, H. W., M. W. Trotter, D. Lagos, D. Bourboulia, S. Henderson, T. Makinen, S. Elliman, A. M. Flanagan, K. Alitalo, and C. Boshoff. 2004. Kaposi sarcoma herpesvirus-induced cellular reprogramming contributes to the lymphatic endothelial gene expression in Kaposi sarcoma. Nat. Genet. 36:687-693.
46. Wang, L., N. Wakisaka, C. C. Tomlinson, S. M. DeWire, S. Krall, J. S. Pagano, and B. Damania. 2004. The Kaposi's sarcoma-associated herpesvirus (KSHV/HHV-8) K1 protein induces expression of angiogenic and invasion factors. Cancer Res. 64:2774-2781.
47. Xie, J., H. Pan, S. Yoo, and S. J. Gao. 2005. Kaposi's sarcoma-associated herpesvirus induction of AP-1 and interleukin 6 during primary infection mediated by multiple mitogen-activated protein kinase pathways. J. Virol. 79:15027-15037.
48. Ye, F. C., D. J. Blackbourn, M. Mengel, J. P. Xie, L. W. Qian, W. Greene, I. T. Yeh, D. Graham, and S. J. Gao. 2007. Kaposi's sarcoma-associated herpes-virus promotes angiogenesis by inducing angiopoietin-2 expression via AP-1 and Ets1. J. Virol. 81:3980-3991.
49. Yoo, S. M., F. C. Zhou, F. C. Ye, H. Y. Pan, and S. J. Gao. 2005. Early and sustained expression of latent and host modulating genes in coordinated transcriptional program of KSHV productive primary infection of human primary endothelial cells. Virology 343:47-64.
50. Yoshizaki, T., H. Sato, M. Furukawa, and J. S. Pagano. 1998. The expression of matrix metalloproteinase 9 is enhanced by Epstein-Barr virus latent membrane protein 1. Proc. Natl. Acad. Sci. USA 95:3621-3626.
51. Zhou, F. C., Y. J. Zhang, J. H. Deng, X. P. Wang, H. Y. Pan, E. Hettler, and S. J. Gao. 2002. Efficient infection by a recombinant Kaposi's sarcoma-associated herpesvirus cloned in a bacterial artificial chromosome: application for genetic analysis. J. Virol. 76:6185-6196.