Latent Kaposi's sarcoma-associated herpesvirus infection of endothelial cells activates hypoxia-induced factors

Journal of Virology

Volumn 80, Issue 21, 2006, Pages 10802-10812

  Carroll, Patrick A ^a   Kenerson, Heidi L ^b   Yeung, Raymond S ^b   Lagunoff, Michael ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 1BETA; MESSENGER RNA; OXYGEN; PROTEIN SUBUNIT; PROTEIN TYROSINE KINASE; TRANSCRIPTION FACTOR; VASCULOTROPIN RECEPTOR 1;

ANGIOGENESIS; ARTICLE; CELL HYPOXIA; CONTROLLED STUDY; ENDOTHELIUM CELL; GENE EXPRESSION; GENE INDUCTION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; HUMAN HERPESVIRUS 8; HUMAN TISSUE; IN VIVO STUDY; KAPOSI SARCOMA; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN STABILITY; RECEPTOR GENE; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; TUMOR GROWTH; VIRUS GENE;

BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELLS, CULTURED; ENDOTHELIAL CELLS; GENE EXPRESSION; HERPESVIRIDAE INFECTIONS; HERPESVIRUS 8, HUMAN; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; RNA, MESSENGER; SARCOMA, KAPOSI; TRANSCRIPTION, GENETIC; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-1;

HUMAN HERPESVIRUS 8;

EID: 33750367972     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00673-06     Document Type: Article

References (63)

1. Bechtel, J. T., Y. Liang, J. Hvidding, and D. Ganem. 2003. Host range of Kaposi's sarcoma-associated herpesvirus in cultured cells. J. Virol. 77:6474-6481.
2. Bedogni, B., S. M. Welford, D. S. Cassarino, B. J. Nickoloff, A. J. Giaccia, and M. B. Powell. 2005. The hypoxic microenvironment of the skin contributes to Akt-mediated melanocyte transformation. Cancer Cells 8:443-454.
3. Blackbourn, D. J., S. Fujimura, T. Kutzkey, and J. A. Levy. 2000. Induction of human herpesvirus-8 gene expression by recombinant Interferon gamma. AIDS 14:98-99.
4. Blake, R. A., M. A. Broome, X. Liu, J. Wu, M. Gishizky, L. Sun, and S. A. Courtneidge. 2000. SU6656, a selective Src family kinase inhibitor, used to probe growth factor signaling. Mol. Cell. Biol. 20:9018-9027.
5. Bosco, M. C., M. Puppo, S. Pastorino, Z. Mi, G. Melillo, S. Massazza, A. Rapisarda, and L. Varesio. 2004. Hypoxia selectively inhibits monocyte chemoattractant protein-1 production by macrophages. J. Immunol. 172:1681-1690.
6. 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.
7. Cesarman, E., Y. Chang, P. S. Moore, J. W. Said, and D. M. Knowles. 1995. Kaposi's sarcoma-associated herpesvirus-like DNA sequences in AIDS-related body-cavity-based lymphomas. N. Engl. J. Med. 332:1186-1191.
8. Chang, J., R. Renne, D. Dittmer, and D. Ganem. 2000. Inflammatory cytokines and the reactivation of Kaposi's sarcoma-associated herpesvirus lytic replication. Virology 266:17-25.
9. 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.
10. Chen, W. J., H. W. Chen, S. L. Yu, C. H. Huang, T. D. Wang, J. J. Chen, C. T. Chien, H. Y. Chen, P. C. Yang, and Y. T. Lee. 2005. Gene expression profiles in hypoxic preconditioning using cDNA microarray analysis: altered expression of an angiogenic factor, carcinoembryonic antigen-related cell adhesion molecule 1. Shock 24:124-131.
11. Chilov, D., G. Camenisch, I. Kvietikova, U. Ziegler, M. Gassmann, and R. H. Wenger. 1999. Induction and nuclear translocation of hypoxia-inducible factor-1 (HIF-1): heterodimerization with ARNT is not necessary for nuclear accumulation of HIF-1α. J. Cell Sci. 112:1203-1212.
12. Cuneo, K. C., L. Geng, J. Tan, J. Brousal, E. T. Shinohara, K. Osusky, A. Fu, Y. Shyr, H. Wu, and D. E. Hallahan. 2006. SRC family kinase inhibitor SU6656 enhances antiangiogenic effect of irradiation. Int. J. Radiat. Oncol. Biol. Phys. 64:1197-1203.
13. Davis, D. A., A. S. Rinderknecht, J. P. Zoeteweij, Y. Aoki, E. L. Read-Connole, G. Tosato, A. Blauvelt, and R. Yarchoan. 2001. Hypoxia induces lytic replication of Kaposi sarcoma-associated herpesvirus. Blood 97:3244-3250.
14. Dery, M. A., M. D. Michaud, and D. E. Richard. 2005. Hypoxia-inducible factor 1: regulation by hypoxic and non-hypoxic activators. Int. J. Biochem. Cell. Biol. 37:535-540.
15. de Vries, C., J. A. Escobedo, H. Ueno, K. Houck, N. Ferrara, and L. T. Williams. 1992. The fms-like tyrosine kinase, a receptor for vascular endothelial growth factor. Science 255:989-991.
16. Ensoli, B., C. Sgadari, G. Barillari, M. C. Sirianni, M. Sturzl, and P. Monini. 2001. Biology of Kaposi's sarcoma. Eur. J. Cancer 37:1251-1269.
17. Epstein, A. C., J. M. Gleadle, L. A. McNeill, K. S. Hewitson, J. O'Rourke, D. R. Mole, M. Mukherji, E. Metzen, M. I. Wilson, A. Dhanda, Y. M. Tian, N. Masson, D. L. Hamilton, P. Jaakkola, R. Barstead, J. Hodgkin, P. H. Maxwell, C. W. Pugh, C. J. Schofield, and P. J. Ratcliffe. 2001. C. elegans EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation. Cell 107:43-54.
18. Frede, S., P. Freitag, T. Otto, C. Heilmaier, and J. Fandrey. 2005. The proinflammatory cytokine interleukin 1β and hypoxia cooperatively induce the expression of adrenomedullin in ovarian carcinoma cells through hypoxia inducible factor 1 activation. Cancer Res. 65:4690-4697.
19. Friedman-Birnbaum, R., S. Weltfriend, and I. Katz. 1990. Kaposi's sarcoma: retrospective study of 67 cases with the classical form. Dermatologica 180:13-17.
20. Gerber, H. P., F. Condorelli, J. Park, and N. Ferrara. 1997. Differential transcriptional regulation of the two vascular endothelial growth factor receptor genes. Flt-1, but not Flk-1/KDR, is up-regulated by hypoxia. J. Biol. Chem. 272:23659-23667.
21. Glaunsinger, B., and D. Ganem. 2004. Highly selective escape from KSHV-mediated host mRNA shutoff and its implications for viral pathogenesis. J. Exp. Med. 200:391-398.
22. Glaunsinger, B., and D. Ganem. 2004. Lytic KSHV infection inhibits host gene expression by accelerating global mRNA turnover. Mol. Cell 13:713-723.
23. Haque, M., D. A. Davis, V. Wang, I. Widmer, and R. Yarchoan. 2003. Kaposi's sarcoma-associated herpesvirus (human herpesvirus 8) contains hypoxia response elements: relevance to lytic induction by hypoxia. J. Virol. 77:6761-6768.
24. Hoffman, E. C., H. Reyes, F. F. Chu, F. Sander, L. H. Conley, B. A. Brooks, and O. Hankinson. 1991. Cloning of a factor required for activity of the Ah (dioxin) receptor. Science 252:954-958.
25. Hong, Y. K., K. Foreman, J. W. Shin, S. Hirakawa, C. L. Curry, D. R. Sage, T. Libermann, B. J. Dezube, J. D. Fingeroth, and M. Detmar. 2004. Lymphatic reprogramming of blood vascular endothelium by Kaposi sarcoma-associated herpesvirus. Nat. Genet. 36:683-685.
26. 2-dependent degradation domain via the ubiquitin-proteasome pathway. Proc. Natl. Acad. Sci. USA 95:7987-7992.
27. 2 sensing. Science 292:464-468.
28. 2-regulated prolyl hydroxylation. Science 292:468-472.
29. Jiang, B. H., F. Agani, A. Passaniti, and G. L. Semenza. 1997. V-SRC induces expression of hypoxia-inducible factor 1 (HIF-1) and transcription of genes encoding vascular endothelial growth factor and enolase 1: involvement of HIF-1 in tumor progression. Cancer Res. 57:5328-5335.
30. Koshikawa, N., A. Iyozumi, M. Gassmann, and K. Takenaga. 2003. Constitutive upregulation of hypoxia-inducible factor-1α mRNA occurring in highly metastatic lung carcinoma cells leads to vascular endothelial growth factor overexpression upon hypoxic exposure. Oncogene 22:6717-6724.
31. Kvietikova, I., R. H. Wenger, H. H. Marti, and M. Gassmann. 1995. The transcription factors ATF-1 and CREB-1 bind constitutively to the hypoxia-inducible factor-1 (HIF-1) DNA recognition site. Nucleic Acids Res. 23:4542-4550.
32. Lagunoff, M., J. Bechtel, E. Venetsanakos, A. M. Roy, N. Abbey, B. Herndier, M. McMahon, and D. Ganem. 2002. De novo infection and serial transmission of Kaposi's sarcoma-associated herpesvirus in cultured endothelial cells. J. Virol. 76:2440-2448.
33. Laor, Y., and R. A. Schwartz. 1979. Epidemiologic aspects of American Kaposi's sarcoma. J. Surg. Oncol. 12:299-303.
34. Licht, A. H., F. Muller-Holtkamp, I. Flamme, and G. Breier. 2006. Inhibition of hypoxia-inducible factor activity in endothelial cells disrupts embryonic cardiovascular development. Blood 107:584-590.
35. Makinen, T., T. Veikkola, S. Mustjoki, T. Karpanen, B. Catimel, E. C. Nice, L. Wise, A. Mercer, H. Kowalski, D. Kerjaschki, S. A. Stacker, M. G. Achen, and K. Alitalo. 2001. Isolated lymphatic endothelial cells transduce growth, survival and migratory signals via the VEGF-C/D receptor VEGFR-3. EMBO J. 20:4762-4773.
36. Maxwell, P. H., M. S. Wiesener, G. W. Chang, S. C. Clifford, E. C. Vaux, M. E. Cockman, C. C. Wykoff, C. W. Pugh, E. R. Maher, and P. J. Ratcliffe. 1999. The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 399:271-275.
37. Mercader, M., B. Taddeo, J. R. Panella, B. Chandran, B. J. Nickoloff, and K. E. Foreman. 2000. Induction of HHV-8 lytic cycle replication by inflammatory cytokines produced by HIV-1-infected T cells. Am. J. Pathol. 156:1961-1971.
38. Milligan, S., M. Robinson, E. O'Donnell, and D. J. Blackbourn. 2004. Inflammatory cytokines inhibit Kaposi's sarcoma-associated herpesvirus lytic gene transcription in in vitro-infected endothelial cells. J. Virol. 78:2591-2596.
39. Nakagawa, Y., N. Yamada, H. Shimizu, M. Shiota, M. Tamura, S. Kim-Mitsuyama, and H. Miyazaki. 2004. Tyrosine phosphatase epsilonM stimulates migration and survival of porcine aortic endothelial cells by activating c-Src. Biochem. Biophys. Res. Commun. 325:314-319.
40. 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.
41. Olofsson, B., E. Korpelainen, M. S. Pepper, S. J. Mandriota, K. Aase, V. Kumar, Y. Gunji, M. M. Jeltsch, M. Shibuya, K. Alitalo, and U. Eriksson. 1998. Vascular endothelial growth factor B (VEGF-B) binds to VEGF receptor-1 and regulates plasminogen activator activity in endothelial cells. Proc. Natl. Acad. Sci. USA 95:11709-11714.
42. Park, J. E., H. H. Chen, J. Winer, K. A. Houck, and N. Ferrara. 1994. Placenta growth factor. Potentiation of vascular endothelial growth factor bioactivity, in vitro and in vivo, and high affinity binding to Flt-1 but not to Flk-1/KDR. J. Biol. Chem. 269:25646-25654.
43. Podgrabinska, S., P. Braun, P. Velasco, B. Kloos, M. S. Pepper, and M. Skobe. 2002. Molecular characterization of lymphatic endothelial cells. Proc. Natl. Acad. Sci. USA 99:16069-16074.
44. Poole, L. J., Y. Yu, P. S. Kim, Q. Z. Zheng, J. Pevsner, and G. S. Hayward. 2002. Altered patterns of cellular gene expression in dermal microvascular endothelial cells infected with Kaposi's sarcoma-associated herpesvirus. J. Virol. 76:3395-3420.
45. Raghunand, N., R. A. Gatenby, and R. J. Gillies. 2003. Microenvironmental and cellular consequences of altered blood flow in tumours. Br. J. Radiol. 76:S11-S22.
46. Salceda, S., and J. Caro. 1997. Hypoxia-inducible factor 1α (HIF-1α) protein is rapidly degraded by the ubiquitin-proteasome system under normoxic conditions. Its stabilization by hypoxia depends on redox-induced changes. J. Biol. Chem. 272:22642-22647.
47. Samaniego, F., P. D. Markham, R. Gendelman, Y. Watanabe, V. Kao, K. Kowalski, J. A. Sonnabend, A. Pintus, R. C. Gallo, and B. Ensoli. 1998. Vascular endothelial growth factor and basic fibroblast growth factor present in Kaposi's sarcoma (KS) are induced by inflammatory cytokines and synergize to promote vascular permeability and KS lesion development. Am. J. Pathol. 152:1433-1443.
48. Sato, M., T. Tanaka, T. Maeno, Y. Sando, T. Suga, Y. Maeno, H. Sato, R. Nagai, and M. Kurabayashi. 2002. Inducible expression of endothelial PAS domain protein-1 by hypoxia in human lung adenocarcinoma A549 cells. Role of Src family kinases-dependent pathway. Am. J. Respir. Cell Mol. Biol. 26:127-134.
49. 2 homeostasis by hypoxia-inducible factor 1. Annu. Rev. Cell Dev. Biol. 15:551-578.
50. Skobe, M., L. F. Brown, K. Tognazzi, R. K. Ganju, B. J. Dezube, K. Alitalo, and M. Detmar. 1999. Vascular endothelial growth factor-C (VEGF-C) and its receptors KDR and flt-4 are expressed in AIDS-associated Kaposi's sarcoma. J. Investig. Dermatol. 113:1047-1053.
51. Sodhi, A., S. Montaner, V. Patel, M. Zohar, C. Bais, E. A. Mesri, and J. S. Gutkind. 2000. The Kaposi's sarcoma-associated herpes virus G protein-coupled receptor up-regulates vascular endothelial growth factor expression and secretion through mitogen-activated protein kinase and p38 pathways acting on hypoxia-inducible factor 1α. Cancer Res. 60:4873-4880.
52. Soulier, J., L. Grollet, E. Oksenhendler, P. Cacoub, D. Cazals-Hatem, P. Babinet, M. F. d'Agay, J. P. Clauvel, M. Raphael, L. Degos, and et al. 1995. Kaposi's sarcoma-associated herpesvirus-like DNA sequences in multicentric Castleman's disease. Blood 86:1276-1280.
53. Staskus, K. A., W. Zhong, K. Gebhard, B. Herndier, H. Wang, R. Renne, J. Beneke, J. Pudney, D. J. Anderson, D. Ganem, and A. T. Haase. 1997. Kaposi's sarcoma-associated herpesvirus gene expression in endothelial (spindle) tumor cells. J. Virol. 71:715-719.
54. Sturzl, M., H. Brandstetter, C. Zietz, B. Eisenburg, G. Raivich, D. P. Gearing, N. H. Brockmeyer, and P. H. Hofschneider. 1995. Identification of interleukin-1 and platelet-derived growth factor-B as major mitogens for the spindle cells of Kaposi's sarcoma: a combined in vitro and in vivo analysis. Oncogene 10:2007-2016.
55. Takeda, N., K. Maemura, Y. Imai, T. Harada, D. Kawanami, T. Nojiri, I. Manabe, and R. Nagai. 2004. Endothelial PAS domain protein 1 gene promotes angiogenesis through the transactivation of both vascular endothelial growth factor and its receptor, Flt-1. Circ. Res. 95:146-153.
56. Tanaka, T., H. Akiyama, H. Kanai, M. Sato, S. Takeda, K. Sekiguchi, T. Yokoyama, and M. Kurabayashi. 2002. Endothelial PAS domain protein 1 (EPAS1) induces adrenomedullin gene expression in cardiac myocytes: role of EPAS1 in an inflammatory response in cardiac myocytes. J. Mol. Cell. Cardiol. 34:739-748.
57. Tian, H., S. L. McKnight, and D. W. Russell. 1997. Endothelial PAS domain protein 1 (EPAS1), a transcription factor selectively expressed in endothelial cells. Genes Dev. 11:72-82.
58. Venetsanakos, E., A. Mirza, C. Fanton, S. R. Romanov, T. Tlsty, and M. McMahon. 2002. Induction of tubulogenesis in telomerase-immortalized human microvascular endothelial cells by glioblastoma cells. Exp. Cell Res. 273:21-33.
59. 2 tension. Proc. Natl. Acad. Sci. USA 92:5510-5514.
60. Wang, G. L., and G. L. Semenza. 1995. Purification and characterization of hypoxia-inducible factor 1. J. Biol. Chem. 270:1230-1237.
61. 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.
62. Webster-Cyriaque, J. 2002. Development of Kaposi's sarcoma in a surgical wound. N. Engl. J. Med. 346:1207-1210.
63. Yang, L., J. R. Kowalski, X. Zhan, S. M. Thomas, and F. W. Luscinskas. 2006. Endothelial cell cortactin phosphorylation by Src contributes to polymorphonuclear leukocyte transmigration in vitro. Circ. Res. 98:394-402.