Kaposi's sarcoma-associated herpesvirus K-cyclin interacts with Cdk9 and stimulates Cdk9-mediated phosphorylation of p53 tumor suppressor

Journal of Virology

Volumn 82, Issue 1, 2008, Pages 278-290

  Chang, Pei Ching ^a   Li, Mengtao ^a,b  

^a UNIVERSITY OF KENTUCKY COLLEGE OF DENTISTRY   (United States)

^b NONE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE 6; CYCLIN DEPENDENT KINASE 9; K CYCLIN; PROTEIN P53; SERINE; SHORT HAIRPIN RNA; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ARTICLE; BINDING SITE; CELL CYCLE REGULATION; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; ENZYME REGULATION; ENZYME SUBUNIT; GENE MAPPING; GROWTH INHIBITION; HUMAN; HUMAN CELL; HUMAN HERPESVIRUS 8; IN VIVO STUDY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION;

CELL CYCLE; CELL LINE; CYCLIN-DEPENDENT KINASE 9; CYCLINS; HERPESVIRUS 8, HUMAN; HUMANS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; TUMOR SUPPRESSOR PROTEIN P53; VIRAL PROTEINS;

HERPESVIRIDAE;

EID: 37349085275     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01552-07     Document Type: Article

References (79)

1. Bark-Jones, S. J., H. M. Webb, and M. J. West. 2006. EBV EBNA 2 stimulates CDK9-dependent transcription and RNA polymerase II phosphorylation on serine 5. Oncogene 25:1775-1785.
2. Bergman, R., M. Ramon, S. Kilim, C. Lichtig, and R. Friedman-Birnbaum. 1996. An immunohistochemical study of p53 protein expression in classical Kaposi's sarcoma. Am. J. Dermatopathol. 18:367-370.
3. Bode, A. M., and Z. Dong. 2004. Post-translational modification of p53 in tumorigenesis. Nat. Rev. Cancer 4:793-805.
4. Boshoff, C. 2003. Kaposi virus scores cancer coup. Nat. Med. 9:261-262.
5. Boshoff, C., T. F. Schulz, M. M. Kennedy, A. K. Graham, C. Fisher, A. Thomas, J. O. McGee, R. A. Weiss, and J. J. O'Leary. 1995. Kaposis sarcoma-associated herpesvirus infects endothelial and spindle cells. Nat. Med. 1:1274-1278.
6. Boulanger, E., L. Gerard, J. Gabarre, J. M. Molina, C. Rapp, J. F. Abino, J. Cadranel, S. Chevret, and E. Oksenhendler. 2005. Prognostic factors and outcome of human herpesvirus 8-associated primary effusion lymphoma in patients with AIDS. J. Clin. Oncol. 23:4372-4380.
7. Brooks, C. L., and W. Gu. 2003. Ubiquitination, phosphorylation and acetylation: the molecular basis for p53 regulation. Curr. Opin. Cell Biol. 15:164-171.
8. Brooks, L. A., A. J. Wilson, and T. Crook. 1997. Kaposi's sarcoma-associated herpesvirus (KSHV)/human herpesvirus 8 (HHV8) - a new human tumour virus. J. Pathol. 182:262-265.
9. Bulavin, D. V., S. Saito, M. C. Hollander, K. Sakaguchi, C. W. Anderson, E. Appella, and A. J. Fornace, Jr. 1999. Phosphorylation of human p53 by p38 kinase coordinates N-terminal phosphorylation and apoptosis in response to UV radiation. EMBO J. 18:6845-6854.
10. Bullrich, F., T. K. MacLachlan, N. Sang, T. Druck, M. L. Veronese, S. L. Allen, N. Chiorazzi, A. Koff, K. Heubner, C. M. Croce, et al. 1995. Chromosomal mapping of members of the cdc2 family of protein kinases, cdk3, cdk6, PISSLRE, and PITALRE, and a cdk inhibitor, p27Kip1, to regions involved in human cancer. Cancer Res. 55:1199-1205.
11. Cannell, E., and S. Mittnacht. 1999. Viral encoded cyclins. Semin. Cancer Biol. 9:221-229.
12. Cesarman, E., R. G. Nador, F. Bai, R. A. Bohenzky, J. J. Russo, P. S. Moore, Y. Chang, and D. M. Knowles. 1996. Kaposi's sarcoma-associated herpesvirus contains G protein-coupled receptor and cyclin D homologs which are expressed in Kaposi's sarcoma and malignant lymphoma. J. Virol. 70:8218-8223.
13. 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.
14. Child, E. S., and D. J. Mann. 2001. Novel properties of the cyclin encoded by human herpesvirus 8 that facilitate exit from quiescence. Oncogene 20:3311-3322.
15. Claudio, P. P., J. Cui, M. Ghafouri, C. Mariano, M. K. White, M. Safak, J. B. Sheffield, A. Giordano, K. Khalili, S. Amini, and B. E. Sawaya. 2006. Cdk9 phosphorylates p53 on serine 392 independently of CKII. J. Cell Physiol. 208:602-612.
16. Coqueret, O. 2002. Linking cyclins to transcriptional control. Gene 299:35-55.
17. Cuomo, M. E., A. Knebel, G. Platt, N. Morrice, P. Cohen, and S. Mittnacht. 2005. Regulation of microfilament organization by Kaposi sarcoma-associated herpes virus-cyclin.CDK6 phosphorylation of caldesmon. J. Biol. Chem. 280:35844-35858.
18. Dada, M. A., R. Chetty, S. C. Biddolph, J. W. Schneider, and K. C. Gatter. 1996. The immunocxpression of bcl-2 and p53 in Kaposi's sarcoma. Histopathology 29:159-163.
19. Davis, M. A., M. A. Sturzl, C. Blasig, A. Schreier, H. G. Guo, M. Reitz, S. R. Opalenik, and P. J. Browning. 1997. Expression of human herpesvirus 8-encoded cyclin D in Kaposi's sarcoma spindle cells. J. Natl. Cancer Inst. 89:1868-1874.
20. De Falco, G., and A. Giordano. 2002. CDK9: from basal transcription to cancer and AIDS. Cancer Biol. Ther. 1:342-347.
21. Dittmer, D. P. 2003. Transcription profile of Kaposi's sarcoma-associated herpesvirus in primary Kaposi's sarcoma lesions as determined by real-time PCR arrays. Cancer Res. 63:2010-2015.
22. Durand, L. O., S. J. Advani, A. P. Poon, and B. Roizman. 2005. The carboxyl-terminal domain of RNA polymerase II is phosphorylated by a complex containing cdk9 and infected-cell protein 22 of herpes simplex virus 1. J. Virol. 79:6757-6762.
23. Duro, D., A. Schulze, B. Vogt, J. Bartek, S. Mittnacht, and P. Jansen-Durr. 1999. Activation of cyclin A gene expression by the cyclin encoded by human herpesvirus-8. J. Gen. Virol. 80:549-555.
24. Dynlacht, B. D. 1997. Regulation of transcription by proteins that control the cell cycle. Nature 389:149-152.
25. Ellis, M., Y. P. Chew, L. Fallis, S. Freddersdorf, C. Boshoff, R. A. Weiss, X. Lu, and S. Mittnacht. 1999. Degradation of p27(Kip) cdk inhibitor triggered by Kaposi's sarcoma virus cyclin-cdk6 complex. EMBO J. 18:644-653.
26. Flemington, E. K. 2001. Herpesvirus lytic replication and the cell cycle: arresting new developments. J. Virol. 75:4475-4481.
27. Friborg, J., Jr., W. Kong, M. O. Hottiger, and G. J. Nabel. 1999. p53 inhibition by the LANA protein of KSHV protects against cell death. Nature 402:889-894.
28. Fu, T. J., J. Peng, G. Lee, D. H. Price, and O. Flores. 1999. Cyclin K functions as a CDK9 regulatory subunit and participates in RNA polymerase II transcription. J. Biol. Chem. 274:34527-34530.
29. Ganem, D. 1997. KSHV and Kaposi's sarcoma: the end of the beginning? Cell 91:157-160.
30. Garriga, J., and X. Grana. 2004. Cellular control of gene expression by T-type cyclin/CDK9 complexes. Gene 337:15-23.
31. Garriga, J., X. Mayol, and X. Grana. 1996. The CDC2-relatcd kinase PITALRE is the catalytic subunit of active multimeric protein complexes. Biochem. J. 319:293-298.
32. Godden-Kent, D., S. J. Talbot, C. Boshoff, Y. Chang, P. Moore, R. A. Weiss, and S. Mittnacht. 1997. The cyclin encoded by Kaposi's sarcoma-associated herpesvirus stimulates cdk6 to phosphorylate the retinoblastoma protein and histone H1. J. Virol. 71:4193-4198.
33. Gold, M. O., X. Yang, C. H. Herrmann, and A. P. Rice. 1998. PITALRE, the catalytic subunit of TAK, is required for human immunodeficiency virus Tat transactivation in vivo. J. Virol. 72:4448-4453.
34. Hodak, E., I. Hammel, M. Feinmesser, A. Zelinger, L. Maron, J. Sulkes, and M. David. 1999. Differential expression of p53 and Ki-67 proteins in classic and iatrogenic Kaposi's sarcoma. Am. J. Dermatopathol. 21:138-145.
35. Hollstein, M., D. Sidransky, B. Vogelstein, and C. C. Harris. 1991. p53 mutations in human cancers. Science 253:49-53.
36. Izumiya, Y., S. F. Lin, T. J. Ellison, A. M. Levy, G. L. Mayeur, C. Izumiya, and H. J. Kung. 2003. Cell cycle regulation by Kaposi's sarcoma-associated herpesvirus K-bZIP: direct interaction with cyclin-CDK2 and induction of G, growth arrest. J. Virol. 77:9652-9661.
37. 1 arrest. Mol. Cell. Biol. 26:2430-2440.
38. Jarviluoma, A., and P. M. Ojala. 2006. Cell signaling pathways engaged by KSHV. Biochim. Biophys. Acta 1766:140-158.
39. Jung, J. U., M. Stager, and R. C. Desrosiers. 1994. Virus-encoded cyclin. Mol. Cell. Biol. 14:7235-7244.
40. Kaldis, P., P. M. Ojala, L. Tong, T. P. Makela, and M. J. Solomon. 2001. CAK-independent activation of CDK6 by a viral cyclin. Mol. Biol. Cell 12:3987-3999.
41. Katano, H., Y. Sato, and T. Sata. 2001. Expression of p53 and human herpesvirus-8 (HHV-8)-encoded latency-associated nuclear antigen with inhibition of apoptosis in HHV-8-associated malignancies. Cancer 92:3076-3084.
42. 1 arrest through p53 phosphorylation at Ser33 by activated p38MAPK without phosphorylation at Ser15 and Ser20. J. Biol. Chem. 276:39115-39122.
43. Laman, H., D. Coverley, T. Krude, R. Laskey, and N. Jones. 2001. Viral cyclin-cyclin-dependent kinase 6 complexes initiate nuclear DNA replication. Mol. Cell. Biol. 21:624-635.
44. Lee, J. H., and K. T. Kim. 2007. Regulation of cyclin-dependent kinase 5 and p53 by ERK1/2 pathway in the DNA damage-induced neuronal death. J. Cell Physiol. 210:784-797.
45. Li, J. J., Y. Q. Huang, C. J. Cockerell, W. G. Zhang, A. Nicolaides, and A. E. Friedman-Kien. 1997. Expression and mutation of the tumor suppressor gene p53 in AIDS-associated Kaposi's sarcoma. Am. J. Dermatopathol. 19:373-378.
46. Li, M., H. Lee, D. W. Yoon, J. C. Albrecht, B. Fleckenstein, F. Neipel, and J. U. Jung. 1997. Kaposi's sarcoma-associated herpesvirus encodes a functional cyclin. J. Virol. 71:1984-1991.
47. Lundquist, A., B. Barre, F. Bienvenu, J. Hermann, S. Avril, and O. Coqueret. 2003. Kaposi sarcoma-associated viral cyclin K overrides cell growth inhibition mediated by oncostatin M through STAT3 inhibition. Blood 101:4070-4077.
48. Kip1 levels by the cyclin encoded by Kaposi's sarcoma-associated herpesvirus. EMBO J. 18:654-663.
49. Marshall, N. F., J. Peng, Z. Xie, and D. H. Price. 1996. Control of RNA polymerase II elongation potential by a novel carboxyl-terminal domain kinase. J. Biol. Chem. 271:27176-27183.
50. Mauser, A., S. Saito, E. Appella, C. W. Anderson, W. T. Seaman, and S. Kenney. 2002. The Epstein-Barr virus immediate-early protein BZLF1 regulates p53 function through multiple mechanisms. J. Virol. 76:12503-12512.
51. Moore, P. S., and Y. Chang. 2003. Kaposi's sarcoma-associated herpesvirus immunoevasion and tumorigenesis: two sides of the same coin? Annu. Rev. Microbiol. 57:609-639.
52. Muller, E., and K. H. Scheidtmann. 1995. Purification and characterization of a protein kinase which is activated by SV40 large T-antigen and phosphorylatcs the tumor suppressor protein p53. Oncogene 10:1175-1185.
53. Nador, R. G., E. Cesarman, A. Chadburn, D. B. Dawson, M. Q. Ansari, J. Said, and D. M. Knowles. 1996. Primary effusion lymphoma: a distinct clinicopathologic entity associated with the Kaposi's sarcoma-associated herpes virus. Blood 88:645-656.
54. Nakamura, H., M. Li, J. Zarycki, and J. U. Jung. 2001. Inhibition of p53 tumor suppressor by viral interferon regulatory factor. J. Virol. 75:7572-7582.
55. Noel, J. C., F. De Thier, T. Simonart, J. Andre, P. Hermans, J. P. Van Vooren, and M. Heenen. 1997. p53 protein overexpression is a common but late event in the pathogenesis of iatrogenic and AIDS-related Kaposi's sarcoma. Arch. Dermatol. Res. 289:660-661.
56. Ojala, P. M., M. Tiainen, P. Salven, T. Veikkola, E. Castanos-Velez, R. Sarid, P. Biberfeld, and T. P. Makela. 1999. Kaposi's sarcoma-associated herpesvirus-encoded v-cyclin triggers apoptosis in cells with high levels of cyclin-dependent kinase 6. Cancer Res. 59:4984-4989.
57. Ojala, P. M., K. Yamamoto, E. Castanos-Velez, P. Biberfeld, S. J. Korsmeyer, and T. P. Makela. 2000. The apoptotic v-cyclin-CDK6 complex phosphorylates and inactivates Bcl-2. Nat. Cell Biol. 2:819-825.
58. Oksenhendler, E., E. Boulanger, L. Galicier, M. Q. Du, N. Dupin, T. C. Diss, R. Hamoudi, M. T. Daniel, F. Agbalika, C. Boshoff, J. P. Clauvel, P. G. Isaacson, and V. Meignin. 2002. High incidence of Kaposi sarcoma-associated herpesvirus-related non-Hodgkin lymphoma in patients with HIV infection and multicentric Castleman disease. Blood 99:2331-2336.
59. Park, J., T. Seo, S. Hwang, D. Lee, Y. Gwack, and J. Choe. 2000. The K-bZIP protein from Kaposi's sarcoma-associated herpesvirus interacts with p53 and represses its transcriptional activity. J. Virol. 74:11977-11982.
60. Peng, J., Y. Zhu, J. T. Milton, and D. H. Price. 1998. Identification of multiple cyclin subunits of human P-TEFb. Genes Dev. 12:755-762.
61. Petre, C. E., S. H. Sin, and D. P. Dittmer. 2007. Functional p53 signaling in Kaposi's sarcoma-associated herpesvirus lymphomas: implications for therapy. J. Virol. 81:1912-1922.
62. Pillay, P., R. Chetty, and R. Reddy. 1999. Bcl-2 and p53 immunoprofile in Kaposi's sarcoma. Pathol. Oncol. Res. 5:17-20.
63. Platt, G. M., E. Cannell, M. E. Cuomo, S. Singh, and S. Mittnacht. 2000. Detection of the human herpesvirus 8-encoded cyclin protein in primary effusion lymphoma-dcrived cell lines. Virology 272:257-266.
64. Radhakrishnan, S. K., and A. L. Gartel. 2006. CDK9 phosphorylates p53 on serine residues 33, 315 and 392. Cell Cycle 5:519-521.
65. Romano, G., M. Kasten, G. De Falco, P. Micheli, K. Khalili, and A. Giordano. 1999. Regulatory functions of Cdk9 and of cyclin T1 in HIV tat transactivation pathway gene expression. J. Cell. Biochem. 75:357-368.
66. Rubinson, D. A., C. P. Dillon, A. V. Kwiatkowski, C. Sievers, L. Yang, J. Kopinja, D. L. Rooney, M. Zhang, M. M. Ihrig, M. T. McManus, F. B. Gertler, M. L. Scott, and L. Van Parijs. 2003. A lentivirus-based system to functionally silence genes in primary mammalian cells, stem cells and transgenic mice by RNA interference. Nat. Genet. 33:401-406.
67. Sanchez-Prieto, R., J. M. Rojas, Y. Taya, and J. S. Gutkind. 2000. A role for the p38 mitogen-acitvated protein kinase pathway in the transcriptional activation of p53 on genotoxic stress by chcmotherapeutic agents. Cancer Res. 60:2464-2472.
68. Sarek, G., A. Jarviluoma, and P. M. Ojala. 2006. KSHV viral cyclin inactivates p27KIP1 through Ser10 and Thr187 phosphorylation in proliferating primary effusion lymphomas. Blood 107:725-732.
69. Sarek, G., S. Kurki, J. Enback, G. Iotzova, J. Haas, P. Laakkonen, M. Laiho, and P. M. Ojala. 2007. Reactivation of the p53 pathway as a treatment modality for KSHV-induced lymphomas. J. Clin. Investig. 117:1019-1028.
70. Scinicariello, F., M. J. Dolan, I. Nedelcu, S. K. Tyring, and J. K. Hilliard. 1994. Occurrence of human papillomavirus and p53 gene mutations in Kaposi's sarcoma. Virology 203:153-157.
71. Simonart, T., and J. C. Noel. 2000. Increased p53 staining in non-sunexposed epidermis overlying Kaposi sarcoma. Am. J. Dermatopathol. 22:373-374.
72. Soulier, J., L. Grollet, E. Oksenhendler, P. Cacoub, D. Cazals-Hatem, P. Babinet, M. F. d'Agay, J. P. Clauvel, M. Raphael, L. Degos, et al. 1995. Kaposi's sarcoma-associated herpesvirus-like DNA sequences in multicentric Castleman's disease. Blood 86:1276-1280.
73. Swanton, C., D. J. Mann, B. Fleckenstein, F. Neipel, G. Peters, and N. Jones. 1997. Herpes viral cyclin/Cdk6 complexes evade inhibition by CDK inhibitor proteins. Nature 390:184-187.
74. Tamrakar, S., A. J. Kapasi, and D. H. Spector. 2005. Human cytomegalovirus infection induces specific hyperphosphorylation of the carboxyl-terminal domain of the large subunit of RNA polymerase II that is associated with changes in the abundance, activity, and localization of cdk9 and cdk7. J. Virol. 79:15477-15493.
75. Van Dross, R., S. Yao, S. Asad, G. Westlake, D. J. Mays, L. Barquero, S. Duell, J. A. Pietenpol, and P. J. Browning. 2005. Constitutively active K-cyclin/cdk6 kinase in Kaposi sarcoma-associated herpesvirus-infected cells. J. Natl. Cancer Inst. 97:656-666.
76. Verschuren, E. W., J. G. Hodgson, J. W. Gray, S. Kogan, N. Jones, and G. I. Evan. 2004. The role of p53 in suppression of KSHV cyclin-induced lymphomagenesis. Cancer Res. 64:581-589.
77. Verschuren, E. W., N. Jones, and G. I. Evan. 2004. The cell cycle and how it is steered by Kaposi's sarcoma-associated herpesvirus cyclin. J. Gen. Virol. 85:1347-1361.
78. Verschuren, E. W., J. Klefstrom, G. I. Evan, and N. Jones. 2002. The oncogenic potential of Kaposi's sarcoma-associated herpesvirus cyclin is exposed by p53 loss in vitro and in vivo. Cancer Cell 2:229-241.
79. Zhong, W., H. Wang, B. Herndier, and D. Ganem. 1996. Restricted expression of Kaposi sarcoma-associated herpesvirus (human herpesvirus 8) genes in Kaposi sarcoma. Proc. Natl. Acad. Sci. USA 93:6641-6646.