The human cytomegalovirus UL82 gene product (pp71) accelerates progression through the G1 phase of the cell cycle

Journal of Virology

Volumn 77, Issue 6, 2003, Pages 3451-3459

  Kalejta, Robert F ^a   Shenk, Thomas ^a  

^a PRINCETON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENE PRODUCT; MUTANT PROTEIN;

ANIMAL CELL; ARTICLE; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; CONTROLLED STUDY; DNA SYNTHESIS; HOST CELL; HUMAN CYTOMEGALOVIRUS; MOUSE; NONHUMAN; PRIORITY JOURNAL; RAT; UL82 GENE; VIRUS GENE; VIRUS REPLICATION;

ANIMALS; CELL CYCLE; CELL LINE; CYTOMEGALOVIRUS; G0 PHASE; G1 PHASE; GENE EXPRESSION REGULATION, VIRAL; HUMANS; MICE; RATS; TRANSFECTION; VIRAL PROTEINS;

EID: 0037333503     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.77.6.3451-3459.2003     Document Type: Article

References (81)

1. 1/S transition by cyclins D2 and D3 in hematopoietic cells. Proc. Natl. Acad. Sci. USA 90:9571-9575.
2. Baldick, C. J., Jr., A. Marchini, C. E. Patterson, and T. Shenk. 1997. Human cytomegalovirus tegument protein pp71 (ppUL82) enhances the infectivity of viral DNA and accelerates the infectious cycle. J. Virol. 71:4400-4408.
3. Bello-Fernandez, C., G. Packham, and J. L. Cleveland. 1993. The ornithine decarboxylase gene is a transcriptional target of c-Myc. Proc. Natl. Acad. Sci. USA 90:7804-7808.
4. Boldogh, I., S. AbuBakar, and T. Albrecht. 1990. Activation of proto-oncogenes: an immediate early event in human cytomegalovirus infection. Science 247:561-564.
5. 1. Virology 224:150-160.
6. Bresnahan, W. A., and T. Shenk. 2000. UL82 virion protein activates expression of immediate early viral genes in human cytomegalovirus-infected cells. Proc. Natl. Acad. Sci. USA 97:14506-14511.
7. Brideau, A. D., B. Banfield, and L. W. Enquist. 1998. The Us9 gene product of pseudorabies virus, an alphaherpesvirus, is a phosphorylated, tail-anchored type II membrane protein. J. Virol. 72:4560-4570.
8. Browne, E. P., B. Wing, D. Coleman, and T. Shenk. 2001. Altered cellular mRNA levels in human cytomegalovirus-infected fibroblasts: viral block to the accumulation of antiviral mRNAs. J. Virol. 75:12319-12330.
9. Castillo, J. P., A. D. Yurochko, and T. F. Kowalik 2000. Role of human cytomegalovirus immediate-early proteins in cell growth control. J. Virol. 74:8028-8037.
10. Castillo, J. P., and T. F. Kowalik. 2002. Human cytomegalovirus immediate early proteins and cell growth control. Gene 290:19-34.
11. Chellappan, S., V. B. Kraus, B. Kroger, K. Munger, P. M. Howley, W. C. Phelps, and J. R. Nevins. 1992. Adenovirus E1A, simian virus 40 tumor antigen, and human papillomavirus E7 protein share the capacity to disrupt the interaction between transcription factor E2F and the retinoblastoma gene product. Proc. Natl. Acad. Sci. USA 89:4549-4553.
12. Classon, M., and N. Dyson. 2001. p107 and p130: versatile proteins with interesting pockets. Exp. Cell Res. 264:135-147.
13. 1/S transition. J. Virol. 71:1629-1634.
14. Dyson, N. 1998. The regulation of E2F proteins. Genes Dev. 12:2245-2262.
15. Estes, J. E., and E.-S. Huang. 1977. Stimulation of cellular thymidine kinases by human cytomegalovirus. J. Virol. 24:13-21.
16. Flint, J., and T. Shenk. 1997. Viral transactivating proteins. Annu. Rev. Genet. 31:177-212.
17. Goodrum, F., C. Jordan, K. High, and T. Shenk. 2002. Human cytomegalovirus gene expression during infection of primary hematopoietic progenitor cells: a model for latency. Proc. Natl. Acad. Sci. USA 99:16255-16260.
18. Goto, H., S. Motomura, A. C. Wilson, R. N. Freiman, Y. Nakabeppu, K. Fukushima, M. Fujishima, W. Herr, and T. Nishimoto. 1997. A single-point mutation in HCF causes temperature-sensitive cell-cycle arrest and disrupts VP16 function. Genes Dev. 11:726-737.
19. 1 phase dependent upon the N-terminal INK4 interaction domain. J. Biol. Chem. 274:29960-29967.
20. 1 phase of the cell cycle. Proc. Natl. Acad. Sci. USA 97:2692-2696.
21. He, T.-C., S. Zhou, L. T. DaCosta, J. Yu, K. W. Kinzler, and B. Vogelstein. 1998. A simplified system for generating recombinant adenoviruses. Proc. Natl. Acad. Sci. USA 95:2509-2514.
22. Heider, J. A., W. A. Bresnahan, and T. Shenk. 2002. Construction of a rationally designed human cytomegalovirus variant encoding a temperature-sensitive immediate-early 2 protein. Proc. Natl. Acad. Sci. USA 99:3141-3145.
23. 1/S phase transition in fibroblasts. J. Biol. Chem. 273:14958-14961.
24. Hoge, A. T., S. B. Hendrickson, and W. H. Burns. 2000. Murine gammaherpesvirus 68 cyclin D homologue is required for efficient reactivation from latency. J. Virol. 74:7016-7023.
25. Jault, F. M., J. M. Jault, F. Ruchti, E. A. Fortunato, C. Clark, J. Corbeil, D. D. Richman, and D. H. Spector. 1995. Cytomegalovirus infection induces high levels of cyclins, phosphorylated Rb, and p53, leading to cell cycle arrest. J. Virol. 69:6697-6704.
26. Jiang, W., S. M. Kahn, P. Zhou, Y. J. Zhang, A. M. Cacace, A. S. Infante, S. Doi, R. M. Santella, and I. B. Weinstein. 1993. Overexpression of cyclin D1 in rat fibroblasts causes abnormalities in growth control, cell cycle progression and gene expression. Oncogene 8:3447-3457.
27. a. Kalejta, R. F., J. T. Bechtel, and T. Shenk. Human cytomegalovirus pp71 stimulates cell cycle progression by inducing the proteasome-dependent degradation of the retinoblastoma family of tumor suppressors. Mol. Cell. Biol., in press.
28. Kalejta, R. F., T. Shenk, and A. J. Beavis. 1997. Use of a membrane-localized green fluorescent protein allows simultaneous identification of transfected cells and cell cycle analysis by flow cytometry. Cytometry 29:286-291.
29. Kalejta, R. F., A. D. Brideau, B. W. Banfield, and A. J. Beavis. 1999. An integral membrane green fluorescent protein marker, Us9-GFP, is quantitatively retained in cells during propidium iodide-based cell cycle analysis by flow cytometry. Exp. Cell Res. 248:322-328.
30. Kalejta, R. F., and T. Shenk. 2002. Manipulation of the cell cycle by human cytomegalovirus. Front. Biosci. 7:d295-d306.
31. 1 cyclins D2 and D3, but not D1. Proc. Natl. Acad. Sci. USA 90:11513-11517.
32. 1 phase progression induced by the human T cell leukemia virus type 1 (HTLV-1) Tax oncoprotein. J. Biol. Chem. 276:31851-31857.
33. Lipinski, M. M., and T. Jacks. 1999. The retinoblastoma gene family in differentiation and development. Oncogene 55:7873-7882.
34. Liu, B., and M. F. Stinski. 1992. Human cytomegalovirus contains a tegument protein that enhances transcription from promoters with upstream ATF and AP-1 cis-acting elements. J. Virol. 66:4434-4444.
35. 1 progression in NIH 3T3 cells. Mol. Cell. Biol. 15:3654-3663.
36. 1 to S. J. Virol. 70:8850-8857.
37. 1 phase of the cell cycle. J. Virol. 73:676-683.
38. Marchini, A., H. Liu, and H. Zhu. 2001. Human cytomegalovirus with IE-2 (UL122) deleted fails to express early lytic genes. J. Virol. 75:1870-1878.
39. 1/S transition in human papillomavirus type 16 E7-expressing human cells is associated with altered regulation of cyclin E. J. Virol. 72:975-985.
40. + bone marrow progenitors. J. Gen. Virol. 77:3099-3102.
41. 1/S-phase boundary is suppressed by inhibitory c-Myc mutants. Mol. Cell. Biol. 15:2527-2535.
42. Minton, E. J., C. Tysoe, J. H. Sinclair, and J. G. P. Sissons. 1994. Human cytomegalovirus infection of the monocyte/macrophage lineage in bone marrow. J. Virol. 68:4017-4021.
43. Mittereder, N., K. L. March, and B. C. Trapnell. 1996. Evaluation of the concentration and bioactivity of adenovirus vectors for gene therapy. J. Virol. 70:7498-7509.
44. Mocarski, E. S., G. W. Kemble, J. M. Lyle, and R. F. Greaves. 1996. A deletion mutant in the human cytomegalovirus gene encoding IE1 (491aa) is replication defective due to a failure in autoregulation. Proc. Natl. Acad. Sci. USA 93:11321-11326.
45. Mocarski, E. S., and C. T. Courcelle. 2001. Cytomegaloviruses and their replication, p. 2629-2673. In D. M. Knipe, P. M. Howley, D. E. Griffin, R. A. Lamb, M. A. Martin, B. Roizman, and S. E. Straus (ed.), Fields virology. Lippincott Williams & Wilkins, Philadelphia, Pa.
46. Murphy, E. A., D. N. Streblow, J. A. Nelson, and M. F. Stinski. 2000. The human cytomegalovirus IE86 protein can block cell cycle progression after inducing transition into the S phase of permissive cells. J. Virol. 74:7108-7118.
47. 1 to complete the cell cycle. Proc. Natl. Acad. Sci. USA 91:8022-8026.
48. Nowak, B., C. Sullivan, P. Sarnow, R. Thomas, F. Bricout, J. C. Nicolas, B. Fleckenstein, and A. J. Levine. 1984. Characterization of monoclonal antibodies and polyclonal immune sera directed against human cytomegalovirus virion proteins. Virology 132:325-338.
49. Nowak, B., A. Gmeiner, P. Sarnow, A. J. Levine, and B. Fleckenstein. 1984. Physical mapping of human cytomegalovirus genes: identification of DNA sequences coding for a virion phosphoprotein of 71 kDa and a viral 65-kDa polypeptide. Virology 134:91-102.
50. Ohtani, K., J. DeGregori, and J. R. Nevins. 1995. Regulation of the cyclin E gene by transcription factor E2F1. Proc. Natl. Acad. Sci. USA 92:12146-12150.
51. 1 in mammalian fibroblasts. Science 259:1908-1912.
52. 1to-S phase transition. Mol. Cell. Biol. 15:2612-2624.
53. Pajovic, S., E. L. Wong, A. R. Black, and J. C. Azizkhan. 1997. Identification of a viral kinase that phosphorylates specific E2Fs and pocket proteins. Mol. Cell. Biol. 17:6459-6464.
54. Poma, E. E., T. F. Kowalik, L. Zhu, J. H. Sinclair, and E.-S. Huang. 1996. The human cytomegalovirus IE1-72 protein interacts with the cellular p107 protein and relieves p107-mediated transcriptional repression of an E2F-responsive promoter. J. Virol. 70:7867-7877.
55. 1 phase in rodent fibroblasts. Genes Dev. 7:1559-1571.
56. 1 control in mammalian cells. J. Cell Sci. Suppl. 18:69-73.
57. 1/S phase transition by expression of cyclins D1 and E with an inducible system. Mol. Cell. Biol. 14:1669-1679.
58. 1-to-S transition. Mol. Cell. Biol. 15:3463-3469.
59. Kip1. Mol. Cell. Biol. 15:4347-4352.
60. Romanowski, M. J., and T. Shenk. 1997. Characterization of the human cytomegalovirus irsl and trsl genes: a second immediate-early transcription unit within irsl whose product antagonizes transcriptional activation. J. Virol. 71:1485-1496.
61. Rosenberg, A. R., F. Zindy, F. L. Deist, H. Mouly, P. Metezeau, C. Brechot, and E. Lamas. 1995. Overexpression of human cyclin A advances entry into S phase. Oncogene 10:1501-1509.
62. Ruger, B., S. Klages, B. Walla, J. Albrecht, B. Fleckenstein, P. Tomlinson, and B. Barrell. 1987. Primary structure and transcription of the genes coding for the two virion phosphoproteins pp65 and pp71 of human cytomegalovirus. J. Virol. 61:446-453.
63. Salvant, B. S., E. A. Fortunato, and D. H. Spector. 1998. Cell cycle dysregulation by human cytomegalovirus: influence of the cell cycle phase at the time of infection and effects on cyclin transcription. J. Virol. 72:3729-3741.
64. Shen, Y., H. Zhu, and T. Shenk. 1997. Human cytomegalovirus IE1 and IE2 proteins are mutagenic and mediate "hit-and-run" oncogenic transformation in cooperation with the adenovirus E1A proteins. Proc. Natl. Acad. Sci. USA 94:3341-3345.
65. 1 cyclin-dependent kinases. Genes Dev. 9:1149-1163.
66. Soderberg-Naucler, C., K. N. Fish, and J. A. Nelson. 1997. Reactivation of latent human cytomegalovirus by allogenic stimulation of blood cells from healthy donors. Cell 91:119-126.
67. Song, Y. J., and M. F. Stinski. 2002. Effect of the human cytomegalovirus IE86 protein on expression of E2F-responsive genes: a DNA microarray analysis. Proc. Natl. Acad. Sci. USA 99:2836-2841.
68. Stokke, T., K. Solberg, P. DeAngelis, and H. B. Steen. 1998. Propidium iodide quenches the fluorescence of TdT-incorporated FITC-labeled dUTP in apoptotic cells. Cytometry 33:428-434.
69. 1 phase of the cell cycle. J. Biol. Chem. 275:3438-3445.
70. Taylor-Wiedeman, J., P. Sissons, and J. Sinclair. 1994. Induction of endogenous human cytomegalovirus gene expression after differentiation of monocytes from healthy carriers. J. Virol. 68:1597-1604.
71. Tseng, Y. H., D. Vicent, J. Zhu, Y. Niu, A. Adeyinka, J. S. Moyers, P. H. Watson, and C. R. Kahn. 2001. Regulation of growth and tumorigenicity of breast cancer cells by the low molecular weight GTPase Rad and Nm23. Cancer Res. 61:2071-2079.
72. Van Dyk, L. F., J. L. Hess, J. D. Katz, M. Jacoby, S. H. Speck, and H. W. Virgin IV. 1999. The murine gammaherpesvirus 68 v-cyclin gene is an oncogene that promotes cell cycle progression in primary lymphocytes. J. Virol. 73:5110-5122.
73. Van Dyk, L. F., H. W. Virgin IV, and S. H. Speck. 2000. The murine gammaherpesvirus 68 v-cyclin is a critical regulator of reactivation from latency. J. Virol. 74:7451-7461.
74. Wade, M., T. F. Kowalik, M. Mudryj, E.-S. Huang, and J. C. Azizkhan. 1992. E2F mediates dihydrofolate reductase promoter activation and multiprotein complex formation in human cytomegalovirus infection. Mol. Cell. Biol. 12:4364-4374.
75. Weinberg, R. A. 1995. The retinoblastoma protein and cell cycle control. Cell 81:323-330.
76. 1. J. Virol. 73:9274-9283.
77. Wiebusch, L., and C. Hagemeier. 2001. The human cytomegalovirus immediate early 2 protein dissociates cellular DNA synthesis from cyclin-dependent kinase activation. EMBO J. 20:1086-1098.
78. 1 progression through tetracycline-regulated expression of human cyclin E. Oncogene 9:995-997.
79. Zhu, H., Y. Shen, and T. Shenk. 1995. Human cytomegalovirus IE1 and IE2 proteins block apoptosis. J. Virol. 69:7960-7970.
80. Zhu, H., J. P. Cong, and T. Shenk. 1997. Use of differential display analysis to asses the effect of human cytomegalovirus infection on the accumulation of cellular RNAs: induction of interferon-responsive RNAs. Proc. Natl. Acad. Sci. USA 94:13985-13990.
81. Zhu, H., J. P. Cong, G. Mamtora, T. Gingeras, and T. Shenk. 1998. Cellular gene expression altered by human cytomegalovirus: global monitoring with oligonucleotide arrays. Proc. Natl. Acad. Sci. USA 95:14470-14475.