Human cytomegalovirus UL28 and UL29 open reading frames encode a spliced mRNA and stimulate accumulation of immediate-early RNAs

Journal of Virology

Volumn 83, Issue 19, 2009, Pages 10187-10197

  Mitchell, Dora P ^a   Savaryn, John P ^b   Moorman, Nathaniel J ^a   Shenk, Thomas ^a   Terhune, Scott S ^a,b  

^a PRINCETON UNIVERSITY   (United States)

^b MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; MESSENGER RNA; POLYADENYLATED RNA; PROTEINASE; VIRUS DNA; VIRUS RNA;

3' UNTRANSLATED REGION; AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; CONTROLLED STUDY; CYTOPLASM; DNA REPLICATION; EMBRYO; GENE ACTIVATION; GENE DISRUPTION; GENE EXPRESSION; GENE LOCUS; GENE MUTATION; GENETIC CODE; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; HUMAN CYTOMEGALOVIRUS; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; POLYSOME; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN FOLDING; PROTEIN LOCALIZATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ISOLATION; RNA SEQUENCE; RNA SPLICING; RNA TRANSLATION; SIGNAL TRANSDUCTION; TRANSIENT EXPRESSION; VIRION; VIRUS EXPRESSION; VIRUS INFECTION; VIRUS PARTICLE; VIRUS REPLICATION;

AMINO ACID SEQUENCE; CELL NUCLEUS; CYTOMEGALOVIRUS; FIBROBLASTS; GENES, IMMEDIATE-EARLY; HUMANS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; OPEN READING FRAMES; PLASMIDS; PROMOTER REGIONS, GENETIC; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA SPLICING; RNA, VIRAL; VIRAL PROTEINS; VIRUS REPLICATION;

HUMAN HERPESVIRUS 5;

EID: 70349290582     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00396-09     Document Type: Article

References (51)

1. Adamo, J. E., J. Schroer, and T. Shenk. 2004. Human cytomegalovirus TRS1 protein is required for efficient assembly of DNA-containing capsids. J. Virol. 78:10221-10229.
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. Blais, J. D., V. Filipenko, M. Bi, H. P. Harding, D. Ron, C. Koumenis, B. G. Wouters, and J. C. Bell. 2004. Activating transcription factor 4 is translationally regulated by hypoxic stress. Mol. Cell. Biol. 24:7469-7482.
4. Bowen, N. J., N. Fujita, M. Kajita, and P. A. Wade. 2004. Mi-2/NuRD: multiple complexes for many purposes. Biochim. Biophys. Acta 1677:52-57.
5. Bresnahan, W. A., and T. E. 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.
6. Chambers, J., A. Angulo, D. Amaratunga, H. Guo, Y. Jiang, J. S. Wan, A. Bittner, K. Frueh, M. R. Jackson, P. A. Peterson, M. G. Erlander, and P. Ghazal. 1999. DNA microarrays of the complex human cytomegalovirus genome: profiling kinetic class with drug sensitivity of viral gene expression. J. Virol. 73:5757-5766. (Pubitemid 29274862)
7. Chee, M. S., A. T. Bankier, S. Beck, R. Bohni, C. M. Brown, R. Cerny, T. Horsnell, C. A. Hutchison III, T. Kouzarides, J. A. Martignetti, et al. 1990. Analysis of the protein-coding content of the sequence of human cytomegalovirus strain AD169. Curr. Top. Microbiol. Immunol. 154:125-169.
8. Chen, F., C. C. MacDonald, and J. Wilusz. 1995. Cleavage site determinants in the mammalian polyadenylation signal. Nucleic Acids Res. 23:2614-2620.
9. Child, S. J., M. Hakki, K. L. De Niro, and A. P. Geballe. 2004. Evasion of cellular antiviral responses by human cytomegalovirus TRS1 and IRS1. J. Virol. 78:197-205. (Pubitemid 37549732)
10. Chou, S., G. I. Marousek, A. E. Senters, M. G. Davis, and K. K. Biron. 2004. Mutations in the human cytomegalovirus UL27 gene that confer resistance to maribavir. J. Virol. 78:7124-7130. (Pubitemid 38781550)
11. Cicin-Sain, L., Z. Ruzsics, J. Podlech, I. Bubic, C. Menard, S. Jonjic, M. J. Reddehase, and U. H. Koszinowski. 2008. Dominant-negative FADD rescues the in vivo fitness of a cytomegalovirus lacking an antiapoptotic viral gene. J. Virol. 82:2056-2064. (Pubitemid 351293508)
12. Cuevas-Bennett, C., and T. Shenk. 2008. Dynamic histone H3 acetylation and methylation at human cytomegalovirus promoters during replication in fibroblasts. J. Virol. 82:9525-9536.
13. Davison, A. J., A. Dolan, P. Akter, C. Addison, D. J. Dargan, D. J. Alcendor, D. J. McGeoch, and G. S. Hayward. 2003. The human cytomegalovirus genome revisited: comparison with the chimpanzee cytomegalovirus genome. J. Gen. Virol. 84:17-28.
14. Denslow, S. A., and P. A. Wade. 2007. The human Mi-2/NuRD complex and gene regulation. Oncogene 26:5433-5438. (Pubitemid 47255925)
15. Efstathiou, S., G. L. Lawrence, C. M. Brown, and B. G. Barrell. 1992. Identification of homologues to the human cytomegalovirus US22 gene family in human herpesvirus 6. J. Gen. Virol. 73(Pt. 7):1661-1671.
16. Feng, X., J. Schroer, D. Yu, and T. Shenk. 2006. Human cytomegalovirus pUS24 is a virion protein that functions very early in the replication cycle. J. Virol. 80:8371-8378. (Pubitemid 44384850)
17. Hakki, M., and A. P. Geballe. 2005. Double-stranded RNA binding by human cytomegalovirus pTRS1. J. Virol. 79:7311-7318. (Pubitemid 40756766)
18. Hwang, J., and R. F. Kalejta. 2007. Proteasome-dependent, ubiquitin-independent degradation of Daxx by the viral pp71 protein in human cytomegalovirus-infected cells. Virology 367:334-338. (Pubitemid 47494530)
19. Ioudinkova, E., M. C. Arcangeletti, A. Rynditch, F. De Conto, F. Motta, S. Covan, F. Pinardi, S. V. Razin, and C. Chezzi. 2006. Control of human cytomegalovirus gene expression by differential histone modifications during lytic and latent infection of a monocytic cell line. Gene 384:120-128. (Pubitemid 44738333)
20. 1 phase of the cell cycle. J. Virol. 77:3451-3459.
21. Kawai, T., J. Fan, K. Mazan-Mamczarz, and M. Gorospe. 2004. Global mRNA stabilization preferentially linked to translational repression during the endoplasmic reticulum stress response. Mol. Cell. Biol. 24:6773-6787.
22. Li, J., G. Pan, K. Cui, Y. Liu, S. Xu, and D. Pei. 2007. A dominant-negative form of mouse SOX2 induces trophectoderm differentiation and progressive polyploidy in mouse embryonic stem cells. J. Biol. Chem. 282:19481-19492.
23. Lorz, K., H. Hofmann, A. Berndt, N. Tavalai, R. Mueller, U. Schlotzer-Schrehardt, and T. Stamminger. 2006. Deletion of open reading frame UL26 from the human cytomegalovirus genome results in reduced viral growth, which involves impaired stability of viral particles. J. Virol. 80:5423-5434. (Pubitemid 43752788)
24. Lu, M., and T. Shenk. 1999. Human cytomegalovirus UL69 protein induces cells to accumulate in G1 phase of the cell cycle. J. Virol. 73:676-683.
25. Menard, C., M. Wagner, Z. Ruzsics, K. Holak, W. Brune, A. E. Campbell, and U. H. Koszinowski. 2003. Role of murine cytomegalovirus US22 gene family members in replication in macrophages. J. Virol. 77:5557-5570. (Pubitemid 36538948)
26. Mocarski, E., T. Shenk, and R. F. Pass. 2007. Cytomegaloviruses, p. 2702-2772. 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, 5th ed. Lippincott-Raven Publishers, Philadelphia, PA.
27. Moorman, N. J., I. M. Cristea, S. S. Terhune, M. P. Rout, B. T. Chait, and T. Shenk. 2008. Human cytomegalovirus protein UL38 inhibits host cell stress responses by antagonizing the tuberous sclerosis protein complex. Cell Host Microbe 3:253-262.
28. Munger, J., D. Yu, and T. Shenk. 2006. UL26-deficient human cytomegalovirus produces virions with hypophosphorylated pp28 tegument protein that is unstable within newly infected cells. J. Virol. 80:3541-3548.
29. Murphy, E., J. Vanicek, H. Robins, T. Shenk, and A. J. Levine. 2008. Suppression of immediate-early viral gene expression by herpesvirus-coded microRNAs: implications for latency. Proc. Natl. Acad. Sci. USA 105:5453-5458.
30. Murphy, E., D. Yu, J. Grimwood, J. Schmutz, M. Dickson, M. A. Jarvis, G. Hahn, J. A. Nelson, R. M. Myers, and T. E. Shenk. 2003. Coding potential of laboratory and clinical strains of human cytomegalovirus. Proc. Natl. Acad. Sci. USA 100:14976-14981.
31. Murphy, J. C., W. Fischle, E. Verdin, and J. H. Sinclair. 2002. Control of cytomegalovirus lytic gene expression by histone acetylation. EMBO J. 21:1112-1120.
32. Nevels, M., C. Paulus, and T. Shenk. 2004. Human cytomegalovirus immediate-early 1 protein facilitates viral replication by antagonizing histone deacetylation. Proc. Natl. Acad. Sci. USA 101:17234-17239.
33. Nitzsche, A., C. Paulus, and M. Nevels. 2008. Temporal dynamics of cytomegalovirus chromatin assembly in productively infected human cells. J. Virol. 82:11167-11180.
34. Novotny, J., I. Rigoutsos, D. Coleman, and T. Shenk. 2001. In silico structural and functional analysis of the human cytomegalovirus (HHV5) genome. J. Mol. Biol. 310:1151-1166.
35. 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. (Pubitemid 14194482)
36. Park, J. J., Y. E. Kim, H. T. Pham, E. T. Kim, Y. H. Chung, and J. H. Ahn. 2007. Functional interaction of the human cytomegalovirus IE2 protein with histone deacetylase 2 in infected human fibroblasts. J. Gen. Virol. 88:3214-3223.
37. Patterson, C. E., and T. Shenk. 1999. Human cytomegalovirus UL36 protein is dispensable for viral replication in cultured cells. J. Virol. 73:7126-7131.
38. Prichard, M. N., D. C. Quenelle, D. J. Bidanset, G. Komazin, S. Chou, J. C. Drach, and E. R. Kern. 2006. Human cytomegalovirus UL27 is not required for viral replication in human tissue implanted in SCID mice. Virol. J. 3:18.
39. Rawlinson, W. D., H. E. Farrell, and B. G. Barrell. 1996. Analysis of the complete DNA sequence of murine cytomegalovirus. J. Virol. 70:8833-8849. (Pubitemid 26378467)
40. Reeves, M., J. Murphy, R. Greaves, J. Fairley, A. Brehm, and J. Sinclair. 2006. Autorepression of the human cytomegalovirus major immediate-early promoter/enhancer at late times of infection is mediated by the recruitment of chromatin remodeling enzymes by IE86. J. Virol. 80:9998-10009. (Pubitemid 44522594)
41. Romanowski, M. J., E. Garrido-Guerrero, and T. Shenk. 1997. pIRS1 and pTRS1 are present in human cytomegalovirus virions. J. Virol. 71:5703-5705.
42. Romanowski, M. J., and T. Shenk. 1997. Characterization of the human cytomegalovirus irs1 and trs1 genes: a second immediate-early transcription unit within irs1 whose product antagonizes transcriptional activation. J. Virol. 71:1485-1496.
43. Schierling, K., T. Stamminger, T. Mertens, and M. Winkler. 2004. Human cytomegalovirus tegument proteins ppUL82 (pp71) and ppUL35 interact and cooperatively activate the major immediate-early enhancer. J. Virol. 78:9512-9523. (Pubitemid 39096558)
44. Skaletskaya, A., L. M. Bartle, T. Chittenden, A. L. McCormick, E. S. Mocarski, and V. S. Goldmacher. 2001. A cytomegalovirus-encoded inhibitor of apoptosis that suppresses caspase-8 activation. Proc. Natl. Acad. Sci. USA 98:7829-7834.
45. Stamminger, T., M. Gstaiger, K. Weinzierl, K. Lorz, M. Winkler, and W. Schaffner. 2002. Open reading frame UL26 of human cytomegalovirus encodes a novel tegument protein that contains a strong transcriptional activation domain. J. Virol. 76:4836-4847. (Pubitemid 34441689)
46. Terhune, S., E. Torigoi, N. Moorman, M. Silva, Z. Qian, T. Shenk, and D. Yu. 2007. Human cytomegalovirus UL38 protein blocks apoptosis. J. Virol. 81:3109-3123.
47. Valchanova, R. S., M. Picard-Maureau, M. Budt, and W. Brune. 2006. Murine cytomegalovirus m142 and m143 are both required to block protein kinase R-mediated shutdown of protein synthesis. J. Virol. 80:10181-10190.
48. Varnum, S. M., D. N. Streblow, M. E. Monroe, P. Smith, K. J. Auberry, L. Pasa-Tolic, D. Wang, D. G. Camp, 2nd, K. Rodland, S. Wiley, W. Britt, T. Shenk, R. D. Smith, and J. A. Nelson. 2004. Identification of proteins in human cytomegalovirus (HCMV) particles: the HCMV proteome. J. Virol. 78:10960-10966.
49. Warming, S., N. Costantino, D. L. Court, N. A. Jenkins, and N. G. Copeland. 2005. Simple and highly efficient BAC recombineering using galK selection. Nucleic Acids Res. 33:e36. (Pubitemid 41439937)
50. Yu, D., M. C. Silva, and T. Shenk. 2003. Functional map of human cytomegalovirus AD169 defined by global mutational analysis. Proc. Natl. Acad. Sci. USA 100:12396-12401.
51. Yu, D., G. A. Smith, L. W. Enquist, and T. Shenk. 2002. Construction of a self-excisable bacterial artificial chromosome containing the human cytomegalovirus genome and mutagenesis of the diploid TRL/IRL13 gene. J. Virol. 76:2316-2328. (Pubitemid 34150700)