Cytomegalovirus UL91 is essential for transcription of viral true late (γ2) genes

Journal of Virology

Volumn 87, Issue 15, 2013, Pages 8651-8664

  Omoto, Shinya ^a   Mocarski, Edward S ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

UL91 PROTEIN; UNCLASSIFIED DRUG; VIRUS ANTIGEN; VIRUS DNA; VIRUS PROTEIN; VIRUS RNA;

AMINO TERMINAL SEQUENCE; ARTICLE; BETAHERPESVIRINAE; CONTROLLED STUDY; DNA SEQUENCE; DNA SYNTHESIS; GAMMAHERPESVIRINAE; GENE EXPRESSION REGULATION; GENETIC CONSERVATION; HUMAN; HUMAN CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; VIRAL TRUE LATE GAMMA 2 GENE; VIRION; VIRUS ASSEMBLY; VIRUS CAPSID; VIRUS GENE; VIRUS REPLICATION;

EID: 84880617982     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01052-13     Document Type: Article

References (78)

1. Mocarski ES, Jr, Shenk T, Griffith P, Pass RF. 2013. Cytomegaloviruses, p 1960-2014. In Knipe DM, Howley PM (ed), Fields virology, 6th ed. Lippincott Williams & Wilkins, Philadelphia, PA.
2. Liu B, Stinski MF. 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.
3. Cantrell SR, Bresnahan WA. 2005. Interaction between the human cytomegalovirus UL82 gene product (pp71) and hDaxx regulates immediate- early gene expression and viral replication. J. Virol. 79:7792-7802.
4. Bresnahan WA, Shenk TE. 2000. UL82 virion protein activates expression of immediate early viral genes in human cytomegalovirus-infected cells Proc. Natl. Acad. Sci. U. S. A. 97:14506-14511.
5. Lukashchuk V, McFarlane S, Everett RD, Preston CM. 2008. Human cytomegalovirus protein pp71 displaces the chromatin-associated factor ATRX from nuclear domain 10 at early stages of infection. J. Virol. 82: 12543-12554.
6. Tavalai N, Stamminger T. 2011. Intrinsic cellular defense mechanisms targeting human cytomegalovirus. Virus Res. 157:128-133.
7. Stinski MF, Petrik DT. 2008. Functional roles of the human cytomegalovirus essential IE86 protein. Curr. Top. Microbiol. Immunol. 325:133-152.
8. Greaves RF, Mocarski ES. 1998. Defective growth correlates with reduced accumulation of a viral DNA replication protein after low multiplicity infection by a human cytomegalovirus ie1 mutant. J. Virol. 72:366-379.
9. Gawn JM, Greaves RF. 2002. Absence of IE1 p72 protein function during low-multiplicity infection by human cytomegalovirus results in a broad block to viral delayed-early gene expression. J. Virol. 76:4441-4455.
10. Stinski MF, Meier JL. 2007. Immediate-early CMV gene regulation and function, p 241-263. In Arvin AM, Campadelli-Fiume G, Mocarski ES, Moore PS, Roizman B, Whitley R, Yamanishi K (ed), Human herpesviruses: biology, therapy and immunoprophylaxis, 2011/02/25 ed. Cambridge Press, Cambridge, United Kingdom.
11. White EA, Spector DH. 2007. Early CMV gene expression and function, p 264-294. In Arvin AM, Campadelli-Fiume G, Mocarski ES, Moore PS, Roizman B, Whitley R, Yamanishi K (ed), Human herpesviruses: biology, therapy and immunoprophylaxis, 2011/02/25 ed. Cambridge Press, Cambridge, United Kingdom.
12. Marshall EE, Bierle CJ, Brune W, Geballe AP. 2009. Essential role for either TRS1 or IRS1 in human cytomegalovirus replication. J. Virol. 83: 4112-4120.
13. Brune W. 2011. Inhibition of programmed cell death by cytomegaloviruses. Virus Res. 157:144-150.
14. McCormick AL, Mocarski ES. 2013. Cell death pathways controlled by cytomegaloviruses, p 263-276. In Reddehase MJ (ed), Cytomegaloviruses: from molecular pathogenesis to intervention. Caister Scientific Press, Norfolk, United Kingdom.
15. Reeves MB. 2011. Chromatin-mediated regulation of cytomegalovirus gene expression. Virus Res. 157:134-143.
16. Mocarski ES, Upton JW, Kaiser WJ. 2012. Viral infection and the evolution of caspase 8-regulated apoptotic and necrotic death pathways. Nat. Rev. Immunol. 12:79-88.
17. Tandon R, Mocarski ES. 2012. Viral and host control of cytomegalovirus maturation. Trends Microbiol. 20:392-401.
18. Ishov AM, Maul GG. 1996. The periphery of nuclear domain 10 (ND10) as site of DNA virus deposition. J. Cell Biol. 134:815-826.
19. Ishov AM, Stenberg RM, Maul GG. 1997. Human cytomegalovirus immediate early interaction with host nuclear structures: definition of an immediate transcript environment. J. Cell Biol. 138:5-16.
20. Anders DG, Kerry JA, Pari GS. 2007. CMV DNA synthesis and late viral gene expression, p 295-310. In Arvin AM, Campadelli-Fiume G, Mocarski ES, Moore PS, Roizman B, Whitley R, Yamanishi K (ed), Human herpesviruses: biology, therapy and immunoprophylaxis, 2011/02/25 ed. Cambridge Press, Cambridge, United Kingdom.
21. Pari GS. 2008. Nuts and bolts of human cytomegalovirus lytic DNA replication. Curr. Top. Microbiol. Immunol. 325:153-166.
22. Kim YE, Ahn JH. 2010. Role of the specific interaction of UL112-113 p84 with UL44 DNA polymerase processivity factor in promoting DNA replication of human cytomegalovirus. J. Virol. 84:8409-8421.
23. Kagele D, Rossetto CC, Tarrant MT, Pari GS. 2012. Analysis of the interactions of viral and cellular factors with human cytomegalovirus lytic origin of replication, oriLyt. Virology 424:106-114.
24. Penfold ME, Mocarski ES. 1997. Formation of cytomegalovirus DNA replication compartments defined by localization of viral proteins and DNA synthesis. Virology 239:46-61.
25. Wang Y, Tang Q, Maul GG, Yuan Y. 2006. Kaposi's sarcoma-associated herpesvirus ori-Lyt-dependent DNA replication: dual role of replication and transcription activator. J. Virol. 80:12171-12186.
26. El-Guindy A, Ghiassi-Nejad M, Golden S, Delecluse HJ, Miller G. 2013. Essential role of Rta in lyticDNAreplication of Epstein-Barr virus. J. Virol. 87:208-223.
27. Wells R, Stensland L, Vieira J. 2009. The human cytomegalovirus UL112-113 locus can activate the full Kaposi's sarcoma-associated herpesvirus lytic replication cycle. J. Virol. 83:4695-4699.
28. Mocarski ES. 2007. Betaherpes viral genes and their functions, p 204-230. In Arvin AM, Campadelli-Fiume G, Mocarski ES, Moore PS, Roizman B, Whitley R, Yamanishi K (ed), Human herpesviruses: biology, therapy and immunoprophylaxis, 2011/02/25 ed. Cambridge Press, Cambridge, United Kingdom.
29. Adam BL, Jervey TY, Kohler CP, Wright GL, Jr, Nelson JA, Stenberg RM. 1995. The human cytomegalovirus UL98 gene transcription unit overlaps with the pp28 true late gene (UL99) and encodes a 58-kilodalton early protein. J. Virol. 69:5304-5310.
30. Wing BA, Huang ES. 1995. Analysis and mapping of a family of 3'- coterminal transcripts containing coding sequences for human cytomegalovirus open reading frames UL93 through UL99. J. Virol. 69:1521-1531.
31. Wing BA, Johnson RA, Huang ES. 1998. Identification of positive and negative regulatory regions involved in regulating expression of the human cytomegalovirus UL94 late promoter: role of IE2-86 and cellular p53 in mediating negative regulatory function. J. Virol. 72:1814-1825.
32. Leatham MP, Witte PR, Stinski MF. 1991. Alternate promoter selection within a human cytomegalovirus immediate-early and early transcription unit (UL119-115) defines true late transcripts containing open reading frames for putative viral glycoproteins. J. Virol. 65:6144-6153.
33. McWatters BJ, Stenberg RM, Kerry JA. 2002. Characterization of the human cytomegalovirus UL75 (glycoprotein H) late gene promoter. Virology 303:309-316.
34. Wang SK, Duh CY, Wu CW. 2004. Human cytomegalovirus UL76 encodes a novel virion-associated protein that is able to inhibit viral replication. J. Virol. 78:9750-9762.
35. Sanchez V, Greis KD, Sztul E, Britt WJ. 2000. Accumulation of virion tegument and envelope proteins in a stable cytoplasmic compartment during human cytomegalovirus replication: characterization of a potential site of virus assembly J. Virol. 74:975-986.
36. Perng YC, Qian Z, Fehr AR, Xuan B, Yu D. 2011. Human cytomegalovirus gene UL79 is required for the accumulation of late viral transcripts. J. Virol. 85:4841-4852.
37. Leach FS, Mocarski ES. 1989. Regulation of cytomegalovirus late-gene expression: differential use of three start sites in the transcriptional activation of ICP36 gene expression. J. Virol. 63:1783-1791.
38. Isomura H, Stinski MF, Kudoh A, Nakayama S, Iwahori S, Sato Y, Tsurumi T. 2007. The late promoter of the human cytomegalovirus viral DNA polymerase processivity factor has an impact on delayed early and late viral gene products but not on viral DNA synthesis. J. Virol. 81:6197- 6206.
39. Isomura H, Stinski MF, Kudoh A, Murata T, Nakayama S, Sato Y, Iwahori S, Tsurumi T. 2008. Noncanonical TATA sequence in the UL44 late promoter of human cytomegalovirus is required for the accumulation of late viral transcripts. J. Virol. 82:1638-1646.
40. White EA, Del Rosario CJ, Sanders RL, Spector DH. 2007. The IE2 60-kilodalton and 40-kilodalton proteins are dispensable for human cytomegalovirus replication but are required for efficient delayed early and late gene expression and production of infectious virus. J. Virol. 81:2573- 2583.
41. Kohler CP, Kerry JA, Carter M, Muzithras VP, Jones TR, Stenberg RM. 1994. Use of recombinant virus to assess human cytomegalovirus early and late promoters in the context of the viral genome. J. Virol. 68:6589- 6597.
42. Homa FL, Glorioso JC, Levine M. 1988. A specific 15-bp TATA box promoter element is required for expression of a herpes simplex virus type 1 late gene. Genes Dev. 2:40-53.
43. Kerry JA, Priddy MA, Kohler CP, Staley TL, Weber D, Jones TR, Stenberg RM. 1997. Translational regulation of the human cytomegalovirus pp28 (UL99) late gene. J. Virol. 71:981-987.
44. Geiduschek EP, Kassavetis GA. 2010. Transcription of the T4 late genes. Virol. J. 7:288.
45. Arumugaswami V, Wu TT, Martinez-Guzman D, Jia Q, Deng H, Reyes N, Sun R. 2006. ORF18 is a transfactor that is essential for late gene transcription of a gammaherpesvirus. J. Virol. 80:9730-9740.
46. Jia Q, Wu TT, Liao HI, Chernishof V, Sun R. 2004. Murine gammaherpesvirus 68 open reading frame 31 is required for viral replication. J. Virol. 78:6610-6620.
47. Wong E, Wu TT, Reyes N, Deng H, Sun R. 2007. Murine gammaherpesvirus 68 open reading frame 24 is required for late gene expression after DNA replication. J. Virol. 81:6761-6764.
48. Wu TT, Park T, Kim H, Tran T, Tong L, Martinez-Guzman D, Reyes N, Deng H, Sun R. 2009. ORF30 and ORF34 are essential for expression of late genes in murine gammaherpesvirus 68. J. Virol. 83:2265-2273.
49. Wyrwicz LS, Rychlewski L. 2007. Identification of herpes TATT-binding protein. Antiviral Res. 75:167-172.
50. Gruffat H, Kadjouf F, Mariame B, Manet E. 2012. The Epstein-Barr virus BcRF1 gene product is a TBP-like protein with an essential role in late gene expression. J. Virol. 86:6023-6032.
51. Dunn W, Chou C, Li H, Hai R, Patterson D, Stolc V, Zhu H, Liu F. 2003. Functional profiling of a human cytomegalovirus genome. Proc. Natl. Acad. Sci. U. S. A. 100:14223-14228.
52. Yu D, Silva MC, Shenk T. 2003. Functional map of human cytomegalovirus AD169 defined by global mutational analysis. Proc. Natl. Acad. Sci. U. S. A. 100:12396-12401.
53. Isomura H, Stinski MF, Murata T, Yamashita Y, Kanda T, Toyokuni S, Tsurumi T. 2011. The human cytomegalovirus gene products essential for late viral gene expression assemble into prereplication complexes before viral DNA replication. J. Virol. 85:6629-6644.
54. Dolan A, Cunningham C, Hector RD, Hassan-Walker AF, Lee L, Addison C, Dargan DJ, McGeoch DJ, Gatherer D, Emery VC, Griffiths PD, Sinzger C, McSharry BP, Wilkinson GW, Davison AJ. 2004. Genetic content of wild-type human cytomegalovirus. J. Gen. Virol. 85:1301-1312.
55. Davison AJ, Bhella D. 2007. Comparative betaherpes viral genome and virion structure, p 177-203. In Arvin AM, Campadelli-Fiume G, Mocarski ES, Moore PS, Roizman B, Whitley R, Yamanishi K (ed), Human herpesviruses: biology, therapy and immunoprophylaxis, 2011/02/25 ed. Cambridge Press, Cambridge, United Kingdom.
56. Searles RP, Bergquam EP, Axthelm MK, Wong SW. 1999. Sequence and genomic analysis of a rhesus macaque rhadinovirus with similarity to Ka- posi's sarcoma-associated herpesvirus/human herpesvirus 8. J. Virol. 73: 3040-3053.
57. Alexander L, Denekamp L, Knapp A, Auerbach MR, Damania B, Desrosiers RC. 2000. The primary sequence of rhesus monkey rhadinovirus isolate 26-95: sequence similarities to Kaposi's sarcoma-associated herpesvirus and rhesus monkey rhadinovirus isolate 17577. J. Virol. 74: 3388-3398.
58. Rawlinson WD, Farrell HE, Barrell BG. 1996. Analysis of the complete DNA sequence of murine cytomegalovirus. J. Virol. 70:8833-8849.
59. Brocchieri L, Kledal TN, Karlin S, Mocarski ES. 2005. Predicting coding potential from genome sequence: application to betaherpesviruses infecting rats and mice. J. Virol. 79:7570-7596.
60. Marchini A, Liu H, Zhu H. 2001. Human cytomegalovirus with IE-2 (UL122) deleted fails to express early lytic genes. J. Virol. 75:1870-1878.
61. AuCoin DP, Smith GB, Meiering CD, Mocarski ES. 2006. Betaherpesvirus-conserved cytomegalovirus tegument protein ppUL32 (pp150) controls cytoplasmic events during virion maturation. J. Virol. 80:8199- 8210.
62. Hansen SG, Strelow LI, Franchi DC, Anders DG, Wong SW. 2003. Complete sequence and genomic analysis of rhesus cytomegalovirus. J. Virol. 77:6620-6636.
63. Rivailler P, Kaur A, Johnson RP, Wang F. 2006. Genomic sequence of rhesus cytomegalovirus 180.92: insights into the coding potential of rhesus cytomegalovirus. J. Virol. 80:4179-4182.
64. Naldini L, Blomer U, Gallay P, Ory D, Mulligan R, Gage FH, Verma IM, Trono D. 1996. In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science 272:263-267.
65. Warming S, Costantino N, Court DL, Jenkins NA, Copeland NG. 2005. Simple and highly efficient BAC recombineering using galK selection. Nucleic Acids Res. 33:e36. doi:10.1093/nar/gni035.
66. McCormick AL, Meiering CD, Smith GB, Mocarski ES. 2005. Mitochondrial cell death suppressors carried by human and murine cytomegalovirus confer resistance to proteasome inhibitor-induced apoptosis. J. Virol. 79:12205-12217.
67. Baldick CJ, Jr, Marchini A, Patterson CE, Shenk T. 1997. Human cytomegalovirus tegument protein pp71 (ppUL82) enhances the infectivity of viral DNA and accelerates the infectious cycle. J. Virol. 71:4400- 4408
68. McCormick AL, Roback L, Wynn G, Mocarski ES. 2013. Multiplicitydependent activation of a serine protease-dependent cytomegalovirusassociated programmed cell death pathway. Virology 435:250-257.
69. Chee M, Rudolph SA, Plachter B, Barrell B, Jahn G. 1989. Identification of the major capsid protein gene of human cytomegalovirus. J. Virol. 63:1345-1353.
70. Tandon R, Mocarski ES. 2011. Cytomegalovirus pUL96 is critical for the stability of pp150-associated nucleocapsids. J. Virol. 85:7129-7141.
71. Ahlqvist J, Mocarski E. 2011. Cytomegalovirus UL103 controls virion and dense body egress. J. Virol. 85:5125-5135.
72. Potena L, Holweg CT, Vana ML, Bashyam L, Rajamani J, McCormick AL, Cooke JP, Valantine HA, Mocarski ES. 2007. Frequent occult infection with cytomegalovirus in cardiac transplant recipients despite antiviral prophylaxis. J. Clin. Microbiol. 45:1804-1810.
73. Mitchell DP, Savaryn JP, Moorman NJ, Shenk T, Terhune SS. 2009. Human cytomegalovirus UL28 and UL29 open reading frames encode a spliced mRNA and stimulate accumulation of immediate-early RNAs. J. Virol. 83:10187-10197.
74. Gatherer D, Seirafian S, Cunningham C, Holton M, Dargan DJ, Baluchova K, Hector RD, Galbraith J, Herzyk P, Wilkinson GW, Davison AJ. 2011. High-resolution human cytomegalovirus transcriptome. Proc. Natl. Acad. Sci. U. S. A. 108:19755-19760.
75. Stern-Ginossar N, Weisburd B, Michalski A, Le VT, Hein MY, Huang SX, Ma M, Shen B, Qian SB, Hengel H, Mann M, Ingolia NT, Weissman JS. 2012. Decoding human cytomegalovirus. Science 338:1088- 1093.
76. Banaszynski LA, Chen LC, Maynard-Smith LA, Ooi AG, Wandless TJ. 2006. A rapid, reversible, and tunable method to regulate protein function in living cells using synthetic small molecules. Cell 126:995-1004.
77. Glass M, Busche A, Wagner K, Messerle M, Borst EM. 2009. Conditional and reversible disruption of essential herpesvirus proteins. Nat. Methods 6:577-579.
78. Gibson W. 2008. Structure and formation of the cytomegalovirus virion. Curr. Top. Microbiol. Immunol. 325:187-204.