Human cytomegalovirus pUL83 stimulates activity of the viral immediate-early promoter through its interaction with the cellular IFI16 protein

Journal of Virology

Volumn 84, Issue 15, 2010, Pages 7803-7814

  Cristea, Ileana M ^a   Moorman, Nathaniel J ^a   Terhune, Scott S ^b   Cuevas, Christian D ^a   O'Keefe, Erin S ^a   Rout, Michael P ^c   Chait, Brian T ^c   Shenk, Thomas ^a  

^a PRINCETON UNIVERSITY   (United States)

^b MEDICAL COLLEGE OF WISCONSIN   (United States)

^c ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; CELL PROTEIN IFI16; CYTOMEGALOVIRUS ANTIGEN PP65; EPITOPE; IMMEDIATE EARLY PROTEIN; TRANSLATION TERMINATION FACTOR; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; CYTOMEGALOVIRUS INFECTION; GENE EXPRESSION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; HUMAN CYTOMEGALOVIRUS; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN INTERACTION; TRANSACTIVATION; VIROGENESIS;

CELLS, CULTURED; CODON, NONSENSE; CYTOMEGALOVIRUS; DNA, VIRAL; FIBROBLASTS; GENE KNOCKDOWN TECHNIQUES; GENES, IMMEDIATE-EARLY; GENES, REPORTER; HOST-PATHOGEN INTERACTIONS; HUMANS; MUTATION, MISSENSE; NUCLEAR PROTEINS; PHOSPHOPROTEINS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; TRANSCRIPTIONAL ACTIVATION; VIRAL MATRIX PROTEINS;

HUMAN HERPESVIRUS 5;

EID: 77954485440     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00139-10     Document Type: Article

References (90)

1. Abate, D. A., S. Watanabe, and E. S. Mocarski. 2004. Major human cytomegalovirus structural protein pp65 (ppUL83) prevents interferon response factor 3 activation in the interferon response. J. Virol. 78:10995-11006.
2. Aglipay, J. A., S. W. Lee, S. Okada, N. Fujiuchi, T. Ohtsuka, J. C. Kwak, Y. Wang, R. W. Johnstone, C. Deng, J. Qin, and T. Ouchi. 2003. A member of the Pyrin family, IFI16, is a novel BRCA1-associated protein involved in the p53-mediated apoptosis pathway. Oncogene 22:8931-8938.
3. Arcangeletti, M. C., F. De Conto, F. Ferraglia, F. Pinardi, R. Gatti, G. Orlandini, A. Calderaro, F. Motta, M. C. Medici, M. Martinelli, P. Valcavi, S. V. Razin, C. Chezzi, and G. Dettori. 2003. Human cytomegalovirus proteins PP65 and IEP72 are targeted to distinct compartments in nuclei and nuclear matrices of infected human embryo fibroblasts. J. Cell Biochem. 90:1056-1067.
4. Arcangeletti, M. C., I. Rodighiero, F. De Conto, R. Gatti, G. Orlandini, F. Ferraglia, F. Motta, S. Covan, S. V. Razin, G. Dettori, and C. Chezzi. 2009. Modulatory effect of rRNA synthesis and ppUL83 nucleolar compartmentalization on human cytomegalovirus gene expression in vitro. J. Cell Biochem. 108:415-423.
5. Arlt, H., D. Lang, S. Gebert, and T. Stamminger. 1994. Identification of binding sites for the 86-kilodalton IE2 protein of human cytomegalovirus within an IE2-responsive viral early promoter. J. Virol. 68:4117-4125. (Pubitemid 24183005)
6. 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.
7. Baldick, C. J., Jr., and T. Shenk. 1996. Proteins associated with purified human cytomegalovirus particles. J. Virol. 70:6097-6105. (Pubitemid 26266825)
8. Boehme, K. W., M. Guerrero, and T. Compton. 2006. Human cytomegalovirus envelope glycoproteins B and H are necessary for TLR2 activation in permissive cells. J. Immunol. 177:7094-7102.
9. Bourette, R. P., and G. Mouchiroud. 2008. The biological role of interferon-inducible P204 protein in the development of the mononuclear phagocyte system. Front. Biosci. 13:879-886.
10. Boyle, K. A., R. L. Pietropaolo, and T. Compton. 1999. Engagement of the cellular receptor for glycoprotein B of human cytomegalovirus activates the interferon-responsive pathway. Mol. Cell. Biol. 19:3607-3613.
11. 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. U. S. A. 97:14506-14511.
12. Browne, E. P., and T. Shenk. 2003. Human cytomegalovirus UL83-coded pp65 virion protein inhibits antiviral gene expression in infected cells. Proc. Natl. Acad. Sci. U. S. A. 100:11439-11444.
13. Búrckstúmmer, T., C. Baumann, S. Bluml, E. Dixit, G. Durnberger, H. Jahn, M. Planyavsky, M. Bilban, J. Colinge, K. L. Bennett, and G. Superti-Furga. 2009. An orthogonal proteomic-genomic screen identifies AIM2 as a cytoplasmic DNA sensor for the inflammasome. Nat. Immunol. 10:266-272.
14. Caposio, P., F. Gugliesi, C. Zannetti, S. Sponza, M. Mondini, E. Medico, J. Hiscott, H. A. Young, G. Gribaudo, M. Gariglio, and S. Landolfo. 2007. A novel role of the interferon-inducible protein IFI16 as inducer of proinflammatory molecules in endothelial cells. J. Biol. Chem. 282:33515-33529.
15. Caposio, P., A. Luganini, G. Hahn, S. Landolfo, and G. Gribaudo. 2007. Activation of the virus-induced IKK/NF-kappaB signalling axis is critical for the replication of human cytomegalovirus in quiescent cells. Cell. Microbiol. 9:2040-2054.
16. Cassady, K. A. 2005. Human cytomegalovirus TRS1 and IRS1 gene products block the double-stranded-RNA-activated host protein shutoff response induced by herpes simplex virus type 1 infection. J. Virol. 79:8707-8715.
17. Castillo, J. P., and T. F. Kowalik. 2002. Human cytomegalovirus immediate early proteins and cell growth control. Gene 290:19-34.
18. 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.
19. Chan, G., E. R. Bivins-Smith, M. S. Smith, and A. D. Yurochko. 2008. Transcriptome analysis of NF-kappaB- and phosphatidylinositol 3-kinase-regulated genes in human cytomegalovirus-infected monocytes. J. Virol. 82:1040-1046.
20. Chevillotte, M., S. Landwehr, L. Linta, G. Frascaroli, A. Luske, C. Buser, T. Mertens, and J. von Einem. 2009. Major tegument protein pp65 of human cytomegalovirus is required for the incorporation of pUL69 and pUL97 into the virus particle and for viral growth in macrophages. J. Virol. 83:2480-2490.
21. Choubey, D., R. Deka, and S. M. Ho. 2008. Interferon-inducible IFI16 protein in human cancers and autoimmune diseases. Front. Biosci. 13:598-608.
22. Choubey, D., and R. Panchanathan. 2008. Interferon-inducible Ifi200-family genes in systemic lupus erythematosus. Immunol. Lett. 119:32-41.
23. Compton, T. 2004. Receptors and immune sensors: the complex entry path of human cytomegalovirus. Trends Cell Biol. 14:5-8. (Pubitemid 38076854)
24. Cristea, I. M., J. W. Carroll, M. P. Rout, C. M. Rice, B. T. Chait, and M. R. MacDonald. 2006. Tracking and elucidating alphavirus-host protein interactions. J. Biol. Chem. 281:30269-30278.
25. Cristea, I. M., R. Williams, B. T. Chait, and M. P. Rout. 2005. Fluorescent proteins as proteomic probes. Mol. Cell. Proteomics 4:1933-1941.
26. 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.
27. Dawson, M. J., and J. A. Trapani. 1995. The interferon-inducible autoantigen, IFI 16: localization to the nucleolus and identification of a DNA-binding domain. Biochem. Biophys. Res. Commun. 214:152-162.
28. DeMeritt, I. B., L. E. Milford, and A. D. Yurochko. 2004. Activation of the NF-kappaB pathway in human cytomegalovirus-infected cells is necessary for efficient transactivation of the major immediate-early promoter. J. Virol. 78:4498-4507.
29. DeMeritt, I. B., J. P. Podduturi, A. M. Tilley, M. T. Nogalski, and A. D. Yurochko. 2006. Prolonged activation of NF-kappaB by human cytomegalovirus promotes efficient viral replication and late gene expression. Virology 346:15-31.
30. Fujiuchi, N., J. A. Aglipay, T. Ohtsuka, N. Maehara, F. Sahin, G. H. Su, S. W. Lee, and T. Ouchi. 2004. Requirement of IFI16 for the maximal activation of p53 induced by ionizing radiation. J. Biol. Chem. 279:20339-20344.
31. Gibson, W. 1981. Structural and nonstructural proteins of strain Colburn cytomegalovirus. Virology 111:516-537.
32. Gugliesi, F., M. Mondini, R. Ravera, A. Robotti, M. de Andrea, G. Gribaudo, M. Gariglio, and S. Landolfo. 2005. Up-regulation of the interferon-inducible IFI16 gene by oxidative stress triggers p53 transcriptional activity in endothelial cells. J. Leukoc. Biol. 77:820-829.
33. Hakki, M., E. E. Marshall, K. L. De Niro, and A. P. Geballe. 2006. Binding and nuclear relocalization of protein kinase R by human cytomegalovirus TRS1. J. Virol. 80:11817-11826.
34. Hayashi, M. L., C. Blankenship, and T. Shenk. 2000. Human cytomegalovirus UL69 protein is required for efficient accumulation of infected cells in the G1 phase of the cell cycle. Proc. Natl. Acad. Sci. U. S. A. 97:2692-2696.
35. Hertel, L., M. De Andrea, B. Azzimonti, A. Rolle, M. Gariglio, and S. Landolfo. 1999. The interferon-inducible 204 gene, a member of the Ifi 200 family, is not involved in the antiviral state induction by IFN-alpha, but is required by the mouse cytomegalovirus for its replication. Virology 262:1-8.
36. Hiscott, J. 2007. Convergence of the NF-kappaB and IRF pathways in the regulation of the innate antiviral response. Cytokine Growth Factor Rev. 18:483-490.
37. Irmiere, A., and W. Gibson. 1983. Isolation and characterization of a noninfectious virion-like particle released from cells infected with human strains of cytomegalovirus. Virology 130:118-133. (Pubitemid 14226847)
38. Jenkins, D. E., C. L. Martens, and E. S. Mocarski. 1994. Human cytomegalovirus late protein encoded by ie2: a trans-activator as well as a repressor of gene expression. J. Gen. Virol. 75(9):2337-2348.
39. Johnson, D. C., and N. R. Hegde. 2002. Inhibition of the MHC class II antigen presentation pathway by human cytomegalovirus. Curr. Top. Microbiol. Immunol. 269:101-115.
40. Johnstone, R. W., J. A. Kerry, and J. A. Trapani. 1998. The human interferon-inducible protein, IFI 16, is a repressor of transcription. J. Biol. Chem. 273:17172-17177.
41. Johnstone, R. W., M. H. Kershaw, and J. A. Trapani. 1998. Isotypic variants of the interferon-inducible transcriptional repressor IFI 16 arise through differential mRNA splicing. Biochemistry 37:11924-11931.
42. Kalejta, R. F. 2008. Functions of human cytomegalovirus tegument proteins prior to immediate early gene expression. Curr. Top. Microbiol. Immunol. 325:101-115.
43. Kalejta, R. F. 2008. Tegument proteins of human cytomegalovirus. Microbiol. Mol. Biol. Rev. 72:249-265.
44. Kim, K. S., K. W. Kang, Y. B. Seu, S. H. Baek, and J. R. Kim. 2009. Interferon-gamma induces cellular senescence through p53-dependent DNA damage signaling in human endothelial cells. Mech. Ageing Dev. 130:179-188.
45. Krutchinsky, A. N., M. Kalkum, and B. T. Chait. 2001. Automatic identification of proteins with a MALDI-quadrupole ion trap mass spectrometer. Anal. Chem. 73:5066-5077.
46. Krutchinsky, A. N., W. Zhang, and B. T. Chait. 2000. Rapidly switchable matrix-assisted laser desorption/ionization and electrospray quadrupoletime-of-flight mass spectrometry for protein identification. J. Am. Soc. Mass Spectrom. 11:493-504.
47. Kwak, J. C., P. P. Ongusaha, T. Ouchi, and S. W. Lee. 2003. IFI16 as a negative regulator in the regulation of p53 and p21(Waf1). J. Biol. Chem. 278:40899-40904.
48. Liu, Z., M. Winkler, and B. Biegalke. 2009. Human cytomegalovirus: host immune modulation by the viral US3 gene. Int. J. Biochem. Cell Biol. 41:503-506.
49. Lodoen, M., K. Ogasawara, J. A. Hamerman, H. Arase, J. P. Houchins, E. S. Mocarski, and L. L. Lanier. 2003. NKG2D-mediated natural killer cell protection against cytomegalovirus is impaired by viral gp40 modulation of retinoic acid early inducible 1 gene molecules. J. Exp. Med. 197:1245-1253.
50. Lois, C., E. J. Hong, S. Pease, E. J. Brown, and D. Baltimore. 2002. Germline transmission and tissue-specific expression of transgenes delivered by lentiviral vectors. Science 295:868-872.
51. Lukac, D. M., J. R. Manuppello, and J. C. Alwine. 1994. Transcriptional activation by the human cytomegalovirus immediate-early proteins: requirements for simple promoter structures and interactions with multiple components of the transcription complex. J. Virol. 68:5184-5193.
52. Luo, Y., T. Li, F. Yu, T. Kramer, and I. M. Cristea. 2010. Resolving the composition of protein complexes using a MALDI LTQ Orbitrap. J. Am. Soc. Mass Spectrom. 21:34-46.
53. Luu, P., and O. Flores. 1997. Binding of SP1 to the immediate-early protein-responsive element of the human cytomegalovirus DNA polymerase promoter. J. Virol. 71:6683-6691.
54. Marshall, E. E., C. J. Bierle, W. Brune, and A. P. Geballe. 2009. Essential role for either TRS1 or IRS1 in human cytomegalovirus replication. J. Virol. 83:4112-4120.
55. Misaghi, S., Z. Y. Sun, P. Stern, R. Gaudet, G. Wagner, and H. Ploegh. 2004. Structural and functional analysis of human cytomegalovirus US3 protein. J. Virol. 78:413-423.
56. 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.
57. Murphy, E., I. Rigoutsos, T. Shibuya, and T. E. Shenk. 2003. Reevaluation of human cytomegalovirus coding potential. Proc. Natl. Acad. Sci. U. S. A. 100:13585-13590.
58. 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. U. S. A. 105:5453-5458.
59. 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. U. S. A. 100:14976-14981.
60. 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. U. S. A. 101:17234-17239.
61. Nogalski, M. T., J. P. Podduturi, I. B. DeMeritt, L. E. Milford, and A. D. Yurochko. 2007. The human cytomegalovirus virion possesses an activated casein kinase II that allows for the rapid phosphorylation of the inhibitor of NF-kappaB, IkappaBalpha. J. Virol. 81:5305-5314.
62. 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.
63. Ouchi, M., and T. Ouchi. 2008. Role of IFI16 in DNA damage and checkpoint. Front. Biosci. 13:236-239.
64. Paulus, C., S. Krauss, and M. Nevels. 2006. A human cytomegalovirus antagonist of type I IFN-dependent signal transducer and activator of transcription signaling. Proc. Natl. Acad. Sci. U. S. A. 103:3840-3845.
65. Pizzorno, M. C., M. A. Mullen, Y. N. Chang, and G. S. Hayward. 1991. The functionally active IE2 immediate-early regulatory protein of human cytomegalovirus is an 80-kilodalton polypeptide that contains two distinct activator domains and a duplicated nuclear localization signal. J. Virol. 65:3839-3852.
66. Pizzorno, M. C., P. O'Hare, L. Sha, R. L. LaFemina, and G. S. Hayward. 1988. trans-activation and autoregulation of gene expression by the immediate-early region 2 gene products of human cytomegalovirus. J. Virol. 62:1167-1179. (Pubitemid 18082930)
67. Poole, E., I. Groves, A. MacDonald, Y. Pang, A. Alcami, and J. Sinclair. 2009. Identification of TRIM23 as a cofactor involved in the regulation of NF-kappaB by human cytomegalovirus. J. Virol. 83:3581-3590.
68. Ranjan, P., J. B. Bowzard, J. W. Schwerzmann, V. Jeisy-Scott, T. Fujita, and S. Sambhara. 2009. Cytoplasmic nucleic acid sensors in antiviral immunity. Trends Mol. Med. 15:359-368.
69. Roberts, T. L., A. Idris, J. A. Dunn, G. M. Kelly, C. M. Burnton, S. Hodgson, L. L. Hardy, V. Garceau, M. J. Sweet, I. L. Ross, D. A. Hume, and K. J. Stacey. 2009. HIN-200 proteins regulate caspase activation in response to foreign cytoplasmic DNA. Science 323:1057-1060.
70. Rolle, S., M. De Andrea, D. Gioia, D. Lembo, L. Hertel, S. Landolfo, and M. Gariglio. 2001. The interferon-inducible 204 gene is transcriptionally activated by mouse cytomegalovirus and is required for its replication. Virology 286:249-255.
71. Romanowski, M. J., E. Garrido-Guerrero, and T. Shenk. 1997. pIRS1 and pTRS1 are present in human cytomegalovirus virions. J. Virol. 71:5703-5705.
72. Rúger, 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.
73. Saffert, R. T., and R. F. Kalejta. 2006. Inactivating a cellular intrinsic immune defense mediated by Daxx is the mechanism through which the human cytomegalovirus pp71 protein stimulates viral immediate-early gene expression. J. Virol. 80:3863-3871.
74. Schroder, K., D. A. Muruve, and J. Tschopp. 2009. Innate immunity: cytoplasmic DNA sensing by the AIM2 inflammasome. Curr. Biol. 19:R262-R265.
75. Simmen, K. A., J. Singh, B. G. Luukkonen, M. Lopper, A. Bittner, N. E. Miller, M. R. Jackson, T. Compton, and K. Fruh. 2001. Global modulation of cellular transcription by human cytomegalovirus is initiated by viral glycoprotein B. Proc. Natl. Acad. Sci. U. S. A. 98:7140-7145.
76. Sponza, S., M. De Andrea, M. Mondini, F. Gugliesi, M. Gariglio, and S. Landolfo. 2009. Role of the interferon-inducible IFI16 gene in the induction of ICAM-1 by TNF-alpha. Cell. Immunol. 257:55-60.
77. Stinski, M. F., and H. Isomura. 2008. Role of the cytomegalovirus major immediate early enhancer in acute infection and reactivation from latency. Med. Microbiol. Immunol. 197:223-231.
78. Tawara, H., N. Fujiuchi, J. Sironi, S. Martin, J. Aglipay, M. Ouchi, M. Taga, P. L. Chen, and T. Ouchi. 2008. Loss of p53-regulatory protein IFI16 induces NBS1 leading to activation of p53-mediated checkpoint by phosphorylation of p53 SER37. Front. Biosci. 13:240-248.
79. Taylor, R. T., and W. A. Bresnahan. 2006. Human cytomegalovirus IE86 attenuates virus- and tumor necrosis factor alpha-induced NF-kappaB-dependent gene expression. J. Virol. 80:10763-10771.
80. Taylor, R. T., and W. A. Bresnahan. 2005. Human cytomegalovirus immediate-early 2 gene expression blocks virus-induced beta interferon production. J. Virol. 79:3873-3877.
81. Taylor, R. T., and W. A. Bresnahan. 2006. Human cytomegalovirus immediate-early 2 protein IE86 blocks virus-induced chemokine expression. J. Virol. 80:920-928.
82. Terhune, S. S., J. Schroer, and T. Shenk. 2004. RNAs are packaged into human cytomegalovirus virions in proportion to their intracellular concentration. J. Virol. 78:10390-10398.
83. Tevethia, M. J., D. J. Spector, K. M. Leisure, and M. F. Stinski. 1987. Participation of two human cytomegalovirus immediate early gene regions in transcriptional activation of adenovirus promoters. Virology 161:276-285.
84. Trapani, J. A., M. Dawson, V. A. Apostolidis, and K. A. Browne. 1994. Genomic organization of IFI16, an interferon-inducible gene whose expression is associated with human myeloid cell differentiation: correlation of predicted protein domains with exon organization. Immunogenetics 40:415-424.
85. 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.
86. 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.
87. Yurochko, A. D., M. W. Mayo, E. E. Poma, A. S. Baldwin, Jr., and E. S. Huang. 1997. Induction of the transcription factor Sp1 during human cytomegalovirus infection mediates upregulation of the p65 and p105/p50 NF-kappaB promoters. J. Virol. 71:4638-4648.
88. Zhu, H., J. P. Cong, and T. Shenk. 1997. Use of differential display analysis to assess the effect of human cytomegalovirus infection on the accumulation of cellular RNAs: induction of interferon-responsive RNAs. Proc. Natl. Acad. Sci. U. S. A. 94:13985-13990.
89. Zhu, H., Y. Shen, and T. Shenk. 1995. Human cytomegalovirus IE1 and IE2 proteins block apoptosis. J. Virol. 69:7960-7970.
90. Zini, N., M. C. Battista, S. Santi, M. Riccio, G. Bergamini, M. P. Landini, and N. M. Maraldi. 1999. The novel structural protein of human cytomegalovirus, pUL25, is localized in the viral tegument. J. Virol. 73:6073-6075.