Human cytomegalovirus gene UL21a encodes a short-lived cytoplasmic protein and facilitates virus replication in fibroblasts

Journal of Virology

Volumn 84, Issue 1, 2010, Pages 291-302

  Fehr, Anthony R ^a   Yu, Dong ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; CYTOPLASM PROTEIN; GENE PRODUCT; PROTEASOME; UBIQUITIN; UL20 PROTEIN; UL21.5 PROTEIN; UL21A PROTEIN; UL23 PROTEIN; UNCLASSIFIED DRUG; VIRUS DNA; VIRUS PROTEIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CYTOMEGALOVIRUS INFECTION; CYTOPLASM; DNA REPLICATION; EMBRYO; ENZYME SPECIFICITY; FIBROBLAST; GENE DELETION; GENE EXPRESSION; GENE LOCUS; GENE MAPPING; GENE MUTATION; GENE REPLICATION; GENETIC CODE; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; HUMAN CYTOMEGALOVIRUS; KINETICS; LUNG FIBROBLAST; MOUSE; MUTANT; NEWBORN; NONHUMAN; OPEN READING FRAME; PREPUCE; PRIORITY JOURNAL; PROGENY; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN STABILITY; PROTEIN SYNTHESIS; VIRION; VIROGENESIS; VIRUS DETECTION; VIRUS GENE; VIRUS MUTANT; VIRUS REPLICATION; WILD TYPE;

CELLS, CULTURED; CYTOMEGALOVIRUS; CYTOPLASM; FIBROBLASTS; HUMANS; INFECTION; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN STABILITY; VIRAL PROTEINS; VIRUS REPLICATION;

HUMAN HERPESVIRUS 5; PONGINE HERPESVIRUS 4;

EID: 72849131562     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01116-09     Document Type: Article

References (46)

1. Adair, R., E. R. Douglas, J. B. Maclean, S. Y. Graham, J. D. Aitken, F. E. Jamieson, and D. J. Dargan. 2002. The products of human cytomegalovirus genes UL23, UL24, UL43, and US22 are tegument components. J. Gen. Virol. 83:1315-1324.
2. Ben-Saadon, R., I. Fajerman, T. Ziv, U. Hellman, A. L. Schwartz, and A. Ciechanover. 2004. The tumor suppressor protein p16(INK4a) and the human papillomavirus oncoprotein-58 E7 are naturally occurring lysine-less proteins that are degraded by the ubiquitin system: direct evidence for ubiquitination at the N-terminal residue. J. Biol. Chem. 279:41414-41421.
3. Borst, E. M., G. Hahn, U. H. Koszinowski, and M. Messerle. 1999. Cloning of the human cytomegalovirus (HCMV) genome as an infectious bacterial artificial chromosome in Escherichia coli: a new approach for construction of HCMV mutants. J. Virol. 73:8320-8329.
4. Bresnahan, W. A., and T. Shenk. 2000. A subset of viral transcripts packaged within human cytomegalovirus particles. Science 288:2373-2376.
5. Britt, W. J., and C. A. Alford (ed.). 1996. Cytomegalovirus, 3rd ed. Lippincott-Raven, Philadelphia, PA.
6. Cadwell, K., and L. Coscoy. 2005. Ubiquitination on nonlysine residues by a viral E3 ubiquitin ligase. Science 309:127-130. (Pubitemid 40934990)
7. Chee, M., S. A. Rudolph, B. Plachter, B. Barrell, and G. Jahn. 1989. Identification of the major capsid protein gene of human cytomegalovirus. J. Virol. 63:1345-1353. (Pubitemid 19061376)
8. 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.
9. Cheeseman, I. M., and A. Desai. 2005. A combined approach for the localization and tandem affinity purification of protein complexes from metazoans. Sci. STKE 2005:pl1.
10. Chowdary, D. R., J. J. Dermody, K. K. Jha, and H. L. Ozer. 1994. Accumulation of p53 in a mutant cell line defective in the ubiquitin pathway. Mol. Cell. Biol. 14:1997-2003.
11. Ciechanover, A., and R. Ben-Saadon. 2004. N-terminal ubiquitination: more protein substrates join in. Trends Cell Biol. 14:103-106. (Pubitemid 38293450)
12. 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.
13. Dolan, A., C. Cunningham, R. D. Hector, A. F. Hassan-Walker, L. Lee, C. Addison, D. J. Dargan, D. J. McGeoch, D. Gatherer, V. C. Emery, P. D. Griffiths, C. Sinzger, B. P. McSharry, G. W. Wilkinson, and A. J. Davison. 2004. Genetic content of wild-type human cytomegalovirus. J. Gen. Virol. 85:1301-1312.
14. Dunn, W., C. Chou, H. Li, R. Hai, D. Patterson, V. Stolc, H. Zhu, and F. Liu. 2003. Functional profiling of a human cytomegalovirus genome. Proc. Natl. Acad. Sci. USA 100:14223-14228.
15. Dunn, W., P. Trang, Q. Zhong, E. Yang, C. van Belle, and F. Liu. 2005. Human cytomegalovirus expresses novel microRNAs during productive viral infection. Cell Microbiol. 7:1684-1695. (Pubitemid 41511924)
16. Goila-Gaur, R., and K. Strebel. 2008. HIV-1 Vif, APOBEC, and intrinsic immunity. Retrovirology 5:51.
17. Grattan, M. T., C. E. Moreno-Cabral, V. A. Starnes, P. E. Oyer, E. B. Stinson, and N. E. Shumway. 1989. Cytomegalovirus infection is associated with cardiac allograft rejection and atherosclerosis. JAMA 261:3561-3566. (Pubitemid 19155945)
18. Grey, F., A. Antoniewicz, E. Allen, J. Saugstad, A. McShea, J. C. Carrington, and J. Nelson. 2005. Identification and characterization of human cytomegalovirus- encoded microRNAs. J. Virol. 79:12095-12099. (Pubitemid 41279327)
19. 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)
20. Kalejta, R. F., and T. Shenk. 2003. Proteasome-dependent, ubiquitin-independent degradation of the Rb family of tumor suppressors by the human cytomegalovirus pp71 protein. Proc. Natl. Acad. Sci. USA 100:3263-3268.
21. Kuvin, J. T., and C. D. Kimmelstiel. 1999. Infectious causes of atherosclerosis. Am. Heart J. 137:216-226.
22. McCormick, A. L., C. D. Meiering, G. B. Smith, and E. S. Mocarski. 2005. Mitochondrial cell death suppressors carried by human and murine cytomegalovirus confer resistance to proteasome inhibitor-induced apoptosis. J. Virol. 79:12205-12217.
23. Melnick, J. L., E. Adam, and M. E. Debakey. 1993. Cytomegalovirus and atherosclerosis. Eur. Heart J. 14(Suppl. K):30-38.
24. Miller, C. L., and D. J. Pintel. 2001. The NS2 protein generated by the parvovirus minute virus of mice is degraded by the proteasome in a manner independent of ubiquitin chain elongation or activation. Virology 285:346-355.
25. Mocarski, E. S., and C. T. Courcelle (ed.). 2001. Cytomegaloviruses and their replication, 4th ed., vol.2. Lippincott-Raven, Philadelphia, PA.
26. Muhlestein, J. B., B. D. Horne, J. F. Carlquist, T. E. Madsen, T. L. Bair, R. R. Pearson, and J. L. Anderson. 2000. Cytomegalovirus seropositivity and C-reactive protein have independent and combined predictive value for mortality in patients with angiographically demonstrated coronary artery disease. Circulation 102:1917-1923.
27. Mullberg, J., M. L. Hsu, C. T. Rauch, M. J. Gerhart, A. Kaykas, and D. Cosman. 1999. The R27080 glycoprotein is abundantly secreted from human cytomegalovirus-infected fibroblasts. J. Gen. Virol. 80(Pt. 2):437-440.
28. Murphy, E., I. Rigoutsos, T. Shibuya, and T. E. Shenk. 2003. Reevaluation of human cytomegalovirus coding potential. Proc. Natl. Acad. Sci. USA 100:13585-13590.
29. 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.
30. Petrik, D. T., K. P. Schmitt, and M. F. Stinski. 2006. Inhibition of cellular DNA synthesis by the human cytomegalovirus IE86 protein is necessary for efficient virus replication. J. Virol. 80:3872-3883.
31. Qian, Z., B. Xuan, T. T. Hong, and D. Yu. 2008. The full-length protein encoded by human cytomegalovirus gene UL117 is required for the proper maturation of viral replication compartments. J. Virol. 82:3452-3465.
32. Rawlinson, W. D., and B. G. Barrell. 1993. Spliced transcripts of human cytomegalovirus. J. Virol. 67:5502-5513.
33. Rivailler, P., A. Kaur, R. P. Johnson, and F. Wang. 2006. Genomic sequence of rhesus cytomegalovirus 180.92: insights into the coding potential of rhesus cytomegalovirus. J. Virol. 80:4179-4182.
34. Speir, E., R. Modali, E. S. Huang, M. B. Leon, F. Shawl, T. Finkel, and S. E. Epstein. 1994. Potential role of human cytomegalovirus and p53 interaction in coronary restenosis. Science 265:391-394. (Pubitemid 24259971)
35. Streblow, D. N., S. L. Orloff, and J. A. Nelson. 2001. Do pathogens accelerate atherosclerosis? J. Nutr. 131:2798S-2804S.
36. 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.
37. Varnum, S. M., D. N. Streblow, M. E. Monroe, P. Smith, K. J. Auberry, L. Pasa-Tolic, D. Wang, D. G. Camp II, 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.
38. Wang, D., W. Bresnahan, and T. Shenk. 2004. Human cytomegalovirus encodes a highly specific RANTES decoy receptor. Proc. Natl. Acad. Sci. USA 101:16642-16647.
39. Wang, J., A. N. Loveland, L. M. Kattenhorn, H. L. Ploegh, and W. Gibson. 2006. High-molecular-weight protein (pUL48) of human cytomegalovirus is a competent deubiquitinating protease: mutant viruses altered in its activesite cysteine or histidine are viable. J. Virol. 80:6003-6012. (Pubitemid 43849178)
40. Wang, X., R. A. Herr, W. J. Chua, L. Lybarger, E. J. Wiertz, and T. H. Hansen. 2007. Ubiquitination of serine, threonine, or lysine residues on the cytoplasmic tail can induce ERAD of MHC-I by viral E3 ligase mK3. J. Cell Biol. 177:613-624. (Pubitemid 46799833)
41. Winkler, M., and T. Stamminger. 1996. A specific subform of the human cytomegalovirus transactivator protein pUL69 is contained within the tegument of virus particles. J. Virol. 70:8984-8987. (Pubitemid 26378483)
42. Xuan, B., Z. Qian, E. Torigoi, and D. Yu. 2009. Human cytomegalovirus protein pUL38 induces ATF4 expression, inhibits persistent JNK phosphorylation, and suppresses endoplasmic reticulum stress-induced cell death. J. Virol. 83:3463-3474.
43. 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.
44. 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)
45. Yuksek, K., W. L. Chen, D. Chien, and J. H. Ou. 2009. Ubiquitin-independent degradation of hepatitis C virus F protein. J. Virol. 83:612-621.
46. Zhou, Y. F., M. B. Leon, M. A. Waclawiw, J. J. Popma, Z. X. Yu, T. Finkel, and S. E. Epstein. 1996. Association between prior cytomegalovirus infection and the risk of restenosis after coronary atherectomy. N. Engl. J. Med. 335:624-630.