Human cytomegalovirus pUL93 is required for viral genome cleavage and packaging

Journal of Virology

Volumn 89, Issue 23, 2015, Pages 12221-12225

  DeRussy, Bernadette M ^a   Tandon, Ritesh ^a  

^a UNIVERSITY OF MISSISSIPPI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PUL93 PROTEIN; UNCLASSIFIED DRUG; VIRUS DNA; VIRUS PROTEIN; CAPSID PROTEIN; STOP CODON; UL93 PROTEIN, HUMAN CYTOMEGALOVIRUS; VIRAL PROTEIN;

ARTICLE; CONTROLLED STUDY; DNA CLEAVAGE; DNA PACKAGING; GENE EXPRESSION; HUMAN CYTOMEGALOVIRUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; VIRUS GENE; VIRUS GENOME; VIRUS NUCLEOCAPSID; CYTOMEGALOVIRUS; GENE EXPRESSION REGULATION; GENETIC ENGINEERING; GENETICS; HUMAN; METABOLISM; PHYSIOLOGY; PROCEDURES; STOP CODON; TRANSMISSION ELECTRON MICROSCOPY; VIRUS ASSEMBLY;

CAPSID PROTEINS; CODON, NONSENSE; CYTOMEGALOVIRUS; GENE EXPRESSION REGULATION, VIRAL; GENETIC ENGINEERING; HUMANS; MICROSCOPY, ELECTRON, TRANSMISSION; VIRAL PROTEINS; VIRUS ASSEMBLY;

EID: 84949665646     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02382-15     Document Type: Article

References (42)

1. 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. http://dx.doi.org/10.1073/pnas.2334032100.
2. 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. http://dx.doi.org/10.1073/pnas.1635160100.
3. Taus NS, Salmon B, Baines JD. 1998. The herpes simplex virus 1 UL 17 gene is required for localization of capsids and major and minor capsid proteins to intranuclear sites where viral DNA is cleaved and packaged. Virology 252:115-125. http://dx.doi.org/10.1006/viro.1998.9439.
4. Scholtes L, Baines JD. 2009. Effects of major capsid proteins, capsid assembly, and DNA cleavage/packaging on the pUL17/pUL25 complex of herpes simplex virus 1. J Virol 83:12725-12737. http://dx.doi.org/10.1128/JVI.01658-09.
5. Thurlow JK, Murphy M, Stow ND, Preston VG. 2006. Herpes simplex virus type 1 DNA-packaging protein UL17 is required for efficient binding of UL25 to capsids. J Virol 80:2118-2126. http://dx.doi.org/10.1128/JVI.80.5.2118-2126.2006.
6. Newcomb WW, Homa FL, Brown JC. 2006. Herpes simplex virus capsid structure: DNA packaging protein UL25 is located on the external surface of the capsid near the vertices. J Virol 80:6286-6294. http://dx.doi.org/10.1128/JVI.02648-05.
7. Trus BL, Newcomb WW, Cheng N, Cardone G, Marekov L, Homa FL, Brown JC, Steven AC. 2007. Allosteric signaling and a nuclear exit strategy: binding of UL25/UL17 heterodimers to DNA-filled HSV-1 capsids. Mol Cell 26:479-489. http://dx.doi.org/10.1016/j.molcel.2007.04.010.
8. Preston VG, Murray J, Preston CM, McDougall IM, Stow ND. 2008. The UL25 gene product of herpes simplex virus type 1 is involved in uncoating of the viral genome. J Virol 82:6654-6666. http://dx.doi.org/10.1128/JVI.00257-08.
9. Cockrell SK, Huffman JB, Toropova K, Conway JF, Homa FL. 2011. Residues of the UL25 protein of herpes simplex virus that are required for its stable interaction with capsids. J Virol 85:4875-4887. http://dx.doi.org/10.1128/JVI.00242-11.
10. Toropova K, Huffman JB, Homa FL, Conway JF. 2011. The herpes simplex virus 1 UL17 protein is the second constituent of the capsid vertex-specific component required for DNA packaging and retention. J Virol 85:7513-7522. http://dx.doi.org/10.1128/JVI.00837-11.
11. Klupp BG, Granzow H, Keil GM, Mettenleiter TC. 2006. The capsidassociated UL25 protein of the alphaherpesvirus pseudorabies virus is nonessential for cleavage and encapsidation of genomic DNA but is required for nuclear egress of capsids. J Virol 80:6235-6246. http://dx.doi.org/10.1128/JVI.02662-05.
12. Yang K, Baines JD. 2011. Selection of HSV capsids for envelopment involves interaction between capsid surface components pUL31, pUL17, and pUL25. Proc Natl Acad Sci U S A 108:14276-14281. http://dx.doi.org/10.1073/pnas.1108564108.
13. Yang K, Wills E, Lim HY, Zhou ZH, Baines JD. 2014. Association of herpes simplex virus pUL31 with capsid vertices and components of the capsid vertex-specific complex. J Virol 88:3815-3825. http://dx.doi.org/10.1128/JVI.03175-13.
14. McNab AR, Desai P, Person S, Roof LL, Thomsen DR, Newcomb WW, Brown JC, Homa FL. 1998. The product of the herpes simplex virus type 1 UL25 gene is required for encapsidation but not for cleavage of replicated viral DNA. J Virol 72:1060-1070.
15. Sharma M, Kamil JP, Coughlin M, Reim NI, Coen DM. 2014. Human cytomegalovirus UL50 and UL53 recruit viral protein kinase UL97, not protein kinase C, for disruption of nuclear lamina and nuclear egress in infected cells. J Virol 88:249-262. http://dx.doi.org/10.1128/JVI.02358-13.
16. Tanner EJ, Liu HM, Oberste MS, Pallansch M, Collett MS, Kirkegaard K. 2014. Dominant drug targets suppress the emergence of antiviral resistance. eLife 3:e03830. http://dx.doi.org/10.7554/eLife.03830.
17. Tischer BK, von Einem J, Kaufer B, Osterrieder N. 2006. Two-step red-mediated recombination for versatile high-efficiency markerlessDNA manipulation in Escherichia coli. Biotechniques 40:191-197. http://dx.doi.org/10.2144/000112096.
18. Thomason L, Court DL, Bubunenko M, Costantino N, Wilson H, Datta S, Oppenheim A. 2007. Recombineering: genetic engineering in bacteria using homologous recombination. Curr Protoc Mol Biol Chapter 1:Unit 1.16. http://dx.doi.org/10.1002/0471142727.mb0116s78.
19. Brechtel TM, Mocarski ES, Tandon R. 2014. Highly acidic C-terminal region of cytomegalovirus pUL96 determines its functions during virus maturation independently of a direct pp150 interaction. J Virol 88:4493-4503.http://dx.doi.org/10.1128/JVI.03784-13.
20. Omoto S, Mocarski ES. 2013. Cytomegalovirus UL91 is essential for transcription of viral true late (gamma2) genes. J Virol 87:8651-8664. http://dx.doi.org/10.1128/JVI.01052-13.
21. Tandon R, Mocarski ES. 2008. Control of cytoplasmic maturation events by cytomegalovirus tegument protein pp150. J Virol 82:9433-9444. http://dx.doi.org/10.1128/JVI.00533-08.
22. Tandon R, AuCoin DP, Mocarski ES. 2009. Human cytomegalovirus exploits ESCRT machinery in the process of virion maturation. J Virol 83:10797-10807. http://dx.doi.org/10.1128/JVI.01093-09.
23. Tandon R, Mocarski ES. 2012. Viral and host control of cytomegalovirus maturation. Trends Microbiol 20:392-401. http://dx.doi.org/10.1016/j.tim.2012.04.008.
24. Tandon R, Mocarski ES, Conway JF. 2015. The A, B, Cs of herpesvirus capsids. Viruses 7:899-914. http://dx.doi.org/10.3390/v7030899.
25. Black LW, Silverman DJ. 1978. Model for DNA packaging into bacteriophage T4 heads. J Virol 28:643-655.
26. Laemmli UK, Favre M. 1973. Maturation of the head of bacteriophage T4. I. DNA packaging events. J Mol Biol 80:575-599.
27. Fuller DN, Raymer DM, Kottadiel VI, Rao VB, Smith DE. 2007. Single phage T4 DNA packaging motors exhibit large force generation, high velocity, and dynamic variability. Proc Natl Acad Sci U S A 104:16868-16873.http://dx.doi.org/10.1073/pnas.0704008104.
28. Fuller DN, Raymer DM, Rickgauer JP, Robertson RM, Catalano CE, Anderson DL, Grimes S, Smith DE. 2007. Measurements of single DNA molecule packaging dynamics in bacteriophage lambda reveal high forces, high motor processivity, and capsid transformations. J Mol Biol 373: 1113-1122. http://dx.doi.org/10.1016/j.jmb.2007.09.011.
29. Rickgauer JP, Fuller DN, Grimes S, Jardine PJ, Anderson DL, Smith DE. 2008. Portal motor velocity and internal force resisting viral DNA packaging in bacteriophage phi29. Biophys J 94:159-167. http://dx.doi.org/10.1529/biophysj.107.104612.
30. Mocarski ES, Jr, Shenk T, Pass RF. 2006. Cytomegaloviruses, p 2701-2772. In Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin MA, Roizman B, Straus SE (ed), Fields virology, 5th ed. Lippincott Williams & Wilkins, Philadelphia, PA.
31. McVoy MA, Nixon DE, Hur JK, Adler SP. 2000. The ends on herpesvirus DNA replicative concatemers contain pac2 cis cleavage/packaging elements and their formation is controlled by terminal cis sequences. J Virol 74:1587-1592. http://dx.doi.org/10.1128/JVI.74.3.1587-1592.2000.
32. Przech AJ, Yu D, Weller SK. 2003. Point mutations in exon I of the herpes simplex virus putative terminase subunit, UL15, indicate that the most conserved residues are essential for cleavage and packaging. J Virol 77: 9613-9621. http://dx.doi.org/10.1128/JVI.77.17.9613-9621.2003.
33. McVoy MA, Adler SP. 1994. Human cytomegalovirus DNA replicates after early circularization by concatemer formation, and inversion occurs within the concatemer. J Virol 68:1040-1051.
34. Spaete RR, Mocarski ES. 1985. The alpha sequence of the cytomegalovirus genome functions as a cleavage/packaging signal for herpes simplex virus defective genomes. J Virol 54:817-824.
35. Borst EM, Wagner K, Binz A, Sodeik B, Messerle M. 2008. The essential human cytomegalovirus gene UL52 is required for cleavage-packaging of the viral genome. J Virol 82:2065-2078. http://dx.doi.org/10.1128/JVI.01967-07.
36. Underwood MR, Harvey RJ, Stanat SC, Hemphill ML, Miller T, Drach JC, Townsend LB, Biron KK. 1998. Inhibition of human cytomegalovirus DNA maturation by a benzimidazole ribonucleoside is mediated through the UL89 gene product. J Virol 72:717-725.
37. Krosky PM, Underwood MR, Turk SR, Feng KW, Jain RK, Ptak RG, Westerman AC, Biron KK, Townsend LB, Drach JC. 1998. Resistance of human cytomegalovirus to benzimidazole ribonucleosides maps to two open reading frames: UL89 and UL56. J Virol 72:4721-4728.
38. Townsend LB, Devivar RV, Turk SR, Nassiri MR, Drach JC. 1995. Design, synthesis, and antiviral activity of certain 2, 5, 6-trihalo-1-(beta-Dribofuranosyl) benzimidazoles. J Med Chem 38:4098-4105. http://dx.doi.org/10.1021/jm00020a025.
39. Cayatte C, Schneider-Ohrum K, Wang Z, Irrinki A, Nguyen N, Lu J, Nelson C, Servat E, Gemmell L, Citkowicz A, Liu Y, Hayes G, Woo J, Van Nest G, Jin H, Duke G, McCormick AL. 2013. Cytomegalovirus vaccine strain Towne-derived dense bodies induce broad cellular immune responses and neutralizing antibodies that prevent infection of fibroblasts and epithelial cells. J Virol 87:11107-11120. http://dx.doi.org/10.1128/JVI.01554-13.
40. Hwang JS, Kregler O, Schilf R, Bannert N, Drach JC, Townsend LB, Bogner E. 2007. Identification of acetylated, tetrahalogenated benzimidazole D-ribonucleosides with enhanced activity against human cytomegalovirus. J Virol 81:11604-11611. http://dx.doi.org/10.1128/JVI.01130-07.
41. Williams SL, Hartline CB, Kushner NL, Harden EA, Bidanset DJ, Drach JC, Townsend LB, Underwood MR, Biron KK, Kern ER. 2003. In vitro activities of benzimidazole D-and L-ribonucleosides against herpesviruses. Antimicrob Agents Chemother 47:2186-2192. http://dx.doi.org/10.1128/AAC.47.7.2186-2192.2003.
42. Krosky PM, Borysko KZ, Nassiri MR, Devivar RV, Ptak RG, Davis MG, Biron KK, Townsend LB, Drach JC. 2002. Phosphorylation of beta-Dribosylbenzimidazoles is not required for activity against human cytomegalovirus. Antimicrob Agents Chemother 46:478-486. http://dx.doi.org/10.1128/AAC.46.2.478-486.2002.