Viral and Host Control of Cytomegalovirus Maturation

Overview

Journal Trends Microbiol

Date 2012 May 29

PMID 22633075

Citations 84

Authors

Ritesh Tandon

Edward S Mocarski

Affiliations

Soon will be listed here.

Abstract

Maturation in herpesviruses initiates in the nucleus of the infected cell, with encapsidation of viral DNA to form nucleocapsids, and concludes with envelopment in the cytoplasm to form infectious virions that egress the cell. The entire process of virus maturation is orchestrated by protein-protein interactions and enzymatic activities of viral and host origin. Viral tegument proteins play important roles in maintaining the structural stability of capsids and directing the acquisition of virus envelope. Envelopment occurs at modified host membranes and exploits host vesicular trafficking. In this review, we summarize current knowledge of and concepts in human cytomegalovirus (HCMV) maturation and their parallels in other herpesviruses, with an emphasis on viral and host factors that regulate this process.

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References

Crump C, Hung C, Thomas L, Wan L, Thomas G . Role of PACS-1 in trafficking of human cytomegalovirus glycoprotein B and virus production. J Virol. 2003; 77(20):11105-13. PMC: 224974. DOI: 10.1128/jvi.77.20.11105-11113.2003. View

Muranyi W, Haas J, Wagner M, Krohne G, Koszinowski U . Cytomegalovirus recruitment of cellular kinases to dissolve the nuclear lamina. Science. 2002; 297(5582):854-7. DOI: 10.1126/science.1071506. View

Milbradt J, Auerochs S, Marschall M . Cytomegaloviral proteins pUL50 and pUL53 are associated with the nuclear lamina and interact with cellular protein kinase C. J Gen Virol. 2007; 88(Pt 10):2642-2650. DOI: 10.1099/vir.0.82924-0. View

Rupp B, Ruzsics Z, Buser C, Adler B, Walther P, Koszinowski U . Random screening for dominant-negative mutants of the cytomegalovirus nuclear egress protein M50. J Virol. 2007; 81(11):5508-17. PMC: 1900260. DOI: 10.1128/JVI.02796-06. View

Seo J, Britt W . Multimerization of tegument protein pp28 within the assembly compartment is required for cytoplasmic envelopment of human cytomegalovirus. J Virol. 2008; 82(13):6272-87. PMC: 2447089. DOI: 10.1128/JVI.02345-07. View

Marschall M, Feichtinger S, Milbradt J . Regulatory roles of protein kinases in cytomegalovirus replication. Adv Virus Res. 2011; 80:69-101. DOI: 10.1016/B978-0-12-385987-7.00004-X. View

Sam M, Evans B, Coen D, Hogle J . Biochemical, biophysical, and mutational analyses of subunit interactions of the human cytomegalovirus nuclear egress complex. J Virol. 2009; 83(7):2996-3006. PMC: 2655548. DOI: 10.1128/JVI.02441-08. View

Yang K, Baines J . Selection of HSV capsids for envelopment involves interaction between capsid surface components pUL31, pUL17, and pUL25. Proc Natl Acad Sci U S A. 2011; 108(34):14276-81. PMC: 3161533. DOI: 10.1073/pnas.1108564108. View

Liu S, Sharon-Friling R, Ivanova P, Milne S, Myers D, Rabinowitz J . Synaptic vesicle-like lipidome of human cytomegalovirus virions reveals a role for SNARE machinery in virion egress. Proc Natl Acad Sci U S A. 2011; 108(31):12869-74. PMC: 3150939. DOI: 10.1073/pnas.1109796108. View

10.

Womack A, Shenk T . Human cytomegalovirus tegument protein pUL71 is required for efficient virion egress. mBio. 2010; 1(5). PMC: 2999941. DOI: 10.1128/mBio.00282-10. View

11.

Schauflinger M, Fischer D, Schreiber A, Chevillotte M, Walther P, Mertens T . The tegument protein UL71 of human cytomegalovirus is involved in late envelopment and affects multivesicular bodies. J Virol. 2011; 85(8):3821-32. PMC: 3126135. DOI: 10.1128/JVI.01540-10. View

12.

Bottcher S, Granzow H, Maresch C, Mohl B, Klupp B, Mettenleiter T . Identification of functional domains within the essential large tegument protein pUL36 of pseudorabies virus. J Virol. 2007; 81(24):13403-11. PMC: 2168856. DOI: 10.1128/JVI.01643-07. View

13.

Mettenleiter T . Herpesvirus assembly and egress. J Virol. 2002; 76(4):1537-47. PMC: 135924. DOI: 10.1128/jvi.76.4.1537-1547.2002. View

14.

Zipeto D, Baldanti F, Percivalle E, Gerna G, Milanesi G . Identification of a human cytomegalovirus mutant in the pp150 matrix phosphoprotein gene with a growth-defective phenotype. J Gen Virol. 1993; 74 ( Pt 8):1645-8. DOI: 10.1099/0022-1317-74-8-1645. View

15.

Baxter M, Gibson W . Cytomegalovirus basic phosphoprotein (pUL32) binds to capsids in vitro through its amino one-third. J Virol. 2001; 75(15):6865-73. PMC: 114414. DOI: 10.1128/JVI.75.15.6865-6873.2001. View

16.

Dunn W, Chou C, Li H, Hai R, Patterson D, Stolc V . Functional profiling of a human cytomegalovirus genome. Proc Natl Acad Sci U S A. 2003; 100(24):14223-8. PMC: 283573. DOI: 10.1073/pnas.2334032100. View

17.

Newcomb W, Homa F, Thomsen D, Trus B, Cheng N, Steven A . Assembly of the herpes simplex virus procapsid from purified components and identification of small complexes containing the major capsid and scaffolding proteins. J Virol. 1999; 73(5):4239-50. PMC: 104203. DOI: 10.1128/JVI.73.5.4239-4250.1999. View

18.

Moorman N, Sharon-Friling R, Shenk T, Cristea I . A targeted spatial-temporal proteomics approach implicates multiple cellular trafficking pathways in human cytomegalovirus virion maturation. Mol Cell Proteomics. 2009; 9(5):851-60. PMC: 2871419. DOI: 10.1074/mcp.M900485-MCP200. View

19.

Salsman J, Jagannathan M, Paladino P, Chan P, Dellaire G, Raught B . Proteomic profiling of the human cytomegalovirus UL35 gene products reveals a role for UL35 in the DNA repair response. J Virol. 2011; 86(2):806-20. PMC: 3255807. DOI: 10.1128/JVI.05442-11. View

20.

Bottcher S, Maresch C, Granzow H, Klupp B, Teifke J, Mettenleiter T . Mutagenesis of the active-site cysteine in the ubiquitin-specific protease contained in large tegument protein pUL36 of pseudorabies virus impairs viral replication in vitro and neuroinvasion in vivo. J Virol. 2008; 82(12):6009-16. PMC: 2395145. DOI: 10.1128/JVI.00280-08. View