Varicella-zoster virus ORF49 functions in the efficient production of progeny virus through its interaction with essential tegument protein ORF44

Journal of Virology

Volumn 88, Issue 1, 2014, Pages 188-201

  Sadaoka, Tomohiko ^a,b   Serada, Satoshi ^b   Kato, Junko ^a   Hayashi, Mayuko ^a,b   Gomi, Yasuyuki ^c   Naka, Tetsuji ^b   Yamanishi, Koichi ^b   Mori, Yasuko ^a,b  

^a KOBE UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b NATIONAL INSTITUTE OF BIOMEDICAL INNOVATION   (Japan)

^c Osaka University   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARTIC ACID; GLUTAMIC ACID; PHENYLALANINE; UNCLASSIFIED DRUG; VIRUS PROTEIN; VIRUS PROTEIN ORF44; VIRUS PROTEIN ORF49;

AMINO ACID SUBSTITUTION; ARTICLE; CONTROLLED STUDY; GENE; GENE CLUSTER; GENE DELETION; GENE EXPRESSION; GENE FUNCTION; GENE IDENTIFICATION; GENE INTERACTION; GENETIC CONSERVATION; HERPES ZOSTER; HUMAN; HUMAN CELL; MUTAGENESIS; NONHUMAN; OPEN READING FRAME; ORF44 GENE; ORF49 GENE; PHENOTYPE; PRIORITY JOURNAL; PROGENY; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; VARICELLA ZOSTER VIRUS; VIROGENESIS;

BASE SEQUENCE; DNA PRIMERS; HERPESVIRUS 3, HUMAN; MASS SPECTROMETRY; OPEN READING FRAMES; VIRAL PLAQUE ASSAY; VIRAL PROTEINS;

EID: 84890862425     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02245-13     Document Type: Article

References (52)

1. Moffat J, Ku CC, Zerboni L, Sommer M, Arvin A. 2007. VZV: pathogenesis and the disease consequences of primary infection, p 675-688. In Arvin A, Campadelli-Fiume G, Mocarski E, Moore PS, Roizman B, Whitley R, Yamanishi K (ed), Human herpesviruses: biology, therapy, and immunoprophylaxis. Cambridge University Press, Cambridge, United Kingdom.
2. Baines JD, Pellett PE. 2007. Genetic comparison of human alphaherpesvirus genomes, p 61-69. In Arvin A, Campadelli-Fiume G, Mocarski E, Moore PS, Roizman B, Whitley R, Yamanishi K (ed), Human herpesviruses: biology, therapy, and immunoprophylaxis. Cambridge University Press, Cambridge, United Kingdom.
3. Davison AJ, Scott JE. 1986. The complete DNA sequence of varicellazoster virus. J. Gen. Virol. 67:1759-1816. http://dx.doi.org/10.1099/0022 -1317-67-9-1759.
4. Davison AJ. 2007. Comparative analysis of the genomes, p 10-26. In Arvin A, Campadelli-Fiume G, Mocarski E, Moore PS, Roizman B, Whitley R, Yamanishi K (ed), Human herpesviruses: biology, therapy, and immunoprophylaxis. Cambridge University Press, Cambridge, United Kingdom.
5. Zhang Z, Selariu A, Warden C, Huang G, Huang Y, Zaccheus O, Cheng T, Xia N, Zhu H. 2010. Genome-wide mutagenesis reveals that ORF7 is a novel VZV skin-tropic factor. PLoS Pathog. 6:e1000971. http://dx.doi.org /10.1371/journal.ppat.1000971.
6. Sadaoka T, Yoshii H, Imazawa T, Yamanishi K, Mori Y. 2007. Deletion in open reading frame 49 of varicella-zoster virus reduces virus growth in human malignant melanoma cells but not in human embryonic fibroblasts. J. Virol. 81:12654-12665. http://dx.doi.org/10.1128/JVI.01183-07.
7. Baines JD, Jacob RJ, Simmerman L, Roizman B. 1995. The herpes simplex virus 1 UL11 proteins are associated with cytoplasmic and nuclear membranes and with nuclear bodies of infected cells. J. Virol. 69:825-833.
8. Britt WJ, Jarvis M, Seo JY, Drummond D, Nelson J. 2004. Rapid genetic engineering of human cytomegalovirus by using a lambda phage linear recombination system: demonstration that pp28 (UL99) is essential for production of infectious virus. J. Virol. 78:539-543. http://dx.doi.org/10 .1128/JVI.78.1.539-543.2004.
9. Silva MC, Yu QC, Enquist L, Shenk T. 2003. Human cytomegalovirus UL99-encoded pp28 is required for the cytoplasmic envelopment of tegument- associated capsids. J. Virol. 77:10594-10605. http://dx.doi.org/10 .1128/JVI.77.19.10594-10605.2003.
10. MacLean CA, Dolan A, Jamieson FE, McGeoch DJ. 1992. The myristylated virion proteins of herpes simplex virus type 1: investigation of their role in the virus life cycle. J. Gen. Virol. 73:539-547. http://dx.doi.org/10 .1099/0022-1317-73-3-539.
11. Silva MC, Schroer J, Shenk T. 2005. Human cytomegalovirus cell-to-cell spread in the absence of an essential assembly protein. Proc. Natl. Acad. Sci. U. S. A. 102:2081-2086. http://dx.doi.org/10.1073/pnas.0409597102.
12. Loomis JS, Courtney RJ, Wills JW. 2003. Binding partners for the UL11 tegument protein of herpes simplex virus type 1. J. Virol. 77:11417-11424. http://dx.doi.org/10.1128/JVI.77.21.11417-11424.2003.
13. Guo H, Wang L, Peng L, Zhou ZH, Deng H. 2009. Open reading frame 33 of a gammaherpesvirus encodes a tegument protein essential for virion morphogenesis and egress. J. Virol. 83:10582-10595. http://dx.doi.org/10 .1128/JVI.00497-09.
14. Liu Y, Cui Z, Zhang Z, Wei H, Zhou Y, Wang M, Zhang XE. 2009. The tegument protein UL94 of human cytomegalovirus as a binding partner for tegument protein pp28 identified by intracellular imaging. Virology 388:68-77. http://dx.doi.org/10.1016/j.virol.2009.03.007.
15. Maninger S, Bosse JB, Lemnitzer F, Pogoda M, Mohr CA, von Einem J, Walther P, Koszinowski UH, Ruzsics Z. 2011. M94 is essential for the secondary envelopment of murine cytomegalovirus. J. Virol. 85:9254-9267. http://dx.doi.org/10.1128/JVI.00443-11.
16. Meckes DG, Jr, Wills JW. 2007. Dynamic interactions of the UL16 tegument protein with the capsid of herpes simplex virus. J. Virol. 81:13028- 13036. http://dx.doi.org/10.1128/JVI.01306-07.
17. Nalwanga D, Rempel S, Roizman B, Baines JD. 1996. The UL 16 gene product of herpes simplex virus 1 is a virion protein that colocalizes with intranuclear capsid proteins. Virology 226:236-242. http://dx.doi.org/10 .1006/viro.1996.0651.
18. Oshima S, Daikoku T, Shibata S, Yamada H, Goshima F, Nishiyama Y. 1998. Characterization of the UL16 gene product of herpes simplex virus type 2. Arch. Virol. 143:863-880. http://dx.doi.org/10.1007/s007050050338.
19. Yeh PC, Meckes DG, Jr, Wills JW. 2008. Analysis of the interaction between the UL11 and UL16 tegument proteins of herpes simplex virus. J. Virol. 82:10693-10700. http://dx.doi.org/10.1128/JVI.01230-08.
20. Johnson DC, Baines JD. 2011. Herpesviruses remodel host membranes for virus egress. Nat. Rev. Microbiol. 9:382-394. http://dx.doi.org/10.1038 /nrmicro2559.
21. Baines JD, Roizman B. 1991. The open reading frames UL3, UL4, UL10, and UL16 are dispensable for the replication of herpes simplex virus 1 in cell culture. J. Virol. 65:938-944.
22. 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.
23. Klupp BG, Bottcher S, Granzow H, Kopp M, Mettenleiter TC. 2005. Complex formation between the UL16 and UL21 tegument proteins of pseudorabies virus. J. Virol. 79:1510-1522. http://dx.doi.org/10.1128/JVI .79.3.1510-1522.2005.
24. Phillips SL, Bresnahan WA. 2012. The human cytomegalovirus (HCMV) tegument protein UL94 is essential for secondary envelopment of HCMV virions. J. Virol. 86:2523-2532. http://dx.doi.org/10.1128/JVI.06548-11.
25. 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.
26. Chadha P, Han J, Starkey JL, Wills JW. 2012. Regulated interaction of tegument proteins UL16 and UL11 from herpes simplex virus. J. Virol. 86:11886-11898. http://dx.doi.org/10.1128/JVI.01879-12.
27. Phillips SL, Cygnar D, Thomas A, Bresnahan WA. 2012. Interaction between the human cytomegalovirus tegument proteins UL94 and UL99 is essential for virus replication. J. Virol. 86:9995-10005. http://dx.doi.org /10.1128/JVI.01078-12.
28. Stellberger T, Hauser R, Baiker A, Pothineni VR, Haas J, Uetz P. 2010. Improving the yeast two-hybrid system with permutated fusions proteins: the varicella zoster virus interactome. Proteome Sci. 8:8. http://dx.doi.org /10.1186/1477-5956-8-8.
29. Uetz P, Dong YA, Zeretzke C, Atzler C, Baiker A, Berger B, Rajagopala SV, Roupelieva M, Rose D, Fossum E, Haas J. 2006. Herpesviral protein networks and their interaction with the human proteome. Science 311: 239-242. http://dx.doi.org/10.1126/science.1116804.
30. Sadaoka T, Yanagi T, Yamanishi K, Mori Y. 2010. Characterization of the varicella-zoster virus ORF50 gene, which encodes glycoprotein M. J. Virol. 84:3488-3502. http://dx.doi.org/10.1128/JVI.01838-09.
31. Niwa H, Yamamura K, Miyazaki J. 1991. Efficient selection for highexpression transfectants with a novel eukaryotic vector. Gene 108:193- 199. http://dx.doi.org/10.1016/0378-1119(91)90434-D.
32. Sadaoka T, Yamanishi K, Mori Y. 2006. Human herpesvirus 7 U47 gene products are glycoproteins expressed in virions and associate with glycoprotein H. J. Gen. Virol. 87:501-508. http://dx.doi.org/10.1099/vir.0 .81374-0.
33. Okuno T, Yamanishi K, Shiraki K, Takahashi M. 1983. Synthesis and processing of glycoproteins of varicella-zoster virus (VZV) as studied with monoclonal antibodies to VZV antigens. Virology 129:357-368. http://dx .doi.org/10.1016/0042-6822(83)90175-7.
34. Nagaike K, Mori Y, Gomi Y, Yoshii H, Takahashi M, Wagner M, Koszinowski U, Yamanishi K. 2004. Cloning of the varicella-zoster virus genome as an infectious bacterial artificial chromosome in Escherichia coli. Vaccine 22:4069-4074. http://dx.doi.org/10.1016/j.vaccine.2004.03 .062.
35. Narayanan K, Williamson R, Zhang Y, Stewart AF, Ioannou PA. 1999. Efficient and precise engineering of a 200 kb beta-globin human/bacterial artificial chromosome in E. coli DH10B using an inducible homologous recombination system. Gene Ther. 6:442-447. http://dx.doi.org/10.1038 /sj.gt.3300901.
36. Cherepanov PP, Wackernagel W. 1995. Gene disruption in Escherichia coli: TcR and KmR cassettes with the option of Flp-catalyzed excision of the antibiotic-resistance determinant. Gene 158:9-14. http://dx.doi.org /10.1016/0378-1119(95)00193-A.
37. Hobom U, Brune W, Messerle M, Hahn G, Koszinowski UH. 2000. Fast screening procedures for random transposon libraries of cloned herpesvirus genomes: mutational analysis of human cytomegalovirus envelope glycoprotein genes. J. Virol. 74:7720-7729. http://dx.doi.org/10.1128/JVI .74.17.7720-7729.2000.
38. Shevchenko A, Wilm M, Vorm O, Mann M. 1996. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 68:850-858. http://dx.doi.org/10.1021/ac950914h.
39. Carpenter JE, Henderson EP, Grose C. 2009. Enumeration of an extremely high particle-to-PFU ratio for varicella-zoster virus. J. Virol. 83: 6917-6921. http://dx.doi.org/10.1128/JVI.00081-09.
40. Shiraki K, Takahashi M. 1982. Virus particles and glycoprotein excreted from cultured cells infected with varicella-zoster virus (VZV). J. Gen. Virol. 61:271-275. http://dx.doi.org/10.1099/0022-1317-61-2-271.
41. Gabel CA, Dubey L, Steinberg SP, Sherman D, Gershon MD, Gershon AA. 1989. Varicella-zoster virus glycoprotein oligosaccharides are phosphorylated during posttranslational maturation. J. Virol. 63:4264-4276.
42. Gershon AA, Sherman DL, Zhu Z, Gabel CA, Ambron RT, Gershon MD. 1994. Intracellular transport of newly synthesized varicella-zoster virus: final envelopment in the trans-Golgi network. J. Virol. 68:6372- 6390.
43. Harson R, Grose C. 1995. Egress of varicella-zoster virus from the melanoma cell: a tropism for the melanocyte. J. Virol. 69:4994-5010.
44. Ali MA, Li Q, Fischer ER, Cohen JI. 2009. The insulin degrading enzyme binding domain of varicella-zoster virus (VZV) glycoprotein E is important for cell-to-cell spread and VZV infectivity, while a glycoprotein I binding domain is essential for infection. Virology 386:270-279. http://dx .doi.org/10.1016/j.virol.2009.01.023.
45. Tischer BK, Kaufer BB, Sommer M, Wussow F, Arvin AM, Osterrieder N. 2007. A self-excisable infectious bacterial artificial chromosome clone of varicella-zoster virus allows analysis of the essential tegument protein encoded by ORF9. J. Virol. 81:13200-13208. http://dx.doi.org/10.1128 /JVI.01148-07.
46. Yamagishi Y, Sadaoka T, Yoshii H, Somboonthum P, Imazawa T, Nagaike K, Ozono K, Yamanishi K, Mori Y. 2008. Varicella-zoster virus glycoprotein M homolog is glycosylated, is expressed on the viral envelope, and functions in virus cell-to-cell spread. J. Virol. 82:795-804. http: //dx.doi.org/10.1128/JVI.01722-07.
47. Betts MJ, Russell RB. 22 May 2003. Amino acid properties and consequences of substitutions. Chapter 14. In Barnes MR, Gray IC (ed), Bioinformatics for geneticists. Wiley, Chichester, West Sussex, England. http: //dx.doi.org/10.1002/0470867302.ch14.
48. Burley SK, Petsko GA. 1985. Aromatic-aromatic interaction: a mechanism of protein structure stabilization. Science 229:23-28. http://dx.doi .org/10.1126/science.3892686.
49. Eidenschink LA, Kier BL, Andersen NH. 2009. Determinants of fold stabilizing aromatic-aromatic interactions in short peptides. Adv. Exp. Med. Biol. 611:73-74. http://dx.doi.org/10.1007/978-0-387-73657-0_32.
50. Meckes DG, Jr, Marsh JA, Wills JW. 2010. Complex mechanisms for the packaging of the UL16 tegument protein into herpes simplex virus. Virology 398:208-213. http://dx.doi.org/10.1016/j.virol.2009.12.004.
51. Han J, Chadha P, Meckes DG, Jr, Baird NL, Wills JW. 2011. Interaction and interdependent packaging of tegument protein UL11 and glycoprotein E of herpes simplex virus. J. Virol. 85:9437-9446. http://dx.doi.org/10 .1128/JVI.05207-11.
52. Harper AL, Meckes DG, Jr, Marsh JA, Ward MD, Yeh PC, Baird NL, Wilson CB, Semmes OJ, Wills JW. 2010. Interaction domains of the UL16 and UL21 tegument proteins of herpes simplex virus. J. Virol. 84: 2963-2971. http://dx.doi.org/10.1128/JVI.02015-09.