Differences in the regulatory and functional effects of the Us3 protein kinase activities of herpes simplex virus 1 and 2

Journal of Virology

Volumn 83, Issue 22, 2009, Pages 11624-11634

  Morimoto, Tomomi ^a   Arii, Jun ^a,b   Tanaka, Michiko ^c   Sata, Tetsutaro ^c   Akashi, Hiroomi ^b   Yamada, Masao ^d   Nishiyama, Yukihiro ^e   Uema, Masashi ^a   Kawaguchi, Yasushi ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

^d OKAYAMA UNIVERSITY MEDICAL SCHOOL   (Japan)

^e NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; ASPARTIC ACID; GLYCOPROTEIN B; PROTEIN KINASE; UNCLASSIFIED DRUG; US3 PROTEIN KINASE; VIRUS ENVELOPE PROTEIN;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; AUTOPHOSPHORYLATION; CELL SURFACE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME REGULATION; FEMALE; HERPES SIMPLEX VIRUS 1; HERPES SIMPLEX VIRUS 2; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; INOCULATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; SOUTHERN BLOTTING; VIRUS NUCLEOCAPSID; VIRUS VIRULENCE;

ANIMALS; CERCOPITHECUS AETHIOPS; CHROMOSOMES, ARTIFICIAL, BACTERIAL; FEMALE; GENE EXPRESSION REGULATION, VIRAL; HERPESVIRUS 1, HUMAN; HERPESVIRUS 2, HUMAN; MICE; MICE, INBRED ICR; MUTAGENESIS, SITE-DIRECTED; NUCLEAR PROTEINS; NUCLEOCAPSID; PROTEIN-SERINE-THREONINE KINASES; VERO CELLS; VIRAL ENVELOPE PROTEINS; VIRAL PROTEINS; VIRULENCE;

HUMAN HERPESVIRUS 1; HUMAN HERPESVIRUS 2; MUS;

EID: 70350309676     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00993-09     Document Type: Article

References (46)

1. Asano, S., T. Honda, F. Goshima, D. Watanabe, Y. Miyake, Y. Sugiura, and Y. Nishiyama. 1999. US3 protein kinase of herpes simplex virus type 2 plays a role in protecting corneal epithelial cells from apoptosis in infected mice. J. Gen. Virol. 80(Pt. 1):51-56.
2. Cunningham, C., and A. J. Davison. 1993. A cosmid-based system for constructing mutants of herpes simplex virus type 1. Virology 197:116-124. (Pubitemid 23313539)
3. Dephoure, N., C. Zhou, J. Villen, S. A. Beausoleil, C. E. Bakalarski, S. J. Elledge, and S. P. Gygi. 2008. A quantitative atlas of mitotic phosphorylation. Proc. Natl. Acad. Sci. USA 105:10762-10767.
4. Dolan, A., F. E. Jamieson, C. Cunningham, B. C. Barnett, and D. J. Mc- Geoch. 1998. The genome sequence of herpes simplex virus type 2. J. Virol. 72:2010-2021. (Pubitemid 28100755)
5. Ejercito, P. M., E. D. Kieff, and B. Roizman. 1968. Characterization of herpes simplex virus strains differing in their effects on social behavior of infected cells. J. Gen. Virol. 2:357-364.
6. Frame, M. C., F. C. Purves, D. J. McGeoch, H. S. Marsden, and D. P. Leader. 1987. Identification of the herpes simplex virus protein kinase as the product of viral gene US3. J. Gen. Virol. 68(Pt. 10):2699-2704.
7. Hanks, S. K., A. M. Quinn, and T. Hunter. 1988. The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science 241:42-52.
8. He, Z., Y. S. He, Y. Kim, L. Chu, C. Ohmstede, K. K. Biron, and D. M. Coen. 1997. The human cytomegalovirus UL97 protein is a protein kinase that autophosphorylates on serines and threonines. J. Virol. 71:405-411. (Pubitemid 26412306)
9. Inoue, Y., Y. Ohashi, Y. Shimomura, R. Manabe, M. Yamada, S. Ueda, and S. Kato. 1990. Herpes simplex virus glycoprotein D. Protective immunity against murine herpetic keratitis. Investig. Ophthalmol. Vis. Sci. 31:411-418.
10. Jarosinski, K. W., N. G. Margulis, J. P. Kamil, S. J. Spatz, V. K. Nair, and N. Osterrieder. 2007. Horizontal transmission of Marek's disease virus requires US2, the UL13 protein kinase, and gC. J. Virol. 81:10575-10587.
11. Kanamori, M., S. Watanabe, R. Honma, M. Kuroda, S. Imai, K. Takada, N. Yamamoto, Y. Nishiyama, and Y. Kawaguchi. 2004. Epstein-Barr virus nuclear antigen leader protein induces expression of thymus- and activation-regulated chemokine in B cells. J. Virol. 78:3984-3993. (Pubitemid 38437204)
12. Kato, A., J. Arii, I. Shiratori, H. Akashi, H. Arase, and Y. Kawaguchi. 2009. Herpes simplex virus 1 protein kinase Us3 phosphorylates viral envelope glycoprotein B and regulates its expression on the cell surface. J. Virol. 83:250-261.
13. Kato, A., M. Tanaka, M. Yamamoto, R. Asai, T. Sata, Y. Nishiyama, and Y. Kawaguchi. 2008. Identification of a physiological phosphorylation site of the herpes simplex virus 1-encoded protein kinase Us3 which regulates its optimal catalytic activity in vitro and influences its function in infected cells. J. Virol. 82:6172-6189. (Pubitemid 351875099)
14. Kato, A., M. Yamamoto, T. Ohno, H. Kodaira, Y. Nishiyama, and Y. Kawaguchi. 2005. Identification of proteins phosphorylated directly by the Us3 protein kinase encoded by herpes simplex virus 1. J. Virol. 79:9325-9331. (Pubitemid 40934845)
15. Kato, A., M. Yamamoto, T. Ohno, M. Tanaka, T. Sata, Y. Nishiyama, and Y. Kawaguchi. 2006. Herpes simplex virus 1-encoded protein kinase UL13 phosphorylates viral Us3 protein kinase and regulates nuclear localization of viral envelopment factors UL34 and UL31. J. Virol. 80:1476-1486. (Pubitemid 43134104)
16. Kawaguchi, Y., K. Kato, M. Tanaka, M. Kanamori, Y. Nishiyama, and Y. Yamanashi. 2003. Conserved protein kinases encoded by herpesviruses and cellular protein kinase cdc2 target the same phosphorylation site in eukaryotic elongation factor 1δ. J. Virol. 77:2359-2368. (Pubitemid 36222759)
17. Kawaguchi, Y., C. Van Sant, and B. Roizman. 1997. Herpes simplex virus 1 alpha regulatory protein ICP0 interacts with and stabilizes the cell cycle regulator cyclin D3. J. Virol. 71:7328-7336. (Pubitemid 27391671)
18. Klupp, B. G., H. Granzow, W. Fuchs, G. M. Keil, S. Finke, and T. C. Mettenleiter. 2007. Vesicle formation from the nuclear membrane is induced by coexpression of two conserved herpesvirus proteins. Proc. Natl. Acad. Sci. USA 104:7241-7246.
19. Klupp, B. G., H. Granzow, and T. C. Mettenleiter. 2001. Effect of the pseudorabies virus US3 protein on nuclear membrane localization of the UL34 protein and virus egress from the nucleus. J. Gen. Virol. 82:2363-2371.
20. Koshizuka, T., Y. Kawaguchi, F. Goshima, I. Mori, and Y. Nishiyama. 2006. Association of two membrane proteins encoded by herpes simplex virus type 2, UL11 and UL56. Virus Genes 32:153-163.
21. Leach, N., S. L. Bjerke, D. K. Christensen, J. M. Bouchard, F. Mou, R. Park, J. Baines, T. Haraguchi, and R. J. Roller. 2007. Emerin is hyperphosphorylated and redistributed in herpes simplex virus type 1-infected cells in a manner dependent on both UL34 and US3. J. Virol. 81:10792-10803. (Pubitemid 47463352)
22. Leopardi, R., C. Van Sant, and B. Roizman. 1997. The herpes simplex virus 1 protein kinase US3 is required for protection from apoptosis induced by the virus. Proc. Natl. Acad. Sci. USA 94:7891-7896.
23. McGeoch, D. J., M. A. Dalrymple, A. J. Davison, A. Dolan, M. C. Frame, D. McNab, L. J. Perry, J. E. Scott, and P. Taylor. 1988. The complete DNA sequence of the long unique region in the genome of herpes simplex virus type 1. J. Gen. Virol. 69(Pt. 7):1531-1574.
24. McGeoch, D. J., and A. J. Davison. 1986. Alphaherpesviruses possess a gene homologous to the protein kinase gene family of eukaryotes and retroviruses. Nucleic Acids Res. 14:1765-1777.
25. Meignier, B., R. Longnecker, P. Mavromara-Nazos, A. E. Sears, and B. Roizman. 1988. Virulence of and establishment of latency by genetically engineered deletion mutants of herpes simplex virus 1. Virology 162:251-254. (Pubitemid 18063116)
26. Morimoto, T., J. Arii, H. Akashi, and Y. Kawaguchi. 2009. Identification of multiple sites suitable for insertion of foreign genes in herpes simplex virus genomes. Microbiol. Immunol. 53:155-161.
27. Morris, J. B., H. Hofemeister, and P. O'Hare. 2007. Herpes simplex virus infection induces phosphorylation and delocalization of emerin, a key inner nuclear membrane protein. J. Virol. 81:4429-4437.
28. Mou, F., T. Forest, and J. D. Baines. 2007. US3 of herpes simplex virus type 1 encodes a promiscuous protein kinase that phosphorylates and alters localization of lamin A/C in infected cells. J. Virol. 81:6459-6470. (Pubitemid 46878051)
29. Mou, F., E. Wills, and J. D. Baines. 2009. Phosphorylation of the U(L)31 protein of herpes simplex virus 1 by the U(S)3-encoded kinase regulates localization of the nuclear envelopment complex and egress of nucleocapsids. J. Virol. 83:5181-5191.
30. Munger, J., A. V. Chee, and B. Roizman. 2001. The U(S)3 protein kinase blocks apoptosis induced by the d120 mutant of herpes simplex virus 1 at a premitochondrial stage. J. Virol. 75:5491-5497. (Pubitemid 32488142)
31. Munger, J., and B. Roizman. 2001. The US3 protein kinase of herpes simplex virus 1 mediates the posttranslational modification of BAD and prevents BAD-induced programmed cell death in the absence of other viral proteins. Proc. Natl. Acad. Sci. USA 98:10410-10415.
32. Murata, T., F. Goshima, Y. Nishizawa, T. Daikoku, H. Takakuwa, K. Ohtsuka, T. Yoshikawa, and Y. Nishiyama. 2002. Phosphorylation of cytokeratin 17 by herpes simplex virus type 2 US3 protein kinase. Microbiol. Immunol. 46:707-719.
33. Nishiyama, Y., Y. Yamada, R. Kurachi, and T. Daikoku. 1992. Construction of a US3 lacZ insertion mutant of herpes simplex virus type 2 and characterization of its phenotype in vitro and in vivo. Virology 190:256-268.
34. Nozawa, N., Y. Kawaguchi, M. Tanaka, A. Kato, A. Kato, H. Kimura, and Y. Nishiyama. 2005. Herpes simplex virus type 1 UL51 protein is involved in maturation and egress of virus particles. J. Virol. 79:6947-6956. (Pubitemid 40677326)
35. Ogg, P. D., P. J. McDonell, B. J. Ryckman, C. M. Knudson, and R. J. Roller. 2004. The HSV-1 Us3 protein kinase is sufficient to block apoptosis induced by overexpression of a variety of Bcl-2 family members. Virology 319:212-224.
36. Purves, F. C., R. M. Longnecker, D. P. Leader, and B. Roizman. 1987. Herpes simplex virus 1 protein kinase is encoded by open reading frame US3 which is not essential for virus growth in cell culture. J. Virol. 61:2896-2901.
37. Purves, F. C., D. Spector, and B. Roizman. 1991. The herpes simplex virus 1 protein kinase encoded by the US3 gene mediates posttranslational modification of the phosphoprotein encoded by the UL34 gene. J. Virol. 65:5757-5764.
38. Reynolds, A. E., B. J. Ryckman, J. D. Baines, Y. Zhou, L. Liang, and R. J. Roller. 2001. U(L)31 and U(L)34 proteins of herpes simplex virus type 1 form a complex that accumulates at the nuclear rim and is required for envelopment of nucleocapsids. J. Virol. 75:8803-8817.
39. Reynolds, A. E., E. G. Wills, R. J. Roller, B. J. Ryckman, and J. D. Baines. 2002. Ultrastructural localization of the herpes simplex virus type 1 UL31, UL34, and US3 proteins suggests specific roles in primary envelopment and egress of nucleocapsids. J. Virol. 76:8939-8952.
40. Ryckman, B. J., and R. J. Roller. 2004. Herpes simplex virus type 1 primary envelopment: UL34 protein modification and the US3-UL34 catalytic relationship. J. Virol. 78:399-412.
41. Sagou, K., T. Imai, H. Sagara, M. Uema, and Y. Kawaguchi. 2009. Regulation of the catalytic activity of herpes simplex virus 1 protein kinase Us3 by autophosphorylation and its role in pathogenesis. J. Virol. 83:5773-5783.
42. Smith, R. F., and T. F. Smith. 1989. Identification of new protein kinase-related genes in three herpesviruses, herpes simplex virus, varicella-zoster virus, and Epstein-Barr virus. J. Virol. 63:450-455.
43. Sugimoto, K., M. Uema, H. Sagara, M. Tanaka, T. Sata, Y. Hashimoto, and Y. Kawaguchi. 2008. Simultaneous tracking of capsid, tegument, and envelope protein localization in living cells infected with triply fluorescent herpes simplex virus 1. J. Virol. 82:5198-5211. (Pubitemid 351705229)
44. Tanaka, M., H. Kagawa, Y. Yamanashi, T. Sata, and Y. Kawaguchi. 2003. Construction of an excisable bacterial artificial chromosome containing a full-length infectious clone of herpes simplex virus type 1: viruses reconstituted from the clone exhibit wild-type properties in vitro and in vivo. J. Virol. 77:1382-1391. (Pubitemid 36055560)
45. Wisner, T. W., C. C. Wright, A. Kato, Y. Kawaguchi, F. Mou, J. D. Baines, R. J. Roller, and D. C. Johnson. 2009. Herpesvirus gB-induced fusion between the virion envelope and outer nuclear membrane during virus egress is regulated by the viral US3 kinase. J. Virol. 83:3115-3126.
46. Yokoyama, A., M. Tanaka, G. Matsuda, K. Kato, M. Kanamori, H. Kawasaki, H. Hirano, I. Kitabayashi, M. Ohki, K. Hirai, and Y. Kawaguchi. 2001. Identification of major phosphorylation sites of Epstein-Barr virus nuclear antigen leader protein (EBNA-LP): ability of EBNA-LP to induce latent membrane protein 1 cooperatively with EBNA-2 is regulated by phosphorylation. J. Virol. 75:5119-5128. (Pubitemid 32448534)