Herpes simplex virus 2 UL13 protein kinase disrupts nuclear lamins

Virology

Volumn 392, Issue 1, 2009, Pages 137-147

  Cano Monreal, Gina L ^a   Wylie, Kristine M ^a   Cao, Feng ^a   Tavis, John E ^a   Morrison, Lynda A ^a  

^a SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Egress; Herpes simplex virus; HSV 2; Lamin; Nuclear; Phosphorylation; UL13

Indexed keywords

HERPES SIMPLEX VIRUS 2 PROTEIN KINASE UL13; LAMIN; LAMIN A; LAMIN A1; LAMIN B; LAMIN B1; LAMIN C; PROTEIN KINASE; UNCLASSIFIED DRUG; VIRUS ENZYME;

ARTICLE; CELL STRUCTURE; CELLULAR DISTRIBUTION; HERPES SIMPLEX; HUMAN; HUMAN CELL; IN VITRO STUDY; NONHUMAN; NUCLEAR LAMINA; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION;

ACTIVE TRANSPORT, CELL NUCLEUS; BASE SEQUENCE; BINDING SITES; DNA PRIMERS; DNA, VIRAL; HELA CELLS; HERPESVIRUS 2, HUMAN; HUMANS; LAMIN TYPE A; LAMIN TYPE B; LAMINS; NUCLEAR LAMINA; PHOSPHORYLATION; PROTEIN CONFORMATION; PROTEIN KINASES; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; TRANSFECTION;

HUMAN HERPESVIRUS 1; HUMAN HERPESVIRUS 2; SIMPLEXVIRUS;

EID: 69249222501     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2009.06.051     Document Type: Article

References (35)

1. Advani S.J., Brandimarti R., Weichselbaum R.R., and Roizman B. The disappearance of cyclins A and B and the increase in activity of the G(2)/M-phase cellular kinase cdc2 in herpes simplex virus 1-infected cells require expression of the alpha22/U(S)1.5 and U(L)13 viral genes. J. Virol. 74 (2000) 8-15
2. Cano-Monreal G.L., Tavis J.E., and Morrison L.A. Substrate specificity of the herpes simplex virus type 2 UL13 protein kinase. Virology 374 (2008) 1-10
3. Fields A.P., and Thompson L.J. The regulation of mitotic nuclear envelope breakdown: a role for multiple lamin kinases. Prog. Cell Cycle Res. 1 (1995) 271-286
4. Geiss B.J., Cano G.L., Tavis J.E., and Morrison L.A. Herpes simplex virus 2 VP22 phosphorylation induced by cellular and viral kinases does not influence intracellular localization. Virology 330 (2004) 74-81
5. Gerace L., and Blobel G. The nuclear envelope lamina is reversibly depolymerized during mitosis. Cell 19 (1980) 277-287
6. Gruenbaum Y., Margalit A., Goldman R.D., Shumaker D.K., and Wilson K.L. The nuclear lamina comes of age. Nat. Rev., Mol. Cell Biol. 6 (2005) 21-31
7. Haas M., and Jost E. Functional analysis of phosphorylation sites in human lamin A controlling lamin disassembly, nuclear transport and assembly. Eur. J. Cell Biol. 62 (1993) 237-247
8. Hamirally S., Kamil J.P., Ndassa-Colday Y.M., Lin A.J., Jahng W.J., Baek M.C., Noton S., Silva L.A., Simpson-Holley M., Knipe D.M., Golan D.E., Marto J.A., and Coen D.M. Viral mimicry of Cdc2/cyclin-dependent kinase 1 mediates disruption of nuclear lamina during human cytomegalovirus nuclear egress. PLoS Pathog. 5 (2009) e1000275
9. Heald R., and McKeon F. Mutations of phosphorylation sites in lamin A that prevent nuclear lamina disassembly in mitosis. Cell 61 (1990) 579-589
10. Kato A., Yamamoto M., Ohno T., Tanaka M., Sata T., Nishiyama Y., and Kawaguchi Y. 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 (2006) 1476-1486
11. Kawaguchi Y., and Kato K. Protein kinases conserved in herpesviruses potentially share a function mimicking the cellular protein kinase cdc2. Rev. Med. Virol. 13 (2003) 331-340
12. Korom M., Wylie K.M., and Morrison L.A. Selective ablation of virion host shutoff protein RNase activity attenuates herpes simplex virus 2 in mice. J. Virol. 82 (2008) 3642-3653
13. Lee C.P., Huang Y.H., Lin S.F., Chang Y., Chang Y.H., Takada K., and Chen M.R. Epstein-Barr virus BGLF4 kinase induces disassembly of the nuclear lamina to facilitate virion production. J. Virol. 82 (2008) 11913-11926
14. Likhacheva E.V., and Bogachev S.S. Lamins and their functions in cell cycle. Membr.Cell Biol. 14 (2001) 565-577
15. Lin F., and Worman H.J. Structural organization of the human gene encoding nuclear lamin A and nuclear lamin C. J. Biol. Chem. 268 (1993) 16321-16326
16. Marschall M., Marzi A., aus dem S.P., Jochmann R., Kalmer M., Auerochs S., Lischka P., Leis M., and Stamminger T. Cellular p32 recruits cytomegalovirus kinase pUL97 to redistribute the nuclear lamina. J. Biol. Chem. 280 (2005) 33357-33367
17. Mettenleiter T.C. Herpesvirus assembly and egress. J. Virol. 76 (2002) 1537-1547
18. Milbradt J., Auerochs S., and Marschall M. Cytomegaloviral proteins pUL50 and pUL53 are associated with the nuclear lamina and interact with cellular protein kinase C. J. Gen. Virol. 88 (2007) 2642-2650
19. Morrison E.E., Wang Y.F., and Meredith D.M. Phosphorylation of structural components promotes dissociation of the herpes simplex virus type 1 tegument. J. Virol. 72 (1998) 7108-7114
20. Mou F., Forest T., and Baines J.D. 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 (2007) 6459-6470
21. Mou F., Wills E.G., Park R., and Baines J.D. Effects of lamin A/C, lamin B1, and viral US3 kinase activity on viral infectivity, virion egress, and the targeting of herpes simplex virus U(L)34-encoded protein to the inner nuclear membrane. J. Virol. 82 (2008) 8094-8104
22. Mou F., Wills E., and Baines J.D. 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 (2009) 5181-5191
23. Muranyi W., Haas J., Wagner M., Krohne G., and Koszinowski U.H. Cytomegalovirus recruitment of cellular kinases to dissolve the nuclear lamina. Science 297 (2002) 854-857
24. Overton H.A., McMillan D.J., Klavinskis L.S., Hope L., Ritchie A.J., and Wong-kai-in P. Herpes simplex virus type 1 gene UL13 encodes a phosphoprotein that is a component of the virion. Virology 190 (1992) 184-192
25. Park R., and Baines J.D. Herpes simplex virus type 1 infection induces activation and recruitment of protein kinase C to the nuclear membrane and increased phosphorylation of lamin B. J. Virol. 80 (2006) 494-504
26. Peter M., Sanghera J.S., Pelech S.L., and Nigg E.A. Mitogen-activated protein kinases phosphorylate nuclear lamins and display sequence specificity overlapping that of mitotic protein kinase p34cdc2. Eur. J. Biochem. 205 (1992) 287-294
27. Purves F.C., Longnecker R.M., Leader D.P., and Roizman B. 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 (1987) 2896-2901
28. Purves F.C., and Roizman B. The UL13 gene of herpes simplex virus 1 encodes the functions for posttranslational processing associated with phosphorylation of the regulatory protein alpha 22. Proc. Natl. Acad. Sci. U.S.A 89 (1992) 7310-7314
29. Purves F.C., Ogle W.O., and Roizman B. Processing of the herpes simplex virus regulatory protein alpha 22 mediated by the UL13 protein kinase determines the accumulation of a subset of alpha and gamma mRNAs and proteins in infected cells. Proc. Natl. Acad. Sci. U.S.A 90 (1993) 6701-6705
30. Reynolds A.E., Ryckman B.J., Baines J.D., Zhou Y., Liang L., and Roller R.J. 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 (2001) 8803-8817
31. Reynolds A.E., Liang L., and Baines J.D. Conformational changes in the nuclear lamina induced by herpes simplex virus type 1 require genes U(L)31 and U(L)34. J. Virol. 78 (2004) 5564-5575
32. Scott E.S., and O'Hare P. Fate of the inner nuclear membrane protein lamin B receptor and nuclear lamins in herpes simplex virus type 1 infection. J. Virol. 75 (2001) 8818-8830
33. Simpson-Holley M., Baines J., Roller R., and Knipe D.M. Herpes simplex virus 1 U(L)31 and U(L)34 gene products promote the late maturation of viral replication compartments to the nuclear periphery. J. Virol. 78 (2004) 5591-5600
34. Smith R.F., and Smith T.F. Identification of new protein kinase-related genes in three herpesviruses, herpes simplex virus, varicella-zoster virus, and Epstein-Barr virus. J. Virol. 63 (1989) 450-455
35. Tanaka M., Nishiyama Y., Sata T., and Kawaguchi Y. The role of protein kinase activity expressed by the UL13 gene of herpes simplex virus 1: the activity is not essential for optimal expression of UL41 and ICP0. Virology 341 (2005) 301-312