Nucleolin is required for efficient nuclear egress of herpes simplex virus type 1 nucleocapsids

Journal of Virology

Volumn 84, Issue 4, 2010, Pages 2110-2121

  Sagou, Ken ^a,b   Uema, Masashi ^a   Kawaguchi, Yasushi ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b NIPPON INSTITUTE FOR BIOLOGICAL SCIENCE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

FLUORESCENT DYE; NUCLEASE; NUCLEOLIN; VIRUS DNA;

ANIMAL CELL; ARTICLE; CELL FRACTIONATION; CELL NUCLEUS MEMBRANE; COMPLEX FORMATION; CONTROLLED STUDY; CYTOPLASM; GENETIC CODE; HERPES SIMPLEX VIRUS 1; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; NONHUMAN; NUCLEOLUS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; VIROGENESIS; VIRUS ASSEMBLY; VIRUS NUCLEOCAPSID; VIRUS RECOMBINANT;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; BASE SEQUENCE; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; DEOXYRIBONUCLEASES; DNA PRIMERS; HERPESVIRUS 1, HUMAN; MICROSCOPY, ELECTRON, TRANSMISSION; MULTIPROTEIN COMPLEXES; NUCLEOCAPSID; PHOSPHOPROTEINS; RABBITS; RECOMBINANT FUSION PROTEINS; RNA, SMALL INTERFERING; RNA-BINDING PROTEINS; VERO CELLS; VIRAL PROTEINS; VIRUS ASSEMBLY;

HERPESVIRIDAE; HUMAN HERPESVIRUS 1; MIRIDAE;

EID: 75449116596     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02007-09     Document Type: Article

References (73)

1. Bjerke, S. L., and R. J. Roller. 2006. Roles for herpes simplex virus type 1 UL34 and US3 proteins in disrupting the nuclear lamina during herpes simplex virus type 1 egress. Virology 347:261-276.
2. Calle, A., I. Ugrinova, A. L. Epstein, P. Bouvet, J. J. Diaz, and A. Greco. 2008. Nucleolin is required for an efficient herpes simplex virus type 1 infection. J. Virol. 82:4762-4773.
3. Campadelli-Fiume, G., and B. Roizman. 2006. The egress of herpesviruses from cells: the unanswered questions. J. Virol. 80:6716-6719.
4. De, A., S. L. Donahue, A. Tabah, N. E. Castro, N. Mraz, J. L. Cruise, and C. Campbell. 2006. A novel interaction of nucleolin with Rad51. Biochem. Biophys. Res. Commun. 344:206-213.
5. Elliott, G., and P. O'Hare. 1999. Live-cell analysis of a green fluorescent protein-tagged herpes simplex virus infection. J. Virol. 73:4110-4119.
6. Farnsworth, A., T. W. Wisner, M. Webb, R. Roller, G. Cohen, R. Eisenberg, and D. C. Johnson. 2007. Herpes simplex virus glycoproteins gB and gH function in fusion between the virion envelope and the outer nuclear membrane. Proc. Natl. Acad. Sci. U. S. A. 104:10187-10192.
7. Forest, T., S. Barnard, and J. D. Baines. 2005. Active intranuclear movement of herpesvirus capsids. Nat. Cell Biol. 7:429-431.
8. Francke, B., H. Moss, M. C. Timbury, and J. Hay. 1978. Alkaline DNase activity in cells infected with a temperature-sensitive mutant of herpes simplex virus type 2. J. Virol. 26:209-213.
9. Ginisty, H., H. Sicard, B. Roger, and P. Bouvet. 1999. Structure and functions of nucleolin. J. Cell Sci. 112(Pt. 6):761-772.
10. Goldstein, J. N., and S. K. Weller. 1998. In vitro processing of herpes simplex virus type 1 DNA replication intermediates by the viral alkaline nuclease, UL12. J. Virol. 72:8772-8781.
11. Goldstein, J. N., and S. K. Weller. 1998. The exonuclease activity of HSV-1 UL12 is required for in vivo function. Virology 244:442-457.
12. Haraguchi, T., T. Mizutani, N. Yamamichi, T. Ito, S. Minoguchi, and H. Iba. 2007. siRNAs do not induce RNA-dependent transcriptional silencing of retrovirus in human cells. FEBS Lett. 581:4949-4954.
13. Harley, C. A., A. Dasgupta, and D. W. Wilson. 2001. Characterization of herpes simplex virus-containing organelles by subcellular fractionation: role for organelle acidification in assembly of infectious particles. J. Virol. 75:1236-1251.
14. Hofemeister, H., and P. O'Hare. 2008. Nuclear pore composition and gating in herpes simplex virus-infected cells. J. Virol. 82:8392-8399.
15. Hoffmann, P. J. 1981. Mechanism of degradation of duplex DNA by the DNase induced by herpes simplex virus. J. Virol. 38:1005-1014.
16. Hoffmann, P. J., and Y. C. Cheng. 1978. The deoxyribonuclease induced after infection of KB cells by herpes simplex virus type 1 or type 2. I. Purification and characterization of the enzyme. J. Biol. Chem. 253:3557-3562.
17. 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.
18. 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.
19. 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.
20. 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 1delta. J. Virol. 77:2359-2368.
21. 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.
22. Khurts, S., K. Masutomi, L. Delgermaa, K. Arai, N. Oishi, H. Mizuno, N. Hayashi, W. C. Hahn, and S. Murakami. 2004. Nucleolin interacts with telomerase. J. Biol. Chem. 279:51508-51515.
23. 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.
24. Lentine, A. F., and S. L. Bachenheimer. 1990. Intracellular organization of herpes simplex virus type 1 DNA assayed by staphylococcal nuclease sensitivity. Virus Res. 16:275-292.
25. Leuzinger, H., U. Ziegler, E. M. Schraner, C. Fraefel, D. L. Glauser, I. Heid, M. Ackermann, M. Mueller, and P. Wild. 2005. Herpes simplex virus 1 envelopment follows two diverse pathways. J. Virol. 79:13047-13059.
26. Lopez, M. R., E. F. Schlegel, S. Wintersteller, and J. A. Blaho. 2008. The major tegument structural protein VP22 targets areas of dispersed nucleolin and marginalized chromatin during productive herpes simplex virus 1 infection. Virus Res. 136:175-188.
27. Luxton, G. W., S. Haverlock, K. E. Coller, S. E. Antinone, A. Pincetic, and G. A. Smith. 2005. Targeting of herpesvirus capsid transport in axons is coupled to association with specific sets of tegument proteins. Proc. Natl. Acad. Sci. U. S. A. 102:5832-5837.
28. Lymberopoulos, M. H., and A. Pearson. 2007. Involvement of UL24 in herpes-simplex-virus-1-induced dispersal of nucleolin. Virology 363:397-409.
29. Martinez, R., R. T. Sarisky, P. C. Weber, and S. K. Weller. 1996. Herpes simplex virus type 1 alkaline nuclease is required for efficient processing of viral DNA replication intermediates. J. Virol. 70:2075-2085.
30. Mettenleiter, T. C. 2002. Herpesvirus assembly and egress. J. Virol. 76:1537-1547.
31. Mettenleiter, T. C. 2006. Intriguing interplay between viral proteins during herpesvirus assembly or: the herpesvirus assembly puzzle. Vet. Microbiol. 113:163-169.
32. Mettenleiter, T. C., B. G. Klupp, and H. Granzow. 2006. Herpesvirus assembly: a tale of two membranes. Curr. Opin. Microbiol. 9:423-429.
33. Mettenleiter, T. C., and T. Minson. 2006. Egress of alphaherpesviruses. J. Virol. 80:1610-1612.
34. Mongelard, F., and P. Bouvet. 2007. Nucleolin: a multiFACeTed protein. Trends Cell Biol. 17:80-86.
35. Morimoto, T., J. Arii, M. Tanaka, T. Sata, H. Akashi, M. Yamada, Y. Nishiyama, M. Uema, and Y. Kawaguchi. 2009. Differences in the regulatory and functional effects of the Us3 protein kinase activities of herpes simplex virus 1 and 2. J. Virol. 83:11624-11634.
36. 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.
37. 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.
38. 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.
39. Park, R., and J. D. Baines. 2006. 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. 80:494-504.
40. Purves, F. C., D. Spector, and B. Roizman. 1991. The herpes simplex virus 1 protein kinase encoded by the US3 gene mediates posttranslational modifi-cation of the phosphoprotein encoded by the UL34 gene. J. Virol. 65:5757-5764.
41. Randall, R. E., and N. Dinwoodie. 1986. Intranuclear localization of herpes simplex virus immediate-early and delayed-early proteins: evidence that ICP 4 is associated with progeny virus DNA. J. Gen. Virol. 67(Pt. 10):2163-2177.
42. Reuven, N. B., A. E. Staire, R. S. Myers, and S. K. Weller. 2003. The herpes simplex virus type 1 alkaline nuclease and single-stranded DNA binding protein mediate strand exchange in vitro. J. Virol. 77:7425-7433.
43. Reuven, N. B., and S. K. Weller. 2005. Herpes simplex virus type 1 singlestrand DNA binding protein ICP8 enhances the nuclease activity of the UL12 alkaline nuclease by increasing its processivity. J. Virol. 79:9356-9358.
44. Reuven, N. B., S. Willcox, J. D. Griffith, and S. K. Weller. 2004. Catalysis of strand exchange by the HSV-1 UL12 and ICP8 proteins: potent ICP8 recombinase activity is revealed upon resection of dsDNA substrate by nuclease. J. Mol. Biol. 342:57-71.
45. Reynolds, A. E., L. Liang, and J. D. Baines. 2004. Conformational changes in the nuclear lamina induced by herpes simplex virus type 1 require genes U(L)31 and U(L)34. J. Virol. 78:5564-5575.
46. 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.
47. 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.
48. Roizman, B., D. M. Knipe, and R. J. Whitley. 2007. Herpes simplex viruses. In D. M. Knipe, P. M. Howley, D. E. Griffin, R. A. Lamb, M. A. Martin, B. Roizman, and S. E. Straus (ed.), Fields virology, 5th ed. Lippincott-Raven Publishers, Philadelphia, PA.
49. Roizman, B., D. M. Knipe, and R. J. Whitley. 2007. The family Herpesviridae: a brief introduction, 5th ed. Lippincott/The Williams & Wilkins Co., Philadelphia, PA.
50. Roller, R. J., Y. Zhou, R. Schnetzer, J. Ferguson, and D. DeSalvo. 2000. Herpes simplex virus type 1 U(L)34 gene product is required for viral envelopment. J. Virol. 74:117-129.
51. 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.
52. Sagou, K., T. Imai, H. Sagara, M. Uema, and Y. Kawaguchi. 2009. Regula-tion of the catalytic activity of herpes simplex virus 1 protein kinase Us3 by autophosphorylation and its role in pathogenesis. J. Virol. 83:5773-5783.
53. Scott, E. S., and P. O'Hare. 2001. Fate of the inner nuclear membrane protein lamin B receptor and nuclear lamins in herpes simplex virus type 1 infection. J. Virol. 75:8818-8830.
54. Seinsoth, S., H. Uhlmann-Schiffler, and H. Stahl. 2003. Bidirectional DNA unwinding by a ternary complex of T antigen, nucleolin and topoisomerase I. EMBO Rep. 4:263-268.
55. Shao, L., L. M. Rapp, and S. K. Weller. 1993. Herpes simplex virus 1 alkaline nuclease is required for efficient egress of capsids from the nucleus. Virology 196:146-162.
56. Shimakami, T., M. Honda, T. Kusakawa, T. Murata, K. Shimotohno, S. Kaneko, and S. Murakami. 2006. Effect of hepatitis C virus (HCV) NS5Bnucleolin interaction on HCV replication with HCV subgenomic replicon. J. Virol. 80:3332-3340.
57. Simpson-Holley, M., J. Baines, R. Roller, and D. M. Knipe. 2004. 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. 78:5591-5600.
58. Simpson-Holley, M., R. C. Colgrove, G. Nalepa, J. W. Harper, and D. M. Knipe. 2005. Identification and functional evaluation of cellular and viral factors involved in the alteration of nuclear architecture during herpes simplex virus 1 infection. J. Virol. 79:12840-12851.
59. Skepper, J. N., A. Whiteley, H. Browne, and A. Minson. 2001. Herpes simplex virus nucleocapsids mature to progeny virions by an envelopment 3 deenvelopment 3 reenvelopment pathway. J. Virol. 75:5697-5702.
60. Smith, G. A., S. P. Gross, and L. W. Enquist. 2001. Herpesviruses use bidirectional fast-axonal transport to spread in sensory neurons. Proc. Natl. Acad. Sci. U. S. A. 98:3466-3470.
61. Srivastava, M., and H. B. Pollard. 1999. Molecular dissection of nucleolin's role in growth and cell proliferation: new insights. FASEB J. 13:1911-1922.
62. Strobel-Fidler, M., and B. Francke. 1980. Alkaline deoxyribonuclease induced by herpes simplex virus type 1: composition and properties of the purified enzyme. Virology 103:493-501.
63. Subramanian, R. P., and R. J. Geraghty. 2007. Herpes simplex virus type 1 mediates fusion through a hemifusion intermediate by sequential activity of glycoproteins D, H, L, and B. Proc. Natl. Acad. Sci. U. S. A. 104:2903-2908.
64. 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.
65. 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.
66. Thomas, M. S., M. Gao, D. M. Knipe, and K. L. Powell. 1992. Association between the herpes simplex virus major DNA-binding protein and alkaline nuclease. J. Virol. 66:1152-1161.
67. Turcotte, S., J. Letellier, and R. Lippe. 2005. Herpes simplex virus type 1 capsids transit by the trans-Golgi network, where viral glycoproteins accumulate independently of capsid egress. J. Virol. 79:8847-8860.
68. Vlazny, D. A., A. Kwong, and N. Frenkel. 1982. Site-specific cleavage/packaging of herpes simplex virus DNA and the selective maturation of nucleocapsids containing full-length viral DNA. Proc. Natl. Acad. Sci. U. S. A. 79:1423-1427.
69. Weller, S. K., M. R. Seghatoleslami, L. Shao, D. Rowse, and E. P. Carmichael. 1990. The herpes simplex virus type 1 alkaline nuclease is not essential for viral DNA synthesis: isolation and characterization of a lacZ insertion mutant. J. Gen. Virol. 71(Pt. 12):2941-2952.
70. Wild, P., M. Engels, C. Senn, K. Tobler, U. Ziegler, E. M. Schraner, E. Loepfe, M. Ackermann, M. Mueller, and P. Walther. 2005. Impairment of nuclear pores in bovine herpesvirus 1-infected MDBK cells. J. Virol. 79:1071-1083.
71. 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.
72. Yamamichi, N., M. Yamamichi-Nishina, T. Mizutani, H. Watanabe, S. Minoguchi, N. Kobayashi, S. Kimura, T. Ito, N. Yahagi, M. Ichinose, M. Omata, and H. Iba. 2005. The Brm gene suppressed at the posttranscriptional level in various human cell lines is inducible by transient HDAC inhibitor treatment, which exhibits antioncogenic potential. Oncogene 24:5471-5481.
73. Ye, G. J., and B. Roizman. 2000. The essential protein encoded by the UL31 gene of herpes simplex virus 1 depends for its stability on the presence of UL34 protein. Proc. Natl. Acad. Sci. U. S. A. 97:11002-11007.