UL31 and UL34 proteins of herpes simplex virus type 1 form a complex that accumulates at the nuclear rim and is required for envelopment of nucleocapsids

Journal of Virology

Volumn 75, Issue 18, 2001, Pages 8803-8817

  Reynolds, A E ^a   Ryckman, B J ^b   Baines, J D ^a   Zhou, Y ^b   Liang, L ^a   Roller, R J ^b  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTATHIONE TRANSFERASE; PROTEIN UL31; PROTEIN UL34; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ANIMAL CELL; ARTICLE; CELL NUCLEUS MEMBRANE; COMPLEX FORMATION; CONTROLLED STUDY; HERPES SIMPLEX VIRUS 1; HUMAN; HUMAN CELL; MONKEY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROGENY; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; VIRION; VIRUS ENVELOPE; VIRUS INFECTION; VIRUS NUCLEOCAPSID; VIRUS REPLICATION;

EID: 0034892972     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.75.18.8803-8817.2001     Document Type: Article

References (48)

1. Baines J. D., Roizman B. The UL10 gene of herpes simplex virus 1 encodes a novel viral glycoprotein, gM, which is present in the virion and in the plasma membrane of infected cells.J. Virol. 67 1993 1441 1452
2. Baines J. D., Koyama A. H., Huang T., Roizman B. The UL21 gene products of herpes simplex virus 1 are dispensable for growth in cultured cells.J. Virol. 68 1994 2929 2936
3. Bankier A. T., Beck S., Bohni R., Brown C. M., Cerny R., Chee M. S., Hutchison C. A. III, Kouzarides T., Martignetti J. A., Preddie E., Satchwell S. C., Tomlinson P., Weston K. M., Barrell B. G. The DNA sequence of the human cytomegalovirus genome.DNA Seq. 2 1991 1 12
4. Barth W., Chatterje S., Stochaj U. Targeting of the mammalian nucleoporin p62 to the nuclear envelope in the yeast Saccharomyces cerevisiae and HeLa cells.Biochem. Cell Biol. 77 1999 355 365
5. Berezney R., Mortillaro M. J., Ma H., Wei X., Samarabandu J. The nuclear matrix: a structural milieu for genomic function Nuclear matrix—structure and function 1st ed Berezney R., Jeon K. W. 1995 1 66 Academic Press San Diego, Calif
6. Bibor-Hardy V., Suh M., Pouchelet M., Simard R. Modifications of the nuclear envelope of BHK cells after infection with herpes simplex virus type 1.J. Gen. Virol. 63 1982 81 94
7. Blaho J., Mitchell C., Roizman B. An amino acid sequence shared by the herpes simplex virus 1 alpha regulatory proteins 0, 4, 22, and 27 predicts the nucleotidylylation of the UL21, UL31, UL47, and UL49 gene products.J. Biol. Chem. 269 1994 17401 17410
8. Chang Y. E., Roizman B. The product of the UL31 gene of herpes simplex virus 1 is a nuclear phosphoprotein, which partitions with the nuclear matrix.J. Virol. 67 1993 6348 6356
9. Chang Y. E., Van Sant C., Krug P. W., Sears A. E., Roizman B. The null mutant of the UL31 gene of herpes simplex virus 1: construction and phenotype in infected cells.J. Virol. 71 1997 8307 8315
10. Darlington R. W., Moss L. H. Herpesvirus envelopment.J. Virol. 2 1968 48 55
11. Davison A. J., Scott J. E. The complete DNA sequence of varicella-zoster virus.J. Gen. Virol. 67 1986 1759 1816
12. Dolan A., Jamieson F. E., Cunningham C., Barnett B. C., McGeoch D. J. The genome sequence of herpes simplex virus type 2.J. Virol. 72 1998 2010 2021
13. Ejercito P. M., Kieff E. D., Roizman B. Characterization of herpes simplex virus strains differing in their effects on social behavior of infected cells.J. Gen. Virol. 2 1968 357 364
14. Ellenberg J., Siggia E. D., Moreria J. E., Smith C. L., Presley J. F., Worman H. J., Lippincott-Schwartz J. Nuclear membrane dynamics and reassembly in living cells: targeting of an inner nuclear membrane protein in interphase and mitosis.J. Cell Biol. 138 1997 1193 1206
15. Farina A., Santarelli R., Gonnella R., Bei R., Muraro R., Cardinali G., Uccini S, Ragona G., Frati L., Faggioni A., Angeloni A. The BFRF1 gene of Epstein-Barr virus encodes a novel protein.J. Virol. 74 2000 3235 3244
16. Frame M. C., Purves F. C., McGeoch D. J., Marsden H. S., Leader D. P. Identification of the herpes simplex virus protein kinase as the product of the viral gene US3.J. Gen. Virol. 68 1987 2699 2704
17. Fricker M., Hollinshead M., White N., Vaux D. Interphase nuclei of many mammalian cell types contain deep, dynamic, tubular membrane-bound invaginations of the nuclear envelope.J. Cell Biol. 136 1997 531 544
18. Gant T. M., Wilson K. L. Nuclear assembly.Annu. Rev. Cell Dev. Biol. 13 1997 669 695
19. Gruenbaum Y., Wilson K. L., Harel A., Goldberg M., Cohen M. Review: nuclear lamins—structural proteins with fundamental functions.J. Struct. Biol. 129 2000 313 323
20. Haines H., Baerwald R. J. Nuclear membrane changes in herpes simplex virus-infected BHK-21 cells as seen by freeze-fracture.J. Virol. 17 1976 1038 1042
21. Hutchinson L., Johnson D. C. Herpes simplex virus glycoprotein K promotes egress of virus particles.J. Virol. 69 1995 5401 5413
22. Jerome K. R., Fox R., Chen Z., Sears A. E., Lee H. Y., Corey L. Herpes simplex virus inhibits apoptosis through the action of two genes, US5 and US3.J. Virol. 73 1999 8950 8957
23. Klupp B. G., Granzow H., Mettenleiter T. C. Primary envelopment of pseudorabies virus at the nuclear membrane requires the UL34 gene product.J. Virol. 74 2000 10063 10073
24. Knipe D. M., Senechek D., Rice S. A., Smith J. L. Stages in the nuclear association of the herpes simplex virus transcriptional activator protein ICP4.J. Virol. 61 1987 276 284
25. Leopardi R., Van Sant C., Roizman B. The herpes simplex virus 1 protein kinase US3 is required for protection from apoptosis induced by the virus.Proc. Natl. Acad. Sci. USA 94 1997 7891 7896
26. Long E. O., Rosen-Bronson S., Karp D. R., Malnati M., Sekaly R. P., Jaraquemada D. Efficient cDNA expression vectors for stable and transient expression of HLA-DR in transfected fibroblast and lymphoid cells.Hum. Immunol. 31 1991 229 235
27. Longnecker R., Roizman B. Clustering of genes dispensable for growth in culture in the S component of the HSV-1 genome.Science 236 1987 573 576
28. McGeoch D. J., Dalrymple M. A., Davison A. J., Dolan A., Frame M. C., McNab D., Perry L. J., Scott J. E., Taylor P. The complete DNA sequence of the long unique region in the genome of herpes simplex virus type 1.J. Gen. Virol. 69 1988 1531 1574
29. Nishiyama Y., Yamada Y., Kurachi R., Daikoku T. 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 1992 256 268
30. Ostlund C., Ellenberg J., Hallberg E., Lippincott-Schwatrz J., Worman H. J. Intracellular trafficking of emerin, the Emery-Dreifuss muscular dystrophy protein.J. Cell Sci. 112 1999 1709 1719
31. Parks G. D., Lamb R. A. Topology of eukaryotic type II membrane proteins: importance of N-terminal positively charged residues flanking the hydrophobic domain.Cell 64 1991 777 787
32. Post L. E., Mackem S., Roizman B. Regulation of alpha genes of herpes simplex virus: expression of chimeric genes produced by fusion of thymidine kinase with alpha gene promoters.Cell 25 1981 227 232
33. Purves F. C., Longnecker R. M., Leader D. P., Roizman B. Herpes simplex virus 1 protein kinase is encoded by open reading frame US3 that is not essential for virus growth in cell culture.J. Virol. 61 1987 2896 2901
34. Purves F. C., Spector D., Roizman B. The herpes simplex virus protein kinase encoded by the US3 gene mediates posttranslational modification of the phosphoprotein encoded by the UL34 gene.J. Virol. 65 1991 5757
35. Purves F. C., Spector D., Roizman B. UL34, the target of the herpes simplex virus US3 protein kinase, is a membrane protein that in its unphosphorylated state associates with novel phosphoproteins.J. Virol. 66 1992 4295 4303
36. Reynolds A. E., Fan Y., Baines J. D. Characterization of the UL33 gene product of herpes simplex virus 1.Virology 266 2000 310 318
37. Roller R. J., Zhou Y., Schnetzer R., Ferguson J., DeSalvo D. Herpes simplex virus type 1 UL34 gene product is required for viral envelopment.J. Virol. 74 2000 117 129
38. Sambrook J., Fritsch E. F., Maniatis T. Molecular cloning: a laboratory manual 2nd ed. 1989 Cold Spring Harbor Laboratory Cold Spring Harbor, N.Y
39. Shiba C., Daikoku T., Goshima F., Takakuwa H., Yamauchi Y., Koiwai O., Nishiyama Y. The UL34 gene product of herpes simplex virus type 2 is a tail-anchored type II membrane protein that is significant for virus envelopment.J. Gen. Virol. 81 2000 2397 2405
40. Smith S., Blobel G. The first membrane-spanning region of the lamin B receptor is sufficient for sorting to the inner nuclear membrane.J. Cell Biol. 120 1993 631 637
41. Soullam B., Worman H. J. The amino-terminal domain of the lamin B receptor is a nuclear envelope targeting signal.J. Cell Biol. 120 1993 1093 1100
42. Soullam B., Worman H. J. Signals and structural features involved in integral membrane protein targeting to the inner nuclear membrane.J. Cell Biol. 130 1995 15 27
43. Staufenbiel M., Deppert W. Preparation of nuclear matrices from cultured cells: subfractionation of nuclei in situ.J. Cell Biol. 98 1984 1886 1894
44. Taus N. S., Salmon B., Baines J. D. The herpes simplex virus 1 UL17 gene is required for localization of capsids and major and minor capsid proteins to intranuclear sites where viral DNA is cleaved and packaged.Virology 252 1998 115 125
45. Telford E. A., Watson M. S., McBride K., Davison A. J. The DNA sequence of equine herpesvirus-1.Virology 189 1992 304 316
46. Ye G. J., Vaughan K. T., Vallee R. B., Roizman B. The herpes simplex virus 1 UL34 protein interacts with a cytoplasmic dynein intermediate chain and targets nuclear membrane.J. Virol. 74 2000 1355 1363
47. Ye G. J., Roizman B. 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. USA 97 2000 11002 11007
48. Zhu H. Y., Yamada H., Jiang Y. M., Yamada M., Nishiyama Y. Intracellular localization of the UL31 protein of herpes simplex virus type 2.Arch. Virol. 144 1999 1923 1935