The UL31 and UL34 gene products of herpes simplex virus 1 are required for optimal localization of viral glycoproteins D and M to the inner nuclear membranes of infected cells

Journal of Virology

Volumn 83, Issue 10, 2009, Pages 4800-4809

  Wills, Elizabeth ^a   Mou, Fan ^a   Baines, Joel D ^a  

^a Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENE PRODUCT; GLUTATHIONE TRANSFERASE; GLYCOPROTEIN D; GLYCOPROTEIN M; UNCLASSIFIED DRUG; VIRUS GLYCOPROTEIN; GLYCOPROTEIN D, HUMAN HERPESVIRUS 1; NUCLEAR PROTEIN; UL31 PROTEIN, HUMAN HERPESVIRUS 1; UL34 PROTEIN, HUMAN HERPESVIRUS 1; VIRUS ENVELOPE PROTEIN; VIRUS PROTEIN;

ANALYSIS OF VARIANCE; ARTICLE; CELL NUCLEUS MEMBRANE; CYTOSOL; ELECTRON; ENDOPLASMIC RETICULUM; FLOW CYTOMETRY; HERPES SIMPLEX VIRUS 1; HUMAN; HUMAN CELL; IMMUNOGOLD ELECTRON MICROSCOPY; IMMUNOREACTIVITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; RETICULOCYTE LYSATE; VIRUS NUCLEOCAPSID; ANIMAL; CELL LINE; ELECTRON MICROSCOPY; METABOLISM; PHYSIOLOGY; RABBIT; VIROLOGY; VIRUS REPLICATION;

HUMAN HERPESVIRUS 1; ORYCTOLAGUS CUNICULUS;

ANIMALS; CELL LINE; HERPESVIRUS 1, HUMAN; HUMANS; MICROSCOPY, ELECTRON; NUCLEAR ENVELOPE; NUCLEAR PROTEINS; RABBITS; VIRAL ENVELOPE PROTEINS; VIRAL PROTEINS; VIRUS REPLICATION;

EID: 65349186030     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02431-08     Document Type: Article

References (56)

1. Atanasiu, D., J. C. Whitbeck, T. M. Cairns, B. Reilly, G. H. Cohen, and R. J. Eisenberg. 2007. Bimolecular complementation reveals that glycoproteins gB and gH/gL of herpes simplex virus interact with each other during cell fusion. Proc. Natl. Acad. Sci. USA 104:18718-18723.
2. Avitabile, E., C. Forghieri, and G. Campadelli-Fiume. 2007. Complexes between herpes simplex virus glycoproteins gD, gB, and gH detected in cells by complementation of split enhanced green fluorescent protein. J. Virol. 81:11532-11537.
3. Avitabile, E., G. Lombardi, and G. Campadelli-Fiume. 2003. Herpes simplex virus glycoprotein K, but not its syncytial allele, inhibits cell-cell fusion mediated by the four fusogenic glycoproteins, gD, gB, gH, and gL. J. Virol. 77:6836-6844.
4. L11 proteins are associated with cytoplasmic and nuclear membranes and with nuclear bodies of infected cells. J. Virol. 69:825-833.
5. Baines, J. D., E. G. Wills, J. Pennington, R. J. Jacob, and B. Roizman. 2007. Glycoprotein M of herpes simplex virus type 1 is incorporated into virions during budding at the inner nuclear membrane. J. Virol. 81:800-812. (Pubitemid 46067906)
6. Baines, J. D., C. E. Hsieh, E. Wills, C. Mannella, and M. Marko. 2007. Electron tomography of nascent herpes simplex virions. J. Virol. 81:2726-2735. (Pubitemid 46447037)
7. Bhattacharya, J., A. Repik, and P. R. Clapham. 2006. Gag regulates association of human immunodeficiency virus type 1 envelope with detergent-resistant membranes. J. Virol. 80:5292-5300. (Pubitemid 43752774)
8. Browne, H., B. Bruun, and T. Minson. 2001. Plasma membrane requirements for cell fusion induced by herpes simplex virus type 1 glycoproteins gB, gD, gH and gL. J. Gen. Virol. 82:1419-1422.
9. Cai, W., B. Gu, and S. Person. 1988. Role of glycoprotein B of herpes simplex virus type 1 in viral entry and cell fusion. J. Virol. 62:2596-2604. (Pubitemid 18193850)
10. L31 gene of herpes simplex virus 1: construction and phenotype of infected cells. J. Virol. 71:8307-8315.
11. Crump, C. M., B. Bruun, S. Bell, L. E. Pomeranz, T. Minson, and H. M. Browne. 2004. Alphaherpesvirus glycoprotein M causes the relocalization of plasma membrane proteins. J. Gen. Virol. 85:3517-3527. (Pubitemid 39591859)
12. Davis-Poynter, N., S. Bell, T. Minson, and H. Browne. 1994. Analysis of the contributions of herpes simplex virus type 1 membrane proteins to the induction of cell-cell fusion. J. Virol. 68:7586-7590. (Pubitemid 24328820)
13. 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.
14. Farina, A., R. Feederle, S. Raffa, R. Gonnella, R. Santarelli, L. Frati, A. Angeloni, M. R. Torrisi, A. Faggioni, and H. J. Delecluse. 2005. BFRF1 of Epstein-Barr virus is essential for efficient primary viral envelopment and egress. J. Virol. 79:3703-3712. (Pubitemid 40327958)
15. 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. USA 104:10187-10192.
16. Forrester, A., H. Farrell, G. Wilkinson, J. Kaye, N. Davis-Poynter, and T. Minson. 1992. Construction and properties of a mutant of herpes simplex virus type 1 with glycoprotein H coding sequences deleted. J. Virol. 66:341-348.
17. Frangioni, J. V., and B. G. Neel. 1993. Solubilization and purification of enzymatically active glutathione-S-transferase (pGEX) fusion proteins. Anal. Biochem. 210:179-187.
18. L34 gene products of pseudorabies virus are involved in egress from the host-cell nucleus and represent components of primary enveloped but not mature virions. J. Virol. 76:364-378.
19. Gilbert, R., K. Ghosh, L. Rasile, and H. P. Ghosh. 1994. Membrane anchoring domain of herpes simplex virus glycoprotein gB is sufficient for nuclear envelope localization. J. Virol. 68:2272-2285. (Pubitemid 24091905)
20. Granato, M., R. Feederle, A. Farina, R. Gonnella, R. Santarelli, B. Hub, A. Faggioni, and H. J. Delecluse. 2008. Deletion of Epstein-Barr virus BFLF2 leads to impaired viral DNA packaging and primary egress as well as to the production of defective viral particles. J. Virol. 82:4042-4051.
21. Granzow, H., B. G. Klupp, W. Fuchs, J. Veits, N. Osterrieder, and T. C. Mettenleiter. 2001. Egress of alphaherpesviruses: comparative ultrastructural study. J. Virol. 75:3675-3684.
22. Hayes, T. L., F. T. Lindgren, and J. W. Gofman. 1963. A quantitative determination of the osmium tetroxide-lipoprotein interaction. J. Cell Biol. 19:251-255.
23. Heine, J. W., P. G. Spear, and B. Roizman. 1972. Proteins specified by herpes simplex virus. VI. Viral proteins in the plasma membrane. J. Virol. 9:431-439.
24. Heldwein, E. E., H. Lou, F. C. Bender, G. H. Cohen, R. J. Eisenberg, and S. C. Harrison. 2006. Crystal structure of glycoprotein B from herpes simplex virus 1. Science 313:217-220.
25. Jensen, H. L., and B. Norrild. 1998. Herpes simplex virus type 1-infected human embryonic lung cells studied by optimized immunogold cryosection electron microscopy. J. Histochem. Cytochem. 46:487-496. (Pubitemid 28158468)
26. Klupp, B., J. Altenschmidt, H. Granzow, W. Fuchs, and T. C. Mettenleiter. 2008. Glycoproteins required for entry are not necessary for egress of pseudorabies virus. J. Virol. 82:6299-6309.
27. 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.
28. 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. (Pubitemid 32936770)
29. Leung, K., J. O. Kim, L. Ganesh, J. Kabat, O. Schwartz, and G. J. Nabel. 2008. HIV-1 assembly: viral glycoproteins segregate quantally to lipid rafts that associate individually with HIV-1 capsids and virions. Cell Host Microbe 3:285-292.
30. Liang, L., M. Tanaka, Y. Kawaguchi, and J. D. Baines. 2004. Cell lines that support replication of a novel herpes simplex 1 UL31 deletion mutant can properly target UL34 protein to the nuclear rim in the absence of UL31. Virology 329:68-76.
31. Ligas, M. W., and D. C. Johnson. 1988. A herpes simplex virus mutant in which glycoprotein D sequences are replaced by β-galactosidase sequences binds to but is unable to penetrate into cells. J. Virol. 62:1486-1494. (Pubitemid 18133165)
32. Lötzerich, M., Z. Ruzsics, and U. H. Koszinowski. 2006. Functional domains of murine cytomegalovirus nuclear egress protein M53/p38. J. Virol. 80:73-84.
33. 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. 69:1531-1574. (Pubitemid 18171672)
34. Mettenleiter, T. C., B. G. Klupp, and H. Granzow. 2006. Herpesvirus assembly: a tale of two membranes. Curr. Opin. Microbiol. 9:423-429.
35. Montgomery, R. I., M. S. Warner, B. J. Lum, and P. G. Spear. 1996. Herpes simplex virus-1 entry into cells mediated by a novel member of the TNF/NGF receptor family. Cell 87:427-436.
36. 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)
37. Naldinho-Souto, R., H. Browne, and T. Minson. 2006. Herpes simplex virus tegument protein VP16 is a component of primary enveloped virions. J. Virol. 80:2582-2584. (Pubitemid 43271564)
38. Nayak, D. P., E. K.-W. Hui, and S. Barman. 2004. Assembly and budding of influenza virus. Virus Res. 106:147-165. (Pubitemid 39572961)
39. L34 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.
40. S3 proteins suggests specific roles in primary envelopment and egress of nucleocapsids. J. Virol. 76:8939-8952.
41. Roizman, B., and D. Furlong. 1974. The replication of herpesviruses, p. 229-403. In H. Fraenkel-Conrat and R. R. Wagner (ed.), Comprehensive virology. Plenum Press, New York, NY.
42. L34 gene product is required for viral envelopment. J. Virol. 74:117-129.
43. Roop, C., L. Hutchinson, and D. C. Johnson. 1993. A mutant herpes simplex virus type 1 unable to express glycoprotein L cannot enter cells, and its particles lack glycoprotein H. J. Virol. 67:2285-2297.
44. 2) in virion infectivity. J. Virol. 29:1149-1158.
45. L31 protein family members revealed by protein complementation assay. J. Virol. 80:11658-11666.
46. L34 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. 81:2397-2405.
47. Skepper, J. N., A. Whiteley, H. Browne, and A. Minson. 2001. Herpes simplex virus nucleocapsids mature to progeny virions by an envelopment → deenvelopment → reenvelopment pathway. J. Virol. 75:5697-5702.
48. Spear, P. G. 2004. Herpes simplex virus: receptors and ligands for cell entry. Cell. Microbiol. 6:401-410.
49. Stackpole, C. W. 1969. Herpes-type virus of the frog renal adenocarcinoma. I. Virus development in tumor transplants maintained at low temperature. J. Virol. 4:75-93.
50. Stannard, L. M., S. Himmelhoch, and S. Wynchank. 1996. Intra-nuclear localization of two envelope proteins, gB and gD, of herpes simplex virus. Arch. Virol. 141:505-524.
51. Steven, A. C., and P. G. Spear. 1997. Herpesvirus capsid assembly and envelopment, p. 312-351. In W. Chiu, R. M. Burnett, and R. L. Garcea (ed.), Structural biology of viruses. Oxford University Press, New York, NY.
52. 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. USA 104:2903-2908. (Pubitemid 46327976)
53. 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.
54. Tischer, B. K., J. von Einem, B. Kaufer, and N. Osterrieder. 2006. Two-step RED-mediated recombination for versatile high-efficiency markerless DNA manipulation in Escherichia coli. BioTechniques 40:191-197. (Pubitemid 46542640)
55. Torrisi, M. R., C. Di Lazzaro, A. Pavan, L. Pereira, and G. Campadelli-Fiume. 1992. Herpes simplex virus envelopment and maturation studies by fracture label. J. Virol. 66:554-561.
56. L34 protein interacts with a cytoplasmic dynein intermediate chain and targets nuclear membrane. J. Virol. 74:1355-1363.