Postentry events are responsible for restriction of productive varicella-zoster virus infection in Chinese hamster ovary cells

Journal of Virology

Volumn 80, Issue 21, 2006, Pages 10325-10334

  Finnen, Renée L ^a   Mizokami, Kara R ^a   Banfield, Bruce W ^a   Cai, Guang Yun ^a   Simpson, Scott A ^a   Pizer, Lewis I ^a   Levin, Myron J ^a  

^a UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GALACTOSIDASE; GENE PRODUCT; GLYCOSAMINOGLYCAN; HEPARAN SULFATE GLYCOSAMINOGLYCAN; INFECTED CELL PROTEIN 8; LYSOSOMOTROPIC AGENT; PROTEIN ICP4; SOMATOMEDIN B RECEPTOR; UNCLASSIFIED DRUG; VIRUS DNA;

ANIMAL CELL; ARTICLE; CELL INVASION; CELL SURFACE; CHO CELL; CONTROLLED STUDY; ENDOCYTOSIS; GENE EXPRESSION REGULATION; HERPES SIMPLEX VIRUS 1; IMMEDIATE EARLY GENE; IN VITRO STUDY; LATE GENE; NONHUMAN; PH MEASUREMENT; PRIMATE; PRIORITY JOURNAL; PROGENY; REPORTER GENE; VARICELLA ZOSTER VIRUS; VIROGENESIS; VIRUS CELL INTERACTION; VIRUS INFECTION; VIRUS INFECTIVITY; VIRUS INHIBITION;

ANIMALS; CELL LINE; CHO CELLS; CRICETINAE; ENDOCYTOSIS; GENE EXPRESSION; GENES, VIRAL; HEPARITIN SULFATE; HERPESVIRUS 3, HUMAN; HUMANS; HYDROGEN-ION CONCENTRATION; MICE; NIH 3T3 CELLS; RECEPTOR, IGF TYPE 2; RECEPTORS, VIRUS; SPECIES SPECIFICITY; VIRUS REPLICATION;

CRICETULUS GRISEUS; HUMAN HERPESVIRUS 1; HUMAN HERPESVIRUS 3; PRIMATES;

EID: 33750298267     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00939-06     Document Type: Article

References (70)

1. Annunziato, P., P. LaRussa, P. Lee, S. Steinberg, O. Lungu, A. A. Gershon, and S. Silverstein. 1998. Evidence of latent varicella-zoster virus in rat dorsal root ganglia. J. Infect. Dis. 178(Suppl. 1):S48-S51.
2. Banfield, B. W., Y. Leduc, L. Esford, K. Schubert, and F. Tufaro. 1995. Sequential isolation of proteoglycan synthesis mutants by using herpes simplex virus as a selective agent: evidence for a proteoglycan-independent virus entry pathway. J. Virol. 69:3290-3298.
3. Banfield, B. W., Y. Leduc, L. Esford, R. J. Visalli, C. R. Brandt, and F. Tufaro. 1995. Evidence for an interaction of herpes simplex virus with chondroitin sulfate proteoglycans during infection. Virology 208:531-539.
4. Bourdon-Wouters, C., M. P. Merville-Louis, C. Sadzot-Delvaux, P. Marc, J. Piette, P. Delree, G. Moonen, and B. Rentier. 1990. Acute and persistent varicella-zoster virus infection of human and murine neuroblastoma cell lines. J. Neurosci. Res. 26:90-97.
5. 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.
6. Brunell, P. A., L. C. Ren, J. I. Cohen, and S. E. Straus. 1999. Viral gene expression in rat trigeminal ganglia following neonatal infection with varicella-zoster virus. J. Med. Virol. 58:286-290.
7. Chen, J. J., Z. Zhu, A. A. Gershon, and M. D. Gershon. 2004. Mannose 6-phosphate receptor dependence of varicella zoster virus infection in vitro and in the epidermis during varicella and zoster. Cell 119:915-926.
8. Cohen, J. I., Y. Wang, R. Nussenblatt, S. E. Straus, and J. J. Hooks. 1998. Chronic uveitis in guinea pigs infected with varicella-zoster virus expressing Escherichia coli beta-galactosidase. J. Infect. Dis. 177:293-300.
9. Cole, N. L., and C. Grose. 2003. Membrane fusion mediated by herpesvirus glycoproteins: the paradigm of varicella-zoster virus. Rev. Med. Virol. 13:207-222.
10. Dahms, N. M., P. A. Rose, J. D. Molkentin, Y. Zhang, and M. A. Brzycki. 1993. The bovine mannose 6-phosphate/insulin-like growth factor II receptor. The role of arginine residues in mannose 6-phosphate binding. J. Biol. Chem. 268:5457-5463.
11. Duus, K. M., and C. Grose. 1996. Multiple regulatory effects of varicella-zoster virus (VZV) gL on trafficking patterns and fusogenic properties of VZV gH. J. Virol. 70:8961-8971.
12. Duus, K. M., C. Hatfield, and C. Grose. 1995. Cell surface expression and fusion by the varicella-zoster virus gH:gL glycoprotein complex: analysis by laser scanning confocal microscopy. Virology 210:429-440.
13. Eisfeld, A. J., S. E. Turse, S. A. Jackson, E. C. Lerner, and P. R. Kinchington. 2006. Phosphorylation of the varicella-zoster virus (VZV) major transcriptional regulatory protein IE62 by the VZV open reading frame 66 protein kinase. J. Virol. 80:1710-1723.
14. Frampton, A. R., Jr., W. F. Goins, J. B. Cohen, J. von Einem, N. Osterrieder, D. J. O'Callaghan, and J. C. Glorioso. 2005. Equine herpesvirus 1 utilizes a novel herpesvirus entry receptor. J. Virol. 79:3169-3173.
15. Fuller, A. O., R. E. Santos, and P. G. Spear. 1989. Neutralizing antibodies specific for glycoprotein H of herpes simplex virus permit viral attachment to cells but prevent penetration. J. Virol. 63:3435-3443.
16. Fuller, A. O., and P. G. Spear. 1987. Anti-glycoprotein D antibodies that permit adsorption but block infection by herpes simplex virus 1 prevent virion-cell fusion at the cell surface. Proc. Natl. Acad. Sci. USA 84:5454-5458.
17. Gabel, C. A., L. Dubey, S. P. Steinberg, D. Sherman, M. D. Gershon, and A. A. Gershon. 1989. Varicella-zoster virus glycoprotein oligosaccharides are phosphorylated during posttranslational maturation. J. Virol. 63:4264-4276.
18. Garry, E. M., A. Delaney, H. A. Anderson, E. C. Sirinathsinghji, R. H. Clapp, W. J. Martin, P. R. Kinchington, D. L. Krah, C. Abbadie, and S. M. Fleetwood-Walker. 2005. Varicella zoster virus induces neuropathic changes in rat dorsal root ganglia and behavioral reflex sensitisation that is attenuated by gabapentin or sodium channel blocking drugs. Pain 118:97-111.
19. Geraghty, R. J., C. Krummenacher, G. H. Cohen, R. J. Eisenberg, and P. G. Spear. 1998. Entry of alphaherpesviruses mediated by poliovirus receptor-related protein 1 and poliovirus receptor. Science 280:1618-1620.
20. Goff, S. P. 2004. Genetic control of retrovirus susceptibility in mammalian cells. Annu. Rev. Genet. 38:61-85.
21. Gold, E. 1965. Characteristics of herpes zoster and varicella viruses propagated in vitro. J. Immunol. 95:683-691.
22. Grinfeld, E., and P. G. Kennedy. 2004. Translation of varicella-zoster virus genes during human ganglionic latency. Virus Genes 29:317-319.
23. Hood, C., A. L. Cunningham, B. Slobedman, A. M. Arvin, M. H. Sommer, P. R. Kinchington, and A. Abendroth. 2006. Varicella-zoster virus ORF63 inhibits apoptosis of primary human neurons. J. Virol. 80:1025-1031.
24. Huang, A. S., and R. R. Wagner. 1964. Penetration of herpes simplex virus into human epidermoid cells. Proc. Soc. Exp. Biol. Med. 116:863-869.
25. Jacquet, A., M. Haumont, D. Chellun, M. Massaer, F. Tufaro, A. Bollen, and P. Jacobs. 1998. The varicella zoster virus glycoprotein B (gB) plays a role in virus binding to cell surface heparan sulfate proteoglycans. Virus Res. 53:197-207.
26. Karger, A., A. Saalmuller, F. Tufaro, B. W. Banfield, and T. C. Mettenleiter. 1995. Cell surface proteoglycans are not essential for infection by pseudo-rabies virus. J. Virol. 69:3482-3489.
27. Kennedy, P. G., E. Grinfeld, S. Bontems, and C. Sadzot-Delvaux. 2001. Varicella-zoster virus gene expression in latently infected rat dorsal root ganglia. Virology 289:218-223.
28. Kinchington, P. R., K. Fite, A. Seman, and S. E. Turse. 2001. Virion association of IE62, the varicella-zoster virus (VZV) major transcriptional regulatory protein, requires expression of the VZV open reading frame 66 protein kinase. J. Virol. 75:9106-9113.
29. Kinchington, P. R., K. Fite, and S. E. Turse. 2000. Nuclear accumulation of IE62, the varicella-zoster virus (VZV) major transcriptional regulatory protein, is inhibited by phosphorylation mediated by the VZV open reading frame 66 protein kinase. J. Virol. 74:2265-2277.
30. Kinchington, P. R., and S. E. Turse. 1998. Regulated nuclear localization of the varicella-zoster virus major regulatory protein, IE62. J. Infect. Dis. 178(Suppl. 1):S16-S21.
31. Krummenacher, C., F. Baribaud, M. Ponce de Leon, I. Baribaud, J. C. Whitbeck, R. Xu, G. H. Cohen, and R. J. Eisenberg. 2004. Comparative usage of herpesvirus entry mediator A and nectin-1 by laboratory strains and clinical isolates of herpes simplex virus. Virology 322:286-299.
32. Ku, C. C., J. Besser, A. Abendroth, C. Grose, and A. M. Arvin. 2005. Varicella-zoster virus pathogenesis and immunobiology: new concepts emerging from investigations with the SCIDhu mouse model. J. Virol. 79:2651-2658.
33. Lungu, O., C. A. Panagiotidis, P. W. Annunziato, A. A. Gershon, and S. J. Silverstein. 1998. Aberrant intracellular localization of varicella-zoster virus regulatory proteins during latency. Proc. Natl. Acad. Sci. USA 95:7080-7085.
34. Mao, J. C., and E. E. Robishaw. 1975. Mode of inhibition of herpes simplex virus DNA polymerase by phosphonoacetate. Biochemistry 14:5475-5479.
35. May, D. C., M. R. Miller, and F. Rapp. 1977. The effect of phosphonoacetic acid on the in vitro replication of varicella-zoster virus. Intervirology 8:83-91.
36. McFadden, G. 2005. Poxvirus tropism. Nat. Rev. Microbiol. 3:201-213.
37. Merville-Louis, M. P., C. Sadzot-Delvaux, P. Delree, J. Piette, G. Moonen, and B. Rentier. 1989. Varicella-zoster virus infection of adult rat sensory neurons in vitro. J. Virol. 63:3155-3160.
38. Milne, R. S., A. V. Nicola, J. C. Whitbeck, R. J. Eisenberg, and G. H. Cohen. 2005. Glycoprotein D receptor-dependent, low-pH-independent endocytic entry of herpes simplex virus type 1. J. Virol. 79:6655-6663.
39. + T lymphocytes and epidermal cells in SCID-hu mice. J. Virol. 69:5236-5242.
40. 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.
41. Moriuchi, H., M. Moriuchi, S. E. Straus, and J. I. Cohen. 1993. Varicella-zoster virus open reading frame 10 protein, the herpes simplex virus VP16 homolog, transactivates herpesvirus immediate-early gene promoters. J. Virol. 67:2739-2746.
42. Nicola, A. V., J. Hou, E. O. Major, and S. E. Straus. 2005. Herpes simplex virus type 1 enters human epidermal keratinocytes, but not neurons, via a pH-dependent endocytic pathway. J. Virol. 79:7609-7616.
43. Nicola, A. V., A. M. McEvoy, and S. E. Straus. 2003. Roles for endocytosis and low pH in herpes simplex virus entry into HeLa and Chinese hamster ovary cells. J. Virol. 77:5324-5332.
44. Nicola, A. V., and S. E. Straus. 2004. Cellular and viral requirements for rapid endocytic entry of herpes simplex virus. J. Virol. 78:7508-7517.
45. Nixdorf, R., J. Schmidt, A. Karger, and T. C. Mettenleiter. 1999. Infection of Chinese hamster ovary cells by pseudorabies virus. J. Virol. 73:8019-8026.
46. Pasieka, T. J., L. Maresova, K. Shiraki, and C. Grose. 2004. Regulation of varicella-zoster virus-induced cell-to-cell fusion by the endocytosis-competent glycoproteins gH and gE. J. Virol. 78:2884-2896.
47. Pertel, P. E., A. Fridberg, M. L. Parish, and P. G. Spear. 2001. Cell fusion induced by herpes simplex virus glycoproteins gB, gD, and gH-gL requires a gD receptor but not necessarily heparan sulfate. Virology 279:313-324.
48. Rahaus, M., S. Schunemann, and M. H. Wolff. 1999. Morphological and biological characteristics of varicella-zoster virus, p. 1-10. In M. H. Wolff, S. Schunemann, and A. Schmidt (ed.), Varicella-zoster virus. Molecular biology, pathogenesis, and clinical aspects, vol. 3. Karger, Basel, Switzerland.
49. Rodriguez, J. E., T. Moninger, and C. Grose. 1993. Entry and egress of varicella virus blocked by same anti-gH monoclonal antibody. Virology 196:840-844.
50. Ruyechan, W., P. Ling, P. R. Kinchington, and J. Hay. 1991. The correlation between varicella-zoster virus transcription and the sequence of the viral genome, p. 301-318. In E. K. Wagner (ed.), Herpesvirus transcription and its regulation. CRC Press, Boca Raton, Fla.
51. Sadzot-Delvaux, C., S. Debrus, A. Nikkels, J. Piette, and B. Rentier. 1995. Varicella-zoster virus latency in the adult rat is a useful model for human latent infection. Neurology 45:S18-S20.
52. Sadzot-Delvaux, C., M. P. Merville-Louis, P. Delree, P. Marc, J. Piette, G. Moonen, and B. Rentier. 1990. An in vivo model of varicella-zoster virus latent infection of dorsal root ganglia. J. Neurosci. Res. 26:83-89.
53. Sato, H., L. Pesnicak, and J. I. Cohen. 2003. Use of a rodent model to show that varicella-zoster virus ORF61 is dispensable for establishment of latency. J. Med. Virol. 70(Suppl. 1):S79-S81.
54. Sato, H., L. Pesnicak, and J. I. Cohen. 2002. Varicella-zoster virus open reading frame 2 encodes a membrane phosphoprotein that is dispensable for viral replication and for establishment of latency. J. Virol. 76:3575-3578.
55. Schaap, A., J. F. Fortin, M. Sommer, L. Zerboni, S. Stamatis, C. C. Ku, G. P. Nolan, and A. M. Arvin. 2005. T-cell tropism and the role of ORF66 protein in pathogenesis of varicella-zoster virus infection. J. Virol. 79:12921-12933.
56. Shieh, M. T., D. WuDunn, R. I. Montgomery, J. D. Esko, and P. G. Spear. 1992. Cell surface receptors for herpes simplex virus are heparan sulfate proteoglycans. J. Cell Biol. 116:1273-1281.
57. Shiraki, K., H. Sato, J. Yamamura, Z. H. Li, T. Yokoyama, T. Hasegawa, T. Okuno, M. Kurokawa, and S. Kageyama. 1997. Functions of purified gB, gE:gI, and gH:gL, and their sialyl residues in varicella-zoster virus infection. Arch. Virol. 142:2295-2301.
58. Shukla, D., J. Liu, P. Blaiklock, N. W. Shworak, X. Bai, J. D. Esko, G. H. Cohen, R. J. Eisenberg, R. D. Rosenberg, and P. G. Spear. 1999. A novel role for 3-O-sulfated heparan sulfate in herpes simplex virus 1 entry. Cell 99:13-22.
59. Shukla, D., and P. G. Spear. 2001. Herpesviruses and heparan sulfate: an intimate relationship in aid of viral entry. J. Clin. Investig. 108:503-510.
60. Spear, P. G., R. J. Eisenberg, and G. H. Cohen. 2000. Three classes of cell surface receptors for alphaherpesvirus entry. Virology 275:1-8.
61. Spear, P. G., and R. Longnecker. 2003. Herpesvirus entry: an update. J. Virol. 77:10179-10185.
62. Takahashi, M., and S. A. Plotkin. 2000. Development of the Oka vaccine, p. 442-459. In A. M. Arvin and A. A. Gershon (ed.), Varicella-zoster virus virology and clinical management. Cambridge University Press, Cambridge, United Kingdom.
63. Tal-Singer, R., C. Peng, M. Ponce De Leon, W. R. Abrams, B. W. Banfield, F. Tufaro, G. H. Cohen, and R. J. Eisenberg. 1995. Interaction of herpes simplex virus glycoprotein gC with mammalian cell surface molecules. J. Virol. 69:4471-4483.
64. Taylor-Robinson, D., and A. E. Caunt 1972. Varicella virus. Springer-Verlag, New York, N.Y.
65. Turner, A., B. Bruun, T. Minson, and H. Browne. 1998. Glycoproteins gB, gD, and gHgL of herpes simplex virus type 1 are necessary and sufficient to mediate membrane fusion in a Cos cell transfection system. J. Virol. 72:873-875.
66. Vafai, A., Z. Wroblewska, M. Wellish, M. Green, and D. Gilden. 1984. Analysis of three late varicella-zoster virus proteins, a 125,000-molecular- weight protein and gp1 and gp3. J. Virol. 52:953-959.
67. Warner, M. S., R. J. Geraghty, W. M. Martinez, R. I. Montgomery, J. C. Whitbeck, R. Xu, R. J. Eisenberg, G. H. Cohen, and P. G. Spear. 1998. A cell surface protein with herpesvirus entry activity (HveB) confers susceptibility to infection by mutants of herpes simplex virus type 1, herpes simplex virus type 2, and pseudorabies virus. Virology 246:179-189.
68. Weller, T. H., H. M. Witton, and E. J. Bell. 1958. The etiologic agents of varicella and herpes zoster; isolation, propagation, and cultural characteristics in vitro. J. Exp. Med. 108:843-868.
69. Wroblewska, Z., T. Valyi-Nagy, J. Otte, A. Dillner, A. Jackson, D. P. Sole, and N. W. Fraser. 1993. A mouse model for varicella-zoster virus latency. Microb. Pathog. 15:141-151.
70. Zhu, Z., M. D. Gershon, R. Ambron, C. Gabel, and A. A. Gershon. 1995. Infection of cells by varicella zoster virus: inhibition of viral entry by mannose 6-phosphate and heparin. Proc. Natl. Acad. Sci. USA 92:3546-3550.