Essential functions of the unique N-terminal region of the varicella-zoster virus glycoprotein E ectodomain in viral replication and in the pathogenesis of skin infection

Journal of Virology

Volumn 80, Issue 19, 2006, Pages 9481-9496

  Berarducci, Barbara ^a   Ikoma, Minako ^b   Stamatis, Shaye ^a   Sommer, Marvin ^a   Grose, Charles ^b   Arvin, Ann M ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; GLYCOPROTEIN E; MUTANT PROTEIN; SERINE; VIRUS GLYCOPROTEIN;

AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ARTICLE; BIOINFORMATICS; CHICKENPOX; GENE DELETION; GENE INSERTION; HERPES VIRUS; HUMAN; HUMAN CELL; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; PROTEIN TRANSPORT; SITE DIRECTED MUTAGENESIS; SKIN INFECTION; STRUCTURE ANALYSIS; VARICELLA ZOSTER VIRUS; VIRION; VIRUS PATHOGENESIS; VIRUS REPLICATION;

AMINO ACID SEQUENCE; ANIMALS; CELL LINE, TUMOR; GLYCOPROTEINS; HERPESVIRUS 3, HUMAN; HUMANS; KINETICS; MICE; MICE, SCID; MICROSCOPY, ELECTRON; MOLECULAR SEQUENCE DATA; MUTATION; SEQUENCE ALIGNMENT; SKIN DISEASES, INFECTIOUS; VIRAL PROTEINS; VIRUS REPLICATION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

HUMAN HERPESVIRUS 3;

EID: 33748934626     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00533-06     Document Type: Article

References (64)

1. Alconada, A., U. Bauer, and B. Hoflack. 1996. A tyrosine-based motif and a casein kinase II phosphorylation site regulate the intracellular trafficking of the varicella-zoster virus glycoprotein I, a protein localized in the trans-Golgi network. EMBO J. 15:6096-6110.
2. Altschul, S. F., T. L. Madden, A. A. Schaffer, J. Zhang, Z. Zhang, W. Miller, and D. J. Lipman. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
3. Arvin, A. M. 2001. Varicella-zoster virus, p. 2731-2768. 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, 4th ed., vol. 2. Lippincott Williams & Wilkins, Philadelphia, Pa.
4. Baiker, A., C. Bagowski, H. Ito, M. Sommer, L. Zerboni, K. Fabel, J. Hay, W. Ruyechan, and A. M. Arvin. 2004. The immediate-early 63 protein of varicella-zoster virus: analysis of functional domains required for replication in vitro and for T-cell and skin tropism in the SCIDhu model in vivo. J. Virol. 78:1181-1194.
5. Bailey, T. L., and C. Elkan. 1994. Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc. Int. Conf. Intell. Syst. Mol. Biol. 2:28-36.
6. Basu, S., G. Dubin, M. Basu, V. Nguyen, and H. M. Friedman. 1995. Characterization of regions of herpes simplex virus type 1 glycoprotein E involved in binding the Fc domain of monomeric IgG and in forming a complex with glycoprotein I. J. Immunol. 154:260-267.
7. Besser, J., M. Ikoma, K. Fabel, M. H. Sommer, L. Zerboni, C. Grose, and A. M. Arvin. 2004. Differential requirement for cell fusion and virion formation in the pathogenesis of varicella-zoster virus infection in skin and T cells. J. Virol. 78:13293-13305.
8. Brack, A. R., B. G. Klupp, H. Granzow, R. Tirabassi, L. W. Enquist, and T. C. Mettenleiter. 2000. Role of the cytoplasmic tail of pseudorabies virus glycoprotein E in virion formation. J. Virol. 74:4004-4016.
9. Campadelli-Fiume, G., F. Cocchi, L. Menotti, and M. Lopez. 2000. The novel receptors that mediate the entry of herpes simplex viruses and animal alphaherpesviruses into cells. Rev. Med. Virol. 10:305-319.
10. Cohen, J. I., and S. E. Straus. 2001. Varicella-zoster virus and its replication, p. 2707-2730. 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, 4th ed., vol. 2. Lippincott Williams & Wilkins, Philadelphia, Pa.
11. Cohen, J. I., and H. Nguyen. 1997. Varicella-zoster virus glycoprotein I is essential for growth of virus in Vero cells. J. Virol. 71:6913-6920.
12. Cohen, J. I., and K. E. Seidel. 1993. Generation of varicella-zoster virus (VZV) and viral mutants from cosmid DNAs: VZV thymidylate synthetase is not essential for replication in vitro. Proc. Natl. Acad. Sci. USA 90:7376-7380.
13. 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.
14. Collins, W. J., and D. C. Johnson. 2003. Herpes simplex virus gE/gI expressed in epithelial cells interferes with cell-to-cell spread. J. Virol. 77: 2686-2695.
15. Davison, A. J. 1983. DNA sequence of the US component of the varicella-zoster virus genome. EMBO J. 2:2203-2209.
16. Davison, A. J., and D. J. McGeoch. 1986. Evolutionary comparisons of the S segments in the genomes of herpes simplex virus type 1 and varicella-zoster virus. J. Gen. Virol. 67:597-611.
17. Davison, A. J., and J. E. Scott. 1986. The complete DNA sequence of varicella-zoster virus. J. Gen. Virol. 67:1759-1816.
18. Dingwell, K. S., and D. C. Johnson. 1998. The herpes simplex virus gE-gI complex facilitates cell-to-cell spread and binds to components of cell junctions. J. Virol. 72:8933-8942.
19. Farnsworth, A., K. Goldsmith, and D. C. Johnson. 2003. Herpes simplex virus glycoproteins gD and gE/gI serve essential but redundant functions during acquisition of the virion envelope in the cytoplasm. J. Virol. 77:8481-8494.
20. Grose, C. 2002. The predominant varicella-zoster virus gE and gI glycoprotein complex, p. 195-223. In A. Holzenburg and E. Bogner (ed.), Structure-function relationships of human pathogenic viruses. Kluwer Academic/Plenum Publishers, New York, N.Y.
21. Grose, C., D. M. Perrotta, P. A. Brunell, and G. C. Smith. 1979. Cell-free varicella-zoster virus in cultured human melanoma cells. J. Gen. Virol. 43: 15-27.
22. Grose, C., S. Tyler, G. Peters, J. Hiebert, G. M. Stephens, W. T. Ruyechan, W. Jackson, J. Storlie, and G. A. Tipples. 2004. Complete DNA sequence analyses of the first two varicella-zoster virus glycoprotein E (D150N) mutant viruses found in North America: evolution of genotypes with an accelerated cell spread phenotype. J. Virol. 78:6799-6807.
23. Harson, R., and C. Grose. 1995. Egress of varicella-zoster virus from the melanoma cell: a tropism for the melanocyte. J. Virol. 69:4994-5010.
24. Johnson, D. C., M. Webb, T. W. Wisner, and C. Brunetti. 2001. Herpes simplex virus gE/gI sorts nascent virions to epithelial cell junctions, promoting virus spread. J. Virol. 75:821-833.
25. Kemble, G. W., P. Annunziato, O. Lungu, R. E. Winter, T. A. Cha, S. J. Silverstein, and R. R. Spaete. 2000. Open reading frame S/L of varicellazoster virus encodes a cytoplasmic protein expressed in infected cells. J. Virol. 74:11311-11321.
26. Kenyon, T. K., J. I. Cohen, and C. Grose. 2002. Phosphorylation by the varicella-zoster virus ORF47 protein serine kinase determines whether endocytosed viral gE traffics to the trans-Golgi network or recycles to the cell membrane. J. Virol. 76:10980-10993.
27. Kimura, H., S. E. Straus, and R. K. Williams. 1997. Varicella-zoster virus glycoproteins E and I expressed in insect cells form a heterodimer that requires the N-terminal domain of glycoprotein I. Virology 233:382-391.
28. Krummenacher, C., I. Baribaud, R. J. Eisenberg, and G. H. Cohen. 2003. Cellular localization of nectin-1 and glycoprotein D during herpes simplex virus infection. J. Virol. 77:8985-8999.
29. 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.
30. Litwin, V., W. Jackson, and C. Grose. 1992. Receptor properties of two varicella-zoster virus glycoproteins, gpI and gpIV, homologous to herpes simplex virus gE and gI. J. Virol. 66:3643-3651.
31. Mallory, S., M. Sommer, and A. M. Arvin. 1997. Mutational analysis of the role of glycoprotein I in varicella-zoster virus replication and its effects on glycoprotein E conformation and trafficking. J. Virol. 71:8279-8288.
32. Marchler-Bauer, A., and S. H. Bryant. 2004. CD-Search: protein domain annotations on the fly. Nucleic Acids Res. 32:W327-W331.
33. Maresova, L., T. J. Pasieka, and C. Grose. 2001. Varicella-zoster virus gB and gE coexpression, but not gB or gE alone, leads to abundant fusion and syncytium formation equivalent to those from gH and gL coexpression. J. Virol. 75:9483-9492.
34. Maresova, L., T. J. Pasieka, E. Homan, E. Gerday, and C. Grose. 2005. Incorporation of three endocytosed varicella-zoster virus glycoproteins, gE, gH, and gB, into the virion envelope. J. Virol. 79:997-1007.
35. McMillan, T. N., and D. C. Johnson. 2001. Cytoplasmic domain of herpes simplex virus gE causes accumulation in the trans-Golgi network, a site of virus envelopment and sorting of virions to cell junctions. J. Virol. 75:1928-1940.
36. Mo, C., J. Lee, M. Sommer, C. Grose, and A. M. Arvin. 2002. The requirement of varicella zoster virus glycoprotein E (gE) for viral replication and effects of glycoprotein I on gE in melanoma cells. Virology 304:176-186.
37. Mo, C., E. E. Schneeberger, and A. M. Arvin. 2000. Glycoprotein E of varicella-zoster virus enhances cell-cell contact in polarized epithelial cells. J. Virol. 74:11377-11387.
38. Moffat, J., H. Ito, M. Sommer, S. Taylor, and A. M. Arvin. 2002. Glycoprotein I of varicella-zoster virus is required for viral replication in skin and T cells. J. Virol. 76:8468-8471.
39. Moffat, J., C. Mo, J. J. Cheng, M. Sommer, L. Zerboni, S. Stamatis, and A. M. Arvin. 2004. Functions of the C-terminal domain of varicella-zoster virus glycoprotein E in viral replication in vitro and skin and T-cell tropism in vivo. J. Virol. 78:12406-12415.
40. MoOat, J. F., M. D. Stein, H. Kaneshima, and A. M. Arvin. 1995. Tropism of varicella-zoster virus for human CD4+ and CD8+ T lymphocytes and epidermal cells in SCID-hu mice. J. Virol. 69:5236-5242.
41. Moffat, J. F., L. Zerboni, P. R. Kinchington, C. Grose, H. Kaneshima, and A. M. Arvin. 1998. Attenuation of the vaccine Oka strain of varicella-zoster virus and role of glycoprotein C in alphaherpesvirus virulence demonstrated in the SCID-hu mouse. J. Virol. 72:965-974.
42. Moffat, J. F., L. Zerboni, M. H. Sommer, T. C. Heineman, J. I. Cohen, M. Kaneshima, and A. M. Arvin. 1998. The ORF47 and ORF66 putative protein kinases of varicella-zoster virus determine tropism for human T cells and skin in the SCID-hu mouse. Proc. Natl. Acad. Sci. USA 95:11969-11974.
43. Montalvo, E. A., R. T. Parmley, and C. Grose. 1985. Structural analysis of the varicella-zoster virus gp98-gp62 complex: posttranslational addition of re-linked and O-linked oligosaccharide moieties. J. Virol. 53:761-770.
44. Niizuma, T., L. Zerboni, M. H. Sommer, H. Ito, S. Hinchliffe, and A. M. Arvin. 2003. Construction of varicella-zoster virus recombinants from parent Oka cosmids and demonstration that ORF65 protein is dispensable for infection of human skin and T cells in the SCID-hu mouse model. J. Virol. 77:6062-6065.
45. Notredame, C., D. G. Higgins, and J. Heringa. 2000. T-Coffee: a novel method for fast and accurate multiple sequence alignment. J. Mol. Biol. 302:205-217.
46. Olson, J. K., G. A. Bishop, and C. Grose. 1997. Varicella-zoster virus Fc receptor gE glycoprotein: serine/threonine and tyrosine phosphorylation of monomeric and dimeric forms. J. Virol. 71:110-119.
47. Olson, J. K., and C. Grose. 1998. Complex formation facilitates endocytosis of the varicella-zoster virus gE:gI Fc receptor. J. Virol. 72:1542-1551.
48. Olson, J. K., and C. Grose. 1997. Endocytosis and recycling of varicellazoster virus Fc receptor glycoprotein gE: internalization mediated by a YXXL motif in the cytoplasmic tail. J. Virol. 71:4042-4054.
49. Polcicova, K., K. Goldsmith, B. L. Rainish, T. W. Wisner, and D.C. Johnson. 2005. The extracellular domain of herpes simplex virus gE is indispensable for efficient cell-to-cell spread: evidence for gE/gI receptors. J. Virol. 79: 11990-12001.
50. Rizvi, S. M., and M. Raghavan. 2001. An N-terminal domain of herpes simplex virus type I gE is capable of forming stable complexes with gI. J. Virol. 75:11897-11901.
51. Santos, R. A., C. C. Hatfield, N. L. Cole, J. A. Padilla, J. F. Moffat, A. M. Arvin, W. T. Ruyechan, J. Hay, and C. Grose. 2000. Varicella-zoster virus gE escape mutant VZV-MSP exhibits an accelerated cell-to-cell spread phenotype in both infected cell cultures and SCID-hu mice. Virology 275:306-317.
52. Silva, M. C., J. Schroer, and T. Shenk. 2005. Human cytomegalovirus cell-to-cell spread in the absence of an essential assembly protein. Proc. Natl. Acad. Sci. USA 102:2081-2086.
53. Sommer, M. H., E. Zagha, O. K. Serrano, C. C. Ku, L. Zerboni, A. Baiker, R. Santos, M. Spengler, J. Lynch, C. Grose, W. Ruyechan, J. Hay, and A. M. Arvin. 2001. Mutational analysis of the repeated open reading frames, ORFs 63 and 70 and ORFs 64 and 69, of varicella-zoster virus. J. Virol. 75:8224-8239.
54. Spear, P. G., R. J. Eisenberg, and G. H. Cohen. 2000. Three classes of cell surface receptors for alphaherpesvirus entry. Virology 275:1-8.
55. Spear, P. G., and R. Longnecker. 2003. Herpesvirus entry: an update. J. Virol. 77:10179-10185.
56. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
57. Tirabassi, R. S., and L. W. Enquist. 1999. Mutation of the YXXL endocytosis motif in the cytoplasmic tail of pseudorabies virus gE. J. Virol. 73:2717-2728.
58. Tyborowska, J., K. Bienkowska-Szewczyk, M. Rychlowski, J. T. Van Oirschot, and F. A. Rijsewijk. 2000. The extracellular part of glycoprotein E of bovine herpesvirus 1 is sufficient for complex formation with glycoprotein I but not for cell-to-cell spread. Arch. Virol. 145:333-351.
59. Wang, Z. H., M. D. Gershon, O. Lungu, Z. Zhu, S. Mallon, A. M. Arvin, and A. A. Gershon. 2001. Essential role played by the C-terminal domain of glycoprotein I in envelopment of varicella-zoster virus in the trans-Golgi network: interactions of glycoproteins with tegument. J. Virol. 75:323-340.
60. Wisner, T., C. Brunetti, K. Dingwell, and D. C. Johnson. 2000. The extracellular domain of herpes simplex virus gE is sufficient for accumulation at cell junctions but not for cell-to-cell spread. J. Virol. 74:2278-2287.
61. Yao, Z., W. Jackson, B. Forghani, and C. Grose. 1993. Varicella-zoster virus glycoprotein gpI/gpIV receptor: expression, complex formation, and antigenicity within the vaccinia virus-T7 RNA polymerase transfection system. J. Virol. 67:305-314.
62. Yao, Z., W. Jackson, and C. Grose. 1993. Identification of the phosphorylation sequence in the cytoplasmic tail of the varicella-zoster virus Fc receptor glycoprotein gpI. J. Virol. 67:4464-4473.
63. Zhu, Z., M. D. Gershon, Y. Hao, R. T. Ambron, C. A. Gabel, and A. A. Gershon. 1995. Envelopment of varicella-zoster virus: targeting of viral glycoproteins to the trans-Golgi network. J. Virol. 69:7951-7959.
64. Zhu, Z., Y. Hao, M. D. Gershon, R. T. Ambron, and A. A. Gershon. 1996. Targeting of glycoprotein I (gE) of varicella-zoster virus to the trans-Golgi network by an AYRV sequence and an acidic amino acid-rich patch in the cytosolic domain of the molecule. J. Virol. 70:6563-6575.