Herpes simplex virus type 1 enters human epidermal keratinocytes, but not neurons, via a pH-dependent endocytic pathway

Journal of Virology

Volumn 79, Issue 12, 2005, Pages 7609-7616

  Nicola, Anthony V ^a,c   Hou, Jean ^b   Major, Eugene O ^b   Straus, Stephen E ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

^c NONE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENISTEIN; ISOFLAVONE; PROTEIN TYROSINE KINASE;

APICAL MEMBRANE; ARTICLE; BASOLATERAL MEMBRANE; CELL NUCLEUS; CELL TRANSFORMATION; CONTROLLED STUDY; ENDOCYTOSIS; GENE EXPRESSION; HERPES SIMPLEX VIRUS 1; HUMAN; HUMAN CELL; KERATINOCYTE; MONOLAYER CULTURE; NERVE CELL; NEUROBLASTOMA CELL; NONHUMAN; PATHOGENESIS; PH; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; VIRUS CELL INTERACTION; VIRUS PARTICLE;

ANIMALS; CELL LINE; ENDOCYTOSIS; EPIDERMIS; GENISTEIN; HERPESVIRUS 1, HUMAN; HUMANS; HYDROGEN-ION CONCENTRATION; KERATINOCYTES; NEURONS; PROTEIN-TYROSINE KINASES; VIRION;

HERPES; HUMAN HERPESVIRUS 1;

EID: 19944423114     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.79.12.7609-7616.2005     Document Type: Article

References (57)

1. Berlin, R. D., and J. M. Oliver. 1980. Surface functions during mitosis. II. Quantitation of pinocytosis and kinetic characterization of the mitotic cycle with a new fluorescence technique. J. Cell Biol. 85:660-671.
2. Bodaghi, B., M. E. Slobbe-van Drunen, A. Topilko, E. Perret, R. C. Vossen, M. C. van Dam-Mieras, D. Zipeto, J. L. Virelizier, P. LeHoang, C. A. Bruggeman, and S. Michelson. 1999. Entry of human cytomegalovirus into retinal pigment epithelial and endothelial cells by endocytosis. Investig. Ophthalmol. Vis. Sci. 40:2598-2607.
3. Boukamp, P., R. T. Petrussevska, D. Breitkreutz, J. Hornung, A. Markham, and N. E. Fusenig. 1988. Normal keratinization in a spontaneously immortalized aneuploid human keratinocyte cell line. J. Cell Biol. 106:761-771.
4. 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.
5. Cai, W., and P. A. Schaffer. 1991. A cellular function can enhance gene expression and plating efficiency of a mutant defective in the gene for ICP0, a transactivating protein of herpes simplex virus type 1. J. Virol. 65:4078-4090.
6. Cairns, T. M., R. S. Milne, M. Ponce-de-Leon, D. K. Tobin, G. H. Cohen, and R. J. Eisenberg. 2003. Structure-function analysis of herpes simplex virus type 1 gD and gH-gL: clues from gDgH chimeras. J. Virol. 77:6731-6742.
7. 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.
8. Carfí, A., S. H. Willis, J. C. Whitbeck, C. Krummenacher, G. H. Cohen, R. J. Eisenberg, and D. C. Wiley. 2001. Herpes simplex virus glycoprotein D bound to the human receptor HveA. Mol. Cell 8:169-179.
9. Compton, T., R. R. Nepomuceno, and D. M. Nowlin. 1992. Human cytomegalovirus penetrates host cells by pH-independent fusion at the cell surface. Virology 191:387-395.
10. Conner, S. D., and S. L. Schmid. 2003. Regulated portals of entry into the cell. Nature 422:37-44.
11. Cywes, C., and M. R. Wessels. 2001. Group A Streptococcus tissue invasion by CD44-mediated cell signalling. Nature 414:648-652.
12. Desai, P., and S. Person. 1998. Incorporation of the green fluorescent protein into the herpes simplex virus type 1 capsid. J. Virol. 72:7563-7568.
13. Earp, L. J., S. E. Delos, H. E. Park, and J. M. White. 2004. The many mechanisms of viral membrane fusion proteins. Curr. Top. Microbiol. Immunol. 285:25-66.
14. 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.
15. Gianni, T., G. Campadelli-Fiume, and L. Menotti. 2004. Entry of herpes simplex virus mediated by chimeric forms of nectin1 retargeted to endosomes or to lipid rafts occurs through acidic endosomes. J. Virol. 78:12268-12276.
16. Griffiths, A., S. Renfrey, and T. Minson. 1998. Glycoprotein C-deficient mutants of two strains of herpes simplex virus type 1 exhibit unaltered adsorption characteristics on polarized or non-polarized cells. J. Gen. Virol. 79:807-812.
17. Hayashi, K. 1995. Role of tight junctions of polarized epithelial MDCK cells in the replication of herpes simplex virus type 1. J. Med. Virol. 47:323-329.
18. Huber, M. T., T. W. Wisner, N. R. Hegde, K. A. Goldsmith, D. A. Rauch, R. J. Roller, C. Krummenacher, R. J. Eisenberg, G. H. Cohen, and D. C. Johnson. 2001. Herpes simplex virus with highly reduced gD levels can efficiently enter and spread between human keratinocytes. J. Virol. 75:10309-10318.
19. Hukkanen, V., H. Mikola, M. Nykanen, and S. Syrjanen. 1999. Herpes simplex virus type 1 infection has two separate modes of spread in three-dimensional keratinocyte culture. J. Gen. Virol. 80:2149-2155.
20. Hung, S. L., Y. Y. Cheng, Y. H. Wang, K. W. Chang, and Y. T. Chen. 2002. Expression and roles of herpesvirus entry mediators A and C in cells of oral origin. Oral Microbiol. Immunol. 17:215-223.
21. Ivanov, A. I., A. Nusrat, and C. A. Parkos. 2004. Endocytosis of epithelial apical junctional proteins by a clathrin-mediated pathway into a unique storage compartment. Mol. Biol. Cell 15:176-188.
22. 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.
23. Koyama, A. H., and T. Uchida. 1987. The mode of entry of herpes simplex virus type 1 into Vero cells. Microbiol. Immunol. 31:123-130.
24. Lycke, E., B. Hamark, M. Johansson, A. Krotochwil, J. Lycke, and B. Svennerholm. 1988. Herpes simplex virus infection of the human sensory neuron. An electron microscopy study. Arch. Virol. 101:87-104.
25. Marozin, S., U. Prank, and B. Sodeik. 2004. Herpes simplex virus type 1 infection of polarized epithelial cells requires microtubules and access to receptors present at cell-cell contact sites. J. Gen. Virol. 85:775-786.
26. Marsh, M., and A. Helenius. 1989. Virus entry into animal cells. Adv. Virus Res. 36:107-151.
27. Messam, C. A., J. Hou, R. M. Gronostajski, and E. O. Major. 2003. Lineage pathway of human brain progenitor cells identified by JC virus susceptibility. Ann. Neurol. 53:636-646.
28. Meyers, C., S. S. Andreansky, and R. J. Courtney. 2003. Replication and interaction of herpes simplex virus and human papillomavirus in differentiating host epithelial tissue. Virology 315:43-55.
29. Miller, N., and L. M. Hutt-Fletcher. 1992. Epstein-Barr virus enters B cells and epithelial cells by different routes. J. Virol. 66:3409-3414.
30. Muggeridge, M. I. 2000. Characterization of cell-cell fusion mediated by herpes simplex virus 2 glycoproteins gB, gD, gH and gL in transfected cells. J. Gen. Virol. 81:2017-2027.
31. Nemerow, G. R., and N. R. Cooper. 1984. Early events in the infection of human B lymphocytes by Epstein-Barr virus: the internalization process. Virology 132:186-198.
32. 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.
33. 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.
34. Pelkmans, L., and A. Helenius. 2003. Insider information: what viruses tell us about endocytosis. Curr. Opin. Cell Biol. 15:414-422.
35. Penfold, M. E., P. Armati, and A. L. Cunningham. 1994. Axonal transport of herpes simplex virions to epidermal cells: evidence for a specialized mode of virus transport and assembly. Proc. Natl. Acad. Sci. USA 91:6529-6533.
36. 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.
37. Roizman, B., and D. M. Knipe. 2001. Herpes simplex viruses and their replication, p. 2399-2459. In D. M. Knipe and P. M. Howley (ed.), Fields virology, vol. 2. Lippincott Williams & Wilkins, Philadelphia, Pa.
38. Schelhaas, M., M. Jansen, I. Haase, and D. Knebel-Morsdorf. 2003. Herpes simplex virus type 1 exhibits a tropism for basal entry in polarized epithelial cells. J. Gen. Virol. 84:2473-2484.
39. Sears, A. E., B. S. McGwire, and B. Roizman. 1991. Infection of polarized MDCK cells with herpes simplex virus 1: two asymmetrically distributed cell receptors interact with different viral proteins. Proc. Natl. Acad. Sci. USA 88:5087-5091.
40. Sieczkarski, S. B., and G. R. Whittaker. 2002. Dissecting virus entry via endocytosis. J. Gen. Virol. 83:1535-1545.
41. Spear, P. G., R. J. Eisenberg, and G. H. Cohen. 2000. Three classes of cell surface receptors for alphaherpesvirus entry. Virology 275:1-8.
42. Spear, P. G., and R. Longnecker. 2003. Herpesvirus entry: an update. J. Virol. 77:10179-10185.
43. Spinozzi, F., M. C. Pagliacci, G. Migliorati, R. Moraca, F. Grignani, C. Riccardi, and I. Nicoletti. 1994. The natural tyrosine kinase inhibitor genistein produces cell cycle arrest and apoptosis in Jurkat T-leukemia cells. Leuk. Res. 18:431-439.
44. Syrjanen, S., H. Mikola, M. Nykanen, and V. Hukkanen. 1996. In vitro establishment of lytic and nonproductive infection by herpes simplex virus type 1 in three-dimensional keratinocyte culture. J. Virol. 70:6524-6528.
45. 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.
46. Topp, K. S., A. L. Rothman, and J. H. Lavail. 1997. Herpes virus infection of RPE and MDCK cells: polarity of infection. Exp. Eye Res. 64:343-354.
47. Tran, L. C., J. M. Kissner, L. E. Westerman, and A. E. Sears. 2000. A herpes simplex virus 1 recombinant lacking the glycoprotein G coding sequences is defective in entry through apical surfaces of polarized epithelial cells in culture and in vivo. Proc. Natl. Acad. Sci. USA 97:1818-1822.
48. 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.
49. Vanhaesebroeck, B., S. J. Leevers, K. Ahmadi, J. Timms, R. Katso, P. C. Driscoll, R. Woscholski, P. J. Parker, and M. D. Waterfield. 2001. Synthesis and function of 3-phosphorylated inositol lipids. Annu. Rev. Biochem. 70:535-602.
50. Visalli, R. J., R. J. Courtney, and C. Meyers. 1997. Infection and replication of herpes simplex virus type 1 in an organotypic epithelial culture system. Virology 230:236-243.
51. Watanabe, T., K. Kondo, and M. Oishi. 1991. Induction of in vitro differentiation of mouse erythroleukemia cells by genistein, an inhibitor of tyrosine protein kinases. Cancer Res. 51:764-768.
52. Whitley, R. J., and B. Roizman. 2001. Herpes simplex virus infections. Lancet 357:1513-1518.
53. Wilson, D. W., N. Davis-Poynter, and A. C. Minson. 1994. Mutations in the cytoplasmic tail of herpes simplex virus glycoprotein H suppress cell fusion by a syncytial strain. J. Virol. 68:6985-6993.
54. Wittels, M., and P. G. Spear. 1991. Penetration of cells by herpes simplex virus does not require a low pH-dependent endocytic pathway. Virus Res. 18:271-290.
55. Yoon, M., and P. G. Spear. 2002. Disruption of adherens junctions liberates nectin-1 to serve as receptor for herpes simplex virus and pseudorabies virus entry. J. Virol. 76:7203-7208.
56. Zenni, M. K., P. C. Giardina, H. A. Harvey, J. Shao, M. R. Ketterer, D. M. Lubaroff, R. D. Williams, and M. A. Apicella. 2000. Macropinocytosis as a mechanism of entry into primary human urethral epithelial cells by Neisseria gonorrhoeae. Infect. Immun. 68:1696-1699.
57. Zhou, G., and B. Roizman. 2002. Cation-independent mannose 6-phosphate receptor blocks apoptosis induced by herpes simplex virus 1 mutants lacking glycoprotein D and is likely the target of antiapoptotic activity of the glycoprotein. J. Virol. 76:6197-6204.