Human cytomegalovirus entry into epithelial and endothelial cells depends on genes UL128 to UL150 and occurs by endocytosis and low-pH fusion

Journal of Virology

Volumn 80, Issue 2, 2006, Pages 710-722

  Ryckman, Brent J ^a   Jarvis, Michael A ^a   Drummond, Derek D ^a   Nelson, Jay A ^a   Johnson, David C ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BAFILOMYCIN A1; CHLOROQUINE; GENE PRODUCT; MACROGOL; THYMIDINE; TRITIUM; VIRUS DNA;

ARTICLE; CELL TYPE; CONTROLLED STUDY; CYTOMEGALOVIRUS; DELETION MUTANT; ENDOCYTOSIS; ENDOSOME; ENDOTHELIUM CELL; EPITHELIUM CELL; FIBROBLAST; GENE EXPRESSION; HUMAN; HUMAN CELL; INTERNALIZATION; ISOTOPE LABELING; NEWBORN; NONHUMAN; NUCLEOTIDE SEQUENCE; PH; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; VIRUS ADSORPTION; VIRUS CELL INTERACTION; VIRUS GENE; VIRUS REPLICATION;

CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTIONS; ENDOCYTOSIS; ENDOTHELIAL CELLS; EPITHELIAL CELLS; GENES, VIRAL; HUMANS; HYDROGEN-ION CONCENTRATION; MEMBRANE FUSION; MUTATION; VIRUS REPLICATION;

CYTOMEGALOVIRUS; DNA VIRUSES; HUMAN HERPESVIRUS 5;

EID: 30344435010     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.80.2.710-722.2006     Document Type: Article

References (66)

1. Benyesh-Melnick, M., F. Probstmeyer, R. McCombs, J. P. Brunschwig, and V. Vonka. 1966. Correlation between infectivity and physical virus particles in human cytomegalovirus. J. Bacteriol. 92:1555-1561.
2. Bissinger, A. L., C. Sinzger, E. Kaiserling, and G. Jahn. 2002. Human cytomegalovirus as a direct pathogen: correlation of multiorgan involvement and cell distribution with clinical and pathological findings in a case of congenital inclusion disease. J. Med. Virol. 67:200-206.
3. Bodaghi, B., M. E. P. Slobbe-Vandrunen, A. Topilko, E. Perret, R. C. R. M. Vossen, M. C. E. 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.
4. Borza, C. M., and L. M. Hutt-Fletcher. 2002. Alternate replication in B cells and epithelial cells switches tropism of Epstein-Barr virus. Nat. Med. 8:594-599.
5. Bowman, E. J., A. Siebers, and K. Altendorf. 1988. Bafilomycins: a class of inhibitors of membrane ATPases from microorganisms, animal cells, and plant cells. Proc. Natl. Acad. Sci. USA 85:7972-7976.
6. Britt, W. J., and C. A. Alford. 1996. Cytomegaloviruses, p. 2493-2523. In B. N. Fields, D. M. Knipe, and P. M. Howley (ed.), Fields virology, 3rd ed. Lippincott-Raven Press, Philadelphia, Pa.
7. Britt, W. J., M. Jarvis, J.-Y. Seo, D. Drummond, and J. Nelson. 2004. Rapid genetic engineering of human cytomegalovirus by using a lambda phage linear recombination system: demonstration that pp28 (UL99) is essential for production of infectious virus. J. Virol. 78:539-543.
8. Cai, W. H., 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.
9. Campadelli-Fiume, G., M. Arsenakis, F. Farabegoli, and B. Roizman. 1988. Entry of herpes simplex virus 1 in BJ cells that constitutively express viral glycoprotein D is by endocytosis and results in degradation of the virus. J. Virol. 62:159-167.
10. Cha, T.-A., E. Tom, G. W. Kemble, G. M. Duke, E. S. Mocarski, and R. R. Spaete. 1996. Human cytomegalovirus clinical isolates carry at least 19 genes not found in laboratory strains. J. Virol. 70:78-83.
11. 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.
12. Compton, T., D. M. Nowlin, and N. R. Cooper. 1993. Initiation of human cytomegalovirus infection requires initial interaction with cell surface heparan sulfate. Virology 193:834-841.
13. Dolan, A., C. Cunningham, R. D. Hector, A. F. Hassan-Walker, L. Lee, C. Addison, D. J. Dargan, D. J. McGeoch, D. Gatherer, V. C. Emery, P. D. Griffiths, C. Sinzger, B. P. McSharry, G. W. G. Wilkinson, and A. J. Davison. 2004. Genetic content of wild-type human cytomegalovirus. J. Gen. Virol. 85:1301-1312.
14. Feire, A. L., H. Koss, and T. Compton. 2004. Cellular integrins function as entry receptors for human cytomegalovirus via a highly conserved disintegrin-like domain. Proc. Natl. Acad. Sci. USA 101:15470-15475.
15. 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.
16. Gerna, G., F. Baldanti, and M. G. Revello. 2004. Pathogenesis of human cytomegalovirus infection and cellular targets. Hum. Immunol. 65:381-386.
17. Gerna, G., E. Percivalle, A. Sarasini, F. Baldanti, G. Campanini, and M. G. Revello. 2003. Rescue of human cytomegalovirus strain AD169 tropism for both leukocytes and human endothelial cells. J. Gen. Virol. 84:1431-1436.
18. Guinea, R., and L. Carrasco. 1995. Requirement for vacuolar proton-ATPase activity during entry of influenza virus into cells. J. Virol. 69:2306-2312.
19. Hahn, G., H. Khan, F. Baldanti, U. H. Koszinowski, M. G. Revello, and G. Gerna. 2002. The human cytomegalovirus ribonucleotide reductase homolog UL45 is dispensable for growth in endothelial cells, as determined by a BAC-cloned clinical isolate of human cytomegalovirus with preserved wild-type characteristics. J. Virol. 76:9551-9555.
20. Hahn, G., M. G. Revello, M. Patrone, E. Percivalle, G. Campanini, A. Sarasini, M. Wagner, A. Gallina, G. Milanesi, U. Koszinowski, F. Baldanti, and G. Gerna. 2004. Human cytomegalovirus UL131-128 genes are indispensable for virus growth in endothelial cells and virus transfer to leukocytes. J. Virol. 78:10023-10033.
21. Helenius, A., J. Kartenbeck, K. Simons, and E. Fries. 1980. On the entry of Semliki forest virus into BHK-21 cells. J. Cell Biol. 84:404-420.
22. Huber, M. T., R. Tomazin, T. Wisner, J. Boname, and D. C. Johnson. 2002. Human cytomegalovirus US7, US8, US9, and US10 are cytoplasmic glycoproteins, not found at cell surfaces, and US9 does not mediate cell-to-cell spread. J. Virol. 76:5748-5758.
23. Jarvis, M. A., C. E. Wang, H. L. Meyers, P. P. Smith, C. L. Corless, G. J. Henderson, J. Vieira, W. J. Britt, and J. A. Nelson. 1999. Human cytomegalovirus infection of Caco-2 cells occurs at the basolateral membrane and is differentiation state dependent. J. Virol. 73:4552-4560.
24. Johnson, D. C., and M. T. Huber. 2002. Directed egress of animal viruses promotes cell-to-cell spread. J. Virol. 76:1-8.
25. Johnson, D. C., and M. W. Ligas. 1988. Herpes simplex viruses lacking glycoprotein D are unable to inhibit virus penetration: quantitative evidence for virus-specific cell surface receptors. J. Virol. 62:4605-4612.
26. Johnson, D. C., M. Webb, T. W. Wisner, and C. Brunetti. 2002. Herpes simplex virus gE/gI sorts nascent virions to epithelial cell junctions, promoting virus spread. J. Virol. 75:821-833.
27. Lakadamyali, M., M. J. Rust, and X. Zhuang. 2004. Endocytosis of influenza viruses. Microbes Infect. 6:929-936.
28. Landolfo, S., M. Gariglio, G. Gribaudo, and D. Lembo. 2003. The human cytomegalovirus. Pharmacol. Ther. 98:269-297.
29. Lee, E. C., D. Yu, J. Martinez De Velasco, L. Tessarollo, D. A. Swing, D. L. Court, N. A. Jenkins, and N. G. Copeland. 2001. A highly efficient Escherichia coli-based chromosome engineering system adapted for recombinogenic targeting and subcloning of BAC DNA. Genomics 73:56-65.
30. Lentz, B. R., and J. K. Lee. 1999. Poly(ethylene glycol) (PEG)-mediated fusion between pure lipid bilayers: a mechanism in common with viral fusion and secretory vesicle release? Mol. Membr. Biol. 16:279-296.
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.
32. Matlin, K. S., H. Reggio, A. Helenius, and K. Simons. 1982. Pathway of vesicular stomatitis virus entry leading to infection. J. Mol. Biol. 156:609-631.
33. 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.
34. Milne, R. S. B., 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.
35. Murphy, E., D. Yu, J. Grimwood, J. Schmutz, M. Dickson, M. A. Jarvis, G. Hahn, J. A. Nelson, R. M. Myers, and T. E. Shenk. 2003. Coding potential of laboratory and clinical strains of human cytomegalovirus. Proc. Natl. Acad. Sci. USA 100:14976-14981.
36. 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.
37. 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.
38. 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.
39. Ogawa-Goto, K., K. Tanaka, W. Gibson, E. Moriishi, Y. Miura, T. Kurata, S. Irie, and T. Sata. 2003. Microtubule network facilitates nuclear targeting of human cytomegalovirus capsid. J. Virol. 77:8541-8547.
40. Patrone, M., M. Secchi, L. Fiorina, M. Ierardi, G. Milanesi, and A. Gallina. 2005. Human cytomegalovirus UL130 protein promotes endothelial cell infection through a producer cell modification of the virion. J. Virol. 79:8361-8373.
41. Peeters, B., J. Pol, A. Gielkens, and R. Moormann. 1993. Envelope glycoprotein gp50 of pseudorabies virus is essential for virus entry but is not required for viral spread in mice. J. Virol. 67:170-177.
42. Plachter, B., C. Sinzger, and G. Jahn. 1996. Cell types involved in replication and distribution of human cytomegalovirus. Adv. Virus Res. 46:195-261.
43. Prichard, M. N., M. E. Penfold, G. M. Duke, R. R. Spaete, and G. W. Kemble. 2001. A review of genetic differences between limited and extensively passaged human cytomegalovirus strains. Rev. Med. Virol. 11:191-200.
44. Rauch, D. A., N. Rodriguez, and R. J. Roller. 2000. Mutations in herpes simplex virus glycoprotein D distinguish entry of free virus from cell-cell spread. J. Virol. 74:11437-11446.
45. Rauh, I., and T. C. Mettenleiter. 1991. Pseudorabies virus glycoproteins g11 and gp50 are essential for virus penetration. J. Virol. 65:5348-5356.
46. S11-expressing cell line is resistant to herpes simplex virus infection at a step in viral entry mediated by glycoprotein D. J. Virol. 68:2830-2839.
47. 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.
48. 2) in virion infectivity. J. Virol. 29:1149-1158.
49. Scholz, M., H. W. Doerr, and J. Cinatl. 2003. Human cytomegalovirus retinitis: pathogenicity, immune evasion and persistence. Trends Microbiol. 11:171-178.
50. 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.
51. 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.
52. Sinzger, C., M. Kahl, K. Laib, K. Klingel, P. Rieger, B. Plachter, and G. Jahn. 2000. Tropism of human cytomegalovirus for endothelial cells is determined by a post-entry step dependent on efficient translocation to the nucleus. J. Gen. Virol. 81:3021-3035.
53. Slobbe-Van Drunen, M. E., A. T. Hendrickx, R. C. Vossen, E. J. Speel, M. C. Van Dam-Mieras, and C. A. Bruggeman. 1998. Nuclear import as a barrier to infection of human umbilical vein endothelial cells by human cytomegalovirus strain AD169. Virus Res. 56:149-156.
54. Smith, I. L., I. Taskintuna, F. M. Rahhal, H. C. Powell, E. Ai, A. J. Mueller, S. A. Spector, and W. R. Freeman. 1998. Clinical failure of CMV retinitis with intravitreal cidofovir is associated with antiviral resistance. Arch. Ophthalmol. 116:178-185.
55. Smith, M. S., G. L. Bentz, J. S. Alexander, and A. D. Yurochko. 2004. Human cytomegalovirus induces monocyte differentiation and migration as a strategy for dissemination and persistence. J. Virol. 78:4444-4453.
56. Spaderna, S., B. Kropff, Y. Ködel, S. Shen, S. Coley, S. Lu, W. Britt, and M. Mach. 2005. Deletion of gpUL132, a structural component of human cytomegalovirus, results in impaired virus replication in fibroblasts. J. Virol. 79:11837-11847.
57. Spear, P. G., and R. Longnecker. 2003. Herpesvirus entry: an update. J. Virol. 77:10179-10185.
58. Streblow, D. N., S. L. Orloff, and J. A. Nelson. 2001. Do pathogens accelerate atherosclerosis? J. Nutr. 131:2798S-2804S.
59. Varnum, S. M., D. N. Streblow, M. E. Monroe, P. Smith, K. J. Auberry, L. Paša-Tolić, D. Wang, D. G. Camp II, K. Rodland, S. Wiley, W. Britt, T. Shenk, R. D. Smith, and J. A. Nelson. 2004. Identification of proteins in human cytomegalovirus (HCMV) particles: the HCMV proteome. J. Virol. 78:10960-10966.
60. Wang, D., and T. Shenk. 2005. Human cytomegalovirus UL131 open reading frame is required for epithelial cell tropism. J. Virol. 79:10330-10338.
61. Wang, X., D. Y. Huang, S. M. Huong, and E. S. Huang. 2005. Integrin alphavbeta3 is a coreceptor for human cytomegalovirus. Nat. Med. 11:515-521.
62. Wang, X., S. M. Huong, M. L. Chiu, N. Raab-Traub, and E. S. Huang. 2003. Epidermal growth factor receptor is a cellular receptor for human cytomegalovirus. Nature 424:456-461.
63. 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.
64. Yoshimura, A., K. Kuroda, K. Kawasaki, S. Yamashina, T. Maeda, and S. Ohnishi. 1982. Infectious cell entry mechanism of influenza virus. J. Virol. 43:284-293.
65. Yu, D., H. M. Ellis, E. C. Lee, N. A. Jenkins, N. G. Copeland, and D. L. Court. 2000. An efficient recombination system for chromosome engineering in Escherichia coli. Proc. Natl. Acad. Sci. USA 97:5978-5983.
66. Zhou, Y. F., M. B. Leon, M. A. Waclawiw, J. J. Popma, Z. X. Yu, T. Finkel, and S. E. Epstein. 1996. Association between prior cytomegalovirus infection and the risk of restenosis after coronary atherectomy. N. Engl. J. Med. 335:624-630.