Human cytomegalovirus UL130 protein promotes endothelial cell infection through a producer cell modification of the virion

Journal of Virology

Volumn 79, Issue 13, 2005, Pages 8361-8373

  Patrone, Marco ^a,c   Secchi, Massimiliano ^a,c   Fiorina, Loretta ^a,c   Ierardi, Mariagrazia ^b   Milanesi, Gabriele ^a,c   Gallina, Andrea ^a,c  

^a UNIVERSITY OF MILAN   (Italy)

^b SAN PAOLO HOSPITAL   (Italy)

^c CNR   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

GENE PRODUCT; GLYCOPROTEIN; RETROVIRUS VECTOR; UL130 PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ARTICLE; CELL LINE; CONTROLLED STUDY; EMBRYO; ENDOTHELIUM CELL; GENE LOCUS; GENETIC COMPLEMENTATION; GOLGI COMPLEX; HUMAN; HUMAN CELL; HUMAN CYTOMEGALOVIRUS; LUNG FIBROBLAST; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; VIRION; VIROGENESIS; VIRUS CELL INTERACTION; VIRUS ENVELOPE; VIRUS INFECTION; VIRUS INFECTIVITY; VIRUS MUTANT; VIRUS PLAQUE; VIRUS PURIFICATION;

AMINO ACID SEQUENCE; BASE SEQUENCE; CYTOMEGALOVIRUS; ENDOTHELIUM, VASCULAR; HELA CELLS; HUMANS; MEMBRANE GLYCOPROTEINS; MOLECULAR SEQUENCE DATA; RESTRICTION MAPPING; VIRAL ENVELOPE PROTEINS; VIRAL PROTEINS; VIRION;

HUMAN HERPESVIRUS 5;

EID: 20744438485     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.79.13.8361-8373.2005     Document Type: Article

References (48)

1. Akter, P., C. Cunningham, B. P. McSharry, A. Dolan, C. Addison, D. J. Dargan, A. F. Hassan-Walker, V. C. Emery, P. D. Griffiths, G. W. Wilkinson, and A. J. Davison. 2003. Two novel spliced genes in human cytomegalovirus. J. Gen. Virol. 84:1117-1122.
2. Bason, C., R. Corrocher, C. Lunardi, P. Puccetti, O. Olivieri, D. Girelli, R. Navone, R. Beri, E. Millo, A. Margonato, N. Martinelli, and A. Puccetti. 2003. Interaction of antibodies against cytomegalovirus with heat-shock protein 60 in pathogenesis of atherosclerosis. Lancet 362:1971-1977.
3. Bolovan-Fritts, C., and J. A. Wiedeman. 2001. Human cytomegalovirus strain Toledo lacks a virus-encoded tropism factor required for infection of aortic endothelial cells. J. Infect. Dis. 184:1252-1261.
4. Bolovan-Fritts, C. A., and J. A. Wiedeman. 2002. Mapping the viral genetic determinants of endothelial cell tropism in human cytomegalovirus. J. Clin. Virol. 25:S97-S109.
5. Britt, W. J., and C. A. Alford. 1996. Cytomegalovirus, p. 2493-2523. In B. N. Fields, D. M. Knipe, and P. M. Howley (ed.), Fields virology, 3rd ed. Lippincott-Raven, Philadelphia, Pa.
6. Brune, W., C. Menard, J. Heesemann, and U. H. Koszinowski. 2001. A ribonucleotide reductase homolog of cytomegalovirus and endothelial cell tropism. Science 291:303-305.
7. 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. Wilkinson, and A. J. Davison. 2004. Genetic content of wild-type human cytomegalovirus. J. Gen. Virol. 85:1301-1312.
8. Dunn, W., C. Chou, H. Li, R. Hai, D. Patterson, V. Stolc, H. Zhu, and F. Liu. 2003. Functional profiling of a human cytomegalovirus genome. Proc. Natl. Acad. Sci. USA 100:14223-14228.
9. Fish, K. N., C. Soderberg-Naucler, L. K. Mills, S. Stenglein, and J. A. Nelson. 1998. Human cytomegalovirus persistently infects aortic endothelial cells. J. Virol. 72:5661-5668.
10. Gallina, A., L. Simoncini, S. Garbelli, E. Percivalle, G. Pedrali-Noy, K. S. Lee, R. L. Erikson, B. Plachter, G. Gerna, and G. Milanesi. 1999. Polo-like kinase 1 as a target for human cytomegalovirus pp65 lower matrix protein. J. Virol. 73:1468-1478.
11. Gerna, G., E. Percivalle, F. Baldanti, S. Sozzani, P. Lanzarini, E. Genini, D. Lilleri, and M. G. Revello. 2000. Human cytomegalovirus replicates abortively in polymorphonuclear leukocytes after transfer from infected endothelial cells via transient microfusion events. J. Virol. 74:5629-5638.
12. Gerna, G., E. Percivalle, A. Sarasini, F. Baldanti, and M. G. Revello. 2002. The attenuated Towne strain of human cytomegalovirus may revert to both endothelial cell tropism and leuko- (neutrophil- and monocyte-) tropism in vitro. J. Gen. Virol. 83:1993-2000.
13. Goff, S. P. 2003. Death by deamination: a novel host restriction system for HIV-1. Cell 114:281-283.
14. Grundy, J. E., K. M. Lawson, L. P. MacCormac, J. M. Fletcher, and K. L. Yong. 1998. Cytomegalovirus-infected endothelial cells recruit neutrophils by the secretion of C-X-C chemokines and transmit virus by direct neutrophil-endothelial cell contact and during neutrophil transendothelial migration. J. Infect. Dis. 177:1465-1474.
15. 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.
16. Hahn, G., M. G. Revello, M. Patrone, E. Percivalle, E. Campanini, A. Sarasini, A. Wagner, A. Gallina, G. Milanesi, U. Koszinowski, and F. Baldanti. 2004. Human cytomegalovirus UL131-128 genes are indispensable for virus growth in endothelial cells and virus transfer to leukocytes. J. Virol. 78:10023-10033.
17. Halary, F., A. Amara, H. Lortat-Jacob, M. Messerle, T. Delaunay, C. Houles, F. Fieschi, F. Arenzana-Seisdedos, J. F. Moreau, and J. Dechanet-Merville. 2002. Human cytomegalovirus binding to DC-SIGN is required for dendritic cell infection and target cell trans-infection. Immunity 17:653-664.
18. Hanson, L. K., J. S. Slater, Z. Karabekian, G. Ciocco-Schmitt, and A. E. Campbell. 2001. Products of US22 genes M140 and M141 confer efficient replication of murine cytomegalovirus in macrophages and spleen. J. Virol. 75:6292-6302.
19. Hengel, H., and C. Weber. 2000. Driving cells into atherosclerotic lesions - a deleterious role for viral chemokine receptors? Trends Microbiol. 8:294-296.
20. Jarvis, M. A., and J. A. Nelson. 2002. Human cytomegalovirus persistence and latency in endothelial cells and macrophages. Curr. Opin. Microbiol. 5:403-407.
21. 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.
22. Kahl, M., D. Siegel-Axel, S. Stenglein, G. Jahn, and C. Sinzger. 2000. Efficient lytic infection of human arterial endothelial cells by human cytomegalovirus strains. J. Virol. 74:7628-7635.
23. Knight, D. A., W. J. Waldman, and D. D. Sedmak. 1999. Cytomegalovirus-mediated modulation of adhesion molecule expression by human arterial and microvascular endothelial cells. Transplantation 68:1814-1818.
24. Lai, L., and W. J. Britt. 2003. The interaction between the major capsid protein and the smallest capsid protein of human cytomegalovirus is dependent on two linear sequences in the smallest capsid protein. J. Virol. 77: 2730-2735.
25. Maidji, E., E. Percivalle, G. Gerna, S. Fisher, and L. Pereira. 2002. Transmission of human cytomegalovirus from infected uterine microvascular endothelial cells to differentiating/invasive placental cytotrophoblasts. Virology 304:53-69.
26. McCracken, A. A., and J. L. Brodsky. 2003. Evolving questions and paradigm shifts in endoplasmic-reticulum-associated degradation (ERAD). Bioessays 25:868-877.
27. 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.
28. Murphy, J. C., W. Fischle, E. Verdin, and J. H. Sinclair. 2002. Control of cytomegalovirus lytic gene expression by histone acetylation. EMBO J. 21: 1112-1120.
29. Novotny, J., I. Rigoutsos, D. Coleman, and T. Shenk. 2001. In silico structural and functional analysis of the human cytomegalovirus (HHV5) genome. J. Mol. Biol. 310:1151-1166.
30. Patrone, M., E. Percivalle, M. Secchi, L. Fiorina, G. Pedrali-Noy, M. Zoppe, F. Baldanti, G. Hahn, U. H. Koszinowski, G. Milanesi, and A. Gallina. 2003. The human cytomegalovirus UL45 gene product is a late, virion-associated protein and influences virus growth at low multiplicities of infection, J. Gen. Virol. 84:3359-3370.
31. Pelham, H. R. 1996. The dynamic organisation of the secretory pathway. Cell Struct. Funct. 21:413-419.
32. Percivalle, E., M. G. Revello, L. Vago, F. Morini, and G. Gerna. 1993. Circulating endothelial giant cells permissive for human cytomegalovirus (HCMV.) are detected in disseminated HCMV infections with organ involvement. J. Clin. Investig. 92:663-670.
33. Revello, M. G., E. Percivalle, A. Di Matteo, F. Morini, and G. Gerna. 1992. Nuclear expression of the lower matrix protein of human cytomegalovirus in peripheral blood leukocytes of immunocompromised viraemic patients. J. Gen. Virol. 73:437-442.
34. Revello, M. G., E. Percivalle, E. Arbustini, R. Pardi, S. Sozzani, and G. Gerna. 1998. In vitro generation of human cytomegalovirus pp65 antigenemia, viremia, and leukoDNAemia. J. Clin. Investig. 101:2686-2692.
35. Revello, M. G., F. Baldanti, E. Percivalle, A. Sarasini, L. De-Giuli, E. Genini, D. Lilleri, N. Labò, and G. Gerna. 2001. In vitro selection of human cytomegalovirus variants unable to transfer virus and virus products from infected cells to polymorphonuclear leukocytes and to grow in endothelial cells. J. Gen. Virol. 82:1429-1438.
36. 35a. Rue, C. A., M. A. Jarvis, A. J. Knoche, H. L. Meyers, V. R. DeFilippis, S. G. Hansen, M. Wagner, K. Fruh, D. G. Anders, S. W. Wong, P. A. Barry, and J. A. Nelson. 2004. A cyclooxygenase-2 homologue encoded by rhesus cytomegalovirus is a determinant for endothelial cell tropism. J. Virol. 78:12529-12536.
37. Schiavoni, I., S. Trapp, A. C. Santarcangelo, V. Piacentini, K. Pugliese, A. Baur, and M. Federico. 2004. HIV-1 Nef enhances both membrane expression and virion incorporation of Env products. A model for the Nef-dependent increase of HIV-1 infectivity. J. Biol. Chem. 279:22996-23006.
38. Shen, Y. H., B. Utama, J. Wang, M. Raveendran, D. Senthil, W. J. Waldman, J. D. Belcher, G. Vercellotti, D. Martin, B. M. Mitchelle, and X. L. Wang, 2004. Human cytomegalovirus causes endothelial injury through the ataxia telangiectasia mutant and p53 DNA damage signaling pathways. Circ. Res. 94:1310-1317.
39. Sinzger, C., A. Grefte, B. Plachter, A. S. Gouw, T. H. The, and G. Jahn. 1995. Fibroblasts, epithelial cells, endothelial cells and smooth muscle cells are major targets of human cytomegalovirus infection in lung and gastrointestinal tissues. J. Gen. Virol. 76:741-750.
40. 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.
41. Sinzger, C., K. Schmidt, J. Knapp, M. Kahl, R. Beck, J. Waldman, H. Hebart, H. Einsele, and G. Jahn. 1999. Modification of human cytomegalovirus tropism through propagation in vitro is associated with changes in the viral genome. J. Gen. Virol. 80:2867-2877.
42. 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.
43. Somia, N. V., H. Miyoshi, M. J. Schmitt, and I. M. Verma. 2000. Retroviral vector targeting to human immunodeficiency virus type 1-infected cells by receptor pseudotyping. J. Virol. 74:4420-4424.
44. Trombetta, E. S., and A. J. Parodi. 2003. Quality control and protein folding in the secretory pathway. Annu. Rev. Cell Dev. Biol. 19:649-676.
45. Waldman, W. J., D. A. Knight, E. H. Huang, and D. D. Sedmak. 1995. Bidirectional transmission of infectious cytomegalovirus between monocytes and vascular endothelial cells: an in vitro model. J. Infect. Dis. 171:263-272.
46. 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.
47. Weis, M., T. N. Kledal, K. Y. Lin, S. N. Panchal, S. Z. Gao, H. A. Valantine, E. S. Mocarski, and J. P. Cooke. 2004. Cytomegalovirus infection impairs the nitric oxide synthase pathway: role of asymmetric dimethylarginine in transplant arteriosclerosis. Circulation 109:500-505.
48. Yamamoto-Tabata, T., S. McDonagh, H. T. Chang, S. Fisher, and L. Pereira. 2004. Human cytomegalovirus interleukin-10 downregulates metalloproteinase activity and impairs endothelial cell migration and placental cytotrophoblast invasiveness in vitro. J. Virol. 78:2831-2840.