A novel human cytomegalovirus glycoprotein, gpUS9, which promotes cell- to-cell spread in polarized epithelial cells, colocalizes with the cytoskeletal proteins E-cadherin and F-actin

Journal of Virology

Volumn 72, Issue 7, 1998, Pages 5717-5727

  Maidji, Ekaterina ^a   Tugizov, Sharof ^a   Abenes, Gerardo ^a   Jones, Thomas ^b   Pereira, Lenore ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b PFIZER INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOSKELETON PROTEIN; F ACTIN; GLYCOPROTEIN US9; TRITON X 100; UNCLASSIFIED DRUG; UVOMORULIN; VIRUS GLYCOPROTEIN;

ANIMAL CELL; ARTICLE; CELL JUNCTION; CELL STRAIN; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOSKELETON; ENDOPLASMIC RETICULUM; EPITHELIUM CELL; GOLGI COMPLEX; HUMAN CYTOMEGALOVIRUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SOLUBILITY; VIRUS INFECTIVITY;

EID: 0031777958     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.72.7.5717-5727.1998     Document Type: Article

References (60)

1. Ahn, K., A. Gruhler, B. Galocha, T. R. Jones, E. J. Wiertz, H. L. Ploegh, P. A. Peterson, Y. Yang, and K. Fruh. 1997. The ER-luminal domain of the HCMV glycoprotein US6 inhibits peptide translocation by TAP. Immunity 6:613-621.
2. Anderson, J. M., B. R. Stevenson, A. Jesaitis, D. A. Goodenough, and M. S. Mooseker. 1988. Characterisation of ZO-1, a protein component of the tight junction from mouse liver and Madin-Darby canine kidney cells. J. Cell Biol. 106:1141-1149.
3. Balan, P., P. N. Davis, S. Bell, H. Atkinson, H. Browne, and T. Minson. 1994. An analysis of the in vitro and in vivo phenotypes of mutants of herpes simplex virus type 1 lacking glycoproteins gG, gE, gI or the putative gJ. J. Gen. Virol. 75:1245-1258.
4. Baldick, C. J., Jr., and T. Shenk. 1996. Proteins associated with purified human cytomegalovirus particles. J. Virol. 70:6097-6105.
5. Bockholt, S. M., C. A. Otey, J. R. Glenney, and K. Burridge. 1992. Localization of a 215-kDa tyrosine-phosphorylated protein that cross-reacts with tensin antibodies. Exp. Cell Res. 203:39-46.
6. Bowen, E. F., P. Wilson, A. Cope, C. Sabin, P. Griffiths, C. Davey, M. Johnson, and V. Emery. 1996. Cytomegalovirus retinitis in AIDS patients: influence of cytomegaloviral load on response to ganciclovir, time to recurrence and survival. AIDS 10:1515-1520.
7. 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. Lippincott-Raven, Philadelphia, Pa.
8. 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.
9. Chee, M. S., A. T. Bankier, S. Beck, R. Bohni, C. M. Brown, R. Cerny, T. Horsnell, C. A. Hutchison, T. Kouzarides, J. A. Martignetti, E. Preddie, S. C. Satchwell, P. Tomlinson, K. M. Weston, and B. G. Barrell. 1990. Analysis of the protein-coding content of the sequence of human cytomegalovirus strain AD169. Curr. Top. Microbiol. Immunol. 154:125-170.
10. Cohen, G. H., B. Dietzschold, M. Ponce de Leon, D. Long, E. Golub, A. Varrichio, L. Pereira, and R. J. Eisenberg. 1984. Localization and synthesis of an antigenic determinant of herpes simplex virus glycoprotein D that stimulates the production of neutralizing antibody. J. Virol. 49:102-108.
11. Coskuncan, N. M., D. A. Jabs, J. P. Dunn, J. A. Haller, W. R. Green, G. B. Vogelsang, and G. W. Santos. 1994. The eye in bone marrow transplantation. VI. Retinal complications. Arch. Ophthalmol. 112:372-379.
12. Cudmore, S., I. Reckmann, and M. Way. 1997. Viral manipulations of the actin cytoskeleton. Trends Microbiol. 5:142-148.
13. Davis, S., M. L. Lu, S. H. Lo, S. Lin, J. A. Butler, B. J. Druker, T. M. Roberts, Q. An, and L. B. Chen. 1991. Presence of an SH2 domain in the actin-binding protein tensin. Science 252:712-715.
14. Dingwell, K. S., C. R. Brunetti, R. L. Hendricks, Q. Tang, M. Tang, A. J. Rainbow, and D. C. Johnson. 1994. Herpes simplex virus glycoproteins E and I facilitate cell-to-cell spread in vivo and across junctions of cultured cells. J. Virol. 68:834-845.
15. Drew, L. 1988. Cytomegalovirus infection in patients with AIDS. J. Infect. Dis. 158:449-456.
16. Dunn, K. C., K. A. Aotaki, F. R. Putkey, and L. M. Hjelmeland. 1996. ARPE-19, a human retinal pigment epithelial cell line with differentiated properties. Exp. Eye Res. 62:155-169.
17. Furuse, M., T. Hirase, M. Itoh, A. Nagafuchi, S. Yonemura, S. Tsukita, and S. Tsukita. 1993. Occludin: a novel integral membrane protein localizing at tight junctions. J. Cell Biol. 123:1777-1788.
18. Furuse, M., M. Itoh, T. Hirase, A. Nagafuchi, S. Yonemura, S. Tsukita, and S. Tsukita. 1994. Direct association of occludin with ZO-1 and its possible involvement in the localization of occludin at tight junctions. J. Cell Biol. 127:1617-1626.
19. Geiger, B., and O. Ayalon. 1992. Cadherins. Annu. Rev. Cell Biol. 8:307-332.
20. Gumbiner, B. 1987. Structure, biochemistry, and assembly of epithelial tight junctions. Am. J. Physiol. 253:C749-C758.
21. Gumbiner, B., T. Lowenkopf, and D. Apatira. 1991. Identification of a 160-kDa polypeptide that binds to the tight junction protein ZO-1. Proc. Natl. Acad. Sci. USA 88:3460-3464.
22. Gumbiner, B. M. 1993. Breaking through the tight junction barrier. J. Cell Biol. 123:1631-1633.
23. Gumbiner, B. M. 1996. Cell adhesion: the molecular basis of tissue architecture and morphogenesis. Cell 84:345-357.
24. Holland, G. N. 1994. AIDS: retinal and choroidal infections, p. 415-433. In H. Lewis and S. J. Ryan (ed.), Medical and surgical retina: advances, controversies, and management. Mosby, St. Louis, Mo.
25. Hubenthal-Voss, J., R. A. Houghten, L. Pereira, and B. Roizman. 1988. Mapping of functional and antigenic domains of the α4 protein of herpes simplex virus 1. J. Virol. 62:454-462.
26. Jabs, D. A. 1995. Ocular manifestations of HIV infection. Trans. Am. Ophthalmol. Soc. 93:623-683.
27. Jabs, D. A., J. P. Dunn, C. Enger, M. Forman, N. Bressler, and P. Charache. 1996. Cytomegalovirus retinitis and viral resistance. Prevalence of resistance at diagnosis, 1994. Cytomegalovirus Retinitis and Viral Resistance Study Group. Arch. Ophthalmol. 114:809-814.
28. Jones, N. L., J. C. Lewis, and B. A. Kilpatrick. 1986. Cytoskeletal disruption during human cytomegalovirus infection of human lung fibroblasts. Eur. J. Cell Biol. 41:304-312.
29. Jones, T. R., L. K. Hanson, L. Sun, J. S. Slater, R. M. Stenberg, and A. E. Campbell. 1995. Multiple independent loci within the human cytomegalovirus unique short region down-regulate expression of major histocompatibility complex class I heavy chains. J. Virol. 69:4830-4841.
30. Jones, T. R., and V. P. Muzithras. 1991. Fine mapping of transcripts expressed from the US6 gene family of human cytomegalovirus strain AD169. J. Virol. 65:2024-2036.
31. Jones, T. R., and V. P. Muzithras. 1992. A cluster of dispensable genes within the human cytomegalovirus genome short component: IRS1, US1 through US5, and the US6 family. J. Virol. 66:2541-2546.
32. Jones, T. R., V. P. Muzithras, and Y. Gluzman. 1991. Replacement mutagenesis of the human cytomegalovirus genome: US10 and US11 gene products are nonessential. J. Virol. 65:5860-5872.
33. Jones, T. R., and L. Sun. 1997. Human cytomegalovirus US2 destabilizes major histocompatibility complex class I heavy chains. J. Virol. 71:2970-2979.
34. Jones, T. R., E. J. Wiertz, L. Sun, K. N. Fish, J. A. Nelson, and H. L. Ploegh. 1996. Human cytomegalovirus US3 impairs transport and maturation of major histocompatibility complex class I heavy chains. Proc. Natl. Acad. Sci. USA 93:11327-11333.
35. Kondo, K., H. Kaneshima, and E. S. Mocarski. 1994. Human cytomegalovirus latent infection of granulocyte-macrophage progenitors. Proc. Natl. Acad. Sci. USA 91:11879-11883.
36. LaFemina, R. L., and G. S. Hayward. 1980. Structural organization of the DNA molecules from human cytomegalovirus, p. 39-55. In B. N. Fields, R. Jaenisch, and C. F. Fox (ed.), Animal virus genetics. Academic Press, New York, N.Y.
37. Lo, S. H., E. Weisberg, and L. B. Chen. 1994. Tensin: a potential link between the cytoskeleton and signal transduction. Bioessays 16:817-823.
38. Machold, R. P., E. J. Wiertz, T. R. Jones, and H. L. Ploegh. 1997. The HCMV gene products US11 and US2 differ in their ability to attack allelic forms of murine major histocompatibility complex (MHC) class I heavy chains. J. Exp. Med. 185:363-366.
39. Maidji, E., S. Tugizov, T. Jones, Z. Zheng, and L. Pereira. 1996. Accessory human cytomegalovirus glycoprotein US9 in the unique short component of the viral genome promotes cell-to-cell transmission of virus in polarized epithelial cells. J. Virol. 70:8402-8410.
40. Mays, R. W., K. A. Beck, and W. J. Nelson. 1994. Organization and function of the cytoskeleton in polarized epithelial cells: a component of the protein sorting machinery. Curr. Opin. Cell Biol. 6:16-24.
41. Mocarski, E. S. 1996. Cytomegaloviruses and their replication, p. 2447-2492. In B. N. Fields, D. M. Knipe, and P. M. Howley (ed.), Fields virology. Lippincott-Raven, Philadelphia, Pa.
42. Mostov, K. E. 1995. Regulation of protein traffic in polarized epithelial cells. Histol. Histopathol. 10:423-431.
43. Nathke, I. S., L. Hinck, J. R. Swedlow, J. Papkoff, and W. J. Nelson. 1994. Defining interactions and distributions of cadherin and catenin complexes in polarized epithelial cells. J. Cell Biol. 125:1341-1352.
44. Nusrat, A., M. Giry, J. R. Turner, S. P. Colgan, C. A. Parkos, D. Carnes, E. Lemichez, P. Boquet, and J. L. Madara. 1995. Rho protein regulates tight junctions and perijunctional actin organization in polarized epithelia. Proc. Natl. Acad. Sci. USA 92:10629-10633.
45. Pereira, L., E. Maidji, S. Tugizov, and T. Jones. 1995. Deletion mutants in human cytomegalovirus glycoprotein US9 are impaired in cell-cell transmission and in altering tight junctions of polarized human retinal pigment epithelial cells. Scand. J. Infect. Dis. Suppl. 99:82-87.
46. Rodriguez-Boulan, E., and S. K. Powell. 1992. Polarity of epithelial and neuronal cells. Annu. Rev. Cell Biol. 8:395-427.
47. Sargiacomo, M., M. Sudol, Z. Tang, and M. P. Lisanti. 1993. Signal transducing molecules and glycosyl-phosphatidylinositol-linked proteins form a caveolin-rich insoluble complex in MDCK cells. J. Cell Biol. 122:789-807.
48. Soderberg-Naucler, C., K. N. Fish, and J. A. Nelson. 1997. Reactivation of latent human cytomegalovirus by allogeneic stimulation of blood cells from healthy donors. Cell 91:119-126.
49. Spaete, R. R., R. C. Gehrz, and M. P. Landini. 1994. Human cytomegalovirus structural proteins. J. Gen. Virol. 75:3287-3308.
50. Takeichi, M. 1991. Cadherin cell adhesion receptors as a morphogenetic regulator. Science 251:1451-1455.
51. Taylor-Weideman, J. A., J. G. P. Sissons, L. K. Borysiewicz, and J. H. Sinclair. 1991. Monocytes are a major site of persistence of human cytomegalovirus in peripheral blood mononuclear cells. J. Gen. Virol. 72:2059-2064.
52. Theriot, J. A. 1995. The cell biology of infection by intracellular bacterial pathogens. Annu. Rev. Cell Dev. Biol. 11:213-239.
53. Tsukita, S., S. Tsukita, A. Nagafuchi, and S. Yonemura. 1992. Molecular linkage between cadherins and actin filaments in cell-cell adherens junctions. Curr. Opin. Cell Biol. 4:834-839.
54. Tugizov, S., E. Maidji, and L. Pereira. Unpublished observation.
55. Tugizov, S., E. Maidji, and L. Pereira. 1996. Role of apical and basolateral membranes in replication of human cytomegalovirus in polarized retinal pigment epithelial cells. J. Gen. Virol. 77:61-74.
56. Tugizov, S., D. Navarro, P. Paz, Y. Wang, I. Qadri, and L. Pereira. 1994. Function of human cytomegalovirus glycoprotein B: syncytium formation in cells constitutively expressing gB is blocked by virus-neutralizing antibodies. Virology 201:263-276.
57. Turner, C. E., and K. Burridge. 1991. Transmembrane molecular assemblies in cell-extracellular matrix interactions. Curr. Opin. Cell Biol. 3:849-853.
58. van der Meer, J., W. L. Drew, R. A. Bowden, G. J. Galasso, P. D. Griffiths, D. A. Jabs, C. Katlama, S. A. Spector, and R. J. Whitley. 1996. Summary of the International Consensus Symposium on Advances in the Diagnosis, Treatment and Prophylaxis of Cytomegalovirus Infection. Antivir. Res. 32: 119-140.
59. Wiertz, E. J., T. R. Jones, L. Sun, M. Bogyo, H. J. Geuze, and H. L. Ploegh. 1996. The human cytomegalovirus US11 gene product dislocates MHC class I heavy chains from the endoplasmic reticulum to the cytosol. Cell 84:769-779.
60. Wiertz, E. J., D. Tortorella, M. Bogyo, J. Yu, W. Mothes, T. R. Jones, T. A. Rapoport, and H. L. Ploegh. 1996. Sec61-mediated transfer of a membrane protein from the endoplasmic reticulum to the proteasome for destruction. Nature 384:432-438.