1887

Abstract

Human retinal pigment epithelial (RPE) cells, which are permissive for human cytomegalovirus (HCMV) replication, were used to evaluate virus infection from apical and basolateral membranes of polarized cells. Tests of HCMV infectivity showed that the apical membrane was 20–30-fold more susceptible to infection than the basolateral membrane; in contrast, both membranes were equally susceptible to infection by herpes simplex virus type 1 (HSV-1). Neutralizing monoclonal antibodies (MAbs) to HCMV glycoprotein B (gB) blocked penetration of virions into polarized RPE cells. This indicated that gB has a function in fusion of the virion envelope with the apical membrane of these cells, as it has with the cell membrane of unpolarized human fibroblasts. In contrast to HSV-1-infected RPE cells, the paracellular permeability of polarized RPE cells changed slowly following infection with HCMV. Confocal microscopy examination of HCMV-infected RPE cells revealed that the pattern of ZO-1 staining was altered at late times. Addition of gB-specific neutralizing MAbs to the apical and basolateral membranes of HCMV-infected RPE cells failed to inhibit plaque development; this indicated that progeny virions infect adjacent cells before disassembly of tight junctions and are sequestered from neutralization during spread across lateral cell membranes. The finding that progeny HCMV virions cross lateral cell membranes, which differ substantially in protein composition from apical membranes, suggests that polarized RPE cells contain multiple receptors for HCMV.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-77-1-61
1996-01-01
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/jgv/77/1/JV0770010061.html?itemId=/content/journal/jgv/10.1099/0022-1317-77-1-61&mimeType=html&fmt=ahah

References

  1. Andreoni M., Faircloth M., Vulgar L., Britt W. 1989; A rapid microneutralization assay for the measurement of neutralizing antibody reactive with human cytomegalovirus. Journal of Virological Methods 23:157–168
    [Google Scholar]
  2. Basgoz N., Qadri I., Navarro D., Sears A., Lennette E., Youngblom J., Pereira L. 1992; The amino terminus of human cytomegalovirus glycoprotein B contains epitopes that vary among strains. Journal of General Virology 73:983–988
    [Google Scholar]
  3. Bloom J. N., Palestine A. G. 1988; The diagnosis of cytomegalovirus retinitis. Annals of Internal Medicine 109:963–969
    [Google Scholar]
  4. Bok D., O’Day W., Rodriguez-Boulan E. 1992; Polarized budding of vesicular stomatitis and influenza virus from cultured human and bovine retinal pigment epithelium. Experimental Eye Research 55:853–860
    [Google Scholar]
  5. Caplan M. J., Anderson H. C., Pallade G. E., Jamieson J. D. 1986; Intracellular sorting and polarized cell surface delivery of (Na+, K+)ATPase, an endogenous component of MDCK cell basolateral plasma membranes. Cell 46:623–631
    [Google Scholar]
  6. Dondero D. V., Pereira L. 1990; Monoclonal antibody production. In Diagnostic Procedures for Viral, Rickettsial and Chlamydial Infections pp 101–124 Edited by Emmons R., Schmidt N. Washington, DC: American Public Health Association;
    [Google Scholar]
  7. Drew L. 1988; Cytomegalovirus infection in patients with AIDS. Journal of Infectious Diseases 158:449–456
    [Google Scholar]
  8. Dunn K. C., Aotaki-Keen A. E., Putkey F. R., Hjelmeland L. M. 1995; ARPE–19, a human retinal pigment epithelial cell line with differentiated properties. Experimental Eye Research (in press)
    [Google Scholar]
  9. Egbert P. R., Pollard R. B., Gallagher J. G., Merigan T. C. 1980; Cytomegalovirus retinitis in immunosuppressed hosts: ocular manifestations. Annals of Internal Medicine 93:664–670
    [Google Scholar]
  10. Ejercito P. M., Kieff E. D., Roizman B. 1968; Characterization of herpes simplex virus strains differing in their effects on social behaviour of infected cells. Journal of General Virology 2:357–364
    [Google Scholar]
  11. Fay M. T., Freeman W. R., Wiley C. A., Hardy D., Bozzette S. 1988; Atypical retinitis in patients with the acquired immunodeficiency syndrome. American Journal of Ophthalmology 105:483–490
    [Google Scholar]
  12. Furuse M., Hirase T., Itoh M., Nagafuchi A., Yonomura S., Tsukita S., Tsukita S. 1993; Occludin: a novel integral membrane protein localizing at tight junctions. Journal of Cell Biology 123:1777–1788
    [Google Scholar]
  13. Gumbiner B., Lowenkopf T., Apatira D. 1991; Identification of a 160-kDa polypeptide that binds to the tight junction protein ZO-1. Proceedings of the National Academy of Sciences, USA 88:3460–3464
    [Google Scholar]
  14. Gundersen D., Orlowski J., Rodriguez-Boulan E. 1991; Apical polarity of Na, K-ATPase in retinal pigment epithelium is linked to a reversal of the ankyrin-fodrin submembrane cytoskeleton. Journal of Cell Biology 112:863–872
    [Google Scholar]
  15. Gundersen D., Powell S. K., Rodriguez-Boulan E. 1993; Apical polarization of N-CAM in retinal pigment epithelium is dependent on contact with the neural retina. Journal of Cell Biology 121:335–343
    [Google Scholar]
  16. Holland G. N. 1994; AIDS: retinal and choroidal infections. In Medical and Surgical Retina; Advances, Controversies, and Management pp 415–433 Edited by Lewis H., Ryan S. J. St Louis: Mosby;
    [Google Scholar]
  17. Jabs D. A., Green W. R., Fox R., Polk B. F., Bartlett J. G. 1989; Ocular manifestations of acquired immune deficiency syndrome. Ophthalmology 96:1092–1099
    [Google Scholar]
  18. Kondo K., Kaneshima H., Mocarski E. S. 1994; Human cytomegalovirus latent infection of granulocyte-macrophage progenitors. Proceedings of the National Academy of Sciences, USA 91:11879–11883
    [Google Scholar]
  19. Lathey J. L., Spector S. A. 1991; Unrestricted replication of human cytomegalovirus in hydrocortisone-treated macrophages. Journal of Virology 65:6371–6375
    [Google Scholar]
  20. Lopez-Vancell R., Beaty G., Stefani E., Rodriguez-Boulan E. E., Cereijido M. 1984; Changes in the paracellular and cellular ionic permeabilities of monolayers of MDCK cells infected with influenza or vesicular stomatitis viruses. Journal of Membrane Biology 81:171–180
    [Google Scholar]
  21. Miceli M., Newsome D., Navak L., Beuerman R. 1989; Cytomegalovirus replication in cultured retinal pigment epithelial cells. Current Eye Research 8:835–839
    [Google Scholar]
  22. Miller S. S., Steinberg R. H., Oakley B. 1978; The electrogenic sodium pump of the frog retinal pigment epithelium. Journal of Membrane Biology 44:259
    [Google Scholar]
  23. Mocarski E. S., Pereira L., Michael N. 1985; Precise localization of genes on large animal virus genomes: use of λ gt 11 and monoclonal antibodies to map the gene for a cytomegalovirus protein family. Proceedings of the National Academy of Sciences, USA 82:1266–1270
    [Google Scholar]
  24. Mocarski E. S., Pereira L., McCormick A. L. 1988; Human cytomegalovirus ICP22, the product of the HWLF1 reading frame, is an early nuclear protein that is released from cells. Journal of General Virology 69:2613–2621
    [Google Scholar]
  25. Murphy–Erdosh C., Napolitano E. W., Reichardt L. F. 1994; The expression of B–cadherin during embryonic chick development. Developmental Biology 161:107–125
    [Google Scholar]
  26. Napolitano E. W., Venstrom K., Wheeler E. F., Reichardt L.E. 1991; Molecular cloning and characterization of B-cadherin, a novel chick cadherin. Journal of Cell Biology 113:893–905
    [Google Scholar]
  27. Navarro D., Paz P., Tugizov S., Topp K., La vail J., Pereira L. 1993; Glycoprotein B of human cytomegalovirus promotes virion penetration into cells, the transmission of infection from cell to cell, and fusion of infected cells. Virology 197:143–158
    [Google Scholar]
  28. Neill J. M., Barnstable C. J. 1990; Expression of the cell surface antigens RET-PE2 and N-CAM by rat retinal pigment epithelial cells during development and in tissue culture. Experimental Eye Research 51:573–583
    [Google Scholar]
  29. Ostwald T. J., Steinberg R. H. 1980; Localization of frog retinal pigment epithelium Na+-K+ ATPase. Experimental Eye Research 31:351
    [Google Scholar]
  30. Pepose J., Holland G., Nestor M., Cochran A., Foos R. 1985; Acquired immune deficiency syndrome: pathogenic mechanisms of ocular disease. Ophthalmology 92:472–484
    [Google Scholar]
  31. Pepose J. S., Newman C., Bach M. C., Quinn T. C., Ambinder R. F., Holland G., Hosstrom P. S., Frey H. M., Foos R. Y. 1987; Pathologic features of cytomegalovirus retinopathy after treatment with the antiviral agent ganciclovir. Ophthalmology 94:414–424
    [Google Scholar]
  32. Pereira L. 1994; Function of glycoprotein B homologues of the family herpesviridae . Infectious Agents and Disease 3:9–28
    [Google Scholar]
  33. Pereira L., Hoffman M., Gallo D., Cremer N. 1982; Monoclonal antibodies to human cytomegalovirus. I. Three cell surface proteins with unique immunologic and electrophoretic properties specify cross–reactive determinants. Infection and Immunity 36:924–932
    [Google Scholar]
  34. Pereira L., Hoffman M., Tatsuno M., Dondero D. 1984; Polymorphism of human cytomegalovirus glycoproteins characterized by monoclonal antibodies. Virology 139:73–86
    [Google Scholar]
  35. Pereira L., Basgoz N., Navarro D., Qadri L., Youngblom J., Sears A., Lennette E. 1991; Mapping conserved antigenic regions and strain-specific epitopes within the glycoprotein B gene of human cytomegalovirus. In Progress in Cytomegalovirus Research: Proceedings of the Third International Cytomegalovirus Workshop pp 195–198 Edited by Landini P. M. Amsterdam: Elsevier;
    [Google Scholar]
  36. Qadri L., Navarro D., Paz P., Pereira L. 1992; Assembly of conformation-dependent neutralizing domains on glycoprotein B of human cytomegalovirus. Journal of General Virology 73:2913–2921
    [Google Scholar]
  37. Rodriguez-Boulan E., Sabatini D. D. 1978; Asymmetric budding of viruses in epithelial cell monolayers: a model system for study of epithelial cell polarity. Proceedings of the National Academy of Sciences, USA 75:5071–5075
    [Google Scholar]
  38. Rodriguez-Boulan E., Pendergast M. 1980; Polarized dis-tribution of viral envelope proteins in the plasma membrane of infected epithelial cells. Cell 20:45–54
    [Google Scholar]
  39. Sears A. E., McGwire B. S., Roizman B. 1991; Infection of polarized MDCK cells with herpes simplex virus 1: two asymmetrically distributed cell receptors interact with different viral proteins. Proceedings of the National Academy of Sciences, USA 88:5087–5091
    [Google Scholar]
  40. Shyjan A. W., Lbvbnson R. 1989; Antisera specific for the αl, α2, α3, and β subunits of the Na, K–ATPase: differential expression of α and β subunits in rat tissue membranes. Biochemistry 28:4531–4535
    [Google Scholar]
  41. Simons K., Fuller S. D. 1985; Cell surface polarity in epithelia. Annual Review of Cell Biology 1:243–288
    [Google Scholar]
  42. Spear P. G. 1993; Membrane fusion induced by herpes simplex virus. In Viral Fusion Mechanisms pp 201–232 Edited by Bentz J. Boca Raton: CRC Press;
    [Google Scholar]
  43. Stevenson B. R., Siliciano J. D., Mooseker M. S., Goodenough D. A. 1986; Identification of ZO–1: a high molecular weight polypeptide associated with the tight junction (zonula occludens) in a variety of epithelia. Journal of Cell Biology 103:755–766
    [Google Scholar]
  44. Svensson L., Finlay B. B., Bass D., von Bonsdorff C.-H., Greenberg H. B. 1991; Symmetric infection of rotavirus on polarized human intestinal epithelial (Caco-2) cells. Journal of Virology 65:4190–4197
    [Google Scholar]
  45. Tanaka J., Ogura T., Kamiya S., Sato H., Yoshie T., Ogura H., Hatano M. 1984; Enhanced replication of human cytomegalovirus in human fibroblasts treated with dexamethasone. Journal of General Virology 65:1759–1767
    [Google Scholar]
  46. Taylor–Weideman J., Sissons J. G. P., Borysiewicz L. K., Sinclair J. H. 1991; Monocytes are a major site of persistence of human cytomegalovirus in peripheral blood mononuclear cells. Journal of General Virology 72:2059–2064
    [Google Scholar]
  47. Tugizov S., Navarro D., Paz P., Wang Y., Qadri I., Pereira L. 1994; Function of human cytomegalovirus glycoprotein B: syncytium formation in cells constitutively expressing gB is blocked by virus-neutralizing antibodies. Virology 201:263–276
    [Google Scholar]
  48. Zettl K. S., Sjaastad M. D., Riskin P. M., Parry G., Machen T. E., Firestone G. L. 1992; Glucocorticoid-induced formation of tight junctions in mouse mammary epithelial cells in vitro . Proceedings of the National Academy of Sciences, USA 89:9069–9073
    [Google Scholar]
  49. Zinn K. M., Benjamin-Henkind J. V. 1979; Anatomy of the human retinal pigment epithelium. In The Retinal Pigment Epithelium pp 3–31 Edited by Zinn K., Marmor M. Cambridge: Harvard University Press;
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-77-1-61
Loading
/content/journal/jgv/10.1099/0022-1317-77-1-61
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error