1887

Abstract

Mucosal epithelia are invaded from the apical surface during a primary infection by herpes simplex virus type 1 (HSV-1). HSV-1 progeny virus, synthesized from latently infected peripheral neurons that innervate such epithelia, reinfects the epithelia most likely from the basolateral surface. The epithelial cell lines MDCK and Caco-2 can be induced to differentiate into polarized cells with distinct apical and plasma membrane domains separated by tight junctions if they are cultured on porous membrane filters. Our data using these culture systems showed that highly polarized epithelial cells were not susceptible to apical HSV-1 infection. However, HSV-1 infected these cells if added from the basolateral surface or if a depletion of extracellular Ca had weakened the strength of the cell–cell contacts. Basolateral infection and apical infection after the Ca switch required an intact microtubule network for genome targeting to the nucleus. This system can be used to identify the microtubule motors that HSV-1 uses during virus entry in polarized epithelial cells.

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2004-04-01
2019-11-14
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References

  1. Balcarova-Stander, J., Pfeiffer, S., Fuller, S. & Simons, K. ( 1984; ). Development of cell surface polarity in the epithelial Madin–Darby canine kidney (MDCK) cell line. EMBO J 3, 2687–2694.
    [Google Scholar]
  2. Caplan, M., Stow, J., Newman, A., Madri, J., Anderson, H., Farquhar, M., Palade, G. & Jamieson, J. ( 1987; ). Dependence of pH of polarized sorting of secreted proteins. Nature 329, 632–635.[CrossRef]
    [Google Scholar]
  3. Compans, R. W. ( 1995; ). Virus entry and release in polarized epithelial cells. Curr Top Microbiol Immunol 202, 209–219.
    [Google Scholar]
  4. Döhner, K. & Sodeik, B. ( 2004; ). The role of the cytoskeleton during viral infection. Curr Top Microbiol Immunol 285 (in press).
    [Google Scholar]
  5. Döhner, K., Wolfstein, A., Prank, U., Echeverri, C., Dujardin, D., Vallee, R. & Sodeik, B. ( 2002; ). Function of dynein and dynactin in herpes simplex virus capsid transport. Mol Biol Cell 13, 2795–2809.[CrossRef]
    [Google Scholar]
  6. Eilers, U., Klumpermann, J. & Hauri, H. P. ( 1989; ). Nocodazole, a microtubule-active drug, interferes with apical protein delivery in cultured intestinal epithelial cells (Caco-2). J Cell Biol 108, 13–22.[CrossRef]
    [Google Scholar]
  7. Eisenberg, R. J., Ponce de Leon, M., Friedman, H. M., Fries, L. F., Frank, M. M., Hastings, J. C. & Cohen, G. H. ( 1987; ). Complement component C3b binds directly to purified glycoprotein C of herpes simplex virus types 1 and 2. Microb Pathog 3, 423–435.[CrossRef]
    [Google Scholar]
  8. Enquist, L. W., Husak, P. J., Banfield, B. W. & Smith, G. A. ( 1998; ). Infection and spread of alphaherpesviruses in the nervous system. Adv Virus Res 51, 237–347.
    [Google Scholar]
  9. Fath, K., Trimbur, G. & Burgess, D. ( 1997; ). Molecular motors and a spectrin matrix associate with Golgi membranes in vitro. J Cell Biol 139, 1169–1181.[CrossRef]
    [Google Scholar]
  10. Geraghty, R. J., Krummenacher, C., Cohen, G. H., Eisenberg, R. J. & Spear, P. G. ( 1998; ). Entry of alphaherpesviruses mediated by poliovirus receptor-related protein 1 and poliovirus receptor. Science 280, 1618–1620.[CrossRef]
    [Google Scholar]
  11. Griffiths, A., Renfrey, S. & Minson, T. ( 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.
    [Google Scholar]
  12. Grindstaff, K. K., Bacallao, R. L. & Nelson, W. J. ( 1998; ). Apiconuclear organization of microtubules does not specify protein delivery from the trans-Golgi network to different membrane domains in polarized epithelial cells. Mol Biol Cell 9, 685–699.[CrossRef]
    [Google Scholar]
  13. Hayashi, K. ( 1995; ). Role of tight junctions or polarized epithelial MDCK cells in the replication of herpes simplex virus type 1. J Med Virol 47, 323–329.[CrossRef]
    [Google Scholar]
  14. Hemmings, D. & Guilbert, L. ( 2002; ). Polarized release of human cytomegaloviurs from placental trophoblasts. J Virol 76, 6710–6717.[CrossRef]
    [Google Scholar]
  15. Jordan, M. A. & Wilson, L. ( 1999; ). The use and action of drugs in analyzing mitosis. Methods Cell Biol 61, 267–295.
    [Google Scholar]
  16. Kolset, S., Vuong, T. & Prydz, K. ( 1999; ). Apical secretion of chondroitin sulphate in polarized Madin–Darby canine kidney cells. J Cell Sci 112, 1797–1801.
    [Google Scholar]
  17. Krummenacher, C., Baribaud, I., de Leon, M. P., Whitbeck, J. C., Lou, H., Cohen, G. H. & Eisenberg, R. J. ( 2000; ). Localization of a binding site for herpes simplex virus glycoprotein D on herpesvirus entry mediator C by using antireceptor monoclonal antibodies. J Virol 74, 10863–10872.[CrossRef]
    [Google Scholar]
  18. Lafont, F., Burkhardt, J. K. & Simons, K. ( 1994; ). Involvement of microtubule motors in basolateral and apical transport in kidney cells. Nature 372, 801–803.[CrossRef]
    [Google Scholar]
  19. Mabit, H., Nakano, M. Y., Prank, U., Saam, B., Döhner, K., Sodeik, B. & Greber, U. F. ( 2002; ). Intact microtubules support adenovirus and herpes simplex virus infections. J Virol 76, 9962–9971.[CrossRef]
    [Google Scholar]
  20. Mardberg, K., Trybala, E., Tufaro, F. & Bergstrom, T. ( 2002; ). Herpes simplex virus type 1 glycoprotein C is necessary for efficient infection of chondroitin sulfate-expressing gro2C cells. J Gen Virol 83, 291–300.
    [Google Scholar]
  21. Meads, T. & Schroer, T. ( 1995; ). Polarity and nucleation of microtubules in polarized epithelial cells. Cell Motil Cytoskeleton 32, 272–288.
    [Google Scholar]
  22. Mettenleiter, T. C. ( 2002; ). Herpesvirus assembly and egress. J Virol 76, 1537–1547.[CrossRef]
    [Google Scholar]
  23. Montgomery, R. I., Warner, M. S., Lum, B. J. & Spear, P. G. ( 1996; ). Herpes simplex virus-1 entry into cells mediated by a novel member of the TNF/NGF receptor family. Cell 87, 427–436.[CrossRef]
    [Google Scholar]
  24. Murphy, C., Zacchi, P., Parton, R., Zerial, M. & Lim, P. ( 1997; ). HSV infection of polarized epithelial cells on filter supports: implications for transport assays and protein localization. Eur J Cell Biol 72, 278–281.
    [Google Scholar]
  25. Nicola, A. V., McEvoy, A. M. & Straus, S. E. ( 2003; ). Roles for endocytosis and low pH in herpes simplex virus entry into HeLa and Chinese hamster ovary cells. J Virol 77, 5324–5332.[CrossRef]
    [Google Scholar]
  26. Noda, Y., Okada, Y., Saito, N., Setou, M., Xu, Y., Zhang, Z. & Hirokawa, N. ( 2001; ). KIFC3, a microtubule minus end-directed motor for the apical transport of annexin XIIIb-associated Triton-insoluble membranes. J Cell Biol 155, 77–88.[CrossRef]
    [Google Scholar]
  27. Ojala, P. M., Sodeik, B., Ebersold, M. W., Kutay, U. & Helenius, A. ( 2000; ). Herpes simplex virus type 1 entry into host cells: reconstitution of capsid binding and uncoating at the nuclear pore complex in vitro. Mol Cell Biol 20, 4922–4931.[CrossRef]
    [Google Scholar]
  28. Reinsch, S., Eaton, S. & Stelzer, E. ( 1998; ). Confocal microscopy of polarized epithelial cells. In Cell Biology: a Laboratory Handbook, pp. 170–178. Edited by J. E. Celis. San Diego: Academic Press.
  29. Roizman, B. & Knipe, D. M. ( 2001; ). Herpes simplex viruses and their replication. In Fundamental Virology, 4th edn, pp. 1123–1183. Edited by D. M. Knipe & P. M. Howley. Philadelphia: Lippincott Williams & Wilkins.
  30. Rothen-Rutishauser, B., Krämer, S., Braun, A., Günthert, M. & Wunderli-Allenspach, H. ( 1998; ). MDCK cell cultures as an epithelial in vitro model: cytoskeleton and tight junctions as indicators for the definition of age-related stages by confocal microscopy. Pharm Res 15, 964–971.[CrossRef]
    [Google Scholar]
  31. Rothen-Rutishauser, B., Riesen, F., Günthert, M. & Wunderli-Allenspach, H. ( 2002; ). Dynamics of tight and adherens junctions under EGTA treatment. J Membr Biol 188, 151–162.[CrossRef]
    [Google Scholar]
  32. Rousset, M. ( 1986; ). The human colon carcinoma cell lines HT-29 and Caco-2: two in vitro models for the study of intestinal differentiation. Biochimie 68, 1035–1040.[CrossRef]
    [Google Scholar]
  33. Schelhaas, M., Jansen, M., Haase, I. & Knebel-Mörsdorf, D. ( 2003; ). Herpes simplex virus type 1 exhibits a tropism for basal entry in polarized epithelial cells. J Gen Virol 84, 2473–2484.[CrossRef]
    [Google Scholar]
  34. Sears, A. E., McGwire, B. S. & Roizman, B. ( 1991; ). Infection of polarized MDCK cells with HSV1: two asymmetrically distributed cell receptors interact with different viral proteins. Proc Natl Acad Sci U S A 88, 5087–5091.[CrossRef]
    [Google Scholar]
  35. Showalter, S. D., Zweig, M. & Hampar, B. ( 1981; ). Monoclonal antibodies to herpes simplex virus type 1 proteins, including the immediate-early protein ICP 4. Infect Immun 34, 684–692.
    [Google Scholar]
  36. Shukla, D., Liu, J., Blaiklock, P. & 7 other authors ( 1999; ). A novel role for 3-O-sulfated heparan sulfate in herpes simplex virus 1 entry. Cell 99, 13–22.[CrossRef]
    [Google Scholar]
  37. Simons, K. & Virta, H. ( 1998; ). Growing Madin–Darby canine kidney cells for studying epithelial cell biology. In Cell Biology: a Laboratory Handbook, pp. 101–106. Edited by J. E. Celis. San Diego: Academic Press.
  38. Sodeik, B. ( 2000; ). Mechanisms of viral transport in the cytoplasm. Trends Microbiol 8, 465–472.[CrossRef]
    [Google Scholar]
  39. Sodeik, B., Ebersold, M. W. & Helenius, A. ( 1997; ). Microtubule-mediated transport of incoming herpes simplex virus 1 capsids to the nucleus. J Cell Biol 136, 1007–1021.[CrossRef]
    [Google Scholar]
  40. Spear, P. G. ( 2002; ). Viral interactions with receptors in cell junctions and effects on junctional stability. Dev Cell 3, 462–464.[CrossRef]
    [Google Scholar]
  41. Spear, P. G., Eisenberg, R. J. & Cohen, G. H. ( 2000; ). Three classes of cell surface receptors for alphaherpesvirus entry. Virology 275, 1–8.[CrossRef]
    [Google Scholar]
  42. Takai, Y. & Nakanishi, H. ( 2003; ). Nectin and afadin: novel organizers of intercellular junctions. J Cell Sci 116, 17–27.[CrossRef]
    [Google Scholar]
  43. Topp, K. S., Rothman, A. L. & Lavail, J. H. ( 1997; ). Herpes virus infection of RPE and MDCK cells: polarity of infection. Exp Eye Res 64, 343–354.[CrossRef]
    [Google Scholar]
  44. Tran, L., Kissner, J., Westerman, L. & Sears, A. E. ( 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 U S A 97, 1818–1822.[CrossRef]
    [Google Scholar]
  45. Wagner, E. K. & Bloom, D. C. ( 1997; ). Experimental investigation of herpes simplex virus latency. Clin Microbiol Rev 10, 419–443.
    [Google Scholar]
  46. Wang, Y., Jerdeva, G., Yarber, F. & 8 other authors ( 2003; ). Cytoplasmic dynein participates in apically targeted stimulated secretory traffic in primary rabbit lacrimal acinar epithelial cells. J Cell Sci 116, 2051–2065.[CrossRef]
    [Google Scholar]
  47. Warner, M. S., Geraghty, R. J., Martinez, W. M., Montgomery, R. I., Whitbeck, J. C., Xu, R., Eisenberg, R. J., Cohen, G. H. & Spear, P. G. ( 1998; ). A cell surface protein with herpesvirus entry activity (HveB) confers susceptibility to infection by mutants of herpes simplex virus type 1, herpes simplex virus type 2, and pseudorabies virus. Virology 246, 179–189.[CrossRef]
    [Google Scholar]
  48. Whittaker, G. R., Kann, M. & Helenius, A. ( 2000; ). Viral entry into the nucleus. Annu Rev Cell Dev Biol 16, 627–651.[CrossRef]
    [Google Scholar]
  49. Yoon, M. & Spear, P. G. ( 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.[CrossRef]
    [Google Scholar]
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