Nothing Special   »   [go: up one dir, main page]
Skip to main content
PMC home page
Journal of Virology logoLink to Journal of Virology
. 1993 Oct;67(10):5902–5910. doi: 10.1128/jvi.67.10.5902-5910.1993

Possible involvement of microtubule disruption in bipolar budding of a Sendai virus mutant, F1-R, in epithelial MDCK cells.

M Tashiro 1, J T Seto 1, H D Klenk 1, R Rott 1
PMCID: PMC238010  PMID: 8396659

Abstract

Envelope glycoproteins F and HN of wild-type Sendai virus are transported to the apical plasma membrane domain of polarized epithelial MDCK cells, where budding of progeny virus occurs. On the other hand, a pantropic mutant, F1-R, buds bipolarly at both the apical and basolateral domains, and the viral glycoproteins have also been shown to be transported to both of these domains (M. Tashiro, M. Yamakawa, K. Tobita, H.-D. Klenk, R. Rott, and J.T. Seto, J. Virol. 64:4672-4677, 1990). MDCK cells were infected with wild-type virus and treated with the microtubule-depolymerizing drugs colchicine and nocodazole. Budding of the virus and surface expression of the glycoproteins were found to occur in a nonpolarized fashion similar to that found in cells infected with F1-R. In uninfected cells, the drugs were shown to interfere with apical transport of a secretory cellular glycoprotein, gp80, and basolateral uptake of [35S]methionine as well as to disrupt microtubule structure, indicating that cellular polarity of MDCK cells depends on the presence of intact microtubules. Infection by the F1-R mutant partially affected the transport of gp80, uptake of [35S]methionine, and the microtubule network, whereas wild-type virus had a marginal effect. These results suggest that apical transport of the glycoproteins of wild-type Sendai virus in MDCK cells depends on intact microtubules and that bipolar budding by F1-R is possibly due, at least in part, to the disruption of microtubules. Nucleotide sequence analyses of the viral genes suggest that the mutated M protein of F1-R might be involved in the alteration of microtubules.

Full text

PDF
5902

Images in this article

5907Image
on p.5907

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Achler C., Filmer D., Merte C., Drenckhahn D. Role of microtubules in polarized delivery of apical membrane proteins to the brush border of the intestinal epithelium. J Cell Biol. 1989 Jul;109(1):179–189. doi: 10.1083/jcb.109.1.179. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bacallao R., Antony C., Dotti C., Karsenti E., Stelzer E. H., Simons K. The subcellular organization of Madin-Darby canine kidney cells during the formation of a polarized epithelium. J Cell Biol. 1989 Dec;109(6 Pt 1):2817–2832. doi: 10.1083/jcb.109.6.2817. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Balcarova-Ständer J., Pfeiffer S. E., Fuller S. D., Simons K. Development of cell surface polarity in the epithelial Madin-Darby canine kidney (MDCK) cell line. EMBO J. 1984 Nov;3(11):2687–2694. doi: 10.1002/j.1460-2075.1984.tb02194.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bergmann J. E., Fusco P. J. The M protein of vesicular stomatitis virus associates specifically with the basolateral membranes of polarized epithelial cells independently of the G protein. J Cell Biol. 1988 Nov;107(5):1707–1715. doi: 10.1083/jcb.107.5.1707. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Breitfeld P. P., McKinnon W. C., Mostov K. E. Effect of nocodazole on vesicular traffic to the apical and basolateral surfaces of polarized MDCK cells. J Cell Biol. 1990 Dec;111(6 Pt 1):2365–2373. doi: 10.1083/jcb.111.6.2365. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Brewer C. B., Roth M. G. A single amino acid change in the cytoplasmic domain alters the polarized delivery of influenza virus hemagglutinin. J Cell Biol. 1991 Aug;114(3):413–421. doi: 10.1083/jcb.114.3.413. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Brown D. A., Crise B., Rose J. K. Mechanism of membrane anchoring affects polarized expression of two proteins in MDCK cells. Science. 1989 Sep 29;245(4925):1499–1501. doi: 10.1126/science.2571189. [DOI] [PubMed] [Google Scholar]
  8. Caplan M. J., Anderson H. C., Palade G. E., Jamieson J. D. Intracellular sorting and polarized cell surface delivery of (Na+,K+)ATPase, an endogenous component of MDCK cell basolateral plasma membranes. Cell. 1986 Aug 15;46(4):623–631. doi: 10.1016/0092-8674(86)90888-3. [DOI] [PubMed] [Google Scholar]
  9. Compans R. W., Srinivas R. V. Protein sorting in polarized epithelial cells. Curr Top Microbiol Immunol. 1991;170:141–181. doi: 10.1007/978-3-642-76389-2_5. [DOI] [PubMed] [Google Scholar]
  10. Compton T., Ivanov I. E., Gottlieb T., Rindler M., Adesnik M., Sabatini D. D. A sorting signal for the basolateral delivery of the vesicular stomatitis virus (VSV) G protein lies in its luminal domain: analysis of the targeting of VSV G-influenza hemagglutinin chimeras. Proc Natl Acad Sci U S A. 1989 Jun;86(11):4112–4116. doi: 10.1073/pnas.86.11.4112. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Eilers U., Klumperman J., Hauri H. P. Nocodazole, a microtubule-active drug, interferes with apical protein delivery in cultured intestinal epithelial cells (Caco-2). J Cell Biol. 1989 Jan;108(1):13–22. doi: 10.1083/jcb.108.1.13. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Fuller S., von Bonsdorff C. H., Simons K. Vesicular stomatitis virus infects and matures only through the basolateral surface of the polarized epithelial cell line, MDCK. Cell. 1984 Aug;38(1):65–77. doi: 10.1016/0092-8674(84)90527-0. [DOI] [PubMed] [Google Scholar]
  13. Gilbert T., Le Bivic A., Quaroni A., Rodriguez-Boulan E. Microtubular organization and its involvement in the biogenetic pathways of plasma membrane proteins in Caco-2 intestinal epithelial cells. J Cell Biol. 1991 Apr;113(2):275–288. doi: 10.1083/jcb.113.2.275. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Gonzalez A., Rizzolo L., Rindler M., Adesnik M., Sabatini D. D., Gottlieb T. Nonpolarized secretion of truncated forms of the influenza hemagglutinin and the vesicular stomatitus virus G protein from MDCK cells. Proc Natl Acad Sci U S A. 1987 Jun;84(11):3738–3742. doi: 10.1073/pnas.84.11.3738. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Gottlieb T. A., Gonzalez A., Rizzolo L., Rindler M. J., Adesnik M., Sabatini D. D. Sorting and endocytosis of viral glycoproteins in transfected polarized epithelial cells. J Cell Biol. 1986 Apr;102(4):1242–1255. doi: 10.1083/jcb.102.4.1242. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Griffiths G., Simons K. The trans Golgi network: sorting at the exit site of the Golgi complex. Science. 1986 Oct 24;234(4775):438–443. doi: 10.1126/science.2945253. [DOI] [PubMed] [Google Scholar]
  17. Kelly R. B. Microtubules, membrane traffic, and cell organization. Cell. 1990 Apr 6;61(1):5–7. doi: 10.1016/0092-8674(90)90206-t. [DOI] [PubMed] [Google Scholar]
  18. Kreis T. E. Role of microtubules in the organisation of the Golgi apparatus. Cell Motil Cytoskeleton. 1990;15(2):67–70. doi: 10.1002/cm.970150202. [DOI] [PubMed] [Google Scholar]
  19. Matlin K. S. The sorting of proteins to the plasma membrane in epithelial cells. J Cell Biol. 1986 Dec;103(6 Pt 2):2565–2568. doi: 10.1083/jcb.103.6.2565. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Matter K., Bucher K., Hauri H. P. Microtubule perturbation retards both the direct and the indirect apical pathway but does not affect sorting of plasma membrane proteins in intestinal epithelial cells (Caco-2). EMBO J. 1990 Oct;9(10):3163–3170. doi: 10.1002/j.1460-2075.1990.tb07514.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. McQueen N. L., Nayak D. P., Stephens E. B., Compans R. W. Basolateral expression of a chimeric protein in which the transmembrane and cytoplasmic domains of vesicular stomatitis virus G protein have been replaced by those of the influenza virus hemagglutinin. J Biol Chem. 1987 Nov 25;262(33):16233–16240. [PubMed] [Google Scholar]
  22. McQueen N., Nayak D. P., Stephens E. B., Compans R. W. Polarized expression of a chimeric protein in which the transmembrane and cytoplasmic domains of the influenza virus hemagglutinin have been replaced by those of the vesicular stomatitis virus G protein. Proc Natl Acad Sci U S A. 1986 Dec;83(24):9318–9322. doi: 10.1073/pnas.83.24.9318. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Middleton Y., Tashiro M., Thai T., Oh J., Seymour J., Pritzer E., Klenk H. D., Rott R., Seto J. T. Nucleotide sequence analyses of the genes encoding the HN, M, NP, P, and L proteins of two host range mutants of Sendai virus. Virology. 1990 Jun;176(2):656–657. doi: 10.1016/0042-6822(90)90040-x. [DOI] [PubMed] [Google Scholar]
  24. Mostov K. E., Simister N. E. Transcytosis. Cell. 1985 Dec;43(2 Pt 1):389–390. doi: 10.1016/0092-8674(85)90166-7. [DOI] [PubMed] [Google Scholar]
  25. Mostov K., Apodaca G., Aroeti B., Okamoto C. Plasma membrane protein sorting in polarized epithelial cells. J Cell Biol. 1992 Feb;116(3):577–583. doi: 10.1083/jcb.116.3.577. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Nayak D. P., Jabbar M. A. Structural domains and organizational conformation involved in the sorting and transport of influenza virus transmembrane proteins. Annu Rev Microbiol. 1989;43:465–501. doi: 10.1146/annurev.mi.43.100189.002341. [DOI] [PubMed] [Google Scholar]
  27. Nelson W. J. Cytoskeleton functions in membrane traffic in polarized epithelial cells. Semin Cell Biol. 1991 Dec;2(6):375–385. [PubMed] [Google Scholar]
  28. Nelson W. J. Regulation of cell surface polarity from bacteria to mammals. Science. 1992 Nov 6;258(5084):948–955. doi: 10.1126/science.1439806. [DOI] [PubMed] [Google Scholar]
  29. Ojakian G. K., Schwimmer R. Antimicrotubule drugs inhibit the polarized insertion of an intracellular glycoprotein pool into the apical membrane of Madin-Darby canine kidney (MDCK) cells. J Cell Sci. 1992 Nov;103(Pt 3):677–687. doi: 10.1242/jcs.103.3.677. [DOI] [PubMed] [Google Scholar]
  30. Parczyk K., Haase W., Kondor-Koch C. Microtubules are involved in the secretion of proteins at the apical cell surface of the polarized epithelial cell, Madin-Darby canine kidney. J Biol Chem. 1989 Oct 5;264(28):16837–16846. [PubMed] [Google Scholar]
  31. Pfeiffer S., Fuller S. D., Simons K. Intracellular sorting and basolateral appearance of the G protein of vesicular stomatitis virus in Madin-Darby canine kidney cells. J Cell Biol. 1985 Aug;101(2):470–476. doi: 10.1083/jcb.101.2.470. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Philp N. J., Nachmias V. T. Components of the cytoskeleton in the retinal pigmented epithelium of the chick. J Cell Biol. 1985 Aug;101(2):358–362. doi: 10.1083/jcb.101.2.358. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Puddington L., Woodgett C., Rose J. K. Replacement of the cytoplasmic domain alters sorting of a viral glycoprotein in polarized cells. Proc Natl Acad Sci U S A. 1987 May;84(9):2756–2760. doi: 10.1073/pnas.84.9.2756. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Rindler M. J., Ivanov I. E., Sabatini D. D. Microtubule-acting drugs lead to the nonpolarized delivery of the influenza hemagglutinin to the cell surface of polarized Madin-Darby canine kidney cells. J Cell Biol. 1987 Feb;104(2):231–241. doi: 10.1083/jcb.104.2.231. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Rodriguez Boulan E., Pendergast M. Polarized distribution of viral envelope proteins in the plasma membrane of infected epithelial cells. Cell. 1980 May;20(1):45–54. doi: 10.1016/0092-8674(80)90233-0. [DOI] [PubMed] [Google Scholar]
  36. Rodriguez-Boulan E., Nelson W. J. Morphogenesis of the polarized epithelial cell phenotype. Science. 1989 Aug 18;245(4919):718–725. doi: 10.1126/science.2672330. [DOI] [PubMed] [Google Scholar]
  37. Rogalski A. A., Singer S. J. Associations of elements of the Golgi apparatus with microtubules. J Cell Biol. 1984 Sep;99(3):1092–1100. doi: 10.1083/jcb.99.3.1092. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Roth M. G., Compans R. W., Giusti L., Davis A. R., Nayak D. P., Gething M. J., Sambrook J. Influenza virus hemagglutinin expression is polarized in cells infected with recombinant SV40 viruses carrying cloned hemagglutinin DNA. Cell. 1983 Jun;33(2):435–443. doi: 10.1016/0092-8674(83)90425-7. [DOI] [PubMed] [Google Scholar]
  39. Roth M. G., Srinivas R. V., Compans R. W. Basolateral maturation of retroviruses in polarized epithelial cells. J Virol. 1983 Mar;45(3):1065–1073. doi: 10.1128/jvi.45.3.1065-1073.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Salas P. J., Misek D. E., Vega-Salas D. E., Gundersen D., Cereijido M., Rodriguez-Boulan E. Microtubules and actin filaments are not critically involved in the biogenesis of epithelial cell surface polarity. J Cell Biol. 1986 May;102(5):1853–1867. doi: 10.1083/jcb.102.5.1853. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Sanderson C. M., McQueen N. L., Nayak D. P. Sendai virus assembly: M protein binds to viral glycoproteins in transit through the secretory pathway. J Virol. 1993 Feb;67(2):651–663. doi: 10.1128/jvi.67.2.651-663.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Srinivas R. V., Balachandran N., Alonso-Caplen F. V., Compans R. W. Expression of herpes simplex virus glycoproteins in polarized epithelial cells. J Virol. 1986 May;58(2):689–693. doi: 10.1128/jvi.58.2.689-693.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Stephens E. B., Compans R. W. Nonpolarized expression of a secreted murine leukemia virus glycoprotein in polarized epithelial cells. Cell. 1986 Dec 26;47(6):1053–1059. doi: 10.1016/0092-8674(86)90820-2. [DOI] [PubMed] [Google Scholar]
  44. Tashiro M., Homma M. Pneumotropism of Sendai virus in relation to protease-mediated activation in mouse lungs. Infect Immun. 1983 Feb;39(2):879–888. doi: 10.1128/iai.39.2.879-888.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Tashiro M., James I., Karri S., Wahn K., Tobita K., Klenk H. D., Rott R., Seto J. T. Pneumotropic revertants derived from a pantropic mutant, F1-R, of Sendai virus. Virology. 1991 Sep;184(1):227–234. doi: 10.1016/0042-6822(91)90839-4. [DOI] [PubMed] [Google Scholar]
  46. Tashiro M., Pritzer E., Khoshnan M. A., Yamakawa M., Kuroda K., Klenk H. D., Rott R., Seto J. T. Characterization of a pantropic variant of Sendai virus derived from a host range mutant. Virology. 1988 Aug;165(2):577–583. doi: 10.1016/0042-6822(88)90601-0. [DOI] [PubMed] [Google Scholar]
  47. Tashiro M., Seto J. T., Choosakul S., Yamakawa M., Klenk H. D., Rott R. Budding site of Sendai virus in polarized epithelial cells is one of the determinants for tropism and pathogenicity in mice. Virology. 1992 Apr;187(2):413–422. doi: 10.1016/0042-6822(92)90443-s. [DOI] [PubMed] [Google Scholar]
  48. Tashiro M., Yamakawa M., Tobita K., Klenk H. D., Rott R., Seto J. T. Organ tropism of Sendai virus in mice: proteolytic activation of the fusion glycoprotein in mouse organs and budding site at the bronchial epithelium. J Virol. 1990 Aug;64(8):3627–3634. doi: 10.1128/jvi.64.8.3627-3634.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Tashiro M., Yamakawa M., Tobita K., Klenk H. D., Seto J. T., Rott R. Significance of basolateral domain of polarized MDCK cells for Sendai virus-induced cell fusion. Arch Virol. 1992;125(1-4):129–139. doi: 10.1007/BF01309633. [DOI] [PubMed] [Google Scholar]
  50. Tashiro M., Yamakawa M., Tobita K., Seto J. T., Klenk H. D., Rott R. Altered budding site of a pantropic mutant of Sendai virus, F1-R, in polarized epithelial cells. J Virol. 1990 Oct;64(10):4672–4677. doi: 10.1128/jvi.64.10.4672-4677.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Thomas D. C., Brewer C. B., Roth M. G. Vesicular stomatitis virus glycoprotein contains a dominant cytoplasmic basolateral sorting signal critically dependent upon a tyrosine. J Biol Chem. 1993 Feb 15;268(5):3313–3320. [PubMed] [Google Scholar]
  52. Thyberg J., Moskalewski S. Microtubules and the organization of the Golgi complex. Exp Cell Res. 1985 Jul;159(1):1–16. doi: 10.1016/s0014-4827(85)80032-x. [DOI] [PubMed] [Google Scholar]
  53. Tucker S. P., Compans R. W. Virus infection of polarized epithelial cells. Adv Virus Res. 1993;42:187–247. doi: 10.1016/S0065-3527(08)60086-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Turner J. R., Tartakoff A. M. The response of the Golgi complex to microtubule alterations: the roles of metabolic energy and membrane traffic in Golgi complex organization. J Cell Biol. 1989 Nov;109(5):2081–2088. doi: 10.1083/jcb.109.5.2081. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Urban J., Parczyk K., Leutz A., Kayne M., Kondor-Koch C. Constitutive apical secretion of an 80-kD sulfated glycoprotein complex in the polarized epithelial Madin-Darby canine kidney cell line. J Cell Biol. 1987 Dec;105(6 Pt 1):2735–2743. doi: 10.1083/jcb.105.6.2735. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Van der Sluijs P., Bennett M. K., Antony C., Simons K., Kreis T. E. Binding of exocytic vesicles from MDCK cells to microtubules in vitro. J Cell Sci. 1990 Apr;95(Pt 4):545–553. doi: 10.1242/jcs.95.4.545. [DOI] [PubMed] [Google Scholar]
  57. Wandinger-Ness A., Bennett M. K., Antony C., Simons K. Distinct transport vesicles mediate the delivery of plasma membrane proteins to the apical and basolateral domains of MDCK cells. J Cell Biol. 1990 Sep;111(3):987–1000. doi: 10.1083/jcb.111.3.987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. van Zeijl M. J., Matlin K. S. Microtubule perturbation inhibits intracellular transport of an apical membrane glycoprotein in a substrate-dependent manner in polarized Madin-Darby canine kidney epithelial cells. Cell Regul. 1990 Nov;1(12):921–936. doi: 10.1091/mbc.1.12.921. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of Virology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES