Skip to main content
Journal of Virology logoLink to Journal of Virology
. 1993 Feb;67(2):651–663. doi: 10.1128/jvi.67.2.651-663.1993

Sendai virus assembly: M protein binds to viral glycoproteins in transit through the secretory pathway.

C M Sanderson 1, N L McQueen 1, D P Nayak 1
PMCID: PMC237416  PMID: 8380460

Abstract

We have examined the relative ability of Sendai virus M (matrix) protein to associate with membranes containing viral glycoproteins at three distinct stages of the exocytic pathway prior to cell surface appearance. By the use of selective low-temperature incubations or the ionophore monensin, the transport of newly synthesized viral glycoproteins was restricted to either the pre-Golgi intermediate compartment (by incubation at 15 degrees C), the medial Golgi (in the presence of monensin), or the trans-Golgi network (by incubation at 20 degrees C). All three of these treatments resulted in a marked accumulation of the M protein on perinuclear Golgi-like membranes which in each case directly reflected the distribution of the viral F protein. Subsequent redistribution of the F protein to the plasma membrane by removal of the low-temperature (20 degrees C) block resulted in a concomitant redistribution of the M protein, thus implying association of the two components during intracellular transit. The extent of M protein-glycoprotein association was further examined by cell fractionation studies performed under each of the three restrictive conditions. Following equilibrium sedimentation of membranes derived from monensin-treated cells, approximately 40% of the recovered M protein was found to cofractionate with membranes containing the viral glycoproteins. Also, by flotation analyses, a comparable subpopulation of M protein was found to be membrane associated whether viral glycoproteins were restricted to the trans-Golgi network, the medial Golgi, or the pre-Golgi intermediate compartment. Additionally, transient expression of M protein alone from cloned cDNA showed that neither membrane association nor Golgi localization occurs in the absence of Sendai virus glycoproteins.

Full text

PDF
651

Images in this article

Selected References

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

  1. Blumberg B., Giorgi C., Roux L., Raju R., Dowling P., Chollet A., Kolakofsky D. Sequence determination of the Sendai virus HN gene and its comparison to the influenza virus glycoproteins. Cell. 1985 May;41(1):269–278. doi: 10.1016/0092-8674(85)90080-7. [DOI] [PubMed] [Google Scholar]
  2. Bosch J. V., Schwarz R. T. Processing of gPr92env, the precursor to the glycoproteins of Rous sarcoma virus: use of inhibitors of oligosaccharide trimming and glycoprotein transport. Virology. 1984 Jan 15;132(1):95–109. doi: 10.1016/0042-6822(84)90094-1. [DOI] [PubMed] [Google Scholar]
  3. Bowen H. A., Lyles D. S. Kinetics of incorporation of Sendai virus proteins into host plasma membranes and virions. Virology. 1982 Aug;121(1):1–11. doi: 10.1016/0042-6822(82)90113-1. [DOI] [PubMed] [Google Scholar]
  4. Brown M. S., Goldstein J. L. A receptor-mediated pathway for cholesterol homeostasis. Science. 1986 Apr 4;232(4746):34–47. doi: 10.1126/science.3513311. [DOI] [PubMed] [Google Scholar]
  5. Bächi T. Intramembrane structural differentiation in Sendai virus maturation. Virology. 1980 Oct 15;106(1):41–49. doi: 10.1016/0042-6822(80)90219-6. [DOI] [PubMed] [Google Scholar]
  6. Büechi M., Bächi T. Microscopy of internal structures of Sendai virus associated with the cytoplasmic surface of host membranes. Virology. 1982 Jul 30;120(2):349–359. doi: 10.1016/0042-6822(82)90036-8. [DOI] [PubMed] [Google Scholar]
  7. Duden R., Griffiths G., Frank R., Argos P., Kreis T. E. Beta-COP, a 110 kd protein associated with non-clathrin-coated vesicles and the Golgi complex, shows homology to beta-adaptin. Cell. 1991 Feb 8;64(3):649–665. doi: 10.1016/0092-8674(91)90248-w. [DOI] [PubMed] [Google Scholar]
  8. Duncan J. R., Kornfeld S. Intracellular movement of two mannose 6-phosphate receptors: return to the Golgi apparatus. J Cell Biol. 1988 Mar;106(3):617–628. doi: 10.1083/jcb.106.3.617. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Faaberg K. S., Peeples M. E. Association of soluble matrix protein of Newcastle disease virus with liposomes is independent of ionic conditions. Virology. 1988 Sep;166(1):123–132. doi: 10.1016/0042-6822(88)90153-5. [DOI] [PubMed] [Google Scholar]
  10. Felgner P. L., Gadek T. R., Holm M., Roman R., Chan H. W., Wenz M., Northrop J. P., Ringold G. M., Danielsen M. Lipofection: a highly efficient, lipid-mediated DNA-transfection procedure. Proc Natl Acad Sci U S A. 1987 Nov;84(21):7413–7417. doi: 10.1073/pnas.84.21.7413. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Fuerst T. R., Earl P. L., Moss B. Use of a hybrid vaccinia virus-T7 RNA polymerase system for expression of target genes. Mol Cell Biol. 1987 Jul;7(7):2538–2544. doi: 10.1128/mcb.7.7.2538. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Gregoriades A. Interaction of influenza M protein with viral lipid and phosphatidylcholine vesicles. J Virol. 1980 Nov;36(2):470–479. doi: 10.1128/jvi.36.2.470-479.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Griffiths G., Pfeiffer S., Simons K., Matlin K. Exit of newly synthesized membrane proteins from the trans cisterna of the Golgi complex to the plasma membrane. J Cell Biol. 1985 Sep;101(3):949–964. doi: 10.1083/jcb.101.3.949. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Griffiths G., Quinn P., Warren G. Dissection of the Golgi complex. I. Monensin inhibits the transport of viral membrane proteins from medial to trans Golgi cisternae in baby hamster kidney cells infected with Semliki Forest virus. J Cell Biol. 1983 Mar;96(3):835–850. doi: 10.1083/jcb.96.3.835. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. 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]
  16. Hewitt J. A., Nermut M. V. A morphological study of the M-protein of Sendai virus. J Gen Virol. 1977 Jan;34(1):127–136. doi: 10.1099/0022-1317-34-1-127. [DOI] [PubMed] [Google Scholar]
  17. Johnson D. C., Schlesinger M. J. Vesicular stomatitis virus and sindbis virus glycoprotein transport to the cell surface is inhibited by ionophores. Virology. 1980 Jun;103(2):407–424. doi: 10.1016/0042-6822(80)90200-7. [DOI] [PubMed] [Google Scholar]
  18. Jones T. A., Blaug G., Hansen M., Barklis E. Assembly of gag-beta-galactosidase proteins into retrovirus particles. J Virol. 1990 May;64(5):2265–2279. doi: 10.1128/jvi.64.5.2265-2279.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Käriäinen L., Hashimoto K., Saraste J., Virtanen I., Penttinen K. Monensin and FCCP inhibit the intracellular transport of alphavirus membrane glycoproteins. J Cell Biol. 1980 Dec;87(3 Pt 1):783–791. doi: 10.1083/jcb.87.3.783. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Lamb R. A., Choppin P. W. The synthesis of Sendai virus polypeptides in infected cells. II. Intracellular distribution of polypeptides. Virology. 1977 Sep;81(2):371–381. doi: 10.1016/0042-6822(77)90153-2. [DOI] [PubMed] [Google Scholar]
  21. Matlin K. S., Simons K. Reduced temperature prevents transfer of a membrane glycoprotein to the cell surface but does not prevent terminal glycosylation. Cell. 1983 Aug;34(1):233–243. doi: 10.1016/0092-8674(83)90154-x. [DOI] [PubMed] [Google Scholar]
  22. Mottet G., Portner A., Roux L. Drastic immunoreactivity changes between the immature and mature forms of the Sendai virus HN and F0 glycoproteins. J Virol. 1986 Jul;59(1):132–141. doi: 10.1128/jvi.59.1.132-141.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Orci L., Ravazzola M., Amherdt M., Perrelet A., Powell S. K., Quinn D. L., Moore H. P. The trans-most cisternae of the Golgi complex: a compartment for sorting of secretory and plasma membrane proteins. Cell. 1987 Dec 24;51(6):1039–1051. doi: 10.1016/0092-8674(87)90590-3. [DOI] [PubMed] [Google Scholar]
  24. Sanderson C. M., Meyer D. I. Purification and functional characterization of membranes derived from the rough endoplasmic reticulum of Saccharomyces cerevisiae. J Biol Chem. 1991 Jul 15;266(20):13423–13430. [PubMed] [Google Scholar]
  25. Saraste J., Kuismanen E. Pre- and post-Golgi vacuoles operate in the transport of Semliki Forest virus membrane glycoproteins to the cell surface. Cell. 1984 Sep;38(2):535–549. doi: 10.1016/0092-8674(84)90508-7. [DOI] [PubMed] [Google Scholar]
  26. Schweizer A., Fransen J. A., Matter K., Kreis T. E., Ginsel L., Hauri H. P. Identification of an intermediate compartment involved in protein transport from endoplasmic reticulum to Golgi apparatus. Eur J Cell Biol. 1990 Dec;53(2):185–196. [PubMed] [Google Scholar]
  27. Shimizu K., Isida N. The smallest protein of Sendi virus: its candidate function of binding nucleocaspsid to envelope. Virology. 1975 Oct;67(2):427–437. [PubMed] [Google Scholar]
  28. 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]
  29. 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]
  30. Uchida N., Smilowitz H., Tanzer M. L. Monovalent ionophores inhibit secretion of procollagen and fibronectin from cultured human fibroblasts. Proc Natl Acad Sci U S A. 1979 Apr;76(4):1868–1872. doi: 10.1073/pnas.76.4.1868. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Wood S. A., Park J. E., Brown W. J. Brefeldin A causes a microtubule-mediated fusion of the trans-Golgi network and early endosomes. Cell. 1991 Nov 1;67(3):591–600. doi: 10.1016/0092-8674(91)90533-5. [DOI] [PubMed] [Google Scholar]
  32. Yoshida T., Nagai Y'Yoshii S., Maeno K., Matsumoto T. Membrane (M) protein of HVJ (Sendai virus): its role in virus assembly. Virology. 1976 May;71(1):143–161. doi: 10.1016/0042-6822(76)90101-x. [DOI] [PubMed] [Google Scholar]
  33. Yoshida T., Nagai Y., Maeno K., Iinuma M., Hamaguchi M., Matsumoto T., Nagayoshi S., Hoshino M. Studies on the role of M protein in virus assembly using a ts mutant of HVJ (Sendai virus). Virology. 1979 Jan 15;92(1):139–154. doi: 10.1016/0042-6822(79)90220-4. [DOI] [PubMed] [Google Scholar]

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

RESOURCES