1887

Journal of General Virology header logo

Volume 87, Issue 6

Murine leukemia virus transmembrane protein R-peptide is found in small virus core-like complexes in cells Free

Abstract

The core of the retrovirus (MLV) consists of the Gag precursor protein and viral RNA. It assembles at the cytoplasmic face of the cell membrane where, by an unclear mechanism, it collects viral envelope proteins embedded in the cell membrane and buds off. The C-terminal half of the short cytoplasmic tail of the envelope transmembrane protein (TM) is cleaved off to yield R-peptide and fusion-active TM. In Moloney MLV particles, R-peptide was found to bind to core particles. In cells, R-peptide and low amounts of uncleaved TM were found to be associated with small core-like complexes, i.e. mild detergent-insoluble, Gag-containing complexes with a density of 1.23 g ml and a size of 150–200 S. Our results suggest that TM associates with the assembling core particle through the R-peptide before budding and that this is the mechanism by which the budding virus acquires the envelope proteins.

  • Received:
  • Accepted:
  • Published Online:
SGM
Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.81527-0
2006-06-01
2024-04-28
Loading full text...

Full text loading...

/deliver/fulltext/jgv/87/6/1583.html?itemId=/content/journal/jgv/10.1099/vir.0.81527-0&mimeType=html&fmt=ahah

References

  1. Bellamy A. R., Gillies S. C., Harvey J. D. 1974; Molecular weight of two oncornavirus genomes: derivation from particle molecular weights and RNA content. J Virol 14:1388–1393
     [Google Scholar]
  2. Bobkova M., Stitz J., Engelstädter M., Cichutek K., Buchholz C. J. 2002; Identification of R-peptides in envelope proteins of C-type retroviruses. J Gen Virol 83:2241–2246
     [Google Scholar]
  3. Brody B. A., Rhee S. S., Sommerfelt M. A., Hunter E. 1992; A viral protease-mediated cleavage of the transmembrane glycoprotein of Mason–Pfizer monkey virus can be suppressed by mutations within the matrix protein. Proc Natl Acad Sci U S A 89:3443–3447 [CrossRef]
     [Google Scholar]
  4. Brody B. A., Rhee S. S., Hunter E. 1994; Postassembly cleavage of a retroviral glycoprotein cytoplasmic domain removes a necessary incorporation signal and activates fusion activity. J Virol 68:4620–4627
     [Google Scholar]
  5. Chen C., Weisz O. A., Stolz D. B., Watkins S. C., Montelaro R. C. 2004; Differential effects of actin cytoskeleton dynamics on equine infectious anemia virus particle production. J Virol 78:882–891 [CrossRef]
     [Google Scholar]
  6. Cimarelli A., Darlix J. L. 2002; Assembling the human immunodeficiency virus type 1. Cell Mol Life Sci 59:1166–1184 [CrossRef]
     [Google Scholar]
  7. Demirov D. G., Freed E. O. 2004; Retrovirus budding. Virus Res 106:87–102 [CrossRef]
     [Google Scholar]
  8. Einfeld D., Hunter E. 1988; Oligomeric structure of a prototype retrovirus glycoprotein. Proc Natl Acad Sci U S A 85:8688–8692 [CrossRef]
     [Google Scholar]
  9. Fischer N., Heinkelein M., Lindemann D., Enssle J., Baum C., Werder E., Zentgraf H., Müller J. G., Rethwilm A. 1998; Foamy virus particle formation. J Virol 72:1610–1615
     [Google Scholar]
  10. Freed E. O., Martin M. A. 1995; Virion incorporation of envelope glycoproteins with long but not short cytoplasmic tails is blocked by specific, single amino acid substitutions in the human immunodeficiency virus type 1 matrix. J Virol 69:1984–1989
     [Google Scholar]
  11. Freed E. O., Martin M. A. 1996; Domains of the human immunodeficiency virus type 1 matrix and gp41 cytoplasmic tail required for envelope incorporation into virions. J Virol 70:341–351
     [Google Scholar]
  12. Green N., Shinnick T. M., Witte O., Ponticelli A., Sutcliffe J. G., Lerner R. A. 1981; Sequence-specific antibodies show that maturation of Moloney leukemia virus envelope polyprotein involves removal of a COOH-terminal peptide. Proc Natl Acad Sci U S A 78:6023–6027 [CrossRef]
     [Google Scholar]
  13. Hansen M., Jelinek L., Jones R. S., Stegeman-Olsen J., Barklis E. 1993; Assembly and composition of intracellular particles formed by Moloney murine leukemia virus. J Virol 67:5163–5174
     [Google Scholar]
  14. Henderson L. E., Sowder R., Copeland T. D., Smythers G., Oroszlan S. 1984; Quantitative separation of murine leukemia virus proteins by reversed-phase high-pressure liquid chromatography reveals newly described gag and env cleavage products. J Virol 52:492–500
     [Google Scholar]
  15. Hermida-Matsumoto L., Resh M. D. 2000; Localization of human immunodeficiency virus type 1 Gag and Env at the plasma membrane by confocal imaging. J Virol 74:8670–8679 [CrossRef]
     [Google Scholar]
  16. Kubo Y., Amanuma H. 2003; Mutational analysis of the R peptide cleavage site of Moloney murine leukaemia virus envelope protein. J Gen Virol 84:2253–2257 [CrossRef]
     [Google Scholar]
  17. Kuznetsov Y. G., Low A., Fan H., McPherson A. 2004; Atomic force microscopy investigation of wild-type Moloney murine leukemia virus particles and virus particles lacking the envelope protein. Virology 323:189–196 [CrossRef]
     [Google Scholar]
  18. Lingappa J. R., Hill R. L., Wong M. L., Hegde R. S. 1997; A multistep, ATP-dependent pathway for assembly of human immunodeficiency virus capsids in a cell-free system. J Cell Biol 136:567–581 [CrossRef]
     [Google Scholar]
  19. Maeda T., Balakrishnan K., Mehdi S. Q. 1983; A simple and rapid method for the preparation of plasma membranes. Biochim Biophys Acta 731:115–120 [CrossRef]
     [Google Scholar]
  20. Mammano F., Kondo E., Sodroski J., Bukovsky A., Göttlinger H. G. 1995; Rescue of human immunodeficiency virus type 1 matrix protein mutants by envelope glycoproteins with short cytoplasmic domains. J Virol 69:3824–3830
     [Google Scholar]
  21. Melamed D., Mark-Danieli M., Kenan-Eichler M. & 7 other authors 2004; The conserved carboxy terminus of the capsid domain of human immunodeficiency virus type 1 Gag protein is important for virion assembly and release. J Virol 78:9675–9688 [CrossRef]
     [Google Scholar]
  22. Olsen K. E. P., Andersen K. B. 1999; Palmitoylation of the intracytoplasmic R peptide of the transmembrane envelope protein in Moloney murine leukemia virus. J Virol 73:8975–8981
     [Google Scholar]
  23. Oshima M., Muriaux D., Mirro J., Nagashima K., Dryden K., Yeager M., Rein A. 2004; Effects of blocking individual maturation cleavages in murine leukemia virus Gag. J Virol 78:1411–1420 [CrossRef]
     [Google Scholar]
  24. Parker S. D., Hunter E. 2000; A cell-line-specific defect in the intracellular transport and release of assembled retroviral capsids. J Virol 74:784–795 [CrossRef]
     [Google Scholar]
  25. Parker S. D., Wall J. S., Hunter E. 2001; Analysis of Mason-Pfizer monkey virus Gag particles by scanning transmission electron microscopy. J Virol 75:9543–9548 [CrossRef]
     [Google Scholar]
  26. Ragheb J. A., Anderson W. F. 1994; pH-independent murine leukemia virus ecotropic envelope-mediated cell fusion: implications for the role of the R peptide and p12E TM in viral entry. J Virol 68:3220–3231
     [Google Scholar]
  27. Reik W., Weiher H., Jaenisch R. 1985; Replication-competent Moloney murine leukemia virus carrying a bacterial suppressor tRNA gene: selective cloning of proviral and flanking host sequences. Proc Natl Acad Sci U S A 82:1141–1145 [CrossRef]
     [Google Scholar]
  28. Rein A., Mirro J., Haynes J. G., Ernst S. M., Nagashima K. 1994; Function of the cytoplasmic domain of a retroviral transmembrane protein: p15E-p2E cleavage activates the membrane fusion capability of the murine leukemia virus Env protein. J Virol 68:1773–1781
     [Google Scholar]
  29. Schägger H., von Jagow G. 1987; Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal Biochem 166:368–379 [CrossRef]
     [Google Scholar]
  30. Sharma S., Murai F., Miyanohara A., Friedmann T. 1997; Noninfectious virus-like particles produced by Moloney murine leukemia virus-based retrovirus packaging cells deficient in viral envelope become infectious in the presence of lipofection reagents. Proc Natl Acad Sci U S A 94:10803–10808 [CrossRef]
     [Google Scholar]
  31. Sherer N. M., Lehmann M. J., Jimenez-Soto L. F. & 7 other authors 2003; Visualization of retroviral replication in living cells reveals budding into multivesicular bodies. Traffic 4:785–801 [CrossRef]
     [Google Scholar]
  32. Suomalainen M., Hultenby K., Garoff H. 1996; Targeting of Moloney murine leukemia virus Gag precursor to the site of virus budding. J Cell Biol 135:1841–1852 [CrossRef]
     [Google Scholar]
  33. Wilk T., Gowen B., Fuller S. D. 1999; Actin associates with the nucleocapsid domain of the human immunodeficiency virus Gag polyprotein. J Virol 73:1931–1940
     [Google Scholar]
  34. Wyma D. J., Kotov A., Aiken C. 2000; Evidence for a stable interaction of gp41 with Pr55Gag in immature human immunodeficiency virus type 1 particles. J Virol 74:9381–9387 [CrossRef]
     [Google Scholar]
  35. Wyma D. J., Jiang J., Shi J., Zhou J., Lineberger J. E., Miller M. D., Aiken C. 2004; Coupling of human immunodeficiency virus type 1 fusion to virion maturation: a novel role of the gp41 cytoplasmic tail. J Virol 78:3429–3435 [CrossRef]
     [Google Scholar]
  36. Yu X., Yuan X., Matsuda Z., Lee T.-H., Essex M. 1992; The matrix protein of human immunodeficiency virus type 1 is required for incorporation of viral envelope protein into mature virions. J Virol 66:4966–4971
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.81527-0
Loading
Murine leukemia virus transmembrane protein R-peptide is found in small virus core-like complexes in cells
J. Gen. Virol. 87, 1583 (2006); https://doi.org/10.1099/vir.0.81527-0
/content/journal/jgv/10.1099/vir.0.81527-0
/content/journal/jgv/10.1099/vir.0.81527-0
Loading

Data & Media loading...

Most cited Most Cited RSS feed

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