This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow E-mail this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Pietschmann, T.
Right arrow Articles by Lindemann, D.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Pietschmann, T.
Right arrow Articles by Lindemann, D.

 Previous Article  |  Next Article 

Journal of Virology, April 1999, p. 2613-2621, Vol. 73, No. 4
0022-538X/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.

Foamy Virus Capsids Require the Cognate Envelope Protein for Particle Export

Thomas Pietschmann,1 Martin Heinkelein,1 Martina Heldmann,2 Hanswalter Zentgraf,3 Axel Rethwilm,1,4,* and Dirk Lindemann1

Institut für Virologie und Immunbiologie1 and Klinik und Poliklinik für Haut- und Geschlechtskrankheiten,2 Universität Würzburg, Würzburg, Angewandte Tumorvirologie, Deutsches Krebsforschungszentrum, Heidelberg,3 and Institut für Virologie, Medizinische Fakultät Carl Gustav Carus, Technische Universität Dresden,4 Germany

Received 17 August 1998/Accepted 14 December 1998

Unlike other subclasses of the Retroviridae the Spumavirinae, its prototype member being the so-called human foamy virus (HFV), require the expression of the envelope (Env) glycoprotein for viral particle egress. Both the murine leukemia virus (MuLV) Env and the vesicular stomatitis virus G protein, which efficiently pseudotype other retrovirus capsids, were not able to support export of HFV particles. Analysis of deletion and point mutants of the HFV Env protein revealed that the HFV Env cytoplasmic domain (CyD) is dispensable for HFV particle envelopment, release, and infectivity, whereas deletion of the membrane-spanning-domain (MSD) led to an accumulation of naked capsids in the cytoplasm. Neither alternative membrane association of HFV Env deletion mutants lacking the MSD and CyD via phosphoglycolipid anchor nor domain swapping mutants, with the MSD or CyD of MuLV Env and VSV-G exchanged against the corresponding HFV domains, could restore particle envelopment and the release defect of pseudotypes. However, replacement of the HFV MSD with that of MuLV led to budding of HFV capsids at the intracellular membranes. These virions were of apparently wild-type morphology but were not naturally released into the supernatant and they were noninfectious.


* Corresponding author. Present address: Institut für Virologie, Medizinische Fakultät Carl Gustav Carus, Technische Universität Dresden, Gerichtsstr. 5, 01069 Dresden, Germany. Phone: (49)-351-441-5739. Fax: (49)-351-459-3530. E-mail: Axel.Rethwilm{at}mailbox.tu-dresden.de.


Journal of Virology, April 1999, p. 2613-2621, Vol. 73, No. 4
0022-538X/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.



This article has been cited by other articles:

  • Perkovic, M., Schmidt, S., Marino, D., Russell, R. A., Stauch, B., Hofmann, H., Kopietz, F., Kloke, B.-P., Zielonka, J., Strover, H., Hermle, J., Lindemann, D., Pathak, V. K., Schneider, G., Lochelt, M., Cichutek, K., Munk, C. (2009). Species-specific Inhibition of APOBEC3C by the Prototype Foamy Virus Protein Bet. J. Biol. Chem. 284: 5819-5826 [Abstract] [Full Text]  
  • Jouvenet, N., Neil, S. J. D., Zhadina, M., Zang, T., Kratovac, Z., Lee, Y., McNatt, M., Hatziioannou, T., Bieniasz, P. D. (2009). Broad-Spectrum Inhibition of Retroviral and Filoviral Particle Release by Tetherin. J. Virol. 83: 1837-1844 [Abstract] [Full Text]  
  • Stange, A., Luftenegger, D., Reh, J., Weissenhorn, W., Lindemann, D. (2008). Subviral Particle Release Determinants of Prototype Foamy Virus. J. Virol. 82: 9858-9869 [Abstract] [Full Text]  
  • Life, R. B., Lee, E.-G., Eastman, S. W., Linial, M. L. (2008). Mutations in the Amino Terminus of Foamy Virus Gag Disrupt Morphology and Infectivity but Do Not Target Assembly. J. Virol. 82: 6109-6119 [Abstract] [Full Text]  
  • Yap, M. W., Lindemann, D., Stanke, N., Reh, J., Westphal, D., Hanenberg, H., Ohkura, S., Stoye, J. P. (2008). Restriction of Foamy Viruses by Primate Trim5{alpha}. J. Virol. 82: 5429-5439 [Abstract] [Full Text]  
  • Kohl, R., Preiss, S., von Knethen, A., Brune, B. (2006). Oxidized low-density lipoprotein depletes PKC{alpha} and attenuates reactive oxygen species formation in monocytes/macrophages. Cardiovasc Res 71: 574-585 [Abstract] [Full Text]  
  • Nowrouzi, A., Dittrich, M., Klanke, C., Heinkelein, M., Rammling, M., Dandekar, T., von Kalle, C., Rethwilm, A. (2006). Genome-wide mapping of foamy virus vector integrations into a human cell line.. J. Gen. Virol. 87: 1339-1347 [Abstract] [Full Text]  
  • Stanke, N., Stange, A., Luftenegger, D., Zentgraf, H., Lindemann, D. (2005). Ubiquitination of the Prototype Foamy Virus Envelope Glycoprotein Leader Peptide Regulates Subviral Particle Release. J. Virol. 79: 15074-15083 [Abstract] [Full Text]  
  • Cartellieri, M., Herchenroder, O., Rudolph, W., Heinkelein, M., Lindemann, D., Zentgraf, H., Rethwilm, A. (2005). N-Terminal Gag Domain Required for Foamy Virus Particle Assembly and Export. J. Virol. 79: 12464-12476 [Abstract] [Full Text]  
  • Feldhahn, N., Rio, P., Soh, B. N. B., Liedtke, S., Sprangers, M., Klein, F., Wernet, P., Jumaa, H., Hofmann, W.-K., Hanenberg, H., Rowley, J. D., Muschen, M. (2005). Deficiency of Bruton's tyrosine kinase in B cell precursor leukemia cells. Proc. Natl. Acad. Sci. USA 102: 13266-13271 [Abstract] [Full Text]  
  • Dodding, M. P., Bock, M., Yap, M. W., Stoye, J. P. (2005). Capsid Processing Requirements for Abrogation of Fv1 and Ref1 Restriction. J. Virol. 79: 10571-10577 [Abstract] [Full Text]  
  • Russell, R. A., Wiegand, H. L., Moore, M. D., Schafer, A., McClure, M. O., Cullen, B. R. (2005). Foamy Virus Bet Proteins Function as Novel Inhibitors of the APOBEC3 Family of Innate Antiretroviral Defense Factors. J. Virol. 79: 8724-8731 [Abstract] [Full Text]  
  • Lehmann-Che, J., Giron, M.-L., Delelis, O., Lochelt, M., Bittoun, P., Tobaly-Tapiero, J., de The, H., Saib, A. (2005). Protease-Dependent Uncoating of a Complex Retrovirus. J. Virol. 79: 9244-9253 [Abstract] [Full Text]  
  • Luftenegger, D., Picard-Maureau, M., Stanke, N., Rethwilm, A., Lindemann, D. (2005). Analysis and Function of Prototype Foamy Virus Envelope N Glycosylation. J. Virol. 79: 7664-7672 [Abstract] [Full Text]  
  • Patton, G. S., Morris, S. A., Chung, W., Bieniasz, P. D., McClure, M. O. (2005). Identification of Domains in Gag Important for Prototypic Foamy Virus Egress. J. Virol. 79: 6392-6399 [Abstract] [Full Text]  
  • von Knethen, A., Tautenhahn, A., Link, H., Lindemann, D., Brune, B. (2005). Activation-Induced Depletion of Protein Kinase C{alpha} Provokes Desensitization of Monocytes/Macrophages in Sepsis. J. Immunol. 174: 4960-4965 [Abstract] [Full Text]  
  • Geiselhart, V., Bastone, P., Kempf, T., Schnolzer, M., Lochelt, M. (2004). Furin-Mediated Cleavage of the Feline Foamy Virus Env Leader Protein. J. Virol. 78: 13573-13581 [Abstract] [Full Text]  
  • Duda, A., Stange, A., Luftenegger, D., Stanke, N., Westphal, D., Pietschmann, T., Eastman, S. W., Linial, M. L., Rethwilm, A., Lindemann, D. (2004). Prototype Foamy Virus Envelope Glycoprotein Leader Peptide Processing Is Mediated by a Furin-Like Cellular Protease, but Cleavage Is Not Essential for Viral Infectivity. J. Virol. 78: 13865-13870 [Abstract] [Full Text]  
  • Patton, G. S., Erlwein, O., McClure, M. O. (2004). Cell-cycle dependence of foamy virus vectors. J. Gen. Virol. 85: 2925-2930 [Abstract] [Full Text]  
  • Kreiss, M., Asmuss, A., Krejci, K., Lindemann, D., Miyoshi-Akiyama, T., Uchiyama, T., Rink, L., Broeren, C. P. M., Herrmann, T. (2004). Contrasting contributions of complementarity-determining region 2 and hypervariable region 4 of rat BV8S2+ (V{beta}8.2) TCR to the recognition of myelin basic protein and different types of bacterial superantigens. Int Immunol 16: 655-663 [Abstract] [Full Text]  
  • Dressel, R., Grzeszik, C., Kreiss, M., Lindemann, D., Herrmann, T., Walter, L., Gunther, E. (2003). Differential Effect of Acute and Permanent Heat Shock Protein 70 Overexpression in Tumor Cells on Lysability by Cytotoxic T Lymphocytes. Cancer Res. 63: 8212-8220 [Abstract] [Full Text]  
  • Roy, J., Rudolph, W., Juretzek, T., Gartner, K., Bock, M., Herchenroder, O., Lindemann, D., Heinkelein, M., Rethwilm, A. (2003). Feline Foamy Virus Genome and Replication Strategy. J. Virol. 77: 11324-11331 [Abstract] [Full Text]  
  • Heinkelein, M., Rammling, M., Juretzek, T., Lindemann, D., Rethwilm, A. (2003). Retrotransposition and Cell-to-Cell Transfer of Foamy Viruses. J. Virol. 77: 11855-11858 [Abstract] [Full Text]  
  • Petit, C., Giron, M.-L., Tobaly-Tapiero, J., Bittoun, P., Real, E., Jacob, Y., Tordo, N., de The, H., Saib, A. (2003). Targeting of incoming retroviral Gag to the centrosome involves a direct interaction with the dynein light chain 8. J. Cell Sci. 116: 3433-3442 [Abstract] [Full Text]  
  • Shikova-Lekova, E., Lindemann, D., Pietschmann, T., Juretzek, T., Rudolph, W., Herchenroder, O., Gelderblom, H. R., Rethwilm, A. (2003). Replication-Competent Hybrids between Murine Leukemia Virus and Foamy Virus. J. Virol. 77: 7677-7681 [Abstract] [Full Text]  
  • Fehrmann, F., Jung, M., Zimmermann, R., Krausslich, H.-G. (2003). Transport of the Intracisternal A-Type Particle Gag Polyprotein to the Endoplasmic Reticulum Is Mediated by the Signal Recognition Particle. J. Virol. 77: 6293-6304 [Abstract] [Full Text]  
  • Luhder, F., Huang, Y., Dennehy, K. M., Guntermann, C., Muller, I., Winkler, E., Kerkau, T., Ikemizu, S., Davis, S. J., Hanke, T., Hunig, T. (2003). Topological Requirements and Signaling Properties of T Cell-activating, Anti-CD28 Antibody Superagonists. JEM 197: 955-966 [Abstract] [Full Text]  
  • Picard-Maureau, M., Jarmy, G., Berg, A., Rethwilm, A., Lindemann, D. (2003). Foamy Virus Envelope Glycoprotein-Mediated Entry Involves a pH-Dependent Fusion Process. J. Virol. 77: 4722-4730 [Abstract] [Full Text]  
  • Shaw, K. L., Lindemann, D., Mulligan, M. J., Goepfert, P. A. (2003). Foamy Virus Envelope Glycoprotein Is Sufficient for Particle Budding and Release. J. Virol. 77: 2338-2348 [Abstract] [Full Text]  
  • Heinkelein, M., Leurs, C., Rammling, M., Peters, K., Hanenberg, H., Rethwilm, A. (2002). Pregenomic RNA Is Required for Efficient Incorporation of Pol Polyprotein into Foamy Virus Capsids. J. Virol. 76: 10069-10073 [Abstract] [Full Text]  
  • Lecellier, C.-H., Neves, M., Giron, M.-L., Tobaly-Tapiero, J., Saib, A. (2002). Further Characterization of Equine Foamy Virus Reveals Unusual Features among the Foamy Viruses. J. Virol. 76: 7220-7227 [Abstract] [Full Text]  
  • Lecellier, C.-H., Vermeulen, W., Bachelerie, F., Giron, M.-L., Saib, A. (2002). Intra- and Intercellular Trafficking of the Foamy Virus Auxiliary Bet Protein. J. Virol. 76: 3388-3394 [Abstract] [Full Text]  
  • Hatama, S., Otake, K., Omoto, S., Murase, Y., Ikemoto, A., Mochizuki, M., Takahashi, E., Okuyama, H., Fujii, Y. (2001). Isolation and sequencing of infectious clones of feline foamy virus and a human/feline foamy virus Env chimera. J. Gen. Virol. 82: 2999-3004 [Abstract] [Full Text]  
  • Wilk, T., Geiselhart, V., Frech, M., Fuller, S. D., Flugel, R. M., Lochelt, M. (2001). Specific Interaction of a Novel Foamy Virus Env Leader Protein with the N-Terminal Gag Domain. J. Virol. 75: 7995-8007 [Abstract] [Full Text]  
  • Lindemann, D., Pietschmann, T., Picard-Maureau, M., Berg, A., Heinkelein, M., Thurow, J., Knaus, P., Zentgraf, H., Rethwilm, A. (2001). A Particle-Associated Glycoprotein Signal Peptide Essential for Virus Maturation and Infectivity. J. Virol. 75: 5762-5771 [Abstract] [Full Text]  
  • Tobaly-Tapiero, J., Bittoun, P., Giron, M.-L., Neves, M., Koken, M., Saib, A., de The, H. (2001). Human Foamy Virus Capsid Formation Requires an Interaction Domain in the N Terminus of Gag. J. Virol. 75: 4367-4375 [Abstract] [Full Text]  
  • Cain, D., Erlwein, O., Grigg, A., Russell, R. A., McClure, M. O. (2001). Palindromic Sequence Plays a Critical Role in Human Foamy Virus Dimerization. J. Virol. 75: 3731-3739 [Abstract] [Full Text]  
  • Meiering, C. D., Maxine L. Linial, (2001). Historical Perspective of Foamy Virus Epidemiology and Infection. Clin. Microbiol. Rev. 14: 165-176 [Abstract] [Full Text]  
  • Pietschmann, T., Zentgraf, H., Rethwilm, A., Lindemann, D. (2000). An Evolutionarily Conserved Positively Charged Amino Acid in the Putative Membrane-Spanning Domain of the Foamy Virus Envelope Protein Controls Fusion Activity. J. Virol. 74: 4474-4482 [Abstract] [Full Text]  
  • Heinkelein, M., Thurow, J., Dressler, M., Imrich, H., Neumann-Haefelin, D., McClure, M. O., Rethwilm, A. (2000). Complex Effects of Deletions in the 5' Untranslated Region of Primate Foamy Virus on Viral Gene Expression and RNA Packaging. J. Virol. 74: 3141-3148 [Abstract] [Full Text]  
  • Bansal, A., Shaw, K. L., Edwards, B. H., Goepfert, P. A., Mulligan, M. J. (2000). Characterization of the R572T Point Mutant of a Putative Cleavage Site in Human Foamy Virus Env. J. Virol. 74: 2949-2954 [Abstract] [Full Text]  
  • Wang, G., Mulligan, M. J., Baldwin, D. N., Linial, M. L. (1999). Endogenous Virus of BHK-21 Cells Complicates Electron Microscopy Studies of Foamy Virus Maturation. J. Virol. 73: 8917-8917 [Full Text]  
  • Enssle, J, Moebes, A, Heinkelein, M, Panhuysen, M, Mauer, B, Schweizer, M, Neumann-Haefelin, D, Rethwilm, A (1999). An active foamy virus integrase is required for virus replication. J. Gen. Virol. 80: 1445-1452 [Abstract]