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
Services
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 Patnaik, A.
Right arrow Articles by Wills, J. W.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Patnaik, A.
Right arrow Articles by Wills, J. W.

 Previous Article  |  Next Article 

Journal of Virology, March 2002, p. 2641-2647, Vol. 76, No. 6
0022-538X/02/$04.00+0     DOI: 10.1128/JVI.76.6.2641-2647.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.

Budding of Equine Infectious Anemia Virus Is Insensitive to Proteasome Inhibitors

Akash Patnaik,1 Vincent Chau,2 Feng Li,3 Ronald C. Montelaro,3 and John W. Wills1*

Department of Microbiology and Immunology,1 Department of Cellular and Molecular Physiology, The Pennsylvania State University College of Medicine, Hershey, Pennsylvania 17033,2 Department of Molecular Genetics and Biochemistry, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania 152613

Received 31 August 2001/ Accepted 12 December 2001

The only retrovirus protein required for the budding of virus-like particles is the Gag protein; however, recent studies of Rous sarcoma virus (RSV) and human immunodeficiency virus have suggested that modification of Gag with ubiquitin (Ub) is also required. As a consequence, the release of these viruses is reduced in the presence of proteasome inhibitors, which indirectly reduce the levels of free Ub within the cell. Here we show that the budding of equine infectious anemia virus (EIAV) from infected equine cells is largely unaffected by these drugs, although use of one inhibitor (MG-132) resulted in a dramatic block to proteolytic processing of Gag. This lack of sensitivity was also observed in transiently transfected avian cells under conditions that greatly reduce RSV budding. Moreover, insensitivity was observed when the EIAV Gag protein was expressed in the absence of all the other virus products, indicating that they are not required for this phenotype. An activity that enables EIAV to tolerate exposure to proteasome inhibitors was mapped to the C-terminal p9 sequence, as demonstrated by the ability of an RSV Gag-p9 chimera to bud in the presence of the drugs. Intriguingly, the p9 sequence contains a short sequence motif that is similar to a surface-exposed helix of Ub, suggesting that EIAV Gag may have captured a function that allows it to bypass the need for ubiquitination. Thus, the mechanism of EIAV budding may not be substantially different from that of other retroviruses, even though it behaves differently in the presence of proteasome inhibitors.

* Corresponding author. Mailing address: Department of Microbiology and Immunology, The Pennsylvania State University College of Medicine, 500 University Dr., P.O. Box 850, Hershey, PA 17033. Phone: (717) 531-3528. Fax: (717) 531-6522. E-mail: jwills{at}psu.edu.

Journal of Virology, March 2002, p. 2641-2647, Vol. 76, No. 6
0022-538X/02/$04.00+0     DOI: 10.1128/JVI.76.6.2641-2647.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Utley, T. J., Ducharme, N. A., Varthakavi, V., Shepherd, B. E., Santangelo, P. J., Lindquist, M. E., Goldenring, J. R., Crowe, J. E. Jr. (2008). Respiratory syncytial virus uses a Vps4-independent budding mechanism controlled by Rab11-FIP2. Proc. Natl. Acad. Sci. USA 105: 10209-10214 [Abstract] [Full Text]  
  • Luttge, B. G., Shehu-Xhilaga, M., Demirov, D. G., Adamson, C. S., Soheilian, F., Nagashima, K., Stephen, A. G., Fisher, R. J., Freed, E. O. (2008). Molecular Characterization of Feline Immunodeficiency Virus Budding. J. Virol. 82: 2106-2119 [Abstract] [Full Text]  
  • Taylor, G. M., Hanson, P. I., Kielian, M. (2007). Ubiquitin Depletion and Dominant-Negative VPS4 Inhibit Rhabdovirus Budding without Affecting Alphavirus Budding. J. Virol. 81: 13631-13639 [Abstract] [Full Text]  
  • Jin, J., Sturgeon, T., Chen, C., Watkins, S. C., Weisz, O. A., Montelaro, R. C. (2007). Distinct Intracellular Trafficking of Equine Infectious Anemia Virus and Human Immunodeficiency Virus Type 1 Gag during Viral Assembly and Budding Revealed by Bimolecular Fluorescence Complementation Assays. J. Virol. 81: 11226-11235 [Abstract] [Full Text]  
  • Calistri, A., Sette, P., Salata, C., Cancellotti, E., Forghieri, C., Comin, A., Gottlinger, H., Campadelli-Fiume, G., Palu, G., Parolin, C. (2007). Intracellular Trafficking and Maturation of Herpes Simplex Virus Type 1 gB and Virus Egress Require Functional Biogenesis of Multivesicular Bodies. J. Virol. 81: 11468-11478 [Abstract] [Full Text]  
  • Munshi, U. M., Kim, J., Nagashima, K., Hurley, J. H., Freed, E. O. (2007). An Alix Fragment Potently Inhibits HIV-1 Budding: CHARACTERIZATION OF BINDING TO RETROVIRAL YPXL LATE DOMAINS. J. Biol. Chem. 282: 3847-3855 [Abstract] [Full Text]  
  • Odorizzi, G. (2006). The multiple personalities of Alix.. J. Cell Sci. 119: 3025-3032 [Abstract] [Full Text]  
  • Gottwein, E., Jager, S., Habermann, A., Krausslich, H.-G. (2006). Cumulative mutations of ubiquitin acceptor sites in human immunodeficiency virus type 1 gag cause a late budding defect.. J. Virol. 80: 6267-6275 [Abstract] [Full Text]  
  • Noble, B., Abada, P., Nunez-Iglesias, J., Cannon, P. M. (2006). Recruitment of the Adaptor Protein 2 Complex by the Human Immunodeficiency Virus Type 2 Envelope Protein Is Necessary for High Levels of Virus Release. J. Virol. 80: 2924-2932 [Abstract] [Full Text]  
  • Hui, E. K.-W., Barman, S., Tang, D. H.-P., France, B., Nayak, D. P. (2006). YRKL Sequence of Influenza Virus M1 Functions as the L Domain Motif and Interacts with VPS28 and Cdc42. J. Virol. 80: 2291-2308 [Abstract] [Full Text]  
  • Ott, D. E., Coren, L. V., Gagliardi, T. D., Nagashima, K. (2005). Heterologous Late-Domain Sequences Have Various Abilities To Promote Budding of Human Immunodeficiency Virus Type 1. J. Virol. 79: 9038-9045 [Abstract] [Full Text]  
  • Gottwein, E., Krausslich, H.-G. (2005). Analysis of Human Immunodeficiency Virus Type 1 Gag Ubiquitination. J. Virol. 79: 9134-9144 [Abstract] [Full Text]  
  • Johnson, M. C., Spidel, J. L., Ako-Adjei, D., Wills, J. W., Vogt, V. M. (2005). The C-Terminal Half of TSG101 Blocks Rous Sarcoma Virus Budding and Sequesters Gag into Unique Nonendosomal Structures. J. Virol. 79: 3775-3786 [Abstract] [Full Text]  
  • Schmitt, A. P., Leser, G. P., Morita, E., Sundquist, W. I., Lamb, R. A. (2005). Evidence for a New Viral Late-Domain Core Sequence, FPIV, Necessary for Budding of a Paramyxovirus. J. Virol. 79: 2988-2997 [Abstract] [Full Text]  
  • Martin-Serrano, J., Eastman, S. W., Chung, W., Bieniasz, P. D. (2005). HECT ubiquitin ligases link viral and cellular PPXY motifs to the vacuolar protein-sorting pathway. JCB 168: 89-101 [Abstract] [Full Text]  
  • Spidel, J. L., Craven, R. C., Wilson, C. B., Patnaik, A., Wang, H., Mansky, L. M., Wills, J. W. (2004). Lysines Close to the Rous Sarcoma Virus Late Domain Critical for Budding. J. Virol. 78: 10606-10616 [Abstract] [Full Text]  
  • Martin-Serrano, J., Perez-Caballero, D., Bieniasz, P. D. (2004). Context-Dependent Effects of L Domains and Ubiquitination on Viral Budding. J. Virol. 78: 5554-5563 [Abstract] [Full Text]  
  • Blot, V., Perugi, F., Gay, B., Prevost, M.-C., Briant, L., Tangy, F., Abriel, H., Staub, O., Dokhelar, M.-C., Pique, C. (2004). Nedd4.1-mediated ubiquitination and subsequent recruitment of Tsg101 ensure HTLV-1 Gag trafficking towards the multivesicular body pathway prior to virus budding. J. Cell Sci. 117: 2357-2367 [Abstract] [Full Text]  
  • Wang, H., Machesky, N. J., Mansky, L. M. (2004). Both the PPPY and PTAP Motifs Are Involved in Human T-Cell Leukemia Virus Type 1 Particle Release. J. Virol. 78: 1503-1512 [Abstract] [Full Text]  
  • Shehu-Xhilaga, M., Ablan, S., Demirov, D. G., Chen, C., Montelaro, R. C., Freed, E. O. (2004). Late Domain-Dependent Inhibition of Equine Infectious Anemia Virus Budding. J. Virol. 78: 724-732 [Abstract] [Full Text]  
  • Bouamr, F., Melillo, J. A., Wang, M. Q., Nagashima, K., de Los Santos, M., Rein, A., Goff, S. P. (2003). PPPYEPTAP Motif Is the Late Domain of Human T-Cell Leukemia Virus Type 1 Gag and Mediates Its Functional Interaction with Cellular Proteins Nedd4 and Tsg101. J. Virol. 77: 11882-11895 [Abstract] [Full Text]  
  • Martin-Serrano, J., Yarovoy, A., Perez-Caballero, D., Bieniasz, P. D. (2003). Divergent retroviral late-budding domains recruit vacuolar protein sorting factors by using alternative adaptor proteins. Proc. Natl. Acad. Sci. USA 100: 12414-12419 [Abstract] [Full Text]  
  • Tanzi, G. O., Piefer, A. J., Bates, P. (2003). Equine Infectious Anemia Virus Utilizes Host Vesicular Protein Sorting Machinery during Particle Release. J. Virol. 77: 8440-8447 [Abstract] [Full Text]  
  • Martin-Serrano, J., Zang, T., Bieniasz, P. D. (2003). Role of ESCRT-I in Retroviral Budding. J. Virol. 77: 4794-4804 [Abstract] [Full Text]  
  • Ott, D. E., Coren, L. V., Sowder, R. C. II, Adams, J., Schubert, U. (2003). Retroviruses Have Differing Requirements for Proteasome Function in the Budding Process. J. Virol. 77: 3384-3393 [Abstract] [Full Text]  
  • Licata, J. M., Simpson-Holley, M., Wright, N. T., Han, Z., Paragas, J., Harty, R. N. (2003). Overlapping Motifs (PTAP and PPEY) within the Ebola Virus VP40 Protein Function Independently as Late Budding Domains: Involvement of Host Proteins TSG101 and VPS-4. J. Virol. 77: 1812-1819 [Abstract] [Full Text]  
  • Freed, E. O. (2002). Viral Late Domains. J. Virol. 76: 4679-4687 [Full Text]  


Copyright © 2009 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»