This Article
Right arrow Abstract Freely available
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 Puffer, B. A.
Right arrow Articles by Montelaro, R. C.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Puffer, B. A.
Right arrow Articles by Montelaro, R. C.

 Previous Article  |  Next Article 

Journal of Virology, December 1998, p. 10218-10221, Vol. 72, No. 12
0022-538X/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.

Equine Infectious Anemia Virus Gag Polyprotein Late Domain Specifically Recruits Cellular AP-2 Adapter Protein Complexes during Virion Assembly

Bridget A. Puffer,1 S. C. Watkins,2 and Ronald C. Montelaro1,*

Department of Molecular Genetics and Biochemistry1 and Department of Cell Biology and Physiology,2 University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania 15261

Received 16 June 1998/Accepted 21 August 1998

    ABSTRACT
Top
Abstract
Text
References

We have identified an interaction between the equine infectious anemia virus (EIAV) late assembly domain and the cellular AP-2 clathrin-associated adapter protein complex. A YXXL motif within the EIAV Gag late assembly domain was previously characterized as a sequence critical for release of assembling virions. We now show that this YXXL sequence interacts in vitro with the AP-50 subunit of the AP-2 complex, while the functionally interchangeable late assembly domains carried by the Rous sarcoma virus p2b protein and human immunodeficiency virus type 1 p6 protein, which utilize PPPY and PTAPP L domains, respectively, do not bind AP-50 in vitro. In addition, EIAV late domain mutants containing mutations that have previously been shown to abrogate budding also exhibit marked decreases in AP-50 binding efficiencies. A role for AP-2 complex in viral assembly is supported by immunofluorescence analysis of EIAV-infected equine dermal cells demonstrating specific colocalization of the alpha  adaptin subunit of AP-2 with the EIAV p9 protein at sites of virus budding on the plasma membrane. These data provide strong evidence that EIAV utilizes the cellular AP-2 complex to accomplish virion assembly and release.

    TEXT
Top
Abstract
Text
References

The assembly of retroviral particles is driven by the Gag polyprotein. Gag polyproteins are synthesized in the cytoplasm from genome-length mRNA and are targeted to the plasma membrane, where approximately 2,000 associate to form immature budding particles (21). Maturation of the virion to an infectious particle occurs at some point either late in budding or immediately after release of the virus particle when the Gag polyproteins are processed by the virus-encoded protease. The equine infectious anemia virus (EIAV) Gag polyprotein is processed to generate the matrix (MA; p15), capsid (CA; p26), nucleocapsid (NC; p11), and p9 proteins (8, 11). The p9 sequence at the C terminus of Gag has been shown to function at a point late in virus assembly and is critical for release of assembled virus particles (14, 16). The human immunodeficiency virus type 1 (HIV-1) p6, Rous sarcoma virus (RSV) p2b, and EIAV p9 proteins were identified to be functional homologs by construction of chimeric Gag polyproteins and analysis of particle assembly (14, 16). While HIV-1 p6, RSV p2b and EIAV p9 are functionally interchangeable, they share little amino acid sequence similarity. It has been determined that a PTAP sequence contained in HIV-1 p6 and conserved among all lentiviruses, with the exception of EIAV, was critical for late domain function (4, 7, 9). This sequence is suggestive of PXXP binding motifs which have been shown to interact with the SH3 domain protein structural module (15). Mutational analysis of RSV p2b and, recently, pp16 of Mason-Pfizer monkey virus identified a PPPY sequence, also highly conserved among the oncoviruses, as being critical for late domain function (22-25). This motif has been shown to interact with a semiconserved structural module referred to as a WW domain (3, 19). The interaction was verified in vitro; however, the "natural partner" in vivo remains to be defined (6).

Alanine scanning mutagenesis of the EIAV late assembly (L) domain identified p9 amino acids Y23, P24, and L26 (YPXL) as critical for a functional late assembly domain, suggesting a YXXL motif (16). YXXL sequences in other proteins have been shown to bind the medium chain subunits of the AP-1 and AP-2 clathrin-associated adapter protein complexes by the yeast two-hybrid assay, and this interaction has been characterized in vitro (13, 20). Based upon this observation, we decided to examine possible interactions between retroviral late assembly domains and the medium chain (AP-50 subunit) of the plasma membrane-localized AP-2 clathrin-associated adapter protein complex. Glutathione S-transferase (GST) and a GST-p9 fusion protein (encoding the first 30 residues of p9) were purified and analyzed for binding to a truncated AP-50 subunit (residues 121 to 435) in a standard binding assay (13). Figure 1 shows that while GST alone did not bind to AP-50 (Fig. 1, lane 1), the GST-p9 protein was able to bind and precipitate AP-50 (Fig. 1, lane 2). We also tested the PTAPP sequence of HIV-1 (in p6) and the PPPPY sequence of RSV (in p2b) for binding to AP-50. The GST-p6 and GST-p2b proteins both failed to bind and precipitate AP-50 (Fig. 1, lanes 3 and 4, respectively). Thus, in vitro the EIAV YXXL sequence critical for release of budding virions does interact with the AP-50 subunit of AP-2, and this binding is specific for the EIAV p9 late domain.


View larger version (59K):
[in this window]
[in a new window]
  		FIG. 1.   Analysis of AP-50 binding to retroviral late domains in the context of GST fusion proteins. Truncated AP-50 was synthesized from the 3M9 cDNA in vitro by using the TNT Quick Coupled Master mix reticulocyte lysate with [35S]methionine. Binding to 10 µg of an eluted GST fusion protein was initiated in 600 µl of binding buffer (0.05% Triton X-100, 50 mM HEPES [pH 7.3], 10% glycerol, 0.1% bovine serum albumin), and protein complexes were precipitated with glutathione-Sepharose beads, washed twice with binding buffer, washed once with binding buffer supplemented with 100 mM NaCl, resolved by sodium dodecyl sulfate-12% polyacrylamide gel electrophoresis, and detected by autoradiography.

To further test our hypothesis that the EIAV L domain interacts with AP-50 to facilitate virion assembly, we constructed EIAV L domain GST fusion protein analogs containing late domain alanine scanning mutations that were shown to be functionally defective in a COS-1 cellular budding assay (16). GST-p9 fusion proteins containing substitution of residue Y23, P24, or L26 with alanine were tested with the in vitro AP-50 binding assay, and the resultant bands were quantitated by densitometry and normalized to the value obtained for GST-p9. We observed that alanine substitution for either Y23, P24, or L26 resulted in a decrease in the ability to bind AP-50 (Fig. 2, lanes 3, 4, and 5, respectively) when compared to GST-p9 binding (Fig. 2, lane 2), reflecting the activity levels obtained in a COS-1 cell budding assay (16). Quantitation of AP-50 bound by GST-p9 analogs demonstrated an average 75% decrease in AP-50 binding compared to the level observed for the GST-p9 wild-type sequence (Fig. 2B), in spite of the high concentrations of protein contained in the reaction mixtures.


View larger version (23K):
[in this window]
[in a new window]
  		FIG. 2.   Analysis of AP-50 binding by EIAV late assembly domain wild-type and mutant sequences. (A) Binding activity was determined as described in the legend to Fig. 1. (B) Quantitation of binding efficiencies relative to that of the native p9 late domain sequence.

Having identified an in vitro interaction between AP-50 and EIAV p9, we next used immunofluorescence analysis to determine whether these proteins colocalize in EIAV-infected cells. To determine if the AP-2 complex associates with EIAV p9, we obtained a commercially available monoclonal antibody directed against the alpha  adaptin subunit, a component of adapter protein complexes that is specific for the plasma membrane-localized complex AP-2 (1, 17, 18). Infected and uninfected equine dermal (ED) cells were fixed, permeabilized, labeled with anti-alpha adaptin and anti-EIAV p9, and examined by fluorescence microscopy. Examination of uninfected ED cells for alpha  adaptin demonstrated a diffuse staining throughout the cell, typical of alpha  adaptin staining (Fig. 3E) (1, 17, 18). Visualization of adaptin staining in EIAV-infected cells (Fig. 3B) revealed normal diffuse staining, in addition to specific sites of concentrated adaptin staining at the plasma membrane of the cell and intense apparently intracellular staining corresponding to a perinuclear localization (Fig. 3B). Visualization of the anti-p9 staining in uninfected cells demonstrated the absence of background antibody reactivity (Fig. 3D). In marked contrast to uninfected cells, infected ED cells showed intense p9 staining of virions at the plasma membrane, as well as an apparently perinuclear staining (Fig. 3A). To identify sites of colocalized adaptin and p9, the Cy3 and fluorescein isothiocyanate staining patterns were merged (Fig. 3C). Importantly, the pattern of dual staining (in orange) indicated specific concentrations of EIAV p9 and adaptin at apparent sites of virus budding. Examination of cells producing lower levels of viral protein also indicated colocalization of adaptin and p9 at cellular membranes (Fig. 3F [see inset]); however, these cells showed more typical diffuse adaptin staining and did not have intense perinuclear staining, as observed above. These results demonstrated that alpha  adaptin, and thus the AP-2 complex, specifically colocalizes with sites of virus assembly in ED cells.


View larger version (34K):
[in this window]
[in a new window]
  		FIG. 3.   Immunofluorescence colocalization of EIAV p9 and AP-2. EIAV-infected (A, B, C, and F) and uninfected (D and E) ED cells were grown on glass coverslips, fixed, permeabilized, and stained for EIAV p9 (A and D) and alpha  adaptin (B and E). EIAV p9 and alpha  adaptin were detected by indirect immunofluorescence microscopy with a rabbit polyclonal p9 antiserum with Cy3-conjugated antirabbit secondary antibody and monoclonal mouse anti-alpha adaptin with fluorescein isothiocyanate-conjugated antimouse antibody. Nuclei (blue) were stained with Hoechst stain (D, E, and F). The p9 (red) and alpha  adaptin (green) colocalization (orange) is shown in panels C and F. Bar, 10 µm.

YXXL sequences in other lentiviral proteins have been identified as also functioning in replication. The simian immunodeficiency virus transmembrane protein contains a YXXPhi sequence critical for the regulation of surface envelope protein levels (10). Specific interactions between the HIV-1 and simian immunodeficiency virus envelope proteins and adapter protein medium chains have also recently been demonstrated (2, 12). Examination of the EIAV transmembrane protein and accessory gene sequences fails to identify YXXPhi motifs; thus, we believe that the demonstrated colocalization of EIAV p9 and AP-2 is the result of the p9 gene-encoded YXXL sequence.

We report here for the first time the characterization of an interaction between the late assembly domain of EIAV p9 and the cellular clathrin-associated adapter protein complex AP-2. We used an in vitro AP-50 binding assay to demonstrate for the first time a specific interaction between that subunit of the AP-2 complex and the EIAV late assembly domain YXXL motif. While the EIAV p9 late assembly domain bound to AP-50, the functionally homologous late domains of HIV-1 and RSV that utilize PTAPP and PPPPY motifs, respectively, did not bind AP-50 in this in vitro assay. We also demonstrated that proteins containing L domain mutations previously shown to abrogate function in a COS-1 cell budding assay were also defective in AP-50 binding. Finally, we demonstrated colocalization of AP-2 complexes with EIAV p9 at sites of virus assembly within the cell, suggesting a role for AP-2 complex in virion assembly and release.

The mechanisms through which retroviral late domains facilitate budding remain to be determined. The identification here of the involvement of clathrin-associated adapter proteins indicates that endocytosis machinery may be necessary for a step in virus assembly, possibly by recruiting other cellular proteins to the site of assembly to facilitate a membrane fission event, or by interacting with the Gag polyprotein and membrane phospholipids to facilitate assembly of the immature virus particle in a manner similar to the native function of adapter protein complexes in clathrin-coated pit formation (5). The cellular partners of the PTAP- and PPPY-type late domains remain to be identified. We have shown here that despite the interchangeable nature of the YXXL and PTAP or PPPY late domains to facilitate Gag budding in vitro, the PTAP and PPPY domains failed to bind with the AP-50, in contrast to the EIAV YXXL late domain. This difference indicates that different retroviruses may utilize different sites in cellular processing pathways to accomplish a common assembly step in virus replication in their respective host cells. For example, the various late domains may interact either with different subunits of a particular complex or with different proteins involved in the same cellular pathway. Alternatively, the cellular protein partners of late domains could be involved in entirely different cellular pathways as dictated by their host cell. While further experiments are necessary to elucidate the cellular machinery involved in late assembly and release of retroviral particles, the results of this study define a cellular process that has been adopted by EIAV and possibly other retroviruses to facilitate a critical step during virus assembly.

    ACKNOWLEDGMENTS

We thank John Wills and Laurence Garnier for helpful conversations and assistance in preparing the manuscript and for providing the wild-type L domain GST fusion proteins. We acknowledge Markus Thali for assistance with AP-50 binding experiments and Juan Bonifacino for kindly providing the 3M2 and 3M9 cDNAs for AP-50. Finally, we recognize John Gibbs, Sean Alber, and Ciprian Almonte for assistance with immunofluorescence staining.

This work was supported by National Institutes of Health grant 5R01CA49296 (R.C.M.).

    FOOTNOTES

* Corresponding author. Mailing address: Department of Molecular Genetics and Biochemistry, University of Pittsburgh School of Medicine, W1144 Biomedical Science Tower, Pittsburgh, PA 15261. Phone: (412) 648-8869. Fax: (412) 383-8859. E-mail: rmont{at}pop.pitt.edu.

    REFERENCES
Top
Abstract
Text
References

1. Ball, C. L., S. P. Hunt, and M. S. Robinson. 1995. Expression and localization of a-adaptin isoforms. J. Cell Sci. 108:2865-2875[Abstract].
2. Boge, M., S. Wyss, J. Bonifacino, and M. Thali. 1998. A membrane-proximal tyrosine-based signal mediates internalization of the HIV-1 envelope glycoprotein via interaction with the AP-2 clathrin adaptor. J. Biol. Chem. 273:15773-15778[Abstract/Free Full Text].
3. Bork, P., and M. Sudol. 1994. The WW domain: a signalling site in dystrophin? Trends Biochem. Sci. 19:531-533[Medline].
4. Checroune, F., X. Yao, H. G. Gottlinger, D. Bergeron, and E. A. Cohen. 1995. Incorporation of Vpr into human immunodeficiency virus type 1: role of conserved regions within the p6 domain of Pr55gag. J. Acquired Immune Defic. Syndr. Hum. Retrovirol. 10:1-7[Medline].
5. DeCamilli, P., S. D. Emr, P. S. McPherson, and P. Novick. 1996. Phosphoinositides as regulators in membrane traffic. Science 271:1533-1538[Abstract].
6. Garnier, L., J. W. Wills, M. F. Verderame, and M. Sudol. 1996. WW domains and retrovirus budding. Nature 381:744-745[Medline].
7. Gottlinger, H. G., T. Dorfman, J. G. Sodroski, and W. A. Haseltine. 1991. Effect of mutations affecting the p6 gag protein on human immunodeficiency virus particle release. Proc. Natl. Acad. Sci. USA 88:3195-3199[Abstract/Free Full Text].
8. Henderson, L. E., R. C. Sowder, G. W. Smythers, and S. Oroszlan. 1987. Chemical and immunological characterizations of equine infectious anemia virus gag-encoded proteins. J. Virol. 61:1116-1124[Abstract/Free Full Text].
9. Huang, M., J. M. Orenstein, M. Martin, and E. O. Freed. 1995. p6Gag is required for particle production from full-length human immunodeficiency virus type 1 molecular clones expressing protease. J. Virol. 69:6810-6818[Abstract].
10. LaBranche, C. C., M. M. Sauter, B. S. Haggarty, P. J. Vance, J. Romano, T. K. Hart, P. J. Bugelski, M. Marsh, and J. A. Hoxie. 1995. A single amino acid change in the cytoplasmic domain of the simian immunodeficiency virus transmembrane molecule increases envelope glycoprotein expression on infected cells. J. Virol. 69:5217-5227[Abstract].
11. Montelaro, R. C., N. Lohrey, B. Parekh, E. W. Blakeney, and C. J. Issel. 1982. Isolation and comparative biochemical properties of the major internal polypeptides of equine infectious anemia virus. J. Virol. 42:1029-1038[Abstract/Free Full Text].
12. Ohno, H., R. C. Aguilar, M. C. Fournier, S. Hennecke, P. Cosson, and J. S. Bonifacino. 1997. Interaction of endocytic signals from the HIV-1 envelope glycoprotein complex with members of the adaptor medium chain families. Virology 238:305-315[Medline].
13. Ohno, H., J. Stewart, M.-C. Fournier, H. Bosshart, I. Rhee, S. Miyatake, T. Saito, A. Gallusser, T. Kirchhausen, and J. S. Bonifacino. 1995. Interaction of tyrosine-based sorting signals with clathrin-associated proteins. Science 269:1872-1875[Abstract/Free Full Text].
14. Parent, L. J., R. P. Bennett, R. C. Craven, T. D. Nelle, N. K. Krishna, J. B. Bowzard, C. B. Wilson, B. A. Puffer, R. C. Montelaro, and J. W. Wills. 1995. Positionally independent and exchangeable late budding functions of the Rous sarcoma virus and human immunodeficiency virus Gag proteins. J. Virol. 69:5455-5460[Abstract].
15. Pawson, T., and G. D. Gish. 1992. SH2 and SH3 domains: from structure to function. Cell 71:359-362[Medline].
16. Puffer, B. A., L. J. Parent, J. W. Wills, and R. C. Montelaro. 1997. Equine infectious anemia virus utilizes a YXXL motif within the late assembly domain of the Gag p9 protein. J. Virol. 71:6541-6546[Abstract].
17. Robinson, M. S. 1989. Cloning of cDNA's encoding two related 100-kD coated vesicle proteins (alpha -adaptins). J. Cell Biol. 108:833-842[Abstract/Free Full Text].
18. Robinson, M. S., and B. M. F. Pearse. 1986. Immunofluorescent localization of 100K coated vesicle proteins. J. Cell Biol. 102:48-54[Abstract/Free Full Text].
19. Sudol, M., P. Bork, A. Einbond, K. Kastury, T. Druck, M. Negrini, K. Huebner, and D. Lehman. 1995. Characterization of the mammalian YAP (Yes-associated protein) gene and its role in defining a novel protein module, the WW domain. J. Biol. Chem. 270:14733-14741[Abstract/Free Full Text].
20. Trowbridge, I. S., J. F. Collawn, and C. R. Hopkins. 1993. Signal-dependent membrane protein trafficking in the endocytic pathway. Annu. Rev. Cell Biol. 9:129-161.
21. Vogt, V., R. Eisenman, and H. Diggleman. 1975. Generation of avian myeloblastosis virus structural proteins by proteolytic cleavage of a precursor polypeptide. J. Mol. Biol. 96:471-493[Medline].
22. Weiss, R., N. Teich, H. Varmus, and J. Coffin (ed.). 1985. RNA tumor viruses, 2nd ed. Cold Spring Harbor Press, Cold Spring Harbor, N.Y.
23. Wills, J. W., C. E. Cameron, C. B. Wilson, Y. Xiang, R. P. Bennett, and J. Leis. 1994. An assembly domain of the Rous sarcoma virus Gag protein required late in budding. J. Virol. 68:6605-6618[Abstract/Free Full Text].
24. Xiang, Y., C. E. Cameron, J. W. Wills, and J. Leis. 1996. Fine mapping and characterization of the Rous sarcoma virus Pr76gag late assembly domain. J. Virol. 70:5695-5700[Abstract/Free Full Text].
25. Yasudo, J., and E. Hunter. 1998. A proline-rich motif (PPPY) in the Gag polyprotein of Mason-Pfizer monkey virus plays a maturation-independent role in virion release. J. Virol. 72:4095-4103[Abstract/Free Full Text].

Journal of Virology, December 1998, p. 10218-10221, Vol. 72, No. 12
0022-538X/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.


This article has been cited by other articles:

  • Pery, E., Rajendran, K. S., Brazier, A. J., Gabuzda, D. (2009). Regulation of APOBEC3 Proteins by a Novel YXXL Motif in Human Immunodeficiency Virus Type 1 Vif and Simian Immunodeficiency Virus SIVagm Vif. J. Virol. 83: 2374-2381 [Abstract] [Full Text]  
  • Ushijima, Y., Koshizuka, T., Goshima, F., Kimura, H., Nishiyama, Y. (2008). Herpes Simplex Virus Type 2 UL56 Interacts with the Ubiquitin Ligase Nedd4 and Increases Its Ubiquitination. J. Virol. 82: 5220-5233 [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]  
  • Watanabe, T., Sorensen, E. M., Naito, A., Schott, M., Kim, S., Ahlquist, P. (2007). Involvement of host cellular multivesicular body functions in hepatitis B virus budding. Proc. Natl. Acad. Sci. USA 104: 10205-10210 [Abstract] [Full Text]  
  • Ciancanelli, M. J., Basler, C. F. (2006). Mutation of YMYL in the Nipah Virus Matrix Protein Abrogates Budding and Alters Subcellular Localization. J. Virol. 80: 12070-12078 [Abstract] [Full Text]  
  • Rost, M., Mann, S., Lambert, C., Doring, T., Thome, N., Prange, R. (2006). {gamma}2-Adaptin, a Novel Ubiquitin-interacting Adaptor, and Nedd4 Ubiquitin Ligase Control Hepatitis B Virus Maturation. J. Biol. Chem. 281: 29297-29308 [Abstract] [Full Text]  
  • Odorizzi, G. (2006). The multiple personalities of Alix.. J. Cell Sci. 119: 3025-3032 [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]  
  • Chen, C., Vincent, O., Jin, J., Weisz, O. A., Montelaro, R. C. (2005). Functions of Early (AP-2) and Late (AIP1/ALIX) Endocytic Proteins in Equine Infectious Anemia Virus Budding. J. Biol. Chem. 280: 40474-40480 [Abstract] [Full Text]  
  • Neumann, G., Ebihara, H., Takada, A., Noda, T., Kobasa, D., Jasenosky, L. D., Watanabe, S., Kim, J. H., Feldmann, H., Kawaoka, Y. (2005). Ebola Virus VP40 Late Domains Are Not Essential for Viral Replication in Cell Culture. J. Virol. 79: 10300-10307 [Abstract] [Full Text]  
  • Jin, S., Chen, C., Montelaro, R. C. (2005). Equine Infectious Anemia Virus Gag p9 Function in Early Steps of Virus Infection and Provirus Production. J. Virol. 79: 8793-8801 [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]  
  • 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]  
  • Abada, P., Noble, B., Cannon, P. M. (2005). Functional Domains within the Human Immunodeficiency Virus Type 2 Envelope Protein Required To Enhance Virus Production. J. Virol. 79: 3627-3638 [Abstract] [Full Text]  
  • Heidecker, G., Lloyd, P. A., Fox, K., Nagashima, K., Derse, D. (2004). Late Assembly Motifs of Human T-Cell Leukemia Virus Type 1 and Their Relative Roles in Particle Release. J. Virol. 78: 6636-6648 [Abstract] [Full Text]  
  • Lindwasser, O. W., Resh, M. D. (2004). Human Immunodeficiency Virus Type 1 Gag Contains a Dileucine-Like Motif That Regulates Association with Multivesicular Bodies. J. Virol. 78: 6013-6023 [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]  
  • Irie, T., Licata, J. M., McGettigan, J. P., Schnell, M. J., Harty, R. N. (2004). Budding of PPxY-Containing Rhabdoviruses Is Not Dependent on Host Proteins TGS101 and VPS4A. J. Virol. 78: 2657-2665 [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]  
  • 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 [Abstract] [Full Text]  
  • Palmarini, M., Mura, M., Spencer, T. E. (2004). Endogenous betaretroviruses of sheep: teaching new lessons in retroviral interference and adaptation. J. Gen. Virol. 85: 1-13 [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]  
  • Hui, E. K.-W., Barman, S., Yang, T. Y., Nayak, D. P. (2003). Basic Residues of the Helix Six Domain of Influenza Virus M1 Involved in Nuclear Translocation of M1 Can Be Replaced by PTAP and YPDL Late Assembly Domain Motifs. J. Virol. 77: 7078-7092 [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]  
  • Le Blanc, I., Prevost, M.-C., Dokhelar, M.-C., Rosenberg, A. R. (2002). The PPPY Motif of Human T-Cell Leukemia Virus Type 1 Gag Protein Is Required Early in the Budding Process. J. Virol. 76: 10024-10029 [Abstract] [Full Text]  
  • Wang, H., Norris, K. M., Mansky, L. M. (2002). Analysis of Bovine Leukemia Virus Gag Membrane Targeting and Late Domain Function. J. Virol. 76: 8485-8493 [Abstract] [Full Text]  
  • Ma, Y. M., Vogt, V. M. (2002). Rous Sarcoma Virus Gag Protein-Oligonucleotide Interaction Suggests a Critical Role for Protein Dimer Formation in Assembly. J. Virol. 76: 5452-5462 [Abstract] [Full Text]  
  • Strack, B., Calistri, A., Gottlinger, H. G. (2002). Late Assembly Domain Function Can Exhibit Context Dependence and Involves Ubiquitin Residues Implicated in Endocytosis. J. Virol. 76: 5472-5479 [Abstract] [Full Text]  
  • Freed, E. O. (2002). Viral Late Domains. J. Virol. 76: 4679-4687 [Full Text]  
  • Schmitt, A. P., Leser, G. P., Waning, D. L., Lamb, R. A. (2002). Requirements for Budding of Paramyxovirus Simian Virus 5 Virus-Like Particles. J. Virol. 76: 3952-3964 [Abstract] [Full Text]  
  • Patnaik, A., Chau, V., Li, F., Montelaro, R. C., Wills, J. W. (2002). Budding of Equine Infectious Anemia Virus Is Insensitive to Proteasome Inhibitors. J. Virol. 76: 2641-2647 [Abstract] [Full Text]  
  • Ott, D. E., Coren, L. V., Sowder, R. C. II, Adams, J., Nagashima, K., Schubert, U. (2002). Equine Infectious Anemia Virus and the Ubiquitin-Proteasome System. J. Virol. 76: 3038-3044 [Abstract] [Full Text]  
  • Li, F., Chen, C., Puffer, B. A., Montelaro, R. C. (2002). Functional Replacement and Positional Dependence of Homologous and Heterologous L Domains in Equine Infectious Anemia Virus Replication. J. Virol. 76: 1569-1577 [Abstract] [Full Text]  
  • Muller, B., Patschinsky, T., Krausslich, H.-G. (2002). The Late-Domain-Containing Protein p6 Is the Predominant Phosphoprotein of Human Immunodeficiency Virus Type 1 Particles. J. Virol. 76: 1015-1024 [Abstract] [Full Text]  
  • Demirov, D. G., Ono, A., Orenstein, J. M., Freed, E. O. (2002). Overexpression of the N-terminal domain of TSG101 inhibits HIV-1 budding by blocking late domain function. Proc. Natl. Acad. Sci. USA 99: 955-960 [Abstract] [Full Text]  
  • Demirov, D. G., Orenstein, J. M., Freed, E. O. (2002). The Late Domain of Human Immunodeficiency Virus Type 1 p6 Promotes Virus Release in a Cell Type-Dependent Manner. J. Virol. 76: 105-117 [Abstract] [Full Text]  
  • Weixel, K. M., Bradbury, N. A. (2001). {micro}2 Binding Directs the Cystic Fibrosis Transmembrane Conductance Regulator to the Clathrin-mediated Endocytic Pathway. J. Biol. Chem. 276: 46251-46259 [Abstract] [Full Text]  
  • Chen, C., Li, F., Montelaro, R. C. (2001). Functional Roles of Equine Infectious Anemia Virus Gag p9 in Viral Budding and Infection. J. Virol. 75: 9762-9770 [Abstract] [Full Text]  
  • Kikonyogo, A., Bouamr, F., Vana, M. L., Xiang, Y., Aiyar, A., Carter, C., Leis, J. (2001). Proteins related to the Nedd4 family of ubiquitin protein ligases interact with the L domain of Rous sarcoma virus and are required for gag budding from cells. Proc. Natl. Acad. Sci. USA 10.1073/pnas.201268998v1 [Abstract] [Full Text]  
  • Hartmann-Stühler, C., Prange, R. (2001). Hepatitis B Virus Large Envelope Protein Interacts with {gamma}2-Adaptin, a Clathrin Adaptor-Related Protein. J. Virol. 75: 5343-5351 [Abstract] [Full Text]  
  • Yu, F., Joshi, S. M., Ma, Y. M., Kingston, R. L., Simon, M. N., Vogt, V. M. (2001). Characterization of Rous Sarcoma Virus Gag Particles Assembled In Vitro. J. Virol. 75: 2753-2764 [Abstract] [Full Text]  
  • Harty, R. N., Brown, M. E., Wang, G., Huibregtse, J., Hayes, F. P. (2000). A PPxY motif within the VP40 protein of Ebola virus interacts physically and functionally with a ubiquitin ligase: Implications for filovirus budding. Proc. Natl. Acad. Sci. USA 10.1073/pnas.250277297v1 [Abstract] [Full Text]  
  • Vogt, V. M. (2000). Ubiquitin in retrovirus assembly: Actor or bystander?. Proc. Natl. Acad. Sci. USA 97: 12945-12947 [Full Text]  
  • Strack, B., Calistri, A., Accola, M. A., Palu, G., Gottlinger, H. G. (2000). A role for ubiquitin ligase recruitment in retrovirus release. Proc. Natl. Acad. Sci. USA 97: 13063-13068 [Abstract] [Full Text]  
  • Patnaik, A., Chau, V., Wills, J. W. (2000). Ubiquitin is part of the retrovirus budding machinery. Proc. Natl. Acad. Sci. USA 97: 13069-13074 [Abstract] [Full Text]  
  • Doms, R. W., Trono, D. (2000). The plasma membrane as a combat zone in the HIV battlefield. Genes Dev. 14: 2677-2688 [Full Text]  
  • Yuan, B., Campbell, S., Bacharach, E., Rein, A., Goff, S. P. (2000). Infectivity of Moloney Murine Leukemia Virus Defective in Late Assembly Events Is Restored by Late Assembly Domains of Other Retroviruses. J. Virol. 74: 7250-7260 [Abstract] [Full Text]  
  • Craven, R. C., Harty, R. N., Paragas, J., Palese, P., Wills, J. W. (1999). Late Domain Function Identified in the Vesicular Stomatitis Virus M Protein by Use of Rhabdovirus-Retrovirus Chimeras. J. Virol. 73: 3359-3365 [Abstract] [Full Text]  
  • Bennett, R. P., Wills, J. W. (1999). Conditions for Copackaging Rous Sarcoma Virus and Murine Leukemia Virus Gag Proteins during Retroviral Budding. J. Virol. 73: 2045-2051 [Abstract] [Full Text]  
  • Garnier, L., Parent, L. J., Rovinski, B., Cao, S.-X., Wills, J. W. (1999). Identification of Retroviral Late Domains as Determinants of Particle Size. J. Virol. 73: 2309-2320 [Abstract] [Full Text]  
  • Kikonyogo, A., Bouamr, F., Vana, M. L., Xiang, Y., Aiyar, A., Carter, C., Leis, J. (2001). Proteins related to the Nedd4 family of ubiquitin protein ligases interact with the L domain of Rous sarcoma virus and are required for gag budding from cells. Proc. Natl. Acad. Sci. USA 98: 11199-11204 [Abstract] [Full Text]  
  • Harty, R. N., Brown, M. E., Wang, G., Huibregtse, J., Hayes, F. P. (2000). A PPxY motif within the VP40 protein of Ebola virus interacts physically and functionally with a ubiquitin ligase: Implications for filovirus budding. Proc. Natl. Acad. Sci. USA 97: 13871-13876 [Abstract] [Full Text]  

This Article
Right arrow Abstract Freely available
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 Puffer, B. A.
Right arrow Articles by Montelaro, R. C.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Puffer, B. A.
Right arrow Articles by Montelaro, R. C.

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