Positionally independent and exchangeable late budding functions of the Rous sarcoma virus and human immunodeficiency virus Gag proteins
Open accessAbstract
The Gag proteins of Rous sarcoma virus and human immunodeficiency virus (HIV) each contain a function involved in a late step in budding, defects in which result in the accumulation of these molecules at the plasma membrane. In the Rous sarcoma virus Gag protein (Pr76gag), this assembly domain is associated with a PPPY motif, which is located at an internal position between the MA and CA sequences. This motif is not contained anywhere within the HIV Gag protein (Pr55gag), and the MA sequence is linked directly to CA. Instead, a late assembly function of HIV has been associated with the p6 sequence situated at the C terminus of Gag. Here we demonstrate the remarkable finding that the late assembly domains from these two unrelated Gag proteins are exchangeable between retroviruses and can function in a positionally independent manner.
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RSV Gag chimeras demonstrated that the L domain function of p2b could be substituted by the C-terminal sequence of HIV-1 p6, regardless of its position in the precursor.
“RSV Gag chimeras demonstrated that the L domain function of p2b could be substituted by the C-terminal sequence of HIV-1 p6, regardless of its position in the precursor”
From Beyond reverse transcription: molecular mechanisms and emerging paradigms in retroviral replication (2026) · cites this paper as Parent et al. 1995
L domains have been reported in many retroviruses, such as HIV, MLV, RSV, EIAV, HIV-2, FIV, HTLV-1, MPMV, and FV.
“The “L” domains have been reported in many retroviruses, such as HIV, MLV, RSV, EIAV, HIV-2, FIV, HTLV-1, MPMV, and FV”
From Beyond reverse transcription: molecular mechanisms and emerging paradigms in retroviral replication (2026) · cites this paper as Parent et al. 1995
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AIP1/ALIX Is a Binding Partner for HIV-1 p6 and EIAV p9 Functioning in Virus Budding
Strack, B., Calistri, A., Craig, S., Popova, E., & Göttlinger, H. G. (2003) · Cell · doi:10.1016/s0092-8674(03)00653-6 · Cited by 825 · see citing works
HIV-1 Gag proteins: diverse functions in the virus life cycle
Freed, E. O. (1998) · Virology · doi:10.1006/viro.1998.9398 · Cited by 717 · see citing works
“Intriguingly, HIV-1 p6 and EIAV p9 can replace the p2b function in RSV, in a manner independent of the location of the late domain in the Gag precursor (Parent et al., 1995).”
BackgroundInfluentialMartin-Serrano, J., Zang, T., & Bieniasz, P. D. (2001) · Nature Medicine · doi:10.1038/nm1201-1313 · Cited by 710 · see citing works
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BackgroundVerPlank, L., Bouamr, F., LaGrassa, T. J., Agresta, B., Kikonyogo, A., Leis, J., & Carter, C. A. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.131059198 · Cited by 584 · see citing works
Demirov, D., & Freed, E. (2004) · Virus Research · doi:10.1016/j.virusres.2004.08.007 · Cited by 547 · see citing works
Virus budding and the ESCRT pathway
Votteler, J., & Sundquist, W. I. (2013) · Cell Host & Microbe · doi:10.1016/j.chom.2013.08.012 · Cited by 547 · see citing works
“In parallel, others identified distinct short peptide motifs within the structural proteins of other viruses and called these motifs ‘‘late assembly domains’’ because their mutation typically arrested virus assembly at a very late stage (Parent et al., 1995; Puffer et al., 1997).”
BackgroundVennema, H., Godeke, G., Rossen, J., Voorhout, W., Horzinek, M. C., Opstelten, D., & Rottier, P. (1996) · EMBO Journal · doi:10.1002/j.1460-2075.1996.tb00553.x · Cited by 499 · see citing works
Harty, R. N., Brown, M. E., Wang, G.-L., Huibregtse, J., & Hayes, F. P. (2000) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.250277297 · Cited by 484 · see citing works
Freed, E. (2002) · Journal of Virology · doi:10.1128/jvi.76.10.4679-4687.2002 · Cited by 444 · see citing works
“(55) introduced the entire EIAV p9 coding region (Fig.”
BackgroundLate budding domains and host proteins in enveloped virus release.
Bieniasz, P. (2006) · Virology · doi:10.1016/j.virol.2005.09.044 · Cited by 411 · see citing works
Endophilins interact with Moloney murine leukemia virus Gag and modulate virion production
Wang, M. Q., Kim, W., Gao, G., Torrey, T. A., Morse, H. C., Camilli, P. V. D., & Goff, S. P. (2003) · Journal of Biology · doi:10.1186/1475-4924-3-4 · Cited by 49 · see citing works
“Despite the lack of sequence homology, many late domains can be functionally interchanged [21-23].”
BackgroundDemirov, D., Ono, A., Orenstein, J., & Freed, E. (2002) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.032511899 · Cited by 381 · see citing works
Campbell, S., & Vogt, V. M. (1995) · Journal of Virology · doi:10.1128/jvi.69.10.6487-6497.1995 · Cited by 350 · see citing works
Garoff, H., Hewson, R., & Opstelten, D.-J. E. (1998) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.62.4.1171-1190.1998 · Cited by 359 · see citing works
A role for ubiquitin ligase recruitment in retrovirus release
Strack, B., Calistri, A., Accola, M. A., Palù, G., & Göttlinger, H. G. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.24.13063 · Cited by 309 · see citing works
Harty, R. N., Paragas, J., Sudol, M., & Palese, P. (1999) · Journal of Virology · doi:10.1128/jvi.73.4.2921-2929.1999 · Cited by 303 · see citing works
“While L domains have been identified in the Gag proteins of other retroviruses, only the Gag proteins of the oncoviruses appear to have the PPxY motif conserved (17, 19, 37, 41, 55, 59).”
BackgroundStructure and function of the WW domain
Sudol, M. (1996) · Progress in Biophysics and Molecular Biology · doi:10.1016/s0079-6107(96)00008-9 · Cited by 296 · see citing works
Ubiquitin is part of the retrovirus budding machinery
Patnaik, A., Chau, V., & Wills, J. W. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.24.13069 · Cited by 292 · see citing works
Self-citationLicata, J. M., Simpson-Holley, M., Wright, N., Han, Z.-Y., Paragas, J., & Harty, R. N. (2003) · Journal of Virology · doi:10.1128/jvi.77.3.1812-1819.2003 · Cited by 289 · see citing works
“As docking sites for cellular proteins, these viral L-domains would be predicted to function when moved to a new location within the viral protein and, indeed, this phenomenon has been observed (8, 27, 31).”
BackgroundAccola, M. A., Strack, B., & Göttlinger, H. G. (2000) · Journal of Virology · doi:10.1128/jvi.74.12.5395-5402.2000 · Cited by 288 · see citing works
“In an effort to distinguish between these possibilities, we examined whether the defect of the D-ZWT chimera could be corrected by the entirely unrelated L domain of RSV.”
BackgroundMethodInfluentialMechanisms of enveloped RNA virus budding.
Pornillos, O., Garrus, J., & Sundquist, W. (2002) · Trends in Cell Biology · doi:10.1016/s0962-8924(02)02402-9 · Cited by 277 · see citing works
Cryo-electron microscopy reveals ordered domains in the immature HIV-1 particle
Fuller, S. D., Wilk, T., Gowen, B. E., Kräusslich, H., & Vogt, V. M. (1997) · Current Biology · doi:10.1016/s0960-9822(06)00331-9 · Cited by 246 · see citing works
“Furthermore, the NC region, which interacts with RNA, contains one of the three essential ‘assembly domains’ that are required for retrovirus budding [1,48].”
BackgroundBinding of Human Immunodeficiency Virus Type 1 Gag to Membrane: Role of the Matrix Amino Terminus
Ono, A., & Freed, E. O. (1999) · Journal of Virology · doi:10.1128/jvi.73.5.4136-4144.1999 · Cited by 238 · see citing works
“These domains, which drive Gag membrane binding, Gag-Gag interactions, and late budding functions, have been referred to as M, I, and L, respectively (35).”
BackgroundRole of ESCRT-I in Retroviral Budding
Martin-Serrano, J., Zang, T., & Bieniasz, P. D. (2003) · Journal of Virology · doi:10.1128/jvi.77.8.4794-4804.2003 · Cited by 250 · see citing works
“Y190 cells were transformed with GAL4-Tsg10(1-390) (full length) or GAL4-Tsg10(1-303) expression plasmids along with a plasmid expressing a full-length or deletion mutant VP16-Tsg101 expression plasmid, as indicated.”
BackgroundMethodInfluentialPuffer, B. A., Parent, L. J., Wills, J. W., & Montelaro, R. C. (1997) · Journal of Virology · doi:10.1128/jvi.71.9.6541-6546.1997 · Cited by 217 · see citing works
“Fusion of p9 to the C terminus of an RSV Gag protein defective for budding results in a functional polyprotein that can assemble and release Gag particles from the cell plasma membrane (16).”
BackgroundMethodInfluentialSelf-citationEquine Infectious Anemia Virus (EIAV): what has HIV's country cousin got to tell us?
Leroux, C., Cadoré, J., & Montelaro, R. (2004) · Veterinary Research · doi:10.1051/vetres:2004020 · Cited by 216 · see citing works
Self-citationRhabdoviruses and the Cellular Ubiquitin-Proteasome System: a Budding Interaction
Harty, R. N., Brown, M. E., McGettigan, J., Wang, G.-L., Jayakar, H. R., Huibregtse, J., Whitt, M., & Schnell, M. (2001) · Journal of Virology · doi:10.1128/jvi.75.22.10623-10629.2001 · Cited by 214 · see citing works
“An important characteristic of the M protein of VSV, shared by the Gag polyprotein of retroviruses (1, 12, 36, 39, 57, 59, 60) and the VP40 protein of Ebola virus (13, 19, 52), is its ability to be released (bud) from cells in the absence of any other viral protein (14, 21, 27).”
BackgroundHost factors involved in retroviral budding and release
Martin‐Serrano, J., & Neil, S. J. D. (2011) · Nature Reviews Microbiology · doi:10.1038/nrmicro2596 · Cited by 196 · see citing works
“L-domains in divergent retroviruses are functionally interchangeable, short amino acid motifs that work in a position-independent manne”
BackgroundDemirov, D. G., Orenstein, J. M., & Freed, E. O. (2002) · Journal of Virology · doi:10.1128/jvi.76.1.105-117.2002 · Cited by 201 · see citing works
“Although the physiological ligand for p6 has not been definitively identified, a variety of observations suggest that retroviral L domains function by interacting with the host ubiquitination machinery (reviewed in reference 60): (i) The L domain-containing proteins of MuLV (p12) and HIV (p6) are ubiquitinated (42), (…”
BackgroundInfluentialNedd4 Regulates Egress of Ebola Virus-Like Particles from Host Cells
Yasuda, J., Nakao, M., Kawaoka, Y., & Shida, H. (2003) · Journal of Virology · doi:10.1128/jvi.77.18.9987-9992.2003 · Cited by 191 · see citing works
“These viral proteins possess a so-called late (or L) domain containing PT/SAP, PPxY, or YxxL, which are critical motifs for efficient budding (9, 11, 14, 16, 21, 23, 27, 28, 29, 32).”
BackgroundOtt, D., Coren, L., Copeland, T., Kane, B., Johnson, D. G., Sowder, R., Yoshinaka, Y., Oroszlan, S., Arthur, L., & Henderson, L. (1998) · Journal of Virology · doi:10.1128/jvi.72.4.2962-2968.1998 · Cited by 188 · see citing works
“This region in HIV-1 appears to be involved in assembly and budding (19, 26, 39).”
BackgroundHow Ubiquitin Functions with ESCRTs
Shields, S. B., & Piper, R. C. (2011) · Traffic · doi:10.1111/j.1600-0854.2011.01242.x · Cited by 175 · see citing works
Chen, H. I., Einbond, A., Kwak, S.-J., Linn, H., Koepf, E., Peterson, S. A., Kelly, J., & Sudol, M. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.27.17070 · Cited by 184 · see citing works
No strings attached: the ESCRT machinery in viral budding and cytokinesis
McDonald, B., & Martin-Serrano, J. (2009) · Journal of Cell Science · doi:10.1242/jcs.028308 · Cited by 182 · see citing works
“Second, L-domains are interchangeable between different viral Gag proteins (Parent et al., 1995; Yuan et al., Jo ur na l o f C el l S ci en ce”
BackgroundHuman immunodeficiency virus type 1 assembly, release, and maturation
Adamson, C. S., & Freed, E. O. (2007) · Advances in Pharmacology · doi:10.1016/s1054-3589(07)55010-6 · Cited by 179 · see citing works
Identification of Novel Human WW Domain-containing Proteins by Cloning of Ligand Targets*
Pirozzi, G., Mcconnell, S., Uveges, A., Carter, J., Sparks, A., Kay, B. K., & Fowlkes, D. M. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.23.14611 · Cited by 171 · see citing works
Vincent, O., Rainbow, L., Tilburn, J., Arst, H., & Peñalva, M. (2003) · Molecular and Cellular Biology · doi:10.1128/mcb.23.5.1647-1655.2003 · Cited by 168 · see citing works
“Despite their different amino acid sequences, the three GAG p9 late-domain motifs are functionally interchangeable, suggesting that they work by recruiting different subunits of a multiprotein complex involved in budding of all three viral particles (19, 32, 35).”
BackgroundDesigned proteins induce the formation of nanocage-containing extracellular vesicles
Votteler, J., Ogohara, C., Yi, S., Hsia, Y., Nattermann, U., Belnap, D. M., King, N. P., & Sundquist, W. I. (2016) · Nature · doi:10.1038/nature20607 · Cited by 149 · see citing works
Yuan, B., Campbell, S., Bacharach, E., Rein, A., & Goff, S. (2000) · Journal of Virology · doi:10.1128/jvi.74.16.7250-7260.2000 · Cited by 165 · see citing works
“However, the recovery of function by heterologous retrovirus L-domains was not complete, and none of the chimeric viruses has been reported to be replication competent (21, 22, 36).”
BackgroundInfluentialMaguire, M. F., Guinea, R., Griffin, P., Macmanus, S., Elston, R., Wolfram, J., Richards, N., Hanlon, M., Porter, D. J. T., Wrin, T., et al. (2002) · Journal of Virology · doi:10.1128/jvi.76.15.7398-7406.2002 · Cited by 164
“This region includes the PTAPP motif and has been shown to be involved in viral maturation events such as packaging of processed Pol proteins during late assembly (14, 28).”
BackgroundYuan, B., Li, X.-Q., & Goff, S. (1999) · EMBO Journal · doi:10.1093/emboj/18.17.4700 · Cited by 164 · see citing works
Campbell, S., & Vogt, V. (1997) · Journal of Virology · doi:10.1128/jvi.71.6.4425-4435.1997 · Cited by 162 · see citing works
“Genetic analyses of RSV Gag have led to the conclusion that only three small regions, called assembly domains, are essential for the release of virus-like particles from transfected cells (34).”
BackgroundInfluentialFine mapping and characterization of the Rous sarcoma virus Pr76gag late assembly domain
Xiang, Y., Cameron, C. E., Wills, J. W., & Leis, J. (1996) · Journal of Virology · doi:10.1128/jvi.70.8.5695-5700.1996 · Cited by 161 · see citing works
“In this latter case, the rescue is of the same magnitude as placing p2b at the end of Gag (16).”
BackgroundMethodInfluentialSelf-citationCiancanelli, M. J., & Basler, C. (2006) · Journal of Virology · doi:10.1128/jvi.01743-06 · Cited by 160 · see citing works
“A second prolinerich late-domain motif, PPxY, first discovered in RSV Gag p2b domain but also present in the Ebola virus VP40, interacts with the Nedd4-like ubiquitin ligase, which also influences MVB function (22, 46).”
Evidence for a New Viral Late-Domain Core Sequence, FPIV, Necessary for Budding of a Paramyxovirus
Schmitt, A., Leser, G. P., Morita, E., Sundquist, W., & Lamb, R. (2005) · Journal of Virology · doi:10.1128/jvi.79.5.2988-2997.2005 · Cited by 160 · see citing works
“The functional interchangeability among different types of late domains (1, 2, 18, 27, 49, 50) suggested an experimental approach that could be used to identify new types of late domains.”
Yasuda, J., & Hunter, E. (1998) · Journal of Virology · doi:10.1128/jvi.72.5.4095-4103.1998 · Cited by 158 · see citing works
“This region has been defined as the late (L) assembly domain of the RSV Gag polyprotein (21).”
BackgroundCellular Factors Required for Lassa Virus Budding
Urata, S., Noda, T., Kawaoka, Y., Yokosawa, H., & Yasuda, J. (2006) · Journal of Virology · doi:10.1128/jvi.80.8.4191-4195.2006 · Cited by 155 · see citing works
Blot, V., Perugi, F., Gay, B., Prévost, M., Briant, L., Tangy, F., Abriel, H., Staub, O., Dokhelar, M., & Pique, C. (2004) · Journal of Cell Science · doi:10.1242/jcs.01095 · Cited by 155 · see citing works
“As L-domains can be functionally exchanged between several retroviruses (Accola et al., 2000; Freed, 2002; Parent et al., 1995; Yuan et al., 2000), it is assumed that YPDL, PPPY and PTAP motifs mediate equivalent, therefore redundant, functions (reviewed by Freed, 2002).”
BackgroundUbiquitination of HIV-1 and MuLV Gag.
Ott, D., Coren, L., Chertova, E., Gagliardi, T. D., & Schubert, U. (2000) · Virology · doi:10.1006/viro.2000.0648 · Cited by 151 · see citing works
Wirblich, C., Bhattacharya, B., & Roy, P. (2006) · Journal of Virology · doi:10.1128/jvi.80.1.460-473.2006 · Cited by 150 · see citing works
“Retroviruses bind to different components of this pathway by means of so-called late-domain motifs, which are highly conserved protein-protein interaction motifs that can be located at different positions within Gag (13, 16, 48, 77).”
BackgroundContext-Dependent Effects of L Domains and Ubiquitination on Viral Budding
Martin-Serrano, J., Pérez-Caballero, D., & Bieniasz, P. (2004) · Journal of Virology · doi:10.1128/jvi.78.11.5554-5563.2004 · Cited by 150 · see citing works
“The fact that viral L domains are functionally interchangeable, in many cases, and can function when placed in various positions within a retroviral Gag protein (21, 25, 31, 51) suggests that they facilitate budding by broadly similar mechanisms involving the recruitment of host factors.”
Craven, R., Harty, R. N., Paragas, J., Palese, P., & Wills, J. (1999) · Journal of Virology · doi:10.1128/jvi.73.4.3359-3365.1999 · Cited by 149 · see citing works
“This leaky phenotype is similar to what has been seen with RSV and M-PMV late domain mutants (18, 30, 33, 34).”
BackgroundResultInfluentialSelf-citationDussupt, V., Javid, M. P., Abou-Jaoudé, G., Jadwin, J. A., de La Cruz, J., Nagashima, K., & Bouamr, F. (2009) · PLoS Pathogens · doi:10.1371/journal.ppat.1000339 · Cited by 148 · see citing works
“In contrast, when expressed next to the MA domain within RSV or MoMLV Gag, the PTAP motif of HIV-1 rescues only ,30% of virus release [58,59].”
BackgroundInfluentialLu, Y.-H., Bennett, R. P., Wills, J. W., Gorelick, R., & Ratner, L. (1995) · Journal of Virology · doi:10.1128/jvi.69.11.6873-6879.1995 · Cited by 148 · see citing works
Self-citationInteraction of the Human Immunodeficiency Virus Type 1 Nucleocapsid with Actin
Liu, B., Dai, R., Tian, C., Dawson, L., Gorelick, R. J., & Yu, X.-F. (1999) · Journal of Virology · doi:10.1128/jvi.73.4.2901-2908.1999 · Cited by 142 · see citing works
“The L domain of HIV-1 Gag maps to the p6 region, which is required for efficient virus release (27, 31, 47, 57, 65).”
BackgroundUsami, Y., Popov, S., & Göttlinger, H. G. (2007) · Journal of Virology · doi:10.1128/jvi.00314-07 · Cited by 143 · see citing works
“Remarkably, L domains do not depend on a particular location within Gag to function and can even be moved between unrelated viruses (37), an observation that suggested that L domains may act as docking sites for cellular factors.”
BackgroundGöttlinger, H. G. (2001) · AIDS · doi:10.1097/00002030-200100005-00003 · Cited by 124 · see citing works
The Mason-Pfizer Monkey Virus PPPY and PSAP Motifs Both Contribute to Virus Release
Gottwein, E., Bodem, J., Müller, B., Schmechel, A., Zentgraf, H., & Kräusslich, H. (2003) · Journal of Virology · doi:10.1128/jvi.77.17.9474-9485.2003 · Cited by 133 · see citing works
“Different L-domain motifs have been shown to be at least partially exchangeable between retroviruses (17, 21, 40).”
BackgroundMethodBouamr, F., Melillo, J. A., Wang, M. Q., Nagashima, K., Santos, M. D. L., Rein, A., & Goff, S. (2003) · Journal of Virology · doi:10.1128/jvi.77.22.11882-11895.2003 · Cited by 132 · see citing works
“The RSV L domain is contained in its small p2 peptide (45), whereas the MLV L domain is found in p12 (68).”
BackgroundWW domains and retrovirus budding
Gamier, L., Wills, J., Verderame, M., & Sudol, M. (1996) · Nature · doi:10.1038/381744a0 · Cited by 132 · see citing works
Self-citationRole of HIV-1 Gag domains in viral assembly
Scarlata, S., & Carter, C. (2003) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/s0005-2736(03)00163-9 · Cited by 111 · see citing works
Escaping from the cell: assembly and budding of negative-strand RNA viruses.
Schmitt, A. P., & Lamb, R. (2004) · Current Topics in Microbiology and Immunology · doi:10.1007/978-3-662-06099-5_5 · Cited by 131 · see citing works
Vogt, D. A., Camus, G., Herker, E., Webster, B., Tsou, C.-L., Greene, W., Yen, T. S., & Ott, M. (2013) · PLoS Pathogens · doi:10.1371/journal.ppat.1003302 · Cited by 126 · see citing works
“Similar to the NS5A membrane anchor in our study, the TIP47-binding region in MA overlaps a hydrophobic region implicated in Gag anchoring and binding at the plasma membrane [38–40].”
BackgroundFilovirus assembly and budding.
Hartlieb, B., & Weissenhorn, W. (2006) · Virology · doi:10.1016/j.virol.2005.09.018 · Cited by 126 · see citing works
Puffer, B. A., Watkins, S. C., & Montelaro, R. (1998) · Journal of Virology · doi:10.1128/jvi.72.12.10218-10221.1998 · Cited by 120 · see citing works
“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).”
BackgroundSelf-citationBowzard, J. B., Bennett, R., Krishna, N. K., Ernst, S. M., Rein, A., & Wills, J. (1998) · Journal of Virology · doi:10.1128/jvi.72.11.9034-9044.1998 · Cited by 119 · see citing works
“, during the virus-cell separation step) (20, 34).”
Self-citationFunctional involvement of a novel Nedd4‐like ubiquitin ligase on retrovirus budding
Yasuda, J., Hunter, E., Nakao, M., & Shida, H. (2002) · EMBO Reports · doi:10.1093/embo-reports/kvf132 · Cited by 116 · see citing works
Towards prediction of cognate complexes between the WW domain and proline‐rich ligands
Einbond, A., & Sudol, M. (1996) · FEBS Letters · doi:10.1016/0014-5793(96)00263-3 · Cited by 106 · see citing works
Nuclear entry and CRM1-dependent nuclear export of the Rous sarcoma virus Gag polyprotein
Scheifele, L. Z., Garbitt, R. A., Rhoads, J. D., & Parent, L. (2002) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.062652199 · Cited by 114 · see citing works
Self-citationThe WW module competes with the SH3 domain?
Sudol, M. (1996) · TIBS -Trends in Biochemical Sciences. Regular ed · doi:10.1016/s0968-0004(96)30018-2 · Cited by 114 · see citing works
Popov, S., Popova, E., Inoue, M., & Göttlinger, H. G. (2008) · Journal of Virology · doi:10.1128/jvi.01912-07 · Cited by 112 · see citing works
“These motifs, which are known as late assembly (L) domains, often remain functional even if moved to a different position within Gag and can be exchanged among unrelated viruses (39, 51).”
BackgroundSandefur, S. L., Smith, R. M., Varthakavi, V., & Spearman, P. W. (2000) · Journal of Virology · doi:10.1128/jvi.74.16.7238-7249.2000 · Cited by 113 · see citing works
“The late (L) domain is required for particle budding and is a determinant of retroviral particle size (13, 27).”
BackgroundThe Role of Ubiquitin in Retroviral Egress
Martin‐Serrano, J. (2007) · Traffic · doi:10.1111/j.1600-0854.2007.00609.x · Cited by 92 · see citing works
“It is now well established that, for the most part, L-domains are interchangeable (61) and recent findings show that viral budding mediated by other L-domains share with HIV-1 the same requirements for ESCRT-III and VPS4 (20,27,35,47,49,57).”
BackgroundDerdowski, A., Ding, L.-M., & Spearman, P. (2004) · Journal of Virology · doi:10.1128/jvi.78.3.1230-1242.2004 · Cited by 110 · see citing works
“The interaction (I) domain was originally defined as a region within NC of Rous sarcoma virus (RSV) Gag that is responsible for the production of particles of normal retroviral density (2, 31).”
BackgroundTsg101 Control of Human Immunodeficiency Virus Type 1 Gag Trafficking and Release
Goff, A., Ehrlich, L. S., Cohen, S. N., & Carter, C. (2003) · Journal of Virology · doi:10.1128/jvi.77.17.9173-9182.2003 · Cited by 105 · see citing works
“The L domains in retroviruses differ in amino acid sequence and location within the respective viral structural proteins but are functionally exchangeable (8, 18, 41, 54, 57), suggesting commonality of function.”
BackgroundUbiquitin in retrovirus assembly: actor or bystander?
Vogt, V. M. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.24.12945 · Cited by 104 · see citing works
Characterization of Rous Sarcoma Virus Gag Particles Assembled In Vitro
Yu, F., Joshi, S., Ma, Y. M., Kingston, R., Simon, M., & Vogt, V. (2001) · Journal of Virology · doi:10.1128/jvi.75.6.2753-2764.2001 · Cited by 104 · see citing works
The role of nucleocapsid of HIV-1 in virus assembly
Dawson, L., & Yu, X.-F. (1998) · Virology · doi:10.1006/viro.1998.9374 · Cited by 100 · see citing works
The Role of Cellular Factors in Promoting HIV Budding
Weiss, E. R., & Göttlinger, H. (2011) · Journal of Molecular Biology · doi:10.1016/j.jmb.2011.04.055 · Cited by 95 · see citing works
“Remarkably, different types of L domains can sometimes be exchanged between unrelated viruses, and the function of L domains does not strictly depend on their position within Gag.(5) Together, these observations supported the concept that L domains are conserved docking sites that serve to recruit host factors to the…”
BackgroundInfluentialCovalent Modification of Human Immunodeficiency Virus Type 1 p6 by SUMO-1
Gurer, C., Berthoux, L., & Luban, J. (2005) · Journal of Virology · doi:10.1128/jvi.79.2.910-917.2005 · Cited by 91 · see citing works
“when swapped among viruses (26, 29, 30, 39, 54), suggests that”
BackgroundThe Ubiquitin-Conjugating System: Multiple Roles in Viral Replication and Infection
Calistri, A., Munegato, D., Carli, I., Parolin, C., & Palù, G. (2014) · Cells · doi:10.3390/cells3020386 · Cited by 91 · see citing works
“Finally, the L-domains act independently from their position in the viral protein, frequently occur in combination and can be exchanged between unrelated viruses without losing their ability to mediate budding [188] [189] [190] [191] [192] .”
BackgroundGrowing functions of the ESCRT machinery in cell biology and viral replication
Scourfield, E. J., & Martin‐Serrano, J. (2017) · Biochemical Society Transactions · doi:10.1042/bst20160479 · Cited by 92 · see citing works
Murcia, P. R., Arnaud, F., & Palmarini, M. (2007) · Journal of Virology · doi:10.1128/jvi.01859-06 · Cited by 84 · see citing works
“Mutation of the M domain alters the ability of retroviral Gag to reach the cell membrane (20, 27, 28, 42).”
BackgroundHIV Type 1 Gag as a Target for Antiviral Therapy
Waheed, A. A., & Freed, E. O. (2011) · AIDS Research and Human Retroviruses · doi:10.1089/aid.2011.0230 · Cited by 81 · see citing works
“These motifs were named ‘‘late domains’’ because of their role in virus budding.(188) Three classes of late domains have been identified in retroviral Gag proteins: PT/SAP, PPXY, and YP(X)nL (where ‘‘X’’ is any amino acid, and n = 1–4 residues).”
BackgroundHeidecker, G., Lloyd, P., Fox, K., Nagashima, K., & Derse, D. (2004) · Journal of Virology · doi:10.1128/jvi.78.12.6636-6648.2004 · Cited by 83 · see citing works
“ficking machinery, the motifs can be interchanged and are independent of location to some extent (27, 36, 64).”
BackgroundThe Role of Exosome and the ESCRT Pathway on Enveloped Virus Infection
Ju, Y., Bai, H., Ren, L., & Zhang, L. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22169060 · Cited by 88 · see citing works
Strack, B., Calistri, A., & Göttlinger, H. G. (2002) · Journal of Virology · doi:10.1128/jvi.76.11.5472-5479.2002 · Cited by 80 · see citing works
“Second, the N-terminal 12 residues of HIV-1 p6, which contain the P(T/ S)APP L domain core motif, were sufficient to rescue VLP production by a RSV L domain mutant (21).”
BackgroundLee, Y. M., & Yu, X.-F. (1998) · Virology · doi:10.1006/viro.1998.9064 · Cited by 74 · see citing works
Ma, Y. M., & Vogt, V. M. (2002) · Journal of Virology · doi:10.1128/jvi.76.11.5452-5462.2002 · Cited by 74 · see citing works
Intracellular Trafficking of HBV Particles
Jiang, B.-F., & Hildt, E. (2020) · Cells · doi:10.3390/cells9092023 · Cited by 76 · see citing works
“PPXY late-assembly domains bind NEDD4 family proteins [146,147].”
BackgroundEnssle, J., Fischer, N., Moebes, A., Mauer, B., Smola, U., & Rethwilm, A. (1997) · Journal of Virology · doi:10.1128/jvi.71.10.7312-7317.1997 · Cited by 76 · see citing works
Synthesis and assembly of retrovirus Gag precursors into immature capsids in vitro
Sakalian, M., Parker, S. D., Weldon, R. A., & Hunter, E. (1996) · Journal of Virology · doi:10.1128/jvi.70.6.3706-3715.1996 · Cited by 74 · see citing works
“Functional conservation of the assembly domains among retroviruses has been demonstrated by the ability of various chimeric Gag proteins to assemble and form particles and has led to the functional designations M, L, and I for membrane-binding, late, and interaction domains, respectively (2, 7, 30).”
BackgroundRetroviruses Have Differing Requirements for Proteasome Function in the Budding Process
Ott, D. E., Coren, L. V., Sowder, R. C., Adams, J., & Schubert, U. (2003) · Journal of Virology · doi:10.1128/jvi.77.6.3384-3393.2003 · Cited by 67 · see citing works
Irie, T., Shimazu, Y., Yoshida, T., & Sakaguchi, T. (2006) · Journal of Virology · doi:10.1128/jvi.02218-06 · Cited by 71 · see citing works
“motifs are functionally interchangeable (19, 20, 27, 31, 35, 52).”
BackgroundResultInfluentialDeterminants of activity of the HIV-1 maturation inhibitor PA-457.
Li, F., Zoumplis, D., Matallana, C., Kilgore, N., Reddick, M., Yunus, A., Adamson, C. S., Salzwedel, K., Martin, D. E., Allaway, G., et al. (2006) · Virology · doi:10.1016/j.virol.2006.07.023 · Cited by 70 · see citing works
“This deletion-based mutagenesis approach has been successfully used to characterize various functional domains of retroviral Gag including MA, CA, NC, and the late-assembly domain (Dorfman et al., 1994; Nelle and Wills, 1996; Ott et al., 2005; Parent et al., 1995; Puffer et al., 1997; Reil et al., 1998; Srinivasakumar…”
MethodBlanc, I., Prévost, M., Dokhélar, M., & Rosenberg, A. R. (2002) · Journal of Virology · doi:10.1128/jvi.76.19.10024-10029.2002 · Cited by 65 · see citing works
“tion despite the lack of sequence homology (1, 22, 24, 40).”
BackgroundLee, Y. M., Liu, B., & Yu, X.-F. (1999) · Journal of Virology · doi:10.1128/jvi.73.7.5654-5662.1999 · Cited by 67 · see citing works
“Although the formation of the HIV-1 DRC does not require a membrane association signal (M domain) or the L domain in p6, which is required for efficient virus release from the cell surface (11, 14, 22, 29, 41), its formation does require the putative protein-protein interaction domain (I domain) located in the NC regi…”
BackgroundFunctional Interchangeability of Late Domains, Late Domain Cofactors and Ubiquitin in Viral Budding
Zhadina, M., & Bieniasz, P. (2010) · PLoS Pathogens · doi:10.1371/journal.ppat.1001153 · Cited by 69 · see citing works
“The intrinsic manipulability of L-domains, the proteins that bind to them (specifically ESCRT-I and HECT ubiquitin ligases) and the apparent lack of importance of the identity of ubiquitination substrate suggests that each serve simply as recruitment factors to engage the downstream machinery that mediates membrane fi…”
BackgroundDynamic Interactions of the Gag Polyprotein
Craven, R. C., & Parent, L. J. (1996) · Current topics in microbiology and immunology · doi:10.1007/978-3-642-80145-7_3 · Cited by 64 · see citing works
Self-citation
- Authors
- Parent, L. J., Bennett, R. P., Craven, R. C., Nelle, T. D., Krishna, N. K., Bowzard, J. B., Wilson, C. B., Puffer, B. A., Montelaro, R. C., & Wills, J. W.
- Affiliations
- Pennsylvania State University (US)
- Venue
- Journal of Virology
- Publisher
- American Society for Microbiology
- Published
- 1995-09
- Volume
- 69
- Issue
- 9
- Pages
- 5455-5460
- ISSN
- 0022-538X (ISSN-L)
- 1098-5514
- PMC
- PMC189393
- OpenAlex
- W2157103983
- Cited by
- 258
- References
- 27
- Citations by year
- 2026: 3 · 2025: 2 · 2024: 1 · 2023: 4 · 2022: 5 · 2021: 4 · 2020: 6 · 2019: 4 · 2018: 4 · 2017: 2 · 2016: 2 · 2015: 6 · 2014: 2 · 2013: 11 · 2012: 8
- FWCI
- 3.85
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Journal of Virology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5k11ai001148-05)
- National Cancer Institute (CA60395, T32CA060395)
- National Institute of Allergy and Infectious Diseases (R01AI025850, AI 25850, K11 AI01148)
- Topics
- Life Sciences › Immunology and Microbiology › Virology › HIV Research and Treatment
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and Retrovirus Studies
- Health Sciences › Medicine › Infectious Diseases › HIV/AIDS drug development and treatment
- Keywords
- Rous sarcoma virus, HIV-1, Gag protein, viral assembly, matrix protein, capsid protein
- MeSH terms
- Alleles, Amino Acid Sequence, Animals, Avian Sarcoma Viruses, Base Sequence, Cell Line, Chlorocebus aethiops, Cloning, Molecular, HIV, Kidney, Molecular Sequence Data, Recombinant Proteins, Species Specificity, Transfection, Gene Products, gag, Genes, gag, Polymerase Chain Reaction, Sequence Deletion, Sequence Homology, Amino Acid, DNA Primers
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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