In vitro assembly properties of human immunodeficiency virus type 1 Gag protein lacking the p6 domain
Open accessAbstract
Human immunodeficiency virus type 1 (HIV-1) normally assembles into particles of 100 to 120 nm in diameter by budding through the plasma membrane of the cell. The Gag polyprotein is the only viral protein that is required for the formation of these particles. We have used an in vitro assembly system to examine the assembly properties of purified, recombinant HIV-1 Gag protein and of Gag missing the C-terminal p6 domain (Gag Deltap6). This system was used previously to show that the CA-NC fragment of HIV-1 Gag assembled into cylindrical particles. We now report that both HIV-1 Gag and Gag Deltap6 assemble into small, 25- to 30-nm-diameter spherical particles in vitro. The multimerization of Gag Deltap6 into units larger than dimers and the formation of spherical particles required nucleic acid. Removal of the nucleic acid with NaCl or nucleases resulted in the disruption of the multimerized complexes. We conclude from these results that (i) N-terminal extension of HIV-1 CA-NC to include the MA domain results in the formation of spherical, rather than cylindrical, particles; (ii) nucleic acid is required for the assembly and maintenance of HIV-1 Gag Deltap6 virus-like particles in vitro and possibly in vivo; (iii) a wide variety of RNAs or even short DNA oligonucleotides will support assembly; (iv) protein-protein interactions within the particle must be relatively weak; and (v) recombinant HIV-1 Gag Deltap6 and nucleic acid are not sufficient for the formation of normal-sized…
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Cites
[6] Use of T7 RNA polymerase to direct expression of cloned genes
Studier, F. W., Rosenberg, A. H., Dunn, J. J., & Dubendorff, J. W. (1990) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/0076-6879(90)85008-c · Cited by 6,562 · see citing works
Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes
Studier, F. W., & Moffatt, B. A. (1986) · Journal of Molecular Biology · doi:10.1016/0022-2836(86)90385-2 · Cited by 6,372 · see citing works
Adachi, A., Gendelman, H., Koenig, S., Folks, T., Willey, R., Rabson, A., & Martin, M. (1986) · Journal of Virology · doi:10.1128/jvi.59.2.284-291.1986 · Cited by 3,019 · see citing works
Mann, R., Mulligan, R. C., & Baltimore, D. (1983) · Cell · doi:10.1016/0092-8674(83)90344-6 · Cited by 1,855 · see citing works
Crystal Structure of Human Cyclophilin A Bound to the Amino-Terminal Domain of HIV-1 Capsid
Gamble, T. R., Vajdos, F. F., Yoo, S., Worthylake, D. K., Houseweart, M., Sundquist, W. I., & Hill, C. P. (1996) · Cell · doi:10.1016/s0092-8674(00)81823-1 · Cited by 706 · see citing works
Effect of mutations affecting the p6 gag protein on human immunodeficiency virus particle release
Göttlinger, H. G., Dorfman, T., Sodroski, J. G., & Haseltine, W. A. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.8.3195 · Cited by 647 · see citing works
Huang, M., Orenstein, J. M., Martin, M. A., & Freed, E. O. (1995) · Journal of Virology · doi:10.1128/jvi.69.11.6810-6818.1995 · Cited by 486 · see citing works
Structure of the Amino-Terminal Core Domain of the HIV-1 Capsid Protein
Gitti, R. K., Lee, B. M., Walker, J., Summers, M. F., Yoo, S., & Sundquist, W. I. (1996) · Science · doi:10.1126/science.273.5272.231 · Cited by 459 · 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
Self-citationProteolytic refolding of the HIV‐1 capsid protein amino‐terminus facilitates viral core assembly
von Schwedler, U. K., Stemmler, T. L., Klishko, V. Y., Li, S., Albertine, K. H., Davis, D. R., & Sundquist, W. I. (1998) · The EMBO Journal · doi:10.1093/emboj/17.6.1555 · Cited by 337 · see citing works
Crystal structure of dimeric HIV-1 capsid protein
Momany, C., Kovari, L. C., Prongay, A., Keller, W., Gitti, R. K., Lee, B. M., Gorbalenya, A. E., Tong, L., McClure, J., Ehrlich, L. S., et al. (1996) · Nature Structural & Molecular Biology · doi:10.1038/nsb0996-763 · Cited by 313 · see citing works
Summers, M. F., Henderson, L. E., Chance, M. R., South, T. L., Blake, P. R., Pérez-Alvarado, G. C., Bess, J. W., Sowder, R. C., Arthur, L. O., Sagi, I., et al. (1992) · Protein Science · doi:10.1002/pro.5560010502 · Cited by 306 · see citing works
Berkowitz, R. D., Fisher, J., & Goff, S. P. (1996) · Current topics in microbiology and immunology · doi:10.1007/978-3-642-80145-7_6 · Cited by 282 · see citing works
Three-dimensional structure of the human immunodeficiency virus type 1 matrix protein
Massiah, M. A., Starich, M. R., Paschall, C., Summers, M. F., Christensen, A. M., & Sundquist, W. I. (1994) · Journal of Molecular Biology · doi:10.1006/jmbi.1994.1719 · Cited by 271 · see citing works
Morellet, N., Jullian, N., de ROCQUIGNY, H., Maigret, B., Darlix, J., & Roques, B. P. (1992) · The EMBO Journal · doi:10.1002/j.1460-2075.1992.tb05377.x · Cited by 256 · see citing works
Méric, C., & Goff, S. P. (1989) · Journal of Virology · doi:10.1128/jvi.63.4.1558-1568.1989 · Cited by 255 · 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
Functional domains of the capsid protein of human immunodeficiency virus type 1
Dorfman, T., Bukovský, A., Öhagen, Å., Höglund, S., & Göttlinger, H. G. (1994) · Journal of Virology · doi:10.1128/jvi.68.12.8180-8187.1994 · Cited by 218 · see citing works
Assembly of recombinant human immunodeficiency virus type 1 capsid protein in vitro
Ehrlich, L. S., Agresta, B. E., & Carter, C. A. (1992) · Journal of Virology · doi:10.1128/jvi.66.8.4874-4883.1992 · Cited by 218 · see citing works
Gross, I., Hohenberg, H., & Kräusslich, H. (1997) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1997.t01-1-00592.x · Cited by 198 · see citing works
Berkowitz, R. D., Luban, J., & Goff, S. P. (1993) · Journal of Virology · doi:10.1128/jvi.67.12.7190-7200.1993 · Cited by 193 · cited 1× · see citing works
“This has been observed by others (6, 12, 30) and appears to be due to cleavage near the C terminus of Gag during expression in E.”
BackgroundYeager, M., Wilson-Kubalek, E. M., Weiner, S. G., Brown, P. O., & Rein, A. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.13.7299 · Cited by 189 · see citing works
Self-citationCrystal structure of SIV matrix antigen and implications for virus assembly
Rao, Z., Belyaev, A. S., Fry, E., Roy, P., Jones, I. M., & Stuart, D. I. (1995) · Nature · doi:10.1038/378743a0 · Cited by 183 · see citing works
Fisher, R., Rein, A., Fivash, M., Urbaneja, M., Casas-Finet, J., Medaglia, M. V., & Henderson, L. (1998) · Journal of Virology · doi:10.1128/jvi.72.3.1902-1909.1998 · Cited by 175 · see citing works
Self-citationGross, I., Hohenberg, H., Huckhagel, C., & Kräusslich, H. (1998) · Journal of Virology · doi:10.1128/jvi.72.6.4798-4810.1998 · Cited by 173 · 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
Self-citationInteractions of retroviral structural proteins with single-stranded nucleic acids.
Karpel, R. L., Henderson, L. E., & Oroszlan, S. I. (1987) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)61139-1 · Cited by 158 · see citing works
Properties of avian retrovirus particles defective in viral protease
Stewart, L., Schatz, G. W., & Vogt, V. M. (1990) · Journal of Virology · doi:10.1128/jvi.64.10.5076-5092.1990 · Cited by 156 · see citing works
Levin, J. G., Grimley, P. M., Ramseur, J. M., & Berezesky, I. K. (1974) · Journal of Virology · doi:10.1128/jvi.14.1.152-161.1974 · Cited by 153 · see citing works
Functional chimeras of the Rous sarcoma virus and human immunodeficiency virus gag proteins
Bennett, R. P., Nelle, T. D., & Wills, J. W. (1993) · Journal of Virology · doi:10.1128/jvi.67.11.6487-6498.1993 · Cited by 130 · see citing works
Structural similarity between the p17 matrix protein of HIV-1 and interferon-γ
Matthews, S., Barlow, P. N., Boyd, J. W., Barton, G. J., Russell, R. B., Mills, H. R., Cunningham, M., Meyers, N., Burns, N. R., Clark, N., et al. (1994) · Nature · doi:10.1038/370666a0 · Cited by 125 · see citing works
Nermut, M. V., HOCKLEY, D. J., Jowett, J. B. M., Jones, I. M., Garreau, M., & Thomas, D. (1994) · Virology · doi:10.1006/viro.1994.1032 · Cited by 123 · see citing works
Lingappa, J. R., Hill, R. L., Wong, M. L., & Hegde, R. S. (1997) · The Journal of Cell Biology · doi:10.1083/jcb.136.3.567 · Cited by 118 · see citing works
Formation of Stable and Functional HIV-1 Nucleoprotein Complexesin Vitro
Tanchou, V., Gabus, C., Rogemond, V., & Darlix, J. L. (1995) · Journal of Molecular Biology · doi:10.1006/jmbi.1995.0520 · Cited by 111 · see citing works
Binding of human immunodeficiency virus type 1 (HIV-1) RNA to recombinant HIV-1 gag polyprotein
Luban, J., & Goff, S. P. (1991) · Journal of Virology · doi:10.1128/jvi.65.6.3203-3212.1991 · Cited by 108 · cited 1× · see citing works
“This has been observed by others (6, 12, 30) and appears to be due to cleavage near the C terminus of Gag during expression in E.”
BackgroundJohnson, J. E., & Speir, J. A. (1999) · Elsevier eBooks · doi:10.1006/rwvi.1999.0308 · Cited by 105 · see citing works
Functional domains of HIV-1gag-polyprotein expressed in baculovirus-infected cells
Royer, M., Cérutti, M., Gay, B., Hong, S. S., Devauchelle, G., & Boulanger, P. A. (1991) · Virology · doi:10.1016/0042-6822(91)90861-5 · Cited by 94 · see citing works
Structural analysis of membrane‐bound retrovirus capsid proteins
Barklis, E., McDermott, J., Wilkens, S., Schabtach, E., Schmid, M. F., Fuller, S., Karanjia, S., Love, Z., Jones, R., Rui, Y., et al. (1997) · The EMBO Journal · doi:10.1093/emboj/16.6.1199 · Cited by 91 · see citing works
Weldon, R., & Wills, J. W. (1993) · Journal of Virology · doi:10.1128/jvi.67.9.5550-5561.1993 · Cited by 88 · see citing works
Identification of retrovirus matrix proteins by lipid-protein cross-linking
Pepinsky, R. B., & Vogt, V. M. (1979) · Journal of Molecular Biology · doi:10.1016/0022-2836(79)90203-1 · Cited by 87 · see citing works
Electron Microscopy of Human Immunodeficiency Virus
HOCKLEY, D. J., Wood, R. D., Jacobs, J. P., & Garrett, A. J. (1988) · Journal of General Virology · doi:10.1099/0022-1317-69-10-2455 · Cited by 86 · see citing works
Klikova, M., Rhee, S. S., Hunter, E., & Ruml, T. (1995) · Journal of Virology · doi:10.1128/jvi.69.2.1093-1098.1995 · Cited by 85 · see citing works
Chazal, N., Carrière, C., Gay, B., & Boulanger, P. A. (1994) · Journal of Virology · doi:10.1128/jvi.68.1.111-122.1994 · Cited by 81 · see citing works
Pepinsky, R. B. (1983) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)44407-3 · Cited by 80 · 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
Massiah, M. A., Worthylake, D. K., Christensen, A. M., Sundquist, W. I., Hill, C. P., & Summers, M. F. (1996) · Protein Science · doi:10.1002/pro.5560051202 · Cited by 65 · see citing works
Partitioning of HIV-1 Gag and Gag-Related Proteins to Membranes
Ehrlich, L. S., Fong, S., Scarlata, S., Zybarth, G., & Carter, C. (1996) · Biochemistry · doi:10.1021/bi952337x · Cited by 62 · see citing works
Morikawa, Y., Hinata, S., Tomoda, H., Goto, T., Nakai, M., Aizawa, C., Tanaka, H., & ̄mura, S. O. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.5.2868 · Cited by 60 · see citing works
Genetic Determinants of Rous Sarcoma Virus Particle Size
Krishna, N. K., Campbell, S., Vogt, V., & Wills, J. (1998) · Journal of Virology · doi:10.1128/jvi.72.1.564-577.1998 · Cited by 57 · see citing works
Self-citationHOCKLEY, D. J., Nermut, M. V., Grief, C., Jowett, J. B. M., & Jones, I. M. (1994) · Journal of General Virology · doi:10.1099/0022-1317-75-11-2985 · Cited by 57 · see citing works
Morphogenesis and Maturation of Retroviruses
Kräusslich, H. (1996) · Current Topics in Microbiology and Immunology · doi:10.1007/978-3-642-80145-7 · Cited by 54 · see citing works
Human immunodeficiency virus type 1 capsid formation in reticulocyte lysates
Spearman, P. W., & Ratner, L. (1996) · Journal of Virology · doi:10.1128/jvi.70.11.8187-8194.1996 · Cited by 51 · see citing works
Pepinsky, R. B., & Vogt, V. M. (1984) · Journal of Virology · doi:10.1128/jvi.52.1.145-153.1984 · Cited by 46 · see citing works
Chemical crosslinking of proteins in avian sarcoma and leukemia viruses
Pepinsky, R. B., Cappiello, D., Wilkowski, C. W., & Vogt, V. M. (1980) · Virology · doi:10.1016/0042-6822(80)90081-1 · Cited by 42 · see citing works
Type D Retrovirus Capsid Assembly and Release Are Active Events Requiring ATP
Weldon, R. A., Parker, W. B., Sakalian, M., & Hunter, E. (1998) · Journal of Virology · doi:10.1128/jvi.72.4.3098-3106.1998 · Cited by 32 · see citing works
Complementation of Human Immunodeficiency Virus (HIV-1) Gag Particle Formation
Zhao, Y., Jones, I. M., HOCKLEY, D. J., Nermut, M. V., & Roy, P. (1994) · Virology · doi:10.1006/viro.1994.1138 · Cited by 20 · see citing works
Gorelick, R. J., Nigida, S. M., Arthur, L. O., Henderson, L. E., & Rein, A. R. (1991) · Springer eBooks · doi:10.1007/978-1-4684-5928-9_24 · Cited by 12 · see citing works
Self-citationSu, L. (1997) · Reviews in Medical Virology · doi:10.1002/(sici)1099-1654(199709)7:3 · Cited by 7 · see citing works
Flagged first, then by citations
1 of the 59 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Pastuzyn, E. D., Day, C. E., Kearns, R. B., Kyrke‐Smith, M., Taibi, A. V., McCormick, J. F., Yoder, N., Belnap, D. M., Erlendsson, S., Morado, D. R., et al. (2018) · Cell · doi:10.1016/j.cell.2017.12.024 · Cited by 642 · 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
The stoichiometry of Gag protein in HIV-1
Briggs, J. A. G., Simon, M. N., Gross, I., Kräusslich, H.-G., Fuller, S. D., Vogt, V. M., & Johnson, M. C. (2004) · Nature Structural & Molecular Biology · doi:10.1038/nsmb785 · Cited by 539 · see citing works
The structural biology of HIV assembly
Ganser‐Pornillos, B. K., Yeager, M. J., & Sundquist, W. I. (2008) · Current Opinion in Structural Biology · doi:10.1016/j.sbi.2008.02.001 · Cited by 500 · see citing works
RNA is a structural element in retrovirus particles
Muriaux, D. M., Mirro, J., Harvin, D., & Rein, A. R. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.091000398 · Cited by 302 · see citing works
Self-citationDimerization of retroviral RNA genomes: an inseparable pair
Paillart, J., Shehu-Xhilaga, M., Marquet, R., & Mak, J. (2004) · Nature Reviews Microbiology · doi:10.1038/nrmicro903 · Cited by 291 · see citing works
Hexagonal assembly of a restricting TRIM5α protein
Ganser‐Pornillos, B. K., Chandrasekaran, V., Pornillos, O., Sodroski, J., Sundquist, W. I., & Yeager, M. J. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1013426108 · Cited by 248 · see citing works
A conformational switch controlling HIV‐1 morphogenesis
Gross, I., Hohenberg, H., Wilk, T., Wiegers, K. J., Grättinger, M., Müller, B., Fuller, S., & Kräusslich, H. (2000) · The EMBO Journal · doi:10.1093/emboj/19.1.103 · Cited by 241 · see citing works
The Molecular Architecture of HIV
Briggs, J. A. G., & Kräusslich, H. (2011) · Journal of Molecular Biology · doi:10.1016/j.jmb.2011.04.021 · Cited by 208 · see citing works
Analysis of the Initiating Events in HIV-1 Particle Assembly and Genome Packaging
Kutluay, S. B., & Bieniasz, P. D. (2010) · PLoS Pathogens · doi:10.1371/journal.ppat.1001200 · Cited by 203 · see citing works
Cimarelli, A., Sandin, S., Höglund, S., & Luban, J. (2000) · Journal of Virology · doi:10.1128/jvi.74.7.3046-3057.2000 · Cited by 220 · see citing works
Modulation of HIV-like particle assembly in vitro by inositol phosphates
Campbell, S., Fisher, R. J., Towler, E. M., Fox, S. D., Issaq, H. J., Wolfe, T. L., Phillips, L. R., & Rein, A. R. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.191224698 · Cited by 199 · see citing works
Self-citationSelective and nonselective packaging of cellular RNAs in retrovirus particles
Rulli, S. J., Hibbert, C. S., Mirro, J., Pederson, T., Biswal, S., & Rein, A. (2007) · Journal of Virology · doi:10.1128/jvi.02833-06 · Cited by 191 · see citing works
Self-citationRole of HIV-1 nucleocapsid protein in HIV-1 reverse transcription
Levin, J. G., Mitra, M., Mascarenhas, A. P., & Musier‐Forsyth, K. (2010) · RNA Biology · doi:10.4161/rna.7.6.14115 · Cited by 181 · see citing works
Human 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
Assembly and Architecture of HIV
Ganser‐Pornillos, B. K., Yeager, M. J., & Pornillos, O. (2011) · Advances in experimental medicine and biology · doi:10.1007/978-1-4614-0980-9_20 · Cited by 161 · see citing works
The generation and use of recombinant extracellular vesicles as biological reference material
Geeurickx, E., Tulkens, J., Dhondt, B., Deun, J. V., Lippens, L., Vergauwen, G., Heyrman, E., Sutter, D. D., Gevaert, K., Impens, F., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-11182-0 · Cited by 165 · see citing works
Nucleocapsid protein function in early infection processes
Thomas, J. A., & Gorelick, R. J. (2008) · Virus Research · doi:10.1016/j.virusres.2007.12.006 · Cited by 162 · see citing works
Feng, Y.-X., Campbell, S., Harvin, D., Ehresmann, B., Ehresmann, C., & Rein, A. (1999) · Journal of Virology · doi:10.1128/jvi.73.5.4251-4256.1999 · Cited by 159 · see citing works
Self-citationNucleic acid binding and chaperone properties of HIV-1 Gag and nucleocapsid proteins
Cruceanu, M. (2006) · Nucleic Acids Research · doi:10.1093/nar/gkj458 · Cited by 149 · see citing works
Dussupt, 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
Pettit, S. C., Everitt, L., Choudhury, S., Dunn, B. M., & Kaplan, A. H. (2004) · Journal of Virology · doi:10.1128/jvi.78.16.8477-8485.2004 · Cited by 145 · see citing works
Conformation of the HIV-1 Gag Protein in Solution
Datta, S. A. K., Curtis, J. E., Ratcliff, W., Clark, P. K., Crist, R. M., Lebowitz, J., Krueger, S., & Rein, A. (2007) · Journal of Molecular Biology · doi:10.1016/j.jmb.2006.10.073 · Cited by 145 · see citing works
Self-citationCellular proteins detected in HIV‐1
Ott, D. E. (2008) · Reviews in Medical Virology · doi:10.1002/rmv.570 · Cited by 141 · see citing works
Virus assembly, allostery and antivirals
Zlotnick, A., & Mukhopadhyay, S. (2010) · Trends in Microbiology · doi:10.1016/j.tim.2010.11.003 · Cited by 141 · see citing works
Interactions between HIV-1 Gag Molecules in Solution: An Inositol Phosphate-mediated Switch
Datta, S. A. K., Zhao, Z., Clark, P. K., Tarasov, S. G., Alexandratos, J. N., Campbell, S. J., Kvaratskhelia, M., Lebowitz, J., & Rein, A. R. (2006) · Journal of Molecular Biology · doi:10.1016/j.jmb.2006.10.072 · Cited by 132 · see citing works
Self-citationCrystal structure of an HIV assembly and maturation switch
Wagner, J. M., Zadrozny, K. K., Chrustowicz, J., Purdy, M. D., Yeager, M. J., Ganser‐Pornillos, B. K., & Pornillos, O. (2016) · eLife · doi:10.7554/elife.17063 · Cited by 131 · see citing works
Hogue, I. B., Grover, J. R., Soheilian, F., Nagashima, K., & Ono, A. (2011) · Journal of Virology · doi:10.1128/jvi.00743-11 · Cited by 129 · see citing works
On the Role of the SP1 Domain in HIV-1 Particle Assembly: a Molecular Switch?
Datta, S. A. K., Temeselew, L. G., Crist, R. M., Soheilian, F., Kamata, A., Mirro, J., Harvin, D., Nagashima, K., Cachau, R. E., & Rein, A. (2011) · Journal of Virology · doi:10.1128/jvi.00006-11 · Cited by 127 · see citing works
Self-citationLanman, J. K., Sexton, J., Sakalian, M., & Prevelige, P. E. (2002) · Journal of Virology · doi:10.1128/jvi.76.14.6900-6908.2002 · Cited by 123 · see citing works
Göttlinger, H. G. (2001) · AIDS · doi:10.1097/00002030-200100005-00003 · Cited by 124 · see citing works
Is HIV-1 RNA dimerization a prerequisite for packaging? Yes, no, probably?
Russell, R., Chen, L., & Wainberg, M. (2004) · Retrovirology · doi:10.1186/1742-4690-1-23 · Cited by 125 · see citing works
Datta, S. A. K., Heinrich, F., Raghunandan, S., Krueger, S., Curtis, J. E., Rein, A. R., & Nanda, H. (2010) · Journal of Molecular Biology · doi:10.1016/j.jmb.2010.11.051 · Cited by 114 · 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
Virus-like particles as HIV-1 vaccines
Doan, L. X., Li, M., Chen, C., & Yao, Q. C. (2004) · Reviews in Medical Virology · doi:10.1002/rmv.449 · Cited by 113 · see citing works
Tritel, M., & Resh, M. D. (2000) · Journal of Virology · doi:10.1128/jvi.74.13.5845-5855.2000 · Cited by 113 · see citing works
The Life-Cycle of the HIV-1 Gag–RNA Complex
Mailler, É., Bernacchi, S., Marquet, R., Paillart, J., Vivet‐Boudou, V., & Smyth, R. P. (2016) · Viruses · doi:10.3390/v8090248 · Cited by 113 · see citing works
Sandefur, 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
Larson, D. R., Ma, Y. M., Vogt, V. M., & Webb, W. W. (2003) · The Journal of Cell Biology · doi:10.1083/jcb.200303200 · Cited by 109 · see citing works
Protein intrinsic disorder as a flexible armor and a weapon of HIV-1
Xue, B., Mizianty, M. J., Kurgan, L., & Uversky, V. N. (2011) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-011-0859-3 · Cited by 107 · see citing works
Nucleic Acid-Independent Retrovirus Assembly Can Be Driven by Dimerization
Johnson, M. C., Scobie, H. M., Ma, Y. M., & Vogt, V. M. (2002) · Journal of Virology · doi:10.1128/jvi.76.22.11177-11185.2002 · Cited by 105 · see citing works
Liang, C., Hu, J., Russell, R. S., Roldán, A., Kleiman, L., & Wainberg, M. A. (2002) · Journal of Virology · doi:10.1128/jvi.76.22.11729-11737.2002 · Cited by 103 · see citing works
Domain-swapped dimerization of the HIV-1 capsid C-terminal domain
Ivanov, D., Tsodikov, O. V., Kasanov, J., Ellenberger, T., Wagner, G., & Collins, T. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0609477104 · Cited by 100 · see citing works
Diverse interactions of retroviral Gag proteins with RNAs
Rein, A. R., Datta, S. A. K., Jones, C. P., & Musier‐Forsyth, K. (2011) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2011.04.001 · Cited by 97 · see citing works
Self-citationLingappa, J. R., Dooher, J. E., Newman, M. A., Kiser, P. K., & Klein, K. C. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m507255200 · Cited by 98 · see citing works
Cruceanu, M., Gorelick, R. J., Musier‐Forsyth, K., Rouzina, I. F., & Williams, M. C. (2006) · Journal of Molecular Biology · doi:10.1016/j.jmb.2006.08.070 · Cited by 97 · see citing works
Rein, A. R. (2019) · Trends in Microbiology · doi:10.1016/j.tim.2019.04.003 · Cited by 96 · see citing works
Self-citationPak, A. J., Grime, J. M. A., Sengupta, P., Chen, A. K., Durumeric, A. E. P., Srivastava, A. K., Yeager, M. J., Briggs, J. A. G., Lippincott‐Schwartz, J., & Voth, G. A. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1706600114 · Cited by 96 · see citing works
Carlson, L. A., & Hurley, J. H. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1211759109 · Cited by 94 · see citing works
Mechanisms of DNA binding determined in optical tweezers experiments
McCauley, M. J., & Williams, M. C. (2006) · Biopolymers · doi:10.1002/bip.20622 · Cited by 94 · see citing works
Matrix domain modulates HIV-1 Gag's nucleic acid chaperone activity via inositol phosphate binding
Jones, C. P., Datta, S. A. K., Rein, A., Rouzina, I., & Musier-Forsyth, K. (2011) · Journal of Virology · doi:10.1128/jvi.01809-10 · Cited by 94 · see citing works
Self-citationCharacterization 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
Derdowski, 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
Crist, R. M., Datta, S. A. K., Stephen, A. G., Soheilian, F., Mirro, J., Fisher, R. J., Nagashima, K., & Rein, A. R. (2008) · Journal of Virology · doi:10.1128/jvi.02031-08 · Cited by 90 · see citing works
Self-citationHIV-1 Gag co-opts a cellular complex containing DDX6, a helicase that facilitates capsid assembly
Reed, J. C., Molter, B., Geary, C. D., McNevin, J. P., McElrath, J., Giri, S., Klein, K. C., & Lingappa, J. R. (2012) · The Journal of Cell Biology · doi:10.1083/jcb.201111012 · Cited by 90 · see citing works
Briggs, J. A. G., Johnson, M. C., Simon, M. N., Fuller, S. D., & Vogt, V. M. (2005) · Journal of Molecular Biology · doi:10.1016/j.jmb.2005.10.025 · Cited by 89 · see citing works
How HIV-1 Gag assembles in cells: Putting together pieces of the puzzle
Lingappa, J. R., Reed, J. C., Tanaka, M., Chutiraka, K., & Robinson, B. A. (2014) · Virus Research · doi:10.1016/j.virusres.2014.07.001 · Cited by 91 · see citing works
Ono, A., Waheed, A. A., Joshi, A., & Freed, E. O. (2005) · Journal of Virology · doi:10.1128/jvi.79.22.14131-14140.2005 · Cited by 91 · see citing works
Ott, D. E., Coren, L. V., & Gagliardi, T. D. (2005) · Journal of Virology · doi:10.1128/jvi.79.22.13839-13847.2005 · Cited by 90 · see citing works
Li, H., Dou, J., Ding, L., & Spearman, P. W. (2007) · Journal of Virology · doi:10.1128/jvi.01280-07 · Cited by 89 · see citing works
Ramalingam, D., Duclair, S., Datta, S. A. K., Ellington, A. D., Rein, A. R., & Prasad, V. R. (2010) · Journal of Virology · doi:10.1128/jvi.02626-09 · Cited by 89 · see citing works
Self-citationShehu-Xhilaga, M., Kraeusslich, H.-G., Pettit, S. C., Swanstrom, R. I., Jy, L., Marshall, J. A., Crowe, S. M., & Mak, J. (2001) · Journal of Virology · doi:10.1128/jvi.75.19.9156-9164.2001 · Cited by 87 · see citing works
Developments in virus-like particle-based vaccines for infectious diseases and cancer
Buonaguro, L., Tagliamonte, M., Tornesello, M. L., & Buonaguro, L. (2011) · Expert Review of Vaccines · doi:10.1586/erv.11.135 · Cited by 85 · see citing works
Llewellyn, G. N., Hogue, I. B., Grover, J. R., & Ono, A. (2010) · PLoS Pathogens · doi:10.1371/journal.ppat.1001167 · Cited by 85 · see citing works
Intracellular HIV-1 Gag localization is impaired by mutations in the nucleocapsid zinc fingers
Grigorov, B., Décimo, D., Smagulova, F. O., Péchoux, C., Mougel, M., Muriaux, D. M., & Darlix, J. (2007) · Retrovirology · doi:10.1186/1742-4690-4-54 · Cited by 84 · see citing works
On the Selective Packaging of Genomic RNA by HIV-1
Comas‐García, M., Davis, S. R., & Rein, A. R. (2016) · Viruses · doi:10.3390/v8090246 · Cited by 79 · see citing works
Self-citationHogue, I. B., Hoppe, A. D., & Ono, A. (2009) · Journal of Virology · doi:10.1128/jvi.02545-08 · Cited by 79 · see citing works
In vitro characterization of the interaction between HIV-1 Gag and human lysyl-tRNA synthetase
Kovaleski, B. J., Kennedy, R., Hong, M. K., Datta, S. A., Kleiman, L., Rein, A., & Musier-Forsyth, K. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m601189200 · Cited by 75 · see citing works
Self-citationRetrovirus Capsid Protein Assembly Arrangements
Mayo, K., Huseby, D. L., McDermott, J., Arvidson, B., Finlay, L. A., & Barklis, E. (2002) · Journal of Molecular Biology · doi:10.1016/s0022-2836(02)01176-2 · Cited by 75 · see citing works
Biomedicine and Diseases: Review¶Assembling the human immunodeficiency virus type 1
Cimarelli, A., & Darlix, J. (2002) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-002-8495-6 · Cited by 79 · 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
Liang, C., Hu, J., Whitney, J. B., Kleiman, L., & Wainberg, M. A. (2003) · Journal of Virology · doi:10.1128/jvi.77.3.1772-1783.2003 · Cited by 72 · see citing works
IP6 Regulation of HIV Capsid Assembly, Stability, and Uncoating
Dick, R. A., Mallery, D. L., Vogt, V. M., & James, L. C. (2018) · Viruses · doi:10.3390/v10110640 · Cited by 71 · see citing works
Human Immunodeficiency Virus Type 1 Gag Polyprotein Modulates Its Own Translation
Anderson, E. C., & Lever, A. (2006) · Journal of Virology · doi:10.1128/jvi.02596-05 · Cited by 84 · see citing works
Ma, Y. M., & Vogt, V. M. (2003) · Journal of Virology · doi:10.1128/jvi.78.1.52-60.2004 · Cited by 70 · see citing works
The molecular basis of HIV capsid assembly—five years of progress
Adamson, C. S., & Jones, I. M. (2004) · Reviews in Medical Virology · doi:10.1002/rmv.418 · Cited by 69 · see citing works
Dooher, J. E., Schneider, B. L., Reed, J. C., & Lingappa, J. R. (2006) · Traffic · doi:10.1111/j.1600-0854.2006.00524.x · Cited by 67 · see citing works
Wrapping up the bad news – HIV assembly and release
Meng, B., & Lever, A. M. (2013) · Retrovirology · doi:10.1186/1742-4690-10-5 · Cited by 68 · see citing works
Klein, K. C., Dellos, S. R., & Lingappa, J. R. (2005) · Journal of Virology · doi:10.1128/jvi.79.11.6814-6826.2005 · Cited by 68 · see citing works
Dissection of specific binding of HIV-1 Gag to the 'packaging signal' in viral RNA
Comas-García, M., Datta, S., Baker, L. A., Varma, R., Gudla, P. R., & Rein, A. (2017) · eLife · doi:10.7554/elife.27055 · Cited by 60 · see citing works
Self-citationHost–rabies virus protein–protein interactions as druggable antiviral targets
Lingappa, U. F., Wu, X., Macieik, A., Yu, S. F., Atuegbu, A. E. R., Corpuz, M., Francis, J., Nichols, C., Calayag, A., Hong, S., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1210198110 · Cited by 63 · see citing works
Müller, B., Patschinsky, T., & Kräusslich, H. (2002) · Journal of Virology · doi:10.1128/jvi.76.3.1015-1024.2002 · Cited by 61 · see citing works
Nucleic acid chaperone activity of retroviral Gag proteins
Rein, A. R. (2010) · RNA Biology · doi:10.4161/rna.7.6.13685 · Cited by 62 · see citing works
Self-citationHIV-1 Pr55<sup>Gag</sup>binds genomic and spliced RNAs with different affinity and stoichiometry
Bernacchi, S., Abd El-Wahab, E. W., Dubois, N., Hijnen, M., Smyth, R. P., Mak, J., Marquet, R., & Paillart, J.-C. (2017) · RNA Biology · doi:10.1080/15476286.2016.1256533 · Cited by 61 · see citing works
In vitro methods for testing antiviral drugs
Rumlová, M., & Ruml, T. (2017) · Biotechnology Advances · doi:10.1016/j.biotechadv.2017.12.016 · Cited by 62 · see citing works
Basic Residues in the Nucleocapsid Domain of Gag Are Critical for Late Events of HIV-1 Budding
Dussupt, V., Sette, P., Bello, N. F., Javid, M. P., Nagashima, K., & Bouamr, F. (2011) · Journal of Virology · doi:10.1128/jvi.01562-10 · Cited by 60 · see citing works
Joshi, A., Nagashima, K., & Freed, E. O. (2006) · Journal of Virology · doi:10.1128/jvi.00355-06 · Cited by 60 · see citing works
Ott, D. E., Coren, L. V., Chertova, E. N., Gagliardi, T. D., Nagashima, K., Sowder, R. C., Poon, D. T. K., & Gorelick, R. J. (2003) · Journal of Virology · doi:10.1128/jvi.77.10.5547-5556.2003 · Cited by 59 · see citing works
Llewellyn, G. N., Grover, J. R., Olety, B., & Ono, A. (2013) · Journal of Virology · doi:10.1128/jvi.00040-13 · Cited by 56 · see citing works
Analysis of the human immunodeficiency virus-1 RNA packageome
Eckwahl, M. J., Arnion, H., Kharytonchyk, S., Zang, T., Bieniasz, P. D., Telesnitsky, A., & Wolin, S. L. (2016) · RNA · doi:10.1261/rna.057299.116 · Cited by 57 · see citing works
The capsid protein of human immunodeficiency virus: intersubunit interactions during virus assembly
Mateu, M. G. (2009) · FEBS Journal · doi:10.1111/j.1742-4658.2009.07313.x · Cited by 56 · see citing works
Role of Murine Leukemia Virus Nucleocapsid Protein in Virus Assembly
Muriaux, D. M., Costes, S. V., Nagashima, K., Mirro, J., Cho, E. H., Lockett, S., & Rein, A. R. (2004) · Journal of Virology · doi:10.1128/jvi.78.22.12378-12385.2004 · Cited by 56 · see citing works
Self-citationAssembly of Human Immunodeficiency Virus Precursor Gag Proteins
Huseby, D. L., Barklis, R. L., Alfadhli, A., & Barklis, E. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m412325200 · Cited by 56 · see citing works
Ghanam, R. H., Samal, A. B., Fernandez, T. F., & Saad, J. S. (2012) · Frontiers in Microbiology · doi:10.3389/fmicb.2012.00055 · Cited by 55 · see citing works
Wang, S.-W., & Aldovini, A. (2002) · Journal of Virology · doi:10.1128/jvi.76.23.11853-11865.2002 · Cited by 55 · see citing works
Guo, F., Saadatmand, J., Niu, M., & Kleiman, L. (2009) · Journal of Virology · doi:10.1128/jvi.00488-09 · Cited by 54 · see citing works
Dooher, J. E., & Lingappa, J. R. (2004) · Journal of Virology · doi:10.1128/jvi.78.4.1645-1656.2004 · Cited by 54 · see citing works
Characterization of the In Vitro HIV-1 Capsid Assembly Pathway
Barklis, E., Alfadhli, A., McQuaw, C. M., Yalamuri, S. M., Still, A., Barklis, R. L., Kukull, B., & López, C. S. (2009) · Journal of Molecular Biology · doi:10.1016/j.jmb.2009.01.058 · Cited by 53 · see citing works
Guo, X., Roldán, A., Hu, J., Wainberg, M. A., & Liang, C. (2005) · Journal of Virology · doi:10.1128/jvi.79.3.1803-1812.2005 · Cited by 53 · see citing works
Jiang, J., Ablan, S. D., Derebail, S. S., Hercík, K., Soheilian, F., Thomas, J. A., Tang, S., HEWLETT, I. K., Nagashima, K., Gorelick, R. J., et al. (2011) · Virology · doi:10.1016/j.virol.2011.09.012 · Cited by 52 · see citing works
- Authors
- Campbell, S., & Rein, A.
- Affiliations
- Frederick National Laboratory for Cancer Research (US)
- ORCID
- Rein, Alan
- Venue
- Journal of Virology
- Publisher
- American Society for Microbiology
- Published
- 1999-03
- Volume
- 73
- Issue
- 3
- Pages
- 2270-2279
- ISSN
- 0022-538X (ISSN-L)
- 1098-5514
- PMC
- PMC104472
- OpenAlex
- W2141194382
- Cited by
- 293
- References
- 59
- Citations by year
- 2026: 5 · 2025: 2 · 2024: 8 · 2023: 3 · 2022: 8 · 2021: 9 · 2020: 5 · 2019: 10 · 2018: 12 · 2017: 15 · 2016: 14 · 2015: 6 · 2014: 13 · 2013: 12 · 2012: 18
- FWCI
- 3.95
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Virology (publishedVersion)
- PubMed Central (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed (publishedVersion)
- Funders
- U.S. Department of Health and Human Services
- National Cancer Institute
- 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
- HIV-1 Gag protein, viral assembly, virus-like particles, spherical particles, Gag multimerization, protein-protein interaction
- MeSH terms
- Escherichia coli, Microscopy, Electron, Recombinant Proteins, Ribonucleases, RNA, Viral, Sodium Chloride, HIV-1, Gene Products, gag, Virus Assembly
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.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review