Requirement for an Intact T-Cell Actin and Tubulin Cytoskeleton for Efficient Assembly and Spread of Human Immunodeficiency Virus Type 1
Open accessAbstract
Human immunodeficiency virus type 1 (HIV-1) infection of CD4 + T cells leads to the production of new virions that assemble at the plasma membrane. Gag and Env accumulate in the context of lipid rafts at the inner and outer leaflets of the plasma membrane, respectively, forming polarized domains from which HIV-1 buds. HIV-1 budding can result in either release of cell-free virions or direct cell-cell spread via a virological synapse (VS). The recruitment of Gag and Env to these plasma membrane caps in T cells is poorly understood but may require elements of the T-cell secretory apparatus coordinated by the cytoskeleton. Using fixed-cell immunofluorescence labeling and confocal microscopy, we observed a high percentage of HIV-1-infected T cells with polarized Env and Gag in capped, lipid raft-like assembly domains. Treatment of infected T cells with inhibitors of actin or tubulin remodeling disrupted Gag and Env compartmentalization within the polarized raft-like domains. Depolymerization of the actin cytoskeleton reduced Gag release and viral infectivity, and actin and tubulin inhibitors reduced Env incorporation into virions. Live- and fixed-cell confocal imaging and assay of de novo DNA synthesis by real-time PCR allowed quantification of HIV-1 cell-cell transfer. Inhibition of actin and tubulin remodeling in infected cells interfered with cell-cell spread across a VS and reduced new viral DNA synthesis. Based on these data, we propose that HIV-1 requires both actin and tubulin components of the T-cell cytoskeleton to direct its assembly and budding and to elaborate a functional VS.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
MTOC polarization facilitates actin- and tubulin-dependent accumulation of Gag, Env, and viral RNA in the intercellular contact zone.
“MTOC polarization facilitates the actin- and tubulin-dependent accumulation of Gag, Env, and viral RNA in the intercellular contact zone [34,39].”
From HIV-1 and HTLV-1 Transmission Modes: Mechanisms and Importance for Virus Spread (2022) · cites this paper as [39]
Cites
Conserved microtubule–actin interactions in cell movement and morphogenesis
Rodriguez, O. C., Schaefer, A. W., Mandato, C. A., Forscher, P., Bement, W. M., & Waterman-Storer, C. M. (2003) · Nature Cell Biology · doi:10.1038/ncb0703-599 · Cited by 844 · see citing works
Visualization of the intracellular behavior of HIV in living cells
McDonald, D. J., Vodicka, M. A., Lucero, G. R., Svitkina, T., Borisy, G. G., Emerman, M., & Hope, T. J. (2002) · The Journal of Cell Biology · doi:10.1083/jcb.200203150 · Cited by 800 · see citing works
Nguyen, D., & Hildreth, J. E. K. (2000) · Journal of Virology · doi:10.1128/jvi.74.7.3264-3272.2000 · Cited by 788 · see citing works
Spread of HTLV-I Between Lymphocytes by Virus-Induced Polarization of the Cytoskeleton
Igakura, T., Stinchcombe, J. C., Goon, P. K. C., Taylor, G. P., Weber, J. N., Griffiths, G. M., Tanaka, Y., Osame, M., & Bangham, C. R. M. (2003) · Science · doi:10.1126/science.1080115 · Cited by 755 · see citing works
Plasma membrane rafts play a critical role in HIV-1 assembly and release
Ono, A., & Freed, E. O. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.241320298 · Cited by 705 · see citing works
HIV-1 Cell to Cell Transfer across an Env-induced, Actin-dependent Synapse
Jolly, C., Kashefi, K., Hollinshead, M., & Sattentau, Q. J. (2004) · The Journal of Experimental Medicine · doi:10.1084/jem.20030648 · Cited by 623 · see citing works
Self-citationMorita, E., & Sundquist, W. I. (2004) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.20.010403.102350 · Cited by 574 · see citing works
Exosomes and HIV Gag bud from endosome-like domains of the T cell plasma membrane
Booth, A. M., Fang, Y., Fallon, J. K., Yang, J.-M., Hildreth, J. E. K., & Gould, S. J. (2006) · The Journal of Cell Biology · doi:10.1083/jcb.200508014 · Cited by 562 · see citing works
Phosphatidylinositol (4,5) bisphosphate regulates HIV-1 Gag targeting to the plasma membrane
Ono, A., Ablan, S. D., Lockett, S. J., Nagashima, K., & Freed, E. O. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0405596101 · Cited by 553 · see citing works
Infectious HIV-1 assembles in late endosomes in primary macrophages
Pelchen–Matthews, A., Kramer, B., & Marsh, M. (2003) · The Journal of Cell Biology · doi:10.1083/jcb.200304008 · Cited by 491 · see citing works
Functional cooperation between the microtubule and actin cytoskeletons
Goode, B. L., Drubin, D. G., & Barnes, G. (2000) · Current Opinion in Cell Biology · doi:10.1016/s0955-0674(99)00058-7 · Cited by 475 · see citing works
A Superhighway to Virus Infection
Greber, U. F., & Way, M. (2006) · Cell · doi:10.1016/j.cell.2006.02.018 · Cited by 382 · see citing works
Role of the cytoskeleton during leukocyte responses
Vicente‐Manzanares, M., & Sánchez‐Madrid, F. (2004) · Nature reviews. Immunology · doi:10.1038/nri1268 · Cited by 360 · see citing works
Actin-based motility of intracellular pathogens
Gouin, E., Welch, M. D., & Cossart, P. (2005) · Current Opinion in Microbiology · doi:10.1016/j.mib.2004.12.013 · Cited by 358 · see citing works
Evidence That HIV Budding in Primary Macrophages Occurs through the Exosome Release Pathway
Nguyen, D. G., Booth, A. M., Gould, S. J., & Hildreth, J. E. K. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m309009200 · Cited by 337 · see citing works
Microbial pathogenesis and cytoskeletal function
Gruenheid, S., & Finlay, B. B. (2003) · Nature · doi:10.1038/nature01603 · Cited by 296 · see citing works
Charting HIV's remarkable voyage through the cell: Basic science as a passport to future therapy
Greene, W. C., & Peterlin, B. M. (2002) · Nature Medicine · doi:10.1038/nm0702-673 · Cited by 293 · see citing works
Bukrinskaya, A. G., Břicháček, B., Mann, A. M., & Stevenson, M. (1998) · The Journal of Experimental Medicine · doi:10.1084/jem.188.11.2113 · Cited by 280 · see citing works
Ono, A., & Freed, E. O. (2004) · Journal of Virology · doi:10.1128/jvi.78.3.1552-1563.2004 · Cited by 275 · see citing works
The immune control and cell-to-cell spread of human T-lymphotropic virus type 1
Bangham, C. R. M. (2003) · Journal of General Virology · doi:10.1099/vir.0.19334-0 · Cited by 266 · see citing works
Mapping of tetraspanin-enriched microdomains that can function as gateways for HIV-1
Nydegger, S., Khurana, S., Krementsov, D. N., Foti, M., & Thali, M. (2006) · The Journal of Cell Biology · doi:10.1083/jcb.200508165 · Cited by 257 · see citing works
Directed Egress of Animal Viruses Promotes Cell-to-Cell Spread
Johnson, D. C., & Huber, M. T. (2002) · Journal of Virology · doi:10.1128/jvi.76.1.1-8.2002 · Cited by 255 · see citing works
AP-3 Directs the Intracellular Trafficking of HIV-1 Gag and Plays a Key Role in Particle Assembly
Dong, X., Li, H., Derdowski, A., Ding, L., Burnett, A. S., Chen, X., Peters, T. R., Dermody, T. S., Woodruff, E. A., Wang, J.-J., et al. (2005) · Cell · doi:10.1016/j.cell.2004.12.023 · Cited by 245 · see citing works
Lindwasser, O. W., & Resh, M. D. (2001) · Journal of Virology · doi:10.1128/jvi.75.17.7913-7924.2001 · Cited by 244 · see citing works
Retroviral spread by induction of virological synapses
Jolly, C., & Sattentau, Q. J. (2004) · Traffic · doi:10.1111/j.1600-0854.2004.00209.x · Cited by 240 · see citing works
Self-citationDangerous liaisons at the virological synapse
Piguet, V., & Sattentau, Q. J. (2004) · Journal of Clinical Investigation · doi:10.1172/jci22812 · Cited by 220 · see citing works
Self-citationHealey, D. G., Dianda, L., Moore, J. P., McDougal, J. S., Moore, M. J., Estess, P., Buck, D., Kwong, P. D., Beverley, P. C. L., & Sattentau, Q. J. (1990) · The Journal of Experimental Medicine · doi:10.1084/jem.172.4.1233 · Cited by 212 · see citing works
Self-citationBöge, M., Wyss, S., Bonifacino, J., & Thali, M. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.25.15773 · Cited by 210 · see citing works
Iyengar, S., Hildreth, J. E. K., & Schwartz, D. H. (1998) · Journal of Virology · doi:10.1128/jvi.72.6.5251-5255.1998 · Cited by 203 · see citing works
Surfing pathogens and the lessons learned for actin polymerization
Frischknecht, F. (2001) · Trends in Cell Biology · doi:10.1016/s0962-8924(00)01871-7 · Cited by 197 · see citing works
HDAC6 Deacetylase Activity Links the Tubulin Cytoskeleton with Immune Synapse Organization
Serrador, J. M., Cabrero, J. R., Sancho, D., Mittelbrunn, M., Urzainqui, A., & Sánchez‐Madrid, F. (2004) · Immunity · doi:10.1016/s1074-7613(04)00078-0 · Cited by 193 · see citing works
Palmitoylation of the HIV-1 envelope glycoprotein is critical for viral infectivity
Rousso, I. Y., Mixon, M. B., Chen, B. K., & Kim, P. S. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.240459697 · Cited by 189 · see citing works
HIV‐1 Egress is Gated Through Late Endosomal Membranes
Nydegger, S., Foti, M., Derdowski, A., Spearman, P. W., & Thali, M. (2003) · Traffic · doi:10.1046/j.1600-0854.2003.00145.x · Cited by 185 · see citing works
Cortical control of microtubule stability and polarization
Gundersen, G. G., Gomes, E. R., & Wen, Y. (2003) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2003.11.010 · Cited by 179 · see citing works
The role of cell-to-cell transmission in HIV infection
Phillips, D. M. (1994) · AIDS · doi:10.1097/00002030-199406000-00001 · Cited by 172 · see citing works
Identification of an Intracellular Trafficking and Assembly Pathway for HIV‐1 Gag
Perlman, M., & Resh, M. D. (2006) · Traffic · doi:10.1111/j.1398-9219.2006.00428.x · Cited by 160 · see citing works
Assembly of Infectious HIV-1 in Human Epithelial and T-Lymphoblastic Cell Lines
Grigorov, B., Arcanger, F., Roingeard, P., Darlix, J., & Muriaux, D. M. (2006) · Journal of Molecular Biology · doi:10.1016/j.jmb.2006.04.017 · Cited by 154 · see citing works
Golub, T., & Caroni, P. (2005) · The Journal of Cell Biology · doi:10.1083/jcb.200407058 · Cited by 154 · see citing works
Wyss, S., Berlioz‐Torrent, C., Boge, M., Blot, G., Höning, S., Bénarous, R., & Thali, M. (2001) · Journal of Virology · doi:10.1128/jvi.75.6.2982-2992.2001 · Cited by 149 · see citing works
Interaction 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
Jolly, C. L., & Sattentau, Q. J. (2005) · Journal of Virology · doi:10.1128/jvi.79.18.12088-12094.2005 · Cited by 140 · see citing works
Self-citationRole of the cytoskeleton in cell-to-cell transmission of human immunodeficiency virus
Pearce-Pratt, R., Malamud, D., & Phillips, D. M. (1994) · Journal of Virology · doi:10.1128/jvi.68.5.2898-2905.1994 · Cited by 137 · see citing works
Holm, K., Weclewicz, K., Hewson, R., & Suomalainen, M. (2003) · Journal of Virology · doi:10.1128/jvi.77.8.4805-4817.2003 · Cited by 132 · see citing works
Sasaki, H., Nakamura, M., Ohno, T., Matsuda, Y., Yuda, Y., & Nonomura, Y. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.6.2026 · Cited by 128 · see citing works
HIV-1 Gag Protein Associates with F-actin Present in Microfilaments
Rey, O., Canon, J. R., & Krogstad, P. A. (1996) · Virology · doi:10.1006/viro.1996.0343 · Cited by 115 · see citing works
Barnard, A. L., Igakura, T., Tanaka, Y., Taylor, G. P., & Bangham, C. R. M. (2005) · Blood · doi:10.1182/blood-2004-07-2850 · Cited by 114 · see citing works
Deschambeault, J., Lalonde, J.-P., Cervantes-Acosta, G., Lodge, R., Cohen, É. A., & Lemay, G. (1999) · Journal of Virology · doi:10.1128/jvi.73.6.5010-5017.1999 · Cited by 111 · see citing works
The secretory synapse: the secrets of a serial killer
Bossi, G., Trambas, C., Booth, S., Clark, R., Stinchcombe, J. C., & Griffiths, G. M. (2002) · Immunological Reviews · doi:10.1034/j.1600-065x.2002.18913.x · Cited by 105 · see citing works
Actin Associates with the Nucleocapsid Domain of the Human Immunodeficiency Virus Gag Polyprotein
Wilk, T., Gowen, B. E., & Fuller, S. D. (1999) · Journal of Virology · doi:10.1128/jvi.73.3.1931-1940.1999 · Cited by 104 · see citing works
Fais, S., Capobianchi, M. R., Abbate, I., Castilletti, C., Gentile, M., Fei, P. C., Ameglio, F., & DIANZANI, F. (1995) · AIDS · doi:10.1097/00002030-199504000-00003 · Cited by 97 · see citing works
Bhattacharya, J., Peters, P. J., & Clapham, P. R. (2004) · Journal of Virology · doi:10.1128/jvi.78.10.5500-5506.2004 · Cited by 94 · see citing works
HIV interaction with endosomes in macrophages and dendritic cells
Kramer, B., Pelchen–Matthews, A., Deneka, M., Garcia, E., Piguet, V., & Marsh, M. (2005) · Blood Cells Molecules and Diseases · doi:10.1016/j.bcmd.2005.06.006 · Cited by 88 · see citing works
Roles of the cytoskeleton and motor proteins in endocytic sorting
Murray, J. W., & Wolkoff, A. W. (2003) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2003.07.008 · Cited by 86 · see citing works
Resh, M. D. (2005) · PubMed · Cited by 83 · see citing works
Sancho, D., Vicente‐Manzanares, M., Mittelbrunn, M., Montoya, M. C., Gordón‐Alonso, M., Serrador, J. M., & Sánchez‐Madrid, F. (2002) · Immunological Reviews · doi:10.1034/j.1600-065x.2002.18908.x · Cited by 78 · see citing works
Cytoskeletal remodeling in lymphocyte activation
Miletic, A. V., Swat, M., Fujikawa, K., & Swat, W. (2003) · Current Opinion in Immunology · doi:10.1016/s0952-7915(03)00054-2 · Cited by 71 · see citing works
Rodgers, W., & Zavzavadjian, J. R. (2001) · Experimental Cell Research · doi:10.1006/excr.2001.5253 · Cited by 70 · see citing works
Control of lymphocyte shape and the chemotactic response by the GTP exchange factor Vav
Vicente‐Manzanares, M., Cruz‐Adalia, A., Martin-Cofreces, N. B., Cabrero, J. R., Dosil, M., Alvarado‐Sánchez, B., Bustelo, X. R., & Sánchez‐Madrid, F. (2004) · Blood · doi:10.1182/blood-2004-07-2925 · 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
Sevrioukov, E. A., Moghrabi, N., Kuhn, M., & Krämer, H. (2005) · Molecular Biology of the Cell · doi:10.1091/mbc.e04-11-1013 · Cited by 51 · see citing works
Vandecandelaere, A., Martin, S. R., & Engelborghs, Y. (1997) · Biochemical Journal · doi:10.1042/bj3230189 · Cited by 50 · see citing works
Chan, W.-E., Lin, H.-H., & Chen, S. S.-L. (2005) · Journal of Virology · doi:10.1128/jvi.79.13.8374-8387.2005 · Cited by 44 · see citing works
Lipid rafts and regulation of the cytoskeleton during T cell activation
Meiri, K. F. (2005) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2005.1704 · Cited by 39 · see citing works
HIV Type 1 Gag and Nucleocapsid Proteins: Cytoskeletal Localization and Effects on Cell Motility
Ibarrondo, F. J., Choi, R., Geng, Y., Canon, J. R., Rey, O., Baldwin, G. C., & Krogstad, P. A. (2001) · AIDS Research and Human Retroviruses · doi:10.1089/08892220152644197 · Cited by 34 · see citing works
Actin filaments play an essential role for transport of nascent HIV-1 proteins in host cells
Sasaki, H., Ozaki, H., Karaki, H., & Nonomura, Y. (2004) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2004.02.088 · Cited by 27 · see citing works
Marsh, M., & Thali, M. (2003) · Nature Medicine · doi:10.1038/nm1003-1262 · Cited by 23 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Avoiding the void: Cell-to-cell spread of human viruses
Sattentau, Q. (2008) · Nature Reviews Microbiology · doi:10.1038/nrmicro1972 · Cited by 614 · see citing works
Self-citationQuantitative 3D Video Microscopy of HIV Transfer Across T Cell Virological Synapses
Hübner, W., McNerney, G. P., Chen, P., Dale, B. M., Gordon, R. E., Chuang, F. Y. S., Li, X.-D., Asmuth, D. M., Huser, T., & Chen, B. K. (2009) · Science · doi:10.1126/science.1167525 · Cited by 486 · see citing works
HIV-1 Envelope Glycoprotein Biosynthesis, Trafficking, and Incorporation
Checkley, M. A., Luttge, B. G., & Freed, E. O. (2011) · Journal of Molecular Biology · doi:10.1016/j.jmb.2011.04.042 · Cited by 477 · see citing works
Subversion of the actin cytoskeleton during viral infection
Taylor, M. P., Koyuncu, O. O., & Enquist, L. (2011) · Nature Reviews Microbiology · doi:10.1038/nrmicro2574 · Cited by 413 · see citing works
Efficient HIV-1 transmission from macrophages to T cells across transient virological synapses
Groot, F., Welsch, S., & Sattentau, Q. J. (2008) · Blood · doi:10.1182/blood-2007-12-130070 · Cited by 252 · see citing works
Self-citationRudnicka, D., Feldmann, J., Porrot, F., Wietgrefe, S., Guadagnini, S., Prévost, M.-C., Estaquier, J., Haase, A. T., Sol-Foulon, N., & Schwartz, O. (2009) · Journal of Virology · doi:10.1128/jvi.00282-09 · Cited by 229 · see citing works
Mazurov, D., Ilinskaya, A., Heidecker, G., Lloyd, P., & Derse, D. (2010) · PLoS Pathogens · doi:10.1371/journal.ppat.1000788 · Cited by 217 · see citing works
Martin, N., Welsch, S., Jolly, C., Briggs, J. A. G., Vaux, D., & Sattentau, Q. J. (2010) · Journal of Virology · doi:10.1128/jvi.02651-09 · Cited by 199 · see citing works
Self-citationJolly, C. L., & Sattentau, Q. J. (2007) · Journal of Virology · doi:10.1128/jvi.01845-06 · Cited by 199 · see citing works
Self-citationMechanisms for Cell-to-Cell Transmission of HIV-1
Bracq, L., Xie, M., Bénichou, S., & Bouchet, J. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.00260 · Cited by 192 · see citing works
Yu, H. J., Reuter, M. A., & McDonald, D. (2008) · PLoS Pathogens · doi:10.1371/journal.ppat.1000134 · Cited by 193 · see citing works
3D visualization of HIV transfer at the virological synapse between dendritic cells and T cells
Felts, R. L., Narayan, K., Estes, J. D., Shi, D., Trubey, C. M., Fu, J., Hartnell, L. M., Ruthel, G. T., Schneider, D. K., Nagashima, K., et al. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1003040107 · Cited by 184 · see citing works
Jolly, C. L., Booth, N. J., & Neil, S. J. D. (2010) · Journal of Virology · doi:10.1128/jvi.01447-10 · Cited by 184 · see citing works
Self-citationHuman Herpesvirus‐6 Induces MVB Formation, and Virus Egress Occurs by an Exosomal Release Pathway
Mori, Y., Koike, M., Moriishi, E., Kawabata, A., Tang, H., Oyaizu, H., Uchiyama, Y., & Yamanishi, K. (2008) · Traffic · doi:10.1111/j.1600-0854.2008.00796.x · Cited by 182 · see citing works
Jolly, C., Mitar, I., & Sattentau, Q. J. (2007) · Journal of Virology · doi:10.1128/jvi.01585-07 · Cited by 178 · see citing works
Self-citationNucleocapsid 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
Cellular proteins detected in HIV‐1
Ott, D. E. (2008) · Reviews in Medical Virology · doi:10.1002/rmv.570 · Cited by 141 · see citing works
Cell-to-cell HIV-1 spread and its implications for immune evasion
Martin, N., & Sattentau, Q. (2009) · Current Opinion in HIV and AIDS · doi:10.1097/coh.0b013e328322f94a · Cited by 143 · see citing works
Self-citationDale, B. M., McNerney, G. P., Thompson, D. L., Hubner, W., de los Reyes, K., Chuang, F. Y. S., Huser, T., & Chen, B. K. (2011) · Cell Host & Microbe · doi:10.1016/j.chom.2011.10.015 · Cited by 133 · see citing works
Cell-to-Cell Spread of Retroviruses
Sattentau, Q. J. (2010) · Viruses · doi:10.3390/v2061306 · Cited by 128 · see citing works
Self-citationHIV-1 Induced Bystander Apoptosis
Garg, H., Mohl, J. E., & Joshi, A. (2012) · Viruses · doi:10.3390/v4113020 · Cited by 126 · see citing works
Barrero-Villar, M., Cabrero, J. R., Gordón‐Alonso, M., González, J. B., Álvarez, S., Muñoz‐Fernández, M. Á., Sánchez‐Madrid, F., & Valenzuela-Fernández, A. (2008) · Journal of Cell Science · doi:10.1242/jcs.035873 · Cited by 121 · see citing works
Relationships between plasma membrane microdomains and HIV‐1 assembly
Ono, A. (2010) · Biology of the Cell · doi:10.1042/bc20090165 · Cited by 115 · see citing works
Hiv-1 Assembly at the Plasma Membrane: Gag Trafficking and Localization
Ono, A. (2009) · Future Virology · doi:10.2217/fvl.09.4 · Cited by 108 · see citing works
Vorster, P., Guo, J., Yoder, A. C., Wang, W., Zheng, Y.-F., Xu, X.-H., Yu, D., Spear, M., & Wu, Y.-T. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.182238 · Cited by 97 · see citing works
HIV-1 Nef Inhibits Ruffles, Induces Filopodia, and Modulates Migration of Infected Lymphocytes
Nobile, C., Rudnicka, D., Hasan, M., Aulner, N., Porrot, F., Machu, C., Renaud, O., Prévost, M., Hivroz, C., Schwartz, O., et al. (2009) · Journal of Virology · doi:10.1128/jvi.02230-09 · Cited by 100 · see citing works
New Insights into HIV Assembly and Trafficking
Balasubramaniam, M., & Freed, E. O. (2011) · Physiology · doi:10.1152/physiol.00051.2010 · Cited by 96 · see citing works
Tetherin restricts direct cell-to-cell infection of HIV-1
Kuhl, B. D., Sloan, R. D., Donahue, D. A., Bar-Magen, T., Liang, C., & Wainberg, M. A. (2010) · Retrovirology · doi:10.1186/1742-4690-7-115 · Cited by 95 · see citing works
Weng, J., Krementsov, D. N., Khurana, S., Roy, N. H., & Thali, M. (2009) · Journal of Virology · doi:10.1128/jvi.00163-09 · Cited by 89 · 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
Prohibitin plays a critical role in Enterovirus 71 neuropathogenesis
Too, I. H. K., Bonne, I., Tan, E. L., Chu, J. J. H., & Alonso, S. (2018) · PLoS Pathogens · doi:10.1371/journal.ppat.1006778 · Cited by 84 · see citing works
Vasiliver-Shamis, G., Cho, M. W., Hioe, C. E., & Dustin, M. L. (2009) · Journal of Virology · doi:10.1128/jvi.01440-09 · Cited by 84 · see citing works
Virus-producing cells determine the host protein profiles of HIV-1 virion cores
Santos, S., Obukhov, Y., Nekhai, S. A., Bukrinsky, M., & Iordanskiy, S. (2012) · Retrovirology · doi:10.1186/1742-4690-9-65 · Cited by 78 · see citing works
Immunological synapse: structures, molecular mechanisms and therapeutic implications in disease
Chao, Z., Mei, Q., Yang, C., Luo, J., Liu, P., Peng, H., Guo, X., Yin, Z., Li, L., & Wang, Z. (2025) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-025-02332-6 · Cited by 81 · see citing works
Jolly, C. L., Welsch, S., Michor, S., & Sattentau, Q. J. (2011) · PLoS Pathogens · doi:10.1371/journal.ppat.1002226 · Cited by 76 · see citing works
Self-citationLive cell imaging of the HIV-1 life cycle
Campbell, E. M., & Hope, T. J. (2008) · Trends in Microbiology · doi:10.1016/j.tim.2008.09.006 · Cited by 74 · see citing works
Selective targeting of ITK blocks multiple steps of HIV replication
Readinger, J. A., Schiralli, G. M., Jiang, J.-K., Thomas, C., August, A., Henderson, A., & Schwartzberg, P. (2008) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.0709659105 · Cited by 75 · see citing works
Protease inhibitors effectively block cell-to-cell spread of HIV-1 between T cells
Titanji, B. K., Aasa-Chapman, M. M. I., Pillay, D., & Jolly, C. L. (2013) · Retrovirology · doi:10.1186/1742-4690-10-161 · Cited by 73 · see citing works
Self-citationThe direct passage of animal viruses between cells
Sattentau, Q. J. (2011) · Current Opinion in Virology · doi:10.1016/j.coviro.2011.09.004 · Cited by 71 · see citing works
Self-citationAll-Round Manipulation of the Actin Cytoskeleton by HIV
Stella, A. O., & Turville, S. G. (2018) · Viruses · doi:10.3390/v10020063 · Cited by 70 · see citing works
HIV-1 cell-to-cell transmission and broadly neutralizing antibodies
Dufloo, J., Bruel, T., & Schwartz, O. (2018) · Retrovirology · doi:10.1186/s12977-018-0434-1 · Cited by 69 · see citing works
HIV-1 and HTLV-1 Transmission Modes: Mechanisms and Importance for Virus Spread
Kalinichenko, S., Komkov, D., & Mazurov, D. (2022) · Viruses · doi:10.3390/v14010152 · Cited by 68 · see citing works
“MTOC polarization facilitates the actin- and tubulin-dependent accumulation of Gag, Env, and viral RNA in the intercellular contact zone [34,39].”
BackgroundUse of HIV as a gene transfer vector.
Pluta, K. D., & Kacprzak, M. M. (2009) · Acta Biochimica Polonica · doi:10.18388/abp.2009_2490 · Cited by 68 · see citing works
Meshri, S. E. E., Dujardin, D., Godet, J., Richert, L., Boudier, C., Darlix, J. L., Didier, P., Mély, Y., & de ROCQUIGNY, H. (2015) · Journal of Molecular Biology · doi:10.1016/j.jmb.2015.01.015 · Cited by 67 · see citing works
Sato, K., Misawa, N., Fukuhara, M., Iwami, S., An, D. S., Ito, M., & Koyanagi, Y. (2012) · Journal of Virology · doi:10.1128/jvi.07062-11 · Cited by 67 · see citing works
Virus assembly and plasma membrane domains: Which came first?
Kerviel, A., Thomas, A., Chaloin, L., Favard, C., & Muriaux, D. M. (2012) · Virus Research · doi:10.1016/j.virusres.2012.08.014 · Cited by 64 · see citing works
Optimized methods for imaging membrane nanotubes between T cells and trafficking of HIV-1
Sowinski, S., Alakoskela, J.-M. I., Jolly, C. L., & Davis, D. M. (2010) · Methods · doi:10.1016/j.ymeth.2010.04.002 · Cited by 65 · see citing works
Self-citationVasiliver-Shamis, G., Tuen, M., Wu, T. W., Starr, T., Cameron, T. O., Thomson, R. P., Kaur, G., Liu, J., Visciano, M. L., Li, H., et al. (2008) · Journal of Virology · doi:10.1128/jvi.00835-08 · Cited by 62 · see citing works
Role of HIV Gp41 mediated fusion/hemifusion in bystander apoptosis
Garg, H., & Blumenthal, R. P. (2008) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-008-8147-6 · Cited by 61 · see citing works
Mechanisms of enhanced HIV spread through T‐cell virological synapses
Dale, B. M., Alvarez, R. A., & Chen, B. K. (2012) · Immunological Reviews · doi:10.1111/imr.12022 · Cited by 60 · see citing works
Three-Dimensional Imaging of Viral Infections
Risco, C., de Castro, I. F., Sanz-Sánchez, L., Narayan, K., Grandinetti, G., & Subramaniam, S. (2014) · Annual Review of Virology · doi:10.1146/annurev-virology-031413-085351 · Cited by 60 · see citing works
Productive Entry of HIV-1 during Cell-to-Cell Transmission via Dynamin-Dependent Endocytosis
Sloan, R. D., Kuhl, B. D., Mésplède, T., Münch, J., Donahue, D. A., & Wainberg, M. A. (2013) · Journal of Virology · doi:10.1128/jvi.00815-13 · Cited by 57 · see citing works
The non-canonical roles of clathrin and actin in pathogen internalization, egress and spread
Humphries, A. C., & Way, M. (2013) · Nature Reviews Microbiology · doi:10.1038/nrmicro3072 · Cited by 53 · see citing works
Proteome analysis of the HIV-1 Gag interactome
Engeland, C. E., Brown, N. P., Börner, K., Schümann, M., Krause, E., Kaderali, L., Müller, G. A., & Kräusslich, H.-G. (2014) · Virology · doi:10.1016/j.virol.2014.04.038 · Cited by 55 · see citing works
Multiple proviral integration events after virological synapse-mediated HIV-1 spread
Russell, R. A., Martin, N., Mitar, I., Jones, E., & Sattentau, Q. J. (2013) · Virology · doi:10.1016/j.virol.2013.05.005 · Cited by 54 · see citing works
Self-citationROCK1 and LIM Kinase Modulate Retrovirus Particle Release and Cell-Cell Transmission Events
Wen, X., Ding, L., Wang, J.-J., Qi, M., Hammonds, J. E., Chu, H., Chen, X., Hunter, E., & Spearman, P. W. (2014) · Journal of Virology · doi:10.1128/jvi.00023-14 · Cited by 54 · see citing works
Analysis of HIV-1 Gag Protein Interactions via Biotin Ligase Tagging
Ritchie, C., Cylinder, I., Platt, E. J., & Barklis, E. (2015) · Journal of Virology · doi:10.1128/jvi.03584-14 · Cited by 54 · see citing works
Milev, M. P., Brown, C. M., & Mouland, A. J. (2010) · Retrovirology · doi:10.1186/1742-4690-7-41 · Cited by 52 · see citing works
Biology of HIV Mucosal Transmission
Wu, L. (2008) · Current Opinion in HIV and AIDS · doi:10.1097/coh.0b013e32830634c6 · Cited by 54 · see citing works
Critical role for the kinesin KIF3A in the HIV life cycle in primary human macrophages
Gaudin, R., de Alencar, B. C., Jouve, M., Berré, S., Bouder, E. L., Schindler, M., Varthaman, A., Gobert, F.-X., & Benaroch, P. (2012) · Journal of Cell Biology · doi:10.1083/jcb.201201144 · Cited by 42 · see citing works
Actin filaments disruption and stabilization affect measles virus maturation by different mechanisms
Dietzel, E., Kolesnikova, L., & Maisner, A. (2013) · Virology Journal · doi:10.1186/1743-422x-10-249 · Cited by 50 · see citing works
Colpitts, T. M., Cox, J., Nguyen, A., Feitosa-Suntheimer, F., Krishnan, M. N., & Fikrig, E. (2011) · Virology · doi:10.1016/j.virol.2011.06.002 · Cited by 48 · see citing works
Wang, J., Wells, C. W., & Wu, L. J. (2008) · Virology · doi:10.1016/j.virol.2008.08.028 · Cited by 48 · see citing works
How HIV-1 Takes Advantage of the Cytoskeleton during Replication and Cell-to-Cell Transmission
Lehmann, M., Nikolic, D. S., & Piguet, V. (2011) · Viruses · doi:10.3390/v3091757 · Cited by 48 · see citing works
Membrane dynamics associated with viral infection
de Armas-Rillo, L., Valera, M.-S., Marrero-Hernández, S., & Valenzuela-Fernández, A. (2016) · Reviews in Medical Virology · doi:10.1002/rmv.1872 · Cited by 44 · see citing works
Post-translational Modification-Based Regulation of HIV Replication
Chen, L., Keppler, O. T., & Scholz, C. W. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.02131 · Cited by 46 · see citing works
The trinity of the cortical actin in the initiation of HIV-1 infection
Spear, M., Guo, J., & Wu, Y.-T. (2012) · Retrovirology · doi:10.1186/1742-4690-9-45 · Cited by 49 · see citing works
Macrophages and Cell-Cell Spread of HIV-1
Waki, K., & Freed, E. O. (2010) · Viruses · doi:10.3390/v2081603 · Cited by 47 · see citing works
Rodriguez-Plata, M. T., Puigdomènech, I., Izquierdo-Useros, N., Puertas, M. C., Carrillo, J., Erkizia, I., Clotet, B., Blanco, J., & Martinez-Picado, J. (2013) · Retrovirology · doi:10.1186/1742-4690-10-42 · Cited by 45 · see citing works
Davé, R. H., Saengsawang, W., Yu, J.-Z., Donati, R. J., & Rasenick, M. M. (2009) · Neurosignals · doi:10.1159/000186693 · Cited by 45 · see citing works
HIV-1 at the immunological and T-lymphocytic virological synapse
Haller, C., & Fackler, O. (2008) · Biological Chemistry · doi:10.1515/bc.2008.143 · Cited by 45 · see citing works
Thomas, A., Floderer, C., López‐Huertas, M. R., Gros, N., Hamard-Péron, É., Favard, C., Ohlmann, T., Alcamı́, J., & Muriaux, D. M. (2015) · Journal of Virology · doi:10.1128/jvi.00469-15 · Cited by 44 · see citing works
Pongsomboon, S., Tang, S., Boonda, S., Aoki, T., Hırono, I., & Tassanakajon, A. (2010) · Fish & Shellfish Immunology · doi:10.1016/j.fsi.2010.10.015 · Cited by 44 · see citing works
Wang, L., Eng, E. T., Law, K., Gordon, R. E., Rice, W. J., & Chen, B. K. (2016) · Journal of Virology · doi:10.1128/jvi.01605-16 · Cited by 44 · see citing works
Targets for Inhibition of HIV Replication: Entry, Enzyme Action, Release and Maturation
Sierra, S., & Walter, H. (2012) · Intervirology · doi:10.1159/000331995 · Cited by 43 · see citing works
Spear, M., Guo, J., Turner, A., Yu, D., Wang, W., Meltzer, B., He, S., Hu, X., Shang, H., Kuhn, J., et al. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.492132 · Cited by 42 · see citing works
HIV-1 Virological Synapse: Live Imaging of Transmission
Feldmann, J., & Schwartz, O. (2010) · Viruses · doi:10.3390/v2081666 · Cited by 42 · see citing works
Roy, N. H., Lambelé, M., Chan, J., Symeonides, M., & Thali, M. (2014) · Journal of Virology · doi:10.1128/jvi.00550-14 · Cited by 42 · see citing works
Jolly, C. L. (2011) · Virology · doi:10.1016/j.virol.2010.12.031 · Cited by 42 · see citing works
Self-citationThe immunological synapse: the gateway to the HIV reservoir
Kulpa, D. A., Brehm, J. H., Fromentin, R., Cooper, A. B., Cooper, C., Ahlers, J. D., Chomont, N., & Sékaly, R. (2013) · Immunological Reviews · doi:10.1111/imr.12080 · Cited by 41 · see citing works
Effects of Microtubule Modulators on HIV-1 Infection of Transformed and Resting CD4 T Cells
Yoder, A., Guo, J., Yu, D., Cui, Z., Zhang, X., & Wu, Y. (2011) · Journal of Virology · doi:10.1128/jvi.02462-10 · Cited by 41 · see citing works
Thymosin β4 and corneal wound healing: visions of the future
Sosne, G., Qiu, P. S., Kurpakus‐Wheater, M., & Matthew, H. W. T. (2010) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2010.05472.x · Cited by 41 · see citing works
Mazurov, D., Ilinskaya, A., Heidecker, G., & Filatov, A. (2012) · Journal of Virology · doi:10.1128/jvi.06993-11 · Cited by 40 · see citing works
Identification of Vimentin as a Potential Therapeutic Target against HIV Infection
Fernández‐Ortega, C., Ramírez, A., Casillas, D., Paneque, T., Ubieta, R., Dubed, M., Navea, L., Castellanos, L., Duarte, C. A., Falcón, V., et al. (2016) · Viruses · doi:10.3390/v8060098 · Cited by 40 · see citing works
Viral exploitation of actin: force-generation and scaffolding functions in viral infection
Spear, M., & Wu, Y. (2014) · Virologica Sinica · doi:10.1007/s12250-014-3476-0 · Cited by 40 · see citing works
Role of Gag and lipids during HIV-1 assembly in CD4+ T cells and macrophages
Mariani, C., Desdouits, M., Favard, C., Benaroch, P., & Muriaux, D. M. (2014) · Frontiers in Microbiology · doi:10.3389/fmicb.2014.00312 · Cited by 40 · see citing works
Productive HIV-1 infection of tissue macrophages by fusion with infected CD4+ T cells
Mascarau, R., Woottum, M., Fromont, L., Gence, R., Cantaloube-Ferrieu, V., Vahlas, Z., Lévêque, K., Bertrand, F., Beunon, T., Métais, A., et al. (2023) · The Journal of Cell Biology · doi:10.1083/jcb.202205103 · Cited by 39 · see citing works
HIV-1 Activates T Cell Signaling Independently of Antigen to Drive Viral Spread
Len, A. C. L., Starling, S., Shivkumar, M., & Jolly, C. L. (2017) · Cell Reports · doi:10.1016/j.celrep.2016.12.057 · Cited by 39 · see citing works
Self-citationActin-myosin network is required for proper assembly of influenza virus particles
Kumakura, M., Kawaguchi, A., & Nagata, K. (2014) · Virology · doi:10.1016/j.virol.2014.12.016 · Cited by 39 · see citing works
The PDZ-adaptor protein syntenin-1 regulates HIV-1 entry
Gordón‐Alonso, M., Rocha‐Perugini, V., Álvarez, S., Moreno-Gonzalo, O., Ursa, Á., López‐Martín, S., Izquierdo‐Useros, N., Martínez‐Picado, J., Muñoz‐Fernández, M. Á., Yáñez‐Mó, M., et al. (2012) · Molecular Biology of the Cell · doi:10.1091/mbc.e11-12-1003 · Cited by 38 · see citing works
Wang, X., Yu, H., Xu, J., Zhang, S.-Z., Yu, D., Liu, M., & Wang, L. (2017) · Scientific Reports · doi:10.1038/srep45690 · Cited by 38 · see citing works
Regulated secretion from CD4+ T cells
Jolly, C. L., & Sattentau, Q. J. (2007) · Trends in Immunology · doi:10.1016/j.it.2007.08.008 · Cited by 37 · see citing works
Self-citationCommon themes in centriole and centrosome movements
Vaughan, S., & Dawe, H. R. (2010) · Trends in Cell Biology · doi:10.1016/j.tcb.2010.09.004 · Cited by 37 · see citing works
Requirement for microtubule integrity in the SOCS1‐mediated intracellular dynamics of HIV‐1 Gag
Nishi, M., Ryo, A., Tsurutani, N., Ohba, K., Sawasaki, T., Morishita, R., Perrem, K., Aoki, I., Morikawa, Y., & Yamamoto, N. (2009) · FEBS Letters · doi:10.1016/j.febslet.2009.03.041 · Cited by 36 · see citing works
Masters of manipulation: Viral modulation of the immunological synapse
Bayliss, R. J., & Piguet, V. (2018) · Cellular Microbiology · doi:10.1111/cmi.12944 · Cited by 35 · see citing works
HIV-1 assembly at the plasma membrane
Ono, A. (2010) · Vaccine · doi:10.1016/j.vaccine.2009.10.021 · Cited by 34 · see citing works
Myelin, DIGs, and membrane rafts in the central nervous system
Dupree, J. L., & Pomicter, A. D. (2009) · Prostaglandins & Other Lipid Mediators · doi:10.1016/j.prostaglandins.2009.04.005 · Cited by 34 · see citing works
LFA-1 Engagement Triggers T Cell Polarization at the HIV-1 Virological Synapse
Starling, S., & Jolly, C. (2016) · Journal of Virology · doi:10.1128/jvi.01152-16 · Cited by 33 · see citing works
Self-citationT Cell Polarization at the Virological Synapse
Jolly, C. L. (2010) · Viruses · doi:10.3390/v2061261 · Cited by 33 · see citing works
Self-citationHybrid Spreading Mechanisms and T Cell Activation Shape the Dynamics of HIV-1 Infection
Zhang, C., Zhou, S., Groppelli, E., Pellegrino, P., Williams, I. G., Borrow, P., Chain, B., & Jolly, C. L. (2015) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1004179 · Cited by 32 · see citing works
Self-citation
- Authors
- Jolly, C., Mitar, I., & Sattentau, Q. J.
- Affiliations
- University of Oxford (GB)
- Venue
- Journal of Virology
- Publisher
- American Society for Microbiology
- Published
- 2007-06
- Volume
- 81
- Issue
- 11
- Pages
- 5547-5560
- ISSN
- 0022-538X (ISSN-L)
- 1098-5514
- PMC
- PMC1900271
- OpenAlex
- W2137870598
- Cited by
- 211
- References
- 66
- Citations by year
- 2025: 3 · 2024: 4 · 2023: 6 · 2022: 13 · 2021: 6 · 2020: 5 · 2019: 4 · 2018: 13 · 2017: 5 · 2016: 9 · 2015: 9 · 2014: 20 · 2013: 15 · 2012: 22
- FWCI
- 7.01
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Journal of Virology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Funders
- National Institutes of Health
- Medical Research Council
- 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, actin cytoskeleton, tubulin, virological synapse, cell-to-cell transmission, viral budding, Gag, Env, lipid rafts, actin depolymerization, tubulin polymerization inhibitors, CD4+ T cells, viral assembly
- MeSH terms
- Actins, Cell Communication, Cytoskeleton, Humans, T-Lymphocytes, Tubulin, HIV-1, HIV Infections, Virus Assembly, Jurkat Cells, Tubulin Modulators
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
