Can Non-lytic CD8+ T Cells Drive HIV-1 Escape?

Seich al Basatena, Nafisa-Katrin; Chatzimichalis, Konstantinos; Graw, Frederik; Frost, Simon D.  W.; Regoes, Roland R.; Asquith, Becca

doi:10.1371/journal.ppat.1003656

Can Non-lytic CD8+ T Cells Drive HIV-1 Escape?

Journal Article · Wed Nov 13 23:00:00 EST 2013 · PLoS Pathogens

DOI:https://doi.org/10.1371/journal.ppat.1003656· OSTI ID:1627908

Seich al Basatena, Nafisa-Katrin ^[1]; Chatzimichalis, Konstantinos ^[2]; Graw, Frederik ^[3]; Frost, Simon D. W. ^[4]; Regoes, Roland R. ^[5]; Asquith, Becca ^[6]

Imperial College, London (United Kingdom); DOE/OSTI
Birkbeck University, London (United Kingdom)
Los Alamos National Laboratory (LANL), Los Alamos, NM (United States); Heidelberg University (Germany)
University of Cambridge (United Kingdom)
Eidgenoessische Technische Hochschule, Zurich (Switzerland)
Imperial College, London (United Kingdom)

The CD8+ T cell effector mechanisms that mediate control of HIV-1 and SIV infections remain poorly understood. Recent work suggests that the mechanism may be primarily non-lytic. This is in apparent conflict with the observation that SIV and HIV-1 variants that escape CD8+ T cell surveillance are frequently selected. Whilst it is clear that a variant that has escaped a lytic response can have a fitness advantage compared to the wild-type, it is less obvious that this holds in the face of nonlytic control where both wild-type and variant infected cells would be affected by soluble factors. In particular, the high motility of T cells in lymphoid tissue would be expected to rapidly destroy local effects making selection of escape variants by non-lytic responses unlikely. The observation of frequent HIV-1 and SIV escape poses a number of questions. Most importantly, is the consistent observation of viral escape proof that HIV-1- and SIV-specific CD8+ T cells lyse infected cells or can this also be the result of non-lytic control? Additionally, the rate at which a variant strain escapes a lytic CD8+ T cell response is related to the strength of the response. Is the same relationship true for a non-lytic response? Finally, the potential anti-viral control mediated by non-lytic mechanisms compared to lytic mechanisms is unknown. These questions cannot be addressed with current experimental techniques nor with the standard mathematical models. Instead we have developed a 3D cellular automaton model of HIV-1 which captures spatial and temporal dynamics. The model reproduces in vivo HIV-1 dynamics at the cellular and population level. Using this model we demonstrate that non-lytic effector mechanisms can select for escape variants but that outgrowth of the variant is slower and less frequent than from a lytic response so that non-lytic responses can potentially offer more durable control.

View Accepted Manuscript (DOE)

Research Organization:: Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); Wellcome Trust; Medical Research Council (MRC)

Grant/Contract Number:: AC52-06NA25396

OSTI ID:: 1627908

Journal Information:: PLoS Pathogens, Journal Name: PLoS Pathogens Journal Issue: 11 Vol. 9; ISSN 1553-7374

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

References (112)

Serial killing by cytotoxic T lymphocytes: T cell receptor triggers degranulation, re-filling of the lytic granules and secretion of lytic proteins via a non-granule pathway Isaaz, Sylvie; Baetz, Kristin; Olsen, Kristin European Journal of Immunology, Vol. 25, Issue 4 https://doi.org/10.1002/eji.1830250432	journal	April 1995
Recombinant human interferon gamma suppresses HTLV-III replicationin vitro Nakashima, Hideki; Yoshida, Tsutomu; Harada, Shinji International Journal of Cancer, Vol. 38, Issue 3 https://doi.org/10.1002/ijc.2910380320	journal	September 1986
Modeling Plasma Virus Concentration during Primary HIV Infection Stafford, Max A.; Corey, Lawrence; Cao, Yunzhen Journal of Theoretical Biology, Vol. 203, Issue 3 https://doi.org/10.1006/jtbi.2000.1076	journal	April 2000
Spatiotemporal Dynamics of HIV Propagation Strain, M. C.; Richman, D. D.; Wong, J. K. Journal of Theoretical Biology, Vol. 218, Issue 1 https://doi.org/10.1006/jtbi.2002.3055	journal	September 2002
Interferon Treatment Inhibits Virus Replication in HIV-1- and SIV-Infected CD4+ T-Cell Lines by Distinct Mechanisms: Evidence for Decreased Stability and Aberrant Processing of HIV-1 Proteins Agy, Michael B.; Acker, Randy L.; Sherbert, Cynthia H. Virology, Vol. 214, Issue 2 https://doi.org/10.1006/viro.1995.0047	journal	December 1995
Modeling LSD1-Mediated Tumor Stagnation Milzman, Jesse; Sheng, Wanqiang; Levy, Doron Bulletin of Mathematical Biology, Vol. 83, Issue 2 https://doi.org/10.1007/s11538-020-00842-8	journal	January 2021
CD8+ lymphocytes suppress HIV production by autologous CD4+ cells without eliminating the infected cells from culture Wiviott, Lory D.; Walker, Christopher M.; Levy, Jay A. Cellular Immunology, Vol. 128, Issue 2 https://doi.org/10.1016/0008-8749(90)90054-U	journal	July 1990
Controlling HIV pathogenesis: the role of the noncytotoxic anti-HIV response of CD8+ T cells Levy, Jay A.; Mackewicz, Carl E.; Barker, Edward Immunology Today, Vol. 17, Issue 5 https://doi.org/10.1016/0167-5699(96)10011-6	journal	May 1996
Rapid production and clearance of HIV-1 and hepatitis C virus assessed by large volume plasma apheresis Ramratnam, Bharat; Bonhoeffer, Sebastian; Binley, James The Lancet, Vol. 354, Issue 9192 https://doi.org/10.1016/S0140-6736(99)02035-8	journal	November 1999
Evidence that Structural Rearrangements and/or Flexibility during TCR Binding Can Contribute to T Cell Activation Krogsgaard, Michelle; Prado, Nelida; Adams, Erin J. Molecular Cell, Vol. 12, Issue 6 https://doi.org/10.1016/S1097-2765(03)00474-X	journal	December 2003
Lymphocyte kinetics: the interpretation of labelling data Asquith, Becca; Debacq, Christophe; Macallan, Derek C. Trends in Immunology, Vol. 23, Issue 12 https://doi.org/10.1016/S1471-4906(02)02337-2	journal	December 2002
Secretion of MIP-1β and MIP-1α by CD8+ T-lymphocytes correlates with HIV-1 inhibition independent of coreceptor usage Saunders, Kevin O.; Ward-Caviness, Cavin; Schutte, Robert J. Cellular Immunology, Vol. 266, Issue 2 https://doi.org/10.1016/j.cellimm.2010.09.011	journal	January 2011
Regulatory T Cells Reversibly Suppress Cytotoxic T Cell Function Independent of Effector Differentiation Mempel, Thorsten R.; Pittet, Mikael J.; Khazaie, Khashayarsha Immunity, Vol. 25, Issue 1 https://doi.org/10.1016/j.immuni.2006.04.015	journal	July 2006
Bacterial Entry to the Splenic White Pulp Initiates Antigen Presentation to CD8+ T Cells Aoshi, Taiki; Zinselmeyer, Bernd H.; Konjufca, Vjollca Immunity, Vol. 29, Issue 3 https://doi.org/10.1016/j.immuni.2008.06.013	journal	September 2008
Dependence of T Cell Antigen Recognition on T Cell Receptor-Peptide MHC Confinement Time Aleksic, Milos; Dushek, Omer; Zhang, Hao Immunity, Vol. 32, Issue 2 https://doi.org/10.1016/j.immuni.2009.11.013	journal	February 2010
Intravital Imaging Reveals Limited Antigen Presentation and T Cell Effector Function in Mycobacterial Granulomas Egen, Jackson G.; Rothfuchs, Antonio Gigliotti; Feng, Carl G. Immunity, Vol. 34, Issue 5 https://doi.org/10.1016/j.immuni.2011.03.022	journal	May 2011
CD4+ T Cells Rely on a Cytokine Gradient to Control Intracellular Pathogens beyond Sites of Antigen Presentation Müller, Andreas J.; Filipe-Santos, Orchidée; Eberl, Gerard Immunity, Vol. 37, Issue 1 https://doi.org/10.1016/j.immuni.2012.05.015	journal	July 2012
Agent-based modeling of host–pathogen systems: The successes and challenges Bauer, Amy L.; Beauchemin, Catherine A. A.; Perelson, Alan S. Information Sciences, Vol. 179, Issue 10 https://doi.org/10.1016/j.ins.2008.11.012	journal	April 2009
The role of chemokines in human immunodeficiency virus infection: Chemokines and HIV Garzino-Demo, Alfredo; DeVico, Anthony L.; Conant, Katherine E. Immunological Reviews, Vol. 177, Issue 1 https://doi.org/10.1034/j.1600-065X.2000.17711.x	journal	October 2000
Human immunodeficiency virus genetic variation that can escape cytotoxic T cell recognition Phillips, Rodney E.; Rowland-Jones, Sarah; Nixon, Douglas F. Nature, Vol. 354, Issue 6353 https://doi.org/10.1038/354453a0	journal	December 1991
Multiply infected spleen cells in HIV patients Jung, Andreas; Maier, Reinhard; Vartanian, Jean-Pierre Nature, Vol. 418, Issue 6894 https://doi.org/10.1038/418144a	journal	July 2002
Rapid on/off cycling of cytokine production by virus-specific CD8+ T cells Slifka, Mark K.; Rodriguez, Fernando; Whitton, J. Lindsay Nature, Vol. 401, Issue 6748 https://doi.org/10.1038/43454	journal	September 1999
Simulating T‐cell motility in the lymph node paracortex with a packed lattice geometry Bogle, Gib; Dunbar, P. Rod Immunology & Cell Biology, Vol. 86, Issue 8 https://doi.org/10.1038/icb.2008.60	journal	August 2008
Challenges in the development of an HIV-1 vaccine Barouch, Dan H. Nature, Vol. 455, Issue 7213 https://doi.org/10.1038/nature07352	journal	October 2008
Antiviral pressure exerted by HIV-l-specific cytotoxic T lymphocytes (CTLs) during primary infection demonstrated by rapid selection of CTL escape virus Borrow, Persephone; Lewicki, Hanna; Wei, Xiping Nature Medicine, Vol. 3, Issue 2 https://doi.org/10.1038/nm0297-205	journal	February 1997
Late escape from an immunodominant cytotoxic T-lymphocyte response associated with progression to AIDS Goulder, Philip J. R.; Phillips, Rodney E.; Colbert, Robert A. Nature Medicine, Vol. 3, Issue 2 https://doi.org/10.1038/nm0297-212	journal	February 1997
Transfer of HIV-1-specific cytotoxic T lymphocytes to an AIDS patient leads to selection for mutant HIV variants and subsequent disease progression Koenig, Scott; Conley, Anthony J.; Brewah, Yambasu A. Nature Medicine, Vol. 1, Issue 4 https://doi.org/10.1038/nm0495-330	journal	April 1995
Control of HIV-1 infection by soluble factors of the immune response DeVico, Anthony L.; Gallo, Robert C. Nature Reviews Microbiology, Vol. 2, Issue 5 https://doi.org/10.1038/nrmicro878	journal	May 2004
Mathematical models of cytotoxic T‐lymphocyte killing Regoes, Roland R.; Yates, Andrew; Antia, Rustom Immunology & Cell Biology, Vol. 85, Issue 4 https://doi.org/10.1038/sj.icb.7100053	journal	April 2007
Spatial modelling of brief and long interactions between T cells and dendritic cells Beltman, Joost B.; Marée, Athanasius F. M.; de Boer, Rob J. Immunology and Cell Biology, Vol. 85, Issue 4 https://doi.org/10.1038/sj.icb.7100054	journal	April 2007
T cell receptor binding kinetics required for T cell activation depend on the density of cognate ligand on the antigen-presenting cell Gonzalez, P. A.; Carreno, L. J.; Coombs, D. Proceedings of the National Academy of Sciences, Vol. 102, Issue 13 https://doi.org/10.1073/pnas.0500922102	journal	March 2005
Cytotoxic T lymphocytes kill multiple targets simultaneously via spatiotemporal uncoupling of lytic and stimulatory synapses Wiedemann, A.; Depoil, D.; Faroudi, M. Proceedings of the National Academy of Sciences, Vol. 103, Issue 29 https://doi.org/10.1073/pnas.0600651103	journal	July 2006
In vivo CD8+ T cell control of immunodeficiency virus infection in humans and macaques Asquith, B.; McLean, A. R. Proceedings of the National Academy of Sciences, Vol. 104, Issue 15 https://doi.org/10.1073/pnas.0700666104	journal	April 2007
Majority of CD4+ T cells from peripheral blood of HIV-1-infected individuals contain only one HIV DNA molecule Josefsson, L.; King, M. S.; Makitalo, B. Proceedings of the National Academy of Sciences, Vol. 108, Issue 27 https://doi.org/10.1073/pnas.1107729108	journal	June 2011
Cytotoxic immunological synapses do not restrict the action of interferon- to antigenic target cells Sanderson, N. S. R.; Puntel, M.; Kroeger, K. M. Proceedings of the National Academy of Sciences, Vol. 109, Issue 20 https://doi.org/10.1073/pnas.1116058109	journal	April 2012
Genetic drift and within-host metapopulation dynamics of HIV-1 infection Frost, S. D. W.; Dumaurier, M. -J.; Wain-Hobson, S. Proceedings of the National Academy of Sciences, Vol. 98, Issue 12 https://doi.org/10.1073/pnas.131056998	journal	May 2001
Autonomous T cell trafficking examined in vivo with intravital two-photon microscopy Miller, M. J.; Wei, S. H.; Cahalan, M. D. Proceedings of the National Academy of Sciences, Vol. 100, Issue 5 https://doi.org/10.1073/pnas.2628040100	journal	February 2003
In vitro modification of human immunodeficiency virus infection by granulocyte-macrophage colony-stimulating factor and gamma interferon. Hammer, S. M.; Gillis, J. M.; Groopman, J. E. Proceedings of the National Academy of Sciences, Vol. 83, Issue 22 https://doi.org/10.1073/pnas.83.22.8734	journal	November 1986
CD8+ T cells suppress human immunodeficiency virus replication by inhibiting viral transcription. Mackewicz, C. E.; Blackbourn, D. J.; Levy, J. A. Proceedings of the National Academy of Sciences, Vol. 92, Issue 6 https://doi.org/10.1073/pnas.92.6.2308	journal	March 1995
Cytotoxic T lymphocytes and viral turnover in HIV type 1 infection Klenerman, P.; Phillips, R. E.; Rinaldo, C. R. Proceedings of the National Academy of Sciences, Vol. 93, Issue 26 https://doi.org/10.1073/pnas.93.26.15323	journal	December 1996
Positive selection of HIV-1 cytotoxic T lymphocyte escape variants during primary infection Price, D. A.; Goulder, P. J. R.; Klenerman, P. Proceedings of the National Academy of Sciences, Vol. 94, Issue 5 https://doi.org/10.1073/pnas.94.5.1890	journal	March 1997
Polymorphism in RANTES chemokine promoter affects HIV-1 disease progression Liu, H.; Chao, D.; Nakayama, E. E. Proceedings of the National Academy of Sciences, Vol. 96, Issue 8 https://doi.org/10.1073/pnas.96.8.4581	journal	April 1999
Endocytosis and Recycling of the HIV Coreceptor Ccr5 Signoret, Nathalie; Pelchen-Matthews, Annegret; Mack, Matthias Journal of Cell Biology, Vol. 151, Issue 6 https://doi.org/10.1083/jcb.151.6.1281	journal	December 2000
In vivo imaging of cytotoxic T cell infiltration and elimination of a solid tumor Boissonnas, Alexandre; Fetler, Luc; Zeelenberg, Ingrid S. The Journal of Cell Biology, Vol. 176, Issue 4 https://doi.org/10.1083/jcb1764oia8	journal	February 2007
Lymph node topology dictates T cell migration behavior Beltman, Joost B.; Marée, Athanasius F. M.; Lynch, Jennifer N. The Journal of Cell Biology, Vol. 177, Issue 1 https://doi.org/10.1083/jcb1771oia2	journal	April 2007
Viral Dynamics of Acute HIV-1 Infection Little, Susan J.; McLean, Angela R.; Spina, Celsa A. The Journal of Experimental Medicine, Vol. 190, Issue 6 https://doi.org/10.1084/jem.190.6.841	journal	September 1999
Increased Turnover of T Lymphocytes in HIV-1 Infection and Its Reduction by Antiretroviral Therapy Mohri, Hiroshi; Perelson, Alan S.; Tung, Keith The Journal of Experimental Medicine, Vol. 194, Issue 9 https://doi.org/10.1084/jem.194.9.1277	journal	October 2001
HIV-1 Cell to Cell Transfer across an Env-induced, Actin-dependent Synapse Jolly, Clare; Kashefi, Kirk; Hollinshead, Michael Journal of Experimental Medicine, Vol. 199, Issue 2 https://doi.org/10.1084/jem.20030648	journal	January 2004
Determinants of Human Immunodeficiency Virus Type 1 Escape from the Primary CD8⁺ Cytotoxic T Lymphocyte Response Jones, Nicola A.; Wei, Xiping; Flower, Darren R. The Journal of Experimental Medicine, Vol. 200, Issue 10, p. 1243-1256 https://doi.org/10.1084/jem.20040511	journal	November 2004
Imaging the Single Cell Dynamics of CD4 ⁺ T Cell Activation by Dendritic Cells in Lymph Nodes Miller, Mark J.; Safrina, Olga; Parker, Ian The Journal of Experimental Medicine, Vol. 200, Issue 7 https://doi.org/10.1084/jem.20041236	journal	October 2004
Lymph node topology dictates T cell migration behavior Beltman, Joost B.; Marée, Athanasius F. M.; Lynch, Jennifer N. The Journal of Experimental Medicine, Vol. 204, Issue 4 https://doi.org/10.1084/jem.20061278	journal	March 2007
CCR7 ligands stimulate the intranodal motility of T lymphocytes in vivo Worbs, Tim; Mempel, Thorsten R.; Bölter, Jasmin Journal of Experimental Medicine, Vol. 204, Issue 3 https://doi.org/10.1084/jem.20061706	journal	February 2007
In vivo imaging of cytotoxic T cell infiltration and elimination of a solid tumor Boissonnas, Alexandre; Fetler, Luc; Zeelenberg, Ingrid S. Journal of Experimental Medicine, Vol. 204, Issue 2 https://doi.org/10.1084/jem.20061890	journal	January 2007
Superior control of HIV-1 replication by CD8+ T cells is reflected by their avidity, polyfunctionality, and clonal turnover Almeida, Jorge R.; Price, David A.; Papagno, Laura Journal of Experimental Medicine, Vol. 204, Issue 10 https://doi.org/10.1084/jem.20070784	journal	September 2007
The first T cell response to transmitted/founder virus contributes to the control of acute viremia in HIV-1 infection Goonetilleke, Nilu; Liu, Michael K. P.; Salazar-Gonzalez, Jesus F. The Journal of Experimental Medicine, Vol. 206, Issue 6 https://doi.org/10.1084/jem.20090365	journal	June 2009
Productive Infection of T Cells in Lymphoid Tissues during Primary and Early Human Immunodeficiency Virus Infection Schacker, Timothy; Little, Susan; Connick, Elizabeth The Journal of Infectious Diseases, Vol. 183, Issue 4 https://doi.org/10.1086/318524	journal	February 2001
Anti-Human Immunodeficiency Virus Noncytolytic CD8 ⁺ T-Cell Response: A Review Geiben-Lynn, Ralf AIDS Patient Care and STDs, Vol. 16, Issue 10 https://doi.org/10.1089/10872910260351249	journal	October 2002
Inhibition of Growth of HIV by Human Natural Interferon In Vitro Yamada, Osamu; Hattori, Naohiko; Kurimura, Takashi AIDS Research and Human Retroviruses, Vol. 4, Issue 4 https://doi.org/10.1089/aid.1988.4.287	journal	January 1988
CD8 ⁺ T Lymphocyte-Mediated Inhibition of HIV-1 Long Terminal Repeat Transcription: A Novel Antiviral Mechanism Chen, Chin-Ho; Weinhold, Kent J.; Bartlett, John A. AIDS Research and Human Retroviruses, Vol. 9, Issue 11 https://doi.org/10.1089/aid.1993.9.1079	journal	November 1993
Suppression of Activation of the Human Immunodeficiency Virus Long Terminal Repeat by CD8 ⁺ T Cells Is Not Lentivirus Specific Copeland, Karen F. T.; McKAY, Paula J.; Rosenthal, Kenneth L. AIDS Research and Human Retroviruses, Vol. 11, Issue 11 https://doi.org/10.1089/aid.1995.11.1321	journal	November 1995
Human Alpha- and Beta-Interferon But Not Gamma- Suppress the In Vitro Replication of LAV, HTLV-III, and ARV-2 Yamamoto, Janet K.; BarrÉ-Sinoussi, FranÇOise; Bolton, Veronica Journal of Interferon Research, Vol. 6, Issue 2 https://doi.org/10.1089/jir.1986.6.143	journal	April 1986
Exocytic responses of single leukaemic human cytotoxic T lymphocytes stimulated by agents that bypass the T cell receptor: Single-CTL exocytosis in response to TCR-independent stimulation Pores-Fernando, Arun T.; Bauer, Roslyn A.; Wurth, Georjeana A. The Journal of Physiology, Vol. 567, Issue 3 https://doi.org/10.1113/jphysiol.2005.089565	journal	September 2005
Two-Photon Imaging of Lymphocyte Motility and Antigen Response in Intact Lymph Node Miller, M. J. Science, Vol. 296, Issue 5574 https://doi.org/10.1126/science.1070051	journal	May 2002
Quantitative 3D Video Microscopy of HIV Transfer Across T Cell Virological Synapses Hubner, W.; McNerney, G. P.; Chen, P. Science, Vol. 323, Issue 5922 https://doi.org/10.1126/science.1167525	journal	March 2009
Cytokines alter production of HIV-1 from primary mononuclear phagocytes Koyanagi, Y.; O'Brien, Wa; Zhao, Jq Science, Vol. 241, Issue 4873 https://doi.org/10.1126/science.241.4873.1673	journal	September 1988
CD8+ lymphocytes can control HIV infection in vitro by suppressing virus replication Walker, C.; Moody, D.; Stites, D. Science, Vol. 234, Issue 4783 https://doi.org/10.1126/science.2431484	journal	December 1986
Identification of RANTES, MIP-1alpha, and MIP-1beta as the Major HIV-Suppressive Factors Produced by CD8+ T Cells Cocchi, F.; DeVico, A. L.; Garzino-Demo, A. Science, Vol. 270, Issue 5243 https://doi.org/10.1126/science.270.5243.1811	journal	December 1995
HIV-1 Dynamics in Vivo: Virion Clearance Rate, Infected Cell Life-Span, and Viral Generation Time Perelson, A. S.; Neumann, A. U.; Markowitz, M. Science, Vol. 271, Issue 5255 https://doi.org/10.1126/science.271.5255.1582	journal	March 1996
Control of Viremia in Simian Immunodeficiency Virus Infection by CD8⁺ Lymphocytes Schmitz, Jorn E.; Kuroda, Marcelo J.; Santra, Sampa Science, Vol. 283, Issue 5403, p. 857-860 https://doi.org/10.1126/science.283.5403.857	journal	February 1999
Cytokines alter production of HIV-1 from primary mononuclear phagocytes Koyanagi, Y.; O'Brien, Wa; Zhao, Jq Science, Vol. 241, Issue 4873 https://doi.org/10.1126/science.3047875	journal	September 1988
HIV population dynamics in vivo: implications for genetic variation, pathogenesis, and therapy Coffin, J. Science, Vol. 267, Issue 5197 https://doi.org/10.1126/science.7824947	journal	January 1995
Antigen Potency and Maximal Efficacy Reveal a Mechanism of Efficient T Cell Activation Dushek, O.; Aleksic, M.; Wheeler, R. J. Science Signaling, Vol. 4, Issue 176 https://doi.org/10.1126/scisignal.2001430	journal	June 2011
Estimation of the Initial Viral Growth Rate and Basic Reproductive Number during Acute HIV-1 Infection Ribeiro, R. M.; Qin, L.; Chavez, L. L. Journal of Virology, Vol. 84, Issue 12 https://doi.org/10.1128/JVI.00127-10	journal	March 2010
Simultaneous Cell-to-Cell Transmission of Human Immunodeficiency Virus to Multiple Targets through Polysynapses Rudnicka, Dominika; Feldmann, Jérôme; Porrot, Françoise Journal of Virology, Vol. 83, Issue 12 https://doi.org/10.1128/JVI.00282-09	journal	April 2009
Fitness Costs and Diversity of the Cytotoxic T Lymphocyte (CTL) Response Determine the Rate of CTL Escape during Acute and Chronic Phases of HIV Infection Ganusov, V. V.; Goonetilleke, N.; Liu, M. K. P. Journal of Virology, Vol. 85, Issue 20 https://doi.org/10.1128/JVI.00655-11	journal	August 2011
Estimating the Effectiveness of Simian Immunodeficiency Virus-Specific CD8+ T Cells from the Dynamics of Viral Immune Escape Mandl, Judith N.; Regoes, Roland R.; Garber, David A. Journal of Virology, Vol. 81, Issue 21 https://doi.org/10.1128/JVI.00946-07	journal	August 2007
Inefficient Human Immunodeficiency Virus Replication in Mobile Lymphocytes Sourisseau, Marion; Sol-Foulon, Nathalie; Porrot, Françoise Journal of Virology, Vol. 81, Issue 2 https://doi.org/10.1128/JVI.01629-06	journal	November 2006
Inhibition of human immunodeficiency virus replication in acutely infected CD4+ cells by CD8+ cells involves a noncytotoxic mechanism. Walker, C. M.; Erickson, A. L.; Hsueh, F. C. Journal of Virology, Vol. 65, Issue 11 https://doi.org/10.1128/JVI.65.11.5921-5927.1991	journal	January 1991
Differential loss of envelope glycoprotein gp120 from virions of human immunodeficiency virus type 1 isolates: effects on infectivity and neutralization. McKeating, J. A.; McKnight, A.; Moore, J. P. Journal of Virology, Vol. 65, Issue 2 https://doi.org/10.1128/JVI.65.2.852-860.1991	journal	January 1991
Recombinant CD4-selected human immunodeficiency virus type 1 variants with reduced gp120 affinity for CD4 and increased cell fusion capacity. McKeating, J.; Balfe, P.; Clapham, P. Journal of Virology, Vol. 65, Issue 9 https://doi.org/10.1128/JVI.65.9.4777-4785.1991	journal	January 1991
Viral dynamics of primary viremia and antiretroviral therapy in simian immunodeficiency virus infection. Nowak, M. A.; Lloyd, A. L.; Vasquez, G. M. Journal of virology, Vol. 71, Issue 10 https://doi.org/10.1128/JVI.71.10.7518-7525.1997	journal	January 1997
Suppression of human immunodeficiency virus type 1 replication by CD8+ cells: evidence for HLA class I-restricted triggering of cytolytic and noncytolytic mechanisms. Yang, O. O.; Kalams, S. A.; Trocha, A. Journal of virology, Vol. 71, Issue 4 https://doi.org/10.1128/JVI.71.4.3120-3128.1997	journal	January 1997
Endogenous Production of β-Chemokines by CD4+, but Not CD8+, T-Cell Clones Correlates with the Clinical State of Human Immunodeficiency Virus Type 1 (HIV-1)-Infected Individuals and May Be Responsible for Blocking Infection with NonSyncytium-Inducing HIV-1 In Vitro Saha, Kunal; Bentsman, Galina; Chess, Leonard Journal of Virology, Vol. 72, Issue 1 https://doi.org/10.1128/JVI.72.1.876-881.1998	journal	January 1998
Rapid Clearance of Simian Immunodeficiency Virus Particles from Plasma of Rhesus Macaques Zhang, Linqi; Dailey, Peter J.; He, Tian Journal of Virology, Vol. 73, Issue 1 https://doi.org/10.1128/JVI.73.1.855-860.1999	journal	January 1999
Lack of Viral Escape and Defective In Vivo Activation of Human Immunodeficiency Virus Type 1-Specific Cytotoxic T Lymphocytes in Rapidly Progressive Infection Hay, Christine M.; Ruhl, Debbie J.; Basgoz, Nesli O. Journal of Virology, Vol. 73, Issue 7 https://doi.org/10.1128/JVI.73.7.5509-5519.1999	journal	July 1999
Identification of Sequential Viral Escape Mutants Associated with Altered T-Cell Responses in a Human Immunodeficiency Virus Type 1-Infected Individual Geels, Mark J.; Cornelissen, Marion; Schuitemaker, Hanneke Journal of Virology, Vol. 77, Issue 23 https://doi.org/10.1128/JVI.77.23.12430-12440.2003	journal	December 2003
A Novel Antiviral Intervention Results in More Accurate Assessment of Human Immunodeficiency Virus Type 1 Replication Dynamics and T-Cell Decay In Vivo Markowitz, M.; Louie, M.; Hurley, A. Journal of Virology, Vol. 77, Issue 8 https://doi.org/10.1128/JVI.77.8.5037-5038.2003	journal	April 2003
Sexual Transmission of Single Human Immunodeficiency Virus Type 1 Virions Encoding Highly Polymorphic Multisite Cytotoxic T-Lymphocyte Escape Variants Milicic, Anita; Edwards, Charles T. T.; Hué, Stéphane Journal of Virology, Vol. 79, Issue 22 https://doi.org/10.1128/JVI.79.22.13953-13962.2005	journal	November 2005
How Antigen Quantity and Quality Determine T-Cell Decisions in Lymphoid Tissue Zheng, Huan; Jin, Bo; Henrickson, Sarah E. Molecular and Cellular Biology, Vol. 28, Issue 12 https://doi.org/10.1128/MCB.00136-08	journal	April 2008
Secretory Mechanisms in Cell-Mediated Cytotoxicity Stinchcombe, Jane C.; Griffiths, Gillian M. Annual Review of Cell and Developmental Biology, Vol. 23, Issue 1 https://doi.org/10.1146/annurev.cellbio.23.090506.123521	journal	November 2007
POPULATION BIOLOGY OF HIV-1 INFECTION: Viral and CD4 ⁺ T Cell Demographics and Dynamics in Lymphatic Tissues Haase, A. T. Annual Review of Immunology, Vol. 17, Issue 1 https://doi.org/10.1146/annurev.immunol.17.1.625	journal	April 1999
Do beta-chemokines have clinical relevance in HIV infection? Mackewicz, C. E.; Barker, E.; Greco, G. Journal of Clinical Investigation, Vol. 100, Issue 4 https://doi.org/10.1172/JCI119608	journal	August 1997
Inefficient Cytotoxic T Lymphocyte–Mediated Killing of HIV-1–Infected Cells In Vivo Asquith, Becca; Edwards, Charles T. T.; Lipsitch, Marc PLoS Biology, Vol. 4, Issue 4 https://doi.org/10.1371/journal.pbio.0040090	journal	March 2006
Investigating CTL Mediated Killing with a 3D Cellular Automaton Graw, Frederik; Regoes, Roland R. PLoS Computational Biology, Vol. 5, Issue 8 https://doi.org/10.1371/journal.pcbi.1000466	journal	August 2009
Quantifying the Impact of Human Immunodeficiency Virus-1 Escape From Cytotoxic T-Lymphocytes Kadolsky, Ulrich D.; Asquith, Becca PLoS Computational Biology, Vol. 6, Issue 11 https://doi.org/10.1371/journal.pcbi.1000981	journal	November 2010
Why Don't CD8+ T Cells Reduce the Lifespan of SIV-Infected Cells In Vivo? Elemans, Marjet; Seich al Basatena, Nafisa-Katrin; Klatt, Nichole R. PLoS Computational Biology, Vol. 7, Issue 9 https://doi.org/10.1371/journal.pcbi.1002200	journal	September 2011
Influence of the Fibroblastic Reticular Network on Cell-Cell Interactions in Lymphoid Organs Graw, Frederik; Regoes, Roland R. PLoS Computational Biology, Vol. 8, Issue 3 https://doi.org/10.1371/journal.pcbi.1002436	journal	March 2012
Estimating the Fitness Cost of Escape from HLA Presentation in HIV-1 Protease and Reverse Transcriptase Mostowy, Rafal; Kouyos, Roger D.; Hoof, Ilka PLoS Computational Biology, Vol. 8, Issue 5 https://doi.org/10.1371/journal.pcbi.1002525	journal	May 2012
Transmission of Single HIV-1 Genomes and Dynamics of Early Immune Escape Revealed by Ultra-Deep Sequencing Fischer, Will; Ganusov, Vitaly V.; Giorgi, Elena E. PLoS ONE, Vol. 5, Issue 8 https://doi.org/10.1371/journal.pone.0012303	journal	August 2010
Biologically-Directed Modeling Reflects Cytolytic Clearance of SIV-Infected Cells In Vivo in Macaques Wick, W. David; Yang, Otto O. PLoS ONE, Vol. 7, Issue 9 https://doi.org/10.1371/journal.pone.0044778	journal	September 2012
CD8+ Lymphocytes Control Viral Replication in SIVmac239-Infected Rhesus Macaques without Decreasing the Lifespan of Productively Infected Cells Klatt, Nichole R.; Shudo, Emi; Ortiz, Alex M. PLoS Pathogens, Vol. 6, Issue 1 https://doi.org/10.1371/journal.ppat.1000747	journal	January 2010
In Vivo CD8+ T-Cell Suppression of SIV Viremia Is Not Mediated by CTL Clearance of Productively Infected Cells Wong, Joseph K.; Strain, Matthew C.; Porrata, Rodin PLoS Pathogens, Vol. 6, Issue 1 https://doi.org/10.1371/journal.ppat.1000748	journal	January 2010
Quantitative Comparison of HTLV-1 and HIV-1 Cell-to-Cell Infection with New Replication Dependent Vectors Mazurov, Dmitriy; Ilinskaya, Anna; Heidecker, Gisela PLoS Pathogens, Vol. 6, Issue 2 https://doi.org/10.1371/journal.ppat.1000788	journal	February 2010
The first T cell response to transmitted/founder virus contributes to the control of acute viremia in HIV-1 infection Nilu, Goonetilleke,; Persephone, Borrow,; Elena, Giorgi, The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/pft2-qa63	text	January 2009
Influence of the Fibroblastic Reticular Network on Cell-Cell Interactions in Lymphoid Organs Graw, Frederik; Regoes, Roland R. ETH Zurich https://doi.org/10.3929/ethz-b-000047853	text	January 2012
Estimating the Fitness Cost of Escape from HLA Presentation in HIV-1 Protease and Reverse Transcriptase Mostowy, Rafal; Kouyos, Roger D.; Hoof, Ilka ETH Zurich https://doi.org/10.3929/ethz-b-000051356	text	January 2012
Investigating CTL Mediated Killing with a 3D Cellular Automaton Graw, Frederik; Regoes, Roland R. ETH Zurich https://doi.org/10.3929/ethz-b-000157184	text	January 2009
The Impact of TCR-Binding Properties and Antigen Presentation Format on T Cell Responsiveness Chervin, Adam S.; Stone, Jennifer D.; Holler, Phillip D. The Journal of Immunology, Vol. 183, Issue 2 https://doi.org/10.4049/jimmunol.0900054	journal	June 2009
Escape from CD8 ⁺ T Cell Responses in Mamu-B00801* ⁺ Macaques Differentiates Progressors from Elite Controllers Mudd, Philip A.; Ericsen, Adam J.; Burwitz, Benjamin J. The Journal of Immunology, Vol. 188, Issue 7 https://doi.org/10.4049/jimmunol.1102470	journal	March 2012
Epitope Escape Mutation and Decay of Human Immunodeficiency Virus Type 1-Specific CTL Responses Jamieson, Beth D.; Yang, Otto O.; Hultin, Lance The Journal of Immunology, Vol. 171, Issue 10 https://doi.org/10.4049/jimmunol.171.10.5372	journal	November 2003
HIV-1 Viral Escape in Infancy Followed by Emergence of a Variant-Specific CTL Response Feeney, M. E.; Tang, Y.; Pfafferott, K. The Journal of Immunology, Vol. 174, Issue 12, p. 7524-7530 https://doi.org/10.4049/jimmunol.174.12.7524	journal	June 2005
Fibroblastic Reticular Cells Guide T Lymphocyte Entry into and Migration within the Splenic T Cell Zone Bajénoff, Marc; Glaichenhaus, Nicolas; Germain, Ronald N. The Journal of Immunology, Vol. 181, Issue 6 https://doi.org/10.4049/jimmunol.181.6.3947	journal	September 2008

Cited By (4)

Mechanisms of CD8 ⁺ T cell-mediated suppression of HIV/SIV replication McBrien, Julia Bergild; Kumar, Nitasha A.; Silvestri, Guido European Journal of Immunology, Vol. 48, Issue 6 https://doi.org/10.1002/eji.201747172	journal	March 2018
The dynamics of simian immunodeficiency virus after depletion of CD8+ cells Cardozo, Erwing Fabian; Apetrei, Cristian; Pandrea, Ivona Immunological Reviews, Vol. 285, Issue 1 https://doi.org/10.1111/imr.12691	journal	August 2018
Differential Impact of In Vivo CD8 ⁺ T Lymphocyte Depletion in Controller versus Progressor Simian Immunodeficiency Virus-Infected Macaques Chowdhury, Ankita; Hayes, Timothy L.; Bosinger, Steven E. Journal of Virology, Vol. 89, Issue 17 https://doi.org/10.1128/jvi.00869-15	journal	June 2015
Limited immune surveillance in lymphoid tissue by cytolytic CD4+ T cells during health and HIV disease Buggert, Marcus; Nguyen, Son; McLane, Laura M. PLOS Pathogens, Vol. 14, Issue 4 https://doi.org/10.1371/journal.ppat.1006973	journal	April 2018

Similar Records

Depletion of CD8+ cells does not affect the lifespan of productively infected cells during pathogenic sivmac239 infection of rhesus macaques

Journal Article · Mon Dec 31 23:00:00 EST 2007 · Nature Medicine · OSTI ID:960599

Rapid selection of escape mutants by the first CD8 T cell responses in acute HIV-1 infection

Journal Article · Mon Dec 31 23:00:00 EST 2007 · Nature Immunology · OSTI ID:960875

Effective Cytotoxic T Lymphocyte Targeting of Persistent HIV-1 during Antiretroviral Therapy Requires Priming of Naive CD8⁺ T Cells

Journal Article · Tue May 31 00:00:00 EDT 2016 · mBio (Online) · OSTI ID:1626106

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
HIV-1
SIV
T cells
cell death
cell motility
cytotoxic T cells
pathogen motility
secretion

Can Non-lytic CD8+ T Cells Drive HIV-1 Escape?

Citation Formats

References (112)

Cited By (4)

Similar Records

Related Subjects