The HIV coreceptor switch: a population dynamical perspective.

Over the course of infection, the coreceptor usage of the HIV virus changes from a preference for CCR5 to a preference for CXCR4 in approximately 50% of infected individuals. The change in coreceptor usage is the result of the complex interaction of the viral population with various cell populations of the immune system. Although many of the molecular processes involved in viral attachment and entry have been resolved, the population dynamical mechanisms leading to the emergence of CXCR4-using HIV variants in some infected individuals are not yet understood. Here, we review various hypotheses that have been proposed to explain the change of HIV coreceptor usage in the course of infection, and conclude that any corroboration or rejection of these hypotheses requires a quantitative analysis of the interaction between the virus and immune cells.

[1]  Kees,et al.  Macrophage-tropic variants initiate human immunodeficiency virus type 1 infection after sexual, parenteral, and vertical transmission. , 1994, The Journal of clinical investigation.

[2]  A. Rodrigo Dynamics of syncytium-inducing and non-syncytium-inducing type 1 human immunodeficiency viruses during primary infection. , 1997, AIDS research and human retroviruses.

[3]  Mario Roederer,et al.  T-Cell Subsets That Harbor Human Immunodeficiency Virus (HIV) In Vivo: Implications for HIV Pathogenesis , 2004, Journal of Virology.

[4]  P. Berman,et al.  Cryptic nature of envelope V3 region epitopes protects primary monocytotropic human immunodeficiency virus type 1 from antibody neutralization , 1994, Journal of virology.

[5]  J. Albert,et al.  Coreceptor usage of primary human immunodeficiency virus type 1 isolates varies according to biological phenotype , 1997, Journal of virology.

[6]  J. Goudsmit,et al.  Minimal requirements for the human immunodeficiency virus type 1 V3 domain to support the syncytium-inducing phenotype: analysis by single amino acid substitution , 1992, Journal of virology.

[7]  P. Simmonds,et al.  Determinants of HIV disease progression: six-year longitudinal study in the Edinburgh haemophilia/HIV cohort , 1991, The Lancet.

[8]  Richard A Koup,et al.  Homozygous Defect in HIV-1 Coreceptor Accounts for Resistance of Some Multiply-Exposed Individuals to HIV-1 Infection , 1996, Cell.

[9]  F Miedema,et al.  Interactions between HIV and the host immune system in the pathogenesis of AIDS. , 1990, AIDS.

[10]  H. Schuitemaker Macrophage‐tropic HIV‐1 variants: initiators of infection and AIDS pathogenesis? , 1994, Journal of leukocyte biology.

[11]  C. Kuiken,et al.  Syncytium-inducing (SI) phenotype suppression at seroconversion after intramuscular inoculation of a non-syncytium-inducing/SI phenotypically mixed human immunodeficiency virus population , 1995, Journal of virology.

[12]  B. Korber,et al.  A new classification for HIV-1 , 1998, Nature.

[13]  John P. Moore,et al.  Use of Inhibitors To Evaluate Coreceptor Usage by Simian and Simian/Human Immunodeficiency Viruses and Human Immunodeficiency Virus Type 2 in Primary Cells , 2000, Journal of Virology.

[14]  A. Trkola,et al.  Neutralization Sensitivity of Human Immunodeficiency Virus Type 1 Primary Isolates to Antibodies and CD4-Based Reagents Is Independent of Coreceptor Usage , 1998, Journal of Virology.

[15]  R. Koup,et al.  A 32-bp deletion within the CCR5 locus protects against transmission of parenterally acquired human immunodeficiency virus but does not affect progression to AIDS-defining illness. , 1998, The Journal of infectious diseases.

[16]  Cell turnover and cell tropism in HIV-1 infection. , 2002, Trends in microbiology.

[17]  R. Ahmed,et al.  Similarities and differences in CD4+ and CD8+ effector and memory T cell generation , 2003, Nature Immunology.

[18]  Alan S. Perelson,et al.  Quantitative Image Analysis of HIV-1 Infection in Lymphoid Tissue , 1996, Science.

[19]  F. Wolf,et al.  Low T-cell responsiveness to activation via CD3/TCR is a prognostic marker for acquired immunodeficiency syndrome (AIDS) in human immunodeficiency virus-1 (HIV-1)-infected men , 1990, Journal of Clinical Immunology.

[20]  T. Gojobori,et al.  Evolutionary mechanisms and population dynamics of the third variable envelope region of HIV within single hosts. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[21]  J. Margolick,et al.  Consistent Viral Evolutionary Changes Associated with the Progression of Human Immunodeficiency Virus Type 1 Infection , 1999, Journal of Virology.

[22]  E. Ebert,et al.  Constitutive expression of stromal derived factor-1 by mucosal epithelia and its role in HIV transmission and propagation , 2000, Current Biology.

[23]  H. Schuitemaker,et al.  In vivo HIV-1 infection of CD45RA(+)CD4(+) T cells is established primarily by syncytium-inducing variants and correlates with the rate of CD4(+) T cell decline. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[24]  C. Mackay,et al.  The HIV coreceptors CXCR4 and CCR5 are differentially expressed and regulated on human T lymphocytes. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[25]  M A Nowak,et al.  The effect of different immune responses on the evolution of virulent CXCR4–tropic HIV , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[26]  J. Kappes,et al.  Primary intestinal epithelial cells selectively transfer R5 HIV-1 to CCR5+ cells , 2002, Nature Medicine.

[27]  Martin A. Nowak,et al.  Causes of HIV diversity , 1995, Nature.

[28]  C. Cheng‐Mayer,et al.  CD8+ T cell-mediated CXC chemokine receptor 4-simian/human immunodeficiency virus suppression in dually infected rhesus macaques , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[29]  J. Reece,et al.  HIV-1 Selection by Epidermal Dendritic Cells during Transmission across Human Skin , 1998, The Journal of experimental medicine.

[30]  I. Keet,et al.  Prognostic Value of HIV-1 Syncytium-Inducing Phenotype for Rate of CD4+ Cell Depletion and Progression to AIDS , 1993, Annals of Internal Medicine.

[31]  J. Farber,et al.  Chemokine receptors as HIV-1 coreceptors: roles in viral entry, tropism, and disease. , 1999, Annual review of immunology.

[32]  J. Grivel,et al.  CCR5- and CXCR4-tropic HIV-1 are equally cytopathic for their T-cell targets in human lymphoid tissue , 1999, Nature Medicine.

[33]  D. Weissman,et al.  Quantification of CD4, CCR5, and CXCR4 levels on lymphocyte subsets, dendritic cells, and differentially conditioned monocyte-derived macrophages. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[34]  S. Spector,et al.  Virologic characterization of primary human immunodeficiency virus type 1 infection in a health care worker following needlestick injury. , 1995, The Journal of infectious diseases.

[35]  E. Holmes,et al.  On the origin and evolution of the human immunodeficiency virus (HIV) , 2001, Biological reviews of the Cambridge Philosophical Society.

[36]  J. Benito,et al.  Quantitative alterations of the functionally distinct subsets of CD4 and CD8 T lymphocytes in asymptomatic HIV infection: changes in the expression of CD45RO, CD45RA, CD11b, CD38, HLA-DR, and CD25 antigens. , 1997, Journal of acquired immune deficiency syndromes and human retrovirology : official publication of the International Retrovirology Association.

[37]  B. Levine,et al.  Differential regulation of HIV-1 fusion cofactor expression by CD28 costimulation of CD4+ T cells. , 1997, Science.

[38]  M. Carrington,et al.  HIV-1 Infection in Individuals With the CCR5-Δ32/Δ32 Genotype: Acquisition of Syncytium-Inducing Virus at Seroconversion , 2002 .

[39]  J. Albert,et al.  Dual effect of interleukin 4 on HIV-1 expression: implications for viral phenotypic switch and disease progression. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[40]  D. Richman,et al.  Sexual transmission and propagation of SIV and HIV in resting and activated CD4+ T cells. , 1999, Science.

[41]  H. Schuitemaker,et al.  Differential coreceptor expression allows for independent evolution of non-syncytium-inducing and syncytium-inducing HIV-1. , 2000, The Journal of clinical investigation.

[42]  H. Schuitemaker,et al.  Phenotype-associated sequence variation in the third variable domain of the human immunodeficiency virus type 1 gp120 molecule , 1992, Journal of virology.

[43]  A. Trkola,et al.  Co-receptors for HIV-1 entry. , 1997, Current opinion in immunology.

[44]  J. Mullins,et al.  Cytopathicity of Human Immunodeficiency Virus Type 1 Primary Isolates Depends on Coreceptor Usage and Not Patient Disease Status , 2001, Journal of Virology.

[45]  C. Cheng‐Mayer,et al.  Distinct pathogenic sequela in rhesus macaques infected with CCR5 or CXCR4 utilizing SHIVs. , 1999, Science.

[46]  H. Schuitemaker,et al.  CC chemokine receptor 5 cell-surface expression in relation to CC chemokine receptor 5 genotype and the clinical course of HIV-1 infection. , 1999, Journal of immunology.

[47]  M. Roederer,et al.  CD8 naive T cell counts decrease progressively in HIV-infected adults. , 1995, The Journal of clinical investigation.

[48]  B. Walker,et al.  Human Immunodeficiency Virus Type 1 Populations in Blood and Semen , 1998, Journal of Virology.

[49]  R. Steinman,et al.  Immature Dendritic Cells Selectively Replicate Macrophagetropic (M-Tropic) Human Immunodeficiency Virus Type 1, while Mature Cells Efficiently Transmit both M- and T-Tropic Virus to T Cells , 1998, Journal of Virology.

[50]  John P. Moore,et al.  AIDS vaccine models: Challenging challenge viruses , 2002, Nature Medicine.

[51]  L. M. Mansky,et al.  Lower in vivo mutation rate of human immunodeficiency virus type 1 than that predicted from the fidelity of purified reverse transcriptase , 1995, Journal of virology.

[52]  A. Perelson Modelling viral and immune system dynamics , 2002, Nature Reviews Immunology.

[53]  Donald E. Mosier,et al.  Intrinsic Obstacles to Human Immunodeficiency Virus Type 1 Coreceptor Switching , 2004, Journal of Virology.

[54]  F Miedema,et al.  T-cell division in human immunodeficiency virus (HIV)-1 infection is mainly due to immune activation: a longitudinal analysis in patients before and during highly active antiretroviral therapy (HAART). , 2000, Blood.

[55]  B. Chesebro,et al.  The Cell Tropism of Human Immunodeficiency Virus Type 1 Determines the Kinetics of Plasma Viremia in SCID Mice Reconstituted with Human Peripheral Blood Leukocytes , 1998, Journal of Virology.

[56]  A. Lackner,et al.  The mucosal immune system and HIV-1 infection. , 2003, AIDS reviews.

[57]  M. L. Penn,et al.  CXCR4 utilization is sufficient to trigger CD4+ T cell depletion in HIV-1-infected human lymphoid tissue. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[58]  M A Nowak,et al.  Dynamics of macrophage and T cell infection by HIV. , 1999, Journal of theoretical biology.

[59]  J. Zimmerberg,et al.  Infection of human tonsil histocultures: A model for HIV pathogenesis , 1995, Nature Medicine.

[60]  R. V. van Lier,et al.  AIDS pathogenesis: a dynamic interaction between HIV and the immune system. , 1990, Immunology today.

[61]  M. Ostrowski,et al.  Expression of chemokine receptors CXCR4 and CCR5 in HIV-1-infected and uninfected individuals. , 1998, Journal of immunology.

[62]  J. Margolick,et al.  Improved Coreceptor Usage Prediction and GenotypicMonitoring of R5-to-X4 Transition by Motif Analysis of HumanImmunodeficiency Virus Type 1 env V3 LoopSequences , 2003, Journal of Virology.

[63]  M A Nowak,et al.  Virus phenotype switching and disease progression in HIV‐1 infection , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.