Macaque Long-Term Nonprogressors Resist Superinfection with Multiple CD8+ T Cell Escape Variants of Simian Immunodeficiency Virus
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| Published in | Journal of Virology Vol. 85; no. 1; pp. 530 - 541 |
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01.01.2011
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ABSTRACT Human immunodeficiency virus (HIV)-positive individuals can be superinfected with different virus strains. Individuals who control an initial HIV infection are therefore still at risk for subsequent infection with divergent viruses, but the barriers to such superinfection remain unclear. Here we tested long-term nonprogressors' (LTNPs') susceptibility to superinfection using Indian rhesus macaques that express the major histocompatibility complex class I (MHC-I) allele Mamu-B*17 , which is associated with control of the pathogenic AIDS virus SIVmac239. The Mamu-B*17-restricted CD8 + T cell repertoire is focused almost entirely on 5 epitopes. We engineered a series of SIVmac239 variants bearing mutations in 3, 4, or all 5 of these epitopes and used them to serially challenge 2 Mamu-B*17- positive LTNPs. None of the escape variants caused breakthrough replication in LTNPs, although they readily infected Mamu-B*17- negative naive macaques. In vitro competing coculture assays and examination of viral evolution in hosts lacking Mamu-B*17 suggested that the mutant viruses had negligible defects in replicative fitness. Both LTNPs maintained robust immune responses, including simian immunodeficiency virus (SIV)-specific CD8 + and CD4 + T cells and neutralizing antibodies. Our results suggest that escape mutations in epitopes bound by “protective” MHC-I molecules may not be sufficient to establish superinfection in LTNPs. Human immunodeficiency virus (HIV)-positive individuals can be superinfected with different virus strains. Individuals who control an initial HIV infection are therefore still at risk for subsequent infection with divergent viruses, but the barriers to such superinfection remain unclear. Here we tested long-term nonprogressors' (LTNPs') susceptibility to superinfection using Indian rhesus macaques that express the major histocompatibility complex class I (MHC-I) allele Mamu-B 17, which is associated with control of the pathogenic AIDS virus SIVmac239. The Mamu-B 17-restricted CD8(+) T cell repertoire is focused almost entirely on 5 epitopes. We engineered a series of SIVmac239 variants bearing mutations in 3, 4, or all 5 of these epitopes and used them to serially challenge 2 Mamu-B 17-positive LTNPs. None of the escape variants caused breakthrough replication in LTNPs, although they readily infected Mamu-B 17-negative naive macaques. In vitro competing coculture assays and examination of viral evolution in hosts lacking Mamu-B 17 suggested that the mutant viruses had negligible defects in replicative fitness. Both LTNPs maintained robust immune responses, including simian immunodeficiency virus (SIV)-specific CD8(+) and CD4(+) T cells and neutralizing antibodies. Our results suggest that escape mutations in epitopes bound by "protective" MHC-I molecules may not be sufficient to establish superinfection in LTNPs. Human immunodeficiency virus (HIV)-positive individuals can be superinfected with different virus strains. Individuals who control an initial HIV infection are therefore still at risk for subsequent infection with divergent viruses, but the barriers to such superinfection remain unclear. Here we tested long-term nonprogressors' (LTNPs') susceptibility to superinfection using Indian rhesus macaques that express the major histocompatibility complex class I (MHC-I) allele Mamu-B*17 , which is associated with control of the pathogenic AIDS virus SIVmac239. The Mamu-B*17-restricted CD8 + T cell repertoire is focused almost entirely on 5 epitopes. We engineered a series of SIVmac239 variants bearing mutations in 3, 4, or all 5 of these epitopes and used them to serially challenge 2 Mamu-B*17- positive LTNPs. None of the escape variants caused breakthrough replication in LTNPs, although they readily infected Mamu-B*17- negative naive macaques. In vitro competing coculture assays and examination of viral evolution in hosts lacking Mamu-B*17 suggested that the mutant viruses had negligible defects in replicative fitness. Both LTNPs maintained robust immune responses, including simian immunodeficiency virus (SIV)-specific CD8 + and CD4 + T cells and neutralizing antibodies. Our results suggest that escape mutations in epitopes bound by “protective” MHC-I molecules may not be sufficient to establish superinfection in LTNPs. Human immunodeficiency virus (HIV)-positive individuals can be superinfected with different virus strains. Individuals who control an initial HIV infection are therefore still at risk for subsequent infection with divergent viruses, but the barriers to such superinfection remain unclear. Here we tested long-term nonprogressors' (LTNPs') susceptibility to superinfection using Indian rhesus macaques that express the major histocompatibility complex class I (MHC-I) allele Mamu-B*17, which is associated with control of the pathogenic AIDS virus SIVmac239. The Mamu-B*17-restricted CD8+ T cell repertoire is focused almost entirely on 5 epitopes. We engineered a series of SIVmac239 variants bearing mutations in 3, 4, or all 5 of these epitopes and used them to serially challenge 2 Mamu-B*17-positive LTNPs. None of the escape variants caused breakthrough replication in LTNPs, although they readily infected Mamu-B*17-negative naive macaques. In vitro competing coculture assays and examination of viral evolution in hosts lacking Mamu-B*17 suggested that the mutant viruses had negligible defects in replicative fitness. Both LTNPs maintained robust immune responses, including simian immunodeficiency virus (SIV)-specific CD8+ and CD4+ T cells and neutralizing antibodies. Our results suggest that escape mutations in epitopes bound by QUOTATION_MARKprotectiveQUOTATION_MARK MHC-I molecules may not be sufficient to establish superinfection in LTNPs. |
| Author | Jessica Furlott Eva G. Rakasz Nancy A. Wilson Caitlin E. MacNair Thomas C. Friedrich Shari M. Piaskowski Kim Weisgrau Ann J. Hessell Enrique J. León Jason Reed Taeko Soma Jason T. Weinfurter Gemma E. May Dennis R. Burton Nicholas J. Maness |
| AuthorAffiliation | Department of Pathobiological Sciences, University of Wisconsin School of Veterinary Medicine, Madison, Wisconsin 53706, 1 Wisconsin National Primate Research Center, Madison, Wisconsin 53715, 2 Department of Immunology and Microbial Science and International AIDS Vaccine Initiative Neutralizing Antibody Center, The Scripps Research Institute, La Jolla, California 92037, 3 Department of Pathology and Laboratory Medicine, University of Wisconsin School of Medicine and Public Health, Madison, Wisconsin 53706, 4 Ragon Institute of Massachusetts General Hospital, Massachusetts Institute of Technology and Harvard University, Boston, Massachusetts 02114 5 |
| AuthorAffiliation_xml | – name: Department of Pathobiological Sciences, University of Wisconsin School of Veterinary Medicine, Madison, Wisconsin 53706, 1 Wisconsin National Primate Research Center, Madison, Wisconsin 53715, 2 Department of Immunology and Microbial Science and International AIDS Vaccine Initiative Neutralizing Antibody Center, The Scripps Research Institute, La Jolla, California 92037, 3 Department of Pathology and Laboratory Medicine, University of Wisconsin School of Medicine and Public Health, Madison, Wisconsin 53706, 4 Ragon Institute of Massachusetts General Hospital, Massachusetts Institute of Technology and Harvard University, Boston, Massachusetts 02114 5 |
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Mendeley... Human immunodeficiency virus (HIV)-positive individuals can be superinfected with different virus strains. Individuals who control an initial HIV infection are... ABSTRACT Human immunodeficiency virus (HIV)-positive individuals can be superinfected with different virus strains. Individuals who control an initial HIV... |
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| SubjectTerms | Amino Acid Sequence Animals Biological and medical sciences CD8-Positive T-Lymphocytes - immunology CD8-Positive T-Lymphocytes - virology Epitopes, T-Lymphocyte - chemistry Epitopes, T-Lymphocyte - genetics Fundamental and applied biological sciences. Psychology Histocompatibility Antigens Class I - genetics Histocompatibility Antigens Class I - metabolism HIV Long-Term Survivors Human immunodeficiency virus Macaca mulatta Macaca mulatta - immunology Macaca mulatta - virology Microbiology Miscellaneous Molecular Sequence Data Mutation Pathogenesis and Immunity Simian Acquired Immunodeficiency Syndrome - immunology Simian Acquired Immunodeficiency Syndrome - virology Simian immunodeficiency virus Simian Immunodeficiency Virus - classification Simian Immunodeficiency Virus - genetics Simian Immunodeficiency Virus - immunology Simian Immunodeficiency Virus - physiology Superinfection - immunology Superinfection - virology Virology |
| Title | Macaque Long-Term Nonprogressors Resist Superinfection with Multiple CD8+ T Cell Escape Variants of Simian Immunodeficiency Virus |
| URI | http://jvi.asm.org/content/85/1/530.abstract https://www.ncbi.nlm.nih.gov/pubmed/20962091 https://search.proquest.com/docview/821598072 https://search.proquest.com/docview/856761838 https://search.proquest.com/docview/856772995 https://pubmed.ncbi.nlm.nih.gov/PMC3014170 |
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