David H O'Connor

University of Wisconsin–Madison, Madison, Wisconsin, United States

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Publications (143)804.34 Total impact

  • [Show abstract] [Hide abstract]
    ABSTRACT: Deletion of Gly-720 and Tyr-721 from a highly conserved GYxxØ trafficking signal in the SIVmac239 envelope glycoprotein cytoplasmic domain, producing a virus termed ΔGY, leads to a striking perturbation in pathogenesis in rhesus macaques (M. mulatta). Infected macaques develop immune activation and progress to AIDS, but with only limited and transient infection of intestinal CD4(+) T cells and an absence of microbial translocation. Here we evaluated ΔGY in pig-tailed macaques (M. nemestrina), a species in which SIVmac239 infection typically leads to increased immune activation and more rapid progression to AIDS than in rhesus macaques. In pig-tailed macaques ΔGY also replicated acutely to high peak plasma RNA levels identical to SIVmac239, and caused only transient infection of CD4(+) T cells in the gut lamina propria and no microbial translocation. However, in marked contrast to rhesus macaques, 19 of 21 pig-tailed macaques controlled ΔGY replication with plasma viral loads of <15-50 RNA copies/ml. CD4(+) T cells were preserved in blood and gut for up to 100 weeks with no immune activation or disease progression. Robust, anti-viral CD4(+) T cell responses were seen, particularly in the gut. Anti-CD8 antibody depletion demonstrated CD8(+) cellular control of viral replication. Two pig-tailed macaques progressed to disease with persisting viremia and possible compensatory mutations in the cytoplasmic tail. These studies demonstrate a marked perturbation in pathogenesis caused by ΔGY's ablation of the GYxxØ trafficking motif and reveal, paradoxically, that viral control is enhanced in a macaque species typically predisposed to more pathogenic manifestations of SIV infection. Pathogenesis of human (HIV) and simian (SIV) immunodeficiency viruses reflects a balance between viral replication host innate and adaptive anti-viral immune responses, and sustained immune activation that in humans and Asian macaques is associated with persistent viremia, immune escape and AIDS. Among nonhuman primates, pig-tailed macaques following SIV infection are predisposed to more rapid disease progression than are rhesus macaques. Here, we show that disruption of a conserved tyrosine-based cellular trafficking motif in the viral transmembrane envelope glycoprotein cytoplasmic tail leads in pig-tailed macaques to a unique phenotype in which high levels of acute viral replication are followed by elite control, robust cellular responses in mucosal tissues, and no disease. Paradoxically, control of this virus in rhesus macaques is only partial, and progression to AIDS occurs. This novel model should provide a powerful tool to help identify host-specific determinants for viral control with potential relevance for vaccine development. Copyright © 2015, American Society for Microbiology. All Rights Reserved.
    Journal of Virology 07/2015; DOI:10.1128/JVI.01134-15 · 4.65 Impact Factor
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    ABSTRACT: CD8 T cells play a crucial role in the control of human immunodeficiency virus (HIV) and simian immunodeficiency virus (SIV). However, the specific qualities and characteristics of an effective CD8 T cell response remain unclear. Although targeting breadth, cross-reactivity, polyfunctionality, avidity, and specificity are correlated with HIV control, further investigation is needed to determine the precise contributions of these various attributes to CD8 T cell efficacy. We developed protocols for isolating and expanding SIV-specific CD8 T cells from SIV-naïve Mauritian cynomolgus macaques (MCM). These cells exhibited an effector memory phenotype, produced cytokines in response to cognate antigen, and suppressed viral replication in vitro. We further cultured cell lines specific for four SIV-derived epitopes: Nef 103-111 RM9, Gag 389-394 GW9, Env 338-346 RF9, and Nef 254-262 LT9. These lines were up to 94.4% pure as determined by MHC-tetramer analysis. After autologous transfer into two MCM recipients, expanded CD8 T cells persisted in peripheral blood and lung tissue for at least 24 weeks, and trafficked to multiple extra-lymphoid tissues. However, these cells did not impact acute phase SIV load after challenge compared to historic controls. The expansion and autologous transfer of SIV-specific T cells into naïve animals provides a unique model for exploring cellular immunity and the control of SIV infection, and facilitates a systematic evaluation of therapeutic adoptive transfer strategies for eradication of the latent reservoir. CD8 T cells play a crucial role in the control of human immunodeficiency virus (HIV) and simian immunodeficiency virus (SIV). Autologous adoptive transfer studies followed by SIV challenge may help define the critical elements of an effective T cell response to HIV and SIV infection. We developed protocols for isolating and expanding SIV-specific CD8 T cells from SIV-naïve Mauritian cynomolgus macaques. This is an important first step toward the development of autologous transfer strategies to explore cellular immunity and potential therapeutic applications in the SIV model. Copyright © 2015, American Society for Microbiology. All Rights Reserved.
    Journal of Virology 07/2015; DOI:10.1128/JVI.00993-15 · 4.65 Impact Factor
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    ABSTRACT: The advent of Next Generation Sequencing (NGS) has created unprecedented opportunities to examine viral populations within individual hosts, among infected individuals, and over time. Comparing sequence variability across viral genomes allows for the construction of complex population structures, the analysis of which can yield powerful biological insights. However, the simultaneous display of sequence variation, coverage depth, and quality scores across thousands of bases presents a unique visualization challenge that has not been fully met by current NGS analysis tools. Here, we present LayerCake, a self-contained visualization tool that allows for the rapid analysis of variation in viral NGS data. LayerCake enables the user to simultaneously visualize variations in multiple viral populations across entire genomes within a highly customizable framework, drawing attention to pertinent and interesting patterns of variation. We have successfully deployed LayerCake to assist with a variety of different genomics datasets. Program downloads and detailed instructions are available at http://graphics.cs.wisc.edu/WP/layercake under a modified MIT license. LayerCake is a cross-platform tool written in the Processing framework for Java. mcorrell@cs.wisc.edu. © The Author (2015). Published by Oxford University Press. All rights reserved. For Permissions, please email: journals.permissions@oup.com.
    Bioinformatics 07/2015; DOI:10.1093/bioinformatics/btv407 · 4.62 Impact Factor
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    ABSTRACT: Although immune pressure exerted by MHC class I-restricted cytotoxic T lymphocytes (CTL) are an important determinant of outcome in pathogenic HIV and SIV infection, lack of data on MHC class I genes has hampered study of its role in natural hosts with nonpathogenic SIV infection. In this study, we cloned and characterized full-length MHC class I genes derived from the cDNA library of two unrelated naturally infected sooty mangabeys (Cercocebus atys) in whom SIV-specific CTL epitopes were previously mapped. Twenty one full-length MHC class I alleles consisting of five MHC-A (Ceat-A), 13 MHC-B (Ceat-B), and three MHC-E (Ceat-E) alleles were identified. Sequence-specific primers (SSP) for high-throughput screening of genomic DNA by PCR were developed for 16 of the 18 Ceat-A and Ceat-B alleles. Screening of 62 SIV-negative and 123 SIV-infected sooty mangabeys at the Yerkes National Primate Research Center (YNPRC) revealed the presence of up to four MHC-A and eight MHC-B alleles in individual mangabeys, indicating that similar to macaque species, mangabeys have at least two duplications of the MHC-A locus and four duplications of the MHC-B locus in the absence of an MHC-C locus. Using stable transfectants of Ceat MHC Class I alleles in the MHC-null 721.221 cell line, we identified Ceat-B*12:01 as the restricting allele of a previously reported Nef20-28 CTL epitope. Ceat-B*1201/Nef20-28 tetramers identified tetramer-positive CD8+ T lymphocytes in Ceat-B*1201-positive SIV-infected mangabeys. This study has laid the groundwork for comprehensive analysis of CTL and SIV evolution in a natural host of SIV infection.
    Immunogenetics 07/2015; 67(8). DOI:10.1007/s00251-015-0853-2 · 2.49 Impact Factor
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    ABSTRACT: Single-molecule real-time (SMRT) sequencing technology with the Pacific Biosciences (PacBio) RS II platform offers the potential to obtain full-length coding regions (∼1,100-bp) from MHC class I cDNAs. Despite the relatively high error rate associated with SMRT technology, high quality sequences can be obtained by circular consensus sequencing (CCS) due to the random nature of the error profile. In the present study we first validated the ability of SMRT-CCS to accurately identify class I transcripts in Mauritian-origin cynomolgus macaques (Macaca fascicularis) that have been characterized previously by cloning and Sanger-based sequencing as well as pyrosequencing approaches. We then applied this SMRT-CCS method to characterize 60 novel full-length class I transcript sequences expressed by a cohort of cynomolgus macaques from China. The SMRT-CCS method described here provides a straightforward protocol for characterization of unfragmented single-molecule cDNA transcripts that will potentially revolutionize MHC class I allele discovery in nonhuman primates and other species. Published by Elsevier Inc.
    Human immunology 05/2015; DOI:10.1016/j.humimm.2015.03.022 · 2.28 Impact Factor
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    ABSTRACT: Sooty mangabeys (Cercocebus atys) are natural SIV hosts and the presumed source of HIV-2 and SIVmac, which makes them a valuable model for HIV/SIV research. However, like other African primates, little is known about their major histocompatibility complex (MHC) genetics. In this study, we used Roche/454 and Illumina MiSeq deep sequencing in order to determine the MHC class I transcripts in a cohort of 165 sooty mangabeys from the Yerkes National Primate Research Center (YNPRC). We have characterized 121 functionally full-length classical (Ceat-A and Ceat-B) and non-classical (Ceat-F and Ceat-I) alleles and have also identified 22 Ceat-A/Ceat-B haplotype chromosomal combinations. We correlated these Ceat-A/Ceat-B haplotype combinations to recently described microsatellite haplotypes from the YNPRC colony. These newly identified alleles and haplotypes establish a resource for studying cellular immunity in sooty mangabeys and provide a framework for rapidly cataloging MHC class I sequences in an understudied, yet important, nonhuman primate species.
    Immunogenetics 05/2015; 67(8). DOI:10.1007/s00251-015-0847-0 · 2.49 Impact Factor
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    ABSTRACT: In 49 patients with known Ebolavirus (EBOV) outcomes during the ongoing outbreak in Sierra Leone, 13 were co-infected with the immunomodulatory pegivirus GB virus C (GBV-C). 53% of these GBV-C+ patients survived; in contrast, only 22% of GBV-C(-) patients survived. Both survival and GBV-C status were associated with age, with older patients having lower survival rates and intermediate-age patients (21-45 years) having the highest rate of GBV-C infection. Understanding the separate and combined effects of GBV-C and age on EBOV survival could lead to new treatment and prevention strategies, perhaps through age-related pathways of immune activation. Copyright © 2014, American Society for Microbiology. All Rights Reserved.
    Journal of Virology 12/2014; 89(4). DOI:10.1128/JVI.02752-14 · 4.65 Impact Factor
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    ABSTRACT: A small percentage of human immunodeficiency virus (HIV)-infected people and simian immunodeficiency virus (SIV)-infected macaques control virus replication without antiretroviral treatment. The major determinant of this control is host expression of certain major histocompatibility complex alleles. However, this association is incompletely penetrant, suggesting that additional loci modify the major histocompatibility complex's protective effect. Here, to identify candidate control-modifying loci, we sequence the genomes of 12 SIV-infected Mauritian cynomolgus macaques that experienced divergent viral load set points despite sharing the protective M1 major histocompatibility complex haplotype. Our genome-wide analysis of haplotype-level variation identifies seven candidate control-modifying loci on chromosomes 2, 3, 7, 8, 9, 10, and 14. The highest variant density marks the candidate on chromosome 7, which is the only control-modifying locus to comprise genes with known immunological function. Upon closer inspection, we found an allele for one of these genes, granzyme B, to be enriched in M1(+) controllers. Given its established role as a cytotoxic effector molecule that participates in CD8-mediated killing of virus-infected cells, we test the role of variation within gzmb in modifying SIV control by prospectively challenging M1(+) granzyme B-defined macaques. Our study establishes a framework for using whole genome sequencing to identify haplotypes that may contribute to complex clinical phenotypes. Further investigation into the immunogenetics underlying spontaneous HIV control may contribute to the rational design of a vaccine that prevents acquired immune deficiency syndrome.
    Genome Biology 11/2014; 15(11):478. DOI:10.1186/s13059-014-0478-z · 10.47 Impact Factor
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    ABSTRACT: Simian hemorrhagic fever virus (SHFV) causes a severe and almost uniformly fatal viral hemorrhagic fever in Asian macaques, but is thought to be nonpathogenic for humans. To date, the SHFV lifecycle is almost completely uncharacterized on the molecular level. Here we describe the first steps of the SHFV lifecycle. Our experiments indicate that SHFV enters target cells by low pH-dependent endocytosis. Dynamin inhibitors, chlorpromazine, methyl-β-cyclodextrin, chloroquine, and concanamycin A dramatically reduced SHFV entry efficiency, whereas the macropinocytosis inhibitors EIPA, blebbistatin, and wortmannin, and the caveolin-mediated endocytosis inhibitors nystatin and filipin III had no effect. Furthermore, overexpression and knock-out study and electron-microscopy results indicate that SHFV entry occurs by a dynamin-dependent clathrin-mediated endocytosis-like pathway. Experiments utilizing latrunculin B, cytochalasin B, and cytochalasin D indicate that SHFV does not hijack the actin polymerization pathway. Treatment of target cells with proteases (proteinase K, papain, α-chymotrypsin, trypsin) abrogated entry, indicating that the SHFV cell-surface receptor is a protein. Phospholipases A2 and D had no effect on SHFV entry. Finally, treatment of cells with antibodies targeting CD163, a cell surface molecule identified as an entry factor for the SHFV-related porcine reproductive and respiratory syndrome virus, diminished SHFV replication, identifying CD163 as an important SHFV entry component.
    Journal of Virology 10/2014; 89(1). DOI:10.1128/JVI.02697-14 · 4.65 Impact Factor
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    ABSTRACT: Simian hemorrhagic fever virus (SHFV) variant NIH LVR42-0/M6941 is the only remaining SHFV in culture, and only a single genome sequence record exists in GenBank/RefSeq. We compared the genomic sequence of NIH LVR42-0/M6941 acquired from the ATCC in 2011 to NIH LVR42-0/M6941 genomes sequenced directly from nonhuman primates experimentally infected in 1989.
    Genome Announcements 10/2014; 2(5). DOI:10.1128/genomeA.00978-14
  • AIDS Research and Human Retroviruses 10/2014; 30 Suppl 1(S1):A41. DOI:10.1089/aid.2014.5067.abstract · 2.46 Impact Factor
  • Journal of Medical Primatology 10/2014; 43(5):391-391. · 0.89 Impact Factor
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    ABSTRACT: The influence of MHC-I alleles on HIV diversity has been well characterised in humans at the population level. MHC-I alleles likely affect viral diversity in the SIV-infected pig-tailed macaque (M. nemestrina) model, but this is poorly characterised. We studied the evolution of SIV in pig-tailed macaques with a range of MHC-I haplotypes. SIVmac251 genomes were amplified from the plasma of 44 pig-tailed macaques infected with SIVmac251 at 4-10 months after infection and characterized by Illumina deep sequencing. MHC-I typing was performed on cellular RNA using Roche/454 pyrosequencing. MHC-I haplotypes and viral sequence polymorphisms were linked using in-house bioinformatics pipelines, both at individual mutations and groups of mutations spanning 10 amino acid segments, since CTL escape can occur at different amino acids within the same epitope in different animals. The approach successfully identified 6 known CTL escape mutations within 3 Mane-A1*084-restricted epitopes. The approach also identified over 70 new SIV polymorphisms linked to a variety of MHC-I haplotypes. Using functional CD8 T cell assays we confirmed that one of these associations, a Mane-B028 haplotype-linked mutation in Nef, corresponded to a CTL epitope. We also identified mutations associated with the Mane-B017 haplotype that were previously described as CTL epitopes restricted by Mamu-B*017:01 in rhesus macaques. This detailed study of pig-tailed macaque MHC-I genetics and SIV polymorphisms will enable a refined level of analysis for future vaccine design and treatment strategies for HIV.
    Journal of Virology 10/2014; DOI:10.1128/JVI.02428-14 · 4.65 Impact Factor
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    ABSTRACT: Since the 1960s, simian hemorrhagic fever virus (SHFV; Nidovirales; Arteriviridae) has caused highly fatal outbreaks of viral hemorrhagic fever in captive Asian macaque colonies. However, the source(s) of these outbreaks and the natural reservoir(s) of this virus remain obscure. Here we report the identification of two novel, highly divergent simian arteriviruses related to SHFV - Mikumi yellow baboon virus 1 (MYBV-1) and Southwest baboon virus 1 (SWBV-1) - in wild and captive baboons, respectively, and demonstrate recent transmission of SWBV-1 among captive baboons. These findings extend our knowledge of the genetic and geographic diversity of the simian arteriviruses, identify baboons as a natural host of these viruses, and provide further evidence that baboons may have played a role in previous outbreaks of simian hemorrhagic fever in macaques, as has long been suspected. This knowledge should aid in the prevention of disease outbreaks in captive macaques and supports the growing body of evidence that suggests simian arterivirus infections are common in Old World monkeys of many different species throughout Africa.
    Journal of Virology 09/2014; 88(22). DOI:10.1128/JVI.02203-14 · 4.65 Impact Factor
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    ABSTRACT: Pig-tailed macaques (Macaca nemestrina) serve as important models for human infectious disease research. Major histocompatibility complex (MHC) class II molecules are important to this research since they present peptides to CD4+ T cells. Despite the importance of characterizing the MHC-II alleles expressed in model species like pig-tailed macaques, to date, less than 150 MHC-II alleles have been named for the six most common classical class II loci (DRA, DRB, DQA, DQB, DPA, and DPB) in this population. Additionally, only a small percentage of these alleles are full-length, making it impossible to use the known sequence for reagent development. To address this, we developed a fast, high-throughput method to discover full-length MHC-II alleles and used it to characterize alleles in 32 pig-tailed macaques. By this method, we identified 128 total alleles across all six loci. We also performed an exon 2-based genotyping assay to validate the full-length sequencing results; this genotyping assay could be optimized for use in determining MHC-II allele frequencies in large cohorts of pig-tailed macaques.
    Immunogenetics 08/2014; 66(11). DOI:10.1007/s00251-014-0797-y · 2.49 Impact Factor
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    ABSTRACT: Within the Flaviviridae, the recently designated genus Pegivirus has expanded greatly due to new discoveries in bats, horses, and rodents. Here we report the discovery and characterization of three simian pegiviruses (SPgV) that resemble human pegivirus (HPgV) and infect red colobus monkeys (Procolobus tephrosceles), red-tailed guenons (Cercopithecus ascanius) and an olive baboon (Papio anubis). We have designated these viruses SPgVkrc, SPgVkrtg and SPgVkbab, reflecting their host species' common names, which include reference to their location of origin in Kibale National Park, Uganda. SPgVkrc and SPgVkrtg were detected in 47% (28/60) of red colobus and 42% (5/12) red-tailed guenons, respectively, while SPgVkbab infection was observed in 1 of 23 olive baboons tested. Infections were not associated with any apparent disease, despite the generally high viral loads observed for each variant. These viruses were monophyletic and equally divergent from HPgV and pegiviruses previously identified in chimpanzees (SPgVcpz). Overall, the high degree of conservation of genetic features among the novel SPgVs, HPgV and SPgVcpz suggests conservation of function among these closely related viruses. Our study describes the first primate pegiviruses detected in Old World monkeys, expanding the known genetic diversity and host range of pegiviruses and providing insight into the natural history of this genus.
    PLoS ONE 06/2014; 9(6):e98569. DOI:10.1371/journal.pone.0098569 · 3.23 Impact Factor
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    ABSTRACT: Key biological properties such as high genetic diversity and high evolutionary rate enhance the potential of certain RNA viruses to adapt and emerge. Identifying viruses with these properties in their natural hosts could dramatically improve disease forecasting and surveillance. Recently, we discovered two novel members of the viral family Arteriviridae: simian hemorrhagic fever virus (SHFV)-krc1 and SHFV-krc2, infecting a single wild red colobus (Procolobus rufomitratus tephrosceles) in Kibale National Park, Uganda. Nearly nothing is known about the biological properties of SHFVs in nature, although the SHFV type strain, SHFV-LVR, has caused devastating outbreaks of viral hemorrhagic fever in captive macaques. Here we detected SHFV-krc1 and SHFV-krc2 in 40% and 47% of 60 wild red colobus tested, respectively. We found viral loads in excess of 106-107 RNA copies per milliliter of blood plasma for each of these viruses. SHFV-krc1 and SHFV-krc2 also showed high genetic diversity at both the inter- and intra-host levels. Analyses of synonymous and non-synonymous nucleotide diversity across viral genomes revealed patterns suggestive of positive selection in SHFV open reading frames (ORF) 5 (SHFV-krc2 only) and 7 (SHFV-krc1 and SHFV-krc2). Thus, these viruses share several important properties with some of the most rapidly evolving, emergent RNA viruses.
    PLoS ONE 03/2014; 9(3):e90714. DOI:10.1371/journal.pone.0090714 · 3.23 Impact Factor
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    ABSTRACT: The identification of MHC class I ligands for rhesus macaque killer cell Ig-like receptors (KIRs) is fundamental to our basic understanding of KIR and MHC class I coevolution and to the study of NK cell responses in this nonhuman primate model for AIDS and other viral diseases. In this study, we show that Mamu-KIR3DL01, which is expressed by ∼90% of rhesus macaques, recognizes MHC class I molecules with a Bw4 motif. Primary NK cells expressing Mamu-KIR3DL01 were identified by staining with a mAb which, in this study, was shown to bind Mamu-KIR3DL01 allotypes with an aspartic acid at position 233. The cytolytic activity of Mamu-KIR3DL01(+) NK cells was suppressed by cell lines expressing the Bw4 molecules Mamu-B*007:01, -B*041:01, -B*058:02, and -B*065:01. The Bw4 motif was necessary for Mamu-KIR3DL01 recognition because substitutions in this region abrogated Mamu-KIR3DL01(+) NK cell inhibition. However, the presence of a Bw4 motif was not sufficient for recognition because another Bw4 molecule, Mamu-B*017:01, failed to suppress the cytolytic activity of these NK cells. Replacement of three residues in Mamu-B*017:01, predicted to be KIR contacts based on the three-dimensional structure of the human KIR3DL1-HLA-Bw4 complex, with the corresponding residues at these positions for the other Mamu-Bw4 ligands restored Mamu-KIR3DL01(+) NK cell inhibition. These results define the ligand specificity of one of the most polymorphic and commonly expressed KIRs in the rhesus macaque and reveal similarities in Bw4 recognition by Mamu-KIR3DL01 and human KIR3DL1, despite the absence of an orthologous relationship between these two KIRs or conservation of surface residues predicted to interact with MHC class I ligands.
    The Journal of Immunology 01/2014; 192(4). DOI:10.4049/jimmunol.1302883 · 5.36 Impact Factor
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    ABSTRACT: A captive juvenile Bornean orangutan (Pongo pygmaeus) died from an unknown disseminated parasitic infection. Deep sequencing of DNA from infected tissues, followed by gene-specific PCR and sequencing, revealed a divergent species within the newly proposed genus Versteria (Cestoda: Taeniidae). Versteria may represent a previously unrecognized risk to primate health.
    Emerging Infectious Diseases 01/2014; 20(1):109-13. DOI:10.3201/eid2001.131191 · 7.33 Impact Factor
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    ABSTRACT: Compensatory mutations offset fitness defects resulting from CD8+ T lymphocyte (CD8TL)-mediated escape, but their impact on viral evolution following transmission to naïve hosts remains unclear. Here, we investigated the reversion kinetics of Gag181-189CM9 CD8TL escape-associated compensatory mutations in SIV-infected macaques. Pre-existing compensatory mutations did not result in acute-phase escape and instead required a tertiary mutation for stabilization in the absence of Gag181-189CM9 escape mutations. Therefore, transmitted compensatory mutations do not necessarily predict rapid CD8TL escape.
    Journal of Virology 12/2013; DOI:10.1128/JVI.03304-13 · 4.65 Impact Factor

Publication Stats

6k Citations
804.34 Total Impact Points

Institutions

  • 2000–2015
    • University of Wisconsin–Madison
      • • Department of Pathology and Laboratory Medicine
      • • Department of Plant Pathology
      • • Wisconsin National Primate Research Center
      Madison, Wisconsin, United States
  • 1999–2014
    • Wisconsin National Primate Research Center
      Madison, Wisconsin, United States
  • 2013
    • McGill University
      • Department of Biology
      Montréal, Quebec, Canada
  • 2008
    • National Institutes of Health
      • Branch of Vaccine
      Bethesda, MD, United States
  • 2003
    • University of Alabama at Birmingham
      Birmingham, Alabama, United States