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Title: High Multiplicity Infection by HIV-1 in Men Who Have Sex with Men

Journal Article · · PLoS Pathogens
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  1. Univ. of Alabama, Birmingham, AL (United States). Dept. of Medicine; DOE/OSTI
  2. Univ. of Alabama, Birmingham, AL (United States). Dept. of Medicine
  3. Univ. of Alabama, Birmingham, AL (United States). Dept. of Biostatistics
  4. Los Alamos National Lab. (LANL), Los Alamos, NM (United States). Theoretical Biology and Biophysics
  5. Los Alamos National Lab. (LANL), Los Alamos, NM (United States). Theoretical Biology and Biophysics; Univ. of Massachusetts, Amherst, MA (United States). Dept. of Mathematics and Statistics
  6. Los Alamos National Lab. (LANL), Los Alamos, NM (United States). Nuclear and partical Physics, Astrophysics and Cosmology; Santa Fe Inst. (SFI), Santa Fe, NM (United States)
  7. Los Alamos National Lab. (LANL), Los Alamos, NM (United States). Theoretical Biology and Biophysics; Santa Fe Inst. (SFI), Santa Fe, NM (United States)
  8. Univ. of North Carolina, Chapel Hill, NC (United States). Dept. of Medicine
  9. Duke Univ., Durham, NC (United States). Dept. of Medicine
  10. Aaron Diamond AIDS Research Center, New York, NY (United States); Rockefeller Univ., New York, NY (United States)
  11. National Cancer Inst., Frederick, MD (United States). SAIC-Frederick
  12. Univ. of Alabama, Birmingham, AL (United States). Dept. of Medicine; Univ. of Alabama, Birmingham, AL (United States). Dept. of Microbiology
+ Show Author Affiliations

Elucidating virus-host interactions responsible for HIV-1 transmission is important for advancing HIV-1 prevention strategies. To this end, single genome amplification (SGA) and sequencing of HIV-1 within the context of a model of random virus evolution has made possible for the first time an unambiguous identification of transmitted/founder viruses and a precise estimation of their numbers. Here, we applied this approach to HIV-1 env analyses in a cohort of acutely infected men who have sex with men (MSM) and found that a high proportion (10 of 28; 36%) had been productively infected by more than one virus. In subjects with multivariant transmission, the minimum number of transmitted viruses ranged from 2 to 10 with viral recombination leading to rapid and extensive genetic shuffling among virus lineages. A combined analysis of these results, together with recently published findings based on identical SGA methods in largely heterosexual (HSX) cohorts, revealed a significantly higher frequency of multivariant transmission in MSM than in HSX [19 of 50 subjects (38%) versus 34 of 175 subjects (19%); Fisher’s exact p = 0.008]. To further evaluate the SGA strategy for identifying transmitted/founder viruses, we analyzed 239 overlapping 59 and 39 half genome or env-only sequences from plasma viral RNA (vRNA) and blood mononuclear cell DNA in an MSM subject who had a particularly well-documented virus exposure history 3–6 days before symptom onset and 14–17 days before peak plasma viremia (47,600,000 vRNA molecules/ml). All 239 sequences coalesced to a single transmitted/founder virus genome in a time frame consistent with the clinical history, and a molecular clone of this genome encoded replication competent virus in accord with model predictions. Higher multiplicity of HIV-1 infection in MSM compared with HSX is consistent with the demonstrably higher epidemiological risk of virus acquisition in MSM and could indicate a greater challenge for HIV-1 vaccines than previously recognized.

Research Organization:
Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division
Grant/Contract Number:
AC52-06NA25396
OSTI ID:
1627896
Journal Information:
PLoS Pathogens, Journal Name: PLoS Pathogens Journal Issue: 5 Vol. 6; ISSN 1553-7374
Publisher:
Public Library of ScienceCopyright Statement
Country of Publication:
United States
Language:
English

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HIV-1 infections with multiple founders are associated with higher viral loads than infections with single founders journal August 2015
Phylogenetic patterns recover known HIV epidemiological relationships and reveal common transmission of multiple variants journal July 2018
HIV-infected sex workers with beneficial HLA-variants are potential hubs for selection of HIV-1 recombinants that may affect disease progression journal June 2015
Transmission of Multiple HIV-1 Subtype C Transmitted/founder Viruses into the Same Recipients Was not Determined by Modest Phenotypic Differences journal December 2016
HIV: Persistence through division journal March 2017
Low Multiplicity of HIV-1 Infection and No Vaccine Enhancement in VAX003 Injection Drug Users journal August 2014
Lessons from acute HIV infection journal January 2016
A Generalized Entropy Measure of Within-Host Viral Diversity for Identifying Recent HIV-1 Infections journal October 2015
New insights into the evolutionary rate of HIV-1 at the within-host and epidemiological levels journal May 2012
Single-Genome Sequencing of Hepatitis C Virus in Donor-Recipient Pairs Distinguishes Modes and Models of Virus Transmission and Early Diversification journal January 2016
The role of neutralizing antibodies in prevention of HIV-1 infection: what can we learn from the mother-to-child transmission context? journal October 2013
The number and genetic relatedness of transmitted/founder virus impact clinical outcome in vaginal R5 SHIVSF162P3N infection journal March 2014
Relative replication capacity of phenotypic SIV variants during primary infections differs with route of inoculation journal October 2010
Phylogenetic analysis consistent with a clinical history of sexual transmission of HIV-1 from a single donor reveals transmission of highly distinct variants journal January 2011
Limited SHIV env diversification in macaques failing oral antiretroviral pre-exposure prophylaxis journal May 2012
Tracing HIV-1 transmission: envelope traits of HIV-1 transmitter and recipient pairs journal September 2016
Effective treatment of SIVcpz-induced immunodeficiency in a captive western chimpanzee journal June 2017
HIV evolution and diversity in ART-treated patients journal January 2018
A Bayesian Approach to Analyse Genetic Variation within RNA Viral Populations journal March 2011
Mathematical modeling to reveal breakthrough mechanisms in the HIV Antibody Mediated Prevention (AMP) trials journal February 2020
Transmission of Single HIV-1 Genomes and Dynamics of Early Immune Escape Revealed by Ultra-Deep Sequencing journal August 2010
Association of HIV Diversity and Survival in HIV-Infected Ugandan Infants journal April 2011
Use of a High Resolution Melting (HRM) Assay to Compare Gag, Pol, and Env Diversity in Adults with Different Stages of HIV Infection journal November 2011
Prevalence and Impact of Minority Variant Drug Resistance Mutations in Primary HIV-1 Infection journal December 2011
Protection in Macaques Immunized with HIV-1 Candidate Vaccines Can Be Predicted Using the Kinetics of Their Neutralizing Antibodies journal December 2011
Detection of Retroviral Super-Infection from Non-Invasive Samples journal May 2012
Sexually-Transmitted/Founder HIV-1 Cannot Be Directly Predicted from Plasma or PBMC-Derived Viral Quasispecies in the Transmitting Partner journal July 2013
High-Accuracy Identification of Incident HIV-1 Infections Using a Sequence Clustering Based Diversity Measure journal June 2014
Analysis of Viral Diversity in Relation to the Recency of HIV-1C Infection in Botswana journal August 2016
Absence of HIV-1 Evolution in the Gut-Associated Lymphoid Tissue from Patients on Combination Antiviral Therapy Initiated during Primary Infection journal February 2012
Early Low-Titer Neutralizing Antibodies Impede HIV-1 Replication and Select for Virus Escape journal May 2012
Elucidation of Hepatitis C Virus Transmission and Early Diversification by Single Genome Sequencing journal August 2012
Cellular Superspreaders: An Epidemiological Perspective on HIV Infection inside the Body journal May 2014
Differences in the Selection Bottleneck between Modes of Sexual Transmission Influence the Genetic Composition of the HIV-1 Founder Virus journal May 2016
Rare HIV-1 transmitted/founder lineages identified by deep viral sequencing contribute to rapid shifts in dominant quasispecies during acute and early infection journal July 2017
Use of Dried Blood Spots to Elucidate Full-Length Transmitted/Founder HIV-1 Genomes journal July 2016
Concurrent Exposure of Neutralizing and Non-neutralizing Epitopes on a Single HIV-1 Envelope Structure journal July 2019
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Molecular Epidemiology of Human Immunodeficiency Virus journal January 2017
The MSM (Non)Identity: Toward Understanding Sexual Behavior and Identity in Health Research and Practice with Straight Men Under the Umbrella journal July 2019
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Characterizing the multiplicity of HIV founder variants during sexual transmission among MSM journal January 2016
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Compartmentalized Replication of R5 T Cell-Tropic HIV-1 in the Central Nervous System Early in the Course of Infection journal March 2015
Differences in the Selection Bottleneck between Modes of Sexual Transmission Influence the Genetic Composition of the HIV-1 Founder Virus journal May 2016
Rare HIV-1 transmitted/founder lineages identified by deep viral sequencing contribute to rapid shifts in dominant quasispecies during acute and early infection journal July 2017
Infant transmitted/founder HIV-1 viruses from peripartum transmission are neutralization resistant to paired maternal plasma journal April 2018
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Rare HIV-1 transmitted/founder lineages identified by deep viral sequencing contribute to rapid shifts in dominant quasispecies during acute and early infection text January 2017
Initial HIV-1 Antigen-Specific CD8+ T Cells in Acute HIV-1 Infection Inhibit Transmitted/Founder Virus Replication text January 2012
Bottlenecks in HIV-1 transmission: insights from the study of founder viruses text January 2015
HIV-1 target cells in the CNS text January 2015
Compartmentalized Replication of R5 T Cell-Tropic HIV-1 in the Central Nervous System Early in the Course of Infection
  • B., Joseph, Sarah; Gretja, Schnell,; Buckheit, Sturdevant, Christa
  • The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/qtqh-hb83
text January 2015
HIV-1 transmission and viral adaptation to the host journal January 2012
Concurrent Exposure of Neutralizing and Non-neutralizing Epitopes on a Single HIV-1 Envelope Structure journal July 2019
Reduction of HIV-1 Reservoir Size and Diversity After 1 Year of cART Among Brazilian Individuals Starting Treatment During Early Stages of Acute Infection journal February 2019
Combining Viral Genetics and Statistical Modeling to Improve HIV-1 Time-of-Infection Estimation towards Enhanced Vaccine Efficacy Assessment journal July 2019
Tracing HIV-1 transmission: envelope traits of HIV-1 transmitter and recipient pairs text January 2016
Estimating the mutational fitness effects distribution during early HIV infection text January 2018
Tracing HIV-1 transmission: envelope traits of HIV-1 transmitter and recipient pairs text January 2016

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59 BASIC BIOLOGICAL SCIENCES
HIV-1
genomics
medical risk factors
men who have sex with men
polymerase chain reaction
sexually transmitted diseases
viral replication
viral transmission and infection