Adaptation to HLA-associated immune pressure over the course of HIV infection and in circulating HIV-1 strains

Eric Alves; Marwah Al-Kaabi; Niamh M. Keane; Shay Leary; Coral-Ann M. Almeida; Pooja Deshpande; Jennifer Currenti; Abha Chopra; Rita Smith; Alison Castley; Simon Mallal; Spyros A. Kalams; Silvana Gaudieri; Mina John

doi:10.1371/journal.ppat.1010965

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Adaptation to HLA-associated immune pressure over the course of HIV infection and in circulating HIV-1 strains

Journal article

Open access

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Adaptation to HLA-associated immune pressure over the course of HIV infection and in circulating HIV-1 strains

Eric Alves, Marwah Al-Kaabi, Niamh M. Keane, Shay Leary, Coral-Ann M. Almeida, Pooja Deshpande, Jennifer Currenti, Abha Chopra, Rita Smith, Alison Castley, …

PLoS pathogens, Vol.18(12), 1010965

2022

DOI: https://doi.org/10.1371/journal.ppat.1010965

PMCID: PMC9803285

PMID: 36525463

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Abstract

Life Sciences & Biomedicine

Microbiology

Parasitology

Science & Technology

Virology

Adaptation to human leukocyte antigen (HLA)-associated immune pressure represents a major driver of human immunodeficiency virus (HIV) evolution at both the individual and population level. To date, there has been limited exploration of the impact of the initial cellular immune response in driving viral adaptation, the dynamics of these changes during infection and their effect on circulating transmitting viruses at the population level. Capturing detailed virological and immunological data from acute and early HIV infection is challenging as this commonly precedes the diagnosis of HIV infection, potentially by many years. In addition, rapid initiation of antiretroviral treatment following a diagnosis is the standard of care, and central to global efforts towards HIV elimination. Yet, acute untreated infection is the critical period in which the diversity of proviral reservoirs is first established within individuals, and associated with greater risk of onward transmissions in a population. Characterizing the viral adaptations evident in the earliest phases of infection, coinciding with the initial cellular immune responses is therefore relevant to understanding which changes are of greatest impact to HIV evolution at the population level. In this study, we utilized three separate cohorts to examine the initial CD8+ T cell immune response to HIV (cross-sectional acute infection cohort), track HIV evolution in response to CD8+ T cell-mediated immunity over time (longitudinal chronic infection cohort) and translate the impact of HLA-driven HIV evolution to the population level (cross-sectional HIV sequence data spanning 30 years). Using next generation viral sequencing and enzyme-linked immunospot interferon-gamma recall responses to peptides representing HLA class I-specific HIV T cell targets, we observed that CD8+ T cell responses can select viral adaptations prior to full antibody seroconversion. Using the longitudinal cohort, we uncover that viral adaptations have the propensity to be retained over time in a non-selective immune environment, which reflects the increasing proportion of pre-adapted HIV strains within the Western Australian population over an approximate 30-year period.

Details

Title: Adaptation to HLA-associated immune pressure over the course of HIV infection and in circulating HIV-1 strains
Authors/Creators: Eric Alves - The University of Western Australia
Marwah Al-Kaabi - The University of Western Australia
Niamh M. Keane - Murdoch University
Shay Leary - Murdoch University
Coral-Ann M. Almeida - Murdoch Univ, Inst Immunol & Infect Dis, Perth, WA, Australia
Pooja Deshpande - The University of Western Australia
Jennifer Currenti - The University of Western Australia
Abha Chopra - Murdoch University
Rita Smith - Vanderbilt University Medical Center
Alison Castley - Royal Perth Hospital
Simon Mallal - Murdoch University
Spyros A. Kalams - Vanderbilt University Medical Center
Silvana Gaudieri - The University of Western Australia
Mina John - Murdoch University
Publication Details: PLoS pathogens, Vol.18(12), 1010965
Publisher: Public Library Science
Number of pages: 26
Grant note: BioZone PhD Scholarship at The University of Western Australia P30 AI110527 / National Institutes of Health; United States Department of Health & Human Services; National Institutes of Health (NIH) - USA R01-AI39966 / NIH; United States Department of Health & Human Services; National Institutes of Health (NIH) - USA APP1148284 / National Health and Medical Research Council; National Health and Medical Research Council (NHMRC) of Australia RA/1/1200/934 / UWA Research Collaboration Award PathWest Australian Government Research Training Program Scholarship; Australian Government; Department of Industry, Innovation and Science Sir Charles Gairdner Hospital Foundation
Identifiers: 991005623568407891
Copyright: This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.
Murdoch Affiliation: Institute for Immunology and Infectious Diseases; Centre for Molecular Medicine and Innovative Therapeutics
Language: English
Resource Type: Journal article

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Collaboration types: Domestic collaboration; International collaboration
Citation topics: 1 Clinical & Life Sciences; 1.66 HIV; 1.66.46 HIV Pathogenesis
Web Of Science research areas: Microbiology; Parasitology; Virology
ESI research areas: Microbiology