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Consistent Viral Evolutionary Changes Associated with the Progression of Human Immunodeficiency Virus Type 1 Infection

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Shankarappa, Raj, Margolick, Joseph B., Gange, Stephen J., Rodrigo, Allen G., Upchurch, David, Farzadegan, Homayoon, Gupta, Phalguni, Rinaldo, Charles R., Learn, Gerald H., He, Xi, Huang, Xiao-Li, Mullins, James I.·1999·Journal of Virology

DOI 10.1128/jvi.73.12.10489-10502.1999PMC PMC113104

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Abstract

To understand the high variability of the asymptomatic interval between primary human immunodeficiency virus type 1 (HIV-1) infection and the development of AIDS, we studied the evolution of the C2-V5 region of the HIV-1 env gene and of T-cell subsets in nine men with a moderate or slow rate of disease progression. They were monitored from the time of seroconversion for a period of 6 to 12 years until the development of advanced disease in seven men. Based on the analysis of viral divergence from the founder strain, viral population diversity within sequential time points, and the outgrowth of viruses capable of utilizing the CXCR4 receptor (X4 viruses), the existence of three distinct phases within the asymptomatic interval is suggested: an early phase of variable duration during which linear increases (∼1% per year) in both divergence and diversity were observed; an intermediate phase lasting an average of 1.8 years, characterized by a continued increase in divergence but with stabilization or decline in diversity; and a late phase characterized by a slowdown or stabilization of divergence and continued stability or decline in diversity. X4 variants emerged around the time of the early- to intermediate-phase transition and then achieved peak representation and began a decline around the transition between the intermediate and late phases. The late-phase transition was also associated with failure of T-cell homeostasis (defined by a downward inflection in CD3+T cells) and decline of CD4+T cells to ≤200 cells/μl. The strength of these temporal associations between viral divergence and diversity, viral coreceptor specificity, and T-cell homeostasis and subset composition supports the concept that the phases described represent a consistent pattern of viral evolution during the course of HIV-1 infection in moderate progressors. Recognition of this pattern may help explain previous conflicting data on the relationship between viral evolution and disease progression and may provide a useful framework for evaluating immune damage and recovery in untreated and treated HIV-1 infections.

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Authors: Shankarappa, R., Margolick, J. B., Gange, S. J., Rodrigo, A. G., Upchurch, D., Farzadegan, H., Gupta, P., Rinaldo, C. R., Learn, G. H., He, X., Huang, X.-L., & Mullins, J. I.
Affiliations: University of Washington (US)
Departments of Molecular Microbiology and Immunology2 and of
Johns Hopkins University (US)
University of Pittsburgh (US)
ORCID: Margolick, Joseph B.
Gange, Stephen J.
Rodrigo, Allen G.
Gupta, Phalguni
Rinaldo, Charles R.
Learn, Gerald H.
He, Xi
Mullins, James I.
Venue: Journal of Virology
Publisher: American Society for Microbiology
Published: 1999-12
Volume: 73
Issue: 12
Pages: 10489-10502
ISSN: 0022-538X (ISSN-L)
1098-5514
DOI: 10.1128/jvi.73.12.10489-10502.1999
PMC: PMC113104
OpenAlex: W2126515754
Cited by: 926
References: 84
Citations by year: 2026: 7 · 2025: 12 · 2024: 14 · 2023: 19 · 2022: 16 · 2021: 13 · 2020: 22 · 2019: 33 · 2018: 24 · 2017: 33 · 2016: 31 · 2015: 35 · 2014: 36 · 2013: 50 · 2012: 57
FWCI: 7.58
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: journals.asm.org/non-commercial-tdm-license (tdm)
Locations: Journal of Virology (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health (5r01ai034783-05, 5r01ai032885-06)
National Institute of Allergy and Infectious Diseases (AI-34783, AI37984, U01AI035040, U01AI037984, U01AI035041, AI-32885, U01AI035039, U01AI035042, P30AI027757)
Topics: Life Sciences › Immunology and Microbiology › Virology › HIV Research and Treatment
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
Health Sciences › Medicine › Infectious Diseases › HIV/AIDS drug development and treatment
Keywords: HIV-1, viral evolution, disease progression, asymptomatic HIV infection, HIV-1 env gene, viral divergence, viral population diversity, CXCR4, T cell homeostasis, CD4+ T cells, CD3+ T cells
MeSH terms: Base Sequence, DNA, Viral, Humans, Male, Molecular Sequence Data, Prospective Studies, HIV-1, HIV Infections, Gene Products, env, Disease Progression, Evolution, Molecular

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Consistent Viral Evolutionary Changes Associated with the Progression of Human Immunodeficiency Virus Type 1 Infection

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