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Pathogenesis and Immunity | Spotlight

Better Viral Control despite Higher CD4+ T Cell Activation during Acute HIV-1 Infection in Zambian Women Is Linked to the Sex Hormone Estradiol

Elina El-Badry, Gladys Macharia, Daniel Claiborne, Kelsie Brooks, Darío A. Dilernia, Paul Goepfert, William Kilembe, Susan Allen, Jill Gilmour, Eric Hunter
Viviana Simon, Editor
Elina El-Badry
aEmory Vaccine Center, Yerkes National Primate Research Center, Emory University, Atlanta, Georgia, USA
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Gladys Macharia
bDepartment of Medicine, Imperial College London, London, United Kingdom
cInternational AIDS Vaccine Initiative Human Immunology Laboratory, London, United Kingdom
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Daniel Claiborne
aEmory Vaccine Center, Yerkes National Primate Research Center, Emory University, Atlanta, Georgia, USA
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Kelsie Brooks
aEmory Vaccine Center, Yerkes National Primate Research Center, Emory University, Atlanta, Georgia, USA
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Darío A. Dilernia
aEmory Vaccine Center, Yerkes National Primate Research Center, Emory University, Atlanta, Georgia, USA
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Paul Goepfert
dDepartment of Medicine, University of Alabama at Birmingham, Birmingham, Alabama, USA
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William Kilembe
eZambia-Emory HIV Research Project, Lusaka, Zambia
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Susan Allen
eZambia-Emory HIV Research Project, Lusaka, Zambia
fDepartment of Global Health, Rollins School of Public Health, Emory University, Atlanta, Georgia, USA
gDepartment of Pathology and Laboratory Medicine, Emory University, Atlanta, Georgia, USA
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Jill Gilmour
bDepartment of Medicine, Imperial College London, London, United Kingdom
cInternational AIDS Vaccine Initiative Human Immunology Laboratory, London, United Kingdom
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Eric Hunter
aEmory Vaccine Center, Yerkes National Primate Research Center, Emory University, Atlanta, Georgia, USA
gDepartment of Pathology and Laboratory Medicine, Emory University, Atlanta, Georgia, USA
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Viviana Simon
Icahn School of Medicine at Mount Sinai
Roles: Editor
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DOI: 10.1128/JVI.00758-20
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ABSTRACT

The influence of biological sex on disease progression in HIV-1-infected individuals has been focused on the chronic stage of infection, but little is known about how sex differences influence acute HIV-1 infection. We observed profound differences in viral load and CD4+ T cell activation from the earliest time points in men and women in a Zambian heterosexual acute infection cohort. Women exhibited a >2-fold higher rate of CD4+ T cell loss despite significantly lower viral loads (VL) than men. The importance of studying acute infection was highlighted by the observation that very early in infection, women exhibited significantly higher levels of CD4+ T cell activation, a difference that was lost over the first 3 years of infection as activation in men increased. In women, activation of CD4+ T cells in the acute phase was significantly correlated with plasma levels of 17β-estradiol (E2). However, unlike in men, higher CD4+ T cell activation in women was not associated with higher VL. In contrast, a higher E2 level in early infection was associated with lower early and set-point VL in women. We attribute this to an inhibitory effect of estradiol on virus replication, which we were able to observe with relevant transmitted/founder viruses in vitro. Thus, estradiol plays a key role in defining major differences between men and women during early HIV-1 infection by contributing to both viral control and CD4+ T cell loss, an effect that extends into the chronic phase of the disease.

IMPORTANCE Previous studies have identified sex-specific differences during chronic HIV-1 infection, but little is known about sex differences in the acute phase, or how disparities in the initial response to the virus may affect disease. We demonstrate that restriction of viral load in women begins during acute infection and is maintained into chronic infection. Despite this, women exhibit more rapid CD4+ T cell loss than men. These profound differences are influenced by 17β-estradiol, which contributes both to T cell activation and to reduced viral replication. Thus, we conclude that estradiol plays a key role in shaping responses to early HIV-1 infection that influence the chronic phase of disease.

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Better Viral Control despite Higher CD4+ T Cell Activation during Acute HIV-1 Infection in Zambian Women Is Linked to the Sex Hormone Estradiol
Elina El-Badry, Gladys Macharia, Daniel Claiborne, Kelsie Brooks, Darío A. Dilernia, Paul Goepfert, William Kilembe, Susan Allen, Jill Gilmour, Eric Hunter
Journal of Virology Jul 2020, 94 (16) e00758-20; DOI: 10.1128/JVI.00758-20

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Better Viral Control despite Higher CD4+ T Cell Activation during Acute HIV-1 Infection in Zambian Women Is Linked to the Sex Hormone Estradiol
Elina El-Badry, Gladys Macharia, Daniel Claiborne, Kelsie Brooks, Darío A. Dilernia, Paul Goepfert, William Kilembe, Susan Allen, Jill Gilmour, Eric Hunter
Journal of Virology Jul 2020, 94 (16) e00758-20; DOI: 10.1128/JVI.00758-20
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KEYWORDS

estrogen
human immunodeficiency virus
sex differences
T cell activation
Viral Load
viral pathogenesis
viral replication

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