Sustained immune activation and impaired epithelial barrier integrity in the ectocervix of women with chronic HIV infection.

Chronic systemic immune activation significantly influences human immunodeficiency virus (HIV) disease progression. Despite evidence of a pro-inflammatory environment in the genital tract of HIV-infected women, comprehensive investigations into cervical tissue from this region remain limited. Simila...

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Main Authors: Mathias Franzén Boger, Tyra Hasselrot, Vilde Kaldhusdal, Gisele H B Miranda, Paulo Czarnewski, Gabriella Edfeldt, Frideborg Bradley, Genta Rexaj, Julie Lajoie, Kenneth Omollo, Joshua Kimani, Keith R Fowke, Kristina Broliden, Annelie Tjernlund
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2024-11-01
Series:PLoS Pathogens
Online Access:https://doi.org/10.1371/journal.ppat.1012709
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author Mathias Franzén Boger
Tyra Hasselrot
Vilde Kaldhusdal
Gisele H B Miranda
Paulo Czarnewski
Gabriella Edfeldt
Frideborg Bradley
Genta Rexaj
Julie Lajoie
Kenneth Omollo
Joshua Kimani
Keith R Fowke
Kristina Broliden
Annelie Tjernlund
author_facet Mathias Franzén Boger
Tyra Hasselrot
Vilde Kaldhusdal
Gisele H B Miranda
Paulo Czarnewski
Gabriella Edfeldt
Frideborg Bradley
Genta Rexaj
Julie Lajoie
Kenneth Omollo
Joshua Kimani
Keith R Fowke
Kristina Broliden
Annelie Tjernlund
author_sort Mathias Franzén Boger
collection DOAJ
description Chronic systemic immune activation significantly influences human immunodeficiency virus (HIV) disease progression. Despite evidence of a pro-inflammatory environment in the genital tract of HIV-infected women, comprehensive investigations into cervical tissue from this region remain limited. Similarly, the consequences of chronic HIV infection on the integrity of the female genital epithelium are poorly understood, despite its importance in HIV transmission and replication. Ectocervical biopsies were obtained from HIV-seropositive (n = 14) and HIV-seronegative (n = 47) female Kenyan sex workers. RNA sequencing and bioimage analysis of epithelial junction proteins (E-cadherin, desmoglein-1, claudin-1, and zonula occludens-1) were conducted, along with CD4 staining. RNA sequencing revealed upregulation of immunoregulatory genes in HIV-seropositive women, primarily associated with heightened T cell activity and interferon signaling, which further correlated with plasma viral load. Transcription factor analysis confirmed the upregulation of pro-inflammatory transcription factors, such as RELA, NFKB1, and IKZF3, which facilitates HIV persistence in T cells. Conversely, genes and pathways associated with epithelial barrier function and structure were downregulated in the context of HIV. Digital bioimage analysis corroborated these findings, revealing significant disruption of various epithelial junction proteins in ectocervical tissues of the HIV-seropositive women. Thus, chronic HIV infection associated with ectocervical inflammation, characterized by induced T cell responses and interferon signaling, coupled with epithelial disruption. These alterations may influence HIV transmission and heighten susceptibility to other sexually transmitted infections. These findings prompt exploration of therapeutic interventions to address HIV-related complications and mitigate the risk of sexually transmitted infection transmission.
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spelling doaj-art-3c9722b44e584aaba018940e8de71ebb2024-12-10T05:31:18ZengPublic Library of Science (PLoS)PLoS Pathogens1553-73661553-73742024-11-012011e101270910.1371/journal.ppat.1012709Sustained immune activation and impaired epithelial barrier integrity in the ectocervix of women with chronic HIV infection.Mathias Franzén BogerTyra HasselrotVilde KaldhusdalGisele H B MirandaPaulo CzarnewskiGabriella EdfeldtFrideborg BradleyGenta RexajJulie LajoieKenneth OmolloJoshua KimaniKeith R FowkeKristina BrolidenAnnelie TjernlundChronic systemic immune activation significantly influences human immunodeficiency virus (HIV) disease progression. Despite evidence of a pro-inflammatory environment in the genital tract of HIV-infected women, comprehensive investigations into cervical tissue from this region remain limited. Similarly, the consequences of chronic HIV infection on the integrity of the female genital epithelium are poorly understood, despite its importance in HIV transmission and replication. Ectocervical biopsies were obtained from HIV-seropositive (n = 14) and HIV-seronegative (n = 47) female Kenyan sex workers. RNA sequencing and bioimage analysis of epithelial junction proteins (E-cadherin, desmoglein-1, claudin-1, and zonula occludens-1) were conducted, along with CD4 staining. RNA sequencing revealed upregulation of immunoregulatory genes in HIV-seropositive women, primarily associated with heightened T cell activity and interferon signaling, which further correlated with plasma viral load. Transcription factor analysis confirmed the upregulation of pro-inflammatory transcription factors, such as RELA, NFKB1, and IKZF3, which facilitates HIV persistence in T cells. Conversely, genes and pathways associated with epithelial barrier function and structure were downregulated in the context of HIV. Digital bioimage analysis corroborated these findings, revealing significant disruption of various epithelial junction proteins in ectocervical tissues of the HIV-seropositive women. Thus, chronic HIV infection associated with ectocervical inflammation, characterized by induced T cell responses and interferon signaling, coupled with epithelial disruption. These alterations may influence HIV transmission and heighten susceptibility to other sexually transmitted infections. These findings prompt exploration of therapeutic interventions to address HIV-related complications and mitigate the risk of sexually transmitted infection transmission.https://doi.org/10.1371/journal.ppat.1012709
spellingShingle Mathias Franzén Boger
Tyra Hasselrot
Vilde Kaldhusdal
Gisele H B Miranda
Paulo Czarnewski
Gabriella Edfeldt
Frideborg Bradley
Genta Rexaj
Julie Lajoie
Kenneth Omollo
Joshua Kimani
Keith R Fowke
Kristina Broliden
Annelie Tjernlund
Sustained immune activation and impaired epithelial barrier integrity in the ectocervix of women with chronic HIV infection.
PLoS Pathogens
title Sustained immune activation and impaired epithelial barrier integrity in the ectocervix of women with chronic HIV infection.
title_full Sustained immune activation and impaired epithelial barrier integrity in the ectocervix of women with chronic HIV infection.
title_fullStr Sustained immune activation and impaired epithelial barrier integrity in the ectocervix of women with chronic HIV infection.
title_full_unstemmed Sustained immune activation and impaired epithelial barrier integrity in the ectocervix of women with chronic HIV infection.
title_short Sustained immune activation and impaired epithelial barrier integrity in the ectocervix of women with chronic HIV infection.
title_sort sustained immune activation and impaired epithelial barrier integrity in the ectocervix of women with chronic hiv infection
url https://doi.org/10.1371/journal.ppat.1012709
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