Intestinal microbial communities and Holdemanella isolated from HIV+/− men who have sex with men increase frequencies of lamina propria CCR5+ CD4+ T cells
Men who have sex with men (MSM), regardless of HIV infection status, have an intestinal microbiome that is compositionally distinct from men who have sex with women (MSW) and women. We recently showed HIV-negative MSM have elevated levels of intestinal CD4+ T cells expressing CCR5, a critical co-rec...
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Taylor & Francis Group
2021
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oai:doaj.org-article:b553dca4e5b1459c96ef58786a6c91842021-11-26T11:19:48ZIntestinal microbial communities and Holdemanella isolated from HIV+/− men who have sex with men increase frequencies of lamina propria CCR5+ CD4+ T cells1949-09761949-098410.1080/19490976.2021.1997292https://doaj.org/article/b553dca4e5b1459c96ef58786a6c91842021-01-01T00:00:00Zhttp://dx.doi.org/10.1080/19490976.2021.1997292https://doaj.org/toc/1949-0976https://doaj.org/toc/1949-0984Men who have sex with men (MSM), regardless of HIV infection status, have an intestinal microbiome that is compositionally distinct from men who have sex with women (MSW) and women. We recently showed HIV-negative MSM have elevated levels of intestinal CD4+ T cells expressing CCR5, a critical co-receptor for HIV. Whether elevated expression of CCR5 is driven by the altered gut microbiome composition in MSM has not been explored. Here we used in vitro stimulation of gut Lamina Propria Mononuclear Cells (LPMCs) with whole intact microbial cells isolated from stool to demonstrate that fecal bacterial communities (FBCs) from HIV-positive/negative MSM induced higher frequencies of CCR5+ CD4+ T cells compared to FBCs from HIV-negative MSW and women. To identify potential microbial drivers, we related the frequency of CCR5+ CD4+ T cells to the abundance of individual microbial taxa in rectal biopsy of HIV-positive/negative MSM and controls, and Holdemanella biformis was strongly associated with increased frequency of CCR5+ CD4+ T cells. We used in vitro stimulation of gut LPMCs with the type strain of H. biformis, a second strain of H. biformis and an isolate of the closely related Holdemanella porci , cultured from either a HIV-positive or a HIV-negative MSM stool. H. porci elevated the frequency of both CCR5+ CD4+ T cells and the ratio of TNF-α/IL-10 Genomic comparisons of the 3 Holdemanella isolates revealed unique cell wall and capsular components, which may be responsible for their differences in immunogenicity. These findings describe a novel mechanism potentially linking intestinal dysbiosis in MSM to HIV transmission and mucosal pathogenesis.Eiko YamadaCasey G. MartinNancy Moreno-HuizarJennifer FouquierC. Preston NeffSara L. ColemanJennifer M. SchneiderJonathan HuberNichole M. NusbacherMartin McCarterThomas B. CampbellCatherine A. LozuponeBrent E. PalmerTaylor & Francis Grouparticleguthiv transmissionmicrobiomemsmt-cell recruitmentccr5Diseases of the digestive system. GastroenterologyRC799-869ENGut Microbes, Vol 13, Iss 1 (2021) |
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gut hiv transmission microbiome msm t-cell recruitment ccr5 Diseases of the digestive system. Gastroenterology RC799-869 |
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gut hiv transmission microbiome msm t-cell recruitment ccr5 Diseases of the digestive system. Gastroenterology RC799-869 Eiko Yamada Casey G. Martin Nancy Moreno-Huizar Jennifer Fouquier C. Preston Neff Sara L. Coleman Jennifer M. Schneider Jonathan Huber Nichole M. Nusbacher Martin McCarter Thomas B. Campbell Catherine A. Lozupone Brent E. Palmer Intestinal microbial communities and Holdemanella isolated from HIV+/− men who have sex with men increase frequencies of lamina propria CCR5+ CD4+ T cells |
description |
Men who have sex with men (MSM), regardless of HIV infection status, have an intestinal microbiome that is compositionally distinct from men who have sex with women (MSW) and women. We recently showed HIV-negative MSM have elevated levels of intestinal CD4+ T cells expressing CCR5, a critical co-receptor for HIV. Whether elevated expression of CCR5 is driven by the altered gut microbiome composition in MSM has not been explored. Here we used in vitro stimulation of gut Lamina Propria Mononuclear Cells (LPMCs) with whole intact microbial cells isolated from stool to demonstrate that fecal bacterial communities (FBCs) from HIV-positive/negative MSM induced higher frequencies of CCR5+ CD4+ T cells compared to FBCs from HIV-negative MSW and women. To identify potential microbial drivers, we related the frequency of CCR5+ CD4+ T cells to the abundance of individual microbial taxa in rectal biopsy of HIV-positive/negative MSM and controls, and Holdemanella biformis was strongly associated with increased frequency of CCR5+ CD4+ T cells. We used in vitro stimulation of gut LPMCs with the type strain of H. biformis, a second strain of H. biformis and an isolate of the closely related Holdemanella porci , cultured from either a HIV-positive or a HIV-negative MSM stool. H. porci elevated the frequency of both CCR5+ CD4+ T cells and the ratio of TNF-α/IL-10 Genomic comparisons of the 3 Holdemanella isolates revealed unique cell wall and capsular components, which may be responsible for their differences in immunogenicity. These findings describe a novel mechanism potentially linking intestinal dysbiosis in MSM to HIV transmission and mucosal pathogenesis. |
format |
article |
author |
Eiko Yamada Casey G. Martin Nancy Moreno-Huizar Jennifer Fouquier C. Preston Neff Sara L. Coleman Jennifer M. Schneider Jonathan Huber Nichole M. Nusbacher Martin McCarter Thomas B. Campbell Catherine A. Lozupone Brent E. Palmer |
author_facet |
Eiko Yamada Casey G. Martin Nancy Moreno-Huizar Jennifer Fouquier C. Preston Neff Sara L. Coleman Jennifer M. Schneider Jonathan Huber Nichole M. Nusbacher Martin McCarter Thomas B. Campbell Catherine A. Lozupone Brent E. Palmer |
author_sort |
Eiko Yamada |
title |
Intestinal microbial communities and Holdemanella isolated from HIV+/− men who have sex with men increase frequencies of lamina propria CCR5+ CD4+ T cells |
title_short |
Intestinal microbial communities and Holdemanella isolated from HIV+/− men who have sex with men increase frequencies of lamina propria CCR5+ CD4+ T cells |
title_full |
Intestinal microbial communities and Holdemanella isolated from HIV+/− men who have sex with men increase frequencies of lamina propria CCR5+ CD4+ T cells |
title_fullStr |
Intestinal microbial communities and Holdemanella isolated from HIV+/− men who have sex with men increase frequencies of lamina propria CCR5+ CD4+ T cells |
title_full_unstemmed |
Intestinal microbial communities and Holdemanella isolated from HIV+/− men who have sex with men increase frequencies of lamina propria CCR5+ CD4+ T cells |
title_sort |
intestinal microbial communities and holdemanella isolated from hiv+/− men who have sex with men increase frequencies of lamina propria ccr5+ cd4+ t cells |
publisher |
Taylor & Francis Group |
publishDate |
2021 |
url |
https://doaj.org/article/b553dca4e5b1459c96ef58786a6c9184 |
work_keys_str_mv |
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