TNF signalling drives expansion of bone marrow CD4+ T cells responsible for HSC exhaustion in experimental visceral leishmaniasis.

Visceral leishmaniasis is associated with significant changes in hematological function but the mechanisms underlying these changes are largely unknown. In contrast to naïve mice, where most long-term hematopoietic stem cells (LT-HSCs; LSK CD150+ CD34- CD48- cells) in bone marrow (BM) are quiescent,...

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Main Authors: Ana Isabel Pinto, Najmeeyah Brown, Olivier Preham, Johannes S P Doehl, Helen Ashwin, Paul M Kaye
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2017-07-01
Series:PLoS Pathogens
Online Access:https://journals.plos.org/plospathogens/article/file?id=10.1371/journal.ppat.1006465&type=printable
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author Ana Isabel Pinto
Ana Isabel Pinto
Najmeeyah Brown
Olivier Preham
Johannes S P Doehl
Helen Ashwin
Paul M Kaye
author_facet Ana Isabel Pinto
Ana Isabel Pinto
Najmeeyah Brown
Olivier Preham
Johannes S P Doehl
Helen Ashwin
Paul M Kaye
author_sort Ana Isabel Pinto
collection DOAJ
description Visceral leishmaniasis is associated with significant changes in hematological function but the mechanisms underlying these changes are largely unknown. In contrast to naïve mice, where most long-term hematopoietic stem cells (LT-HSCs; LSK CD150+ CD34- CD48- cells) in bone marrow (BM) are quiescent, we found that during Leishmania donovani infection most LT-HSCs had entered cell cycle. Loss of quiescence correlated with a reduced self-renewal capacity and functional exhaustion, as measured by serial transfer. Quiescent LT-HSCs were maintained in infected RAG2 KO mice, but lost following adoptive transfer of IFNγ-sufficient but not IFNγ-deficient CD4+ T cells. Using mixed BM chimeras, we established that IFNγ and TNF signalling pathways converge at the level of CD4+ T cells. Critically, intrinsic TNF signalling is required for the expansion and/or differentiation of pathogenic IFNγ+CD4+ T cells that promote the irreversible loss of BM function. These findings provide new insights into the pathogenic potential of CD4+ T cells that target hematopoietic function in leishmaniasis and perhaps other infectious diseases where TNF expression and BM dysfunction also occur simultaneously.
format Article
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institution DOAJ
issn 1553-7366
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publishDate 2017-07-01
publisher Public Library of Science (PLoS)
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series PLoS Pathogens
spelling doaj-art-b0c5ecbf22f146508a62c512174ef1902025-08-20T03:07:20ZengPublic Library of Science (PLoS)PLoS Pathogens1553-73661553-73742017-07-01137e100646510.1371/journal.ppat.1006465TNF signalling drives expansion of bone marrow CD4+ T cells responsible for HSC exhaustion in experimental visceral leishmaniasis.Ana Isabel PintoAna Isabel PintoNajmeeyah BrownOlivier PrehamJohannes S P DoehlHelen AshwinPaul M KayeVisceral leishmaniasis is associated with significant changes in hematological function but the mechanisms underlying these changes are largely unknown. In contrast to naïve mice, where most long-term hematopoietic stem cells (LT-HSCs; LSK CD150+ CD34- CD48- cells) in bone marrow (BM) are quiescent, we found that during Leishmania donovani infection most LT-HSCs had entered cell cycle. Loss of quiescence correlated with a reduced self-renewal capacity and functional exhaustion, as measured by serial transfer. Quiescent LT-HSCs were maintained in infected RAG2 KO mice, but lost following adoptive transfer of IFNγ-sufficient but not IFNγ-deficient CD4+ T cells. Using mixed BM chimeras, we established that IFNγ and TNF signalling pathways converge at the level of CD4+ T cells. Critically, intrinsic TNF signalling is required for the expansion and/or differentiation of pathogenic IFNγ+CD4+ T cells that promote the irreversible loss of BM function. These findings provide new insights into the pathogenic potential of CD4+ T cells that target hematopoietic function in leishmaniasis and perhaps other infectious diseases where TNF expression and BM dysfunction also occur simultaneously.https://journals.plos.org/plospathogens/article/file?id=10.1371/journal.ppat.1006465&type=printable
spellingShingle Ana Isabel Pinto
Ana Isabel Pinto
Najmeeyah Brown
Olivier Preham
Johannes S P Doehl
Helen Ashwin
Paul M Kaye
TNF signalling drives expansion of bone marrow CD4+ T cells responsible for HSC exhaustion in experimental visceral leishmaniasis.
PLoS Pathogens
title TNF signalling drives expansion of bone marrow CD4+ T cells responsible for HSC exhaustion in experimental visceral leishmaniasis.
title_full TNF signalling drives expansion of bone marrow CD4+ T cells responsible for HSC exhaustion in experimental visceral leishmaniasis.
title_fullStr TNF signalling drives expansion of bone marrow CD4+ T cells responsible for HSC exhaustion in experimental visceral leishmaniasis.
title_full_unstemmed TNF signalling drives expansion of bone marrow CD4+ T cells responsible for HSC exhaustion in experimental visceral leishmaniasis.
title_short TNF signalling drives expansion of bone marrow CD4+ T cells responsible for HSC exhaustion in experimental visceral leishmaniasis.
title_sort tnf signalling drives expansion of bone marrow cd4 t cells responsible for hsc exhaustion in experimental visceral leishmaniasis
url https://journals.plos.org/plospathogens/article/file?id=10.1371/journal.ppat.1006465&type=printable
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