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Differential Endometrial Cell Sensitivity to a Cholesterol-Dependent Cytolysin Links Trueperella pyogenes to Uterine Disease in Cattle1

Matthew R. Amos, Gareth Healey Orcid Logo, Robert J. Goldstone, Suman M. Mahan, Anna Düvel, Hans-Joachim Schuberth, Olivier Sandra, Peter Zieger, Isabelle Dieuzy-Labaye, David G.E. Smith, Iain Martin Sheldon, Martin Sheldon Orcid Logo

Biology of Reproduction, Volume: 90, Issue: 3

Swansea University Authors: Gareth Healey Orcid Logo, Martin Sheldon Orcid Logo

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DOI (Published version): 10.1095/biolreprod.113.115972

Abstract

Purulent disease of the uterus develops in 40% of dairy cows after parturition, when the epithelium of the endometrium is disrupted to expose the underlying stroma to bacteria. The severity of endometrial pathology is associated with isolation of Trueperella pyogenes. In the present study, T. pyogen...

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Published in: Biology of Reproduction
ISSN: 0006-3363 1529-7268
Published: 2014
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URI: https://cronfa.swan.ac.uk/Record/cronfa17658
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spelling 2019-06-19T16:23:37.5191358 v2 17658 2014-04-01 Differential Endometrial Cell Sensitivity to a Cholesterol-Dependent Cytolysin Links Trueperella pyogenes to Uterine Disease in Cattle1 5926519f89187489cfd5e1478aa188b1 0000-0001-9531-1220 Gareth Healey Gareth Healey true false ab0f74b794e59cc270c69e63ee1d9748 0000-0001-7902-5558 Martin Sheldon Martin Sheldon true false 2014-04-01 PMSC Purulent disease of the uterus develops in 40% of dairy cows after parturition, when the epithelium of the endometrium is disrupted to expose the underlying stroma to bacteria. The severity of endometrial pathology is associated with isolation of Trueperella pyogenes. In the present study, T. pyogenes alone caused uterine disease when infused into the uterus of cattle where the endometrial epithelium was disrupted. The bacterium secretes a cholesterol-dependent cytolysin, pyolysin (PLO), and the plo gene was identical and the plo gene promoter was highly similar amongst 12 clinical isolates of T. pyogenes. Bacteria-free filtrates of the T. pyogenes cultures caused hemolysis and endometrial cytolysis, and PLO was the main cytolytic agent, because addition of anti-PLO antibody prevented cytolysis. Similarly, a plo-deletion T. pyogenes mutant did not cause hemolysis or endometrial cytolysis. Endometrial stromal cells were notably more sensitive to PLO-mediated cytolysis than epithelial or immune cells. Stromal cells also contained more cholesterol than epithelial cells, and reducing stromal cell cholesterol content using cyclodextrins protected against PLO. Although T. pyogenes or plo-deletion T. pyogenes stimulated accumulation of inflammatory mediators, such as IL-1beta, IL-6, and IL-8, from endometrium, PLO did not stimulate inflammatory responses by endometrial or hematopoietic cells, or in vitro organ cultures of endometrium. The marked sensitivity of stromal cells to PLO-mediated cytolysis provides an explanation for how T. pyogenes acts as an opportunistic pathogen to cause pathology of the endometrium once the protective epithelium is lost after parturition. Journal Article Biology of Reproduction 90 3 0006-3363 1529-7268 1 3 2014 2014-03-01 10.1095/biolreprod.113.115972 The work was supported by Sheldon's United Kingdom’s Biotechnology and Biological Sciences Research Council grants BB/1017240/1 and Zoetis Inc within an ERANET programme grant led by Sheldon.Amos was a postdoc supervised by Sheldon and funded by Sheldon's BBSRC grant. COLLEGE NANME Medicine COLLEGE CODE PMSC Swansea University BBSRC 2019-06-19T16:23:37.5191358 2014-04-01T12:08:12.2698834 Faculty of Medicine, Health and Life Sciences Swansea University Medical School - Medicine Matthew R. Amos 1 Gareth Healey 0000-0001-9531-1220 2 Robert J. Goldstone 3 Suman M. Mahan 4 Anna Düvel 5 Hans-Joachim Schuberth 6 Olivier Sandra 7 Peter Zieger 8 Isabelle Dieuzy-Labaye 9 David G.E. Smith 10 Iain Martin Sheldon 11 Martin Sheldon 0000-0001-7902-5558 12
title Differential Endometrial Cell Sensitivity to a Cholesterol-Dependent Cytolysin Links Trueperella pyogenes to Uterine Disease in Cattle1
spellingShingle Differential Endometrial Cell Sensitivity to a Cholesterol-Dependent Cytolysin Links Trueperella pyogenes to Uterine Disease in Cattle1
Gareth Healey
Martin Sheldon
title_short Differential Endometrial Cell Sensitivity to a Cholesterol-Dependent Cytolysin Links Trueperella pyogenes to Uterine Disease in Cattle1
title_full Differential Endometrial Cell Sensitivity to a Cholesterol-Dependent Cytolysin Links Trueperella pyogenes to Uterine Disease in Cattle1
title_fullStr Differential Endometrial Cell Sensitivity to a Cholesterol-Dependent Cytolysin Links Trueperella pyogenes to Uterine Disease in Cattle1
title_full_unstemmed Differential Endometrial Cell Sensitivity to a Cholesterol-Dependent Cytolysin Links Trueperella pyogenes to Uterine Disease in Cattle1
title_sort Differential Endometrial Cell Sensitivity to a Cholesterol-Dependent Cytolysin Links Trueperella pyogenes to Uterine Disease in Cattle1
author_id_str_mv 5926519f89187489cfd5e1478aa188b1
ab0f74b794e59cc270c69e63ee1d9748
author_id_fullname_str_mv 5926519f89187489cfd5e1478aa188b1_***_Gareth Healey
ab0f74b794e59cc270c69e63ee1d9748_***_Martin Sheldon
author Gareth Healey
Martin Sheldon
author2 Matthew R. Amos
Gareth Healey
Robert J. Goldstone
Suman M. Mahan
Anna Düvel
Hans-Joachim Schuberth
Olivier Sandra
Peter Zieger
Isabelle Dieuzy-Labaye
David G.E. Smith
Iain Martin Sheldon
Martin Sheldon
format Journal article
container_title Biology of Reproduction
container_volume 90
container_issue 3
publishDate 2014
institution Swansea University
issn 0006-3363
1529-7268
doi_str_mv 10.1095/biolreprod.113.115972
college_str Faculty of Medicine, Health and Life Sciences
hierarchytype
hierarchy_top_id facultyofmedicinehealthandlifesciences
hierarchy_top_title Faculty of Medicine, Health and Life Sciences
hierarchy_parent_id facultyofmedicinehealthandlifesciences
hierarchy_parent_title Faculty of Medicine, Health and Life Sciences
department_str Swansea University Medical School - Medicine{{{_:::_}}}Faculty of Medicine, Health and Life Sciences{{{_:::_}}}Swansea University Medical School - Medicine
document_store_str 0
active_str 0
description Purulent disease of the uterus develops in 40% of dairy cows after parturition, when the epithelium of the endometrium is disrupted to expose the underlying stroma to bacteria. The severity of endometrial pathology is associated with isolation of Trueperella pyogenes. In the present study, T. pyogenes alone caused uterine disease when infused into the uterus of cattle where the endometrial epithelium was disrupted. The bacterium secretes a cholesterol-dependent cytolysin, pyolysin (PLO), and the plo gene was identical and the plo gene promoter was highly similar amongst 12 clinical isolates of T. pyogenes. Bacteria-free filtrates of the T. pyogenes cultures caused hemolysis and endometrial cytolysis, and PLO was the main cytolytic agent, because addition of anti-PLO antibody prevented cytolysis. Similarly, a plo-deletion T. pyogenes mutant did not cause hemolysis or endometrial cytolysis. Endometrial stromal cells were notably more sensitive to PLO-mediated cytolysis than epithelial or immune cells. Stromal cells also contained more cholesterol than epithelial cells, and reducing stromal cell cholesterol content using cyclodextrins protected against PLO. Although T. pyogenes or plo-deletion T. pyogenes stimulated accumulation of inflammatory mediators, such as IL-1beta, IL-6, and IL-8, from endometrium, PLO did not stimulate inflammatory responses by endometrial or hematopoietic cells, or in vitro organ cultures of endometrium. The marked sensitivity of stromal cells to PLO-mediated cytolysis provides an explanation for how T. pyogenes acts as an opportunistic pathogen to cause pathology of the endometrium once the protective epithelium is lost after parturition.
published_date 2014-03-01T03:20:27Z
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