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Differential Sensitivity to Plasmodium yoelii Infection in C57BL/6 Mice Impacts Gut-Liver Axis Homeostasis

Experimental models of malaria have shown that infection with specific Plasmodium species in certain mouse strains can transiently modulate gut microbiota and cause intestinal shortening, indicating a disruption of gut homeostasis. Importantly, changes in gut homeostasis have not been characterized...

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Autores principales: Denny, Joshua E., Powers, Joshua B., Castro, Hector F., Zhang, Jingwen, Joshi-Barve, Swati, Campagna, Shawn R., Schmidt, Nathan W.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6401097/
https://www.ncbi.nlm.nih.gov/pubmed/30837607
http://dx.doi.org/10.1038/s41598-019-40266-6
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author Denny, Joshua E.
Powers, Joshua B.
Castro, Hector F.
Zhang, Jingwen
Joshi-Barve, Swati
Campagna, Shawn R.
Schmidt, Nathan W.
author_facet Denny, Joshua E.
Powers, Joshua B.
Castro, Hector F.
Zhang, Jingwen
Joshi-Barve, Swati
Campagna, Shawn R.
Schmidt, Nathan W.
author_sort Denny, Joshua E.
collection PubMed
description Experimental models of malaria have shown that infection with specific Plasmodium species in certain mouse strains can transiently modulate gut microbiota and cause intestinal shortening, indicating a disruption of gut homeostasis. Importantly, changes in gut homeostasis have not been characterized in the context of mild versus severe malaria. We show that severe Plasmodium infection in mice disrupts homeostasis along the gut-liver axis in multiple ways compared to mild infection. High parasite burden results in a larger influx of immune cells in the lamina propria and mice with high parasitemia display specific metabolomic profiles in the ceca and plasma during infection compared to mice with mild parasitemia. Liver damage was also more pronounced and longer lasting during severe infection, with concomitant changes in bile acids in the gut. Finally, severe Plasmodium infection changes the functional capacity of the microbiota, enhancing bacterial motility and amino acid metabolism in mice with high parasite burden compared to a mild infection. Taken together, Plasmodium infections have diverse effects on host gut homeostasis relative to the severity of infection that may contribute to enteric bacteremia that is associated with malaria.
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spelling pubmed-64010972019-03-07 Differential Sensitivity to Plasmodium yoelii Infection in C57BL/6 Mice Impacts Gut-Liver Axis Homeostasis Denny, Joshua E. Powers, Joshua B. Castro, Hector F. Zhang, Jingwen Joshi-Barve, Swati Campagna, Shawn R. Schmidt, Nathan W. Sci Rep Article Experimental models of malaria have shown that infection with specific Plasmodium species in certain mouse strains can transiently modulate gut microbiota and cause intestinal shortening, indicating a disruption of gut homeostasis. Importantly, changes in gut homeostasis have not been characterized in the context of mild versus severe malaria. We show that severe Plasmodium infection in mice disrupts homeostasis along the gut-liver axis in multiple ways compared to mild infection. High parasite burden results in a larger influx of immune cells in the lamina propria and mice with high parasitemia display specific metabolomic profiles in the ceca and plasma during infection compared to mice with mild parasitemia. Liver damage was also more pronounced and longer lasting during severe infection, with concomitant changes in bile acids in the gut. Finally, severe Plasmodium infection changes the functional capacity of the microbiota, enhancing bacterial motility and amino acid metabolism in mice with high parasite burden compared to a mild infection. Taken together, Plasmodium infections have diverse effects on host gut homeostasis relative to the severity of infection that may contribute to enteric bacteremia that is associated with malaria. Nature Publishing Group UK 2019-03-05 /pmc/articles/PMC6401097/ /pubmed/30837607 http://dx.doi.org/10.1038/s41598-019-40266-6 Text en © The Author(s) 2019 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Denny, Joshua E.
Powers, Joshua B.
Castro, Hector F.
Zhang, Jingwen
Joshi-Barve, Swati
Campagna, Shawn R.
Schmidt, Nathan W.
Differential Sensitivity to Plasmodium yoelii Infection in C57BL/6 Mice Impacts Gut-Liver Axis Homeostasis
title Differential Sensitivity to Plasmodium yoelii Infection in C57BL/6 Mice Impacts Gut-Liver Axis Homeostasis
title_full Differential Sensitivity to Plasmodium yoelii Infection in C57BL/6 Mice Impacts Gut-Liver Axis Homeostasis
title_fullStr Differential Sensitivity to Plasmodium yoelii Infection in C57BL/6 Mice Impacts Gut-Liver Axis Homeostasis
title_full_unstemmed Differential Sensitivity to Plasmodium yoelii Infection in C57BL/6 Mice Impacts Gut-Liver Axis Homeostasis
title_short Differential Sensitivity to Plasmodium yoelii Infection in C57BL/6 Mice Impacts Gut-Liver Axis Homeostasis
title_sort differential sensitivity to plasmodium yoelii infection in c57bl/6 mice impacts gut-liver axis homeostasis
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6401097/
https://www.ncbi.nlm.nih.gov/pubmed/30837607
http://dx.doi.org/10.1038/s41598-019-40266-6
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