Early Plasmodium‐induced inflammation does not accelerate aging in mice

Abstract Aging is associated with a decline of performance leading to reduced reproductive output and survival. While the antagonistic pleiotropy theory of aging has attracted considerable attention, the molecular/physiological functions underlying the early‐life benefits/late‐life costs paradigm re...

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Main Authors: Cédric Lippens, Emmanuel Guivier, Sarah E. Reece, Aidan J. O’Donnell, Stéphane Cornet, Bruno Faivre, Gabriele Sorci
Format: Article
Language:English
Published: Wiley 2019-02-01
Series:Evolutionary Applications
Subjects:
Online Access:https://doi.org/10.1111/eva.12718
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spelling doaj-46eaa50cd96b4dd6ab14278f06b2643b2020-11-25T03:21:40ZengWileyEvolutionary Applications1752-45712019-02-0112231432310.1111/eva.12718Early Plasmodium‐induced inflammation does not accelerate aging in miceCédric Lippens0Emmanuel Guivier1Sarah E. Reece2Aidan J. O’Donnell3Stéphane Cornet4Bruno Faivre5Gabriele Sorci6Biogéosciences, CNRS UMR 6282 Université de Bourgogne Franche‐Comté Dijon FranceBiogéosciences, CNRS UMR 6282 Université de Bourgogne Franche‐Comté Dijon FranceInstitutes of Evolutionary Biology, and Immunology and Infection Research University of Edinburgh Edinburgh UKInstitutes of Evolutionary Biology, and Immunology and Infection Research University of Edinburgh Edinburgh UKIRD UMR CBGP INRA IRD Cirad Montpellier SupAgro Montpellier FranceBiogéosciences, CNRS UMR 6282 Université de Bourgogne Franche‐Comté Dijon FranceBiogéosciences, CNRS UMR 6282 Université de Bourgogne Franche‐Comté Dijon FranceAbstract Aging is associated with a decline of performance leading to reduced reproductive output and survival. While the antagonistic pleiotropy theory of aging has attracted considerable attention, the molecular/physiological functions underlying the early‐life benefits/late‐life costs paradigm remain elusive. We tested the hypothesis that while early activation of the inflammatory response confers benefits in terms of protection against infection, it also incurs costs in terms of reduced reproductive output at old age and shortened longevity. We infected mice with the malaria parasite Plasmodium yoelii and increased the inflammatory response using an anti‐IL‐10 receptor antibody treatment. We quantified the benefits and costs of the inflammatory response during the acute phase of the infection and at old age. In agreement with the antagonistic pleiotropy hypothesis, the inflammatory response provided an early‐life benefit, since infected mice that were treated with anti‐IL‐10 receptor antibodies had reduced parasite density and anemia. However, at old age, mice in all treatment groups had similar levels of C‐reactive protein, reproductive output, survival rate, and lifespan. Overall, our results do not support the hypothesis that the benefits of a robust response to malaria infection in early life incur longer term fitness costs.https://doi.org/10.1111/eva.12718antagonistic pleiotropyinflammationPlasmodium yoeliisenescencesurvival
collection DOAJ
language English
format Article
sources DOAJ
author Cédric Lippens
Emmanuel Guivier
Sarah E. Reece
Aidan J. O’Donnell
Stéphane Cornet
Bruno Faivre
Gabriele Sorci
spellingShingle Cédric Lippens
Emmanuel Guivier
Sarah E. Reece
Aidan J. O’Donnell
Stéphane Cornet
Bruno Faivre
Gabriele Sorci
Early Plasmodium‐induced inflammation does not accelerate aging in mice
Evolutionary Applications
antagonistic pleiotropy
inflammation
Plasmodium yoelii
senescence
survival
author_facet Cédric Lippens
Emmanuel Guivier
Sarah E. Reece
Aidan J. O’Donnell
Stéphane Cornet
Bruno Faivre
Gabriele Sorci
author_sort Cédric Lippens
title Early Plasmodium‐induced inflammation does not accelerate aging in mice
title_short Early Plasmodium‐induced inflammation does not accelerate aging in mice
title_full Early Plasmodium‐induced inflammation does not accelerate aging in mice
title_fullStr Early Plasmodium‐induced inflammation does not accelerate aging in mice
title_full_unstemmed Early Plasmodium‐induced inflammation does not accelerate aging in mice
title_sort early plasmodium‐induced inflammation does not accelerate aging in mice
publisher Wiley
series Evolutionary Applications
issn 1752-4571
publishDate 2019-02-01
description Abstract Aging is associated with a decline of performance leading to reduced reproductive output and survival. While the antagonistic pleiotropy theory of aging has attracted considerable attention, the molecular/physiological functions underlying the early‐life benefits/late‐life costs paradigm remain elusive. We tested the hypothesis that while early activation of the inflammatory response confers benefits in terms of protection against infection, it also incurs costs in terms of reduced reproductive output at old age and shortened longevity. We infected mice with the malaria parasite Plasmodium yoelii and increased the inflammatory response using an anti‐IL‐10 receptor antibody treatment. We quantified the benefits and costs of the inflammatory response during the acute phase of the infection and at old age. In agreement with the antagonistic pleiotropy hypothesis, the inflammatory response provided an early‐life benefit, since infected mice that were treated with anti‐IL‐10 receptor antibodies had reduced parasite density and anemia. However, at old age, mice in all treatment groups had similar levels of C‐reactive protein, reproductive output, survival rate, and lifespan. Overall, our results do not support the hypothesis that the benefits of a robust response to malaria infection in early life incur longer term fitness costs.
topic antagonistic pleiotropy
inflammation
Plasmodium yoelii
senescence
survival
url https://doi.org/10.1111/eva.12718
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