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Generation of Individual Diversity: A Too Neglected Fundamental Property of Adaptive Immune System

The fitness gains resulting from development of the adaptive immune system (AIS) during evolution are still the subject of hot debate. A large random repertoire of antigenic receptors is costly to develop and could be the source of autoimmune reactions. And yet, despite their drawbacks, AIS-like sys...

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Autor principal: Muraille, Eric
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4026687/
https://www.ncbi.nlm.nih.gov/pubmed/24860570
http://dx.doi.org/10.3389/fimmu.2014.00208
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author Muraille, Eric
author_facet Muraille, Eric
author_sort Muraille, Eric
collection PubMed
description The fitness gains resulting from development of the adaptive immune system (AIS) during evolution are still the subject of hot debate. A large random repertoire of antigenic receptors is costly to develop and could be the source of autoimmune reactions. And yet, despite their drawbacks, AIS-like systems seem to have been independently acquired in several phyla of metazoans with very different anatomies, longevities, and lifestyles. This article is a speculative attempt to explore the selective pressures, which favored this striking convergent evolution. It is well known that the AIS enables an organism to produce a specific immune response against all natural or artificial antigenic structures. However, it is frequently neglected that this response is highly variable among individuals. In practice, each individual possesses a “private” adaptive immune repertoire. This individualization of immune defenses implies that invasion and escape immune mechanisms developed by pathogens will certainly not always be successful as the specific targets and organization of the immune response are somewhat unpredictable. In a population, where individuals display heterogeneous immune responses to infection, the probability that a pathogen is able to infect all individuals could be reduced compared to a homogeneous population. This suggests that the individual diversity of the immune repertoire is not a by-product of the AIS but of its fundamental properties and could be in part responsible for repeated selection and conservation of the AIS during metazoan evolution. The capacity of the AIS to improve the management of cooperative or parasitic symbiotic relationships at the individual level could be a secondary development due to its progressive integration into the innate immune system. This hypothesis constitutes a new scenario for AIS emergence and explains the selection of MHC restriction and MHC diversification.
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spelling pubmed-40266872014-05-23 Generation of Individual Diversity: A Too Neglected Fundamental Property of Adaptive Immune System Muraille, Eric Front Immunol Immunology The fitness gains resulting from development of the adaptive immune system (AIS) during evolution are still the subject of hot debate. A large random repertoire of antigenic receptors is costly to develop and could be the source of autoimmune reactions. And yet, despite their drawbacks, AIS-like systems seem to have been independently acquired in several phyla of metazoans with very different anatomies, longevities, and lifestyles. This article is a speculative attempt to explore the selective pressures, which favored this striking convergent evolution. It is well known that the AIS enables an organism to produce a specific immune response against all natural or artificial antigenic structures. However, it is frequently neglected that this response is highly variable among individuals. In practice, each individual possesses a “private” adaptive immune repertoire. This individualization of immune defenses implies that invasion and escape immune mechanisms developed by pathogens will certainly not always be successful as the specific targets and organization of the immune response are somewhat unpredictable. In a population, where individuals display heterogeneous immune responses to infection, the probability that a pathogen is able to infect all individuals could be reduced compared to a homogeneous population. This suggests that the individual diversity of the immune repertoire is not a by-product of the AIS but of its fundamental properties and could be in part responsible for repeated selection and conservation of the AIS during metazoan evolution. The capacity of the AIS to improve the management of cooperative or parasitic symbiotic relationships at the individual level could be a secondary development due to its progressive integration into the innate immune system. This hypothesis constitutes a new scenario for AIS emergence and explains the selection of MHC restriction and MHC diversification. Frontiers Media S.A. 2014-05-13 /pmc/articles/PMC4026687/ /pubmed/24860570 http://dx.doi.org/10.3389/fimmu.2014.00208 Text en Copyright © 2014 Muraille. http://creativecommons.org/licenses/by/3.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Immunology
Muraille, Eric
Generation of Individual Diversity: A Too Neglected Fundamental Property of Adaptive Immune System
title Generation of Individual Diversity: A Too Neglected Fundamental Property of Adaptive Immune System
title_full Generation of Individual Diversity: A Too Neglected Fundamental Property of Adaptive Immune System
title_fullStr Generation of Individual Diversity: A Too Neglected Fundamental Property of Adaptive Immune System
title_full_unstemmed Generation of Individual Diversity: A Too Neglected Fundamental Property of Adaptive Immune System
title_short Generation of Individual Diversity: A Too Neglected Fundamental Property of Adaptive Immune System
title_sort generation of individual diversity: a too neglected fundamental property of adaptive immune system
topic Immunology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4026687/
https://www.ncbi.nlm.nih.gov/pubmed/24860570
http://dx.doi.org/10.3389/fimmu.2014.00208
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