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Acute social stress-induced immunomodulation in pigs high and low responders to ACTH
Abstract Pig husbandry is known as an intensive breeding system, piglets being submitted to multiple stressful events such as early weaning, successive mixing, crowding and shipping. These stressors are thought to impair immune defences and might contribute, at least partly, to the prophylactic use...
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Published in: | Physiology & behavior 2017-02, Vol.169, p.1-8 |
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creator | Bacou, Elodie Haurogné, Karine Mignot, Grégoire Allard, Marie De Beaurepaire, Laurence Marchand, Jordan Terenina, Elena Billon, Yvon Jacques, Julien Bach, Jean-Marie Mormède, Pierre Hervé, Julie Lieubeau, Blandine |
description | Abstract Pig husbandry is known as an intensive breeding system, piglets being submitted to multiple stressful events such as early weaning, successive mixing, crowding and shipping. These stressors are thought to impair immune defences and might contribute, at least partly, to the prophylactic use of antibiotics. Robustness was recently defined as the ability of an individual to express a high-production potential in a wide variety of environmental conditions. Increasing robustness thus appears as a valuable option to improve resilience to stressors and could be obtained by selecting piglets upon their adrenocortical activity. In this study, we aimed at depicting the consequences of an acute social stress on the immune capacity of piglets genetically selected upon divergent hypothalamic-pituitary-adrenocortical (HPA) axis activity. For this purpose, we monitored neuroendocrine and immune parameters, in high- (HPAhi ) and low- (HPAlo ) responders to ACTH, just before and immediately after a one-hour mixing with unfamiliar conspecifics. As expected, stressed piglets displayed higher levels of circulating cortisol and norepinephrine. Blood cell count analysis combined to flow cytometry revealed a stress-induced leukocyte mobilization in the bloodstream with a specific recruitment of CD8α+ lymphocytes. Besides, one-hour mixing decreased LPS-induced IL-8 and TNFα secretions in whole-blood assays (WBA) and reduced mononuclear cell phagocytosis. Altogether, our data demonstrate that acute social stress alters immune competence of piglets from both groups, and bring new insights in favour of good farming practices. While for most parameters high- and low-responders to ACTH behaved similarly, HPAhi piglets displayed higher number of CD4+ CD8α − T cells, as well as increased cytokine production in WBA (LPS-induced TNFα and PIL-induced IL-8), which could confer them increased resistance to pathogens. Finally, a principal component analysis including all parameters highlighted that overall stress effects were less pronounced on piglets with a strong HPA axis. Thus, selection upon adrenocortical axis activity seems to reduce the magnitude of response to stress and appears as a good tool to increase piglet robustness. |
doi_str_mv | 10.1016/j.physbeh.2016.11.012 |
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These stressors are thought to impair immune defences and might contribute, at least partly, to the prophylactic use of antibiotics. Robustness was recently defined as the ability of an individual to express a high-production potential in a wide variety of environmental conditions. Increasing robustness thus appears as a valuable option to improve resilience to stressors and could be obtained by selecting piglets upon their adrenocortical activity. In this study, we aimed at depicting the consequences of an acute social stress on the immune capacity of piglets genetically selected upon divergent hypothalamic-pituitary-adrenocortical (HPA) axis activity. For this purpose, we monitored neuroendocrine and immune parameters, in high- (HPAhi ) and low- (HPAlo ) responders to ACTH, just before and immediately after a one-hour mixing with unfamiliar conspecifics. As expected, stressed piglets displayed higher levels of circulating cortisol and norepinephrine. Blood cell count analysis combined to flow cytometry revealed a stress-induced leukocyte mobilization in the bloodstream with a specific recruitment of CD8α+ lymphocytes. Besides, one-hour mixing decreased LPS-induced IL-8 and TNFα secretions in whole-blood assays (WBA) and reduced mononuclear cell phagocytosis. Altogether, our data demonstrate that acute social stress alters immune competence of piglets from both groups, and bring new insights in favour of good farming practices. While for most parameters high- and low-responders to ACTH behaved similarly, HPAhi piglets displayed higher number of CD4+ CD8α − T cells, as well as increased cytokine production in WBA (LPS-induced TNFα and PIL-induced IL-8), which could confer them increased resistance to pathogens. Finally, a principal component analysis including all parameters highlighted that overall stress effects were less pronounced on piglets with a strong HPA axis. Thus, selection upon adrenocortical axis activity seems to reduce the magnitude of response to stress and appears as a good tool to increase piglet robustness.</description><identifier>ISSN: 0031-9384</identifier><identifier>EISSN: 1873-507X</identifier><identifier>DOI: 10.1016/j.physbeh.2016.11.012</identifier><identifier>PMID: 27867043</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Adrenocorticotropic Hormone - pharmacology ; Animals ; Antigens, CD - metabolism ; Catecholamines ; Chi-Square Distribution ; Cortisol ; Cytokines - metabolism ; Dose-Response Relationship, Drug ; Flow Cytometry ; Hydrocortisone - blood ; Hypothalamic-pituitary-adrenocortical axis ; Leukocyte Count ; Leukocytes - physiology ; Life Sciences ; Lipopolysaccharides - pharmacology ; Male ; Neuroimmunomodulation ; Norepinephrine - blood ; Peptide Fragments - pharmacology ; Phagocytosis - drug effects ; Pig ; Principal Component Analysis ; Psychiatry ; Stress ; Stress, Psychological - immunology ; Stress, Psychological - physiopathology ; Swine</subject><ispartof>Physiology & behavior, 2017-02, Vol.169, p.1-8</ispartof><rights>2016 Elsevier Inc.</rights><rights>Copyright © 2016 Elsevier Inc. All rights reserved.</rights><rights>Attribution - ShareAlike</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c454t-7c96849cb8b3bd485c13e3f521c6b6eb0c07fdeb5ff0703beaed21366cda80413</citedby><cites>FETCH-LOGICAL-c454t-7c96849cb8b3bd485c13e3f521c6b6eb0c07fdeb5ff0703beaed21366cda80413</cites><orcidid>0000-0001-9735-5518 ; 0000-0003-0345-1432 ; 0000-0002-1434-1506 ; 0000-0002-0682-0152 ; 0000-0002-1347-3785 ; 0000-0003-4808-2781</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,315,786,790,891,27957,27958</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/27867043$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-01605045$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Bacou, Elodie</creatorcontrib><creatorcontrib>Haurogné, Karine</creatorcontrib><creatorcontrib>Mignot, Grégoire</creatorcontrib><creatorcontrib>Allard, Marie</creatorcontrib><creatorcontrib>De Beaurepaire, Laurence</creatorcontrib><creatorcontrib>Marchand, Jordan</creatorcontrib><creatorcontrib>Terenina, Elena</creatorcontrib><creatorcontrib>Billon, Yvon</creatorcontrib><creatorcontrib>Jacques, Julien</creatorcontrib><creatorcontrib>Bach, Jean-Marie</creatorcontrib><creatorcontrib>Mormède, Pierre</creatorcontrib><creatorcontrib>Hervé, Julie</creatorcontrib><creatorcontrib>Lieubeau, Blandine</creatorcontrib><title>Acute social stress-induced immunomodulation in pigs high and low responders to ACTH</title><title>Physiology & behavior</title><addtitle>Physiol Behav</addtitle><description>Abstract Pig husbandry is known as an intensive breeding system, piglets being submitted to multiple stressful events such as early weaning, successive mixing, crowding and shipping. These stressors are thought to impair immune defences and might contribute, at least partly, to the prophylactic use of antibiotics. Robustness was recently defined as the ability of an individual to express a high-production potential in a wide variety of environmental conditions. Increasing robustness thus appears as a valuable option to improve resilience to stressors and could be obtained by selecting piglets upon their adrenocortical activity. In this study, we aimed at depicting the consequences of an acute social stress on the immune capacity of piglets genetically selected upon divergent hypothalamic-pituitary-adrenocortical (HPA) axis activity. For this purpose, we monitored neuroendocrine and immune parameters, in high- (HPAhi ) and low- (HPAlo ) responders to ACTH, just before and immediately after a one-hour mixing with unfamiliar conspecifics. As expected, stressed piglets displayed higher levels of circulating cortisol and norepinephrine. Blood cell count analysis combined to flow cytometry revealed a stress-induced leukocyte mobilization in the bloodstream with a specific recruitment of CD8α+ lymphocytes. Besides, one-hour mixing decreased LPS-induced IL-8 and TNFα secretions in whole-blood assays (WBA) and reduced mononuclear cell phagocytosis. Altogether, our data demonstrate that acute social stress alters immune competence of piglets from both groups, and bring new insights in favour of good farming practices. While for most parameters high- and low-responders to ACTH behaved similarly, HPAhi piglets displayed higher number of CD4+ CD8α − T cells, as well as increased cytokine production in WBA (LPS-induced TNFα and PIL-induced IL-8), which could confer them increased resistance to pathogens. Finally, a principal component analysis including all parameters highlighted that overall stress effects were less pronounced on piglets with a strong HPA axis. Thus, selection upon adrenocortical axis activity seems to reduce the magnitude of response to stress and appears as a good tool to increase piglet robustness.</description><subject>Adrenocorticotropic Hormone - pharmacology</subject><subject>Animals</subject><subject>Antigens, CD - metabolism</subject><subject>Catecholamines</subject><subject>Chi-Square Distribution</subject><subject>Cortisol</subject><subject>Cytokines - metabolism</subject><subject>Dose-Response Relationship, Drug</subject><subject>Flow Cytometry</subject><subject>Hydrocortisone - blood</subject><subject>Hypothalamic-pituitary-adrenocortical axis</subject><subject>Leukocyte Count</subject><subject>Leukocytes - physiology</subject><subject>Life Sciences</subject><subject>Lipopolysaccharides - pharmacology</subject><subject>Male</subject><subject>Neuroimmunomodulation</subject><subject>Norepinephrine - blood</subject><subject>Peptide Fragments - pharmacology</subject><subject>Phagocytosis - drug effects</subject><subject>Pig</subject><subject>Principal Component Analysis</subject><subject>Psychiatry</subject><subject>Stress</subject><subject>Stress, Psychological - immunology</subject><subject>Stress, Psychological - physiopathology</subject><subject>Swine</subject><issn>0031-9384</issn><issn>1873-507X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><recordid>eNqFks2O0zAURi0EYsrAI4C8ZBYJdvyTdAOqKqBIlVhQJHaWY99MXBK72Mmgvj2OWmbBBm8sW-e7n3R0EXpNSUkJle-O5ak_pxb6ssrPktKS0OoJWtGmZoUg9Y-naEUIo8WaNfwGvUjpSPJhnD1HN1XdyJpwtkKHjZknwCkYpwecpggpFc7b2YDFbhxnH8Zg50FPLnjsPD65-4R7d99j7S0ewm-cI6fgLcSEp4A328PuJXrW6SHBq-t9i75_-njY7or9189ftpt9YbjgU1GbtWz42rRNy1rLG2EoA9aJihrZSmiJIXVnoRVdR2rCWtBgK8qkNFY3hFN2i-4uc3s9qFN0o45nFbRTu81eLX_ZDBGEi4eFfXthTzH8miFNanTJwDBoD2FOija8ErxekwUVF9TEkFKE7nE2JWqRr47qKl8t8hWluanKuTfXirkdwT6m_trOwIcLAFnKg4OoknHgs2oXwUzKBvffivf_TDCD887o4SecIR3DHH02rqhKlSLq27IBywJQyYiQsmJ_AIYDrOE</recordid><startdate>20170201</startdate><enddate>20170201</enddate><creator>Bacou, Elodie</creator><creator>Haurogné, Karine</creator><creator>Mignot, Grégoire</creator><creator>Allard, Marie</creator><creator>De Beaurepaire, Laurence</creator><creator>Marchand, Jordan</creator><creator>Terenina, Elena</creator><creator>Billon, Yvon</creator><creator>Jacques, Julien</creator><creator>Bach, Jean-Marie</creator><creator>Mormède, Pierre</creator><creator>Hervé, Julie</creator><creator>Lieubeau, Blandine</creator><general>Elsevier Inc</general><general>Elsevier</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>1XC</scope><orcidid>https://orcid.org/0000-0001-9735-5518</orcidid><orcidid>https://orcid.org/0000-0003-0345-1432</orcidid><orcidid>https://orcid.org/0000-0002-1434-1506</orcidid><orcidid>https://orcid.org/0000-0002-0682-0152</orcidid><orcidid>https://orcid.org/0000-0002-1347-3785</orcidid><orcidid>https://orcid.org/0000-0003-4808-2781</orcidid></search><sort><creationdate>20170201</creationdate><title>Acute social stress-induced immunomodulation in pigs high and low responders to ACTH</title><author>Bacou, Elodie ; Haurogné, Karine ; Mignot, Grégoire ; Allard, Marie ; De Beaurepaire, Laurence ; Marchand, Jordan ; Terenina, Elena ; Billon, Yvon ; Jacques, Julien ; Bach, Jean-Marie ; Mormède, Pierre ; Hervé, Julie ; Lieubeau, Blandine</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c454t-7c96849cb8b3bd485c13e3f521c6b6eb0c07fdeb5ff0703beaed21366cda80413</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>Adrenocorticotropic Hormone - pharmacology</topic><topic>Animals</topic><topic>Antigens, CD - metabolism</topic><topic>Catecholamines</topic><topic>Chi-Square Distribution</topic><topic>Cortisol</topic><topic>Cytokines - metabolism</topic><topic>Dose-Response Relationship, Drug</topic><topic>Flow Cytometry</topic><topic>Hydrocortisone - blood</topic><topic>Hypothalamic-pituitary-adrenocortical axis</topic><topic>Leukocyte Count</topic><topic>Leukocytes - physiology</topic><topic>Life Sciences</topic><topic>Lipopolysaccharides - pharmacology</topic><topic>Male</topic><topic>Neuroimmunomodulation</topic><topic>Norepinephrine - blood</topic><topic>Peptide Fragments - pharmacology</topic><topic>Phagocytosis - drug effects</topic><topic>Pig</topic><topic>Principal Component Analysis</topic><topic>Psychiatry</topic><topic>Stress</topic><topic>Stress, Psychological - immunology</topic><topic>Stress, Psychological - physiopathology</topic><topic>Swine</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Bacou, Elodie</creatorcontrib><creatorcontrib>Haurogné, Karine</creatorcontrib><creatorcontrib>Mignot, Grégoire</creatorcontrib><creatorcontrib>Allard, Marie</creatorcontrib><creatorcontrib>De Beaurepaire, Laurence</creatorcontrib><creatorcontrib>Marchand, Jordan</creatorcontrib><creatorcontrib>Terenina, Elena</creatorcontrib><creatorcontrib>Billon, Yvon</creatorcontrib><creatorcontrib>Jacques, Julien</creatorcontrib><creatorcontrib>Bach, Jean-Marie</creatorcontrib><creatorcontrib>Mormède, Pierre</creatorcontrib><creatorcontrib>Hervé, Julie</creatorcontrib><creatorcontrib>Lieubeau, Blandine</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><jtitle>Physiology & behavior</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Bacou, Elodie</au><au>Haurogné, Karine</au><au>Mignot, Grégoire</au><au>Allard, Marie</au><au>De Beaurepaire, Laurence</au><au>Marchand, Jordan</au><au>Terenina, Elena</au><au>Billon, Yvon</au><au>Jacques, Julien</au><au>Bach, Jean-Marie</au><au>Mormède, Pierre</au><au>Hervé, Julie</au><au>Lieubeau, Blandine</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Acute social stress-induced immunomodulation in pigs high and low responders to ACTH</atitle><jtitle>Physiology & behavior</jtitle><addtitle>Physiol Behav</addtitle><date>2017-02-01</date><risdate>2017</risdate><volume>169</volume><spage>1</spage><epage>8</epage><pages>1-8</pages><issn>0031-9384</issn><eissn>1873-507X</eissn><notes>ObjectType-Article-1</notes><notes>SourceType-Scholarly Journals-1</notes><notes>ObjectType-Feature-2</notes><notes>content type line 23</notes><abstract>Abstract Pig husbandry is known as an intensive breeding system, piglets being submitted to multiple stressful events such as early weaning, successive mixing, crowding and shipping. These stressors are thought to impair immune defences and might contribute, at least partly, to the prophylactic use of antibiotics. Robustness was recently defined as the ability of an individual to express a high-production potential in a wide variety of environmental conditions. Increasing robustness thus appears as a valuable option to improve resilience to stressors and could be obtained by selecting piglets upon their adrenocortical activity. In this study, we aimed at depicting the consequences of an acute social stress on the immune capacity of piglets genetically selected upon divergent hypothalamic-pituitary-adrenocortical (HPA) axis activity. For this purpose, we monitored neuroendocrine and immune parameters, in high- (HPAhi ) and low- (HPAlo ) responders to ACTH, just before and immediately after a one-hour mixing with unfamiliar conspecifics. As expected, stressed piglets displayed higher levels of circulating cortisol and norepinephrine. Blood cell count analysis combined to flow cytometry revealed a stress-induced leukocyte mobilization in the bloodstream with a specific recruitment of CD8α+ lymphocytes. Besides, one-hour mixing decreased LPS-induced IL-8 and TNFα secretions in whole-blood assays (WBA) and reduced mononuclear cell phagocytosis. Altogether, our data demonstrate that acute social stress alters immune competence of piglets from both groups, and bring new insights in favour of good farming practices. While for most parameters high- and low-responders to ACTH behaved similarly, HPAhi piglets displayed higher number of CD4+ CD8α − T cells, as well as increased cytokine production in WBA (LPS-induced TNFα and PIL-induced IL-8), which could confer them increased resistance to pathogens. Finally, a principal component analysis including all parameters highlighted that overall stress effects were less pronounced on piglets with a strong HPA axis. Thus, selection upon adrenocortical axis activity seems to reduce the magnitude of response to stress and appears as a good tool to increase piglet robustness.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>27867043</pmid><doi>10.1016/j.physbeh.2016.11.012</doi><tpages>8</tpages><orcidid>https://orcid.org/0000-0001-9735-5518</orcidid><orcidid>https://orcid.org/0000-0003-0345-1432</orcidid><orcidid>https://orcid.org/0000-0002-1434-1506</orcidid><orcidid>https://orcid.org/0000-0002-0682-0152</orcidid><orcidid>https://orcid.org/0000-0002-1347-3785</orcidid><orcidid>https://orcid.org/0000-0003-4808-2781</orcidid></addata></record> |
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subjects | Adrenocorticotropic Hormone - pharmacology Animals Antigens, CD - metabolism Catecholamines Chi-Square Distribution Cortisol Cytokines - metabolism Dose-Response Relationship, Drug Flow Cytometry Hydrocortisone - blood Hypothalamic-pituitary-adrenocortical axis Leukocyte Count Leukocytes - physiology Life Sciences Lipopolysaccharides - pharmacology Male Neuroimmunomodulation Norepinephrine - blood Peptide Fragments - pharmacology Phagocytosis - drug effects Pig Principal Component Analysis Psychiatry Stress Stress, Psychological - immunology Stress, Psychological - physiopathology Swine |
title | Acute social stress-induced immunomodulation in pigs high and low responders to ACTH |
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