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Early weaning and biological sex shape long-term immune and metabolic responses in pigs
During the early pre and postnatal life, host and environmental factors can impart a major influence on immune development, thus shaping lifelong disease resistance. Two major factors known to influence immune function and mortality in animals and people are early life stress and biological sex. How...
Autores principales: | , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
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Nature Publishing Group UK
2023
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10517948/ https://www.ncbi.nlm.nih.gov/pubmed/37741873 http://dx.doi.org/10.1038/s41598-023-42553-9 |
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author | Fardisi, Mahsa Thelen, Kyan Groenendal, Allegra Rajput, Mrigendra Sebastian, Kimberly Contreras, G. Andres Moeser, Adam J. |
author_facet | Fardisi, Mahsa Thelen, Kyan Groenendal, Allegra Rajput, Mrigendra Sebastian, Kimberly Contreras, G. Andres Moeser, Adam J. |
author_sort | Fardisi, Mahsa |
collection | PubMed |
description | During the early pre and postnatal life, host and environmental factors can impart a major influence on immune development, thus shaping lifelong disease resistance. Two major factors known to influence immune function and mortality in animals and people are early life stress and biological sex. How these two factors interact to shape long-term immune development and later life disease risk is poorly understood. Here we investigated how early weaning, a common early life stressor in pigs, and biological sex impacts long-term systemic inflammatory responses and hypothalamic–pituitary–adrenal axis (HPA axis) activation later in life. Ten-week-old female (F), intact-male (IM) and castrated-male (CM) pigs that were randomly assigned to early weaning (EW) and later weaning (LW) (at 15 or 28 days of age, respectively) were intramuscularly injected with either saline vehicle or lipopolysaccharide (LPS) to induce a systemic inflammatory response. Complete blood counts (CBC), proinflammatory cytokines, cortisol, testosterone, estradiol, and rectal temp were measured at 0 h, 2 h, and 4 h post-LPS challenge. At 4 h post-LPS, peritoneal fluid (PF) and white blood cells (WBC) were collected for differential analysis. LPS challenge significantly increased rectal temp and plasma cortisol level in all treatment groups. Together, the CBC results and immune cell counts in peritoneal cavity indicated that EW-F exhibited greater systemic immune response characterized by increased neutrophils to lymphocytes ratio (NLR) and enhanced neutrophil trafficking to the peritoneal cavity. Early weaning had an opposite effect on IM and CM pigs, which exhibited a suppressed LPS-induced neutrophil migration. Early weaning induced significantly greater cortisol responses only in IM pigs indicating a heightened HPA axis responses in EW-IM. how early weaning and biological sex affect immune and stress responses in pigs. Together, these results demonstrate that early weaning and biological sex and castration shape later life immune responses in pigs and provides insight into potential mechanisms driving sex differences in later life inflammatory disease risk and mortality. |
format | Online Article Text |
id | pubmed-10517948 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | Nature Publishing Group UK |
record_format | MEDLINE/PubMed |
spelling | pubmed-105179482023-09-25 Early weaning and biological sex shape long-term immune and metabolic responses in pigs Fardisi, Mahsa Thelen, Kyan Groenendal, Allegra Rajput, Mrigendra Sebastian, Kimberly Contreras, G. Andres Moeser, Adam J. Sci Rep Article During the early pre and postnatal life, host and environmental factors can impart a major influence on immune development, thus shaping lifelong disease resistance. Two major factors known to influence immune function and mortality in animals and people are early life stress and biological sex. How these two factors interact to shape long-term immune development and later life disease risk is poorly understood. Here we investigated how early weaning, a common early life stressor in pigs, and biological sex impacts long-term systemic inflammatory responses and hypothalamic–pituitary–adrenal axis (HPA axis) activation later in life. Ten-week-old female (F), intact-male (IM) and castrated-male (CM) pigs that were randomly assigned to early weaning (EW) and later weaning (LW) (at 15 or 28 days of age, respectively) were intramuscularly injected with either saline vehicle or lipopolysaccharide (LPS) to induce a systemic inflammatory response. Complete blood counts (CBC), proinflammatory cytokines, cortisol, testosterone, estradiol, and rectal temp were measured at 0 h, 2 h, and 4 h post-LPS challenge. At 4 h post-LPS, peritoneal fluid (PF) and white blood cells (WBC) were collected for differential analysis. LPS challenge significantly increased rectal temp and plasma cortisol level in all treatment groups. Together, the CBC results and immune cell counts in peritoneal cavity indicated that EW-F exhibited greater systemic immune response characterized by increased neutrophils to lymphocytes ratio (NLR) and enhanced neutrophil trafficking to the peritoneal cavity. Early weaning had an opposite effect on IM and CM pigs, which exhibited a suppressed LPS-induced neutrophil migration. Early weaning induced significantly greater cortisol responses only in IM pigs indicating a heightened HPA axis responses in EW-IM. how early weaning and biological sex affect immune and stress responses in pigs. Together, these results demonstrate that early weaning and biological sex and castration shape later life immune responses in pigs and provides insight into potential mechanisms driving sex differences in later life inflammatory disease risk and mortality. Nature Publishing Group UK 2023-09-23 /pmc/articles/PMC10517948/ /pubmed/37741873 http://dx.doi.org/10.1038/s41598-023-42553-9 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/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 licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . |
spellingShingle | Article Fardisi, Mahsa Thelen, Kyan Groenendal, Allegra Rajput, Mrigendra Sebastian, Kimberly Contreras, G. Andres Moeser, Adam J. Early weaning and biological sex shape long-term immune and metabolic responses in pigs |
title | Early weaning and biological sex shape long-term immune and metabolic responses in pigs |
title_full | Early weaning and biological sex shape long-term immune and metabolic responses in pigs |
title_fullStr | Early weaning and biological sex shape long-term immune and metabolic responses in pigs |
title_full_unstemmed | Early weaning and biological sex shape long-term immune and metabolic responses in pigs |
title_short | Early weaning and biological sex shape long-term immune and metabolic responses in pigs |
title_sort | early weaning and biological sex shape long-term immune and metabolic responses in pigs |
topic | Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10517948/ https://www.ncbi.nlm.nih.gov/pubmed/37741873 http://dx.doi.org/10.1038/s41598-023-42553-9 |
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