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Transcriptomics Analysis of Porcine Caudal Dorsal Root Ganglia in Tail Amputated Pigs Shows Long-Term Effects on Many Pain-Associated Genes

Tail amputation by tail docking or as an extreme consequence of tail biting in commercial pig production potentially has serious implications for animal welfare. Tail amputation causes peripheral nerve injury that might be associated with lasting chronic pain. The aim of this study was to investigat...

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Autores principales: Sandercock, Dale A., Barnett, Mark W., Coe, Jennifer E., Downing, Alison C., Nirmal, Ajit J., Di Giminiani, Pierpaolo, Edwards, Sandra A., Freeman, Tom C.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6760028/
https://www.ncbi.nlm.nih.gov/pubmed/31620455
http://dx.doi.org/10.3389/fvets.2019.00314
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author Sandercock, Dale A.
Barnett, Mark W.
Coe, Jennifer E.
Downing, Alison C.
Nirmal, Ajit J.
Di Giminiani, Pierpaolo
Edwards, Sandra A.
Freeman, Tom C.
author_facet Sandercock, Dale A.
Barnett, Mark W.
Coe, Jennifer E.
Downing, Alison C.
Nirmal, Ajit J.
Di Giminiani, Pierpaolo
Edwards, Sandra A.
Freeman, Tom C.
author_sort Sandercock, Dale A.
collection PubMed
description Tail amputation by tail docking or as an extreme consequence of tail biting in commercial pig production potentially has serious implications for animal welfare. Tail amputation causes peripheral nerve injury that might be associated with lasting chronic pain. The aim of this study was to investigate the short- and long-term effects of tail amputation in pigs on caudal DRG gene expression at different stages of development, particularly in relation to genes associated with nociception and pain. Microarrays were used to analyse whole DRG transcriptomes from tail amputated and sham-treated pigs 1, 8, and 16 weeks following tail treatment at either 3 or 63 days of age (8 pigs/treatment/age/time after treatment; n = 96). Tail amputation induced marked changes in gene expression (up and down) compared to sham-treated intact controls for all treatment ages and time points after tail treatment. Sustained changes in gene expression in tail amputated pigs were still evident 4 months after tail injury. Gene correlation network analysis revealed two co-expression clusters associated with amputation: Cluster A (759 down-regulated) and Cluster B (273 up-regulated) genes. Gene ontology (GO) enrichment analysis identified 124 genes in Cluster A and 61 genes in Cluster B associated with both “inflammatory pain” and “neuropathic pain.” In Cluster A, gene family members of ion channels e.g., voltage-gated potassium channels (VGPC) and receptors e.g., GABA receptors, were significantly down-regulated compared to shams, both of which are linked to increased peripheral nerve excitability after axotomy. Up-regulated gene families in Cluster B were linked to transcriptional regulation, inflammation, tissue remodeling, and regulatory neuropeptide activity. These findings, demonstrate that tail amputation causes sustained transcriptomic expression changes in caudal DRG cells involved in inflammatory and neuropathic pain pathways.
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spelling pubmed-67600282019-10-16 Transcriptomics Analysis of Porcine Caudal Dorsal Root Ganglia in Tail Amputated Pigs Shows Long-Term Effects on Many Pain-Associated Genes Sandercock, Dale A. Barnett, Mark W. Coe, Jennifer E. Downing, Alison C. Nirmal, Ajit J. Di Giminiani, Pierpaolo Edwards, Sandra A. Freeman, Tom C. Front Vet Sci Veterinary Science Tail amputation by tail docking or as an extreme consequence of tail biting in commercial pig production potentially has serious implications for animal welfare. Tail amputation causes peripheral nerve injury that might be associated with lasting chronic pain. The aim of this study was to investigate the short- and long-term effects of tail amputation in pigs on caudal DRG gene expression at different stages of development, particularly in relation to genes associated with nociception and pain. Microarrays were used to analyse whole DRG transcriptomes from tail amputated and sham-treated pigs 1, 8, and 16 weeks following tail treatment at either 3 or 63 days of age (8 pigs/treatment/age/time after treatment; n = 96). Tail amputation induced marked changes in gene expression (up and down) compared to sham-treated intact controls for all treatment ages and time points after tail treatment. Sustained changes in gene expression in tail amputated pigs were still evident 4 months after tail injury. Gene correlation network analysis revealed two co-expression clusters associated with amputation: Cluster A (759 down-regulated) and Cluster B (273 up-regulated) genes. Gene ontology (GO) enrichment analysis identified 124 genes in Cluster A and 61 genes in Cluster B associated with both “inflammatory pain” and “neuropathic pain.” In Cluster A, gene family members of ion channels e.g., voltage-gated potassium channels (VGPC) and receptors e.g., GABA receptors, were significantly down-regulated compared to shams, both of which are linked to increased peripheral nerve excitability after axotomy. Up-regulated gene families in Cluster B were linked to transcriptional regulation, inflammation, tissue remodeling, and regulatory neuropeptide activity. These findings, demonstrate that tail amputation causes sustained transcriptomic expression changes in caudal DRG cells involved in inflammatory and neuropathic pain pathways. Frontiers Media S.A. 2019-09-18 /pmc/articles/PMC6760028/ /pubmed/31620455 http://dx.doi.org/10.3389/fvets.2019.00314 Text en Copyright © 2019 Sandercock, Barnett, Coe, Downing, Nirmal, Di Giminiani, Edwards and Freeman. http://creativecommons.org/licenses/by/4.0/ 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) and the copyright owner(s) 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 Veterinary Science
Sandercock, Dale A.
Barnett, Mark W.
Coe, Jennifer E.
Downing, Alison C.
Nirmal, Ajit J.
Di Giminiani, Pierpaolo
Edwards, Sandra A.
Freeman, Tom C.
Transcriptomics Analysis of Porcine Caudal Dorsal Root Ganglia in Tail Amputated Pigs Shows Long-Term Effects on Many Pain-Associated Genes
title Transcriptomics Analysis of Porcine Caudal Dorsal Root Ganglia in Tail Amputated Pigs Shows Long-Term Effects on Many Pain-Associated Genes
title_full Transcriptomics Analysis of Porcine Caudal Dorsal Root Ganglia in Tail Amputated Pigs Shows Long-Term Effects on Many Pain-Associated Genes
title_fullStr Transcriptomics Analysis of Porcine Caudal Dorsal Root Ganglia in Tail Amputated Pigs Shows Long-Term Effects on Many Pain-Associated Genes
title_full_unstemmed Transcriptomics Analysis of Porcine Caudal Dorsal Root Ganglia in Tail Amputated Pigs Shows Long-Term Effects on Many Pain-Associated Genes
title_short Transcriptomics Analysis of Porcine Caudal Dorsal Root Ganglia in Tail Amputated Pigs Shows Long-Term Effects on Many Pain-Associated Genes
title_sort transcriptomics analysis of porcine caudal dorsal root ganglia in tail amputated pigs shows long-term effects on many pain-associated genes
topic Veterinary Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6760028/
https://www.ncbi.nlm.nih.gov/pubmed/31620455
http://dx.doi.org/10.3389/fvets.2019.00314
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