Cargando…

Hepatic Global Transcriptomic Profiles of Holstein Cows According to Parity Reveal Age-Related Changes in Early Lactation

Cows can live for over 20 years, but their productive lifespan averages only around 3 years after first calving. Liver dysfunction can reduce lifespan by increasing the risk of metabolic and infectious disease. This study investigated the changes in hepatic global transcriptomic profiles in early la...

Descripción completa

Detalles Bibliográficos
Autores principales: Cheng, Zhangrui, Ferris, Conrad, Crowe, Mark A., Ingvartsen, Klaus L., Grelet, Clément, Vanlierde, Amélie, Foldager, Leslie, Becker, Frank, Wathes, D. Claire
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10298156/
https://www.ncbi.nlm.nih.gov/pubmed/37373054
http://dx.doi.org/10.3390/ijms24129906
_version_ 1785064046143209472
author Cheng, Zhangrui
Ferris, Conrad
Crowe, Mark A.
Ingvartsen, Klaus L.
Grelet, Clément
Vanlierde, Amélie
Foldager, Leslie
Becker, Frank
Wathes, D. Claire
author_facet Cheng, Zhangrui
Ferris, Conrad
Crowe, Mark A.
Ingvartsen, Klaus L.
Grelet, Clément
Vanlierde, Amélie
Foldager, Leslie
Becker, Frank
Wathes, D. Claire
author_sort Cheng, Zhangrui
collection PubMed
description Cows can live for over 20 years, but their productive lifespan averages only around 3 years after first calving. Liver dysfunction can reduce lifespan by increasing the risk of metabolic and infectious disease. This study investigated the changes in hepatic global transcriptomic profiles in early lactation Holstein cows in different lactations. Cows from five herds were grouped as primiparous (lactation number 1, PP, 534.7 ± 6.9 kg, n = 41), or multiparous with lactation numbers 2–3 (MP2–3, 634.5 ± 7.5 kg, n = 87) or 4–7 (MP4–7, 686.6 ± 11.4 kg, n = 40). Liver biopsies were collected at around 14 days after calving for RNA sequencing. Blood metabolites and milk yields were measured, and energy balance was calculated. There were extensive differences in hepatic gene expression between MP and PP cows, with 568 differentially expressed genes (DEGs) between MP2–3 and PP cows, and 719 DEGs between MP4–7 and PP cows, with downregulated DEGs predominating in MP cows. The differences between the two age groups of MP cows were moderate (82 DEGs). The gene expression differences suggested that MP cows had reduced immune functions compared with the PP cows. MP cows had increased gluconeogenesis but also evidence of impaired liver functionality. The MP cows had dysregulated protein synthesis and glycerophospholipid metabolism, and impaired genome and RNA stability and nutrient transport (22 differentially expressed solute carrier transporters). The genes associated with cell cycle arrest, apoptosis, and the production of antimicrobial peptides were upregulated. More surprisingly, evidence of hepatic inflammation leading to fibrosis was present in the primiparous cows as they started their first lactation. This study has therefore shown that the ageing process in the livers of dairy cows is accelerated by successive lactations and increasing milk yields. This was associated with evidence of metabolic and immune disorders together with hepatic dysfunction. These problems are likely to increase involuntary culling, thus reducing the average longevity in dairy herds.
format Online
Article
Text
id pubmed-10298156
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher MDPI
record_format MEDLINE/PubMed
spelling pubmed-102981562023-06-28 Hepatic Global Transcriptomic Profiles of Holstein Cows According to Parity Reveal Age-Related Changes in Early Lactation Cheng, Zhangrui Ferris, Conrad Crowe, Mark A. Ingvartsen, Klaus L. Grelet, Clément Vanlierde, Amélie Foldager, Leslie Becker, Frank Wathes, D. Claire Int J Mol Sci Article Cows can live for over 20 years, but their productive lifespan averages only around 3 years after first calving. Liver dysfunction can reduce lifespan by increasing the risk of metabolic and infectious disease. This study investigated the changes in hepatic global transcriptomic profiles in early lactation Holstein cows in different lactations. Cows from five herds were grouped as primiparous (lactation number 1, PP, 534.7 ± 6.9 kg, n = 41), or multiparous with lactation numbers 2–3 (MP2–3, 634.5 ± 7.5 kg, n = 87) or 4–7 (MP4–7, 686.6 ± 11.4 kg, n = 40). Liver biopsies were collected at around 14 days after calving for RNA sequencing. Blood metabolites and milk yields were measured, and energy balance was calculated. There were extensive differences in hepatic gene expression between MP and PP cows, with 568 differentially expressed genes (DEGs) between MP2–3 and PP cows, and 719 DEGs between MP4–7 and PP cows, with downregulated DEGs predominating in MP cows. The differences between the two age groups of MP cows were moderate (82 DEGs). The gene expression differences suggested that MP cows had reduced immune functions compared with the PP cows. MP cows had increased gluconeogenesis but also evidence of impaired liver functionality. The MP cows had dysregulated protein synthesis and glycerophospholipid metabolism, and impaired genome and RNA stability and nutrient transport (22 differentially expressed solute carrier transporters). The genes associated with cell cycle arrest, apoptosis, and the production of antimicrobial peptides were upregulated. More surprisingly, evidence of hepatic inflammation leading to fibrosis was present in the primiparous cows as they started their first lactation. This study has therefore shown that the ageing process in the livers of dairy cows is accelerated by successive lactations and increasing milk yields. This was associated with evidence of metabolic and immune disorders together with hepatic dysfunction. These problems are likely to increase involuntary culling, thus reducing the average longevity in dairy herds. MDPI 2023-06-08 /pmc/articles/PMC10298156/ /pubmed/37373054 http://dx.doi.org/10.3390/ijms24129906 Text en © 2023 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Cheng, Zhangrui
Ferris, Conrad
Crowe, Mark A.
Ingvartsen, Klaus L.
Grelet, Clément
Vanlierde, Amélie
Foldager, Leslie
Becker, Frank
Wathes, D. Claire
Hepatic Global Transcriptomic Profiles of Holstein Cows According to Parity Reveal Age-Related Changes in Early Lactation
title Hepatic Global Transcriptomic Profiles of Holstein Cows According to Parity Reveal Age-Related Changes in Early Lactation
title_full Hepatic Global Transcriptomic Profiles of Holstein Cows According to Parity Reveal Age-Related Changes in Early Lactation
title_fullStr Hepatic Global Transcriptomic Profiles of Holstein Cows According to Parity Reveal Age-Related Changes in Early Lactation
title_full_unstemmed Hepatic Global Transcriptomic Profiles of Holstein Cows According to Parity Reveal Age-Related Changes in Early Lactation
title_short Hepatic Global Transcriptomic Profiles of Holstein Cows According to Parity Reveal Age-Related Changes in Early Lactation
title_sort hepatic global transcriptomic profiles of holstein cows according to parity reveal age-related changes in early lactation
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10298156/
https://www.ncbi.nlm.nih.gov/pubmed/37373054
http://dx.doi.org/10.3390/ijms24129906
work_keys_str_mv AT chengzhangrui hepaticglobaltranscriptomicprofilesofholsteincowsaccordingtoparityrevealagerelatedchangesinearlylactation
AT ferrisconrad hepaticglobaltranscriptomicprofilesofholsteincowsaccordingtoparityrevealagerelatedchangesinearlylactation
AT crowemarka hepaticglobaltranscriptomicprofilesofholsteincowsaccordingtoparityrevealagerelatedchangesinearlylactation
AT ingvartsenklausl hepaticglobaltranscriptomicprofilesofholsteincowsaccordingtoparityrevealagerelatedchangesinearlylactation
AT greletclement hepaticglobaltranscriptomicprofilesofholsteincowsaccordingtoparityrevealagerelatedchangesinearlylactation
AT vanlierdeamelie hepaticglobaltranscriptomicprofilesofholsteincowsaccordingtoparityrevealagerelatedchangesinearlylactation
AT foldagerleslie hepaticglobaltranscriptomicprofilesofholsteincowsaccordingtoparityrevealagerelatedchangesinearlylactation
AT beckerfrank hepaticglobaltranscriptomicprofilesofholsteincowsaccordingtoparityrevealagerelatedchangesinearlylactation
AT wathesdclaire hepaticglobaltranscriptomicprofilesofholsteincowsaccordingtoparityrevealagerelatedchangesinearlylactation
AT hepaticglobaltranscriptomicprofilesofholsteincowsaccordingtoparityrevealagerelatedchangesinearlylactation