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...
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MDPI AG
2023-06-01
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| Series: | International Journal of Molecular Sciences |
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| Online Access: | https://www.mdpi.com/1422-0067/24/12/9906 |
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| author | Zhangrui Cheng Conrad Ferris Mark A. Crowe Klaus L. Ingvartsen Clément Grelet Amélie Vanlierde Leslie Foldager Frank Becker D. Claire Wathes the GplusE Consortium |
| author_facet | Zhangrui Cheng Conrad Ferris Mark A. Crowe Klaus L. Ingvartsen Clément Grelet Amélie Vanlierde Leslie Foldager Frank Becker D. Claire Wathes the GplusE Consortium |
| author_sort | Zhangrui Cheng |
| collection | DOAJ |
| 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, <i>n</i> = 41), or multiparous with lactation numbers 2–3 (MP2–3, 634.5 ± 7.5 kg, <i>n</i> = 87) or 4–7 (MP4–7, 686.6 ± 11.4 kg, <i>n</i> = 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. |
| first_indexed | 2024-03-11T02:22:48Z |
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| issn | 1661-6596 1422-0067 |
| language | English |
| last_indexed | 2024-03-11T02:22:48Z |
| publishDate | 2023-06-01 |
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| spelling | doaj.art-bfd4deb6553b43098d8626797074e08b2023-11-18T10:45:49ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672023-06-012412990610.3390/ijms24129906Hepatic Global Transcriptomic Profiles of Holstein Cows According to Parity Reveal Age-Related Changes in Early LactationZhangrui Cheng0Conrad Ferris1Mark A. Crowe2Klaus L. Ingvartsen3Clément Grelet4Amélie Vanlierde5Leslie Foldager6Frank Becker7D. Claire Wathes8the GplusE ConsortiumDepartment of Pathobiology and Population Sciences, Royal Veterinary College, Hawkshead Lane, North Mymms, Hatfield, Herts AL9 7TA, UKAgri-Food and Biosciences Institute, Newforge Lane, Upper Malone Road, Belfast BT9 5PX, UKSchool of Veterinary Medicine, University College Dublin, Belfield, D04 V1W8 Dublin, IrelandDepartment of Animal and Veterinary Sciences, Aarhus University, Blichers Allé 20, 8830 Tjele, DenmarkValorisation of Agricultural Products Department, Walloon Agricultural Research Centre, 5030 Gembloux, BelgiumValorisation of Agricultural Products Department, Walloon Agricultural Research Centre, 5030 Gembloux, BelgiumDepartment of Animal and Veterinary Sciences, Aarhus University, Blichers Allé 20, 8830 Tjele, DenmarkResearch Institute for Farm Animal Biology, Wilhelm-Stahl-Allee 2, 18196 Dummerstorf, GermanyDepartment of Pathobiology and Population Sciences, Royal Veterinary College, Hawkshead Lane, North Mymms, Hatfield, Herts AL9 7TA, UKCows 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, <i>n</i> = 41), or multiparous with lactation numbers 2–3 (MP2–3, 634.5 ± 7.5 kg, <i>n</i> = 87) or 4–7 (MP4–7, 686.6 ± 11.4 kg, <i>n</i> = 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.https://www.mdpi.com/1422-0067/24/12/9906liverageingcellular senescencetranscriptomeimmunitymetabolism |
| spellingShingle | Zhangrui Cheng Conrad Ferris Mark A. Crowe Klaus L. Ingvartsen Clément Grelet Amélie Vanlierde Leslie Foldager Frank Becker D. Claire Wathes the GplusE Consortium Hepatic Global Transcriptomic Profiles of Holstein Cows According to Parity Reveal Age-Related Changes in Early Lactation International Journal of Molecular Sciences liver ageing cellular senescence transcriptome immunity metabolism |
| 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 | liver ageing cellular senescence transcriptome immunity metabolism |
| url | https://www.mdpi.com/1422-0067/24/12/9906 |
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