Early milk-feeding regimes in calves exert long-term effects on the development of ovarian granulosa cells
Abstract Background Nutrition has not only an impact on the general wellbeing of an animal but can also affect reproductive processes. In cattle, feeding regimes can influence the age of puberty onset and alter gonadal development. We analyzed effects of different milk replacer (MR) feeding regimes...
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| Format: | Article |
| Language: | English |
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BMC
2023-08-01
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| Series: | BMC Genomics |
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| Online Access: | https://doi.org/10.1186/s12864-023-09589-7 |
| _version_ | 1797453811336347648 |
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| author | Volker Röttgen Lisa-Maria Tümmler Dirk Koczan Alexander Rebl Björn Kuhla Jens Vanselow Anja Baufeld |
| author_facet | Volker Röttgen Lisa-Maria Tümmler Dirk Koczan Alexander Rebl Björn Kuhla Jens Vanselow Anja Baufeld |
| author_sort | Volker Röttgen |
| collection | DOAJ |
| description | Abstract Background Nutrition has not only an impact on the general wellbeing of an animal but can also affect reproductive processes. In cattle, feeding regimes can influence the age of puberty onset and alter gonadal development. We analyzed effects of different milk replacer (MR) feeding regimes during rearing on ovarian physiology with specific emphasis on the numbers as well as gene expression characteristics of granulosa cells (GCs) at the age of puberty onset. Two groups of calves received either 10% or 20% of bodyweight MR per day during their first 8 weeks. After weaning, both groups were fed the same mixed ration ad libitum until slaughter at 8 months. Results Animals of the 20% feeding group had a significantly higher body weight, but the proportion of animals having a corpus luteum at the time of slaughter was not different between groups, suggesting a similar onset of puberty. Calves of the 10% group showed a constant GC count regardless of the number of follicles (r = 0.23) whereas in the 20% group increasing numbers of GCs were detected with a higher follicle count (r = 0.71). As a first effort to find a possible molecular explanation for this unexpected limitation of GC numbers in the 10% group, we comparatively analyzed GC transcriptomes in both diet groups. The mRNA microarray analysis revealed a total of 557 differentially expressed genes comparing both groups (fold change > |1.5| and p < 0.05). OAS1X, MX2 and OAS1Z were among the top downregulated genes in the 20% vs. the 10% group, whereas top upregulated genes comprised BOLA and XCL1. All of these genes are known to be regulated by interferon. Subsequent signaling pathway analysis revealed the involvement of several immune response mechanisms in accordance with a number of interferons as upstream regulators. Conclusions The results indicate that the plane of MR feeding in early life has an impact on the number and physiology of GCs later in life. This might influence the overall reproductive life initiated by the onset of puberty in cattle. In addition, the observed alterations in GCs of calves fed less MR might be a consequence of interferon regulated immunological pathways. |
| first_indexed | 2024-03-09T15:28:15Z |
| format | Article |
| id | doaj.art-689662c7267b4c2297c606aae91d0ccf |
| institution | Directory Open Access Journal |
| issn | 1471-2164 |
| language | English |
| last_indexed | 2024-03-09T15:28:15Z |
| publishDate | 2023-08-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Genomics |
| spelling | doaj.art-689662c7267b4c2297c606aae91d0ccf2023-11-26T12:25:15ZengBMCBMC Genomics1471-21642023-08-0124111310.1186/s12864-023-09589-7Early milk-feeding regimes in calves exert long-term effects on the development of ovarian granulosa cellsVolker Röttgen0Lisa-Maria Tümmler1Dirk Koczan2Alexander Rebl3Björn Kuhla4Jens Vanselow5Anja Baufeld6Research Institute for Farm Animal Biology (FBN)Research Institute for Farm Animal Biology (FBN)Institute for Immunology, University of RostockResearch Institute for Farm Animal Biology (FBN)Research Institute for Farm Animal Biology (FBN)Research Institute for Farm Animal Biology (FBN)Research Institute for Farm Animal Biology (FBN)Abstract Background Nutrition has not only an impact on the general wellbeing of an animal but can also affect reproductive processes. In cattle, feeding regimes can influence the age of puberty onset and alter gonadal development. We analyzed effects of different milk replacer (MR) feeding regimes during rearing on ovarian physiology with specific emphasis on the numbers as well as gene expression characteristics of granulosa cells (GCs) at the age of puberty onset. Two groups of calves received either 10% or 20% of bodyweight MR per day during their first 8 weeks. After weaning, both groups were fed the same mixed ration ad libitum until slaughter at 8 months. Results Animals of the 20% feeding group had a significantly higher body weight, but the proportion of animals having a corpus luteum at the time of slaughter was not different between groups, suggesting a similar onset of puberty. Calves of the 10% group showed a constant GC count regardless of the number of follicles (r = 0.23) whereas in the 20% group increasing numbers of GCs were detected with a higher follicle count (r = 0.71). As a first effort to find a possible molecular explanation for this unexpected limitation of GC numbers in the 10% group, we comparatively analyzed GC transcriptomes in both diet groups. The mRNA microarray analysis revealed a total of 557 differentially expressed genes comparing both groups (fold change > |1.5| and p < 0.05). OAS1X, MX2 and OAS1Z were among the top downregulated genes in the 20% vs. the 10% group, whereas top upregulated genes comprised BOLA and XCL1. All of these genes are known to be regulated by interferon. Subsequent signaling pathway analysis revealed the involvement of several immune response mechanisms in accordance with a number of interferons as upstream regulators. Conclusions The results indicate that the plane of MR feeding in early life has an impact on the number and physiology of GCs later in life. This might influence the overall reproductive life initiated by the onset of puberty in cattle. In addition, the observed alterations in GCs of calves fed less MR might be a consequence of interferon regulated immunological pathways.https://doi.org/10.1186/s12864-023-09589-7Gene expressionFollicle countInnate immune systemInterferonPlane of nutrition |
| spellingShingle | Volker Röttgen Lisa-Maria Tümmler Dirk Koczan Alexander Rebl Björn Kuhla Jens Vanselow Anja Baufeld Early milk-feeding regimes in calves exert long-term effects on the development of ovarian granulosa cells BMC Genomics Gene expression Follicle count Innate immune system Interferon Plane of nutrition |
| title | Early milk-feeding regimes in calves exert long-term effects on the development of ovarian granulosa cells |
| title_full | Early milk-feeding regimes in calves exert long-term effects on the development of ovarian granulosa cells |
| title_fullStr | Early milk-feeding regimes in calves exert long-term effects on the development of ovarian granulosa cells |
| title_full_unstemmed | Early milk-feeding regimes in calves exert long-term effects on the development of ovarian granulosa cells |
| title_short | Early milk-feeding regimes in calves exert long-term effects on the development of ovarian granulosa cells |
| title_sort | early milk feeding regimes in calves exert long term effects on the development of ovarian granulosa cells |
| topic | Gene expression Follicle count Innate immune system Interferon Plane of nutrition |
| url | https://doi.org/10.1186/s12864-023-09589-7 |
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