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Nutrient supply alters transcriptome regulation in adipose tissue of pre-weaning Holstein calves.

ABSTRACT: Performance of dairy cows can be influenced by early life nutrient supply. Adipose tissue is diet sensitive and an important component in that process as it is involved in the regulation of energetic, reproductive and immunological functions. However, it is not clear how early life nutrition alters the molecular regulation of adipose tissue in calves and potentially adult individuals. This study aimed at determining how differences in pre-weaning nutrient supply alter gene expression profiles and physiology in omental adipose tissue. A total of 12 female Holstein calves were fed two levels of milk replacer supply: a restricted amount of 11.72 MJ of metabolizable energy (ME) intake per day (n = 6) or an enhanced amount of 1.26 MJ ME intake per kg of metabolic body weight (BW0.75), resulting in supply from 17.58 to 35.17 MJ ME intake per day (n = 6). All calves had ad libitum access to a commercial calf starter and water. Analysis of the transcriptome profiles at 54 ± 2 days of age revealed that a total of 396 out of 19,968 genes were differentially expressed (DE) between groups (p < 0.001, FDR < 0.1). The directional expression of DE genes through Ingenuity Pathway Analysis showed that an enhanced nutrient supply alters adipose tissue physiology of pre-weaned calves. Several biological functions were increased (Z-score > +2), including Lipid Metabolism (Fatty Acid Metabolism), Cell Cycle (Entry into Interphase, Interphase, Mitosis and Cell Cycle Progression), Cellular Assembly and Organization (Cytoskeleton Formation and Cytoplasm Development) and Molecular Transport (Transport of Carboxylic Acid). These changes were potentially orchestrated by the activation/inhibition of 17 upstream regulators genes. Our findings indicate that adipose tissue of calves under an enhanced nutrient supply is physiologically distinct from restricted calves due to an increased development/expansion rate and also a higher metabolic activity through increased fatty acid metabolism.

SUBMITTER: Leal LN

PROVIDER: S-EPMC6078305 | biostudies-literature | 2018

REPOSITORIES: biostudies-literature

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Nutrient supply alters transcriptome regulation in adipose tissue of pre-weaning Holstein calves.

Leal Leonel N LN Romao Josue M JM Hooiveld Guido J GJ Soberon Fernando F Berends Harma H Boekshoten Mark V MV Van Amburgh Michael E ME Martín-Tereso Javier J Steele Michael A MA

PloS one 20180806 8

Performance of dairy cows can be influenced by early life nutrient supply. Adipose tissue is diet sensitive and an important component in that process as it is involved in the regulation of energetic, reproductive and immunological functions. However, it is not clear how early life nutrition alters the molecular regulation of adipose tissue in calves and potentially adult individuals. This study aimed at determining how differences in pre-weaning nutrient supply alter gene expression profiles an ...[more]

PMID: 30080895

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Project description:The objective of this study was to analyze the mammary gland transcriptome to determine how preweaning nutrient supply alters the molecular mechanisms that regulate preweaning mammary development. Holstein heifers were fed via milk replacer either an elevated level of nutrient intake (ELE; on average, 5.9 ± 0.2 Mcal ME in 8.4 L of milk replacer (MR)/d, n = 6) or a restricted amount of nutrients (RES; 2.8 ± 0.2 Mcal ME in 4L MR/day, n = 5) for 54 d postnatal, at which point they were slaughtered and samples of mammary parenchyma tissue were obtained. Parenchymal mRNA was analyzed and the fold changes (FC) of 18,111 genes (ELE relative to RES) were uploaded to Ingenuity Pathway Analysis (IPA) software for transcriptomic analysis. Using a threshold of P < 0.05, IPA identified that the FC of 1,931 of 18,811 differentially expressed genes (DEG) could be utilized for the analysis. A total 18 molecular and cellular functions were relevant (P < 0.05) to DE genes arising from the treatments, with Cell Death and Survival, Cellular Movement, Cellular Development, Cellular Growth and Proliferation, and Lipid Metabolism being the 5 most associated functions with DEG. Based on the directional FC of DEG, the mammary gland of ELE heifers was predicted to have increased Epithelial-Mesenchymal Transition (Z = 2.685) and Accumulation of Lipid (Z = 2.322), while the Synthesis of DNA (Z = -2.137), Transactivation of RNA (Z = -2.254), Expression of RNA (Z = -2.405), Transcription (Z = -2.482) and Transactivation (Z = -2.611) were all predicted to be decreased. Additionally, IPA predicted the activation status of 13 upstream regulators with direct influence on DEG as affected by ELE feeding that were either ligand-dependent nuclear receptors (n = 2), enzyme (n = 1), or transcription regulators (n = 10). Of these, 6 were activated (Z > 2) and 7 were inhibited (Z < -2). In summary, feeding ELE preweaning altered the mammary transcriptome of Holstein heifers affecting cell functions involved in the morphological and physiological development of the mammary gland.

Project description:BackgroundThe aim of the study was to investigate the effect of energy overfeeding during the dry period on adipose tissue transcriptome profiles during the periparturient period in dairy cows.MethodsFourteen primiparous Holstein cows from a larger cohort receiving a higher-energy diet (1.62 Mcal of net energy for lactation/kg of dry matter; 15% crude protein) for ad libitum intake to supply 150% (OVR) or 100% (CTR) of energy requirements from dry off until parturition were used. After calving, all cows received the same lactation diet. Subcutaneous adipose tissue (SAT) biopsies were collected at - 14, 1, and 14 d from parturition (d) and used for transcriptome profiling using a bovine oligonucleotide microarray. Data mining of differentially expressed genes (DEG) between treatments and due to sampling time was performed using the Dynamic Impact Approach (DIA) and Ingenuity Pathway Analysis (IPA).ResultsThere was a strong effect of over-feeding energy on DEG with 2434 (False discovery rate-corrected P < 0.05) between OVR and CTR at - 14 d, and only 340 and 538 at 1 and 14 d. The most-impacted and activated pathways in the Kyoto Encyclopedia of Genes and Genomes (KEGG) database that were highlighted by DIA analysis at - 14 d in OVR vs. CTR included 9 associated with carbohydrate metabolism, with 'Pyruvate metabolism', 'Glycolysis/gluconeogenesis', and 'Pentose phosphate pathway' among the most-activated. Not surprisingly, OVR led to marked activation of lipid metabolism (e.g. 'Fatty acid biosynthesis' and 'Glycerolipid metabolism'). Unexpected metabolic pathways that were activated at - 14 d in OVR included several related to metabolism of amino acids (e.g. branched chain) and of cofactors and vitamins (thiamin). Among endocrine and immune system pathways, at - 14 d OVR led to marked activation of 'PPAR signalling' and 'Antigen processing and presentation'. Among key pathways affected over time in OVR, a number were related to translation (e.g. mTOR signaling), endocrine/immune signaling (CXCR4 and IGF1), and lipid metabolism (oxidative phosphorylation) with greater activation in OVR vs. CTR specifically at - 14 d. Although statistical differences for several pathways in OVR vs. CTR nearly disappeared at 1 and 14 vs. - 14 d, despite the well-known catabolic state of adipose depots after calving, the bioinformatics analyses suggested important roles for a number of signaling mechanisms at - 14 vs. 14 than 1 vs. -14 d. This was particularly evident in cows fed to meet predicted energy requirements during the dry period (CTR).ConclusionsData underscored a strong activation by overfeeding energy of anabolic processes in the SAT exclusively prepartum. The study confirmed that higher-energy diets prepartum drive a transcriptional cascade of events orchestrated in part by the activation of PPARγ that regulate preadipocyte differentiation and lipid storage in SAT. Novel aspects of SAT biology to energy overfeeding or change in physiologic state also were uncovered, including the role of amino acid metabolism, mTOR signaling, and the immune system.

Dataset Information

Nutrient supply alters transcriptome regulation in adipose tissue of pre-weaning Holstein calves.

Publications

Nutrient supply alters transcriptome regulation in adipose tissue of pre-weaning Holstein calves.

Similar Datasets

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