Liver transcriptomics-metabolomics integration reveals biological pathways associated with fetal programming in beef cattle

Abstract We investigated the long-term effects of prenatal nutrition on pre-slaughter Nelore bulls using integrative transcriptome and metabolome analyses of liver tissue. Three prenatal nutritional treatments were administered to 126 cows: NP (control, mineral supplementation only), PP (protein-ene...

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Main Authors: Guilherme Henrique Gebim Polizel, Simara Larissa Fanalli, Wellison J. S. Diniz, Aline Silva Mello Cesar, Nara Regina Brandão Cônsolo, Heidge Fukumasu, Angela Cánovas, Arícia Christofaro Fernandes, Barbara Carolina Teixeira Prati, Édison Furlan, Gabriela do Vale Pombo, Miguel Henrique de Almeida Santana
Format: Article
Language:English
Published: Nature Portfolio 2024-11-01
Series:Scientific Reports
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Online Access:https://doi.org/10.1038/s41598-024-78965-4
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author Guilherme Henrique Gebim Polizel
Simara Larissa Fanalli
Wellison J. S. Diniz
Aline Silva Mello Cesar
Nara Regina Brandão Cônsolo
Heidge Fukumasu
Angela Cánovas
Arícia Christofaro Fernandes
Barbara Carolina Teixeira Prati
Édison Furlan
Gabriela do Vale Pombo
Miguel Henrique de Almeida Santana
author_facet Guilherme Henrique Gebim Polizel
Simara Larissa Fanalli
Wellison J. S. Diniz
Aline Silva Mello Cesar
Nara Regina Brandão Cônsolo
Heidge Fukumasu
Angela Cánovas
Arícia Christofaro Fernandes
Barbara Carolina Teixeira Prati
Édison Furlan
Gabriela do Vale Pombo
Miguel Henrique de Almeida Santana
author_sort Guilherme Henrique Gebim Polizel
collection DOAJ
description Abstract We investigated the long-term effects of prenatal nutrition on pre-slaughter Nelore bulls using integrative transcriptome and metabolome analyses of liver tissue. Three prenatal nutritional treatments were administered to 126 cows: NP (control, mineral supplementation only), PP (protein-energy supplementation in the third trimester), and FP (protein-energy supplementation throughout pregnancy). Liver samples from 22.5 ± 1-month-old bulls underwent RNA-Seq and targeted metabolomics. Weighted correlation network analysis (WGCNA) identified treatment-associated gene and metabolite co-expression modules, further analyzed using MetaboAnalyst 6.0 (metabolite over-representation analysis and transcriptome-metabolome integrative analysis) and Enrichr (gene over-representation analysis). We identified several significant gene and metabolite modules, as well as hub components associated with energy, protein and oxidative metabolism, regulatory mechanisms, epigenetics, and immune function. The NP transcriptome-metabolome analysis identified key pathways (aminoacyl t-RNA biosynthesis, gluconeogenesis, and PPAR signaling) and hub components (glutamic acid, SLC6A14). PP highlighted pathways (arginine and proline metabolism, TGF-beta signaling, glyoxylate and dicarboxylate metabolism) with arginine and ODC1 as hub components. This study highlights the significant impact of prenatal nutrition on the liver tissue of Nelore bulls, shedding light on critical metabolic pathways and hub components related to energy and protein metabolism, as well as immune system and epigenetics.
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spelling doaj-art-cc67340790ee45f3865c071f4b7877572025-02-02T12:24:57ZengNature PortfolioScientific Reports2045-23222024-11-0114112010.1038/s41598-024-78965-4Liver transcriptomics-metabolomics integration reveals biological pathways associated with fetal programming in beef cattleGuilherme Henrique Gebim Polizel0Simara Larissa Fanalli1Wellison J. S. Diniz2Aline Silva Mello Cesar3Nara Regina Brandão Cônsolo4Heidge Fukumasu5Angela Cánovas6Arícia Christofaro Fernandes7Barbara Carolina Teixeira Prati8Édison Furlan9Gabriela do Vale Pombo10Miguel Henrique de Almeida Santana11Department of Animal Science, Faculty of Animal Science and Food Engineering, University of São PauloDepartment of Animal Science, Faculty of Animal Science and Food Engineering, University of São PauloDepartment of Animal Sciences, College of Agriculture, Auburn UniversityDepartment of Food Science and Technology, Luiz de Queiroz College of Agriculture, University of São PauloDepartment of Nutrition and Animal Production, Faculty of Veterinary Medicine and Animal Science, University of São PauloDepartment of Veterinary Medicine, Faculty of Animal Science and Food Engineering, University of São PauloDepartment of Animal Biosciences, University of GuelphDepartment of Animal Science, Faculty of Animal Science and Food Engineering, University of São PauloDepartment of Animal Science, Faculty of Animal Science and Food Engineering, University of São PauloDepartment of Animal Science, Faculty of Animal Science and Food Engineering, University of São PauloDepartment of Animal Science, Faculty of Animal Science and Food Engineering, University of São PauloDepartment of Animal Science, Faculty of Animal Science and Food Engineering, University of São PauloAbstract We investigated the long-term effects of prenatal nutrition on pre-slaughter Nelore bulls using integrative transcriptome and metabolome analyses of liver tissue. Three prenatal nutritional treatments were administered to 126 cows: NP (control, mineral supplementation only), PP (protein-energy supplementation in the third trimester), and FP (protein-energy supplementation throughout pregnancy). Liver samples from 22.5 ± 1-month-old bulls underwent RNA-Seq and targeted metabolomics. Weighted correlation network analysis (WGCNA) identified treatment-associated gene and metabolite co-expression modules, further analyzed using MetaboAnalyst 6.0 (metabolite over-representation analysis and transcriptome-metabolome integrative analysis) and Enrichr (gene over-representation analysis). We identified several significant gene and metabolite modules, as well as hub components associated with energy, protein and oxidative metabolism, regulatory mechanisms, epigenetics, and immune function. The NP transcriptome-metabolome analysis identified key pathways (aminoacyl t-RNA biosynthesis, gluconeogenesis, and PPAR signaling) and hub components (glutamic acid, SLC6A14). PP highlighted pathways (arginine and proline metabolism, TGF-beta signaling, glyoxylate and dicarboxylate metabolism) with arginine and ODC1 as hub components. This study highlights the significant impact of prenatal nutrition on the liver tissue of Nelore bulls, shedding light on critical metabolic pathways and hub components related to energy and protein metabolism, as well as immune system and epigenetics.https://doi.org/10.1038/s41598-024-78965-4Maternal nutritionMetabolitesRNA-seqSystems biologyWGCNA
spellingShingle Guilherme Henrique Gebim Polizel
Simara Larissa Fanalli
Wellison J. S. Diniz
Aline Silva Mello Cesar
Nara Regina Brandão Cônsolo
Heidge Fukumasu
Angela Cánovas
Arícia Christofaro Fernandes
Barbara Carolina Teixeira Prati
Édison Furlan
Gabriela do Vale Pombo
Miguel Henrique de Almeida Santana
Liver transcriptomics-metabolomics integration reveals biological pathways associated with fetal programming in beef cattle
Scientific Reports
Maternal nutrition
Metabolites
RNA-seq
Systems biology
WGCNA
title Liver transcriptomics-metabolomics integration reveals biological pathways associated with fetal programming in beef cattle
title_full Liver transcriptomics-metabolomics integration reveals biological pathways associated with fetal programming in beef cattle
title_fullStr Liver transcriptomics-metabolomics integration reveals biological pathways associated with fetal programming in beef cattle
title_full_unstemmed Liver transcriptomics-metabolomics integration reveals biological pathways associated with fetal programming in beef cattle
title_short Liver transcriptomics-metabolomics integration reveals biological pathways associated with fetal programming in beef cattle
title_sort liver transcriptomics metabolomics integration reveals biological pathways associated with fetal programming in beef cattle
topic Maternal nutrition
Metabolites
RNA-seq
Systems biology
WGCNA
url https://doi.org/10.1038/s41598-024-78965-4
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