Combined Transcriptomics and Metabolomics Identify Regulatory Mechanisms of Porcine Vertebral Chondrocyte Development In Vitro

Mingming Xue; Ning Huang; Yabiao Luo; Xiaoyang Yang; Yubei Wang; Meiying Fang

doi:10.3390/ijms25021189

International Journal of Molecular Sciences (Jan 2024)

Combined Transcriptomics and Metabolomics Identify Regulatory Mechanisms of Porcine Vertebral Chondrocyte Development In Vitro

Mingming Xue,
Ning Huang,
Yabiao Luo,
Xiaoyang Yang,
Yubei Wang,
Meiying Fang

Affiliations

Mingming Xue: Department of Animal Genetics and Breeding, National Engineering Laboratory for Animal Breeding, MOA Key Laboratory of Animal Genetics and Breeding, Beijing Key Laboratory for Animal Genetic Improvement, State Key Laboratory of Animal Biotech Breeding, Frontiers Science Center for Molecular Design Breeding, College of Animal Science and Technology, China Agricultural University, Beijing 100193, China
Ning Huang: Sanya Research Institute, China Agricultural University, Sanya 572025, China
Yabiao Luo: Department of Animal Genetics and Breeding, National Engineering Laboratory for Animal Breeding, MOA Key Laboratory of Animal Genetics and Breeding, Beijing Key Laboratory for Animal Genetic Improvement, State Key Laboratory of Animal Biotech Breeding, Frontiers Science Center for Molecular Design Breeding, College of Animal Science and Technology, China Agricultural University, Beijing 100193, China
Xiaoyang Yang: Department of Animal Genetics and Breeding, National Engineering Laboratory for Animal Breeding, MOA Key Laboratory of Animal Genetics and Breeding, Beijing Key Laboratory for Animal Genetic Improvement, State Key Laboratory of Animal Biotech Breeding, Frontiers Science Center for Molecular Design Breeding, College of Animal Science and Technology, China Agricultural University, Beijing 100193, China
Yubei Wang: Sanya Research Institute, China Agricultural University, Sanya 572025, China
Meiying Fang: Department of Animal Genetics and Breeding, National Engineering Laboratory for Animal Breeding, MOA Key Laboratory of Animal Genetics and Breeding, Beijing Key Laboratory for Animal Genetic Improvement, State Key Laboratory of Animal Biotech Breeding, Frontiers Science Center for Molecular Design Breeding, College of Animal Science and Technology, China Agricultural University, Beijing 100193, China

DOI: https://doi.org/10.3390/ijms25021189
Journal volume & issue: Vol. 25, no. 2
p. 1189

Abstract

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Porcine body length is closely related to meat production, growth, and reproductive performance, thus playing a key role in the profitability of the pork industry. Cartilage development is critical to longitudinal elongation of individual vertebrae. This study isolated primary porcine vertebral chondrocytes (PVCs) to clarify the complex mechanisms of elongation. We used transcriptome and target energy metabolome technologies to confirm crucial genes and metabolites in primary PVCs at different differentiation stages (0, 4, 8, and 12 days). Pairwise comparisons of the four stages identified 4566 differentially expressed genes (DEGs). Time-series gene cluster and functional analyses of these DEGs revealed four clusters related to metabolic processes, cartilage development, vascular development, and cell cycle regulation. We constructed a transcriptional regulatory network determining chondrocyte maturation. The network indicated that significantly enriched transcription factor (TF) families, including zf-C2H2, homeobox, TF_bZIP, and RHD, are important in cell cycle and differentiation processes. Further, dynamic network biomarker (DNB) analysis revealed that day 4 was the tipping point for chondrocyte development, consistent with morphological and metabolic changes. We found 24 DNB DEGs, including the TFs NFATC2 and SP7. Targeted energy metabolome analysis showed that most metabolites were elevated throughout chondrocyte development; notably, 16 differentially regulated metabolites (DRMs) were increased at three time points after cell differentiation. In conclusion, integrated metabolome and transcriptome analyses highlighted the importance of amino acid biosynthesis in chondrocyte development, with coordinated regulation of DEGs and DRMs promoting PVC differentiation via glucose oxidation. These findings reveal the regulatory mechanisms underlying PVC development and provide an important theoretical reference for improving pork production.

Published in International Journal of Molecular Sciences

ISSN: 1661-6596 (Print); 1422-0067 (Online)
Publisher: MDPI AG
Country of publisher: Switzerland
LCC subjects: Science: Biology (General); Science: Chemistry
Website: http://www.mdpi.com/journal/ijms

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