Animal Bioscience

  • 제36권3호
  • /
  • Pages.404-416
  • /
  • 2023
  • /
  • 2765-0189(pISSN)
  • /
  • 2765-0235(eISSN)
아세아태평양축산학회 (Asian Australasian Association of Animal Production Societies)
권호 표지
DOI QR코드

DOI QR Code

Comprehensive analysis of miRNAs, lncRNAs and mRNAs profiles in backfat tissue between Daweizi and Yorkshire pigs

  • Chen Chen (Hunan Institute of Animal and Veterinary Science) ;
  • Yitong Chang (College of Animal Science and Technology, Hunan Agricultural University) ;
  • Yuan Deng (Hunan Institute of Animal and Veterinary Science) ;
  • Qingming Cui (Hunan Institute of Animal and Veterinary Science) ;
  • Yingying Liu (Hunan Institute of Animal and Veterinary Science) ;
  • Huali Li (Hunan Institute of Animal and Veterinary Science) ;
  • Huibo Ren (Hunan Institute of Animal and Veterinary Science) ;
  • Ji Zhu (Hunan Institute of Animal and Veterinary Science) ;
  • Qi Liu (Hunan Tianfu Ecological Agricultural Limited Company) ;
  • Yinglin Peng (Hunan Institute of Animal and Veterinary Science)
  • 투고 : 2022.04.24
  • 심사 : 2022.09.11
  • 발행 : 2023.03.01
PDF 다운로드
⟨ 이전 논문 다음 논문 ⟩

초록

Objective: Daweizi (DWZ) is a famous indigenous pig breed in China and characterized by tender meat and high fat percentage. However, the expression profiles and functions of transcripts in DWZ pigs is still in infancy. The object of this study was to depict the transcript profiles in DWZ pigs and screen the potential pathway influence adipogenesis and fat deposition, Methods: Histological analysis of backfat tissue was firstly performed between DWZ and lean-type Yorkshire pigs, and then RNA sequencing technology was utilized to explore miRNAs, lncRNAs and mRNAs profiles in backfat tissue. 18 differentially expressed (DE) transcripts were randomly selected for quantitative real-time polymerase chain reaction (QPCR) to validate the reliability of the sequencing results. Finally, gene ontology (GO) and Kyoto encyclopedia of genes and genomes (KEGG) enrichment analysis were conducted to investigate the potential pathways influence adipocyte differentiation, adipogenesis and lipid metabolism, and a schematic model was further proposed. Results: A total of 1,625 differentially expressed transcripts were identified in DWZ pigs, including 27 upregulated and 45 downregulated miRNAs, 64 upregulated and 119 down-regulated lncRNA, 814 upregulated and 556 downregulated mRNAs. QPCR analysis exhibited strong consistency with the sequencing data. GO and KEGG analysis elucidated that the differentially expressed transcripts were mainly associated with cell growth and death, signal transduction, peroxisome proliferator-activated receptors (PPAR), AMP-activated protein kinase (AMPK), PI3K-Akt, adipocytokine and foxo signaling pathways, all of which are strongly involved in cell development, lipid metabolism and adipogenesis. Further analysis indicated that the BGIR9823_87926/miR-194a-5p/AQP7 network may be effective in the process of adipocyte differentiation or adipogenesis. Conclusion: Our study provides comprehensive insights into the regulatory network of backfat deposition and lipid metabolism in pigs from the point of view of miRNAs, lncRNAs and mRNAs.

키워드

과제정보

This work was supported by the Natural Science Foundation of Hunan Province (2021JJ30386), Innovation Platform and Talent Plan Program of Hunan Province (2021NK1009), Key Research and Development Program of Hunan Province (2020NK2024), Open Research Program of Hunan Provincial Key Laboratory (2017TP1030), Changsha·China Longping Seed Industry Silicon Valley Program (2020) and Modern Swine Industry Technology System of Hunan Province.

참고문헌

  1. Davoli R, Gaffo E, Zappaterra M, Bortoluzzi S, Zambonelli P. Identification of differentially expressed small RNAs and prediction of target genes in Italian Large White pigs with divergent backfat deposition. Anim Genet 2018;49:205-14. https://doi.org/10.1111/age.12646
  2. Medina-Remon A, Kirwan R, Lamuela-Raventos RM, Estruch R. Dietary patterns and the risk of obesity, type 2 diabetes mellitus, cardiovascular diseases, asthma, and neurodegenerative diseases. Crit Rev Food Sci Nutr 2018;58:262-96. https://doi.org/10.1080/10408398.2016.1158690
  3. Spurlock ME, Gabler NK. The development of porcine models of obesity and the metabolic syndrome. J Nutr 2008;138:397-402. https://doi.org/10.1093/jn/138.2.397
  4. Hou X, Yang Y, Zhu S, et al. Comparison of skeletal muscle miRNA and mRNA profiles among three pig breeds. Mol Genet Genomics 2016;291:559-73. https://doi.org/10.1007/s00438-015-1126-3
  5. Chen C, Deng B, Qiao M, et al. Solexa sequencing identification of conserved and novel microRNAs in backfat of Large White and Chinese Meishan pigs. PLoS One 2012;7:e31426. https://doi.org/10.1371/journal.pone.0031426
  6. Chen C, Cui Q, Zhang X, et al. Long non-coding RNAs regulation in adipogenesis and lipid metabolism: emerging insights in obesity. Cell Signal 2018;51:47-58. https://doi.org/10.1016/j.cellsig.2018.07.012
  7. Gharanei S, Shabir K, Brown JE, et al. Regulatory microRNAs in brown, brite and white adipose tissue. Cells 2020;9:2489. https://doi.org/10.3390/cells9112489
  8. Huang W, Zhang X, Li A, Xie L, Miao X. Differential regulation of mRNAs and lncRNAs related to lipid metabolism in two pig breeds. Oncotarget 2017;8:87539-53. https://doi.org/10.18632/oncotarget.20978
  9. Yu L, Tai L, Zhang L, Chu Y, Li Y, Zhou L. Comparative analyses of long non-coding RNA in lean and obese pig. Oncotarget 2017;8:41440-50. https://doi.org/10.18632/oncotarget.18269
  10. Liu X, Liu K, Shan B, et al. A genome-wide landscape of mRNAs, lncRNAs, and circRNAs during subcutaneous adipogenesis in pigs. J Anim Sci Biotechnol 2018;9:76. https://doi.org/10.1186/s40104-018-0292-7
  11. Miao Z, Wang S, Zhang J, et al. Identification and comparison of long non-conding RNA in Jinhua and Landrace pigs. Biochem Biophys Res Commun 2018;506:765-71. https://doi.org/10.1016/j.bbrc.2018.06.028
  12. Sun Y, Chen X, Qin J, et al. Comparative analysis of long noncoding RNAs expressed during intramuscular adipocytes adipogenesis in fat-type and lean-type pigs. J Agric Food Chem 2018;66:12122-30. https://doi.org/10.1021/acs.jafc.8b04243
  13. Kumar H, Srikanth K, Park W, et al. Transcriptome analysis to identify long non coding RNA (lncRNA) and characterize their functional role in back fat tissue of pig. Gene 2019;703:71-82. https://doi.org/10.1016/j.gene.2019.04.014
  14. Xu D, He C, Li Q, He J, Ma H. The complete mitochondrial genome of the Daweizi pig. Mitochondrial DNA 2015;26:640-1. https://doi.org/10.3109/19401736.2013.836514
  15. Chen C, Ridzon DA, Broomer AJ, et al. Real-time quantification of microRNAs by stem-loop RT-PCR. Nucleic Acids Res 2005;33:e179. https://doi.org/10.1093/nar/gni178
  16. Zhang D, Wu W, Huang X, Xu K, Zheng C, Zhang J. Comparative analysis of gene expression profiles in differentiated subcutaneous adipocytes between Jiaxing Black and Large White pigs. BMC Genomics 2021;22:61. https://doi.org/10.1186/s12864-020-07361-9
  17. Zhang X, Wang Y, Su Y, Zuo F, Wu B, Nian X. MiR-26a regulated adipogenic differentiation of ADSCs induced by insulin through CDK5/FOXC2 pathway. Mol Cell Biochem 2021;476:1705-16. https://doi.org/10.1007/s11010-020-04033-w
  18. Tang R, Ma F, Li W, Ouyang S, Liu Z, Wu J. miR-206-3p inhibits 3T3-L1 cell adipogenesis via the c-Met/PI3K/Akt Pathway. Int J Mol Sci 2017;18:1510. https://doi.org/10.3390/ijms1801510
  19. Liu S, Zhang Y, Gao Y, et al. miR-378 plays an important role in the differentiation of bovine preadipocytes. Cell Physiol Biochem 2015;36:1552-62. https://doi.org/10.1159/000430318
  20. Jiang J, Li P, Ling H, Xu Z, Yi B, Zhu S. MiR-499/PRDM16 axis modulates the adipogenic differentiation of mouse skeletal muscle satellite cells. Hum Cell 2018;31:282-91. https://doi.rg/10.1007/s13577-018-0210-5
  21. Ji S, Li W, Bao L, et al. PU.1 promotes miR-191 to inhibit adipogenesis in 3T3-L1 preadipocytes. Biochem Biophys Res Commun 2014;451:329-33. https://doi.org/10.1016/j.bbrc.2014.07.130
  22. Liu X, Su K, Kuang S, Fu M, Zhang Z. miR-16-5p and miR145-5p trigger apoptosis in human gingival epithelial cells by down-regulating BACH2. Int J Clin Exp Pathol 2020;13:901-11.
  23. Li G, Li Y, Li X, Ning X, Li M, Yang G. MicroRNA identity and abundance in developing swine adipose tissue as determined by Solexa sequencing. J Cell Biochem 2011;112:1318-28. https://doi.org/10.1002/jcb.23045
  24. Li HY, Xi QY, Xiong YY, et al. Identification and comparison of microRNAs from skeletal muscle and adipose tissues from two porcine breeds. Anim Genet 2012;43:704-13. https://doi.org/10.1111/j.1365-2052.2012.02332.x
  25. Li Y. Comparing of backfat microRNAomes of Landrace and Neijiang pig by high-throughput sequencing. Genes Genomics 2021;43:543-51. https://doi.org/10.1007/s13258-021-01078-z
  26. Xing K, Zhao X, Liu Y, et al. Identification of differentially expressed microRNAs and their potential target genes in adipose tissue from pigs with highly divergent backfat thickness. Animals (Basel) 2020;10:624. https://doi.org/10.3390/ani10040624
  27. Zhou X, Beilter A, Xu Z, et al. Wnt/β-catenin-mediated p53 suppression is indispensable for osteogenesis of mesenchymal progenitor cells. Cell Death Dis 2021;12:521. https://doi.org/10.1038/s41419-021-03758-w
  28. Wang Y, Qu X, Yang Y, et al. AMPK promotes osteogenesis and inhibits adipogenesis through AMPK-Gfi1-OPN axis. Cell Signal 2016;28:1270-82. https://doi.org/10.1016/j.cellsig.2016.06.004
  29. Cai R, Tang G, Zhang Q, et al. A novel lnc-RNA, named lncORA, is identified by RNA-Seq analysis, and its knockdown inhibits adipogenesis by regulating the PI3K/AKT/mTOR signaling pathway. Cells 2019;8:477. https://doi.org/10.3390/cells8050477
  30. Wang J, Zhang Y, Tseng Y, Zhang J. miR-222 targets ACOX1, promotes triglyceride accumulation in hepatocytes. Hepatobiliary Pancreat Dis Int 2019;18:360-5. https://doi.org/10.016/j.hbpd.2019.05.002
  31. He A, Chen X, Tan M, et al. Acetyl-CoA derived from hepatic peroxisomal β-oxidation inhibits autophagy and promotes steatosis via mTORC1 activation. Mol Cell 2020;79:30-42. https://doi.org/10.1016/j.molcel.2020.05.007
  32. Pan Z, Wang J, Kang B, et al. Screening and identification of differentially expressed genes in goose hepatocytes exposed to free fatty acid. J Cell Biochem 2010;111:1482-92. https://doi.org/10.1002/jcb.22878
  33. Sperncer-Jones NJ, Ge D, Snieder H, et al. AMP-kinase alpha2 subunit gene PRKAA2 variants are associated with total cholesterol, low-density lipoprotein-cholesterol and high-density lipoprotein-cholesterol in normal women. J Med Genet 2006;43:936-42. https://doi.org/10.1136/jmg.2006.041988
  34. Xu Q, Qi W, Zhang Y, et al. DNA methylation of JAK3/STAT5/PPARγ regulated the changes of lipid levels induced by di (2-ethylhexyl) phthalate and high-fat diet in adolescent rats. Environ Sci Pollut Res 2020;27:30232-42. https://doi.org/10.1007/s11356-020-08976-x
  35. He Z, Zhu HH, Bauler TJ, et al. Nonreceptor tyrosine phosphatase Shp2 promotes adipogenesis through inhibition of p38 MAP kinase. Proc Natl Acad Sci USA 2013;110:E79-88. https://doi.org/10.1073/pnas.1213000110
  36. Viollet B, Foretz M, Guigas B, et al. Activation of AMP-activated protein kinase in the liver: a new strategy for the management of metabolic hepatic disorders. J Physiol 2006;574:41-53. https://doi.org/10.1113/jphysiol.2006.108506
  37. Wang Q, Liu S, Zhai A, Zhang B, Tian G. AMPK-mediated regulation of lipid metabolism by phosphorylation. Biol Pharm Bull 2018;41:985-93. https://doi.org/10.1248/bpb.b17-00724
  38. Boulard M, Storck S, Cong R, Pinto R, Delage H, Bouvet P. Histone variant macroH2A1 deletion in mice causes female-specific steatosis. Epigenetics Chromatin 2010;3:8. https://doi.org/10.1186/1756-8935-3-8
  39. Esau C, Davis S, Murray SF, et al. miR-122 regulation of lipid metabolism revealed by in vivo antisense targeting. Cell Metab 2006;3:87-98. https://doi.org/10.1016/j.cmet.2006.01.005
  40. Long J, Dai W, Zheng Y, Zhao S. miR-122 promotes hepatic lipogenesis via inhibiting the LKB1/AMPK pathway by targeting Sirt1 in non-alcoholic fatty liver disease. Mol Med 2019;25:26. https://doi.org/10.1186/s10020-019-0085-2
  41. Hibuse T, Maeda N, Funahashi T, et al. Aquaporin 7 deficiency is associated with development of obesity through activation of adipose glycerol kinase. Proc Natl Acad Sci USA 2005;102:10993-8. https://doi.org/10.1073/pnas.0503291102