Animal Bioscience

  • 제35권1호
  • /
  • Pages.115-125
  • /
  • 2022
  • /
  • 2765-0189(pISSN)
  • /
  • 2765-0235(eISSN)
아세아태평양축산학회 (Asian Australasian Association of Animal Production Societies)
권호 표지
DOI QR코드

DOI QR Code

Identification and functional prediction of long noncoding RNAs related to intramuscular fat content in Laiwu pigs

  • Wang, Lixue (Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, College of Animal Science and Technology, Shandong Agricultural University) ;
  • Xie, Yuhuai (Department of Immunology, School of Basic Medical Sciences, Fudan University) ;
  • Chen, Wei (Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, College of Animal Science and Technology, Shandong Agricultural University) ;
  • Zhang, Yu (Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, College of Animal Science and Technology, Shandong Agricultural University) ;
  • Zeng, Yongqing (Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, College of Animal Science and Technology, Shandong Agricultural University)
  • 투고 : 2021.02.27
  • 심사 : 2021.06.03
  • 발행 : 2022.01.01
PDF 다운로드
⟨ 이전 논문 다음 논문 ⟩

초록

Objective: Intramuscular fat (IMF) is a critical economic indicator of pork quality. Studies on IMF among different pig breeds have been performed via high-throughput sequencing, but comparisons within the same pig breed remain unreported. Methods: This study was performed to explore the gene profile and identify candidate long noncoding RNA (lncRNAs) and mRNAs associated with IMF deposition among Laiwu pigs with different IMF contents. Based on the longissimus dorsi muscle IMF content, eight pigs from the same breed and management were selected and divided into two groups: a high IMF (>12%, H) and low IMF group (<5%, L). Whole-transcriptome sequencing was performed to explore the differentially expressed (DE) genes between these two groups. Results: The IMF content varied greatly among Laiwu pig individuals (2.17% to 13.93%). Seventeen DE lncRNAs (11 upregulated and 6 downregulated) and 180 mRNAs (112 upregulated and 68 downregulated) were found. Gene Ontology analysis indicated that the following biological processes played an important role in IMF deposition: fatty acid and lipid biosynthetic processes; the extracellular signal-regulated kinase cascade; and white fat cell differentiation. In addition, the peroxisome proliferator-activated receptor, phosphatidylinositol-3-kinase-protein kinase B, and mammalian target of rapamycin pathways were enriched in the pathway analysis. Intersection analysis of the target genes of DE lncRNAs and mRNAs revealed seven candidate genes associated with IMF accumulation. Five DE lncRNAs and 20 DE mRNAs based on the pig quantitative trait locus database were identified and shown to be related to fat deposition. The expression of five DE lncRNAs and mRNAs was verified by quantitative real time polymerase chain reaction (qRT-PCR). The results of qRT-PCR and RNA-sequencing were consistent. Conclusion: These results demonstrated that the different IMF contents among pig individuals may be due to the DE lncRNAs and mRNAs associated with lipid droplets and fat deposition.

키워드

과제정보

This study was supported financially by the Agricultural Animal Breeding Project of Shandong Province (No. 2020LZGC012), Funds of Shandong "Double Tops" Program (No. SYL2017YSTD12), Shandong Modern Pig Technology & Industry System Project (No. SDAIT-08-02), Shandong Provincial Natural Science Foundation (No. ZR2018BC046, ZR2019MC053).

참고문헌

  1. Fernandez X, Monin G, Talmant A, Mourot J, Lebret B. Influence of intramuscular fat content on the quality of pig Meat-1. Composition of the lipid fraction and sensory characteristics of m. Longissimus lumborum. Meat Sci 1999; 53:59-65. https://doi.org/10.1016/s0309-1740(99)00037-6
  2. Harper GS, Pethick D, Oddy V, Tume R, Barendse W, Hygate L. Biological determinants of intramuscular fat deposition in beef cattle: current mechanistic knowledge and sources of variation. Sydney, Australia: Meat & Livestock Australia; 2001.
  3. Guo Y, Huang Y, Hou L, et al. Genome-wide detection of genetic markers associated with growth and fatness in four pig populations using four approaches. Genet Sel Evol 2017; 21:49. https://doi.org/10.1186/s12711-017-0295-4
  4. Qiao R, Gao J, Zhang Z, et al. Genome-wide association analyses reveal significant loci and strong candidate genes for growth and fatness traits in two pig populations. Genet Sel Evol 2015;47:17. https://doi.org/10.1186/s12711-015-0089-5
  5. Ropka Molik K, Zukowski K, Eckert R, Gurgul A, Piorkowska K, Oczkowicz M. Comprehensive analysis of the whole transcriptomes from two different pig breeds using RNA-Seq method. Anim Genet 2014;45:674-84. https://doi.org/10.1111/age.12184
  6. Zhang M, Li F, Sun JW, et al. LncRNA IMFNCR promotes intramuscular adipocyte differentiation by sponging miR128-3p and miR-27b-3p. Front Genet 2019;10:42. https://doi.org/10.3389/fgene.2019.00042
  7. Duan L, Min C, Niu Y, et al. Identification of a novel human long non-coding RNA that regulates hepatic lipid metabolism by inhibiting SREBP-1c. Int J Biol Sci 2017;13:349-57. https://doi.org/10.7150/ijbs.16635
  8. Sun Y, Cai R, Wang Y, Zhao R, Qin J, Pang W. A newly identified lncRNA lncIMF4 controls adipogenesis of porcine intramuscular preadipocyte through attenuating autophagy to inhibit lipolysis. Animals 2020;10:926. https://doi.org/10.3390/ani10060926
  9. Wang J, Chen M, Chen J, et al. LncRNA IMFlnc1 promotes porcine intramuscular adipocyte adipogenesis by sponging miR-199a-5p to up-regulate CAV-1. BMC Mol Cell Biol 2020;21:77. https://doi.org/10.1186/s12860-020-00324-8
  10. Kazak L, Rahbani JF, Samborska B, et al. Ablation of adipocyte creatine transport impairs thermogenesis and causes diet-induced obesity. Nat Metab 2019;3:360-70. https://doi.org/10.1038/s42255-019-0035-x
  11. Chen X, Ayala I, Shannon C, et al. The diabetes gene and Wnt pathway effector TCF7L2 regulates adipocyte development and function. Diabetes 2018;67:554-68. https://doi.org/10.2337/db17-0318
  12. Zhang X, Zhang Y, Wang P, et al. Adipocyte hypoxia-inducible factor 2α suppresses atherosclerosis by promoting adipose ceramide catabolism. Cell Metab 2019;30:937-51. https://doi.org/10.1016/j.cmet.2019.09.016
  13. Chen Q, Zeng Y, Wang H, et al. Molecular characterization and expression analysis of NDUFS4 gene in m. Longissimus dorsi of laiwu pig (sus scrofa). Mol Biol Rep 2013;2:1599-608. https://doi.org/10.1007/s11033-012-2208-5
  14. Chen W, Fang G, Wang S, Wang H, Zeng Y. Longissimus lumborum muscle transcriptome analysis of laiwu and yorkshire pigs differing in intramuscular fat content. Genes Genomics 2017;39:759-66. https://doi.org/10.1007/s13258-017-0540-9
  15. Huang Y, Zhou L, Zhang J, Liu X, Huang L. A large-scale comparison of meat quality and intramuscular fatty acid composition among three Chinese indigenous pig breeds. Meat Sci 2020;168:108182. https://doi.org/10.1016/j.meatsci.2020.108182
  16. Vieth B, Parekh S, Ziegenhain C, Enard W, Hellmann I. A systematic evaluation of single cell RNA-seq analysis pipelines. Nat Commun 2019;10:4667. https://doi.org/10.1038/s41467-019-12266-7
  17. Kanehisa M, Furumichi M, Tanabe M, Sato Y, Morishima K. KEGG: new perspectives on genomes, pathways, diseases and drugs. Nucleic Acids Res 2017;45:D353-61. https://doi.org/10.1093/nar/gkw1092
  18. Young MD, Wakefield MJ, Smyth GK, Oshlack A. Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol 2010;11:R14. https://doi.org/10.1186/gb-2010-11-2-r14
  19. Kanehisa M, Araki M, Goto S, et al. KEGG for linking genomes to life and the environment. Nucleic Acids Res 2007;36 (suppl_1):D480-4. https://doi.org/10.1093/nar/gkm882
  20. Cui JX, Zeng QF, Chen W, Zhang H, Zeng YQ. Analysis and preliminary validation of the molecular mechanism of fat deposition in fatty and lean pigs by high-throughput sequencing. Mamm Genome 2019;30:71-80. https://doi.org/10.1007/s00335-019-09795-3
  21. Huang W, Zhang X, Li A, Xie L, Miao X. Genome-wide analysis of mRNAs and lncRNAs of intramuscular fat related to lipid metabolism in two pig breeds. Cell Physiol Biochem 2018;50:2406-22. https://doi.org/10.1159/000495101
  22. Ansel J, Bottin H, Rodriguez-Beltran C, et al. Cell-to-cell stochastic variation in gene expression is a complex genetic trait. Plos Genet 2008;4:e1000049. https://doi.org/10.1371/journal.pgen.1000049
  23. Loo L, Lin H, Singh DK, Lyons KM, Altschuler SJ, Wu LF. Heterogeneity in the physiological states and pharmacological responses of differentiating 3T3-L1 preadipocytes. J Cell Biol 2009;187:375-84. https://doi.org/10.1083/jcb.200904140
  24. Herms A, Bosch M, Ariotti N, et al. Cell-to-cell heterogeneity in lipid droplets suggests a mechanism to reduce lipotoxicity. Curr Biol 2013;23:1489-96. https://doi.org/10.1016/j.cub.2013.06.032
  25. Cai H, Li M, Jian W, et al. A novel lncRNA BADLNCR1 inhibits bovine adipogenesis by repressing GLRX5 expression. J Cell Mol Med 2020;24:7175-86. https://doi.org/10.1111/jcmm.15181
  26. Zhang S, Kang Z, Cai H, et al. Identification of novel alternative splicing of bovine lncRNA lncFAM200B and its effects on preadipocyte proliferation. J Cell Physiol 2021;236:601-11. https://doi.org/10.1002/jcp.29887
  27. Liu W, Ma C, Yang B, Yin C, Zhang B, Xiao Y. LncRNA Gm15290 sponges miR-27b to promote PPARγ-induced fat deposition and contribute to body weight gain in mice. Biochem Biophys Res Commun 2017;493:1168-75. https://doi.org/10.1016/j.bbrc.2017.09.114
  28. Wang S, Zhang Q, Zhang Y, et al. Agrimol B suppresses adipogenesis through modulation of SIRT1-PPAR gamma signal pathway. Biochem Biophys Res Commun 2016;477:454-60. https://doi.org/10.1016/j.bbrc.2016.06.078
  29. Rachid TL, Silva-Veiga FM, Graus-Nunes F, Bringhenti I, Mandarim-De-Lacerda CA, Souza-Mello V. Differential actions of PPAR-α and PPAR-β/δ on beige adipocyte formation: a study in the subcutaneous white adipose tissue of obese male mice. Plos One 2018;13:e0191365. https://doi.org/10.1371/journal.pone.0191365
  30. Song B, Chi Y, Li X, et al. Inhibition of Notch signaling promotes the adipogenic differentiation of mesenchymal stem cells through autophagy activation and PTEN-PI3K/Akt/mTOR pathway. Cell Physiol Biochem 2015;36:1991-2002. https://doi.org/10.1159/000430167
  31. Yu X, Shen N, Zhang ML, et al. Egr-1 decreases adipocyte insulin sensitivity by tilting PI3K/Akt and MAPK signal balance in mice. EMBO J 2011;30:3754-65. https://doi.org/10.1038/emboj.2011.277
  32. Perez-Mancera PA, Bermejo-Rodriguez C, Gonzalez-Herrero I, et al. Adipose tissue mass is modulated by SLUG (SNAI2). Hum Mol Genet 2007;16:2972-86. https://doi.org/10.1093/hmg/ddm278
  33. Tong Q, Dalgin G, Xu H, Ting C, Leiden JM, Hotamisligil GS. Function of GATA transcription factors in preadipocyte-adipocyte transition. Science 2000;290:134-8. https://doi.org/10.1126/science.290.5489.134
  34. Tong Q, Tsai J, Tan G, Dalgin G, Hotamisligil GS. Interaction between GATA and the C/EBP family of transcription factors is critical in GATA-mediated suppression of adipocyte differentiation. Mol Cell Biol 2005;25:706-15. https://doi.org/10.1128/MCB.25.2.706-715.2005
  35. Pan W, Ciociola E, Saraf M, et al. Metabolic consequences of ENPP1 overexpression in adipose tissue. Am J Physiol Endocrinol Metab 2011;301:E901-11. https://doi.org/10.1152/ajpendo.00087.2011
  36. Hilgendorf KI, Johnson CT, Mezger A, et al. Omega-3 fatty acids activate ciliary FFAR4 to control adipogenesis. Cell 2019;179:1289-305. https://doi.org/10.1016/j.cell.2019.11.005
  37. Masaki S, Kii I, Sumida Y, et al. Design and synthesis of a potent inhibitor of class 1 DYRK kinases as a suppressor of adipogenesis. Bioorgan Med Chem 2015;23:4434-41. https://doi.org/10.1016/j.bmc.2015.06.018
  38. Wang P, Xu J, Wang Y, Cao X. An interferon-independent lncRNA promotes viral replication by modulating cellular metabolism. Science 2017;358:1051-5. https://doi.org/10.1126/science.aao0409
  39. Bortesi L, Zhu C, Zischewski J, et al. Patterns of CRISPR/Cas9 activity in plants, animals and microbes. Plant Biotechnol J 2016;14:2203-16. https://doi.org/10.1111/pbi.12634
  40. China National Commission of Animal Genetic Resources. Animal genetic resources in China: pigs. Beijing, China: Agriculture Press; 2011.