Asian-Australasian Journal of Animal Sciences

Asian Australasian Association of Animal Production Societies (아세아태평양축산학회)
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Hepatic microRNAome reveals potential microRNA-mRNA pairs association with lipid metabolism in pigs

  • Liu, Jingge (Department of Animal Genetics, Breeding and Reproduction, College of Animal Science and Technology, Nanjing Agricultural University) ;
  • Ning, Caibo (Department of Animal Genetics, Breeding and Reproduction, College of Animal Science and Technology, Nanjing Agricultural University) ;
  • Li, Bojiang (Department of Animal Genetics, Breeding and Reproduction, College of Animal Science and Technology, Nanjing Agricultural University) ;
  • Li, Rongyang (Department of Animal Genetics, Breeding and Reproduction, College of Animal Science and Technology, Nanjing Agricultural University) ;
  • Wu, Wangjun (Department of Animal Genetics, Breeding and Reproduction, College of Animal Science and Technology, Nanjing Agricultural University) ;
  • Liu, Honglin (Department of Animal Genetics, Breeding and Reproduction, College of Animal Science and Technology, Nanjing Agricultural University)
  • Received : 2018.06.10
  • Accepted : 2018.09.03
  • Published : 2019.09.01
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Abstract

Objective: As one of the most important metabolic organs, the liver plays vital roles in modulating the lipid metabolism. This study was to compare miRNA expression profiles of the Large White liver between two different developmental periods and to identify candidate miRNAs for lipid metabolism. Methods: Eight liver samples were collected from White Large of 70-day fetus (P70) and of 70-day piglets (D70) (with 4 biological repeats at each development period) to construct sRNA libraries. Then the eight prepared sRNA libraries were sequenced using Illumina next-generation sequencing technology on HiSeq 2500 platform. Results: As a result, we obtained 346 known and 187 novel miRNAs. Compared with the D70, 55 down- and 61 up-regulated miRNAs were shown to be significantly differentially expressed (DE). Gene ontology and Kyoto encyclopedia of genes and genomes enrichment analysis indicated that these DE miRNAs were mainly involved in growth, development and diverse metabolic processes. They were predicted to regulate lipid metabolism through adipocytokine signaling pathway, mitogen-activated protein kinase, AMP-activated protein kinase, cyclic adenosine monophosphate, phosphatidylinositol 3 kinase/protein kinase B, and Notch signaling pathway. The four most abundantly expressed miRNAs were miR-122, miR-26a and miR-30a-5p (miR-122 only in P70), which play important roles in lipid metabolism. Integration analysis (details of mRNAs sequencing data were shown in another unpublished paper) revealed that many target genes of the DE miRNAs (miR-181b, miR-145-5p, miR-199a-5p, and miR-98) might be critical regulators in lipid metabolic process, including acyl-CoA synthetase long chain family member 4, ATP-binding casette A4, and stearyl-CoA desaturase. Thus, these miRNAs were the promising candidates for lipid metabolism. Conclusion: Our study provides the main differences in the Large White at miRNA level between two different developmental stages. It supplies a valuable database for the further function and mechanism elucidation of miRNAs in porcine liver development and lipid metabolism.

Keywords

References

  1. Nguyen P, Leray V, Diez M, et al. Liver lipid metabolism. J Anim Physiol Anim Nutr (Berl) 2008;92:272-83. https://doi.org/10.1111/j.1439-0396.2007.00752.x
  2. Takeuchi-Yorimoto A, Yamaura Y, Kanki M, et al. MicroRNA-21 is associated with fibrosis in a rat model of nonalcoholic steatohepatitis and serves as a plasma biomarker for fibrotic liver disease. Toxicol Lett 2016;258:159-67. https://doi.org/10.1016/j.toxlet.2016.06.012
  3. Krutzfeldt J, Rajewsky N, Braich R, et al. Silencing of microRNAs in vivo with 'antagomirs'. Nature 2005;438:685-9. https://doi.org/10.1038/nature04303
  4. Tsai WC, Hsu SD, Hsu CS, et al. MicroRNA-122 plays a critical role in liver homeostasis and hepatocarcinogenesis. J Clin Invest 2012;122:2884-97. https://doi.org/10.1172/JCI63455
  5. Gerin I, Clerbaux LA, Haumont O, et al. Expression of miR-33 from an SREBP2 intron inhibits cholesterol export and fatty acid oxidation. J Biol Chem 2010;285:33652-61. https://doi.org/10.1074/jbc.M110.152090
  6. Kong Y, Han JH. MicroRNA: biological and computational perspective. Genomics Proteomics Bioinformatics 2005;3:62-72. https://doi.org/10.1016/S1672-0229(05)03011-1
  7. Iliopoulos D, Drosatos K, Hiyama Y, Goldberg IJ, Zannis VI. MicroRNA-370 controls the expression of microRNA-122 and Cpt1alpha and affects lipid metabolism. J Lipid Res 2010;51:1513-23. https://doi.org/10.1194/jlr.M004812
  8. Kovalchuk A, Ilnytskyy Y, Rodriguez-Juarez R, et al. Growth of malignant extracranial tumors alters microRNAome in the prefrontal cortex of TumorGraft mice. Oncotarget 2017;8:88276-93. https://doi.org/10.18632/oncotarget.19835
  9. Wang D, Liang G, Wang B, et al. Systematic microRNAome profiling reveals the roles of microRNAs in milk protein metabolism and quality: insights on low-quality forage utilization. Sci Rep 2016;6:21194. https://doi.org/10.1038/srep21194
  10. Gaffo E, Zambonelli P, Bisognin A, Bortoluzzi S, Davoli R. miRNome of Italian Large White pig subcutaneous fat tissue: new miRNAs, isomiRs and moRNAs. Anim Genet 2014;45:685-98. https://doi.org/10.1111/age.12192
  11. Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 2009;10:R25. https://doi.org/10.1186/gb-2009-10-3-r25
  12. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001;25:402-8. https://doi.org/10.1006/meth.2001.1262
  13. Bohme HJ, Sparmann G, Hofmann E. Biochemistry of liver development in the perinatal period. Experientia 1983;39:473-83. https://doi.org/10.1007/BF01965164
  14. Ponsuksili S, Murani E, Walz C, Schwerin M, Wimmers K. Preand postnatal hepatic gene expression profiles of two pig breeds differing in body composition: insight into pathways of metabolic regulation. Physiol Genomics 2007;29:267-79. https://doi.org/10.1152/physiolgenomics.00178.2006
  15. Yuhong J, Leilei T, Fuyun Z, et al. Identification and characterization of immune-related microRNAs in blunt snout bream, Megalobrama amblycephala. Fish Shellfish Immunol 2016;49:470-92. https://doi.org/10.1016/j.fsi.2015.12.013
  16. 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
  17. Lanford RE, Hildebrandt-Eriksen ES, Petri A, et al. Therapeutic silencing of microRNA-122 in primates with chronic hepatitis C virus infection. Science 2010;327:198-201. https://doi.org/10.1126/science.1178178
  18. Lattka E, Illig T, Koletzko B, Heinrich J. Genetic variants of the FADS1 FADS2 gene cluster as related to essential fatty acid metabolism. Curr Opin Lipidol 2010;21:64-9. https://doi.org/10.1097/MOL.0b013e3283327ca8
  19. Ntambi JM. Regulation of stearoyl-CoA desaturase by polyunsaturated fatty acids and cholesterol. J Lipid Res 1999;40:1549-58. https://doi.org/10.1016/S0022-2275(20)33401-5
  20. Sun D, Zhang J, Xie J, et al. MiR-26 controls LXR-dependent cholesterol efflux by targeting ABCA1 and ARL7. FEBS Lett 2012;586:1472-9. https://doi.org/10.1016/j.febslet.2012.03.068
  21. Soh J, Iqbal J, Queiroz J, Fernandez-Hernando C, Hussain MM. MicroRNA-30c reduces hyperlipidemia and atherosclerosis in mice by decreasing lipid synthesis and lipoprotein secretion. Nat Med 2013;19:892-900. https://doi.org/10.1038/nm.3200
  22. Ma Z, Li H, Zheng H, et al. MicroRNA-101-2-5p targets the ApoB gene in the liver of chicken (Gallus Gallus). Genome 2017;60:673-8. https://doi.org/10.1139/gen-2017-0020
  23. Wan M, Leavens KF, Saleh D, et al. Postprandial hepatic lipid metabolism requires signaling through Akt2 independent of the transcription factors FoxA2, FoxO1, and SREBP1c. Cell Metab 2011;14:516-27. https://doi.org/10.1016/j.cmet.2011.09.001
  24. Yang J, Craddock L, Hong S, Liu ZM. AMP-activated protein kinase suppresses LXR-dependent sterol regulatory elementbinding protein-1c transcription in rat hepatoma McA-RH7777 cells. J Cell Biochem 2009;106:414-26. https://doi.org/10.1002/jcb.22024
  25. Wang Y, Zhu K, Yu W, et al. MiR-181b regulates steatosis in nonalcoholic fatty liver disease via targeting SIRT1. Biochem Biophys Res Commun 2017;493:227-32. https://doi.org/10.1016/j.bbrc.2017.09.042
  26. Kang MH, Zhang LH, Wijesekara N, et al. Regulation of ABCA1 protein expression and function in hepatic and pancreatic islet cells by miR-145. Arterioscler Thromb Vasc Biol 2013;33:2724-32. https://doi.org/10.1161/ATVBAHA.113.302004
  27. el Azzouzi H, Leptidis S, Dirkx E, et al. The hypoxia-inducible microRNA cluster miR-199a approximately 214 targets myocardial PPARdelta and impairs mitochondrial fatty acid oxidation. Cell Metab 2013;18:341-54. https://doi.org/10.1016/j.cmet.2013.08.009
  28. Chen S, Wen X, Zhang W, et al. Hypolipidemic effect of oleanolic acid is mediated by the miR-98-5p/PGC-1beta axis in high-fat diet-induced hyperlipidemic mice. FASEB J 2017;31:1085-96. https://doi.org/10.1096/fj.201601022R
  29. Duarte A, Poderoso C, Cooke M, et al. Mitochondrial fusion is essential for steroid biosynthesis. PLoS One 2012;7:e45829. https://doi.org/10.1371/journal.pone.0045829
  30. Ye D, Hoekstra M, Out R, et al. Hepatic cell-specific ATP-binding cassette (ABC) transporter profiling identifies putative novel candidates for lipid homeostasis in mice. Atherosclerosis 2008;196:650-8. https://doi.org/10.1016/j.atherosclerosis.2007.07.021

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