Skip to main content
SpringerLink
Log in

Biological role of MicroRNA-103 based on expression profile and target genes analysis in pigs

  • Published:
Molecular Biology Reports Aims and scope Submit manuscript

Abstract

MicroRNAs (miRNAs) are endogenously expressed RNAs consisting of 20–24 nucleotides. These molecules are thought to repress protein translation by binding to target mRNAs. However, biological functions have not been assigned to most of the 175 porcine miRNAs registered in miRBase (release 15.0). In an effort to uncover miR-103 important in pigs, we examined the integrative tissue expression profile and gene ontology (GO) term enrichment of predicted target genes to determine the global biological functions of miR-103. Our results demonstrated that miR-103 is involved in various biological processes including brain development, lipid metabolism, adipocyte differentiation, hematopoiesis, and immunity. Moreover, we also experimentally verified effects of miR-103 in porcine preadipocytes. miR-103 levels increased in differentiating adipocytes, and inhibition of miR-103 effectively inhibited preadipocyte differentiation. In addition, mRNA levels of the putative miR-103 target RAI14 were higher in miR-103 inhibitor-treated adipocytes. These results demonstrate that miR-103 is involved in porcine preadipocyte differentiation and may act through the putative target gene RAI14. In a word, our data provide new insights into the global biological role of miR-103.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  1. Aravin AA, Lagos-Quintana M, Yalcin A et al (2003) The small RNA profile during Drosophila melanogaster development. Dev Cell 5(2):337–350

    Article  PubMed  CAS  Google Scholar 

  2. Esau C, Davis S, Murray SF et al (2006) miR-122 regulation of lipid metabolism revealed by in vivo antisense targeting. Cell Metab 3(2):87–98

    Article  PubMed  CAS  Google Scholar 

  3. He L, He X, Lowe SW et al (2007) MicroRNAs join the p53 network—another piece in the tumour-suppression puzzle. Nat Rev Cancer 7(11):819–822

    Article  PubMed  CAS  Google Scholar 

  4. Chen CZ, Li L, Lodish HF et al (2004) MicroRNAs modulate hematopoietic lineage differentiation. Science 303(5654):83–86

    Article  PubMed  CAS  Google Scholar 

  5. Callis TE, Chen JF, Wang DZ (2007) MicroRNAs in skeletal and cardiac muscle development. DNA Cell Biol 26(4):219–225

    Article  PubMed  CAS  Google Scholar 

  6. Rodriguez A, Griffiths-Jones S, Ashurst JL et al (2004) Identification of mammalian microRNA host genes and transcription units. Genome Res 14(10A):1902–1910

    Article  PubMed  CAS  Google Scholar 

  7. Kim J, Krichevsky A, Grad Y et al (2004) Identification of many microRNAs that copurify with polyribosomes in mammalian neurons. Proc Natl Acad Sci USA 101(1):360–365

    Article  PubMed  CAS  Google Scholar 

  8. Coutinho LL, Matukumalli LK, Sonstegard TS et al (2007) Discovery and profiling of bovine microRNAs from immune-related and embryonic tissues. Physiol Genomics 29(1):35–43

    PubMed  CAS  Google Scholar 

  9. Landgraf P, Rusu M, Sheridan R et al (2007) A mammalian microRNA expression atlas based on small RNA library sequencing. Cell 129(7):1401–1414

    Article  PubMed  CAS  Google Scholar 

  10. Miska EA, Alvarez-Saavedra E, Townsend M et al (2004) Microarray analysis of microRNA expression in the developing mammalian brain. Genome Biol 5(9):R68

    Article  PubMed  Google Scholar 

  11. Choong ML, Yang HH, McNiece I (2007) MicroRNA expression profiling during human cord blood-derived CD34 cell erythropoiesis. Exp Hematol 35(4):551–564

    Article  PubMed  CAS  Google Scholar 

  12. Liu SP, Fu RH, Yu HH et al (2009) MicroRNAs regulation modulated self-renewal and lineage differentiation of stem cells. Cell Transplant 18(9):1039–1045

    Article  PubMed  Google Scholar 

  13. Roldo C, Missiaglia E, Hagan JP et al (2006) MicroRNA expression abnormalities in pancreatic endocrine and acinar tumors are associated with distinctive pathologic features and clinical behavior. J Clin Oncol 24(29):4677–4684

    Article  PubMed  CAS  Google Scholar 

  14. Kulshreshtha R, Ferracin M, Wojcik SE et al (2007) A microRNA signature of hypoxia. Mol Cell Biol 27(5):1859–1867

    Article  PubMed  CAS  Google Scholar 

  15. Marsit CJ, Eddy K, Kelsey KT (2006) MicroRNA responses to cellular stress. Cancer Res 66(22):10843–10848

    Article  PubMed  CAS  Google Scholar 

  16. Iliopoulos D, Malizos KN, Oikonomou P et al (2008) Integrative microRNA and proteomic approaches identify novel osteoarthritis genes and their collaborative metabolic and inflammatory networks. PLoS One 3(11):e3740

    Article  PubMed  Google Scholar 

  17. Yang GH, Wang F, Yu J et al (2009) MicroRNAs are involved in erythroid differentiation control. J Cell Biochem 107(3):548–556

    Article  PubMed  CAS  Google Scholar 

  18. Xie H, Lim B, Lodish HF (2009) MicroRNAs induced during adipogenesis that accelerate fat cell development are downregulated in obesity. Diabetes 58(5):1050–1057

    Article  PubMed  CAS  Google Scholar 

  19. Guo Y, Chen Z, Zhang L et al (2008) Distinctive microRNA profiles relating to patient survival in esophageal squamous cell carcinoma. Cancer Res 68(1):26–33

    Article  PubMed  CAS  Google Scholar 

  20. Wernersson R, Schierup MH, Jørgensen FG et al (2005) Pigs in sequence space: a 0.66X coverage pig genome survey based on shotgun sequencing. BMC Genomics 6(1):70

    Article  PubMed  Google Scholar 

  21. Krek A, Grun D, Poy MN et al (2005) Combinatorial microRNA target predictions. Nat Genet 37:495–500

    Article  PubMed  CAS  Google Scholar 

  22. Lewis BP, Shih IH, Jones-Rhoades MW et al (2003) Prediction of mammalian microRNA targets. Cell 115:787–798

    Article  PubMed  CAS  Google Scholar 

  23. Boyle EI, Weng S, Gollub J et al (2004) GO:TermFinder–open source software for accessing gene ontology information and finding significantly enriched gene ontology terms associated with a list of genes. Bioinformatics 20(18):3710–3715

    Article  PubMed  CAS  Google Scholar 

  24. Huixia Li, Luo Xiao, Liu Rongxin et al (2008) Roles of Wnt/_-catenin signaling in adipogenic differentiation potential of adipose-derived mesenchymal stem cells. Mol Cell Endocrinol 291:116–124

    Article  Google Scholar 

  25. Leibrock J, Lottspeich F, Hohn A et al (1989) Molecular cloning and expression of brain-derived neurotrophic factor. Nature 341(6238):149–152

    Article  PubMed  CAS  Google Scholar 

  26. Yokoyama M, Nishi Y, Miyamoto Y et al (1996) Molecular cloning of a human neuroD from a neuroblastoma cell line specifically expressed in the fetal brain and adult cerebellum. Brain Res Mol Brain Res 42(1):135–139

    Article  PubMed  CAS  Google Scholar 

  27. Brunham LR, Singaraja RR, Duong M et al (2009) Tissue-specific roles of ABCA1 influence susceptibility to atherosclerosis. Arterioscler Thromb Vasc Biol 29(4):548–554

    Article  PubMed  CAS  Google Scholar 

  28. Cao Y, Traer E, Zimmerman GA et al (1998) Cloning, expression, and chromosomal localization of human long-chain fatty acid-CoA ligase 4 (FACL4). Genomics 49(2):327–330

    Article  PubMed  CAS  Google Scholar 

  29. Nöhammer C, El-Shabrawi Y, Schauer S et al (2000) cDNA cloning and analysis of tissue-specific expression of mouse peroxisomal straight-chain acyl-CoA oxidase. Eur J Biochem 267(4):1254–1260

    Article  PubMed  Google Scholar 

  30. Inglis-Broadgate SL, Ocaka L, Banerjee R et al (2005) Isolation and characterization of murine Cds (CDP-diacylglycerol synthase) 1 and 2. Gene 356:19–31

    Article  PubMed  CAS  Google Scholar 

  31. Cesta MF (2006) Normal structure, function, and histology of the spleen. Toxicol Pathol 34(5):455–465

    Article  PubMed  Google Scholar 

  32. Crosby WH (1959) Normal functions of the spleen relative to red blood cells: a review. Blood 14(4):399–408

    PubMed  CAS  Google Scholar 

  33. Balakirev MY, Tcherniuk SO, Jaquinod M et al (2003) Otubains: a new family of cysteine proteases in the ubiquitin pathway. EMBO Rep 4(5):517–522

    Article  PubMed  CAS  Google Scholar 

  34. Neilson JR, Zheng GX, Burge CB et al (2007) Dynamic regulation of miRNA expression in ordered stages of cellular development. Genes Dev 21(5):578–589

    Article  PubMed  CAS  Google Scholar 

  35. Sonkoly E, Stahle M, Pivarcsi A (2008) MicroRNAs and immunity: novel players in the regulation of normal immune function and inflammation. Semin Cancer Bio 18(2):131–140

    Article  CAS  Google Scholar 

  36. Cho IS, Kim J, Seo HY et al (2010) Cloning and characterization of microRNAs from porcine skeletal muscle and adipose tissue. Mol Biol Rep 37(7):3567–3574

    Article  PubMed  CAS  Google Scholar 

  37. Liu G, Fang Y, Zhang H et al (2010) Computational identification and microarray-based validation of microRNAs in Oryctolagus cuniculus. Mol Biol Rep 37(7):3575–3581

    Article  PubMed  CAS  Google Scholar 

  38. Sheng X, Song X, Yu Y et al. (2010) Characterization of microRNAs from sheep (Ovis aries) using computational and experimental analyses. Mol Biol Rep, PubMed PMID: 20140706

  39. Huang Y, Zou Q, Tang SM et al (2010) Computational identification and characteristics of novel microRNAs from the silkworm (Bombyx mori L.). Mol Biol Rep 37(7):3171–3176

    Article  PubMed  CAS  Google Scholar 

  40. Chen K, Rajewsky N (2006) Deep conservation of microRNA target relationships and 3′UTR motifs in vertebrates, flies, and nematodes. Cold Spring Harb Symp Quant Biol 71:149–156

    Article  PubMed  CAS  Google Scholar 

  41. Wilfred BR, Wang WX, Nelson PT (2007) Energizing miRNA research: a review of the role of miRNAs in lipid metabolism, with a prediction that miR-103/107 regulates human metabolic pathways. Mol Genet Metab 91(3):209–217

    Article  PubMed  CAS  Google Scholar 

  42. Brandebourg TD, Hu CY (2005) Regulation of differentiating pig preadipocytes by retinoic acid. J Anim Sci 83(1):98–107

    PubMed  CAS  Google Scholar 

  43. Suryawan A, Hu CY (1997) Effect of retinoic acid on differentiation of cultured pig preadipocytes. J Anim Sci 75(1):112–117

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We are grateful to members of our laboratories for critical reading of the manuscript and helpful discussion. This work was supported by National Natural Science Foundation of China (NO.31072014) and the National High Technology Research and Development Program of China (863 Program) (No. 2006AA10Z138).

Author information

Author notes

  1. Gongshe Yang

    Present address: Laboratory of Animal Fat Deposition and Muscle Development, College of Animal Science and Technology, Northwest A&F University, 22 Xinong Road, Yangling, 712100, Shaanxi, People’s Republic of China

Authors and Affiliations

  1. Laboratory of Animal Fat Deposition and Muscle Development, College of Animal Science and Technology, Northwest A&F University, 22 Xinong Road, Yangling, 712100, Shaanxi, People’s Republic of China

    Guoxi Li, Zongsong Wu, Xinjian Li, Xiaomin Ning & Yanjie Li

  2. College of Animal Husbandry and Veterinary Science, Henan Agricultural University, Zhengzhou, 450002, Henan, People’s Republic of China

    Guoxi Li & Xinjian Li

Authors
  1. Guoxi Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zongsong Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xinjian Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xiaomin Ning
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yanjie Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Gongshe Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Gongshe Yang.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 152 kb)

Supplementary material 2 (DOC 111 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Li, G., Wu, Z., Li, X. et al. Biological role of MicroRNA-103 based on expression profile and target genes analysis in pigs. Mol Biol Rep 38, 4777–4786 (2011). https://doi.org/10.1007/s11033-010-0615-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11033-010-0615-z

Keywords

Search

Navigation