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Systematic transcriptome-wide analysis of mRNA–miRNA interactions reveals the involvement of miR-142-5p and its target (FOXO3) in skeletal muscle growth in chickens

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Abstract

The goal of this study was to perform a systematic transcriptome-wide analysis of mRNA–miRNA interactions and to identify candidates involved in the interplay between miRNAs and mRNAs that regulate chicken muscle growth. We used our previously published mRNA (GSE72424) and miRNA (GSE62971) deep sequencing data from two-tailed samples [i.e., the highest (h) and lowest (l) body weights] of Recessive White Rock (WRR) and Xinghua (XH) chickens to conduct integrative analyses of the miRNA–mRNA interactions involved in chicken skeletal muscle growth. A total of 162, 15, 173, and 27 miRNA–mRNA pairs with negatively correlated expression patterns were identified in miRNA–mRNA networks constructed on the basis of the WRRh vs. XHh, WRRh vs. WRRl, WRRl vs. XHl, and XHh vs. XHl comparisons, respectively. Ingenuity Pathway Analysis revealed that gene networks identified for the WRRh vs. XHh contrast were associated with developmental disorders. Importantly, the WRRh vs. XHh contrast miRNA–mRNA network was enriched in IGF-1 signaling pathway genes, including FOXO3. A dual-luciferase reporter assay showed that FOXO3 was a target of miR-142-5p. Furthermore, miR-142-5p overexpression significantly decreased FOXO3 mRNA levels and promoted the expression of growth-related genes. These data demonstrated that miR-142-5p targets FOXO3 and promotes growth-related gene expression and regulates skeletal muscle growth in chicken. Comprehensive analysis facilitated the identification of miRNAs and target genes that might contribute to the regulation of skeletal muscle development. Our results provide new clues for understanding the molecular basis of chicken growth.

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Abbreviations

WRR:

Recessive white rock chicken

XH:

Xinghua chicken

FOXO3 :

Forkhead box O3

MyomiRs:

Myogenic miRNAs

DEGs:

Differentially expressed genes

DEMs:

Differentially expressed miRNAs

IPA:

Ingenuity pathway analysis

References

  • Ambs S, Prueitt RL, Yi M, Hudson RS, Howe TM, Petrocca F, Wallace TA, Liu CG, Volinia S, Calin GA, Yfantis HG, Stephens RM, Croce CM (2008) Genomic profiling of microRNA and messenger RNA reveals deregulated microRNA expression in prostate cancer. Cancer Res 68:6162–6170

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bagga S, Bracht J, Hunter S, Massirer K, Holtz J, Eachus R, Pasquinelli AE (2005) Regulation by let-7 and lin-4 miRNAs results in target mRNA degradation. Cell 122:553–563

    Article  CAS  PubMed  Google Scholar 

  • Chen JF, Mandel EM, Thomson JM, Wu Q, Callis TE, Hammond SM, Conlon FL, Wang DZ (2006) The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation. Nat Genet 38:228–233

    Article  CAS  PubMed  Google Scholar 

  • Chen S, Huang X, Yan X, Liang Y, Wang Y, Li X, Peng X, Ma X, Zhang L, Ca Y, Ma T, Cheng L, Qi D, Zheng H, YangX Li X, Liu G (2013) Transcriptome analysis in sheepgrass (Leymus chinensis): a dominant perennial grass of the Eurasian Steppe. PLoS One 8:e67974

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen B, Xu J, He X, Xu H, Li G, Du H, Nie Q, Zhang X (2015) A genome-wide mRNA screen and functional analysis reveal FOXO3 as a candidate gene for chicken growth. PLoS One 10:e137087

    Google Scholar 

  • Darzi NM, Masoudi AA, Vaez TR (2014) Association of single nucleotide polymorphism of GHSR and TGFB2 genes with growth and body composition traits in sire and dam lines of a broiler chicken. Anim Biotechnol 1:13–22

    Article  Google Scholar 

  • Eriksson J, Larson G, Gunnarsson U, Bed’Hom B, Tixier-Boichard M, Stromstedt L, Wright D, Jungerius A, Vereijken A, Randi E, Jensen P, Andersson L (2008) Identification of the yellow skin gene reveals a hybrid origin of the domestic chicken. PLoS Genet 4:e1000010

    Article  PubMed  PubMed Central  Google Scholar 

  • Glazov EA, Cottee PA, Barris WC, Moore RJ, Dalrymple BP, Tizard ML (2008) A microRNA catalog of the developing chicken embryo identified by a deep sequencing approach. Genome Res 18:957–964

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ke SH, Madison EL (1997) Rapid and efficient site-directed mutagenesis by single-tube ‘megaprimer’ PCR method. Nucleic Acids Res 25:3371–3372

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lei MM, Nie QH, Peng X, Zhang DX, Zhang XQ (2005) Single nucleotide polymorphisms of the chicken insulin-like factor binding protein 2 gene associated with chicken growth and carcass traits. Poult Sci 84:1191–1198

    Article  CAS  PubMed  Google Scholar 

  • Lei M, Peng X, Zhou M, Luo C, Nie Q, Zhang X (2008) Polymorphisms of the IGF1R gene and their genetic effects on chicken early growth and carcass traits. BMC Genet 9:70

    Article  PubMed  PubMed Central  Google Scholar 

  • Lemay MA, Donnelly DJ, Russello MA (2013) Transcriptome-wide comparison of sequence variation in divergent ecotypes of kokanee salmon. BMC Genom 14:308

    Article  CAS  Google Scholar 

  • Lewis BP, Burge CB, Bartel DP (2005) Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120:15–20

    Article  CAS  PubMed  Google Scholar 

  • Li T, Wu R, Zhang Y, Zhu D (2011) A systematic analysis of the skeletal muscle miRNA transcriptome of chicken varieties with divergent skeletal muscle growth identifies novel miRNAs and differentially expressed miRNAs. BMC Genom 12:186

    Article  CAS  Google Scholar 

  • Li H, Sun GR, Lv SJ, Wei Y, Han RL, Tian YD, Kang XT (2012) Association study of polymorphisms inside the miR-1657 seed region with chicken growth and meat traits. Br Poult Sci 53:770–776

    Article  CAS  PubMed  Google Scholar 

  • Li Z, Chen B, Feng M, Ouyang H, Zheng M, Ye Q, Nie Q, Zhang X (2015) MicroRNA-23b promotes avian leukosis virus subgroup J (ALV-J) replication by targeting IRF1. Sci Rep 5:10294

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Luo W, Wu H, Ye Y, Li Z, Hao S, Kong L, Zheng X, Lin S, Nie Q, Zhang X (2014) The transient expression of miR-203 and its inhibiting effects on skeletal muscle cell proliferation and differentiation. Cell Death Dis 5:e1347

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mammucari C, Milan G, Romanello V, Masiero E, Rudolf R, Del PP, Burden SJ, Di Lisi R, Sandri C, Zhao J, Goldberg AL, Schiaffino S, Sandri M (2007) FoxO3 controls autophagy in skeletal muscle in vivo. Cell Metab 6:458–471

    Article  CAS  PubMed  Google Scholar 

  • Nie Q, Sun B, Zhang D, Luo C, Ishag NA, Lei M, Yang G, Zhang X (2005) High diversity of the chicken growth hormone gene and effects on growth and carcass traits. J Hered 96:698–703

    Article  CAS  PubMed  Google Scholar 

  • Ouyang H, He X, Li G, Xu H, Jia X, Nie Q, Zhang X (2015) Deep sequencing analysis of miRNA expression in breast Muscle of fast-growing and slow-growing broilers. Int J Mol Sci 16:16242–16262

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rathjen T, Pais H, Sweetman D, Moulton V, Munsterberg A, Dalmay T (2009) High throughput sequencing of microRNAs in chicken somites. FEBS Lett 583:1422–1426

    Article  CAS  PubMed  Google Scholar 

  • Saito Y, Suzuki H, Tsugawa H, Imaeda H, Matsuzaki J, Hirata K, Hosoe N, Nakamura M, Mukai M, Saito H, Hibi T (2012) Overexpression of miR-142-5p and miR-155 in gastric mucosa-associated lymphoid tissue (MALT) lymphoma resistant to Helicobacter pylori eradication. PLoS One 7:e47396

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sandri M, Sandri C, Gilbert A, Skurk C, Calabria E, Picard A, Walsh K, Schiaffino S, Lecker SH, Goldberg AL (2004) Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy. Cell 117:399–412

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schiaffino S, Mammucari C (2011) Regulation of skeletal muscle growth by the IGF1-Akt/PKB pathway: insights from genetic models. Skelet Muscle 1:4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sodhi SS, Song KD, Ghosh M, Sharma N, Lee SJ, Kim JH, Kim N, Mongre RK, Adhikari P, Kim JY, Hong SP, Oh SJ, Jeong DK (2014) Comparative transcriptomic analysis by RNA-seq to discern differential expression of genes in liver and muscle tissues of adult Berkshire and Jeju Native Pig. Gene 546:233–242

    Article  CAS  PubMed  Google Scholar 

  • Valencia-Sanchez MA, Liu J, Hannon GJ, Parker R (2006) Control of translation and mRNA degradation by miRNAs and siRNAs. Genes Dev 20:515–524

    Article  CAS  PubMed  Google Scholar 

  • Xu Z, Ji C, Zhang Y, Zhang Z, Nie Q, Xu J, Zhang D, Zhang X (2016) Combination analysis of genome-wide association and transcriptome sequencing of residual feed intake in quality chickens. BMC Genom 17:594

    Article  Google Scholar 

  • Zhang X, Yan Z, Zhang J, Gong L, Li W, Cui J, Liu Y, Gao Z, Li J, Shen L, Lu Y (2011) Combination of hsa-miR-375 and hsa-miR-142-5p as a predictor for recurrence risk in gastric cancer patients following surgical resection. Ann Oncol 22:2257–2266

    Article  CAS  PubMed  Google Scholar 

  • Zhao J, Brault JJ, Schild A, Cao P, Sandri M, Schiaffino S, Lecker SH, Goldberg AL (2007) FoxO3 coordinately activates protein degradation by the autophagic/lysosomal and proteasomal pathways in atrophying muscle cells. Cell Metab 6:472–483

    Article  CAS  PubMed  Google Scholar 

  • Zhou H, Mitchell AD, McMurtry JP, Ashwell CM, Lamont SJ (2005) Insulin-like growth factor-I gene polymorphism associations with growth, body composition, skeleton integrity, and metabolic traits in chickens. Poult Sci 2:212–219

    Article  Google Scholar 

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Authors and Affiliations

  1. Department of Animal Genetics, Breeding and Reproduction, College of Animal Science, South China Agricultural University, Wushan Street, Tianhe District, Guangzhou, 510642, Guangdong, China

    Zhenhui Li, Bahareldin Ali Abdalla, Ming Zheng, Xiaomei He, Bolin Cai, Peigong Han, Hongjia Ouyang, Biao Chen, Qinghua Nie & Xiquan Zhang

  2. Guangdong Provincial Key Lab of Agro-Animal Genomics and Molecular Breeding and Key Lab of Chicken Genetics, Breeding and Reproduction, Ministry of Agriculture, Guangzhou, Guangdong, China

    Zhenhui Li, Bahareldin Ali Abdalla, Ming Zheng, Xiaomei He, Bolin Cai, Peigong Han, Hongjia Ouyang, Biao Chen, Qinghua Nie & Xiquan Zhang

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  1. Zhenhui Li
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  2. Bahareldin Ali Abdalla
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  3. Ming Zheng
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  4. Xiaomei He
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  5. Bolin Cai
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  7. Hongjia Ouyang
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  8. Biao Chen
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  9. Qinghua Nie
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  10. Xiquan Zhang
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Corresponding author

Correspondence to Qinghua Nie.

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Funding

This research was supported by the Program for New Century Excellent Talents in University (NCET-13-0803), the Natural Scientific Foundation of China (31472090), and the Foundation for High-level Talents in Higher Education in Guangdong, China.

Conflict of interest

Zhenhui Li declares that he has no conflict of interest. Bahareldin Ali Abdalla declares that he has no conflict of interest. Ming Zheng declares that she has no conflict of interest. Xiaomei He declares that she has no conflict of interest. Bolin Cai declares that he has no conflict of interest. Peigong Han declares that he has no conflict of interest. Hongjia Ouyang declares that he has no conflict of interest. Biao Chen declares that he has no conflict of interest. Qinghua Nie declares that he has no conflict of interest. Xiquan Zhang declares that he has no conflict of interest.

Ethical approval

Experiments were designed and performed in compliance with the protocols and guidelines that were established by the Institutional Animal Care and Use Committee at the South China Agricultural University (Guangzhou, China) (approval ID: SCAU#0011) (Chen et al. 2015; Ouyang et al. 2015).

Additional information

Communicated by S. Hohmann.

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Li, Z., Abdalla, B.A., Zheng, M. et al. Systematic transcriptome-wide analysis of mRNA–miRNA interactions reveals the involvement of miR-142-5p and its target (FOXO3) in skeletal muscle growth in chickens. Mol Genet Genomics 293, 69–80 (2018). https://doi.org/10.1007/s00438-017-1364-7

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  • DOI: https://doi.org/10.1007/s00438-017-1364-7

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