Comparative Analyses of Longissimus Muscle MiRNAomes Reveal MicroRNAs Associated with Differential Regulation of Muscle Fiber Development Between Tongcheng and Yorkshire Pigs

Overview

Journal PLoS One

Specialties General Medicine
Science

Date 2018 Jul 12

PMID 29995940

Citations 6

Authors

Yu Xi

Huijing Liu

Yuqiang Zhao

Ji Li

Wenchao Li

Guorong Liu

Jiayong Lin

Wanghong Liu

Jinlong Zhang

Minggang Lei

Debin Ni

Affiliations

Soon will be listed here.

Abstract

Tongcheng (TC) and Yorkshire (YK) are two pig breeds with distinctive muscle morphology. Porcine microRNAome (miRNAome) of the longissimus muscle during five developmental stages (40, 55, 63, 70, and 90 days post coitum (dpc)) was explored by Solexa sequencing in the present study to find miRNAs involved in the different regulation of skeletal muscle development between the two breeds. A total of 320 known porcine miRNAs, 64 miRNAs corresponding to other mammals, and 224 potentially novel miRNAs were identified. Principal component analysis (PCA) and hierarchical cluster analysis (HCA) suggested that the factor "pig breed" affected the miRNA expression profiles to a lesser extent than the factor "developmental stage". Fifty-seven miRNAs were differentially expressed (DE) between the neighbor developmental stages in TC and 45 such miRNAs were found in YK, 34 in common; there were more down-regulated stage-DE miRNAs than up-regulated. And a total of 23, 30, 12, 6, and 30 breed-DE miRNAs between TC and YK were identified at 40, 55, 63, 70, and 90 dpc, respectively, which were mainly involved in cellular protein modification process, protein transport, and metabolic process. As the only highly expressed breed-DE miRNA found in no less than four developmental stages, and also a stage-DE miRNA found both in TC and YK, miR-499-5p could bind the 3'-UTR of a myofibrillogenesis regulator, destrin/actin depolymerizing factor (DSTN), as validated in dual luciferase reporter assay. The results suggested that miR-499-5p possibly play a noteworthy role in the breed-distinctive porcine muscle fiber development associated with the regulation of DSTN.

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References

Lin M, Nguyen H, Dybala C, Storti R . Myocyte-specific enhancer factor 2 acts cooperatively with a muscle activator region to regulate Drosophila tropomyosin gene muscle expression. Proc Natl Acad Sci U S A. 1996; 93(10):4623-8. PMC: 39328. DOI: 10.1073/pnas.93.10.4623. View

Ma Z, Sun X, Xu D, Xiong Y, Zuo B . MicroRNA, miR-374b, directly targets Myf6 and negatively regulates C2C12 myoblasts differentiation. Biochem Biophys Res Commun. 2015; 467(4):670-5. DOI: 10.1016/j.bbrc.2015.10.086. View

Chen C, Deng B, Qiao M, Zheng R, Chai J, Ding Y . Solexa sequencing identification of conserved and novel microRNAs in backfat of Large White and Chinese Meishan pigs. PLoS One. 2012; 7(2):e31426. PMC: 3280305. DOI: 10.1371/journal.pone.0031426. View

Wimmers K, Ngu N, Jennen D, Tesfaye D, Murani E, Schellander K . Relationship between myosin heavy chain isoform expression and muscling in several diverse pig breeds. J Anim Sci. 2007; 86(4):795-803. DOI: 10.2527/jas.2006-521. View

Bandiera S, Pfeffer S, Baumert T, Zeisel M . miR-122--a key factor and therapeutic target in liver disease. J Hepatol. 2014; 62(2):448-57. DOI: 10.1016/j.jhep.2014.10.004. View

Zhao X, Mo D, Li A, Gong W, Xiao S, Zhang Y . Comparative analyses by sequencing of transcriptomes during skeletal muscle development between pig breeds differing in muscle growth rate and fatness. PLoS One. 2011; 6(5):e19774. PMC: 3102668. DOI: 10.1371/journal.pone.0019774. View

Larzul C, Lefaucheur L, Ecolan P, Gogue J, Talmant A, Sellier P . Phenotypic and genetic parameters for longissimus muscle fiber characteristics in relation to growth, carcass, and meat quality traits in large white pigs. J Anim Sci. 1998; 75(12):3126-37. DOI: 10.2527/1997.75123126x. View

Bober E, Franz T, Arnold H, Gruss P, Tremblay P . Pax-3 is required for the development of limb muscles: a possible role for the migration of dermomyotomal muscle progenitor cells. Development. 1994; 120(3):603-12. DOI: 10.1242/dev.120.3.603. View

Obinata T, Ono S, Kusano K, Mohri K, Ohtaka Y, Yamashiro S . Low molecular-weight G-actin binding proteins involved in the regulation of actin assembly during myofibrillogenesis. Cell Struct Funct. 1997; 22(1):181-9. DOI: 10.1247/csf.22.181. View

10.

Seale P, Sabourin L, Girgis-Gabardo A, Mansouri A, Gruss P, Rudnicki M . Pax7 is required for the specification of myogenic satellite cells. Cell. 2000; 102(6):777-86. DOI: 10.1016/s0092-8674(00)00066-0. View

11.

Lefaucheur L, Vigneron P . Post-natal changes in some histochemical and enzymatic characteristics of three pig muscles. Meat Sci. 2011; 16(3):199-216. DOI: 10.1016/0309-1740(86)90026-4. View

12.

Qin L, Chen Y, Liu X, Ye S, Yu K, Huang Z . Integrative analysis of porcine microRNAome during skeletal muscle development. PLoS One. 2013; 8(9):e72418. PMC: 3770649. DOI: 10.1371/journal.pone.0072418. View

13.

Chitwood D, Timmermans M . Small RNAs are on the move. Nature. 2010; 467(7314):415-9. DOI: 10.1038/nature09351. View

14.

Lai Z, Lin P, Weng X, Su J, Chen Y, He Y . MicroRNA-574-5p promotes cell growth of vascular smooth muscle cells in the progression of coronary artery disease. Biomed Pharmacother. 2017; 97:162-167. DOI: 10.1016/j.biopha.2017.10.062. View

15.

Liu H, Xi Y, Liu G, Zhao Y, Li J, Lei M . Comparative transcriptomic analysis of skeletal muscle tissue during prenatal stages in Tongcheng and Yorkshire pig using RNA-seq. Funct Integr Genomics. 2018; 18(2):195-209. DOI: 10.1007/s10142-017-0584-6. View

16.

Huntzinger E, Izaurralde E . Gene silencing by microRNAs: contributions of translational repression and mRNA decay. Nat Rev Genet. 2011; 12(2):99-110. DOI: 10.1038/nrg2936. View

17.

Ashmore C, Addis P, Doerr L . Development of muscle fibers in the fetal pig. J Anim Sci. 1973; 36(6):1088-93. DOI: 10.2527/jas1973.3661088x. View

18.

Nariyama M, Mori M, Shimazaki E, Ando H, Ohnuki Y, Abo T . Functions of miR-1 and miR-133a during the postnatal development of masseter and gastrocnemius muscles. Mol Cell Biochem. 2015; 407(1-2):17-27. DOI: 10.1007/s11010-015-2450-y. View

19.

Wu F, Zuo J, Yu Q, Zou S, Tan H, Xiao J . Effect of skeletal muscle fibers on porcine meat quality at different stages of growth. Genet Mol Res. 2015; 14(3):7873-82. DOI: 10.4238/2015.July.14.13. View

20.

Calabrese J, Seila A, Yeo G, Sharp P . RNA sequence analysis defines Dicer's role in mouse embryonic stem cells. Proc Natl Acad Sci U S A. 2007; 104(46):18097-102. PMC: 2084302. DOI: 10.1073/pnas.0709193104. View