Evolution and Distribution of Teleost MyomiRNAs: Functionally Diversified MyomiRs in Teleosts

Overview

Journal Mar Biotechnol (NY)

Specialties Biology
Biotechnology

Date 2016 Jun 6

PMID 27262998

Citations 6

Authors

Bhuiyan Sharmin Siddique

Shigeharu Kinoshita

Chaninya Wongkarangkana

Shuichi Asakawa

Shugo Watabe

Affiliations

Soon will be listed here.

Abstract

Myosin heavy chain (MYH) genes belong to a multigene family, and the regulated expression of each member determines the physiological and contractile muscle properties. Among these, MYH6, MYH7, and MYH14 occupy unique positions in the mammalian MYH gene family because of their specific expression in slow/cardiac muscles and the existence of intronic micro(mi) RNAs. MYH6, MYH7, and MYH14 encode miR-208a, miR-208b, and miR-499, respectively. These MYH encoded miRNAs are designated as myomiRs because of their muscle-specific expression and functions. In mammals, myomiRs and host MYHs form a transcription network involved in muscle fiber-type specification; thus, genomic positions and expression patterns of them are well conserved. However, our previous studies revealed divergent distribution and expression of MYH14/miR-499 among teleosts, suggesting the unique evolution of myomiRs and host MYHs in teleosts. Here, we examined distribution and expression of myomiRs and host MYHs in various teleost species. The major cardiac MYH isoforms in teleosts are an intronless gene, atrial myosin heavy chain (amhc), and ventricular myosin heavy chain (vmhc) gene that encodes an intronic miRNA, miR-736. Phylogenetic analysis revealed that vmhc/miR-736 is a teleost-specific myomiR that differed from tetrapoda MYH6/MYH7/miR-208s. Teleost genomes also contain species-specific orthologs in addition to vmhc and amhc, indicating complex gene duplication and gene loss events during teleost evolution. In medaka and torafugu, miR-499 was highly expressed in slow/cardiac muscles whereas the expression of miR-736 was quite low and not muscle specific. These results suggest functional diversification of myomiRs in teleost with the diversification of host MYHs.

Citing Articles

Global Landscape of m6A Methylation of Differently Expressed Genes in Muscle Tissue of Liaoyu White Cattle and Simmental Cattle.

Dang Y, Dong Q, Wu B, Yang S, Sun J, Cui G Front Cell Dev Biol. 2022; 10:840513.

PMID: 35359442 PMC: 8960853. DOI: 10.3389/fcell.2022.840513.

Myocardial protective effect and transcriptome profiling of Naoxintong on cardiomyopathy in zebrafish.

Hu M, Liu P, Lu S, Wang Z, Lyu Z, Liu H Chin Med. 2021; 16(1):119.

PMID: 34775978 PMC: 8591872. DOI: 10.1186/s13020-021-00532-0.

Evolution after Whole-Genome Duplication: Teleost MicroRNAs.

Desvignes T, Sydes J, Montfort J, Bobe J, Postlethwait J Mol Biol Evol. 2021; 38(8):3308-3331.

PMID: 33871629 PMC: 8321539. DOI: 10.1093/molbev/msab105.

miRNA-Coordinated Schizophrenia Risk Network Cross-Talk With Cardiovascular Repair and Opposed Gliomagenesis.

Cao H, Baranova A, Yue W, Yu H, Zhu Z, Zhang F Front Genet. 2020; 11:149.

PMID: 32194626 PMC: 7064629. DOI: 10.3389/fgene.2020.00149.

MicroRNAs Involved in the Regulation of LC-PUFA Biosynthesis in Teleosts: miR-33 Enhances LC-PUFA Biosynthesis in Siganus canaliculatus by Targeting insig1 which in Turn Upregulates srebp1.

Sun J, Zheng L, Chen C, Zhang J, You C, Zhang Q Mar Biotechnol (NY). 2019; 21(4):475-487.

PMID: 31020472 DOI: 10.1007/s10126-019-09895-w.

References

Schiaffino S, Reggiani C . Fiber types in mammalian skeletal muscles. Physiol Rev. 2011; 91(4):1447-531. DOI: 10.1152/physrev.00031.2010. View

Weiss A, McDonough D, Wertman B, Montgomery K, Kucherlapati R, Leinwand L . Organization of human and mouse skeletal myosin heavy chain gene clusters is highly conserved. Proc Natl Acad Sci U S A. 1999; 96(6):2958-63. PMC: 15877. DOI: 10.1073/pnas.96.6.2958. View

Hoegg S, Brinkmann H, Taylor J, Meyer A . Phylogenetic timing of the fish-specific genome duplication correlates with the diversification of teleost fish. J Mol Evol. 2004; 59(2):190-203. DOI: 10.1007/s00239-004-2613-z. View

Bhuiyan S, Kinoshita S, Wongwarangkana C, Asaduzzaman M, Asakawa S, Watabe S . Evolution of the myosin heavy chain gene MYH14 and its intronic microRNA miR-499: muscle-specific miR-499 expression persists in the absence of the ancestral host gene. BMC Evol Biol. 2013; 13:142. PMC: 3716903. DOI: 10.1186/1471-2148-13-142. View

Ikeda D, Ono Y, Snell P, Edwards Y, Elgar G, Watabe S . Divergent evolution of the myosin heavy chain gene family in fish and tetrapods: evidence from comparative genomic analysis. Physiol Genomics. 2007; 32(1):1-15. DOI: 10.1152/physiolgenomics.00278.2006. View

Kim J, Lim K, Hong J, Kang J, Lee Y, Hong K . A polymorphism in the porcine miR-208b is associated with microRNA biogenesis and expressions of SOX-6 and MYH7 with effects on muscle fibre characteristics and meat quality. Anim Genet. 2014; 46(1):73-7. DOI: 10.1111/age.12255. View

Wang X, Ono Y, Tan S, Chai R, Parkin C, Ingham P . Prdm1a and miR-499 act sequentially to restrict Sox6 activity to the fast-twitch muscle lineage in the zebrafish embryo. Development. 2011; 138(20):4399-404. DOI: 10.1242/dev.070516. View

McGuigan K, Phillips P, Postlethwait J . Evolution of sarcomeric myosin heavy chain genes: evidence from fish. Mol Biol Evol. 2004; 21(6):1042-56. DOI: 10.1093/molbev/msh103. View

Morkin E . Control of cardiac myosin heavy chain gene expression. Microsc Res Tech. 2000; 50(6):522-31. DOI: 10.1002/1097-0029(20000915)50:6<522::AID-JEMT9>3.0.CO;2-U. View

10.

Tamura K, Nei M . Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol. 1993; 10(3):512-26. DOI: 10.1093/oxfordjournals.molbev.a040023. View

11.

Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S . MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 2011; 28(10):2731-9. PMC: 3203626. DOI: 10.1093/molbev/msr121. View

12.

Akolkar D, Kinoshita S, Yasmin L, Ono Y, Ikeda D, Yamaguchi H . Fibre type-specific expression patterns of myosin heavy chain genes in adult torafugu Takifugu rubripes muscles. J Exp Biol. 2009; 213(1):137-45. DOI: 10.1242/jeb.030759. View

13.

Andreassen R, Worren M, Hoyheim B . Discovery and characterization of miRNA genes in Atlantic salmon (Salmo salar) by use of a deep sequencing approach. BMC Genomics. 2013; 14:482. PMC: 3728263. DOI: 10.1186/1471-2164-14-482. View

14.

Kloosterman W, Steiner F, Berezikov E, de Bruijn E, van de Belt J, Verheul M . Cloning and expression of new microRNAs from zebrafish. Nucleic Acids Res. 2006; 34(9):2558-69. PMC: 3303176. DOI: 10.1093/nar/gkl278. View

15.

Desjardins P, Burkman J, Shrager J, Allmond L, Stedman H . Evolutionary implications of three novel members of the human sarcomeric myosin heavy chain gene family. Mol Biol Evol. 2002; 19(4):375-93. DOI: 10.1093/oxfordjournals.molbev.a004093. View

16.

Van Rooij E, Quiat D, Johnson B, Sutherland L, Qi X, Richardson J . A family of microRNAs encoded by myosin genes governs myosin expression and muscle performance. Dev Cell. 2009; 17(5):662-73. PMC: 2796371. DOI: 10.1016/j.devcel.2009.10.013. View

17.

Bell M, Buvoli M, Leinwand L . Uncoupling of expression of an intronic microRNA and its myosin host gene by exon skipping. Mol Cell Biol. 2010; 30(8):1937-45. PMC: 2849460. DOI: 10.1128/MCB.01370-09. View

18.

Tajima F, Nei M . Estimation of evolutionary distance between nucleotide sequences. Mol Biol Evol. 1984; 1(3):269-85. DOI: 10.1093/oxfordjournals.molbev.a040317. View

19.

Van Rooij E, Sutherland L, Qi X, Richardson J, Hill J, Olson E . Control of stress-dependent cardiac growth and gene expression by a microRNA. Science. 2007; 316(5824):575-9. DOI: 10.1126/science.1139089. View

20.

Berdougo E, Coleman H, Lee D, Stainier D, Yelon D . Mutation of weak atrium/atrial myosin heavy chain disrupts atrial function and influences ventricular morphogenesis in zebrafish. Development. 2003; 130(24):6121-9. DOI: 10.1242/dev.00838. View