BMC Evolutionary Biology | |
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 | |
Shugo Watabe1  Shuichi Asakawa2  Md Asaduzzaman2  Chaninya Wongwarangkana2  Shigeharu Kinoshita2  Sharmin Siddique Bhuiyan2  | |
[1] School of Marine Bioscience, Kitasato University, Minami, Sagamihara, Kanagawa 252-0373, Japan;Department of Aquatic Bioscience, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Bunkyo, Tokyo 113-8657, Japan | |
关键词: Teleostei; Muscle fiber-type; Muscle; miR-499; microRNA; MYH14 (MYH7b); Myosin heavy chain; | |
Others : 1086890 DOI : 10.1186/1471-2148-13-142 |
|
received in 2012-11-27, accepted in 2013-06-13, 发布年份 2013 | |
![]() |
【 摘 要 】
Background
A novel sarcomeric myosin heavy chain gene, MYH14, was identified following the completion of the human genome project. MYH14 contains an intronic microRNA, miR-499, which is expressed in a slow/cardiac muscle specific manner along with its host gene; it plays a key role in muscle fiber-type specification in mammals. Interestingly, teleost fish genomes contain multiple MYH14 and miR-499 paralogs. However, the evolutionary history of MYH14 and miR-499 has not been studied in detail. In the present study, we identified MYH14/miR-499 loci on various teleost fish genomes and examined their evolutionary history by sequence and expression analyses.
Results
Synteny and phylogenetic analyses depict the evolutionary history of MYH14/miR-499 loci where teleost specific duplication and several subsequent rounds of species-specific gene loss events took place. Interestingly, miR-499 was not located in the MYH14 introns of certain teleost fish. An MYH14 paralog, lacking miR-499, exhibited an accelerated rate of evolution compared with those containing miR-499, suggesting a putative functional relationship between MYH14 and miR-499. In medaka, Oryzias latipes, miR-499 is present where MYH14 is completely absent in the genome. Furthermore, by using in situ hybridization and small RNA sequencing, miR-499 was expressed in the notochord at the medaka embryonic stage and slow/cardiac muscle at the larval and adult stages. Comparing the flanking sequences of MYH14/miR-499 loci between torafugu Takifugu rubripes, zebrafish Danio rerio, and medaka revealed some highly conserved regions, suggesting that cis-regulatory elements have been functionally conserved in medaka miR-499 despite the loss of its host gene.
Conclusions
This study reveals the evolutionary history of the MYH14/miRNA-499 locus in teleost fish, indicating divergent distribution and expression of MYH14 and miR-499 genes in different teleost fish lineages. We also found that medaka miR-499 was even expressed in the absence of its host gene. To our knowledge, this is the first report that shows the conversion of intronic into non-intronic miRNA during the evolution of a teleost fish lineage.
【 授权许可】
2013 Bhuiyan et al.; licensee BioMed Central Ltd.
【 预 览 】
Files | Size | Format | View |
---|---|---|---|
20150116020506787.pdf | 1193KB | ![]() |
|
Figure 5. | 45KB | Image | ![]() |
Figure 4. | 104KB | Image | ![]() |
Figure 3. | 85KB | Image | ![]() |
Figure 2. | 48KB | Image | ![]() |
Figure 1. | 69KB | Image | ![]() |
【 图 表 】
Figure 1.
Figure 2.
Figure 3.
Figure 4.
Figure 5.
【 参考文献 】
- [1]Schiaffino S, Reggiani C: Fiber types in mammalian skeletal muscles. Physiol Rev 2011, 91:1447-1531.
- [2]Mahdavi V, Chambers AP, Nadal-Ginard B: Cardiac alpha- and beta-myosin heavy chain genes are organized in tandem. Proc Natl Acad Sci USA 1984, 81:2626-2630.
- [3]Saez LJ, Gianola KM, McNally EM, Feghali R, Eddy R, Shows TB, Leinwand LA: Human cardiac myosin heavy chain genes and their linkage in the genome. Nucleic Acids Res 1987, 15:5443-5459.
- [4]Weiss A, McDonough D, Wertman B, Acakpo-Satchivi L, Montgomery K, Kucherlapati R, Leinwand L, Krauter K: Organization of human and mouse skeletal myosin heavy chain gene clusters is highly conserved. Proc Natl Acad Sci USA 1999, 96:2958-2963.
- [5]Shrager JB, Desjardins PR, Burkman JM, Konig SK, Stewart SK, Su L, Shah MC, Bricklin E, Tewari M, Hoffman R, Rickels MR, Jullian EH, Rubinstein NA, Stedman HH: Human skeletal myosin heavy chain genes are tightly linked in the order embryonic-IIa-IId/x-ILb-perinatal-extraocular. J Muscle Res Cell Motil 2000, 21:345-355.
- [6]Desjardins PR, Burkman JM, Shrager JB, Allmond LA, Stedman HH: Evolutionary implications of three novel members of the human sarcomeric myosin heavy chain gene family. Mol Biol Evol 2002, 19:375-393.
- [7]van Rooij E, Quiat D, Johnson BA, Sutherland LB, Qi X, Richardson JA, Kelm RJ Jr, Olson EN: A family of microRNAs encoded by myosin genes governs myosin expression and muscle performance. Dev Cell 2009, 17:662-673.
- [8]Bartel DP: MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004, 116:281-297.
- [9]McCarthy JJ, Esser AK, Peterson AC, Dupont-Versteegden EE: Evidence of MyomiR network regulation of β-myosin heavy chain gene expression during skeletal muscle atrophy. Physiol Genomics 2009, 39:219-226.
- [10]Hagiwara N, Yeh M, Liu A: Sox6 is required for normal fiber type differentiation of fetal skeletal muscle in mice. Dev Dyn 2007, 236:2062-2076.
- [11]von Hofsten J, Elworthy S, Gilchrist MJ, Smith JC, Wardle FC, Ingham PW: Prdm1- and Sox6-mediated transcriptional repression specifies muscle fiber type in the zebrafish embryo. EMBO Rep 2008, 9:683-689.
- [12]Watabe S, Ikeda D: Diversity of the pufferfish Takifugu rubripes fast skeletal myosin heavy chain genes. Comp Biochem Physiol 2006, 1:28-34.
- [13]Ikeda D, Ono Y, Snell P, Edwards YJ, 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, 32:1-15.
- [14]Akolkar DB, Kinoshita S, Yasmin L, Ono Y, Ikeda D, Yamaguchi H, Nakaya M, Erdogan O, Watabe S: Fibre type-specific expression patterns of myosin heavy chain genes in adult torafugu Takifugu rubripes muscles. J Exp Biol 2010, 213:137-145.
- [15]Kinoshita S, Bhuiyan SS, Ceyhun SB, Asaduzzaman M, Asakawa S, Watabe S: Species-specific expression variation of fish MYH14, an ancient vertebrate myosin heavy chain gene orthologue. Fish Sci 2011, 77:847-853.
- [16]Wang X, Ono Y, Tan CS, Chai RJ, Philip C, Ingham PW: Prdm1a and miR-499 act sequentially to restrict Sox6 activity to the fast-twitch muscle lineage in the zebrafish embryo. Development 2011, 138:4399-4404.
- [17]Ikeda D, Clark MS, Liang CS, Snell P, Edwards YJK, Elgar G, Watabe S: Genomic structural analysis of the pufferfish (Takifugu rubripes) skeletal muscle myosin heavy chain genes. Mar Biotechnol 2004, 6:S462-S467.
- [18]Liang CS, Kobiyama A, Shimizu A, Sasaki T, Asakawa S, Shimizu N, Watabe S: Fast skeletal muscle myosin heavy chain gene cluster of medaka Oryzias latipes enrolled in temperature adaptation. Physiol Genomics 2007, 29:201-214.
- [19]Monteys AM, Spengler RM, Wan J, Tecedor L, Lennox KA, Xing Y, Davidson BL: Structure and activity of putative intronic miRNA promoters. RNA 2010, 16:495-505.
- [20]Kim VN, Han J, Siomi MC: Biogenesis of small RNAs in animals. Nat Rev Mol Cell Biol 2009, 10:126-139.
- [21]Berezikov E, Chung WJ, Willis J, Cuppen E, Lai EC: Mammalian mirtron genes. Mol Cell 2007, 28:328-336.
- [22]Okamura K, Hagen JW, Duan H, Tyler DM, Lai EC: The mirtron pathway generates microRNA-class regulatory RNAs in drosophila. Cell 2007, 130:89-100.
- [23]Ruby JG, Jan CH, Bartel DP: Intronic microRNA precursors that bypass drosha processing. Nature 2007, 448:83-86.
- [24]Amores A, Force A, Yan YL, Joly L, Amemiya C, Fritz A, Ho RK, Langeland J, Prince V, Wang YL, Westerfield M, Ekker M, Postlethwait JH: Zebrafish hox clusters and vertebrate genome evolution. Science 1998, 282:1711-1714.
- [25]Elgar G, Clark MS, Meek S, Smith S, Warner S, Edwards YJ, Bouchireb N, Cottage A, Yeo GS, Umrania Y, Williams G, Brenner S: Generation and analysis of 25 Mb of genomic DNA from the pufferfish Fugu rubripes by sequence scanning. Genome Res 1999, 9:960-971.
- [26]Postlethwait JH, Woods IG, Ngo-Hazelett P, Yan YL, Kelly PD, Chu F, Huang H, Hill-Force A, Talbot WS: Zebrafish comparative genomics and the origins of vertebrate chromosomes. Genome Res 2000, 10:1890-1902.
- [27]Woods IG, Kelly PD, Chu F, Ngo-Hazelett P, Yan YL, Huang H, Postlethwait JH, Talbot WS: A comparative map of the zebrafish genome. Genome Res 2000, 10:1903-1914.
- [28]Smith SF, Snell P, Gruetzner F, Bench AJ, Haaf T, Metcalfe JA, Green AR, Elgar G: Analyses of the extent of shared synteny and conserved gene orders between the genome of Fugu rubripes and human 20q. Genome Res 2002, 12:776-784.
- [29]Hoegg S, Brinkmann H, Taylor JS, Meyer A: Phylogenetic timing of the fish-specific genome duplication correlates with the diversification of the teleost fish. J Mol Evol 2004, 59:190-203.
- [30]Ono Y, Kinoshita S, Ikeda D, Watabe S: Early development of medaka Oryzias latipes muscles as revealed by transgenic approaches using embryonic and larval types of myosin heavy chain genes. Dev Dyn 2010, 239:1807-1817.
- [31]Liang CS, Ikeda D, Kinoshita S, Shimizu A, Sasaki T, Asakawa S, Shimizu N, Watabe S: Myocyte enhancer factor 2 regulates expression of medaka Oryzias latipes fast skeletal myosin heavy chain genes in a temperature-dependent manner. Gene 2008, 407:42-53.
- [32]Baskerville S, Bartel DP: Microarray profiling of microRNAs reveals frequent coexpression with neighboring miRNAs and host genes. RNA 2005, 11:241-247.
- [33]Kim YK, Kim VN: Processing of intronic microRNAs. EMBO J 2007, 26:775-783.
- [34]Yasmin L, Kinoshita S, Akolkar DB, Asaduzzaman M, Ikeda D, Ono Y, Watabe S: A 5′-flanking region of embryonic-type myosin heavy chain gene, MYHM743-2, from torafugu (Takifugu rubripes) regulates developmental muscle-specific expression. Comp Biochem Physiol 2010, 6:76-81.
- [35]Asaduzzaman M, Kinoshita S, Bhuiyan SS, Asakawa S, Watabe S: Multiple cis-elements in the 5′-flanking region of embryonic/larval fast-type of the myosin heavy chain gene of torafugu, MYHM743-2, function in the transcriptional regulation of its expression. Gene 2011, 489:41-54.
- [36]Yeung F, Chung E, Guess MG, Bell ML, Leinwand LA: Myh7b/miR-499 gene expression is transcriptionally regulated by MRFs and EOS. Nucleic Acids Res 2012, 40:7303-7318.
- [37]Matthew LB, Massimo B, Leslie AL: Uncoupling of expression of an intronic microRNA and its myosin host gene by exon skipping. Mol Cell Biol 2010, 30:1937-1945.
- [38]Isik M, Hendrik CK, Berezikov E: Expression patterns of intronic microRNAs inCaenorhabditis elegans. Silence 2010, 1:1-5. BioMed Central Full Text
- [39]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, 28:2731-2739.
- [40]Nei M, Gojobori T: Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 1986, 3:418-426.
- [41]Tajima F, Nei M: Estimation of evolutionary distance between nucleotide sequences. Mol Biol Evol 1984, 1:269-285.
- [42]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, 10:512-526.
- [43]Kloosterman WP, Wienholds E, de Bruijn E, Kauppinen S, Plasterk RH: In situ detection of miRNAs in animal embryos using LNA-modified oligonucleotide probes. Nat Methods 2006, 3:27-29.