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

Asaduzzaman, Md.; Kinoshita, Shigeharu; Siddique, Bhuiyan Sharmin; Asakawa, Shuichi; Watabe, Shugo

doi:10.1016/j.gene.2011.08.005

Cited by 17 publications

(6 citation statements)

References 63 publications

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“…Interestingly, sequence comparison analysis showed highly conserved 5′-flanking regions between torafugu MYH M5 and medaka miR-499 (see Figure 5A). The spatio-temporal expression of the major skeletal MYHs in teleost fish is regulated by small regions scattered throughout the 5′-flanking sequence [18,30,34,35]. Recently, Yeung et al [36] reported promoter activity in a 6.2-kb upstream sequence of mouse MYH14 that mimics endogenous MYH14 and miR-499 expression.…”

Section: Discussionmentioning

confidence: 99%

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

et al. 2013

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BackgroundA 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.ResultsSynteny 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.ConclusionsThis 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.

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Section: Discussionmentioning

confidence: 99%

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

et al. 2013

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“…In zebrafish, at least 3 fast skeletal MYH s, myhz1 , myhz2 and myhc4 , are dominantly expressed in fast fibers of embryos [9-11]; orthologs of torafugu [18], medaka [14] and common carp [7,8] are also expressed in embryos from the respective fish species. In addition, the proximal promoters of the above-listed MYH s from torafugu [43,44] and medaka [15] drive the reporter gene expression in the fast fibers of zebrafish embryos. These teleost MYH s are all classified as fast C type [18], suggesting that the proximal promoters of fast skeletal MYH s of lampreys and fast C-type MYH s of teleosts have a common ancestor and share common regulatory mechanisms, even though no synteny (see Figures S1 and S2) [18] or strict orthology (see Figure 2) was found between lamprey and teleost MYH s. Indeed, we found CNEs between promoters of Japanese lamprey MYH s 1 and 2 as well as between Japanese lamprey MYH1 and zebrafish myhz2 and myhc4 (Figure S5A).…”

Section: Discussionmentioning

confidence: 99%

Lampreys Have a Single Gene Cluster for the Fast Skeletal Myosin Heavy Chain Gene Family

et al. 2013

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Muscle tissues contain the most classic sarcomeric myosin, called myosin II, which consists of 2 heavy chains (MYHs) and 4 light chains. In the case of humans (tetrapod), a total of 6 fast skeletal-type MYH genes (MYHs) are clustered on a single chromosome. In contrast, torafugu (teleost) contains at least 13 fast skeletal MYHs, which are distributed in 5 genomic regions; the MYHs are clustered in 3 of these regions. In the present study, the evolutionary relationship among fast skeletal MYHs is elucidated by comparing the MYHs of teleosts and tetrapods with those of cyclostome lampreys, one of two groups of extant jawless vertebrates (agnathans). We found that lampreys contain at least 3 fast skeletal MYHs, which are clustered in a head-to-tail manner in a single genomic region. Although there was apparent synteny in the corresponding MYH cluster regions between lampreys and tetrapods, phylogenetic analysis indicated that lamprey and tetrapod MYHs have independently duplicated and diversified. Subsequent transgenic approaches showed that the 5′-flanking sequences of Japanese lamprey fast skeletal MYHs function as a regulatory sequence to drive specific reporter gene expression in the fast skeletal muscle of zebrafish embryos. Although zebrafish MYH promoters showed apparent activity to direct reporter gene expression in myogenic cells derived from mice, promoters from Japanese lamprey MYHs had no activity. These results suggest that the muscle-specific regulatory mechanisms are partially conserved between teleosts and tetrapods but not between cyclostomes and tetrapods, despite the conserved synteny.

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“…Effects of CFL2 on muscle fiber types. Four MyHC isoforms (I, IIa, IIx and IIb) are expressed in adult skeletal muscles (6). MyHCs are the primary molecular markers for distinguishing muscle fiber types and studying their characteristics.…”

Section: Discussionmentioning

confidence: 99%

“…Four isoforms of myosin heavy chain (MyHC) are expressed in skeletal muscle throughout the period of development, and are determinants of muscle development (6): I, slow oxidative; IIa, fast oxidative; IIb, fast glycolytic; and IIx/d, mixed (7). It was previously suggested that MyHC composition affects meat quality in livestock (8).…”

Section: Introductionmentioning

confidence: 99%

Role of the cofilin 2 gene in regulating the myosin heavy chain genes in mouse myoblast C2C12 cells

et al. 2017

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The cofilin 2 (CFL2) and myosin heavy chain (MyHC) genes play a key role in muscle development and myofibrillar formation. The aim of the present study was to investigate the effect of CFL2 on genes involved in fiber formation and the mechanisms underlying this process. Undifferentiated and differentiated C2C12 cells (UDT and DT, respectively) were transfected with CFL2 small interfering RNA (siRNA). CFL2 mRNA and protein levels were assessed using reverse transcription polymerase chain reaction (RT-PCR) and western blotting, respectively. MyHC gene expression in UDT and signaling pathway-related factors were observed with quantitative PCR (RT‑qPCR) and western blotting. Fluorescence microscopy was used to analyze the cytoskeletal effects of CFL2. The mRNA and protein expressions of CFL2, four MyHC isoforms (MyHC-I, MyHC-IIa, MyHC-IIb and MyHC-IIx), p38 mitogen-activated protein kinase, cAMP-response element-binding protein, AMP-activated protein kinase α1, and myocyte enhancer factor 2C, were significantly decreased in UDT. However, extracellular signal-regulated kinase 2 expression was significantly increased. Slightly decreased CFL2 protein and mRNA expression was observed in DT C2C12 cells transfected with CFL2 siRNA. Fluorescence microscopy revealed a significant decrease of CFL2 in the cytoplasm, but not the nucleus, of UDT, compared with normal cells. These results indicated that the mouse CFL2 gene may be involved in the regulation of MyHC via the key signaling molecules of CFL2-related signaling pathways.

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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

Cited by 17 publications

References 63 publications

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

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

Lampreys Have a Single Gene Cluster for the Fast Skeletal Myosin Heavy Chain Gene Family

Role of the cofilin 2 gene in regulating the myosin heavy chain genes in mouse myoblast C2C12 cells

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