Publications by year
2018
Yin J, Lee R, Ono Y, Ingham PW, Saunders TE (2018). Spatiotemporal Coordination of FGF and Shh Signaling Underlies the Specification of Myoblasts in the Zebrafish Embryo.
Developmental Cell,
46(6), 735-750.e4.
Abstract:
Spatiotemporal Coordination of FGF and Shh Signaling Underlies the Specification of Myoblasts in the Zebrafish Embryo
© 2018 Elsevier Inc. Somitic cells give rise to a variety of cell types in response to Hh, BMP, and FGF signaling. Cell position within the developing zebrafish somite is highly dynamic: how, when, and where these signals specify cell fate is largely unknown. Combining four-dimensional imaging with pathway perturbations, we characterize the spatiotemporal specification and localization of somitic cells. Muscle formation is guided by highly orchestrated waves of cell specification. We find that FGF directly and indirectly controls the differentiation of fast and slow-twitch muscle lineages, respectively. FGF signaling imposes tight temporal control on Shh induction of slow muscles by regulating the time at which fast-twitch progenitors displace slow-twitch progenitors from contacting the Shh-secreting notochord. Further, we find a reciprocal regulation of fast and slow muscle differentiation, morphogenesis, and migration. In conclusion, robust cell fate determination in the developing somite requires precise spatiotemporal coordination between distinct cell lineages and signaling pathways. Precise spatiotemporal control of signaling pathway activation is crucial for cell fate control and tissue patterning. Yin et al. map somitic cell fates in the developing zebrafish with four-dimensional imaging. FGF signaling imposes tight temporal control on Shh induction of muscle pioneers by non-autonomously regulating migration timing of slow-twitch muscles.
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2017
Gurung R, Ono Y, Baxendale S, Lee SLC, Moore S, Calvert M, Ingham PW (2017). A Zebrafish Model for a Human Myopathy Associated with Mutation of the Unconventional Myosin MYO18B.
GENETICS,
205(2), 725-735.
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2015
Ono Y, Yu W, Jackson HE, Parkin CA, Ingham PW (2015). Adaxial cell migration in the zebrafish embryo is an active cell autonomous property that requires the Prdm1a transcription factor. Differentiation, 89(3-4), 77-86.
Jackson HE, Ono Y, Wang X, Elworthy S, Cunliffe VT, Ingham PW (2015). The role of Sox6 in zebrafish muscle fiber type specification.
SKELETAL MUSCLE,
5 Author URL.
2013
Ikeda D, Ono Y, Hirano S, Kan-no N, Watabe S (2013). Lampreys have a single gene cluster for the fast skeletal myosin heavy chain gene family.
PLoS One,
8(12).
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Lampreys have a single gene cluster for the fast skeletal myosin heavy chain gene family.
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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2011
Yasmin L, Kinoshita S, Asaduzzaman M, Akolkar DB, Ikeda D, Ono Y, Watabe S (2011). A 5'-flanking region of embryonic-type myosin heavy chain gene, MYH(M)₇₄₃₋₂, from torafugu Takifugu rubripes regulates developmental muscle-specific expression.
Comp Biochem Physiol Part D Genomics Proteomics,
6(1), 76-81.
Abstract:
A 5'-flanking region of embryonic-type myosin heavy chain gene, MYH(M)₇₄₃₋₂, from torafugu Takifugu rubripes regulates developmental muscle-specific expression.
The myosin heavy chain gene, MYH(M)₇₄₃₋₂, is highly expressed in fast muscle fibers of torafugu embryos. However, the regulatory mechanisms involved in its expression have been unclear. In this study, we examined spatio-temporal expression patterns of this gene during development by injecting expression vectors containing the GFP reporter gene fused to the 5'-flanking region of MYH(M)₇₄₃₋₂ into fertilized eggs of zebrafish and medaka. Although the -2.1kb 5'-flanking region of torafugu MYH(M)₇₄₃₋₂ showed no homology with the corresponding regions of zebrafish and medaka orthologous genes on the rVISTA analysis, the torafugu 5'-flanking region activated the GFP expression which was detected in the myotomal compartment for both zebrafish and medaka embryos. The GFP expression was localized to fast and slow muscle fibers in larvae as revealed by immunohistochemical analysis. In addition to the above tissues, GFP was also expressed in jaw, eye and pectoral fin muscles in embryos and larvae. These results clearly demonstrated that the 2.1 kb 5'-flanking region of MYH(M)₇₄₃₋₂ contains essential cis-regulatory sequences for myogenesis that are conserved among torafugu, zebrafish and medaka.
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Wang X, Ono Y, Tan SC, Chai RJ, Parkin C, Ingham PW (2011). Prdm1a and miR-499 act sequentially to restrict Sox6 activity to the fast-twitch muscle lineage in the zebrafish embryo. Development, 138(20), 4399-4404.
2010
Ono Y, Kinoshita S, Ikeda D, Watabe S (2010). Early development of medaka Oryzias latipes muscles as revealed by transgenic approaches using embryonic and larval types of myosin heavy chain genes.
Dev Dyn,
239(6), 1807-1817.
Abstract:
Early development of medaka Oryzias latipes muscles as revealed by transgenic approaches using embryonic and larval types of myosin heavy chain genes.
We cloned three full-length cDNAs encoding myosin heavy chains (MYHs) previously found to be expressed in embryos or larvae of medaka Oryzias latipes. Based on cDNA sequence information, the three medaka MYH genes, mMYH(emb1), mMYH(L1) and mMYH(L2), were localized on the chromosomes. In vivo promoter assay using the gene encoding green or red fluorescent protein and linked to the 5'-flanking region of mMYH demonstrated that the transcripts of fast-type mMYH(emb1), first expressed in embryos but belonging to the adult type in phylogenetic analysis, were located in the horizontal myoseptum. On the other hand, embryonic fast-type mMYH(L1) and mMYH(L2) were expressed in the whole myotomes. Interestingly, cells expressing mMYH(emb1) were localized together with engrailed, and cyclopamine, which blocks hedgehog signaling, inhibited mMYH(emb1) expression as well as the formation of the horizontal myoseptum, suggesting that muscle pioneer cells express mMYH(emb1) as a key protein in the formation of the horizontal myoseptum.
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Akolkar DB, Kinoshita S, Yasmin L, Ono Y, Ikeda D, Yamaguchi H, Nakaya M, Erdogan O, Watabe S (2010). Fibre type-specific expression patterns of myosin heavy chain genes in adult torafugu Takifugu rubripes muscles.
J Exp Biol,
213(1), 137-145.
Abstract:
Fibre type-specific expression patterns of myosin heavy chain genes in adult torafugu Takifugu rubripes muscles.
Comprehensive in silico studies, based on the total fugu genome database, which was the first to appear in fish, revealed that torafugu Takifugu rubripes contains 20 sarcomeric myosin heavy chain (MYH) genes (MYH genes) (Ikeda et al. 2007). The present study was undertaken to identify MYH genes that would be expressed in adult muscles. In total, seven MYH genes were found by screening cDNA clone libraries constructed from fast, slow and cardiac muscles. Three MYH genes, fast-type MYH(M86-1), slow-type MYH(M8248) and slow/cardiac-type MYH(M880), were cloned exclusively from fast, slow and cardiac muscles, respectively. Northern blot hybridization substantiated their specific expression, with the exception of MYH(M880). In contrast, transcripts of fast-type MYH(M2528-1) and MYH(M1034) were found in both fast and slow muscles as revealed by cDNA clone library and northern blot techniques. This result was supported by in situ hybridization analysis using specific RNA probes, where transcripts of fast-type MYH(M2528-1) were expressed in fast fibres with small diameters as well as in fibres of superficial slow muscle with large diameters adjacent to fast muscle. Transcripts of fast-type MYH(M86-1) were expressed in all fast fibres with different diameters, whereas transcripts of slow-type MYH(M8248) were restricted to fibres with small diameters located in a superficial part of slow muscle. Interestingly, histochemical analyses showed that fast fibres with small diameters and slow fibres with large diameters both contained acid-stable myofibrillar ATPase, suggesting that these fibres have similar functions, possibly in the generation of muscle fibres irrespective of their fibre types.
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Ikeda D, Nihei Y, Ono Y, Watabe S (2010). Three embryonic myosin heavy chain genes encoding different motor domain structures from common carp show distinct expression patterns in cranial muscles.
Mar Genomics,
3(1), 1-9.
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Three embryonic myosin heavy chain genes encoding different motor domain structures from common carp show distinct expression patterns in cranial muscles.
Three embryonic myosin heavy chain (MYH) genes > (MYHs) including MYH(emb1), MYH(emb2) and MYH(emb3) and encoding a C-terminal part of MYH were previously cloned and demonstrated to be expressed transiently in this order during development of common carp Cyprinus carpio embryos. The present study determined the full-length cDNA nucleotide sequences encoding the motor domain of the three MYHs, suggesting the implication of loop 1 and loop 2 sequences for the differences in the motor functions. Phylogenetic analysis based on the full-length amino acid sequences showed that MYH(emb1) and MYH(emb2) both belong to the fast types, though clearly differ from fast-type MYHs expressed in adult fast muscle previously reported. In contrast, MYH(emb3) was in a clade containing slow/cardiac type. Whole-mount immunostaining and in situ hybridization showed that the transcripts of the three embryonic MYHs are localized in the same or different cranial muscles of common carp larvae, suggesting that the three MYHs function cooperatively or individually in various cranial muscles.
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2007
Ikeda D, Ono Y, Snell P, Edwards YJK, Elgar G, Watabe S (2007). Divergent evolution of the myosin heavy chain gene family in fish and tetrapods: evidence from comparative genomic analysis.
Physiol Genomics,
32(1), 1-15.
Abstract:
Divergent evolution of the myosin heavy chain gene family in fish and tetrapods: evidence from comparative genomic analysis.
Myosin heavy chain genes (MYHs) are the most important functional domains of myosins, which are highly conserved throughout evolution. The human genome contains 15 MYHs, whereas the corresponding number in teleost appears to be much higher. Although teleosts comprise more than one-half of all vertebrate species, our knowledge of MYHs in teleosts is rather limited. A comprehensive analysis of the torafugu (Takifugu rubripes) genome database enabled us to detect at least 28 MYHs, almost twice as many as in humans. RT-PCR revealed that at least 16 torafugu MYH representatives (5 fast skeletal, 3 cardiac, 2 slow skeletal, 1 superfast, 2 smooth, and 3 nonmuscle types) are actually transcribed. Among these, MYH(M743-2) and MYH(M5) of fast and slow skeletal types, respectively, are expressed during development of torafugu embryos. Syntenic analysis reveals that torafugu fast skeletal MYHs are distributed across five genomic regions, three of which form clusters. Interestingly, while human fast skeletal MYHs form one cluster, its syntenic region in torafugu is duplicated, although each locus contains just a single MYH in torafugu. The results of the syntenic analysis were further confirmed by corresponding analysis of MYHs based on databases from Tetraodon, zebrafish, and medaka genomes. Phylogenetic analysis suggests that fast skeletal MYHs evolved independently in teleosts and tetrapods after fast skeletal MYHs had diverged from four ancestral MYHs.
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2006
Nihei Y, Kobiyama A, Ikeda D, Ono Y, Ohara S, Cole NJ, Johnston IA, Watabe S (2006). Molecular cloning and mRNA expression analysis of carp embryonic, slow and cardiac myosin heavy chain isoforms.
J Exp Biol,
209(Pt 1), 188-198.
Abstract:
Molecular cloning and mRNA expression analysis of carp embryonic, slow and cardiac myosin heavy chain isoforms.
Three embryonic class II myosin heavy chains (MYHs) were cloned from the common carp (Cyprinus carpio L.), MYHemb1, MYHemb2 and MYHemb3. MYH DNA clones were also isolated from the slow muscle of adult carp acclimated to 10 degrees C (MYHS10) and 30 degrees C (MYHS30). Phylogenetic analysis demonstrated that MYHemb1 and MYHemb2 belonged to the fast skeletal muscle MYH clade. By contrast, the sequence of MYHemb3 was similar to the adult slow muscle isoforms, MYHS10 and MYHS30. MYHemb1 and MYHemb2 transcripts were first detected by northern blot analysis in embryos 61 h post-fertilization (h.p.f.) at the heartbeat stage, with peak expression occurring in 1-month-old juveniles. MYHemb1 continued to be expressed at low levels in 7-month-old juveniles when MYHemb2 was not detectable. MYHemb3 transcripts appeared at almost the same stage as MYHemb1 transcripts did (61 h.p.f.), and these genes showed a similar pattern of expression. Whole mount in situ hybridization analysis revealed that the transcripts of MYHemb1 and MYHemb2 were expressed in the inner part of myotome, whereas MYHemb3 was expressed in the superficial compartment. MYHS10 and MYHS30 mRNAs were first detected at hatching. In adult stages, the expression of slow muscle MYH mRNAs was dependent on acclimation temperature. MYHS10 mRNA was expressed at an acclimation temperature of 10 and 20 degrees C, but not at 30 degrees C. In contrast, MYHS30 mRNA was strongly expressed at all acclimation temperatures. The predominant MYH transcripts found in adult slow muscle and in embryos at hatching were expressed in adult fast muscle at some acclimation temperatures but not others. A MYH DNA clone was isolated from the cardiac muscle of 10 degrees C-acclimated adult fish (MYHcard). MYHcard mRNA was first detected at 61 h.p.f. but strong signals were only observed in the adult myocardium. The present study has therefore revealed a complex pattern of expression of MYH genes in relation to developmental stage, muscle type and acclimation temperature. None of the skeletal muscle MYHs identified so far was strongly expressed during the late juvenile stage, indicating further developmentally regulated members of the MYH II gene family remain to be discovered.
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Ono Y, Liang C, Ikeda D, Watabe S (2006). cDNA cloning of myosin heavy chain genes from medaka Oryzias latipes embryos and larvae and their expression patterns during development.
Dev Dyn,
235(11), 3092-3101.
Abstract:
cDNA cloning of myosin heavy chain genes from medaka Oryzias latipes embryos and larvae and their expression patterns during development.
Several sarcomeric myosin heavy chains (MYHs) were cloned from embryos and larvae of medaka Oryzias latipes. Three genes encoding medaka MYHs (mMYHs) predominantly expressed in embryos (mMYH(emb1)) and larvae (mMYH(L1) and mMYH(L2)), all belonged to fast skeletal MYHs, showing spatiotemporally different expression patterns during development. Besides these mMYHs, a few novel mMYHs were cloned from embryos and larvae at hatching. Whereas mMYH(emb2), mMYH(emb3), and mMYH(L3) belonged to fast skeletal MYH, mMYH(C1) and mMYH(C2) did to slow/cardiac MYH. mMYH(emb1) was expressed ahead of mMYH(L1) and mMYH(L2). In situ hybridization analysis demonstrated that the transcripts of mMYH(emb1) and mMYH(C1) were located in the horizontal myoseptum, whereas those of mMYH(L1) and mMYH(L2) in the inner part of myotomes and pharyngeal muscles, and those of mMYH(C2) in the heart rudiment. In silico cloning based on the medaka genome database showed another mMYHs of the slow/cardiac types, mMYH(C3) and mMYH(C4).
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