Pbx homeodomain proteins direct Myod activity to promote fast-muscle differentiation

Maves, Lisa; Waskiewicz, Andrew J.; Paul, Biswajit; Cao, Yi; Tyler, Ashlee E.; Moens, Cecilia B.; Tapscott, Stephen J.

doi:10.1242/dev.003905

Cited by 126 publications

(173 citation statements)

References 56 publications

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“…Quantitative RT-PCR was performed as previously described (Xiong et al, 2006). Specific pairs of primers were referred to followings: 5'-AGACTGCTGTAAGGAGTGTCCTC-3' (chd forward), 5'-CCATGAAGTCCTCTATGCATTCCG-3' (chd reverse), 5'-CAGAGCTCACTTAGGGAAAGGCTC-3' (bmp2 forward), 5'-CCAATAGTCTAGTGATGGGCTCCTG-3' (bmp2 reverse), 5'-CCGGTCTGCTCAGTCCAGACC-3' (gata1 forward), 5'-GGAAAGGGCTACTGGACCAGAC-3' (gata1 reverse), 5'-GGA-CAGCCTCCTCCCTAAGGC-3' (ctn forward), 5'-CAGTTCTAGCT-GGTTGATGCGG-3' (ctn reverse), 5'-ATGGATGATGAAATTGCCG-CAC-3' (β-actin forward), 5'-ACCATCACCAGAGTCCATCACG-3' (β-actin reverse), 5'-TCAGACGAGAAGACGGAACA-3' (myod forward), 5'-CACGATGCTGGACAGACAAT-3' (myod reverse), 5'-GGGAC-CATTGTGGTCGACAG-3' (shha forward), 5'-GCTTGAGTTTACT-GACATCCC-3' (shha reverse), 5'-CCCGCGCGGAGCCGCC-GCTGC-3' (sox9b forward) and 5'-GCAGGTGCGGGTACTGG-TCCGC-3' (sox9b reverse) (Maves et al, 2007;Warga et al, 2009). …”

Section: Morpholinos Design and Microinjectionmentioning

confidence: 99%

Nusap1 is essential for neural crest cell migration in zebrafish

Nie

Wang

et al. 2010

Protein Cell

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Microtubules play important roles in mitotic spindle assembly and chromosome segregation to maintain normal cell cycle progression. A number of microtubule-associated proteins have been identified in epithelial and neural cell cultures; however, their physiological significance is not well characterized due to the lack of appropriate in vivo animal models. Nucleolar spindleassociated protein (NuSAP) is a microtubule-binding protein and is reported to be involved in mitosis by cell culture studies. In this report, we identified the zebrafish homologue of human NuSAP and investigated its expression profile and functions. Using in situ hybridization, we demonstrated that transcripts of zebrafish nusap1 are specifically expressed in the retina, forebrain, hindbrain and neural crest. When the in vivo expression of nusap1 was knocked down through antisense oligonucleotide morpholino technology, the morphants of nusap1 showed impaired morphogenesis in the trunk and yolk extension, implying the involvement of Nusap1 in cell migration. Mechanistic studies revealed that nusap1 morphants have an altered expression pattern of neural crest markers crestin and sox9b, but normal expression of blood vessel and notochord markers gata1 and shh. In addition, nusap1 mRNA injection caused serious apoptosis in retina and hindbrain tissue, and these phenotypes can be rescued by co-injection of morpholino against nusap1. These observations not only suggest a role for Nusap1 in connecting apoptosis with cell migration, but also provide strong evidences that Nusap1 is potentially involved in morphogenesis in vertebrates.

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Section: Morpholinos Design and Microinjectionmentioning

confidence: 99%

Nusap1 is essential for neural crest cell migration in zebrafish

Nie

Wang

et al. 2010

Protein Cell

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“…Furthermore, Myod, Myogenin, and Mrf4 participate to the activation of skeletal muscle gene expression during myogenic differentiation. Analysis of MRF role by loss of function experiments has also been studied in zebrafish, an anamniote species, in which Myod and Myf5 act as determination factors (Maves et al, 2007;Hinits et al, 2009).…”

Section: Introductionmentioning

confidence: 99%

Myogenic waves and myogenic programs during Xenopus embryonic myogenesis

Gaspera

Armand

Sequeira

et al. 2012

Developmental Dynamics

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Background: Although Xenopus is a key model organism in developmental biology, little is known about the myotome formation in this species. Here, we assessed the expression of myogenic regulatory factors of the Myod family (MRFs) during embryonic development and revealed distinct MRF programs. Results: The expression pattern of each MRF during embryonic development highlights three successive myogenic waves. We showed that a first median and lateral myogenesis initiates before dermomyotome formation: the median cell population expresses Myf5, Myod, and Mrf4, whereas the lateral one expresses Myod, moderate levels of Myogenin and Mrf4. The second wave of myoblasts arising from the dermomyotome is characterized by the full MRF program expression, with high levels of Myogenin. The third wave is revealed by Myf5 expression in the myotome and could contribute to the formation of plurinucleated fibers at larval stages. Furthermore, Myf5-or Myod-expressing anlagen are identified in craniofacial myogenesis. Conclusions: The first median and lateral myogenesis and their associated MRF programs have probably disappeared in mammals. However, some aspects of Xenopus myogenesis have been conserved such as the development of somitic muscles by successive myogenic waves and the existence of Myf5-dependent andindependent lineages. Developmental Dynamics 241:995-1007,

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“…Expression of the thin filament genes α-actin and α-tropomyosin (tpma) was not affected [ Fig. 1; as for desmin (Maves et al, 2007)]. Myf5 knockdown did not affect any of the markers examined (Fig.…”

mentioning

confidence: 99%

Differential requirements for myogenic regulatory factors distinguish medial and lateral somitic, cranial and fin muscle fibre populations

2009

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Myogenic regulatory factors of the Myod family (MRFs) are transcription factors essential for mammalian skeletal myogenesis. However, the roles of each gene in myogenesis remain unclear, owing partly to genetic linkage at the Myf5/Mrf4 locus and to rapid morphogenetic movements in the amniote somite. In mice, Myf5 is essential for the earliest epaxial myogenesis, whereas Myod is required for timely differentiation of hypaxially derived muscle. A second major subdivision of the somite is between primaxial muscle of the somite proper and abaxial somite-derived migratory muscle precursors. Here, we use a combination of mutant and morphant analysis to ablate the function of each of the four conserved MRF genes in zebrafish, an organism that has retained a more ancestral bodyplan. We show that a fundamental distinction in somite myogenesis is into medial versus lateral compartments, which correspond to neither epaxial/hypaxial nor primaxial/abaxial subdivisions. In the medial compartment, Myf5 and/or Myod drive adaxial slow fibre and medial fast fibre differentiation. Myod-driven Myogenin activity alone is sufficient for lateral fast somitic and pectoral fin fibre formation from the lateral compartment, as well as for cranial myogenesis. Myogenin activity is a significant contributor to fast fibre differentiation. Mrf4 does not contribute to early myogenesis in zebrafish. We suggest that the differential use of duplicated MRF paralogues in this novel two-component myogenic system facilitated the diversification of vertebrates.KEY WORDS: Muscle, Zebrafish, Myosin, Slow, Fibre, Fast, Head, Fin, mrf4 (myf6), myod, myf5, Myogenin, Hedgehog, prdm1, pax3, meox1, hsp90, mef2d Development 136, 403-414 (2009) Here, we turn to zebrafish in the hope of finding shared and divergent roles for individual MRFs in myogenesis. Each zebrafish somite generates at least four populations of muscle fibres within the first 15 hours of somitogenesis, a timing and diversity that are akin to amniote somite myogenesis (Kahane et al., 2001;Kassar-Duchossoy et al., 2004). Two Hedgehog (Hh)-dependent medial mononucleate slow muscle fibre types derive from the myf5-and myod-expressing adaxial cells lying adjacent to the notochord (Blagden et al., 1997;Coutelle et al., 2001;Weinberg et al., 1996;Wolff et al., 2003). Approximately three muscle pioneer fibres remain at the dorsoventral midline, whereas 20 superficial slow fibres migrate to the lateral myotome surface (Devoto et al., 1996). More lateral paraxial cells within the somite also express the MRFs myf5 and myod (Coutelle et al., 2001;Weinberg et al., 1996) and give rise to two kinds of multinucleate fast fibre: the Fgf8-dependent lateral fast fibres and the Fgf8-independent medial fast fibres, a subset of which becomes the fast Engrailed-expressing cells as a result of later Hh signalling (Groves et al., 2005;Wolff et al., 2003). Both slow and fast lineage cells also express myog and mrf4 Weinberg et al., 1996). Using predicted null mutations in myf5 and mrf4 and morpholino antisense oligo...

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Pbx homeodomain proteins direct Myod activity to promote fast-muscle differentiation

Cited by 126 publications

References 56 publications

Nusap1 is essential for neural crest cell migration in zebrafish

Nusap1 is essential for neural crest cell migration in zebrafish

Myogenic waves and myogenic programs during Xenopus embryonic myogenesis

Differential requirements for myogenic regulatory factors distinguish medial and lateral somitic, cranial and fin muscle fibre populations

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