Defining the transcriptional redundancy of early bodywall muscle development in C. elegans: evidence for a unified theory of animal muscle development.
Myogenic regulatory factors (MRFs) are required for mammalian skeletal myogenesis. In contrast, bodywall muscle is readily detectable in Caenorhabditis elegans embryos lacking activity of the lone MRF ortholog HLH-1, indicating that additional myogenic factors must function in the nematode. We find that two additional C. elegans proteins, UNC-120/SRF and HND-1/HAND, can convert naïve blastomeres to muscle when overproduced ectopically in the embryo. In addition, we have used genetic null mutants to demonstrate that both of these factors act in concert with HLH-1 to regulate myogenesis. Loss of all three factors results in embryos that lack detectable bodywall muscle differentiation, identifying this trio as a set that is both necessary and sufficient for bodywall myogenesis in C. elegans. In mammals, SRF and HAND play prominent roles in regulating smooth and cardiac muscle development. That C. elegans bodywall muscle development is dependent on transcription factors that are associated with all three types of mammalian muscle supports a theory that all animal muscle types are derived from a common ancestral contractile cell type.
Fukushige
Tetsunari
T
Laboratory of Molecular Biology, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, Maryland 20892, USA.
Brodigan
Thomas M
TM
Schriefer
Lawrence A
LA
Waterston
Robert H
RH
Krause
Michael
M
D000818:Animals; D051792:Basic Helix-Loop-Helix Proteins / Q000235:genetics / Q000378:metabolism; D005075:Biological Evolution; D001757:Blastomeres / Q000166:cytology / Q000378:metabolism; D017173:Caenorhabditis elegans / Q000196:embryology* / Q000235:genetics; D029742:Caenorhabditis elegans Proteins / Q000235:genetics / Q000378:metabolism; D002454:Cell Differentiation; D018507:Gene Expression Regulation, Developmental; D026161:MADS Domain Proteins / Q000235:genetics / Q000378:metabolism; D032342:Muscle Cells / Q000166:cytology*; D024510:Muscle Development / Q000235:genetics*; D009124:Muscle Proteins; D009154:Mutation; D018006:Myogenic Regulatory Factors / Q000235:genetics / Q000378:metabolism; D009687:Nuclear Proteins; D014157:Transcription Factors
D051792:Basic Helix-Loop-Helix Proteins; D029742:Caenorhabditis elegans Proteins; D026161:MADS Domain Proteins; D009124:Muscle Proteins; D018006:Myogenic Regulatory Factors; D009687:Nuclear Proteins; D014157:Transcription Factors; C516539:HND-1 protein, C elegans; C516540:UNC-120 protein, C elegans; C066645:HLH-1 protein, C elegans