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Myotome adaptability confers developmental robustness to somitic myogenesis in response to fibre number alteration
Roy, Shukolpa D.1; Williams, Victoria C.1; Pipalia, Tapan G.1; Li, Kuoyu1,3; Hammond, Christina L.1,4; Knappe, Stefanie2; Knight, Robert D.2; Hughes, Simon M.1
Corresponding AuthorHughes, Simon M.(simon.hughes@kcl.ac.uk)
2017-11-15
Source PublicationDEVELOPMENTAL BIOLOGY
ISSN0012-1606
Volume431Issue:2Pages:321-335
AbstractBalancing the number of stem cells and their progeny is crucial for tissue development and repair. Here we examine how cell numbers and overall muscle size are tightly regulated during zebrafish somitic muscle development. Muscle stem/precursor cell (MPCs) expressing Pax7 are initially located in the dermomyotome (DM) external cell layer, adopt a highly stereotypical distribution and thereafter a proportion of MPCs migrate into the myotome. Regional variations in the proliferation and terminal differentiation of MPCs contribute to growth of the myotome. To probe the robustness of muscle size control and spatiotemporal regulation of MPCs, we compared the behaviour of wild type (wt) MPCs with those in mutant zebrafish that lack the muscle regulatory factor Myod. Myod(fh261) mutants form one third fewer multinucleate fast muscle fibres than wt and show a significant expansion of the Pax(7+) MPC population in the DM. Subsequently, myod(fh261) mutant fibres generate more cytoplasm per nucleus, leading to recovery of muscle bulk. In addition, relative to wt siblings, there is an increased number of MPCs in myod(fh261) mutants and these migrate prematurely into the myotome, differentiate and contribute to the hypertrophy of existing fibres. Thus, homeostatic reduction of the excess MPCs returns their number to normal levels, but fibre numbers remain low. The GSK3 antagonist BIO prevents MPC migration into the deep myotome, suggesting that canonical Wnt pathway activation maintains the DM in zebrafish, as in amniotes. BIO does not, however, block recovery of the myod(fh261) mutant myotome, indicating that homeostasis acts on fibre intrinsic growth to maintain muscle bulk. The findings suggest the existence of a critical window for early fast fibre formation followed by a period in which homeostatic mechanisms regulate myotome growth by controlling fibre size. The feedback controls we reveal in muscle help explain the extremely precise grading of myotome size along the body axis irrespective of fish size, nutrition and genetic variation and may form a paradigm for wider matching of organ size.
KeywordMuscle Zebrafish Myosin Myod Myogenin Pax7
DOI10.1016/j.ydbio.2017.08.029
Funding OrganizationMedical Research Council (MRC) Scientist with MRC Programme Grant ; Medical Research Council (MRC) Scientist with MRC Programme Grant ; Medical Research Council (MRC) Scientist with MRC Programme Grant ; Medical Research Council (MRC) Scientist with MRC Programme Grant ; Biotechnology and Biological Sciences Research Council (BBSRC) ; Biotechnology and Biological Sciences Research Council (BBSRC) ; Biotechnology and Biological Sciences Research Council (BBSRC) ; Biotechnology and Biological Sciences Research Council (BBSRC) ; BBSRC ; BBSRC ; BBSRC ; BBSRC ; Wellcome Trust ; Wellcome Trust ; Wellcome Trust ; Wellcome Trust ; MRC PhD studentship ; MRC PhD studentship ; MRC PhD studentship ; MRC PhD studentship ; Medical Research Council (MRC) Scientist with MRC Programme Grant ; Medical Research Council (MRC) Scientist with MRC Programme Grant ; Medical Research Council (MRC) Scientist with MRC Programme Grant ; Medical Research Council (MRC) Scientist with MRC Programme Grant ; Biotechnology and Biological Sciences Research Council (BBSRC) ; Biotechnology and Biological Sciences Research Council (BBSRC) ; Biotechnology and Biological Sciences Research Council (BBSRC) ; Biotechnology and Biological Sciences Research Council (BBSRC) ; BBSRC ; BBSRC ; BBSRC ; BBSRC ; Wellcome Trust ; Wellcome Trust ; Wellcome Trust ; Wellcome Trust ; MRC PhD studentship ; MRC PhD studentship ; MRC PhD studentship ; MRC PhD studentship ; Medical Research Council (MRC) Scientist with MRC Programme Grant ; Medical Research Council (MRC) Scientist with MRC Programme Grant ; Medical Research Council (MRC) Scientist with MRC Programme Grant ; Medical Research Council (MRC) Scientist with MRC Programme Grant ; Biotechnology and Biological Sciences Research Council (BBSRC) ; Biotechnology and Biological Sciences Research Council (BBSRC) ; Biotechnology and Biological Sciences Research Council (BBSRC) ; Biotechnology and Biological Sciences Research Council (BBSRC) ; BBSRC ; BBSRC ; BBSRC ; BBSRC ; Wellcome Trust ; Wellcome Trust ; Wellcome Trust ; Wellcome Trust ; MRC PhD studentship ; MRC PhD studentship ; MRC PhD studentship ; MRC PhD studentship ; Medical Research Council (MRC) Scientist with MRC Programme Grant ; Medical Research Council (MRC) Scientist with MRC Programme Grant ; Medical Research Council (MRC) Scientist with MRC Programme Grant ; Medical Research Council (MRC) Scientist with MRC Programme Grant ; Biotechnology and Biological Sciences Research Council (BBSRC) ; Biotechnology and Biological Sciences Research Council (BBSRC) ; Biotechnology and Biological Sciences Research Council (BBSRC) ; Biotechnology and Biological Sciences Research Council (BBSRC) ; BBSRC ; BBSRC ; BBSRC ; BBSRC ; Wellcome Trust ; Wellcome Trust ; Wellcome Trust ; Wellcome Trust ; MRC PhD studentship ; MRC PhD studentship ; MRC PhD studentship ; MRC PhD studentship
Indexed BySCI ; SCI
Language英语
Funding ProjectMedical Research Council (MRC) Scientist with MRC Programme Grant[G1001029] ; Medical Research Council (MRC) Scientist with MRC Programme Grant[MR/N021231/1] ; Biotechnology and Biological Sciences Research Council (BBSRC)[BB/K010115/1] ; BBSRC[BB/I025883/1] ; Wellcome Trust[101529/Z/13/Z] ; MRC PhD studentship
WOS Research AreaDevelopmental Biology
WOS SubjectDevelopmental Biology
WOS IDWOS:000414622200020
WOS KeywordADULT SKELETAL-MUSCLE ; EMBRYONIC STEM-CELLS ; SATELLITE CELLS ; ZEBRAFISH EMBRYO ; BETA-CATENIN ; GSK-3-SPECIFIC INHIBITOR ; ATLANTIC SALMON ; UP-REGULATION ; DANIO-RERIO ; GROWTH
PublisherACADEMIC PRESS INC ELSEVIER SCIENCE
Funding OrganizationMedical Research Council (MRC) Scientist with MRC Programme Grant ; Medical Research Council (MRC) Scientist with MRC Programme Grant ; Medical Research Council (MRC) Scientist with MRC Programme Grant ; Medical Research Council (MRC) Scientist with MRC Programme Grant ; Biotechnology and Biological Sciences Research Council (BBSRC) ; Biotechnology and Biological Sciences Research Council (BBSRC) ; Biotechnology and Biological Sciences Research Council (BBSRC) ; Biotechnology and Biological Sciences Research Council (BBSRC) ; BBSRC ; BBSRC ; BBSRC ; BBSRC ; Wellcome Trust ; Wellcome Trust ; Wellcome Trust ; Wellcome Trust ; MRC PhD studentship ; MRC PhD studentship ; MRC PhD studentship ; MRC PhD studentship ; Medical Research Council (MRC) Scientist with MRC Programme Grant ; Medical Research Council (MRC) Scientist with MRC Programme Grant ; Medical Research Council (MRC) Scientist with MRC Programme Grant ; Medical Research Council (MRC) Scientist with MRC Programme Grant ; Biotechnology and Biological Sciences Research Council (BBSRC) ; Biotechnology and Biological Sciences Research Council (BBSRC) ; Biotechnology and Biological Sciences Research Council (BBSRC) ; Biotechnology and Biological Sciences Research Council (BBSRC) ; BBSRC ; BBSRC ; BBSRC ; BBSRC ; Wellcome Trust ; Wellcome Trust ; Wellcome Trust ; Wellcome Trust ; MRC PhD studentship ; MRC PhD studentship ; MRC PhD studentship ; MRC PhD studentship ; Medical Research Council (MRC) Scientist with MRC Programme Grant ; Medical Research Council (MRC) Scientist with MRC Programme Grant ; Medical Research Council (MRC) Scientist with MRC Programme Grant ; Medical Research Council (MRC) Scientist with MRC Programme Grant ; Biotechnology and Biological Sciences Research Council (BBSRC) ; Biotechnology and Biological Sciences Research Council (BBSRC) ; Biotechnology and Biological Sciences Research Council (BBSRC) ; Biotechnology and Biological Sciences Research Council (BBSRC) ; BBSRC ; BBSRC ; BBSRC ; BBSRC ; Wellcome Trust ; Wellcome Trust ; Wellcome Trust ; Wellcome Trust ; MRC PhD studentship ; MRC PhD studentship ; MRC PhD studentship ; MRC PhD studentship ; Medical Research Council (MRC) Scientist with MRC Programme Grant ; Medical Research Council (MRC) Scientist with MRC Programme Grant ; Medical Research Council (MRC) Scientist with MRC Programme Grant ; Medical Research Council (MRC) Scientist with MRC Programme Grant ; Biotechnology and Biological Sciences Research Council (BBSRC) ; Biotechnology and Biological Sciences Research Council (BBSRC) ; Biotechnology and Biological Sciences Research Council (BBSRC) ; Biotechnology and Biological Sciences Research Council (BBSRC) ; BBSRC ; BBSRC ; BBSRC ; BBSRC ; Wellcome Trust ; Wellcome Trust ; Wellcome Trust ; Wellcome Trust ; MRC PhD studentship ; MRC PhD studentship ; MRC PhD studentship ; MRC PhD studentship
Citation statistics
Cited Times:3[WOS]   [WOS Record]     [Related Records in WOS]
Document Type期刊论文
Identifierhttp://ir.ihb.ac.cn/handle/342005/30782
Collection其他_期刊论文
Corresponding AuthorHughes, Simon M.
Affiliation1.Kings Coll London, Randall Div Cell & Mol Biophys, New Hunts House,Guys Campus, London SE1 1UL, England
2.Kings Coll London, Guys Hosp, Div Craniofacial Dev & Stem Cell Biol, London, England
3.Chinese Acad Sci, Inst Hydrobiol, China Zebrafish Resource Ctr, Wuhan, Hubei, Peoples R China
4.Univ Bristol, Dept Physiol & Pharmacol, Bristol BS8 1TD, Avon, England
Recommended Citation
GB/T 7714
Roy, Shukolpa D.,Williams, Victoria C.,Pipalia, Tapan G.,et al. Myotome adaptability confers developmental robustness to somitic myogenesis in response to fibre number alteration[J]. DEVELOPMENTAL BIOLOGY,2017,431(2):321-335.
APA Roy, Shukolpa D..,Williams, Victoria C..,Pipalia, Tapan G..,Li, Kuoyu.,Hammond, Christina L..,...&Hughes, Simon M..(2017).Myotome adaptability confers developmental robustness to somitic myogenesis in response to fibre number alteration.DEVELOPMENTAL BIOLOGY,431(2),321-335.
MLA Roy, Shukolpa D.,et al."Myotome adaptability confers developmental robustness to somitic myogenesis in response to fibre number alteration".DEVELOPMENTAL BIOLOGY 431.2(2017):321-335.
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