Myotome adaptability confers developmental robustness to somitic myogenesis in response to fibre number alteration
Balancing 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 th...
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Language: | English |
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ACADEMIC PRESS INC ELSEVIER SCIENCE
2017
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Online Access: | http://ir.ihb.ac.cn/handle/342005/30780 https://doi.org/10.1016/j.ydbio.2017.08.029 |
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ftchinacadsciihb:oai:ir.ihb.ac.cn:342005/30780 2023-05-15T15:33:03+02:00 Myotome adaptability confers developmental robustness to somitic myogenesis in response to fibre number alteration Roy, Shukolpa D. Williams, Victoria C. Pipalia, Tapan G. Li, Kuoyu Hammond, Christina L. Knappe, Stefanie Knight, Robert D. Hughes, Simon M. 2017-11-15 http://ir.ihb.ac.cn/handle/342005/30780 https://doi.org/10.1016/j.ydbio.2017.08.029 英语 eng ACADEMIC PRESS INC ELSEVIER SCIENCE DEVELOPMENTAL BIOLOGY http://ir.ihb.ac.cn/handle/342005/30780 doi:10.1016/j.ydbio.2017.08.029 Muscle Zebrafish Myosin Myod Myogenin Pax7 Developmental Biology ADULT SKELETAL-MUSCLE EMBRYONIC STEM-CELLS SATELLITE CELLS ZEBRAFISH EMBRYO BETA-CATENIN GSK-3-SPECIFIC INHIBITOR ATLANTIC SALMON UP-REGULATION DANIO-RERIO GROWTH 期刊论文 2017 ftchinacadsciihb https://doi.org/10.1016/j.ydbio.2017.08.029 2019-07-12T00:04:10Z Balancing 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. Report Atlantic salmon Institute of Hydrobiology, Chinese Academy of Sciences: IHB OpenIR Developmental Biology 431 2 321 335 |
institution |
Open Polar |
collection |
Institute of Hydrobiology, Chinese Academy of Sciences: IHB OpenIR |
op_collection_id |
ftchinacadsciihb |
language |
English |
topic |
Muscle Zebrafish Myosin Myod Myogenin Pax7 Developmental Biology ADULT SKELETAL-MUSCLE EMBRYONIC STEM-CELLS SATELLITE CELLS ZEBRAFISH EMBRYO BETA-CATENIN GSK-3-SPECIFIC INHIBITOR ATLANTIC SALMON UP-REGULATION DANIO-RERIO GROWTH |
spellingShingle |
Muscle Zebrafish Myosin Myod Myogenin Pax7 Developmental Biology ADULT SKELETAL-MUSCLE EMBRYONIC STEM-CELLS SATELLITE CELLS ZEBRAFISH EMBRYO BETA-CATENIN GSK-3-SPECIFIC INHIBITOR ATLANTIC SALMON UP-REGULATION DANIO-RERIO GROWTH Roy, Shukolpa D. Williams, Victoria C. Pipalia, Tapan G. Li, Kuoyu Hammond, Christina L. Knappe, Stefanie Knight, Robert D. Hughes, Simon M. Myotome adaptability confers developmental robustness to somitic myogenesis in response to fibre number alteration |
topic_facet |
Muscle Zebrafish Myosin Myod Myogenin Pax7 Developmental Biology ADULT SKELETAL-MUSCLE EMBRYONIC STEM-CELLS SATELLITE CELLS ZEBRAFISH EMBRYO BETA-CATENIN GSK-3-SPECIFIC INHIBITOR ATLANTIC SALMON UP-REGULATION DANIO-RERIO GROWTH |
description |
Balancing 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. |
format |
Report |
author |
Roy, Shukolpa D. Williams, Victoria C. Pipalia, Tapan G. Li, Kuoyu Hammond, Christina L. Knappe, Stefanie Knight, Robert D. Hughes, Simon M. |
author_facet |
Roy, Shukolpa D. Williams, Victoria C. Pipalia, Tapan G. Li, Kuoyu Hammond, Christina L. Knappe, Stefanie Knight, Robert D. Hughes, Simon M. |
author_sort |
Roy, Shukolpa D. |
title |
Myotome adaptability confers developmental robustness to somitic myogenesis in response to fibre number alteration |
title_short |
Myotome adaptability confers developmental robustness to somitic myogenesis in response to fibre number alteration |
title_full |
Myotome adaptability confers developmental robustness to somitic myogenesis in response to fibre number alteration |
title_fullStr |
Myotome adaptability confers developmental robustness to somitic myogenesis in response to fibre number alteration |
title_full_unstemmed |
Myotome adaptability confers developmental robustness to somitic myogenesis in response to fibre number alteration |
title_sort |
myotome adaptability confers developmental robustness to somitic myogenesis in response to fibre number alteration |
publisher |
ACADEMIC PRESS INC ELSEVIER SCIENCE |
publishDate |
2017 |
url |
http://ir.ihb.ac.cn/handle/342005/30780 https://doi.org/10.1016/j.ydbio.2017.08.029 |
genre |
Atlantic salmon |
genre_facet |
Atlantic salmon |
op_relation |
DEVELOPMENTAL BIOLOGY http://ir.ihb.ac.cn/handle/342005/30780 doi:10.1016/j.ydbio.2017.08.029 |
op_doi |
https://doi.org/10.1016/j.ydbio.2017.08.029 |
container_title |
Developmental Biology |
container_volume |
431 |
container_issue |
2 |
container_start_page |
321 |
op_container_end_page |
335 |
_version_ |
1766363528789229568 |