Involvement of HGF/MET signaling in appendicular muscle development in cartilaginous fish

Okamoto, Eri; Moriyama, Yuuta; Kuraku, Shigehiro; Kai, Kei-ichi; Tanaka, Mikiko

doi:10.1111/dgd.12591

Cited by 7 publications

(4 citation statements)

References 30 publications

(71 reference statements)

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“…Comparison of these groups suggests the following important developmental innovations: formation and expansion of PPFs across the liver to separate the thoracic and abdominal cavities, recruitment of muscle progenitors to the PPFs and their expansion and differentiation into the radial array of myofibers, and recruitment and targeting of motor neurons to the diaphragm muscle ( Hirasawa et al, 2016 ; Hirasawa and Kuratani, 2013 ; Sefton et al, 2018 ). HGF/MET signaling has important, conserved functions in the development of most vertebrate hypaxial muscles ( Adachi et al, 2018 ; Haines et al, 2004 ; Okamoto et al, 2019 ). Here we identify that Hgf expressed by the PPFs is crucial for recruitment and expansion of diaphragm muscle progenitors.…”

Section: Discussionmentioning

confidence: 99%

Fibroblast-derived Hgf controls recruitment and expansion of muscle during morphogenesis of the mammalian diaphragm

Sefton

Gallardo

Tobin

et al. 2022

eLife

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The diaphragm is a domed muscle between the thorax and abdomen essential for breathing in mammals. Diaphragm development requires the coordinated development of muscle, connective tissue, and nerve, which are derived from different embryonic sources. Defects in diaphragm development cause the common and often lethal birth defect, congenital diaphragmatic hernias (CDH). HGF/MET signaling is required for diaphragm muscularization, but the source of HGF and the specific functions of this pathway in muscle progenitors and effects on phrenic nerve have not been explicitly tested. Using conditional mutagenesis in mice and pharmacological inhibition of MET, we demonstrate that the pleuroperitoneal folds (PPFs), transient embryonic structures that give rise to the connective tissue in the diaphragm, are the source of HGF critical for diaphragm muscularization. PPF-derived HGF is directly required for recruitment of MET+ muscle progenitors to the diaphragm and indirectly (via its effect on muscle development) required for phrenic nerve primary branching. In addition, HGF is continuously required for maintenance and motility of the pool of progenitors to enable full muscularization. Localization of HGF at the diaphragm’s leading edges directs dorsal and ventral expansion of muscle and regulates its overall size and shape. Surprisingly, large muscleless regions in HGF and Met mutants do not lead to hernias. While these regions are likely more susceptible to CDH, muscle loss is not sufficient to cause CDH.

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Section: Discussionmentioning

confidence: 99%

Fibroblast-derived Hgf controls recruitment and expansion of muscle during morphogenesis of the mammalian diaphragm

Sefton

Gallardo

Tobin

et al. 2022

eLife

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“…The copyright holder for this preprint this version posted October 1, 2021. ; https://doi.org/10.1101/2021.09.29.462475 doi: bioRxiv preprint innovations: formation and expansion of PPFs across the liver to separate the thoracic and abdominal cavities, recruitment of muscle progenitors to the PPFs and their expansion and differentiation into the radial array of myofibers, and recruitment and targeting of motor neurons to the diaphragm muscle (Hirasawa et al, 2015;Hirasawa and Kuratani, 2013;Sefton et al, 2018). HGF/MET signaling has important, conserved functions in the development of most vertebrate hypaxial muscles (Adachi et al, 2018;Haines et al, 2004;Okamoto et al, 2019). Here we identify that HGF expressed by the PPFs is crucial for recruitment and expansion of diaphragm muscle progenitors.…”

Section: Discussionmentioning

confidence: 99%

Fibroblast-derived HGF integrates muscle and nerve development during morphogenesis of the mammalian diaphragm

Sefton

Gallardo

et al. 2021

Preprint

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The diaphragm is a domed muscle between the thorax and abdomen essential for breathing in mammals. Diaphragm development requires the coordinated development of muscle, connective tissue, and nerve, which are derived from different embryonic sources. Defects in diaphragm development cause the common and often lethal birth defect, Congenital Diaphragmatic Hernias (CDH). HGF/MET signaling is required for diaphragm muscularization, but the source of HGF and the specific functions of this pathway in muscle progenitors or potentially the phrenic nerve have not been explicitly tested. Using conditional mutagenesis and pharmacological inhibition of MET, we demonstrate that the pleuroperitoneal folds (PPFs), transient embryonic structures that give rise to the connective tissue, are the source of HGF critical for diaphragm muscularization and phrenic nerve primary branching. HGF not only is required for recruitment of muscle progenitors to the diaphragm, but is continuously required for maintenance and motility of the pool of progenitors to enable full muscularization. Thus, the connective tissue fibroblasts and HGF coordinately regulate diaphragm muscularization and innervation. Defects in PPF-derived HGF result in muscleless regions that are susceptible to CDH.

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“…This view has also been supported by nerve supply to the paired fins; each myotome extending into the fin bud receives motor neurons from the ventral roots of the neighboring spinal nerves ( Goodrich, 1930 ). However, recent progress of molecular analysis in chondrichthyan embryos provided important clues that their paired fin muscles would develop with a similar developmental mechanism to that in MMPs in amniote limbs, as detailed below ( Okamoto et al, 2019 ; Turner et al, 2019 ; Kusakabe et al, 2020 ).…”

Section: Skeletal Musculature Of Adult Lampreys and Sharkmentioning

confidence: 99%

Developmental Evolution of Hypaxial Muscles: Insights From Cyclostomes and Chondrichthyans

Kusakabe

Tanaka

Kuratani

2021

Front. Cell Dev. Biol.

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Jawed vertebrates possess two distinct groups of muscles in the trunk (epaxial and hypaxial muscles) primarily defined by the pattern of motor innervation from the spinal cord. Of these, the hypaxial group includes muscles with highly differentiated morphology and function, such as the muscles associated with paired limbs, shoulder girdles and tongue/infrahyoid (hypobranchial) muscles. Here we summarize the latest findings on the evolutionary mechanisms underlying the morphological variety of hypaxial musculature, with special reference to the molecular insights obtained from several living species that diverged early in vertebrate evolution. Lampreys, extant jawless vertebrates, lack many of derived traits characteristic of the gnathostomes, such as jaws, paired fins and epaxial/hypaxial distinction of the trunk skeletal musculatures. However, these animals possess the primitive form of the hypobranchial muscle. Of the gnathostomes, the elasmobranchs exhibit developmental mode of hypaxial muscles that is not identical to that of other gnathostomes in that the muscle primordia relocate as coherent cell aggregates. Comparison of expression of developmental genes, including Lbx genes, has delineated the temporal order of differentiation of various skeletal muscles, such as the hypobranchial, posterior pharyngeal and cucullaris (trapezius) muscles. We have proposed that the sequential addition of distal muscles, associated with expression of duplicated Lbx genes, promoted the elaboration of skeletal musculature. These analyses have revealed the framework of an evolutionary pathway that gave rise to the morphological complexity and diversity of vertebrate body patterns.

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Involvement of HGF/MET signaling in appendicular muscle development in cartilaginous fish

Cited by 7 publications

References 30 publications

Fibroblast-derived Hgf controls recruitment and expansion of muscle during morphogenesis of the mammalian diaphragm

Fibroblast-derived Hgf controls recruitment and expansion of muscle during morphogenesis of the mammalian diaphragm

Fibroblast-derived HGF integrates muscle and nerve development during morphogenesis of the mammalian diaphragm

Developmental Evolution of Hypaxial Muscles: Insights From Cyclostomes and Chondrichthyans

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