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Article ; Online: Connecting muscle development, birth defects, and evolution: An essential role for muscle connective tissue.

Sefton, Elizabeth M / Kardon, Gabrielle

2019 Volume 132, Page(s) 137–176

Abstract: Skeletal muscle powers all movement of the vertebrate body and is distributed in multiple regions that have evolved distinct functions. Axial muscles are ancestral muscles essential for support and locomotion of the whole body. The evolution of the head ... ...

Abstract	Skeletal muscle powers all movement of the vertebrate body and is distributed in multiple regions that have evolved distinct functions. Axial muscles are ancestral muscles essential for support and locomotion of the whole body. The evolution of the head was accompanied by development of cranial muscles essential for eye movement, feeding, vocalization, and facial expression. With the evolution of paired fins and limbs and their associated muscles, vertebrates gained increased locomotor agility, populated the land, and acquired fine motor skills. Finally, unique muscles with specialized functions have evolved in some groups, and the diaphragm which solely evolved in mammals to increase respiratory capacity is one such example. The function of all these muscles requires their integration with the other components of the musculoskeletal system: muscle connective tissue (MCT), tendons, bones as well as nerves and vasculature. MCT is muscle's closest anatomical and functional partner. Not only is MCT critical in the adult for muscle structure and function, but recently MCT in the embryo has been found to be crucial for muscle development. In this review, we examine the important role of the MCT in axial, head, limb, and diaphragm muscles for regulating normal muscle development, discuss how defects in MCT-muscle interactions during development underlie the etiology of a range of birth defects, and explore how changes in MCT development or communication with muscle may have led to the modification and acquisition of new muscles during vertebrate evolution.
MeSH term(s)	Animals ; Body Patterning/genetics ; Connective Tissue/embryology ; Connective Tissue/metabolism ; Evolution, Molecular ; Gene Expression Regulation, Developmental ; Humans ; Mammals/embryology ; Mammals/metabolism ; Muscle Development/genetics ; Muscle, Skeletal/embryology ; Muscle, Skeletal/metabolism ; Vertebrates/embryology ; Vertebrates/genetics
Language	English
Publishing date	2019-01-03
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Review
ISSN	1557-8933 ; 0070-2153
ISSN (online)	1557-8933
ISSN	0070-2153
DOI	10.1016/bs.ctdb.2018.12.004
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Cell culture system to assay candidate genes and molecular pathways implicated in congenital diaphragmatic hernias.

Bogenschutz, Eric L / Sefton, Elizabeth M / Kardon, Gabrielle

Developmental biology

2020 Volume 467, Issue 1-2, Page(s) 30–38

Abstract: The mammalian muscularized diaphragm is essential for respiration and defects in the developing diaphragm cause a common and frequently lethal birth defect, congenital diaphragmatic hernia (CDH). Human genetic studies have implicated more than 150 genes ... ...

Abstract	The mammalian muscularized diaphragm is essential for respiration and defects in the developing diaphragm cause a common and frequently lethal birth defect, congenital diaphragmatic hernia (CDH). Human genetic studies have implicated more than 150 genes and multiple molecular pathways in CDH, but few of these have been validated because of the expense and time to generate mouse mutants. The pleuroperitoneal folds (PPFs) are transient embryonic structures in diaphragm development and defects in PPFs lead to CDH. We have developed a system to culture PPF fibroblasts from E12.5 mouse embryos and show that these fibroblasts, in contrast to the commonly used NIH 3T3 fibroblasts, maintain expression of key genes in normal diaphragm development. Using pharmacological and genetic manipulations that result in CDH in vivo, we also demonstrate that differences in proliferation provide a rapid means of distinguishing healthy and impaired PPF fibroblasts. Thus, the PPF fibroblast cell culture system is an efficient tool for assaying the functional significance of CDH candidate genes and molecular pathways and will be an important resource for elucidating the complex etiology of CDH.
MeSH term(s)	Animals ; Cell Culture Techniques ; Diaphragm/embryology ; Female ; Gene Expression Regulation, Developmental ; Hernias, Diaphragmatic, Congenital/embryology ; Humans ; Male ; Mice ; NIH 3T3 Cells
Language	English
Publishing date	2020-08-19
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	1114-9
ISSN	1095-564X ; 0012-1606
ISSN (online)	1095-564X
ISSN	0012-1606
DOI	10.1016/j.ydbio.2020.07.013
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Article: Cell culture system to assay candidate genes and molecular pathways implicated in congenital diaphragmatic hernias

Bogenschutz, Eric L / Sefton, Elizabeth M / Kardon, Gabrielle

Developmental biology. 2020 Nov. 01, v. 467, no. 1-2

2020

Abstract	The mammalian muscularized diaphragm is essential for respiration and defects in the developing diaphragm cause a common and frequently lethal birth defect, congenital diaphragmatic hernia (CDH). Human genetic studies have implicated more than 150 genes and multiple molecular pathways in CDH, but few of these have been validated because of the expense and time to generate mouse mutants. The pleuroperitoneal folds (PPFs) are transient embryonic structures in diaphragm development and defects in PPFs lead to CDH. We have developed a system to culture PPF fibroblasts from E12.5 mouse embryos and show that these fibroblasts, in contrast to the commonly used NIH 3T3 fibroblasts, maintain expression of key genes in normal diaphragm development. Using pharmacological and genetic manipulations that result in CDH in vivo, we also demonstrate that differences in proliferation provide a rapid means of distinguishing healthy and impaired PPF fibroblasts. Thus, the PPF fibroblast cell culture system is an efficient tool for assaying the functional significance of CDH candidate genes and molecular pathways and will be an important resource for elucidating the complex etiology of CDH.
Keywords	cell culture ; congenital abnormalities ; diaphragm ; etiology ; fibroblasts ; hernia ; humans ; mice
Language	English
Dates of publication	2020-1101
Size	p. 30-38.
Publishing place	Elsevier Inc.
Document type	Article
Note	NAL-AP-2-clean
ZDB-ID	1114-9
ISSN	1095-564X ; 0012-1606
ISSN (online)	1095-564X
ISSN	0012-1606
DOI	10.1016/j.ydbio.2020.07.013
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Article ; Online: Developmental origin and morphogenesis of the diaphragm, an essential mammalian muscle.

Sefton, Elizabeth M / Gallardo, Mirialys / Kardon, Gabrielle

Developmental biology

2018 Volume 440, Issue 2, Page(s) 64–73

Abstract: The diaphragm is a mammalian skeletal muscle essential for respiration and for separating the thoracic and abdominal cavities. Development of the diaphragm requires the coordinated development of muscle, muscle connective tissue, tendon, nerves, and ... ...

Abstract	The diaphragm is a mammalian skeletal muscle essential for respiration and for separating the thoracic and abdominal cavities. Development of the diaphragm requires the coordinated development of muscle, muscle connective tissue, tendon, nerves, and vasculature that derive from different embryonic sources. However, defects in diaphragm development are common and the cause of an often deadly birth defect, Congenital Diaphragmatic Hernia (CDH). Here we comprehensively describe the normal developmental origin and complex spatial-temporal relationship between the different developing tissues to form a functional diaphragm using a developmental series of mouse embryos genetically and immunofluorescently labeled and analyzed in whole mount. We find that the earliest developmental events are the emigration of muscle progenitors from cervical somites followed by the projection of phrenic nerve axons from the cervical neural tube. Muscle progenitors and phrenic nerve target the pleuroperitoneal folds (PPFs), transient pyramidal-shaped structures that form between the thoracic and abdominal cavities. Subsequently, the PPFs expand across the surface of the liver to give rise to the muscle connective tissue and central tendon, and the leading edge of their expansion precedes muscle morphogenesis, formation of the vascular network, and outgrowth and branching of the phrenic nerve. Thus development and morphogenesis of the PPFs is critical for diaphragm formation. In addition, our data indicate that the earliest events in diaphragm development are critical for the etiology of CDH and instrumental to the evolution of the diaphragm. CDH initiates prior to E12.5 in mouse and suggests that defects in the early PPF formation or their ability to recruit muscle are an important source of CDH. Also, the recruitment of muscle progenitors from cervical somites to the nascent PPFs is uniquely mammalian and a key developmental innovation essential for the evolution of the muscularized diaphragm.
MeSH term(s)	Animals ; Connective Tissue/embryology ; Connective Tissue/physiology ; Diaphragm/embryology ; Diaphragm/physiology ; Disease Models, Animal ; Gene Expression Regulation, Developmental/genetics ; Genes, Developmental/genetics ; Mammals ; Mice ; Mice, Inbred C57BL ; Morphogenesis ; Muscle Development/physiology ; Muscle, Skeletal/embryology ; Muscle, Skeletal/growth & development ; Muscle, Skeletal/physiology
Language	English
Publishing date	2018-04-19
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	1114-9
ISSN	1095-564X ; 0012-1606
ISSN (online)	1095-564X
ISSN	0012-1606
DOI	10.1016/j.ydbio.2018.04.010
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Article ; Online: Fibroblast-derived

Sefton, Elizabeth M / Gallardo, Mirialys / Tobin, Claire E / Collins, Brittany C / Colasanto, Mary P / Merrell, Allyson J / Kardon, Gabrielle

eLife

2022 Volume 11

Abstract: 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. ... ...

Abstract	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
MeSH term(s)	Animals ; Diaphragm ; Disease Models, Animal ; Fibroblasts/metabolism ; Hernias, Diaphragmatic, Congenital/genetics ; Mammals ; Mice ; Morphogenesis ; Phenyl Ethers/metabolism ; Thorax/metabolism
Chemical Substances	Phenyl Ethers
Language	English
Publishing date	2022-09-26
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2687154-3
ISSN	2050-084X ; 2050-084X
ISSN (online)	2050-084X
ISSN	2050-084X
DOI	10.7554/eLife.74592
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Article: Developmental origin and morphogenesis of the diaphragm, an essential mammalian muscle

Sefton, Elizabeth M / Gallardo, Mirialys / Kardon, Gabrielle

Developmental biology. 2018 Aug. 15, v. 440

2018

Abstract	The diaphragm is a mammalian skeletal muscle essential for respiration and for separating the thoracic and abdominal cavities. Development of the diaphragm requires the coordinated development of muscle, muscle connective tissue, tendon, nerves, and vasculature that derive from different embryonic sources. However, defects in diaphragm development are common and the cause of an often deadly birth defect, Congenital Diaphragmatic Hernia (CDH). Here we comprehensively describe the normal developmental origin and complex spatial-temporal relationship between the different developing tissues to form a functional diaphragm using a developmental series of mouse embryos genetically and immunofluorescently labeled and analyzed in whole mount. We find that the earliest developmental events are the emigration of muscle progenitors from cervical somites followed by the projection of phrenic nerve axons from the cervical neural tube. Muscle progenitors and phrenic nerve target the pleuroperitoneal folds (PPFs), transient pyramidal-shaped structures that form between the thoracic and abdominal cavities. Subsequently, the PPFs expand across the surface of the liver to give rise to the muscle connective tissue and central tendon, and the leading edge of their expansion precedes muscle morphogenesis, formation of the vascular network, and outgrowth and branching of the phrenic nerve. Thus development and morphogenesis of the PPFs is critical for diaphragm formation. In addition, our data indicate that the earliest events in diaphragm development are critical for the etiology of CDH and instrumental to the evolution of the diaphragm. CDH initiates prior to E12.5 in mouse and suggests that defects in the early PPF formation or their ability to recruit muscle are an important source of CDH. Also, the recruitment of muscle progenitors from cervical somites to the nascent PPFs is uniquely mammalian and a key developmental innovation essential for the evolution of the muscularized diaphragm.
Keywords	axons ; congenital abnormalities ; diaphragm ; embryo (animal) ; etiology ; evolution ; hernia ; liver ; mice ; morphogenesis ; nerve tissue ; skeletal muscle
Language	English
Dates of publication	2018-0815
Size	p. 64-73.
Publishing place	Elsevier Inc.
Document type	Article
ZDB-ID	1114-9
ISSN	1095-564X ; 0012-1606
ISSN (online)	1095-564X
ISSN	0012-1606
DOI	10.1016/j.ydbio.2018.04.010
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Article ; Online: Reconstructing human brown fat developmental trajectory in vitro.

Rao, Jyoti / Djeffal, Yannis / Chal, Jerome / Marchianò, Fabio / Wang, Chih-Hao / Al Tanoury, Ziad / Gapon, Svetlana / Mayeuf-Louchart, Alicia / Glass, Ian / Sefton, Elizabeth M / Habermann, Bianca / Kardon, Gabrielle / Watt, Fiona M / Tseng, Yu-Hua / Pourquié, Olivier

Developmental cell

2023 Volume 58, Issue 21, Page(s) 2359–2375.e8

Abstract: Brown adipocytes (BAs) represent a specialized cell type that is able to uncouple nutrient catabolism from ATP generation to dissipate energy as heat. In humans, the brown fat tissue is composed of discrete depots found throughout the neck and trunk ... ...

Abstract	Brown adipocytes (BAs) represent a specialized cell type that is able to uncouple nutrient catabolism from ATP generation to dissipate energy as heat. In humans, the brown fat tissue is composed of discrete depots found throughout the neck and trunk region. BAs originate from a precursor common to skeletal muscle, but their developmental trajectory remains poorly understood. Here, we used single-cell RNA sequencing to characterize the development of interscapular brown fat in mice. Our analysis identified a transient stage of BA differentiation characterized by the expression of the transcription factor GATA6. We show that recapitulating the sequence of signaling cues identified in mice can lead to efficient differentiation of BAs in vitro from human pluripotent stem cells. These precursors can in turn be efficiently converted into functional BAs that can respond to signals mimicking adrenergic stimuli by increasing their metabolism, resulting in heat production.
MeSH term(s)	Humans ; Animals ; Mice ; Adipose Tissue, Brown/metabolism ; Cell Differentiation/physiology ; Pluripotent Stem Cells ; Signal Transduction ; Adipocytes, Brown/metabolism ; Thermogenesis/physiology
Language	English
Publishing date	2023-08-29
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	2054967-2
ISSN	1878-1551 ; 1534-5807
ISSN (online)	1878-1551
ISSN	1534-5807
DOI	10.1016/j.devcel.2023.08.001
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Article ; Online: Dual embryonic origin and patterning of the pharyngeal skeleton in the axolotl (Ambystoma mexicanum).

Sefton, Elizabeth M / Piekarski, Nadine / Hanken, James

Evolution & development

2015 Volume 17, Issue 3, Page(s) 175–184

Abstract: The impressive morphological diversification of vertebrates was achieved in part by innovation and modification of the pharyngeal skeleton. Extensive fate mapping in amniote models has revealed a primarily cranial neural crest derivation of the ... ...

Abstract	The impressive morphological diversification of vertebrates was achieved in part by innovation and modification of the pharyngeal skeleton. Extensive fate mapping in amniote models has revealed a primarily cranial neural crest derivation of the pharyngeal skeleton. Although comparable fate maps of amphibians produced over several decades have failed to document a neural crest derivation of ventromedial elements in these vertebrates, a recent report provides evidence of a mesodermal origin of one of these elements, basibranchial 2, in the axolotl. We used a transgenic labeling protocol and grafts of labeled cells between GFP+ and white embryos to derive a fate map that describes contributions of both cranial neural crest and mesoderm to the axolotl pharyngeal skeleton, and we conducted additional experiments that probe the mechanisms that underlie mesodermal patterning. Our fate map confirms a dual embryonic origin of the pharyngeal skeleton in urodeles, including derivation of basibranchial 2 from mesoderm closely associated with the second heart field. Additionally, heterotopic transplantation experiments reveal lineage restriction of mesodermal cells that contribute to pharyngeal cartilage. The mesoderm-derived component of the pharyngeal skeleton appears to be particularly sensitive to retinoic acid (RA): administration of exogenous RA leads to loss of the second basibranchial, but not the first. Neural crest was undoubtedly critical in the evolution of the vertebrate pharyngeal skeleton, but mesoderm may have played a central role in forming ventromedial elements, in particular. When and how many times during vertebrate phylogeny a mesodermal contribution to the pharyngeal skeleton evolved remain to be resolved.
MeSH term(s)	Ambystoma mexicanum/embryology ; Ambystoma mexicanum/genetics ; Animals ; Biological Evolution ; Body Patterning ; Bone and Bones/embryology ; Embryo, Nonmammalian/metabolism ; Mesoderm/embryology ; Neural Crest/embryology ; Pharynx/embryology ; Tretinoin/metabolism
Chemical Substances	Tretinoin (5688UTC01R)
Language	English
Publishing date	2015-05
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	2020288-X
ISSN	1525-142X ; 1520-541X
ISSN (online)	1525-142X
ISSN	1520-541X
DOI	10.1111/ede.12124
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Article ; Online: Evolution of the head-trunk interface in tetrapod vertebrates.

Sefton, Elizabeth M / Bhullar, Bhart-Anjan S / Mohaddes, Zahra / Hanken, James

eLife

2016 Volume 5, Page(s) e09972

Abstract: Vertebrate neck musculature spans the transition zone between head and trunk. The extent to which the cucullaris muscle is a cranial muscle allied with the gill levators of anamniotes or is instead a trunk muscle is an ongoing debate. Novel computed ... ...

Abstract	Vertebrate neck musculature spans the transition zone between head and trunk. The extent to which the cucullaris muscle is a cranial muscle allied with the gill levators of anamniotes or is instead a trunk muscle is an ongoing debate. Novel computed tomography datasets reveal broad conservation of the cucullaris in gnathostomes, including coelacanth and caecilian, two sarcopterygians previously thought to lack it. In chicken, lateral plate mesoderm (LPM) adjacent to occipital somites is a recently identified embryonic source of cervical musculature. We fate-map this mesoderm in the axolotl (Ambystoma mexicanum), which retains external gills, and demonstrate its contribution to posterior gill-levator muscles and the cucullaris. Accordingly, LPM adjacent to the occipital somites should be regarded as posterior cranial mesoderm. The axial position of the head-trunk border in axolotl is congruent between LPM and somitic mesoderm, unlike in chicken and possibly other amniotes.
MeSH term(s)	Animals ; Biological Evolution ; Head/anatomy & histology ; Muscle, Skeletal/anatomy & histology ; Neck/anatomy & histology ; Thorax/anatomy & histology ; Vertebrates/anatomy & histology
Language	English
Publishing date	2016-04-19
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2687154-3
ISSN	2050-084X ; 2050-084X
ISSN (online)	2050-084X
ISSN	2050-084X
DOI	10.7554/eLife.09972
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Article: Homology of the cranial vault in birds: new insights based on embryonic fate-mapping and character analysis.

Maddin, Hillary C / Piekarski, Nadine / Sefton, Elizabeth M / Hanken, James

Royal Society open science

2016 Volume 3, Issue 8, Page(s) 160356

Abstract: Bones of the cranial vault appear to be highly conserved among tetrapod vertebrates. Moreover, bones identified with the same name are assumed to be evolutionarily homologous. However, recent developmental studies reveal a key difference in the embryonic ...

Abstract	Bones of the cranial vault appear to be highly conserved among tetrapod vertebrates. Moreover, bones identified with the same name are assumed to be evolutionarily homologous. However, recent developmental studies reveal a key difference in the embryonic origin of cranial vault bones between representatives of two amniote lineages, mammals and birds, thereby challenging this view. In the mouse, the frontal is derived from cranial neural crest (CNC) but the parietal is derived from mesoderm, placing the CNC-mesoderm boundary at the suture between these bones. In the chicken, this boundary is located within the frontal. This difference and related data have led several recent authors to suggest that bones of the avian cranial vault are misidentified and should be renamed. To elucidate this apparent conflict, we fate-mapped CNC and mesoderm in axolotl to reveal the contributions of these two embryonic cell populations to the cranial vault in a urodele amphibian. The CNC-mesoderm boundary in axolotl is located between the frontal and parietal bones, as in the mouse but unlike the chicken. If, however, the avian frontal is regarded instead as a fused frontal and parietal (i.e. frontoparietal) and the parietal as a postparietal, then the cranial vault of birds becomes developmentally and topologically congruent with those of urodeles and mammals. This alternative hypothesis of cranial vault homology is also phylogenetically consistent with data from the tetrapod fossil record, where frontal, parietal and postparietal bones are present in stem lineages of all extant taxa, including birds. It further implies that a postparietal may be present in most non-avian archosaurs, but fused to the parietal or supraoccipital as in many extant mammals.
Language	English
Publishing date	2016-08-10
Publishing country	England
Document type	Journal Article
ZDB-ID	2787755-3
ISSN	2054-5703
ISSN	2054-5703
DOI	10.1098/rsos.160356
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