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Article ; Online: Craniofacial developmental biology in the single-cell era.

Tseng, Kuo-Chang / Crump, J Gage

2023 Volume 150, Issue 19

Abstract: The evolution of a unique craniofacial complex in vertebrates made possible new ways of breathing, eating, communicating and sensing the environment. The head and face develop through interactions of all three germ layers, the endoderm, ectoderm and ... ...

Abstract	The evolution of a unique craniofacial complex in vertebrates made possible new ways of breathing, eating, communicating and sensing the environment. The head and face develop through interactions of all three germ layers, the endoderm, ectoderm and mesoderm, as well as the so-called fourth germ layer, the cranial neural crest. Over a century of experimental embryology and genetics have revealed an incredible diversity of cell types derived from each germ layer, signaling pathways and genes that coordinate craniofacial development, and how changes to these underlie human disease and vertebrate evolution. Yet for many diseases and congenital anomalies, we have an incomplete picture of the causative genomic changes, in particular how alterations to the non-coding genome might affect craniofacial gene expression. Emerging genomics and single-cell technologies provide an opportunity to obtain a more holistic view of the genes and gene regulatory elements orchestrating craniofacial development across vertebrates. These single-cell studies generate novel hypotheses that can be experimentally validated in vivo. In this Review, we highlight recent advances in single-cell studies of diverse craniofacial structures, as well as potential pitfalls and the need for extensive in vivo validation. We discuss how these studies inform the developmental sources and regulation of head structures, bringing new insights into the etiology of structural birth anomalies that affect the vertebrate head.
MeSH term(s)	Animals ; Humans ; Biological Evolution ; Skull ; Vertebrates ; Neural Crest/metabolism ; Developmental Biology ; Gene Expression Regulation, Developmental
Language	English
Publishing date	2023-10-09
Publishing country	England
Document type	Review ; Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	90607-4
ISSN	1477-9129 ; 0950-1991
ISSN (online)	1477-9129
ISSN	0950-1991
DOI	10.1242/dev.202077
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Article ; Online: Reassessing the embryonic origin and potential of craniofacial ectomesenchyme.

Fabian, Peter / Crump, J Gage

Seminars in cell & developmental biology

2022 Volume 138, Page(s) 45–53

Abstract: Of all the cell types arising from the neural crest, ectomesenchyme is likely the most unusual. In contrast to the neuroglial cells generated by neural crest throughout the embryo, consistent with its ectodermal origin, cranial neural crest-derived cells ...

Abstract	Of all the cell types arising from the neural crest, ectomesenchyme is likely the most unusual. In contrast to the neuroglial cells generated by neural crest throughout the embryo, consistent with its ectodermal origin, cranial neural crest-derived cells (CNCCs) generate many connective tissue and skeletal cell types in common with mesoderm. Whether this ectoderm-derived mesenchyme (ectomesenchyme) potential reflects a distinct developmental origin from other CNCC lineages, and/or epigenetic reprogramming of the ectoderm, remains debated. Whereas decades of lineage tracing studies have defined the potential of CNCC ectomesenchyme, these are being revisited by modern genetic techniques. Recent work is also shedding light on the extent to which intrinsic and extrinsic cues determine ectomesenchyme potential, and whether maintenance or reacquisition of CNCC multipotency influences craniofacial repair.
MeSH term(s)	Neural Crest/metabolism ; Mesoderm ; Ectoderm/metabolism ; Embryo, Mammalian
Chemical Substances	N,N'-bis((2-chloroethyl)nitrosocarbamoyl)cystamine (77469-44-4)
Language	English
Publishing date	2022-03-21
Publishing country	England
Document type	Journal Article ; Review ; Research Support, N.I.H., Extramural
ZDB-ID	1312473-0
ISSN	1096-3634 ; 1084-9521
ISSN (online)	1096-3634
ISSN	1084-9521
DOI	10.1016/j.semcdb.2022.03.018
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Article ; Online: Gill developmental program in the teleost mandibular arch.

Thiruppathy, Mathi / Fabian, Peter / Gillis, J Andrew / Crump, J Gage

eLife

2022 Volume 11

Abstract: Whereas no known living vertebrate possesses gills derived from the jaw-forming mandibular arch, it has been proposed that the jaw arose through modifications of an ancestral mandibular gill. Here, we show that the zebrafish pseudobranch, which regulates ...

Abstract	Whereas no known living vertebrate possesses gills derived from the jaw-forming mandibular arch, it has been proposed that the jaw arose through modifications of an ancestral mandibular gill. Here, we show that the zebrafish pseudobranch, which regulates blood pressure in the eye, develops from mandibular arch mesenchyme and first pouch epithelia and shares gene expression, enhancer utilization, and developmental
MeSH term(s)	Animals ; Biological Evolution ; Branchial Region ; Gills ; Jaw ; Zebrafish
Language	English
Publishing date	2022-06-28
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.78170
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Article ; Online: DNA methylation in the mouse cochlea promotes maturation of supporting cells and contributes to the failure of hair cell regeneration.

Nguyen, John D / Llamas, Juan / Shi, Tuo / Crump, J Gage / Groves, Andrew K / Segil, Neil

Proceedings of the National Academy of Sciences of the United States of America

2023 Volume 120, Issue 33, Page(s) e2300839120

Abstract: Mammalian hair cells do not functionally regenerate in adulthood but can regenerate at embryonic and neonatal stages in mice by direct transdifferentiation of neighboring supporting cells into new hair cells. Previous work showed loss of ... ...

Abstract	Mammalian hair cells do not functionally regenerate in adulthood but can regenerate at embryonic and neonatal stages in mice by direct transdifferentiation of neighboring supporting cells into new hair cells. Previous work showed loss of transdifferentiation potential of supporting cells is in part due to H3K4me1 enhancer decommissioning of the hair cell gene regulatory network during the first postnatal week. However, inhibiting this decommissioning only partially preserves transdifferentiation potential. Therefore, we explored other repressive epigenetic modifications that may be responsible for this loss of plasticity. We find supporting cells progressively accumulate DNA methylation at promoters of developmentally regulated hair cell genes. Specifically, DNA methylation overlaps with binding sites of Atoh1, a key transcription factor for hair cell fate. We further show that DNA hypermethylation replaces H3K27me3-mediated repression of hair cell genes in mature supporting cells, and is accompanied by progressive loss of chromatin accessibility, suggestive of facultative heterochromatin formation. Another subset of hair cell loci is hypermethylated in supporting cells, but not in hair cells. Ten-eleven translocation (TET) enzyme-mediated demethylation of these hypermethylated sites is necessary for neonatal supporting cells to transdifferentiate into hair cells. We also observe changes in chromatin accessibility of supporting cell subtypes at the single-cell level with increasing age: Gene programs promoting sensory epithelium development loses chromatin accessibility, in favor of gene programs that promote physiological maturation and function of the cochlea. We also find chromatin accessibility is partially recovered in a chronically deafened mouse model, which holds promise for future translational efforts in hearing restoration.
MeSH term(s)	Animals ; Mice ; DNA Methylation ; Basic Helix-Loop-Helix Transcription Factors/metabolism ; Cochlea/metabolism ; Regeneration/genetics ; Chromatin/metabolism ; Mammals/genetics
Chemical Substances	Basic Helix-Loop-Helix Transcription Factors ; Chromatin
Language	English
Publishing date	2023-08-07
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	209104-5
ISSN	1091-6490 ; 0027-8424
ISSN (online)	1091-6490
ISSN	0027-8424
DOI	10.1073/pnas.2300839120
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Article: Regeneration of Jaw Joint Cartilage in Adult Zebrafish.

Smeeton, Joanna / Natarajan, Natasha / Anderson, Troy / Tseng, Kuo-Chang / Fabian, Peter / Crump, J Gage

Frontiers in cell and developmental biology

2022 Volume 9, Page(s) 777787

Abstract: The poor intrinsic repair capacity of mammalian joint cartilage likely contributes to the high incidence of arthritis worldwide. Adult zebrafish can regenerate many structures that show limited or no healing capacity in mammals, including the jawbone. To ...

Abstract	The poor intrinsic repair capacity of mammalian joint cartilage likely contributes to the high incidence of arthritis worldwide. Adult zebrafish can regenerate many structures that show limited or no healing capacity in mammals, including the jawbone. To test whether zebrafish can also regenerate damaged joints, we developed a surgical injury model in which the zebrafish jaw joint is destabilized
Language	English
Publishing date	2022-01-20
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2737824-X
ISSN	2296-634X
ISSN	2296-634X
DOI	10.3389/fcell.2021.777787
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Article ; Online: Single-cell transcriptomic profiling of the zebrafish inner ear reveals molecularly distinct hair cell and supporting cell subtypes.

Shi, Tuo / Beaulieu, Marielle O / Saunders, Lauren M / Fabian, Peter / Trapnell, Cole / Segil, Neil / Crump, J Gage / Raible, David W

eLife

2023 Volume 12

Abstract: A major cause of human deafness and vestibular dysfunction is permanent loss of the mechanosensory hair cells of the inner ear. In non-mammalian vertebrates such as zebrafish, regeneration of missing hair cells can occur throughout life. While a ... ...

Abstract	A major cause of human deafness and vestibular dysfunction is permanent loss of the mechanosensory hair cells of the inner ear. In non-mammalian vertebrates such as zebrafish, regeneration of missing hair cells can occur throughout life. While a comparative approach has the potential to reveal the basis of such differential regenerative ability, the degree to which the inner ears of fish and mammals share common hair cells and supporting cell types remains unresolved. Here, we perform single-cell RNA sequencing of the zebrafish inner ear at embryonic through adult stages to catalog the diversity of hair cells and non-sensory supporting cells. We identify a putative progenitor population for hair cells and supporting cells, as well as distinct hair and supporting cell types in the maculae versus cristae. The hair cell and supporting cell types differ from those described for the lateral line system, a distributed mechanosensory organ in zebrafish in which most studies of hair cell regeneration have been conducted. In the maculae, we identify two subtypes of hair cells that share gene expression with mammalian striolar or extrastriolar hair cells. In situ hybridization reveals that these hair cell subtypes occupy distinct spatial domains within the three macular organs, the utricle, saccule, and lagena, consistent with the reported distinct electrophysiological properties of hair cells within these domains. These findings suggest that primitive specialization of spatially distinct striolar and extrastriolar hair cells likely arose in the last common ancestor of fish and mammals. The similarities of inner ear cell type composition between fish and mammals validate zebrafish as a relevant model for understanding inner ear-specific hair cell function and regeneration.
MeSH term(s)	Animals ; Humans ; Zebrafish/genetics ; Transcriptome ; Hair Cells, Auditory/physiology ; Ear, Inner ; Hair Cells, Auditory, Inner ; Mammals/genetics
Language	English
Publishing date	2023-01-04
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.82978
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Article ; Online: SoxC transcription factors shape the epigenetic landscape to establish competence for sensory differentiation in the mammalian organ of Corti.

Wang, Xizi / Llamas, Juan / Trecek, Talon / Shi, Tuo / Tao, Litao / Makmura, Welly / Crump, J Gage / Segil, Neil / Gnedeva, Ksenia

Proceedings of the National Academy of Sciences of the United States of America

2023 Volume 120, Issue 34, Page(s) e2301301120

Abstract: The auditory organ of Corti is comprised of only two major cell types-the mechanosensory hair cells and their associated supporting cells-both specified from a single pool of prosensory progenitors in the cochlear duct. Here, we show that competence to ... ...

Abstract	The auditory organ of Corti is comprised of only two major cell types-the mechanosensory hair cells and their associated supporting cells-both specified from a single pool of prosensory progenitors in the cochlear duct. Here, we show that competence to respond to Atoh1, a transcriptional master regulator necessary and sufficient for induction of mechanosensory hair cells, is established in the prosensory progenitors between E12.0 and 13.5. The transition to the competent state is rapid and is associated with extensive remodeling of the epigenetic landscape controlled by the SoxC group of transcription factors. Conditional loss of
MeSH term(s)	Animals ; SOXC Transcription Factors/genetics ; SOXC Transcription Factors/metabolism ; Basic Helix-Loop-Helix Transcription Factors/genetics ; Basic Helix-Loop-Helix Transcription Factors/metabolism ; Cochlea/metabolism ; Hair Cells, Auditory/metabolism ; Cell Differentiation ; Transcription Factors/metabolism ; Epigenesis, Genetic ; Organ of Corti ; Gene Expression Regulation, Developmental ; Mammals/metabolism
Chemical Substances	SOXC Transcription Factors ; Basic Helix-Loop-Helix Transcription Factors ; Transcription Factors
Language	English
Publishing date	2023-08-16
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, N.I.H., Extramural
ZDB-ID	209104-5
ISSN	1091-6490 ; 0027-8424
ISSN (online)	1091-6490
ISSN	0027-8424
DOI	10.1073/pnas.2301301120
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Article ; Online: Skeletal stem cells: insights into maintaining and regenerating the skeleton.

Serowoky, Maxwell A / Arata, Claire E / Crump, J Gage / Mariani, Francesca V

Development (Cambridge, England)

2020 Volume 147, Issue 5

Abstract: Skeletal stem cells (SSCs) generate the progenitors needed for growth, maintenance and repair of the skeleton. Historically, SSCs have been defined as bone marrow-derived cells with inconsistent characteristics. However, ... ...

Abstract	Skeletal stem cells (SSCs) generate the progenitors needed for growth, maintenance and repair of the skeleton. Historically, SSCs have been defined as bone marrow-derived cells with inconsistent characteristics. However, recent
MeSH term(s)	Animals ; Bone Development/physiology ; Bone Marrow Cells/cytology ; Bone Regeneration/physiology ; Chondrocytes/cytology ; Growth Plate/cytology ; Growth Plate/growth & development ; Humans ; Mice ; Osteoblasts/cytology ; Osteogenesis/physiology ; Periosteum/cytology ; Stem Cells/cytology ; Zebrafish
Language	English
Publishing date	2020-03-11
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	90607-4
ISSN	1477-9129 ; 0950-1991
ISSN (online)	1477-9129
ISSN	0950-1991
DOI	10.1242/dev.179325
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Article: Lessons on skeletal cell plasticity from studying jawbone regeneration in zebrafish.

Paul, Sandeep / Crump, J Gage

BoneKEy reports

2016 Volume 5, Page(s) 853

Abstract: Three major mesenchymal cell types have important roles in determining the shapes of vertebrate animals: bone-producing osteoblasts, cartilage-producing chondrocytes, and fat-producing adipocytes. Although often considered discrete cell types, ... ...

Abstract	Three major mesenchymal cell types have important roles in determining the shapes of vertebrate animals: bone-producing osteoblasts, cartilage-producing chondrocytes, and fat-producing adipocytes. Although often considered discrete cell types, accumulating evidence is revealing mesenchymal cells of intermediate identities and interconversion of cell types. Such plasticity is particularly evident during adult skeletal repair. In this Review, we highlight recent work in zebrafish showing a role for hybrid cartilage-bone cells in large-scale regeneration of the adult jawbone, as well as their origins in the periosteum. An emerging theme is that the unique mechanical and signaling environment of the adult wound causes skeletal cell differentiation to diverge from the discrete lineages seen during development, which may aid in rapid and extensive regeneration of bone.
Language	English
Publishing date	2016-11-16
Publishing country	England
Document type	Review ; Journal Article
ZDB-ID	2816308-4
ISSN	2047-6396
ISSN	2047-6396
DOI	10.1038/bonekey.2016.81
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Article ; Online: osr1 couples intermediate mesoderm cell fate with temporal dynamics of vessel progenitor cell differentiation.

Perens, Elliot A / Diaz, Jessyka T / Quesnel, Agathe / Askary, Amjad / Crump, J Gage / Yelon, Deborah

Development (Cambridge, England)

2021 Volume 148, Issue 15

Abstract: Transcriptional regulatory networks refine gene expression boundaries to define the dimensions of organ progenitor territories. Kidney progenitors originate within the intermediate mesoderm (IM), but the pathways that establish the boundary between the ... ...

Abstract	Transcriptional regulatory networks refine gene expression boundaries to define the dimensions of organ progenitor territories. Kidney progenitors originate within the intermediate mesoderm (IM), but the pathways that establish the boundary between the IM and neighboring vessel progenitors are poorly understood. Here, we delineate roles for the zinc-finger transcription factor Osr1 in kidney and vessel progenitor development. Zebrafish osr1 mutants display decreased IM formation and premature emergence of lateral vessel progenitors (LVPs). These phenotypes contrast with the increased IM and absent LVPs observed with loss of the bHLH transcription factor Hand2, and loss of hand2 partially suppresses osr1 mutant phenotypes. hand2 and osr1 are expressed together in the posterior mesoderm, but osr1 expression decreases dramatically prior to LVP emergence. Overexpressing osr1 during this timeframe inhibits LVP development while enhancing IM formation, and can rescue the osr1 mutant phenotype. Together, our data demonstrate that osr1 modulates the extent of IM formation and the temporal dynamics of LVP development, suggesting that a balance between levels of osr1 and hand2 expression is essential to demarcate the kidney and vessel progenitor territories.
MeSH term(s)	Animals ; Basic Helix-Loop-Helix Transcription Factors/metabolism ; Cell Differentiation/physiology ; Gene Expression Regulation, Developmental/physiology ; Kidney/metabolism ; Kidney/physiology ; Mesoderm/metabolism ; Mesoderm/physiology ; Organogenesis/physiology ; Transcription Factors/metabolism ; Zebrafish/metabolism ; Zebrafish/physiology ; Zebrafish Proteins/metabolism
Chemical Substances	Basic Helix-Loop-Helix Transcription Factors ; Transcription Factors ; Zebrafish Proteins
Language	English
Publishing date	2021-08-10
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	90607-4
ISSN	1477-9129 ; 0950-1991
ISSN (online)	1477-9129
ISSN	0950-1991
DOI	10.1242/dev.198408
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