Epithelial Migration and Non-adhesive Periderm Are Required for Digit Separation during Mammalian Development

Kashgari, Ghaidaa; Meinecke, Lina; Gordon, William; Ruiz, Bryan; Yang, Jady; Lan, Amy; Xie, Yong; Ho, Hsiang‐Ling; Plikus, Maksim V.; Nie, Qing; Jester, James V.; Andersen, Bogi

doi:10.1016/j.devcel.2020.01.032

Cited by 21 publications

(21 citation statements)

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“…This aspect of tissue remodeling has been often neglected in developmental studies devoted to cell deathmediated morphogenesis. However, its dysregulation abrogates the formation of free digits (McCulloch et al, 2009;Kashgari et al, 2020). The abundance of secreted matrix metalloproteases in the SASP (described above) sustains without doubt this important aspect of interdigital tissue remodeling.…”

Section: Additional Potential Functions Of Cell Senescence In Interdimentioning

confidence: 96%

“…A final important feature of interdigit remodeling is the degradation of the extracellular matrix, collapse of the blood vessels (Hurle et al, 1985) and the subsequent elimination of waste ectodermal tissue into the amniotic sac (Hurle and Fernandez-Teran, 1983;McCulloch et al, 2009;Kashgari et al, 2020). This aspect of tissue remodeling has been often neglected in developmental studies devoted to cell deathmediated morphogenesis.…”

Section: Additional Potential Functions Of Cell Senescence In Interdimentioning

confidence: 99%

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Confluence of Cellular Degradation Pathways During Interdigital Tissue Remodeling in Embryonic Tetrapods

Montero

Lorda‐Diez

Hurlé

2020

Front. Cell Dev. Biol.

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Digits develop in the distal part of the embryonic limb primordium as radial prechondrogenic condensations separated by undifferentiated mesoderm. In a short time interval the interdigital mesoderm undergoes massive degeneration to determine the formation of free digits. This fascinating process has often been considered as an altruistic cell suicide that is evolutionarily-regulated in species with different degrees of digit webbing. Initial descriptions of interdigit remodeling considered lysosomes as the primary cause of the degenerative process. However, the functional significance of lysosomes lost interest among researcher and was displaced to a secondary role because the introduction of the term apoptosis. Accumulating evidence in recent decades has revealed that, far from being a unique method of embryonic cell death, apoptosis is only one among several redundant dying mechanisms accounting for the elimination of tissues during embryonic development. Developmental cell senescence has emerged in the last decade as a primary factor implicated in interdigit remodeling. Our review proposes that cell senescence is the biological process identified by vital staining in embryonic models and implicates lysosomes in programmed cell death. We review major structural changes associated with interdigit remodeling that may be driven by cell senescence. Furthermore, the identification of cell senescence lacking tissue degeneration, associated with the maturation of the digit tendons at the same stages of interdigital remodeling, allowed us to distinguish between two functionally distinct types of embryonic cell senescence, "constructive" and "destructive."

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Section: Additional Potential Functions Of Cell Senescence In Interdimentioning

confidence: 96%

Section: Additional Potential Functions Of Cell Senescence In Interdimentioning

confidence: 99%

Confluence of Cellular Degradation Pathways During Interdigital Tissue Remodeling in Embryonic Tetrapods

Montero

Lorda‐Diez

Hurlé

2020

Front. Cell Dev. Biol.

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“…irf6 and grhl3 are likely required for limb development in zebrafish, as shown by the loss of pectoral fins in different models, but their roles remain unclear. During mammalian development, loss of either Irf6 or Grhl3 results in shortened forelimbs, ectrodactyly, or syndactyly (Ingraham et al, 2006; Kashgari et al, 2020). Irf6 is thought to be required for formation of the periderm, a single layer of epithelial cells surrounding the embryonic epidermis.…”

Section: Zebrafish Models Of Craniofacial Anomalies With Accompanying Limb Defectsmentioning

confidence: 99%

The power of zebrafish models for understanding the co‐occurrence of craniofacial and limb disorders

Truong

Artinger

2021

Genesis

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Summary Craniofacial and limb defects are two of the most common congenital anomalies in the general population. Interestingly, these defects are not mutually exclusive. Many patients with craniofacial phenotypes, such as orofacial clefting and craniosynostosis, also present with limb defects, including polydactyly, syndactyly, brachydactyly, or ectrodactyly. The gene regulatory networks governing craniofacial and limb development initially seem distinct from one another, and yet these birth defects frequently occur together. Both developmental processes are highly conserved among vertebrates, and zebrafish have emerged as an advantageous model due to their high fecundity, relative ease of genetic manipulation, and transparency during development. Here we summarize studies that have used zebrafish models to study human syndromes that present with both craniofacial and limb phenotypes. We discuss the highly conserved processes of craniofacial and limb/fin development and describe recent zebrafish studies that have explored the function of genes associated with human syndromes with phenotypes in both structures. We attempt to identify commonalities between the two to help explain why craniofacial and limb anomalies often occur together.

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“…Grhl3 functionally interacts with the LIM-only protein LMO4 to regulate the differentiation of the epidermis, where mice lacking functional Grhl3 and LMO4 expression show severe defective skin barrier formation and failure of eyelid development affecting the expression of multiple genes linked to the epidermal terminal differentiation and F-actin cable formation (Yu et al, 2006(Yu et al, , 2008Hislop et al, 2008). Mice deleted for epidermal specific Grhl3 have digit fusion (syndactyly) due to abnormal adhesion of the periderm covering the developing digits (Kashgari et al, 2020). In autosomal-recessive ectodermal dysplasia syndrome, whole exome-sequencing from affected individuals revealed the presence of homozygous mutations in the GRHL2 locus.…”

Section: Grhl Family In Epithelial Morphogenesis and Developmentmentioning

confidence: 99%

Spotlight on the Granules (Grainyhead-Like Proteins) – From an Evolutionary Conserved Controller of Epithelial Trait to Pioneering the Chromatin Landscape

Sundararajan

Pang

Choolani

et al. 2020

Front. Mol. Biosci.

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Among the transcription factors that are conserved across phylogeny, the grainyhead family holds vital roles in driving the epithelial cell fate. In Drosophila , the function of grainyhead ( grh ) gene is essential during developmental processes such as epithelial differentiation, tracheal tube formation, maintenance of wing and hair polarity, and epidermal barrier wound repair. Three main mammalian orthologs of grh : Grainyhead-like 1-3 (GRHL1, GRHL2, and GRHL3) are highly conserved in terms of their gene structures and functions. GRHL proteins are essentially associated with the development and maintenance of the epithelial phenotype across diverse physiological conditions such as epidermal differentiation and craniofacial development as well as pathological functions including hearing impairment and neural tube defects. More importantly, through direct chromatin binding and induction of epigenetic alterations, GRHL factors function as potent suppressors of oncogenic cellular dedifferentiation program – epithelial-mesenchymal transition and its associated tumor-promoting phenotypes such as tumor cell migration and invasion. On the contrary, GRHL factors also induce pro-tumorigenic effects such as increased migration and anchorage-independent growth in certain tumor types. Furthermore, investigations focusing on the epithelial-specific activation of grh and GRHL factors have revealed that these factors potentially act as a pioneer factor in establishing a cell-type/cell-state specific accessible chromatin landscape that is exclusive for epithelial gene transcription. In this review, we highlight the essential roles of grh and GRHL factors during embryogenesis and pathogenesis, with a special focus on its emerging pioneering function.

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Epithelial Migration and Non-adhesive Periderm Are Required for Digit Separation during Mammalian Development

Cited by 21 publications

References 59 publications

Confluence of Cellular Degradation Pathways During Interdigital Tissue Remodeling in Embryonic Tetrapods

Confluence of Cellular Degradation Pathways During Interdigital Tissue Remodeling in Embryonic Tetrapods

The power of zebrafish models for understanding the co‐occurrence of craniofacial and limb disorders

Spotlight on the Granules (Grainyhead-Like Proteins) – From an Evolutionary Conserved Controller of Epithelial Trait to Pioneering the Chromatin Landscape

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