Neurogenesis From Neural Crest Cells: Molecular Mechanisms in the Formation of Cranial Nerves and Ganglia

Méndez-Maldonado, Karla; Vega-Lopez, Guillermo A.; Aybar, Manuel J.; Velasco, Iván

doi:10.3389/fcell.2020.00635

Cited by 53 publications

(38 citation statements)

References 347 publications

(359 reference statements)

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“…Shox2 is expressed in all these neural crest-derived tissues, but a functional requirement has only been observed for the development of the FGn and the mechanosensory neurons of the DRG 20,21 . Interestingly, while no H3K27ac profiles for cranial nerve populations were available from ENCODE, both GDE5 and GDE12 elements showed elevated H3K27ac in craniofacial tissue at E11.5, potentially mirroring the common neural-crest origin of cranial nerve and a subset of craniofacial cell populations 32 . At mid-gestation, Shox2 is also expressed in the diencephalon (DE), midbrain (MB) and hindbrain (HB), and is specifically required for cerebellar development 33 .…”

Section: Resultsmentioning

confidence: 99%

A gene desert required for regulatory control of pleiotropicShox2expression and embryonic survival

Abassah-Oppong

Mannion

Tissières

et al. 2020

Preprint

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The Shox2 homeodomain transcriptional regulator is known for its critical functions during mouse embryogenesis, enabling accurate development of limbs, craniofacial structures, neural populations and the cardiac conduction system. At the genomic level, the Shox2 gene is flanked by an extensive gene desert, a continuous non-coding genomic region spanning over 500 kilobases that contains a multitude of evolutionarily conserved elements with predicted cis-regulatory activities. However, the transcriptional enhancer potential of the vast majority of these elements in combination with the biological necessity of the gene desert have not yet been explored. Using transgenic reporter assays in mouse embryos to validate an extensive set of stringent epigenomic enhancer predictions, we identify several novel gene desert enhancers with distinct tissue-specific activities in Shox2 expressing tissues. 4C-seq chromatin conformation capture further uncovers a repertoire of gene desert enhancers with overlapping activities in the proximal limb, in a compartment essential for Shox2-mediated stylopod formation. Leveraging CRISPR/Cas9 to delete the gene desert region contained in the Shox2 topologically associated domain (TAD), we demonstrate that this complex cis-regulatory platform is essential for embryonic survival and required for control of region-specific Shox2 expression in multiple developing tissues. While transcription of Shox2 in the embryonic limb is only moderately affected by gene desert loss, Shox2 expression in craniofacial and cardiac domains is nearly abolished. In particular, Shox2 transcripts in the sinus venosus (SV) encompassing the sinoatrial node (SAN) were depleted in embryos lacking the gene desert, likely accounting for the embryonic lethality due to Shox2-dependency of the SAN pacemaker. Finally, we discover a 1.5kb SV enhancer within the deleted gene desert region, which may act as a genomic module controlling the development of the cardiac conduction system. In summary, our results identify a gene desert indispensable for pleiotropic patterning and highlight the importance of these extensive regulatory landscapes for embryonic development and viability.

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Section: Resultsmentioning

confidence: 99%

A gene desert required for regulatory control of pleiotropicShox2expression and embryonic survival

Abassah-Oppong

Mannion

Tissières

et al. 2020

Preprint

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“…Some neural crest stem cells differentiate to MSCs to generate oral neural crest-derived mesenchyme (i.e., ectomesenchyme) which will then give rise to the different oral connective tissues, cartilages, muscles and bones. However, these neural crest stem cells are also the precursors of the cranial peripheral nerve system [ 69 ]. Perhaps due to their shared origin, it is not uncommon to observe that hDPSCs express a varied repertoire of both neural progenitor and mature cell markers, even in normal standard (control) culture conditions [ 59 , 70 , 71 , 72 ].…”

Section: Dpscs As Neural Crest Stem Cells the Postnatal Dpsc Nichmentioning

confidence: 99%

Advances and Perspectives in Dental Pulp Stem Cell Based Neuroregeneration Therapies

Luzuriaga

Polo

Pastor-Alonso

et al. 2021

IJMS

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Human dental pulp stem cells (hDPSCs) are some of the most promising stem cell types for regenerative therapies given their ability to grow in the absence of serum and their realistic possibility to be used in autologous grafts. In this review, we describe the particular advantages of hDPSCs for neuroregenerative cell therapies. We thoroughly discuss the knowledge about their embryonic origin and characteristics of their postnatal niche, as well as the current status of cell culture protocols to maximize their multilineage differentiation potential, highlighting some common issues when assessing neuronal differentiation fates of hDPSCs. We also review the recent progress on neuroprotective and immunomodulatory capacity of hDPSCs and their secreted extracellular vesicles, as well as their combination with scaffold materials to improve their functional integration on the injured central nervous system (CNS) and peripheral nervous system (PNS). Finally, we offer some perspectives on the current and possible future applications of hDPSCs in neuroregenerative cell therapies.

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“…The discovery of these derivatives has resulted from research in different model organisms, which allowed specific studies of all cell populations. The cranial NC forms the cartilage and bones of the head, carotid body (Pearse et al, 1973), pericytes and interstitial cells of the adenohypophysis (Etchevers, Vincent, & Couly, 2001), pericytes, and smooth muscle cells of the vasculature (Etchevers, Vincent, Le Douarin, & Couly, 2001), lacrimal gland (de la Cuadra‐Blanco et al, 2003), pigment cells, melanocytes of the hair follicles (and the dermal papillae at the head and neck level) (Sieber‐Blum et al, 2004), connective tissue, corneal endothelium and stroma, trabecular meshwork, iris stroma, ciliary body stroma and anterior sclera (Yoshida et al, 2006), adipocytes (Billon et al, 2007), dental pulp (Waddington et al, 2009), the olfactory epithelium (Barraud et al, 2010), meninges of the brain (Decimo et al, 2012), and cranial nerves and ganglia (Mendez‐Maldonado et al, 2020). The cardiac NC contributes to the development of the heart (George et al, 2020; Lajiness et al, 2014; Verberne et al, 2000; Yamagishi, 2020), the aorticopulmonary septum, the innervation of the lung (Aven & Ai, 2013; Freem et al, 2010), the enteric ganglia of the gut, the PNS, melanocytes, stroma of the thyroid and thymus glands (Figueiredo et al, 2016; Wang et al, 2017; Zachariah & Cyster, 2010), and cardiac ganglia.…”

Section: Nc Derivativesmentioning

confidence: 99%

The crucial role of model systems in understanding the complexity of cell signaling in human neurocristopathies

Cerrizuela

Vega-Lopez

Méndez-Maldonado

et al. 2021

WIREs Mechanisms of Disease

Self Cite

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Animal models are useful to study the molecular, cellular, and morphogenetic mechanisms underlying normal and pathological development. Cell‐based study models have emerged as an alternative approach to study many aspects of human embryonic development and disease. The neural crest (NC) is a transient, multipotent, and migratory embryonic cell population that generates a diverse group of cell types that arises during vertebrate development. The abnormal formation or development of the NC results in neurocristopathies (NCPs), which are characterized by a broad spectrum of functional and morphological alterations. The impaired molecular mechanisms that give rise to these multiphenotypic diseases are not entirely clear yet. This fact, added to the high incidence of these disorders in the newborn population, has led to the development of systematic approaches for their understanding. In this article, we have systematically reviewed the ways in which experimentation with different animal and cell model systems has improved our knowledge of NCPs, and how these advances might contribute to the development of better diagnostic and therapeutic tools for the treatment of these pathologies. This article is categorized under: Congenital Diseases > Genetics/Genomics/Epigenetics Congenital Diseases > Stem Cells and Development Congenital Diseases > Molecular and Cellular Physiology Neurological Diseases > Genetics/Genomics/Epigenetics

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Neurogenesis From Neural Crest Cells: Molecular Mechanisms in the Formation of Cranial Nerves and Ganglia

Cited by 53 publications

References 347 publications

A gene desert required for regulatory control of pleiotropicShox2expression and embryonic survival

A gene desert required for regulatory control of pleiotropicShox2expression and embryonic survival

Advances and Perspectives in Dental Pulp Stem Cell Based Neuroregeneration Therapies

The crucial role of model systems in understanding the complexity of cell signaling in human neurocristopathies

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