Bone Morphogenetic Proteins Are Required In Vivo for the Generation of Sympathetic Neurons

Schneider, Carolin; Wicht, Helmut; Enderich, Jana; Wegner, Michael; Rohrer, Hermann

doi:10.1016/s0896-6273(00)81033-8

Cited by 274 publications

(182 citation statements)

References 52 publications

(3 reference statements)

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“…Sympathoadrenal neural crest cells including those on their way to the adrenal anlage normally start to express Mash1 and Phox2b (Lo et al, 1998;Pattyn et al, 1999) under the influence of BMPs from the dorsal aorta (Reissmann et al, 1996;Schneider et al, 1999). The fact that sympathoadrenal neural crest cells at those axial levels where the adrenal medulla forms mostly fail to express Phox2b in Sox10-deficient embryos is compatible with the postulated role of Sox10 in Phox2b induction.…”

Section: Discussionmentioning

confidence: 85%

SoxE Proteins Are Differentially Required in Mouse Adrenal Gland Development

Reiprich

Stolt

Schreiner

et al. 2008

MBoC

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Sry-box (Sox)8, Sox9, and Sox10 are all strongly expressed in the neural crest. Here, we studied the influence of these closely related transcription factors on the developing adrenal medulla as one prominent neural crest derivative. Whereas Sox9 was not expressed, both Sox8 and Sox10 occurred widely in neural crest cells migrating to the adrenal gland and in the gland itself, and they were down-regulated in cells expressing catecholaminergic traits. Sox10-deficient mice lacked an adrenal medulla. The adrenal anlage was never colonized by neural crest cells, which failed to specify properly at the dorsal aorta and died apoptotically during migration. Furthermore, mutant neural crest cells did not express Sox8. Strong adrenal phenotypes were also observed when the Sox10 dimerization domain was inactivated or when a transactivation domain in the central portion was deleted. Sox8 in contrast had only minimal influence on adrenal gland development. Phenotypic consequences became only visible in Sox8-deficient mice upon additional deletion of one Sox10 allele. Replacement of Sox10 by Sox8, however, led to significant rescue of the adrenal medulla, indicating that functional differences between the two related Sox proteins contribute less to the different adrenal phenotypes of the null mutants than dependence of Sox8 expression on Sox10.

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Section: Discussionmentioning

confidence: 85%

SoxE Proteins Are Differentially Required in Mouse Adrenal Gland Development

Reiprich

Stolt

Schreiner

et al. 2008

MBoC

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“…Such factors include BMP2͞4, which drives NCC to autonomic sympathetic-like neuronal fate (18)(19)(20); neuregulin-1 and Notch ligands, which favor gliogenesis (21)(22)(23); and endothelin 3 (ET3), which promotes survival and proliferation of glial-melanocytic (GM) bipotent precursors as well as committed melanocytic and glial cells (24)(25)(26).…”

mentioning

confidence: 99%

Self-renewal capacity is a widespread property of various types of neural crest precursor cells

Trentin

Glavieux-Pardanaud²,

Douarin³

et al. 2004

Proc. Natl. Acad. Sci. U.S.A.

158

179

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In vertebrates, trunk neural crest (NC) generates glia, neurons, and melanocytes. In addition, it yields mesectodermal derivatives (connective tissues, chondrocytes, and myofibroblasts lining the blood vessels) in the head. Previous in vitro clonal analyses of avian NC cells unraveled a hierarchical succession of highly pluripotent, followed by various intermediate, progenitors, suggesting a model of progressive restrictions in the multiple potentialities of a totipotent stem cell, as prevails in the hematopoietic system. However, which progenitors are able to self-renew within the hierarchy of the NC lineages is still undetermined. Here, we explored further the stem cell properties of quail NC cells by means of in vitro serial subcloning. We identified types of multipotent and oligopotent NC progenitors that differ in their developmental repertoire, ability to self-maintain, and response to exogenous endothelin 3 according to their truncal or cephalic origin. The most striking result is that bipotent progenitors are endowed with self-renewal properties. Thus glia-melanocyte and glia-myofibroblast progenitors behave like stem cells in that they are able both to self-renew and generate a restricted progeny. In our culture conditions, glia-myofibroblast precursors display a modest capacity to self-renew, whereas glia-melanocyte precursors respond to endothelin 3 by extensive self-renewal. These findings may explain the etiology of certain multiphenotypic NC-derived tumors in humans. Moreover, the presence of multiple stem cell phenotypes along the NC-derived lineages may account for the rarity of the ''totipotent NC stem cell'' and may be related to the large variety and widespread dispersion of NC derivatives throughout the body. multipotency ͉ quail embryo ͉ clonal culture ͉ neuron ͉ glia T he neural crest (NC) is a transient structure of the vertebrate embryo formed by the lateral borders of the neural primordium. Its constitutive cells, after losing their epithelial arrangement, migrate away through embryonic tissues to stop at elected sites where they differentiate into many various cell types. These cell types include neurons of the peripheral and enteric ganglia, their associated glial cells, and Schwann cells lining peripheral nerves. The NC is also at the origin of melanocytes and endocrine cells, such as adrenomedullary cells and calcitoninproducing cells. The NC cephalic domain yields mesenchymal cells (forming the ''mesectoderm'') that differentiate into the cartilages and bones that form most of the skull and the entire facial and visceral skeleton. The mesectoderm also provides head connective-tissue cells and the vascular smooth-muscle cells associated with the vessels derived from the aortic arches and with the vessels irrigating the forebrain and face (1-3).Several attempts aimed at elucidating how and when the different NC-lineages become segregated during ontogeny were made by using in vitro cultures of single NC cells (NCC) (4-14) or by labeling single NCC with vital dyes either in the embryo (...

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“…This seems to be the first report of neuronal migration in the peripheral nervous system. The most extensively studied neural crest-derived peripheral neurons are sympathetic and sensory neurons, most of which do not differentiate into neurons until after their precursors have reached their final destination (Schneider et al, 1999). However, examination of fixed embryos has shown that the superior cervical ganglion forms from cells that first migrate ventrally to form a column of cells that is continuous with the stellate ganglion primordium at lower cervical levels; some cells subsequently migrate rostrally to form the superior cervical ganglion (Rubin, 1985).…”

Section: Differentiation and Cell Migrationmentioning

confidence: 99%

“…Although neuronal migration is common in the developing CNS, there is currently little evidence about whether developing peripheral neurons can migrate. In developing parasympathetic, sympathetic and dorsal root ganglia, the neural crest-derived precursors arrive at their final destination before differentiating into neurons (Schneider et al, 1999;Muller and Rohrer, 2002).…”

Section: Introductionmentioning

confidence: 99%

The migratory behavior of immature enteric neurons

Hao

Anderson

Kobayashi

et al. 2008

Developmental Neurobiology

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While they are migrating caudally along the developing gut, around 10%-20% of enteric neural crest-derived cells start to express pan-neuronal markers and tyrosine hydroxylase (TH). We used explants of gut from embryonic TH-green fluorescence protein (GFP) mice and time-lapse microscopy to examine whether these immature enteric neurons migrate and their mode of migration. In the gut of E10.5 and E11.5 TH-GFP mice, around 50% of immature enteric neurons (GFP + cells) migrated, with an average speed of around 15 lm/h. This is slower than the speed at which the population of enteric neural crest-derived cells advances along the developing gut, and hence neuronal differentiation seems to slow, but not necessarily halt, the caudal migration of enteric neural crest cells. Most migrating immature enteric neurons migrated caudally by extending a long-leading process followed by translocation of the cell body. This mode of migration is different from that of non-neuronal enteric neural crestderived cells and neural crest cells in other locations, but resembles that of migrating neurons in many regions of the developing central nervous system (CNS). In migrating immature enteric neurons, a swelling often preceded the movement of the nucleus in the direction of the leading process. However, the centrosomal marker, pericentrin, was not localized to either the leading process or swelling. This seems to be the first detailed report of neuronal migration in the developing mammalian peripheral nervous system. ' 2008 Wiley Periodicals, Inc. Develop Neurobiol 69: 22-35, 2009

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Bone Morphogenetic Proteins Are Required In Vivo for the Generation of Sympathetic Neurons

Cited by 274 publications

References 52 publications

SoxE Proteins Are Differentially Required in Mouse Adrenal Gland Development

SoxE Proteins Are Differentially Required in Mouse Adrenal Gland Development

Self-renewal capacity is a widespread property of various types of neural crest precursor cells

The migratory behavior of immature enteric neurons

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