A Histone2BCerulean BAC transgene identifies differential expression of <i>Phox2b</i> in migrating enteric neural crest derivatives and enteric glia

Corpening, Jennifer C.; Cantrell, V. Ashley; Deal, Karen K.; Southard‐Smith, E. Michelle

doi:10.1002/dvdy.21498

Cited by 50 publications

(64 citation statements)

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“…The appearance of Phox2b at E9.5 is not associated with the transient cell cycle exit seen at E10.5, as 98% of all cells expressed both Phox2b and Sox10, and so most Phox2b ϩ cells lacking Tuj1 and TH must remain cycling. This also means that Phox2b must be present in cells that give rise to both neurons and glia in sympathetic ganglia, as suggested previously (Tsarovina et al, 2008;Nagashimada et al, 2012), similar to the situation in the enteric nervous system (Young et al, 1998;Anderson et al, 2006;Corpening et al, 2008;Lei and Howard, 2011).…”

Section: Differentiation and Cell Cycle Withdrawalsupporting

confidence: 65%

“…Mice were time plug mated, and the morning of the detection of the plug was deemed to be embryonic day (E) 0.5. Wild-type C57BL/6 mice and Ret TGM/TGM mice on a C57BL/6 background (Enomoto et al, 2001) were used. Ret TGM/TGM mice have a fusion protein consisting of the N-terminal region of bovine tau, a full-length EGFP and three repeats of the human Myc tag inserted into the first exon of the Ret gene by homologous recombination.…”

Section: Methodsmentioning

confidence: 99%

“…Ret TGM/TGM mice have a fusion protein consisting of the N-terminal region of bovine tau, a full-length EGFP and three repeats of the human Myc tag inserted into the first exon of the Ret gene by homologous recombination. Mice heterozygous for the Ret-TGM insertion (Ret TGM/ϩ ) develop and survive normally, while homozygote animals die shortly after birth due to kidney and enteric nervous system deficits (Enomoto et al, 2001). Ret TGM/TGM animals were generated by mating Ret TGM/ϩ males with Ret TGM/ϩ females.…”

Section: Methodsmentioning

confidence: 99%

“…All sympathetic ganglia are reduced in size in Ret-null mutant mice (Enomoto et al, 1998). We therefore examined the effect of loss of Ret, the signaling receptor for GDNF family ligands, on cell cycle dynamics in the stellate ganglion in E12.5, E14.5, and E16.5 Ret-null mutants (Enomoto et al, 1998).…”

Section: Ret and Cell Cycle Lengthmentioning

confidence: 99%

“…Previous studies have shown that cell death occurs at very low levels in embryonic mouse sympathetic ganglia. For example, the number of pyknotic (presumably apoptotic) or caspase 3 immunoreactive nuclei reported in mouse sympathetic ganglia vary from none at E12.5 (Enomoto et al, 2001) to a maximum of 0.9% at E16.5 and E17.5 and 1.4% at P0 (Fagan et al, 1996;Francis et al, 1999;Enomoto et al, 2001), with the rate of cell death increasing from E15.5 (Eldredge et al, 2008). If one assumes pyknotic or caspase 3-positive nuclei survive for ϳ8 h, then cell death could be ϳ3% from E16.5 to E18.5.…”

Section: Cell Cycle Lengths Measured For Sox10mentioning

confidence: 99%

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Proliferation and Cell Cycle Dynamics in the Developing Stellate Ganglion

Gonsalvez

Cane²,

Landman

et al. 2013

J. Neurosci.

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Cell proliferation during nervous system development is poorly understood outside the mouse neocortex. We measured cell cycle dynamics in the embryonic mouse sympathetic stellate ganglion, where neuroblasts continue to proliferate following neuronal differentiation. At embryonic day (E) 9.5, when neural crest-derived cells were migrating and coalescing into the ganglion primordium, all cells were cycling, cell cycle length was only 10.6 h, and S-phase comprised over 65% of the cell cycle; these values are similar to those previously reported for embryonic stem cells. At E10.5, Sox10ϩ cells lengthened their cell cycle to 38 h and reduced the length of S-phase. As cells started to express the neuronal markers Tuj1 and tyrosine hydroxylase (TH) at E10.5, they exited the cell cycle. At E11.5, when Ͼ80% of cells in the ganglion were Tuj1 /THϪ cells increased during late embryonic development, and ϳ25% were still cycling at E18.5. Loss of Ret increased neuroblast cell cycle length at E16.5 and decreased the number of neuroblasts at E18.5. A mathematical model generated from our data successfully predicted the relative change in proportions of neuroblasts and non-neuroblasts in wild-type mice. Our results show that, like other neurons, sympathetic neuron differentiation is associated with exit from the cell cycle; sympathetic neurons are unusual in that they then re-enter the cell cycle before later permanently exiting.

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Section: Differentiation and Cell Cycle Withdrawalsupporting

confidence: 65%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Ret and Cell Cycle Lengthmentioning

confidence: 99%

Section: Cell Cycle Lengths Measured For Sox10mentioning

confidence: 99%

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Proliferation and Cell Cycle Dynamics in the Developing Stellate Ganglion

Gonsalvez

Cane²,

Landman

et al. 2013

J. Neurosci.

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Molecular fingerprinting delineates progenitor populations in the developing zebrafish enteric nervous system

Taylor

Montagne

Eisen

et al. 2016

Developmental Dynamics

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Background To understand the basis of nervous system development, we must learn how multipotent progenitors generate diverse neuronal and glial lineages. We addressed this issue in the zebrafish enteric nervous system (ENS), a complex neuronal and glial network that regulates essential intestinal functions. Little is currently known about how ENS progenitor subpopulations generate enteric neuronal and glial diversity. Results We identified temporally and spatially dependent progenitor subpopulations based on coexpression of three genes essential for normal ENS development: phox2bb, sox10, and ret. Our data suggest that combinatorial expression of these genes delineates three major ENS progenitor subpopulations, (1) phox2bb+/ret−/sox10−, (2) phox2bb+/ret+/sox10−, and (3) phox2bb+/ret+/sox10+, that reflect temporal progression of progenitor maturation during migration. We also found that differentiating zebrafish neurons maintain phox2bb and ret expression, and lose sox10 expression. Conclusion Our data show that zebrafish enteric progenitors constitute a heterogeneous population at both early and late stages of ENS development and suggest that marker gene expression is indicative of a progenitor’s fate. We propose that a progenitor’s expression profile reveals its developmental state: “younger” wave front progenitors express all three genes, whereas more mature progenitors behind the wave front selectively lose sox10 and/or ret expression, which may indicate developmental restriction.

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Isolation and live imaging of enteric progenitors based on Sox10‐Histone2BVenus transgene expression

Corpening¹,

Deal²,

Cantrell³

et al. 2011

Genesis

Self Cite

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To facilitate dynamic imaging of neural crest (NC) lineages and discrimination of individual cells in the enteric nervous system (ENS) where close juxtaposition often complicates viewing, we generated a mouse BAC transgenic line that drives a Histone2BVenus (H2BVenus) reporter from Sox10 regulatory regions. This strategy does not alter the endogenous Sox10 locus and thus facilitates analysis of normal NC development. Our Sox10-H2BVenus BAC transgene exhibits temporal, spatial, and cell-type specific expression that reflects endogenous Sox10 patterns. Individual cells exhibiting nuclear–localized fluorescence of the H2BVenus reporter are readily visualized in both fixed and living tissue and are amenable to isolation by fluorescence activated cell sorting (FACS). FACS-isolated H2BVenus+ enteric NC-derived progenitors (ENPs) exhibit multi-potency, readily form neurospheres, self-renew in vitro and express a variety of stem cell genes. Dynamic live imaging as H2BVenus+ ENPs migrate down the fetal gut reveals cell fragmentation suggesting that apoptosis occurs at a low frequency during normal development of the ENS. Confocal imaging both during population of the fetal intestine and in post-natal gut muscle strips revealed differential expression between individual cells consistent with down-regulation of the transgene as progression towards non-glial fates occurs. The expression of the Sox10-H2BVenus transgene in multiple regions of the peripheral nervous system will facilitate future studies of NC lineage segregation as this tool is expressed in early NC progenitors and maintained in enteric glia.

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A Histone2BCerulean BAC transgene identifies differential expression of Phox2b in migrating enteric neural crest derivatives and enteric glia

Cited by 50 publications

References 50 publications

Proliferation and Cell Cycle Dynamics in the Developing Stellate Ganglion

Proliferation and Cell Cycle Dynamics in the Developing Stellate Ganglion

Molecular fingerprinting delineates progenitor populations in the developing zebrafish enteric nervous system

Isolation and live imaging of enteric progenitors based on Sox10‐Histone2BVenus transgene expression

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