Effect of <i>Gdnf</i> haploinsufficiency on rate of migration and number of enteric neural crest‐derived cells

Flynn, Brianna O.; Bergner, Annette J.; Turner, Kirsty; Young, Heather M.; Anderson, Richard B.

doi:10.1002/dvdy.21013

Cited by 22 publications

(24 citation statements)

References 54 publications

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“…In avians, the percentage of neurons rises from zero at E4.5 to around 55% at E6 (18). In the mouse midgut, neurogenesis occurs within a small proportion of NC-derived cells as early as E10.5 (21). It rises dramatically to reach a quarter of these cells by E12.5 and to 45% at E14.5 (21).…”

Section: Discussionmentioning

confidence: 99%

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Appearance of cholinergic myenteric neurons during enteric nervous system development: comparison of different ChAT fluorescent mouse reporter lines

Erickson

Lee

Barlow‐Anacker

et al. 2014

Neurogastroenterology Motil

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Background Cholinergic neurons have been identified with the acetylcholine synthetic enzyme choline acetyltransferase (ChAT). However, ChAT is difficult to localize in newly differentiated peripheral neurons making the study of cholinergic neuronal development problematic. Consequently researchers have used mouse reporter lines to indicate the presence of ChAT. Methods Our objective was to determine which ChAT reporter line was the most sensitive indicator of ChAT expression. We utilized two different fluorescent ChAT reporter lines (ChAT-GFP and ChAT-Cre;R26R:floxSTOP:tdTomato) together with immunolocalization of ChAT protein (ChAT-IR) to characterize the spatial and temporal expression of ChAT in myenteric neurons throughout ENS development. Key Results ChAT-IR cells were first seen in the intestine at E10.5, even within the migration wavefront of neural precursors. Myenteric neurons within the distal small intestine (dSI) and proximal colon were first labeled by ChAT-IR, then ChAT-GFP, and finally ChAT-Cre tdTomato. The percentage of ChAT-IR neurons is equivalent to adult levels in the dSI by E13.5 and proximal colon by P0. After these stages, the percentages remained relatively constant throughout development despite dramatic changes in neuronal density. Conclusions and Inferences These observations indicate that neurotransmitter expression occurs early and there is only a brief gap between neurogenesis and neurotransmitter expression. Our finding that the proportion of ChAT myenteric neurons reached adult levels during embryonic development suggests that the fate of cholinergic neurons is tightly regulated and that their differentiation might influence further neuronal development. ChAT-GFP is a more accurate indicator of early ENS cholinergic neuronal differentiation than the ChAT-Cre;R26R:floxSTOP:tdTomato reporter mouse.

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Section: Discussionmentioning

confidence: 99%

“…In the mouse midgut, neurogenesis occurs within a small proportion of NC-derived cells as early as E10.5 (21). It rises dramatically to reach a quarter of these cells by E12.5 and to 45% at E14.5 (21). We detected cholinergic neurogenesis within the gut as early as E10.5.…”

Section: Discussionmentioning

confidence: 99%

Appearance of cholinergic myenteric neurons during enteric nervous system development: comparison of different ChAT fluorescent mouse reporter lines

Erickson

Lee

Barlow‐Anacker

et al. 2014

Neurogastroenterology Motil

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“…NCC within 300 μm of the wave-front have also been shown to migrate faster than their more rostral neighbours (Druckenbrod and Epstein, 2007). It is clear that the NCC migration wave-front is more sensitive to the influence of the gut microenvironment, as it is these cells within Edn3 mutants and Gdnf heterozygous mice that have a reduced proliferative capacity when compared with the entire population of NCC Flynn et al, 2007). However, data against this critical number model for gut colonisation comes from the work of Sidebotham and colleagues (Sidebotham et al, 2002).…”

Section: /51mentioning

confidence: 99%

Critical numbers of neural crest cells are required in the pathways from the neural tube to the foregut to ensure complete enteric nervous system formation

Barlow¹,

Wallace²,

Thapar³

et al. 2008

Development

113

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The enteric nervous system (ENS) is mainly derived from vagal neural crest cells (NCC) that arise at the level of somites 1-7. To understand how the size and composition of the NCC progenitor pool affects ENS development, we reduced the number of NCC by ablating the neural tube adjacent to somites 3-6 to produce aganglionic gut. We then back-transplanted various somite lengths of quail neural tube into the ablated region to determine the 'tipping point', whereby sufficient progenitors were available for complete ENS formation. The addition of one somite length of either vagal, sacral or trunk neural tube into embryos that had the neural tube ablated adjacent to somites 3-6, resulted in ENS formation along the entire gut. Although these additional cells contributed to the progenitor pool, the quail NCC from different axial levels retained their intrinsic identities with respect to their ability to form the ENS; vagal NCC formed most of the ENS, sacral NCC contributed a limited number of ENS cells, and trunk NCC did not contribute to the ENS. As one somite length of vagal NCC was found to comprise almost the entire ENS, we ablated all of the vagal neural crest and back-transplanted one somite length of vagal neural tube from the level of somite 1 or somite 3 into the vagal region at the position of somite 3. NCC from somite 3 formed the ENS along the entire gut, whereas NCC from somite 1 did not. Intrinsic differences, such as an increased capacity for proliferation, as demonstrated in vitro and in vivo, appear to underlie the ability of somite 3 NCC to form the entire ENS.

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“…Randomly chosen fields within the ileum and proximal colon were imaged using a ϫ63 lens and a Bio-Rad MRC 1024 confocal microscope as previously described (Flynn et al, 2007). It has previously been shown that differentiating neurons show strong nuclear expression of Hu, whereas cells that have not started to differentiate into neurons are either Hu-negative or show weak Hu staining in the cytoplasm only .…”

Section: Cell Countmentioning

confidence: 99%

Cell adhesion molecule L1 affects the rate of differentiation of enteric neurons in the developing gut

Turner

Schachner

Anderson

2009

Developmental Dynamics

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The enteric nervous system arises predominantly from vagal level neural crest cells that migrate into and along the developing gut. As the neural crest-derived cells migrate within the gut, a subpopulation begins to differentiate into enteric neurons. Here, we show that the differentiation of neural crest-derived cells into enteric neurons is delayed in L1-deficient mice, compared with littermate controls. However, glial cell differentiation is not affected in L1-deficient mice. These mice also show a delay in the differentiation of a neurotransmitter-specific subtype of enteric neuron within the gastrointestinal tract. Together, these results suggest a role for the cell adhesion molecule, L1, in the differentiation of neural crestderived cells into enteric neurons within the developing enteric nervous system. Developmental Dynamics 238:708 -715, 2009.

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Effect of Gdnf haploinsufficiency on rate of migration and number of enteric neural crest‐derived cells

Cited by 22 publications

References 54 publications

Appearance of cholinergic myenteric neurons during enteric nervous system development: comparison of different ChAT fluorescent mouse reporter lines

Appearance of cholinergic myenteric neurons during enteric nervous system development: comparison of different ChAT fluorescent mouse reporter lines

Critical numbers of neural crest cells are required in the pathways from the neural tube to the foregut to ensure complete enteric nervous system formation

Cell adhesion molecule L1 affects the rate of differentiation of enteric neurons in the developing gut

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