Regenerative capacity of the enteric nervous system: is immaturity defining the point of no return?

Sochaczewski, Christina Oetzmann von; Wenke, Katharina; Grieve, Andrew; Westgarth-Taylor, Chris; Loveland, Jerome; Metzger, Roman; Kluth, Dietrich

doi:10.1016/j.jss.2016.09.035

Cited by 2 publications

(5 citation statements)

References 44 publications

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“…Regarding the ENS development in the proximal segment, gene expression analysis and immunohistochemistry showed an accelerated maturation and an increased number of large myenteric ganglial spaced knots. These results confirm previous data with a morphological pattern of delayed maturation in the distal segment in a rat model [ 10 ], an accelerated maturation in the proximal segment [ 6 ] and an increased number of myenteric ganglia [ 22 ]. In the literature, morphological changes involve more significantly the proximal than the distal segment ( S2 and S3 Tables) whereas the submucosal plexus appears to be more affected than the myenteric one [ 20 , 24 ].…”

Section: Discussionsupporting

confidence: 92%

“…The morphological changes previously reported in animal models ( S2 Table ) and in human atresia ( S3 Table ) seem to affect more significantly the proximal segment than the distal one. Some publications have reported a similar expression of various parameters between the distal segment and controls [ 7 , 8 , 22 – 31 ]. Recent human studies support an involvement of the proximal segment, with significant abnormalities affecting the ENS and muscle layers, to explain postnatal intestinal motility disorders [ 7 ].…”

Section: Discussionmentioning

confidence: 71%

“…Morphologically, our results confirmed the global changes previously described in several animal models [ 9 , 11 , 20 ] with a large distension of the lumen and muscle hypertrophy above the obstruction. However, the debate is still ongoing in the literature between those promoting the impairment of the proximal segment [ 21 – 22 ] and those promoting that of the distal segment [ 6 , 10 ] for explaining the postnatal pathophysiology of this condition. The morphological changes previously reported in animal models ( S2 Table ) and in human atresia ( S3 Table ) seem to affect more significantly the proximal segment than the distal one.…”

Section: Discussionmentioning

confidence: 99%

“…The prenatal natural history of intestinal obstruction in human atresia is still debated with an assumed occurrence between the second [ 8 ] and third trimester [ 35 ] of gestation. The onset is important because the regenerative potential of the ENS could be related to its degree of immaturity [ 22 ]. According to our model, the reduced number of differentially expressed genes involved in neuron and glial cell development confirms the previous assumption of a limited involvement of the ENS in motility disorders.…”

Section: Discussionmentioning

confidence: 99%

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Involvement of the enteroendocrine system in intestinal obstruction

Ballouhey¹,

Richard²,

Fourcade³

et al. 2017

PLoS ONE

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IntroductionIntestinal atresia, a rare congenital condition, is often associated with intestinal motility disorders despite adequate neonatal surgery. Previous studies have focused on changes in the enteric nervous system (ENS). We hypothesized that other components of the digestive tract could be involved in this condition.Material and methodsIn a rat model of surgically-induced intestinal obstruction, a transcriptome analysis was performed to measure the global gene expression. Then, analyzes were focused on genes expressed in ENS and neuroendocrine cells. Rat fetus small intestines at different developmental stages (ED15, ED17, ED19 and ED21, (n = 22)) were studied as controls and compared to the upper and lower segments of small intestines from rat fetuses with surgically-induced obstruction (n = 14; ligature at ED18). The gene expression pattern was confirmed by immunohistochemistry, electron microscopy and RT-qPCR.ResultsFrom ED15 to ED21, there was a physiological decrease in the gene expression of ENS markers and an increase in that of neuroendocrine genes. Regarding operated embryos, the changes in global gene expression were significantly higher in the proximal segment compared to the distal segment (18% vs. 9%). More precisely, a decrease in ENS gene expression and an increase in neuroendocrine gene expression were observed in the proximal segment compared to controls, indicating an accelerated maturation pattern. Immunohistochemistry and electron microscopy confirmed these findings.ConclusionFetal intestinal obstruction seems to induce an accelerated maturation in the proximal segment. Moreover, neuroendocrine cells undergo significant unexpected changes, suggesting that ENS changes could be associated with other changes to induce intestinal motility disorders.

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Section: Discussionsupporting

confidence: 92%

Section: Discussionmentioning

confidence: 71%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

See 2 more Smart Citations

Involvement of the enteroendocrine system in intestinal obstruction

Ballouhey¹,

Richard²,

Fourcade³

et al. 2017

PLoS ONE

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“…The underlying pathophysiology of intestinal motility disorders is considered to be mainly related to enteric nervous system impairment, and most of the recent studies with animal models have focused on enteric nervous system changes [4][5][6]. Histological assessment of specimens from patients with intestinal atresia has confirmed the presence of an impaired ENS structure in the proximal segment and delayed maturation in the distal segment [7].…”

Section: Introductionmentioning

confidence: 99%

Epithelial changes of congenital intestinal obstruction in a rat model

et al. 2020

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IntroductionIntestinal atresia is a rare congenital affliction that is often associated with severe bacterial infections despite adequate neonatal surgery. Previous studies have focused on enteric nervous system variations. We hypothesized that epithelial systems (ES) may also be involved in the pathophysiology of postnatal disorders. Materials and methodsGlobal gene expression was measured by transcriptomic analysis in a rat model of induced intestinal atresia. The analyses then focused on genes involved in ES (enterocytes and goblet cells). Rat fetus small intestines at various stages of development (ED15, ED17, ED19, and ED21, n = 22), were used as non-operated controls and compared to the upper and lower segments of rat fetus small intestines with an induced atresia (n = 14; ligature at ED18). The pattern of gene expression was then confirmed by histochemistry, electron microscopy, and RT-qPCR. ResultsFrom ED15 to ED21, the expression of several genes exhibited a physiological increase of ES markers, with a significant increase at the end of gestation. The operated embryos exhibited significantly higher variations of gene expression in the proximal segment than in the distal segment in terms of absorption and the epithelial barrier. An increase in goblet cells and markers was observed in the proximal segment compared to the controls. ConclusionFetal intestinal obstruction accelerates maturation in the proximal segment and disrupts the intestinal wall in the distal segment, with a decrease in the number of mucosal cells.

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Regenerative capacity of the enteric nervous system: is immaturity defining the point of no return?

Cited by 2 publications

References 44 publications

Involvement of the enteroendocrine system in intestinal obstruction

Involvement of the enteroendocrine system in intestinal obstruction

Epithelial changes of congenital intestinal obstruction in a rat model

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