Nerve growth factor mediates alterations of colonic sensitivity and mucosal barrier induced by neonatal stress in rats

Barreau, Frédérick; Cartier, Christel; Ferrier, Laurent; Fioramonti, Jean; Buéno, Lionel

doi:10.1053/j.gastro.2004.05.019

Cited by 155 publications

(213 citation statements)

References 51 publications

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“…6,34 Glucocorticoids play a role in the increased intestinal permeability induced by a short acute maternal separation stress in PND10 pups 17 but not in adult rats subjected to repeated maternal separation. 36,37 In the present study, we found no correlation between corticosterone plasma levels and intestinal permeability at weaning, either in LNS or BMS models, suggesting that glucocorticoids are not involved in the mechanisms contributing to the altered permeability. Peripheral corticotropin-releasing factor receptors and nerve growth factors have been identified as major underlying mechanisms of the enhanced intestinal permeability in adult rats exposed to intermittent maternal separation post-natally.…”

Section: Discussioncontrasting

confidence: 68%

“…Peripheral corticotropin-releasing factor receptors and nerve growth factors have been identified as major underlying mechanisms of the enhanced intestinal permeability in adult rats exposed to intermittent maternal separation post-natally. 36,37 Whether similar mechanisms are implicated in the increased permeability during the developmental period at weaning need to be further investigated. Intestinal barrier disruption has been described to occur in IBS patients, [38][39][40][41] although the link between early adverse life events and increased intestinal permeability needs to be evaluated based on the present experimental data.…”

Section: Discussionmentioning

confidence: 99%

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Chronic Early-life Stress in Rat Pups Alters Basal Corticosterone, Intestinal Permeability, and Fecal Microbiota at Weaning: Influence of Sex

Moussaoui

Jacobs

Larauche

et al. 2017

J Neurogastroenterol Motil

103

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Background/AimsWistar rat dams exposed to limited nesting stress (LNS) from post-natal days (PND) 2 to 10 display erratic maternal behavior, and their pups show delayed maturation of the hypothalamic-pituitary-adrenal axis and impaired epithelial barrier at PND10 and a visceral hypersensitivity at adulthood. Little is known about the impact of early life stress on the offspring before adulthood and the influence of sex. We investigated whether male and female rats previously exposed to LNS displays at weaning altered corticosterone, intestinal permeability, and microbiota. MethodsWistar rat dams and litters were maintained from PND2 to 10 with limited nesting/bedding materials and thereafter reverted to normal housing up to weaning (PND21). Control litters had normal housing. At weaning, we monitored body weight, corticosterone plasma levels (enzyme immunoassay), in vivo intestinal to colon permeability (fluorescein isothiocyanate-dextran 4 kDa) and fecal microbiota (DNA extraction and amplification of the V4 region of the 16S ribosomal RNA gene). ResultsAt weaning, LNS pups had hypercorticosteronemia and enhanced intestinal permeability with females > males while body weights were similar. LNS decreased fecal microbial diversity and induced a distinct composition characterized by increased abundance of Gram positive cocci and reduction of fiber-degrading, butyrate-producing, and mucus-resident microbes. ConclusionsThese data indicate that chronic exposure to LNS during the first week post-natally has sustained effects monitored at weaning including hypercorticosteronemia, a leaky gut, and dysbiosis. These alterations may impact on the susceptibility to develop visceral hypersensitivity in adult rats and have relevance to the development of irritable bowel syndrome in childhood.

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Section: Discussioncontrasting

confidence: 68%

Section: Discussionmentioning

confidence: 99%

Chronic Early-life Stress in Rat Pups Alters Basal Corticosterone, Intestinal Permeability, and Fecal Microbiota at Weaning: Influence of Sex

Moussaoui

Jacobs

Larauche

et al. 2017

J Neurogastroenterol Motil

103

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“…stress; colonic; barrier THE NEONATAL PERIOD is an important developmental period in humans and rodents, and stress during this time can have long-lasting effects on behavior and physiology. Maternal separation (MS) is a well-characterized model of early life stress used in the study of anxiety and depression (17, 31) as well as intestinal dysfunction (1,2,7,28,37). The physiological response to stress is controlled by the hypothalamicpituitary adrenal (HPA) axis, which develops during the neonatal period.…”

mentioning

confidence: 99%

“…Maternal separation (MS) is a well-characterized model of early life stress used in the study of anxiety and depression (17,31) as well as intestinal dysfunction (1,2,7,28,37). The physiological response to stress is controlled by the hypothalamicpituitary adrenal (HPA) axis, which develops during the neonatal period.…”

mentioning

confidence: 99%

Neonatal maternal separation of rat pups results in abnormal cholinergic regulation of epithelial permeability

Gareau

Jury

Perdue

2007

American Journal of Physiology-Gastrointestinal and Liver Physi

126

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Gareau MG, Jury J, Perdue MH. Neonatal maternal separation of rat pups results in abnormal cholinergic regulation of epithelial permeability. Am J Physiol Gastrointest Liver Physiol 293: G198-G203, 2007. First published May 17, 2007; doi:10.1152/ajpgi.00392.2006.-Neonatal maternal separation (MS) predisposes adult rats to develop stressinduced mucosal barrier dysfunction/visceral hypersensitivity and rat pups to develop colonic epithelial dysfunction. Our aim was to examine if enhanced epithelial permeability in such pups resulted from abnormal regulation by enteric nerves. Pups were separated from the dam for 3 h/day (days 4 -20); nonseparated (NS) pups served as controls. On day 20, colonic tissues were removed and mounted in Ussing chambers. Horseradish peroxidase (HRP) flux was used to measure macromolecular permeability. HRP flux was increased in MS versus NS pups. The enhanced flux was inhibited by the cholinergic muscarinic antagonist atropine and the nicotinic antagonist hexamethonium. The cholinergic component was greater in tissues from MS versus NS pups, suggesting that increased cholinergic activity was responsible for the MS elevated permeability. Western blots and immunohistochemistry of colonic tissues demonstrated increased expression of choline acetyltransferase (ChAT) in MS pups, indicating greater synthesis of acetylcholine. Since a previous study indicated that corticotrophin-releasing factor (CRF) mediates barrier dysfunction in MS pups, we examined if the two pathways were linked. In MS tissues, nonselective CRF receptor antagonism inhibited the enhanced flux, and the addition of atropine did not produce further inhibition. Using selective receptor antagonists, we identified that CRF receptor 2 was involved in mediating this effect. These findings suggest that CRF, via CRF receptor 2, acts on cholinergic nerves to induce epithelial barrier dysfunction. Our study provides evidence that MS stimulates synthesis of acetylcholine, which, together with released CRF, creates a condition conducive to the development of epithelial barrier defects. stress; colonic; barrier THE NEONATAL PERIOD is an important developmental period in humans and rodents, and stress during this time can have long-lasting effects on behavior and physiology. Maternal separation (MS) is a well-characterized model of early life stress used in the study of anxiety and depression (17, 31) as well as intestinal dysfunction (1,2,7,28,37). The physiological response to stress is controlled by the hypothalamicpituitary adrenal (HPA) axis, which develops during the neonatal period. Exposure to stress during this time results in the formation of a dysregulated axis with a compromised ability to downregulate the synthesis of corticotrophin-releasing factor (CRF), a key stress hormone (26).Adult rats of a stress susceptible strain that are subjected to daily separation from the dam during the neonatal period demonstrate increased colonic permeability (2) and visceral hyperalgesia (28). Adult rats that are not genetically susceptible t...

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“…One quite widely used model of early life stress is maternal separation in rodents. Several groups have reported that stress introduces long lasting hyperactivity of the HPA-axis [157][158][159][160][161][162][163], anxiety-like behavior [161,[164][165][166][167][168], visceral hypersensitivity [166,[169][170][171] and altered cholinergic activity in the gut [172,173] accompanied by increased intestinal permeability [163,172,174,175].…”

Section: B) Neurodegenerative Illnessmentioning

confidence: 99%

Commensal Bugs from the Gut-Shaping Human Health and Disease

Chowdhury¹

2014

JIG

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Nerve growth factor mediates alterations of colonic sensitivity and mucosal barrier induced by neonatal stress in rats

Cited by 155 publications

References 51 publications

Chronic Early-life Stress in Rat Pups Alters Basal Corticosterone, Intestinal Permeability, and Fecal Microbiota at Weaning: Influence of Sex

Chronic Early-life Stress in Rat Pups Alters Basal Corticosterone, Intestinal Permeability, and Fecal Microbiota at Weaning: Influence of Sex

Neonatal maternal separation of rat pups results in abnormal cholinergic regulation of epithelial permeability

Commensal Bugs from the Gut-Shaping Human Health and Disease

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