Butyrate promotes visceral hypersensitivity in an <scp>IBS</scp>‐like model via enteric glial cell‐derived nerve growth factor

Long, Xin; Li, M.; Li, L.-X.; Sun, Yiyuan; Zhang, W.-X.; Zhao, Dong; Li, Y.-Q.

doi:10.1111/nmo.13227

Cited by 48 publications

(37 citation statements)

References 50 publications

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“…For example, one previous study reported that IBS-D patients had higher n-butyrate concentration, 35 and other studies found that rectal instillation of butyrate to Sprague-Dawley rats resulted in a sustained decrease in their pain threshold. 36,37 A number of reasons have been proposed for these conflicts, including reduced absorption of butyrate due to increased motility and shorter transit times, 38 the amount of butyrate administered, the source of butyrate, the timing of butyrate administration, and the differences between the in vivo and in vitro environments. 12 An impaired intestinal barrier may allow for pathogen invasion, and luminal commensal bacteria can also affect the barrier in various ways.…”

Section: Discussionmentioning

confidence: 99%

Beneficial effect of butyrate‐producing Lachnospiraceae on stress‐induced visceral hypersensitivity in rats

Zhang

Song

Wang

et al. 2018

J of Gastro and Hepatol

206

157

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Background and Aim Emerging evidence indicates that psychological stress is involved in the pathogenesis of irritable bowel syndrome, which is characterized by visceral hypersensitivity and may be accompanied by gut dysbiosis. However, how such stress contributes to the development of visceral hypersensitivity is incompletely understood. Here, we aimed to investigate the influence that stress‐induced microbial changes exert on visceral sensitivity, as well as the possible underlying mechanisms associated with this effect. Methods Male Sprague–Dawley rats underwent chronic water avoidance stress (WAS) to induce visceral hypersensitivity. Visceral sensitivity, colonic tight junction protein expression, and short‐chain fatty acids of cecal contents were measured. Fecal samples were collected to characterize microbiota profiles. In a separate study, oral gavage of Roseburia in WAS rats was conducted to verify its potential role in the effectiveness on visceral hypersensitivity. Results Repeated WAS caused visceral hypersensitivity, altered fecal microbiota composition and function, and decreased occludin expression in the colon. Stressed rats exhibited reduced representation of pathways involved in the metabolism of butyrate and reduced abundance of several operational taxonomic units associated with butyrate‐producing bacteria, such as Lachnospiraceae. Consistently, supplementation with Roseburia hominis, a species belonging to Lachnospiraceae, significantly increased cecal butyrate content. Moreover, Roseburia supplementation alleviated visceral hypersensitivity and prevented the decreased expression of occludin. Conclusions Reduction in the abundance of butyrate‐producing Lachnospiraceae, which is beneficial for the intestinal barrier, was involved in the formation of visceral hypersensitivity. R. hominis is a potential probiotic for treating stress‐induced visceral hypersensitivity.

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Section: Discussionmentioning

confidence: 99%

Beneficial effect of butyrate‐producing Lachnospiraceae on stress‐induced visceral hypersensitivity in rats

Zhang

Song

Wang

et al. 2018

J of Gastro and Hepatol

206

157

View full text Add to dashboard Cite

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“…14 (Table 1). 10,12,15,16 NGF level is elevated in the colonic mucosa of patients with IBS, 17,18 and increased expression of NGF is correlated with visceral hypersensitivity in these patients. 18 The mechanisms of NGF action on visceral sensation are not completely understood.…”

Section: Neurotrophi C Fac Tor S and Viscer Al S Ens Itivit Ymentioning

confidence: 97%

“…NGF, by interacting with the primary afferent nerves, contributes to the development of visceral hypersensitivity in several animal models, such as trinitrobenzene sulfonic acid (TNBS), butyrate, neonatal maternal deprivation, chronic stress, and bowel obstruction . Several cell types in the digestive tract are known to produce and release NGF, such as intestinal epithelial cells, mast cells, enteric neurons, enteric glial cells, and smooth muscle cells (Table ) . NGF level is elevated in the colonic mucosa of patients with IBS, and increased expression of NGF is correlated with visceral hypersensitivity in these patients …”

Section: Neurotrophic Factors and Visceral Sensitivitymentioning

confidence: 99%

“…There is an increasing body of evidence suggesting that neurotrophins, particularly NGF and BDNF, are involved in abdominal pain. NGF, by interacting with the primary afferent nerves, contributes to the development of visceral hypersensitivity in several animal models, such as trinitrobenzene sulfonic acid (TNBS), 8,9 butyrate, 10,11 neonatal maternal deprivation, 12 chronic stress, 13 and bowel obstruction. 14 (Table 1).…”

Section: Neurotrophi C Fac Tor S and Viscer Al S Ens Itivit Ymentioning

confidence: 99%

“…BDNF expression in the Caco-2 cell culture is increased following IBS-D fecal supernatant treatment 3,26,31 GDNF Rat Ileum Enteric glial cells Ischemia reperfusion upregulates GDNF expression by the enteric glial cells in the rat ileum, which helps to maintain intestinal barrier function. GDNF level is elevated in the rat ileum during the early stage of diabetes, which protects enteric neurons from hyperglycemia-induced cellular damage 38,41 Human Ileum Enteric glial cells and enterocytes, HT29B6 and Caco-2 cell lines GDNF activates the Ret/GFRα receptor complex and contributes to epithelial barrier stabilization 5 NGF Rat Jejunum, ileum, and colon Epithelial cells, mast cells, smooth muscle cells, enteric neurons and glial cells Many factors can increase NGF expression and release in the gut, including but not limited to: gut infection, gut inflammation, mechanical distension of the gut wall, neonatal maternal separation, diabetes 6,10,12,[14][15][16]35,41 Human Colon Immune cells in the lamina propria NGF expression is elevated in the colonic mucosa from IBS patients, which may contribute to visceral hypersensitivity and impaired gut barrier function in these patients 17,18 NT−3…”

Section: Neurotrophi C Fac Tor S and Viscer Al S Ens Itivit Ymentioning

confidence: 99%

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Neurotrophic factors in enteric physiology and pathophysiology

Liu

2018

Neurogastroenterology Motil

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Neurotrophic factors are traditionally recognized for their roles in differentiation, growth, and survival of specific neurons in the central and peripheral nervous system. Some neurotrophic factors are essential for the development and migration of the enteric nervous system along the fetal and post-natal gut. Over the last two decades, several non-developmental functions of neurotrophic factors have been characterized. In the adult gastrointestinal tract, neurotrophic factors regulate gut sensation, motility, epithelial barrier function, and protect enteric neurons and glial cells from damaging insults in the microenvironment of the gut. In this issue of Neurogastroenterology and Motility, Fu et al. demonstrate that brain-derived neurotrophic factor plays a role in the pathogenesis of distention-induced abdominal pain in bowel obstruction. In light of this interesting finding, this mini-review highlights some of the recent advances in understanding of the physiological and pathophysiological roles of neurotrophic factors in the adult gut.

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Enteric Glia: S100, GFAP, and Beyond

Grundmann

Loris

Maas-Omlor

et al. 2019

The Anatomical Record

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Since several years, the enteric nervous system (ENS) is getting more and more in the focus of gastrointestinal research. While the main interest was credited for years to the enteric neurons and their functional properties, less attention has been paid on the enteric glial cells (EGCs). Although the similarity of EGCs to central nervous system (CNS) astrocytes has been demonstrated a long time ago, EGCs were investigated in more detail only recently. Similar to the CNS, there is not "the" EGC, but also a broad range of diversity. Based on morphology and protein expression, such as glial fibrillary acidic protein (GFAP), S100, or Proteolipid-protein-1 (PLP1), several distinct glial types can be differentiated. Their heterogeneity in morphology, localization, and transcription as well as interaction with surrounding cells indicate versatile functional properties of these cells for gut function in health and disease. Although NG2 is found in a subset of CNS glial cells, it did not colocalize with the glial marker S100 or GFAP in the ENS. Instead, it in part colocalize with PDGFRα, as it does in the CNS, which do stain fibroblast-like cells in the gastrointestinal tract. Moreover, there seem to be species dependent differences. While GFAP is always found in the rodent ENS, this is completely different for the human gut.Only the compromised human ENS shows a significant amount of GFAPpositive glial cells. So, in general we can conclude that the EGC population is species specific and as complex as CNS glia. Anat Rec, 302:1333Rec, 302: -1344Rec, 302: , 2019.

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Butyrate promotes visceral hypersensitivity in an IBS‐like model via enteric glial cell‐derived nerve growth factor

Abstract: Butyrate-EGC interplay may play a pivotal role in regulation of NGF expression and the development of colonic hypersensitivity in IBS-like animal model.

Cited by 48 publications

References 50 publications

Beneficial effect of butyrate‐producing Lachnospiraceae on stress‐induced visceral hypersensitivity in rats

Beneficial effect of butyrate‐producing Lachnospiraceae on stress‐induced visceral hypersensitivity in rats

Neurotrophic factors in enteric physiology and pathophysiology

Enteric Glia: S100, GFAP, and Beyond

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