Dysbiosis of intestinal microbiota and decrease in paneth cell antimicrobial peptide level during acute necrotizing pancreatitis in rats

Chen, Jing; Huang, Chen; Wang, Jingjing; Zhou, Hui; Lǚ, Yingying; Lou, Lihong; Zheng, Jie; Tian, Ling; Wang, Xingpeng; Cao, Zhongwei; Zeng, Yue

doi:10.1371/journal.pone.0176583

Cited by 92 publications

(90 citation statements)

References 35 publications

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“…3A). We also found that E. coli MG1655, which is a commensal E. coli K-12-derived strain, may be associated with intestinal pathological situations (4)(5)(6). By qPCR, we demonstrated a marked increase of E. coli MG1655 in AP patients (P Ͻ 0.05) (Fig.…”

Section: Figsupporting

confidence: 52%

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Commensal Escherichia coli Aggravates Acute Necrotizing Pancreatitis through Targeting of Intestinal Epithelial Cells

Zheng

Lou

Fan

et al. 2019

Appl Environ Microbiol

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An increase of Escherichia-Shigella was previously reported in acute necrotizing pancreatitis (ANP). We investigated whether Escherichia coli MG1655, an Escherichia commensal organism, increased intestinal injury and aggravated ANP in rats. ANP was induced by retrograde injection of 3.5% sodium taurocholate into the biliopancreatic duct. Using gut microbiota-depleted rats, we demonstrated that gut microbiota was involved in the pancreatic injury and intestinal barrier dysfunction in ANP. Using 16S rRNA gene sequencing and quantitative PCR, we found intestinal dysbiosis and a significant increase of E. coli MG1655 in ANP. Afterward, administration of E. coli MG1655 by gavage to gut microbiota-depleted rats with ANP was performed. We observed that after ANP induction, E. coli MG1655-monocolonized rats presented more severe injury in the pancreas and intestinal barrier function than gut microbiota-depleted rats. Furthermore, Toll-like receptor 4 (TLR4)/MyD88/p38 mitogen-activated protein (MAPK) and endoplasmic reticulum stress (ERS) activation in intestinal epithelial cells were also increased more significantly in the MG1655-monocolonized ANP rats. In vitro, the rat ileal epithelial cell line IEC-18 displayed aggravated tumor necrosis factor alpha-induced inflammation and loss of tight-junction proteins in coculture with E. coli MG1655, as well as TLR4, MyD88, and Bip upregulation. In conclusion, our study shows that commensal E. coli MG1655 increases TLR4/MyD88/p38 MAPK and ERS signaling-induced intestinal epithelial injury and aggravates ANP in rats. Our study also describes the harmful potential of commensal E. coli in ANP. IMPORTANCE This study describes the harmful potential of commensal E. coli in ANP, which has not been demonstrated in previous studies. Our work provides new insights into gut bacterium-ANP cross talk, suggesting that nonpathogenic commensals could also exhibit adverse effects in the context of diseases.

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Section: Figsupporting

confidence: 52%

“…Our previous research showed that ANP induced ileal inflammation and increased intestinal permeability in rats, as well as an alteration of gut microbiota and a significantly higher abundance of Escherichia-Shigella by 16S rRNA sequencing (4). In the genus Escherichia, Escherichia coli MG1655 is a commensal, nonpathogenic strain.…”

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confidence: 99%

Commensal Escherichia coli Aggravates Acute Necrotizing Pancreatitis through Targeting of Intestinal Epithelial Cells

Zheng

Lou

Fan

et al. 2019

Appl Environ Microbiol

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“…Inflammatory effectors are activated by intestinal bacteria and toxins, releasing cytokines and inflammatory mediators, which in turn further stimulates serious systemic inflammation and aggravates intestinal mucosal damage (14). DAO is an important indicator for measuring intestinal mucosal damage, and a reduction in DAO indicates that the integrity of the intestinal mucosa is destroyed (33). Lactulose is a disaccharide with a molecular weight of 342, and mannitol is a monosaccharide with a molecular weight of 182.…”

Section: Discussionmentioning

confidence: 99%

Protective effect of emodin on intestinal epithelial tight junction barrier integrity in rats with sepsis induced by cecal ligation and puncture

Guo

Zhang

et al. 2020

Exp Ther Med

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Αbstract. The present study investigated the protective effects of emodin on intestinal epithelial tight junction (TJ) barrier integrity in cecal ligation and puncture (CLP)-induced septic rats and its possible mechanisms of action. Healthy male Sprague-Dawley rats were randomly divided into three groups (n=20 per group): Sham group, CLP group and CLP + emodin group. Animals were sacrificed at 12 and 24 h after the model was established. Abdominal aortic blood and specimens of the ileum were harvested for analysis. The histopathological changes in intestinal mucosa and the ultrastructures of intestinal epithelial cells were investigated using light microscopy and transmission electron microscopy. The integrity of the intestinal barrier was assessed by examining plasma diamine oxidase (DAO) levels and the ratio of urine lactulose to mannitol (L/M). The levels of the intestinal TJ proteins claudin-3, zonula occludens (ZO)-1 and occludin were detected using immunohistochemistry, western blotting and reverse transcription-quantitative PCR. The results showed that the pathological damage to intestinal mucosa and the intestinal tissue injury score in the CLP + emodin group were significantly reduced compared to those of the CLP group, and the differences were more obvious at 24 h compared with 12 h. DAO activity and the L/M ratio in the emodin pre-treatment group decreased significantly at 24 h compared with the CLP groups. The protein and mRNA levels of the TJ proteins claudin-3, ZO-1 and occludin in the emodin pre-treatment groups at 12 and 24 h were increased, while occludin mRNA level was found to be decreased compared with the CLP groups. The present study suggested that emodin may significantly reduce the damage to the intestinal epithelial barrier in sepsis, inhibit intestinal barrier permeability and protect intestinal barrier integrity. Emodin may protect intestinal barrier integrity by elevating expression levels of the TJ proteins claudin-3, ZO-1 and occludin in CLP rats.

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“…Another explanation for the presence of intestinal bacteria in PF fluid after DP may be bacterial translocation, an event known to occur during acute or chronic pancreatitis. Infection of peripancreatic collections during acute pancreatitis is ascribed to such a translocation process from the surrounding intestinal loops, such as colon.…”

Section: Discussionmentioning

confidence: 99%

Association of bacteria in pancreatic fistula fluid with complications after pancreatic surgery

et al. 2020

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Background: Pancreatic fistula (PF) is a common complication after pancreatic surgery. It is unclear how microbes in PF fluid affect outcomes and which microbes are present after pancreatoduodenectomy (PD) and distal pancreatectomy (DP). The aim of this study was to compare the microbiological spectrum of PF fluid after PD versus DP, and its association with postoperative complications. Methods: Bacterial strains and antibiotic resistance rates of bacterial swabs obtained from the PF fluid of patients who underwent DP or PD were analysed. Cultured bacteria were classified as Enterobacterales and as 'other intestinal and non-intestinal microorganisms' based on whether they are typically part of the normal human intestinal flora. Results: A total of 847 patients had a pancreatic resection (PD 600; DP 247) between July 2007 and December 2016. Clinically relevant PF was detected in 131 patients (15⋅5 per cent). Bacterial swabs were obtained from 108 patients (DP 47; PD 61), of which 19 (17⋅6 per cent) were sterile. Enterobacterales were detected in 74 per cent of PF fluid swabs after PD, and in 34 per cent after DP. Infected, polymicrobial or multidrug-resistant PF fluid was more common after PD (rates of 95, 50 and 48 per cent respectively) than after DP (66, 26 and 6 per cent respectively). Patients with higher grade complications (Clavien-Dindo grade IV-V) or grade C PF had more Enterobacterales and multidrug-resistant Enterobacterales in the PF fluid after DP. Conclusion: Enterobacterales and multidrug-resistant bacteria are detected frequently after PD and DP, and are associated with more severe complications and PF in patients undergoing DP.

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Dysbiosis of intestinal microbiota and decrease in paneth cell antimicrobial peptide level during acute necrotizing pancreatitis in rats

Cited by 92 publications

References 35 publications

Commensal Escherichia coli Aggravates Acute Necrotizing Pancreatitis through Targeting of Intestinal Epithelial Cells

Commensal Escherichia coli Aggravates Acute Necrotizing Pancreatitis through Targeting of Intestinal Epithelial Cells

Protective effect of emodin on intestinal epithelial tight junction barrier integrity in rats with sepsis induced by cecal ligation and puncture

Association of bacteria in pancreatic fistula fluid with complications after pancreatic surgery

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