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

被引:233
作者
Zhang, Jindong [1 ]
Song, Lijin [1 ]
Wang, Yujing [2 ]
Liu, Chang [2 ]
Zhang, Lu [1 ]
Zhu, Shiwei [1 ]
Liu, Shuangjiang [2 ]
Duan, Liping [1 ]
机构
[1] Peking Univ, Hosp 3, Dept Gastroenterol, Beijing 100191, Peoples R China
[2] Chinese Acad Sci, State Key Lab Microbial Resources, Inst Microbiol, Beijing, Peoples R China
基金
中国国家自然科学基金;
关键词
butyrate; intestinal barrier; microbiota; stress; visceral hypersensitivity; CHAIN FATTY-ACIDS; IRRITABLE-BOWEL-SYNDROME; GUT MICROBIOTA; HUMAN FECES; MODEL; FERMENTATION; BACTERIA; MARKER; PAIN;
D O I
10.1111/jgh.14536
中图分类号
R57 [消化系及腹部疾病];
学科分类号
摘要
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.
引用
收藏
页码:1368 / 1376
页数:9
相关论文
共 41 条
[1]   Effects of Rifaximin on Transit, Permeability, Fecal Microbiome, and Organic Acid Excretion in Irritable Bowel Syndrome [J].
Acosta, Andres ;
Camilleri, Michael ;
Shin, Andrea ;
Nord, Sara Linker ;
O'Neill, Jessica ;
Gray, Amber V. ;
Lueke, Alan J. ;
Donato, Leslie J. ;
Burton, Duane D. ;
Szarka, Lawrence A. ;
Zinsmeister, Alan R. ;
Golden, Pamela L. ;
Fodor, Anthony .
CLINICAL AND TRANSLATIONAL GASTROENTEROLOGY, 2016, 7
[2]   A new model of chronic visceral hypersensitivity in adult rats induced by colon irritation during postnatal development [J].
Al-Chaer, ED ;
Kawasaki, M ;
Pasricha, PJ .
GASTROENTEROLOGY, 2000, 119 (05) :1276-1285
[3]   Exposure to a social stressor alters the structure of the intestinal microbiota: Implications for stressor-induced immunomodulation [J].
Bailey, Michael T. ;
Dowd, Scot E. ;
Galley, Jeffrey D. ;
Hufnagle, Amy R. ;
Allen, Rebecca G. ;
Lyte, Mark .
BRAIN BEHAVIOR AND IMMUNITY, 2011, 25 (03) :397-407
[4]   Microencapsulated sodium butyrate reduces the frequency of abdominal pain in patients with irritable bowel syndrome [J].
Banasiewicz, T. ;
Krokowicz, L. ;
Stojcev, Z. ;
Kaczmarek, B. F. ;
Kaczmarek, E. ;
Maik, J. ;
Marciniak, R. ;
Krokowicz, P. ;
Walkowiak, J. ;
Drews, M. .
COLORECTAL DISEASE, 2013, 15 (02) :204-209
[5]   Neutralization of IL-8 Prevents the Induction of Dermatologic Adverse Events Associated with the Inhibition of Epidermal Growth Factor Receptor [J].
Bangsgaard, Nannie ;
Houtkamp, Mischa ;
Schuurhuis, Danita H. ;
Parren, Paul W. H. I. ;
Baadsgaard, Ole ;
Niessen, Hans W. M. ;
Skov, Lone .
PLOS ONE, 2012, 7 (06)
[6]   Structural & functional consequences of chronic psychosocial stress on the microbiome & host [J].
Bharwani, Aadil ;
Mian, M. Firoz ;
Foster, Jane A. ;
Surette, Michael G. ;
Bienenstock, John ;
Forsythe, Paul .
PSYCHONEUROENDOCRINOLOGY, 2016, 63 :217-227
[7]   Rectal instillation of butyrate provides a novel clinically relevant model of noninflammatory colonic hypersensitivity in rats [J].
Bourdu, S ;
Dapoigny, M ;
Chapuy, E ;
Artigue, F ;
Vasson, MP ;
Dechelotte, P ;
Bommelaer, G ;
Eschalier, A ;
Ardid, D .
GASTROENTEROLOGY, 2005, 128 (07) :1996-2008
[8]   The regulation of intestinal mucin MUC2 expression by short-chain fatty acids: implications for epithelial protection [J].
Burger-van Paassen, Nanda ;
Vincent, Audrey ;
Puiman, Patrycja J. ;
van der Sluis, Maria ;
Bouma, Janneke ;
Boehm, Gunther ;
van Goudoever, Johannes B. ;
Van Seuningen, Isabelle ;
Renes, Ingrid B. .
BIOCHEMICAL JOURNAL, 2009, 420 :211-219
[9]   Functional dysbiosis within the gut microbiota of patients with constipated-irritable bowel syndrome [J].
Chassard, C. ;
Dapoigny, M. ;
Scott, K. P. ;
Crouzet, L. ;
Del'homme, C. ;
Marquet, P. ;
Martin, J. C. ;
Pickering, G. ;
Ardid, D. ;
Eschalier, A. ;
Dubray, C. ;
Flint, H. J. ;
Bernalier-Donadille, A. .
ALIMENTARY PHARMACOLOGY & THERAPEUTICS, 2012, 35 (07) :828-838
[10]   Antigen Delivery to Macrophages Using Liposomal Nanoparticles Targeting Sialoadhesin/CD169 [J].
Chen, Weihsu C. ;
Kawasaki, Norihito ;
Nycholat, Corwin M. ;
Han, Shoufa ;
Pilotte, Julie ;
Crocker, Paul R. ;
Paulson, James C. .
PLOS ONE, 2012, 7 (06)