4,806
Views
18
CrossRef citations to date
0
Altmetric
Research Article

Bifidobacterium longum alleviates irritable bowel syndrome-related visceral hypersensitivity and microbiota dysbiosis via Paneth cell regulation

ORCID Icon, ORCID Icon, , , , , , ORCID Icon, ORCID Icon, , & show all
Article: 1782156 | Received 06 Jan 2020, Accepted 03 Jun 2020, Published online: 25 Jun 2020

References

  • Chey WD, Kurlander J, Eswaran S. Irritable bowel syndrome: a clinical review. JAMA. 2015;313:949–17. doi:10.1001/jama.2015.0954.
  • Canavan C, West J, Card T. Review article: the economic impact of the irritable bowel syndrome. Aliment Pharmacol Ther. 2014;40:1023–1034. doi:10.1111/apt.12938.
  • Riba A, Olier M, Lacroix-Lamande S, Lencina C, Bacquie V, Harkat C, Gillet M, Baron M, Sommer C, Mallet V, et al. Paneth cell defects induce microbiota dysbiosis in mice and promote visceral hypersensitivity. Gastroenterology. 2017;153:1594–1606 e2. doi:10.1053/j.gastro.2017.08.044.
  • Crosnier C, Stamataki D, Lewis J. Organizing cell renewal in the intestine: stem cells, signals and combinatorial control. Nat Rev Genet. 2006;7:349–359. doi:10.1038/nrg1840.
  • Sato T, van Es JH, Snippert HJ, Stange DE, Vries RG, van den Born M, Barker N, Shroyer NF, van de Wetering M, Clevers H. Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts. Nature. 2011;469:415–418. doi:10.1038/nature09637.
  • Menard S, Forster V, Lotz M, Gutle D, Duerr CU, Gallo RL, Henriques-Normark B, Putsep K, Andersson M, Glocker EO, et al. Developmental switch of intestinal antimicrobial peptide expression. J Exp Med. 2008;205:183–193. doi:10.1084/jem.20071022.
  • Zhang Q, Pan Y, Yan R, Zeng B, Wang H, Zhang X, Li W, Wei H, Liu Z. Commensal bacteria direct selective cargo sorting to promote symbiosis. Nat Immunol. 2015;16:918–926. doi:10.1038/ni.3233.
  • Lamas B, Richard ML, Leducq V, Pham HP, Michel ML, Da Costa G, Bridonneau C, Jegou S, Hoffmann TW, Natividad JM, et al. CARD9 impacts colitis by altering gut microbiota metabolism of tryptophan into aryl hydrocarbon receptor ligands. Nat Med. 2016;22:598–605. doi:10.1038/nm.4102.
  • Bahaka D, Neut C, Khattabi A, Monget D, Gavini F. Phenotypic and genomic analyses of human strains belonging or related to Bifidobacterium longum, Bifidobacterium infantis, and Bifidobacterium breve. Int J Syst Bacteriol. 1993;43:565–573. doi:10.1099/00207713-43-3-565.
  • Zhuang X, Xiong L, Li L, Li M, Chen M. Alterations of gut microbiota in patients with irritable bowel syndrome: A systematic review and meta-analysis. J Gastroenterol Hepatol. 2017;32:28–38. doi:10.1111/jgh.13471.
  • Kerckhoffs AP, Samsom M, van der Rest ME, de Vogel J, Knol J, Ben-Amor K, Akkermans LM. Lower Bifidobacteria counts in both duodenal mucosa-associated and fecal microbiota in irritable bowel syndrome patients. World J Gastroenterol. 2009;15:2887–2892. doi:10.3748/wjg.15.2887.
  • Allen AP, Hutch W, Borre YE, Kennedy PJ, Temko A, Boylan G, Murphy E, Cryan JF, Dinan TG, Clarke G. Bifidobacterium longum 1714 as a translational psychobiotic: modulation of stress, electrophysiology and neurocognition in healthy volunteers. Transl Psychiatry. 2016;6:e939. doi:10.1038/tp.2016.191.
  • Pinto-Sanchez MI, Hall GB, Ghajar K, Nardelli A, Bolino C, Lau JT, Martin FP, Cominetti O, Welsh C, Rieder A, et al. Probiotic bifidobacterium longum ncc3001 reduces depression scores and alters brain activity: A pilot study in patients with irritable bowel syndrome. Gastroenterology. 2017;153:448–459 e8. doi:10.1053/j.gastro.2017.05.003.
  • Giannetti E, Maglione M, Alessandrella A, Strisciuglio C, De Giovanni D, Campanozzi A, Miele E, Staiano A. A mixture of 3 bifidobacteria decreases abdominal pain and improves the quality of life in children with irritable bowel syndrome: A multicenter, randomized, double-blind, placebo-controlled, crossover trial. J Clin Gastroenterol. 2017;51:e5–e10. doi:10.1097/MCG.0000000000000528.
  • Bradesi S, Schwetz I, Ennes HS, Lamy CM, Ohning G, Fanselow M, Pothoulakis C, McRoberts JA, Mayer EA. Repeated exposure to water avoidance stress in rats: a new model for sustained visceral hyperalgesia. Am J Physiol Gastrointest Liver Physiol. 2005;289:G42–53. doi:10.1152/ajpgi.00500.2004.
  • Moloney RD, O’Mahony SM, Dinan TG, Cryan JF. Stress-induced visceral pain: toward animal models of irritable-bowel syndrome and associated comorbidities. Front Psychiatry. 2015;6:15. doi:10.3389/fpsyt.2015.00015.
  • Bai T, Zhang L, Wang H, Qian W, Song J, Hou X. Fecal microbiota transplantation is effective in relieving visceral hypersensitivity in a postinfectious model. Biomed Res Int. 2018;2018:3860743. doi:10.1155/2018/3860743.
  • Ait-Belgnaoui A, Payard I, Rolland C, Harkat C, Braniste V, Theodorou V, Tompkins TA. Bifidobacterium longum and lactobacillus helveticus synergistically suppress stress-related visceral hypersensitivity through hypothalamic-pituitary-adrenal axis modulation. J Neurogastroenterol Motil. 2018;24:138–146. doi:10.5056/jnm16167.
  • Pratt C, Campbell MD. The effect of bifidobacterium on reducing symptomatic abdominal pain in patients with irritable bowel syndrome: A systematic review. Probiotics Antimicrob Proteins. 2019. doi:10.1007/s12602-019-09609-7.
  • Bron PA, Tomita S, Mercenier A, Kleerebezem M. Cell surface-associated compounds of probiotic lactobacilli sustain the strain-specificity dogma. Curr Opin Microbiol. 2013;16:262–269. doi:10.1016/j.mib.2013.06.001.
  • Spiller R, Garsed K. Postinfectious irritable bowel syndrome. Gastroenterology. 2009;136:1979–1988. doi:10.1053/j.gastro.2009.02.074.
  • Barbara G, Stanghellini V, De Giorgio R, Cremon C, Cottrell GS, Santini D, Pasquinelli G, Morselli-Labate AM, Grady EF, Bunnett NW, et al. Activated mast cells in proximity to colonic nerves correlate with abdominal pain in irritable bowel syndrome. Gastroenterology. 2004;126:693–702. doi:10.1053/j.gastro.2003.11.055.
  • Chadwick VS, Chen W, Shu D, Paulus B, Bethwaite P, Tie A, Wilson I. Activation of the mucosal immune system in irritable bowel syndrome. Gastroenterology. 2002;122:1778–1783. doi:10.1053/gast.2002.33579.
  • Goral V, Kucukoner M, Buyukbayram H. Mast cells count and serum cytokine levels in patients with irritable bowel syndrome. Hepatogastroenterology. 2010;57:751–754.
  • Thabane M, Kottachchi DT, Marshall JK. Systematic review and meta-analysis: the incidence and prognosis of post-infectious irritable bowel syndrome. Aliment Pharmacol Ther. 2007;26:535–544. doi:10.1111/j.1365-2036.2007.03399.x.
  • Bevins CL, Salzman NH. Paneth cells, antimicrobial peptides and maintenance of intestinal homeostasis. Nat Rev Microbiol. 2011;9:356–368. doi:10.1038/nrmicro2546.
  • Teltschik Z, Wiest R, Beisner J, Nuding S, Hofmann C, Schoelmerich J, Bevins CL, Stange EF, Wehkamp J. Intestinal bacterial translocation in rats with cirrhosis is related to compromised Paneth cell antimicrobial host defense. Hepatology. 2012;55:1154–1163. doi:10.1002/hep.24789.
  • Sato T, Vries RG, Snippert HJ, van de Wetering M, Barker N, Stange DE, van Es JH, Abo A, Kujala P, Peters PJ, et al. Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature. 2009;459:262–265. doi:10.1038/nature07935.
  • Jung P, Sato T, Merlos-Suarez A, Barriga FM, Iglesias M, Rossell D, Auer H, Gallardo M, Blasco MA, Sancho E, et al. Isolation and in vitro expansion of human colonic stem cells. Nat Med. 2011;17:1225–1227. doi:10.1038/nm.2470.
  • Bar-Ephraim YE, Kretzschmar K, Clevers H. Organoids in immunological research. Nat Rev Immunol. 2019. doi:10.1038/s41577-019-0248-y.
  • Han X, Lee A, Huang S, Gao J, Spence JR, Owyang C. Lactobacillus rhamnosus GG prevents epithelial barrier dysfunction induced by interferon-gamma and fecal supernatants from irritable bowel syndrome patients in human intestinal enteroids and colonoids. Gut Microbes. 2019;10:59–76. doi:10.1080/19490976.2018.1479625.
  • Zhang YG, Wu S, Xia Y, Sun J. Salmonella-infected crypt-derived intestinal organoid culture system for host-bacterial interactions. Physiol Rep. 2014:2. doi:10.14814/phy2.12147.
  • Andresen V, Gschossmann J, Layer P. Heat-inactivated Bifidobacterium bifidum MIMBb75 (SYN-HI-001) in the treatment of irritable bowel syndrome: a multicentre, randomised, double-blind, placebo-controlled clinical trial. Lancet Gastroenterol Hepatol. 2020. doi:10.1016/S2468-1253(20)30056-X.
  • Al-Chaer ED, Kawasaki M, Pasricha PJ. A new model of chronic visceral hypersensitivity in adult rats induced by colon irritation during postnatal development. Gastroenterology. 2000;119:1276–1285. doi:10.1053/gast.2000.19576.
  • Cani PD, Bibiloni R, Knauf C, Waget A, Neyrinck AM, Delzenne NM, Burcelin R. Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet-induced obesity and diabetes in mice. Diabetes. 2008;57:1470–1481. doi:10.2337/db07-1403.
  • Cani PD, Possemiers S, Van de Wiele T, Guiot Y, Everard A, Rottier O, Geurts L, Naslain D, Neyrinck A, Lambert DM, et al. Changes in gut microbiota control inflammation in obese mice through a mechanism involving GLP-2-driven improvement of gut permeability. Gut. 2009;58:1091–1103. doi:10.1136/gut.2008.165886.
  • Guglielmetti S, Tamagnini I, Minuzzo M, Arioli S, Parini C, Comelli E, Mora D. Study of the adhesion of bifidobacterium bifidum MIMBb75 to human intestinal cell lines. Curr Microbiol. 2009;59:167–172. doi:10.1007/s00284-009-9415-x.
  • Yuan J, Wang B, Sun Z, Bo X, Yuan X, He X, Zhao H, Du X, Wang F, Jiang Z, et al. Analysis of host-inducing proteome changes in bifidobacterium longum NCC2705 grown in Vivo. J Proteome Res. 2008;7:375–385. doi:10.1021/pr0704940.