Abstract
Several investigations have been conducted during the past years to examine the correlation between dysbiosis and both intestinal and extra-intestinal diseases such as inflammatory bowel disease (IBD) and ulcerative colitis (UC).E. coli Nissle 1917 (EcN) is a nonpathogenic gram-negative strain utilized in numerous gastrointestinal issues, consisting of diarrhea, uncomplicated diverticular malady, IBD and specifically UC. Many investigations have been done to examine the capability of assertive bacteria, inclusive of commensal and probiotic strains to enhance IBD in clinical testing. Bacterial secreted factors have been investigated to detect the EcN agents that facilitate the regulation of tight junction. These agents candiffuse smoothly through the mucin layer before reaching intestinal epithelial cells. Outer membrane vesicles (OMVs) are known as intercellular communicasomes as they facilitate the distal transfer of active compounds between cells. A few investigations have detailed immune-modulatory attributes for EcN through various systems that could be liable for its clinical viability in IBD. Today, the function of gut microbiota extracellular vesicles in health and disease has become a focus of attention as they serve as vehicles for the transmission of microorganisms to distal tissues of many bacterial effectors.
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References
Scaldaferri F, et al. Gut microbial flora, prebiotics, and probiotics in IBD: their current usage and utility. Biomed Res Int. 2013;2013:435268.
Fabrega MJ, et al. Intestinal anti-inflammatory effects of outer membrane vesicles from Escherichia coli Nissle 1917 in DSS-experimental colitis in mice. Front Microbiol. 2017;8:1274.
Grabig A, Paclik D, Guzy C, Dankof A, Baumgart DC, Erckenbrecht J, et al. Escherichia coli strain Nissle 1917 ameliorates experimental colitis via toll-like receptor 2- and toll-like receptor 4-dependent pathways. Infect Immun. 2006;74(7):4075–82.
Putignani L, et al. Gut microbiota Dysbiosis as risk and premorbid factors of IBD and IBS along the childhood-adulthood transition. Inflamm Bowel Dis. 2016;22(2):487–504.
Frank DN, et al. Disease phenotype and genotype are associated with shifts in intestinal-associated microbiota in inflammatory bowel diseases. Inflamm Bowel Dis. 2011;17(1):179–84.
Morgan XC, Tickle TL, Sokol H, Gevers D, Devaney KL, Ward DV, et al. Dysfunction of the intestinal microbiome in inflammatory bowel disease and treatment. Genome Biol. 2012;13(9):R79.
Manichanh C, Rigottier-Gois L, Bonnaud E, Gloux K, Pelletier E, Frangeul L, et al. Reduced diversity of faecal microbiota in Crohn's disease revealed by a metagenomic approach. Gut. 2006;55(2):205–11.
Dicksved J, Halfvarson J, Rosenquist M, Järnerot G, Tysk C, Apajalahti J, et al. Molecular analysis of the gut microbiota of identical twins with Crohn's disease. Isme j. 2008;2(7):716–27.
Ko JK, Auyeung KK. Inflammatory bowel disease: etiology, pathogenesis and current therapy. Curr Pharm Des. 2014;20(7):1082–96.
Qiao YQ, Cai CW, Ran ZH. Therapeutic modulation of gut microbiota in inflammatory bowel disease: more questions to be answered. J Dig Dis. 2016;17(12):800–10.
Fedorak RN. Probiotics in the management of ulcerative colitis. Gastroenterology & hepatology. 2010;6(11):688–90.
Wasilewski A, Zielińska M, Storr M, Fichna J. Beneficial effects of probiotics, prebiotics, Synbiotics, and Psychobiotics in inflammatory bowel disease. Inflamm Bowel Dis. 2015;21(7):1674–82.
Johnson-Henry KC, et al. Lactobacillus rhamnosus strain GG prevents enterohemorrhagic Escherichia coli O157:H7-induced changes in epithelial barrier function. Infect Immun. 2008;76(4):1340–8.
Liu ZH, Shen TY, Zhang P, Ma YL, Moyer MP, Qin HL. Protective effects of lactobacillus plantarum against epithelial barrier dysfunction of human colon cell line NCM460. World J Gastroenterol. 2010;16(45):5759–65.
Qin H, et al. L. plantarum prevents enteroinvasive Escherichia coli-induced tight junction proteins changes in intestinal epithelial cells. BMC Microbiol. 2009;9:63.
Chibbar R, Dieleman LA. Probiotics in the Management of Ulcerative Colitis. J Clin Gastroenterol. 2015;49(Suppl 1):S50–5.
Kruis W, et al. A double-blind placebo-controlled trial to study therapeutic effects of probiotic Escherichia coli Nissle 1917 in subgroups of patients with irritable bowel syndrome. Int J Color Dis. 2012;27(4):467–74.
Kruis W, Fric P, Pokrotnieks J, Lukás M, Fixa B, Kascák M, et al. Maintaining remission of ulcerative colitis with the probiotic Escherichia coli Nissle 1917 is as effective as with standard mesalazine. Gut. 2004;53(11):1617–23.
Henker J, et al. The probiotic Escherichia coli strain Nissle 1917 (EcN) stops acute diarrhoea in infants and toddlers. Eur J Pediatr. 2007;166(4):311–8.
Henker J, Laass MW, Blokhin BM, Maydannik VG, Bolbot YK, Elze M, et al. Probiotic Escherichia coli Nissle 1917 versus placebo for treating diarrhea of greater than 4 days duration in infants and toddlers. Pediatr Infect Dis J. 2008;27(6):494–9.
Fric P, Zavoral M. The effect of non-pathogenic Escherichia coli in symptomatic uncomplicated diverticular disease of the colon. Eur J Gastroenterol Hepatol. 2003;15(3):313–5.
Schultz M, Clinical use of E. coli Nissle. In inflammatory bowel disease. Inflamm Bowel Dis, 2008. 1917;14(7):1012–8.
Hevia A, et al. Molecular players involved in the interaction between beneficial Bacteria and the immune system. Front Microbiol. 2015;6:1285.
Sanchez B, Urdaci MC, Margolles A. Extracellular proteins secreted by probiotic bacteria as mediators of effects that promote mucosa-bacteria interactions. Microbiology. 2010;156(Pt 11):3232–42.
Hickey CA, et al. Colitogenic Bacteroides thetaiotaomicron antigens access host immune cells in a Sulfatase-dependent manner via outer membrane vesicles. Cell Host Microbe. 2015;17(5):672–80.
Carvalho AL, Fonseca S, Miquel-Clopés A, Cross K, Kok KS, Wegmann U, et al. Bioengineering commensal bacteria-derived outer membrane vesicles for delivery of biologics to the gastrointestinal and respiratory tract. J Extracell Vesicles. 2019;8(1):1632100.
Kaparakis-Liaskos M, Ferrero RL. Immune modulation by bacterial outer membrane vesicles. Nat Rev Immunol. 2015;15(6):375–87.
Shen Y, et al. Outer membrane vesicles of a human commensal mediate immune regulation and disease protection. Cell Host Microbe. 2012;12(4):509–20.
Petersen AM, et al. Treatment of inflammatory bowel disease associated E. coli with ciprofloxacin and E. coli Nissle in the streptomycin-treated mouse intestine. PLoS One. 2011;6(8):e22823.
Scaldaferri F, et al. Role and mechanisms of action of Escherichia coli Nissle 1917 in the maintenance of remission in ulcerative colitis patients: an update. World J Gastroenterol. 2016;22(24):5505–11.
Nguyen N, et al. Treatment and prevention of pouchitis after ileal pouch-anal anastomosis for chronic ulcerative colitis. Cochrane Database Syst Rev. 2019;5:Cd001176.
Hafez M, Hayes K, Goldrick M, Grencis RK, Roberts IS. The K5 capsule of Escherichia coli strain Nissle 1917 is important in stimulating expression of toll-like receptor 5, CD14, MyD88, and TRIF together with the induction of interleukin-8 expression via the mitogen-activated protein kinase pathway in epithelial cells. Infect Immun. 2010;78(5):2153–62.
Wehkamp J, et al. NF-kappaB- and AP-1-mediated induction of human beta defensin-2 in intestinal epithelial cells by Escherichia coli Nissle 1917: a novel effect of a probiotic bacterium. Infect Immun. 2004;72(10):5750–8.
Schlee M, et al. Induction of human beta-defensin 2 by the probiotic Escherichia coli Nissle 1917 is mediated through flagellin. Infect Immun. 2007;75(5):2399–407.
Wehkamp J, et al. Inducible and constitutive beta-defensins are differentially expressed in Crohn's disease and ulcerative colitis. Inflamm Bowel Dis. 2003;9(4):215–23.
Rembacken BJ, et al. Non-pathogenic Escherichia coli versus mesalazine for the treatment of ulcerative colitis: a randomised trial. Lancet. 1999;354(9179):635–9.
Ashrafian F, et al. Comparative study of effect of Akkermansia muciniphila and its extracellular vesicles on toll-like receptors and tight junction. Gastroenterol Hepatol Bed Bench. 2019;12(2):163–8.
Ashrafian F, et al. Akkermansia muciniphila-derived extracellular vesicles as a mucosal delivery vector for amelioration of obesity in mice. Front Microbiol. 2019;10:2155.
Behrouzi A, Vaziri F, Riazi Rad F, Amanzadeh A, Fateh A, Moshiri A, et al. Comparative study of pathogenic and non-pathogenic Escherichia coli outer membrane vesicles and prediction of host-interactions with TLR signaling pathways. BMC research notes. 2018;11(1):539–9.
Kulp A, Kuehn MJ. Biological functions and biogenesis of secreted bacterial outer membrane vesicles. Annu Rev Microbiol. 2010;64:163–84.
Patten DA, et al. Commensal-derived OMVs elicit a mild proinflammatory response in intestinal epithelial cells. Microbiology. 2017;163(5):702–11.
Behrouzi A, Nafari AH, Siadat SD. The significance of microbiome in personalized medicine. Clinical and translational medicine. 2019;8(1):16–6.
Natividad JM, Petit V, Huang X, de Palma G, Jury J, Sanz Y, et al. Commensal and probiotic bacteria influence intestinal barrier function and susceptibility to colitis in Nod1−/−; Nod2−/− mice. Inflamm Bowel Dis. 2012;18(8):1434–46.
Kadurugamuwa JL, Beveridge TJ. Virulence factors are released from Pseudomonas aeruginosa in association with membrane vesicles during normal growth and exposure to gentamicin: a novel mechanism of enzyme secretion. J Bacteriol. 1995;177(14):3998–4008.
Nieves W, et al. A Burkholderia pseudomallei outer membrane vesicle vaccine provides protection against lethal sepsis. Clin Vaccine Immunol. 2014;21(5):747–54.
Nokleby H, et al. Safety review: two outer membrane vesicle (OMV) vaccines against systemic Neisseria meningitidis serogroup B disease. Vaccine. 2007;25(16):3080–4.
Kang CS, Ban M, Choi EJ, Moon HG, Jeon JS, Kim DK, et al. Extracellular vesicles derived from gut microbiota, especially Akkermansia muciniphila, protect the progression of dextran sulfate sodium-induced colitis. PLoS One. 2013;8(10):e76520.
Garrido-Mesa N, Utrilla P, Comalada M, Zorrilla P, Garrido-Mesa J, Zarzuelo A, et al. The association of minocycline and the probiotic Escherichia coli Nissle 1917 results in an additive beneficial effect in a DSS model of reactivated colitis in mice. Biochem Pharmacol. 2011;82(12):1891–900.
Olier M, Marcq I, Salvador-Cartier C, Secher T, Dobrindt U, Boury M, et al. Genotoxicity of Escherichia coli Nissle 1917 strain cannot be dissociated from its probiotic activity. Gut Microbes. 2012;3(6):501–9.
Ukena SN, Singh A, Dringenberg U, Engelhardt R, Seidler U, Hansen W, et al. Probiotic Escherichia coli Nissle 1917 inhibits leaky gut by enhancing mucosal integrity. PLoS One. 2007;2(12):e1308–8.
Zyrek AA, Cichon C, Helms S, Enders C, Sonnenborn U, Schmidt MA. Molecular mechanisms underlying the probiotic effects of Escherichia coli Nissle 1917 involve ZO-2 and PKCzeta redistribution resulting in tight junction and epithelial barrier repair. Cell Microbiol. 2007;9(3):804–16.
Hering NA, Richter JF, Fromm A, Wieser A, Hartmann S, Günzel D, et al. TcpC protein from E. coli Nissle improves epithelial barrier function involving PKCzeta and ERK1/2 signaling in HT-29/B6 cells. Mucosal Immunol. 2014;7(2):369–78.
Canas MA, et al. Outer membrane vesicles from the probiotic Escherichia coli Nissle 1917 and the commensal ECOR12 enter intestinal epithelial cells via Clathrin-dependent endocytosis and elicit differential effects on DNA damage. PLoS One. 2016;11(8):e0160374.
Fabrega MJ, et al. Activation of immune and defense responses in the intestinal mucosa by outer membrane vesicles of commensal and probiotic Escherichia coli strains. Front Microbiol. 2016;7:705.
Zuo T, Ng SC. The gut microbiota in the pathogenesis and therapeutics of inflammatory bowel disease. Front Microbiol. 2018;9:2247–7.
Ewaschuk JB, et al. Secreted bioactive factors from Bifidobacterium infantis enhance epithelial cell barrier function. Am J Physiol Gastrointest Liver Physiol. 2008;295(5):G1025–34.
Martin R, et al. Faecalibacterium prausnitzii prevents physiological damages in a chronic low-grade inflammation murine model. BMC Microbiol. 2015;15:67.
Floch MH, et al. Recommendations for probiotic use-2011 update. J Clin Gastroenterol. 2011;45(Suppl):S168–71.
Altenhoefer A, Oswald S, Sonnenborn U, Enders C, Schulze J, Hacker J, et al. The probiotic Escherichia coli strain Nissle 1917 interferes with invasion of human intestinal epithelial cells by different enteroinvasive bacterial pathogens. FEMS Immunol Med Microbiol. 2004;40(3):223–9.
Kruis W, et al. Double-blind comparison of an oral Escherichia coli preparation and mesalazine in maintaining remission of ulcerative colitis. Aliment Pharmacol Ther. 1997;11(5):853–8.
Matthes H, et al. Clinical trial: probiotic treatment of acute distal ulcerative colitis with rectally administered Escherichia coli Nissle 1917 (EcN). BMC Complement Altern Med. 2010;10:13.
Malchow HA. Crohn's disease and Escherichia coli. A new approach in therapy to maintain remission of colonic Crohn's disease? J Clin Gastroenterol. 1997;25(4):653–8.
Dembiński A, et al. Synergic interaction of Rifaximin and Mutaflor (Escherichia coli Nissle 1917) in the treatment of acetic acid-induced colitis in rats. Gastroenterol Res Pract. 2016;2016:3126280–0.
Guzy C, Paclik D, Schirbel A, Sonnenborn U, Wiedenmann B, Sturm A. The probiotic Escherichia coli strain Nissle 1917 induces gammadelta T cell apoptosis via caspase- and FasL-dependent pathways. Int Immunol. 2008;20(7):829–40.
Sturm A, Rilling K, Baumgart DC, Gargas K, Abou-Ghazalé T, Raupach B, et al. Escherichia coli Nissle 1917 distinctively modulates T-cell cycling and expansion via toll-like receptor 2 signaling. Infect Immun. 2005;73(3):1452–65.
Xu XM, Zhang HJ. miRNAs as new molecular insights into inflammatory bowel disease: crucial regulators in autoimmunity and inflammation. World J Gastroenterol. 2016;22(7):2206–18.
Bian Z, et al. Role of miR-150-targeting c-Myb in colonic epithelial disruption during dextran sulphate sodium-induced murine experimental colitis and human ulcerative colitis. J Pathol. 2011;225(4):544–53.
Ye D, et al. MicroRNA regulation of intestinal epithelial tight junction permeability. Gastroenterology. 2011;141(4):1323–33.
Patton JG, et al. Biogenesis, delivery, and function of extracellular RNA. J Extracell Vesicles. 2015;4:27494.
Garcia-Contreras M, Shah SH, Tamayo A, Robbins PD, Golberg RB, Mendez AJ, et al. Plasma-derived exosome characterization reveals a distinct microRNA signature in long duration type 1 diabetes. Sci Rep. 2017;7(1):5998.
Ghosal A, Upadhyaya BB, Fritz JV, Heintz-Buschart A, Desai MS, Yusuf D, et al. The extracellular RNA complement of Escherichia coli. Microbiologyopen. 2015;4(2):252–66.
Choi JW, et al. Tiny RNAs and their voyage via extracellular vesicles: secretion of bacterial small RNA and eukaryotic microRNA. Exp Biol Med (Maywood). 2017;242(15):1475–81.
Michael A, et al. Exosomes from human saliva as a source of microRNA biomarkers. Oral Dis. 2010;16(1):34–8.
Xie Z, et al. Salivary microRNAs as promising biomarkers for detection of esophageal cancer. PLoS One. 2013;8(4):e57502.
Bryniarski K, Ptak W, Martin E, Nazimek K, Szczepanik M, Sanak M, et al. Free extracellular miRNA functionally targets cells by transfecting Exosomes from their companion cells. PLoS One. 2015;10(4):e0122991.
Stremersch S, Brans T, Braeckmans K, de Smedt S, Raemdonck K. Nucleic acid loading and fluorescent labeling of isolated extracellular vesicles requires adequate purification. Int J Pharm. 2018;548(2):783–92.
Lee H-J. Microbe-host communication by small RNAs in extracellular vesicles: vehicles for Transkingdom RNA transportation. Int J Mol Sci. 2019;20(6):1487.
Furuse Y, et al. Search for microRNAs expressed by intracellular bacterial pathogens in infected mammalian cells. PLoS One. 2014;9(9):e106434.
Ortega AD, et al. Non-coding RNA regulation in pathogenic bacteria located inside eukaryotic cells. Front Cell Infect Microbiol. 2014;4:162.
Sesto N, Koutero M, Cossart P. Bacterial and cellular RNAs at work during Listeria infection. Future Microbiol. 2014;9(9):1025–37.
Singh PP, Li L, Schorey JS. Exosomal RNA from Mycobacterium tuberculosis-infected cells is functional in recipient macrophages. Traffic. 2015;16(6):555–71.
Koeppen K, et al. A novel mechanism of host-pathogen interaction through sRNA in bacterial outer membrane vesicles. PLoS Pathog. 2016;12(6):e1005672.
Jung M, Schaefer A, Steiner I, Kempkensteffen C, Stephan C, Erbersdobler A, et al. Robust microRNA stability in degraded RNA preparations from human tissue and cell samples. Clin Chem. 2010;56(6):998–1006.
Liu S, et al. The host shapes the gut microbiota via fecal MicroRNA. Cell Host Microbe. 2016;19(1):32–43.
Ho MH, et al. Functional advantages of Porphyromonas gingivalis vesicles. PLoS One. 2015;10(4):e0123448.
Sjostrom AE, et al. Membrane vesicle-mediated release of bacterial RNA. Sci Rep. 2015;5:15329.
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We would like to thank all the personnel of Mycobacteriology and Pulmonary Research Department, Pasteur Institute of Iran, for their assistance in this project.
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AB, HM and ZHT wrote the main manuscript text. AB design of Fig. SF edit of manuscript. SD and AM edit of final manuscript. All authors read and approve final manuscript.
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Behrouzi, A., Mazaheri, H., Falsafi, S. et al. Intestinal effect of the probiotic Escherichia coli strain Nissle 1917 and its OMV. J Diabetes Metab Disord 19, 597–604 (2020). https://doi.org/10.1007/s40200-020-00511-6
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DOI: https://doi.org/10.1007/s40200-020-00511-6