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Intestinal effect of the probiotic Escherichia coli strain Nissle 1917 and its OMV

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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

  1. Scaldaferri F, et al. Gut microbial flora, prebiotics, and probiotics in IBD: their current usage and utility. Biomed Res Int. 2013;2013:435268.

    Article  PubMed  PubMed Central  Google Scholar 

  2. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  3. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. 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.

    Article  PubMed  Google Scholar 

  5. 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.

    Article  PubMed  Google Scholar 

  6. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. 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.

    Article  CAS  PubMed  Google Scholar 

  9. Ko JK, Auyeung KK. Inflammatory bowel disease: etiology, pathogenesis and current therapy. Curr Pharm Des. 2014;20(7):1082–96.

  10. 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.

    Article  PubMed  Google Scholar 

  11. Fedorak RN. Probiotics in the management of ulcerative colitis. Gastroenterology & hepatology. 2010;6(11):688–90.

    Google Scholar 

  12. 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.

    Article  PubMed  Google Scholar 

  13. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Qin H, et al. L. plantarum prevents enteroinvasive Escherichia coli-induced tight junction proteins changes in intestinal epithelial cells. BMC Microbiol. 2009;9:63.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  16. Chibbar R, Dieleman LA. Probiotics in the Management of Ulcerative Colitis. J Clin Gastroenterol. 2015;49(Suppl 1):S50–5.

    Article  CAS  PubMed  Google Scholar 

  17. 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.

    Article  Google Scholar 

  18. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  20. 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.

    Article  PubMed  Google Scholar 

  21. 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.

    Article  PubMed  Google Scholar 

  22. Schultz M, Clinical use of E. coli Nissle. In inflammatory bowel disease. Inflamm Bowel Dis, 2008. 1917;14(7):1012–8.

    Article  Google Scholar 

  23. Hevia A, et al. Molecular players involved in the interaction between beneficial Bacteria and the immune system. Front Microbiol. 2015;6:1285.

    Article  PubMed  PubMed Central  Google Scholar 

  24. 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.

    Article  CAS  PubMed  Google Scholar 

  25. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Kaparakis-Liaskos M, Ferrero RL. Immune modulation by bacterial outer membrane vesicles. Nat Rev Immunol. 2015;15(6):375–87.

    Article  CAS  PubMed  Google Scholar 

  28. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. 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.

    PubMed  Google Scholar 

  32. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. 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.

    Article  PubMed  Google Scholar 

  36. 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.

    Article  CAS  PubMed  Google Scholar 

  37. 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.

    PubMed  PubMed Central  Google Scholar 

  38. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  39. 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.

  40. Kulp A, Kuehn MJ. Biological functions and biogenesis of secreted bacterial outer membrane vesicles. Annu Rev Microbiol. 2010;64:163–84.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Patten DA, et al. Commensal-derived OMVs elicit a mild proinflammatory response in intestinal epithelial cells. Microbiology. 2017;163(5):702–11.

    Article  CAS  PubMed  Google Scholar 

  42. Behrouzi A, Nafari AH, Siadat SD. The significance of microbiome in personalized medicine. Clinical and translational medicine. 2019;8(1):16–6.

  43. 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.

    Article  PubMed  Google Scholar 

  44. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Nieves W, et al. A Burkholderia pseudomallei outer membrane vesicle vaccine provides protection against lethal sepsis. Clin Vaccine Immunol. 2014;21(5):747–54.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  46. 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.

    Article  CAS  PubMed  Google Scholar 

  47. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. 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.

    Article  CAS  PubMed  Google Scholar 

  49. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  50. 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.

  51. 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.

    Article  CAS  PubMed  Google Scholar 

  52. 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.

    Article  CAS  PubMed  Google Scholar 

  53. 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.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  54. 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.

    PubMed  PubMed Central  Google Scholar 

  55. Zuo T, Ng SC. The gut microbiota in the pathogenesis and therapeutics of inflammatory bowel disease. Front Microbiol. 2018;9:2247–7.

  56. 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.

    Article  CAS  PubMed  Google Scholar 

  57. Martin R, et al. Faecalibacterium prausnitzii prevents physiological damages in a chronic low-grade inflammation murine model. BMC Microbiol. 2015;15:67.

    Article  PubMed  PubMed Central  Google Scholar 

  58. Floch MH, et al. Recommendations for probiotic use-2011 update. J Clin Gastroenterol. 2011;45(Suppl):S168–71.

    Article  PubMed  Google Scholar 

  59. 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.

    Article  CAS  PubMed  Google Scholar 

  60. 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.

    Article  CAS  PubMed  Google Scholar 

  61. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  62. 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.

    Article  CAS  PubMed  Google Scholar 

  63. 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.

  64. 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.

    Article  CAS  PubMed  Google Scholar 

  65. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. 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.

    Article  CAS  PubMed  Google Scholar 

  68. Ye D, et al. MicroRNA regulation of intestinal epithelial tight junction permeability. Gastroenterology. 2011;141(4):1323–33.

    Article  CAS  PubMed  Google Scholar 

  69. Patton JG, et al. Biogenesis, delivery, and function of extracellular RNA. J Extracell Vesicles. 2015;4:27494.

    Article  PubMed  CAS  Google Scholar 

  70. 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.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  71. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. 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.

    Article  CAS  Google Scholar 

  73. Michael A, et al. Exosomes from human saliva as a source of microRNA biomarkers. Oral Dis. 2010;16(1):34–8.

    Article  CAS  PubMed  Google Scholar 

  74. Xie Z, et al. Salivary microRNAs as promising biomarkers for detection of esophageal cancer. PLoS One. 2013;8(4):e57502.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. 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.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  76. 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.

    Article  CAS  PubMed  Google Scholar 

  77. 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.

    Article  CAS  PubMed Central  Google Scholar 

  78. Furuse Y, et al. Search for microRNAs expressed by intracellular bacterial pathogens in infected mammalian cells. PLoS One. 2014;9(9):e106434.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  79. Ortega AD, et al. Non-coding RNA regulation in pathogenic bacteria located inside eukaryotic cells. Front Cell Infect Microbiol. 2014;4:162.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  80. Sesto N, Koutero M, Cossart P. Bacterial and cellular RNAs at work during Listeria infection. Future Microbiol. 2014;9(9):1025–37.

    Article  CAS  PubMed  Google Scholar 

  81. Singh PP, Li L, Schorey JS. Exosomal RNA from Mycobacterium tuberculosis-infected cells is functional in recipient macrophages. Traffic. 2015;16(6):555–71.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Koeppen K, et al. A novel mechanism of host-pathogen interaction through sRNA in bacterial outer membrane vesicles. PLoS Pathog. 2016;12(6):e1005672.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  83. 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.

    Article  CAS  PubMed  Google Scholar 

  84. Liu S, et al. The host shapes the gut microbiota via fecal MicroRNA. Cell Host Microbe. 2016;19(1):32–43.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Ho MH, et al. Functional advantages of Porphyromonas gingivalis vesicles. PLoS One. 2015;10(4):e0123448.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  86. Sjostrom AE, et al. Membrane vesicle-mediated release of bacterial RNA. Sci Rep. 2015;5:15329.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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Acknowledgments

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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Correspondence to Seyed Davar Siadat.

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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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