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Research Paper

Ulcerative Colitis-associated E. coli pathobionts potentiate colitis in susceptible hosts

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Article: 1847976 | Received 17 Aug 2020, Accepted 23 Oct 2020, Published online: 01 Dec 2020

References

  • Mulder DJ, Noble AJ, Justinich CJ, Duffin JM. A tale of two diseases: the history of inflammatory bowel disease. J Crohns Colitis. 2014;8:341–348. doi:10.1016/j.crohns.2013.09.009.
  • Davis BK, Philipson C, Hontecillas R, Eden K, Bassaganya-Riera J, Allen IC. Emerging significance of NLRs in inflammatory bowel disease. Inflamm Bowel Dis. 2014;20:2412–2432. doi:10.1097/MIB.0000000000000151.
  • de Souza HS, Fiocchi C. Immunopathogenesis of IBD: current state of the art. Nat Rev Gastroenterol Hepatol. 2016;13:13–27. doi:10.1038/nrgastro.2015.186.
  • Sartor RB. Therapeutic manipulation of the enteric microflora in inflammatory bowel diseases: antibiotics, probiotics, and prebiotics. Gastroenterology. 2004;126:1620–1633.
  • Feller M, Huwiler K, Schoepfer A, Shang A, Furrer H, Egger M. Long-term antibiotic treatment for Crohn’s disease: systematic review and meta-analysis of placebo-controlled trials. Clin Infect Dis. 2010;50:473–480.
  • Keighley MR, Arabi Y, Dimock F, Burdon DW, Allan RN, Alexander-Williams J. Influence of inflammatory bowel disease on intestinal microflora. Gut. 1978;19:1099–1104.
  • Burke DA, Axon AT. Adhesive Escherichia coli in inflammatory bowel disease and infective diarrhoea. BMJ. 1988;297:102–104.
  • Ilnyckyj A, Greenberg H, Bernstein CN. Escherichia coli O157:H7 infection mimicking Crohn’s disease. Gastroenterology. 1997;112:995–999.
  • Giaffer MH, Holdsworth CD, Duerden BI. Virulence properties of Escherichia coli strains isolated from patients with inflammatory bowel disease. Gut. 1992;33:646–650.
  • Mirsepasi-Lauridsen HC, Vallance BA, Krogfelt KA, Petersen AM. Escherichia coli pathobionts associated with inflammatory bowel disease. Clin Microbiol Rev. 2019;32(2):e00060-18.
  • Small CL, Reid-Yu SA, McPhee JB, Coombes BK. Persistent infection with Crohn’s disease-associated adherent-invasive Escherichia coli leads to chronic inflammation and intestinal fibrosis. Nat Commun. 2013;4:1957. doi:10.1038/ncomms2957.
  • De la Fuente M, Franchi L, Araya D, Diaz-Jimenez D, Olivares M, Alvarez-Lobos M, Golenbock D, González M-J, López-Kostner F, Quera R, et al. Escherichia coli isolates from inflammatory bowel diseases patients survive in macrophages and activate NLRP3 inflammasome. Int J Med Microbiol. 2014;304:384–392. doi:10.1016/j.ijmm.2014.01.002.
  • Chassaing B, Rolhion N, de Vallee A, Salim SY, Prorok-Hamon M, Neut C, Campbell BJ, Söderholm JD, Hugot J-P, Colombel J-F, et al. Crohn disease–associated adherent-invasive E. coli bacteria target mouse and human Peyer’s patches via long polar fimbriae. J Clin Invest. 2011;121:966–975. doi:10.1172/JCI44632.
  • Palmela C, Chevarin C, Xu Z, Torres J, Sevrin G, Hirten R, Barnich N, Ng SC, Colombel JF. Adherent-invasive Escherichia coli in inflammatory bowel disease. Gut. 2018 Mar;67(3):574–587.
  • Glasser AL, Boudeau J, Barnich N, Perruchot MH, Colombel JF, Darfeuille-Michaud A. Adherent invasive Escherichia coli strains from patients with Crohn’s disease survive and replicate within macrophages without inducing host cell death. Infect Immun. 2001;69:5529–5537. doi:10.1128/IAI.69.9.5529-5537.2001.
  • Boudeau J, Glasser AL, Masseret E, Joly B, Darfeuille-Michaud A. Invasive ability of an Escherichia coli strain isolated from the ileal mucosa of a patient with Crohn’s disease. Infect Immun. 1999;67:4499–4509. doi:10.1128/IAI.67.9.4499-4509.1999.
  • Carvalho FA, Barnich N, Sivignon A, Darcha C, Chan CH, Stanners CP, Darfeuille-Michaud A. Crohn’s disease adherent-invasive Escherichia coli colonize and induce strong gut inflammation in transgenic mice expressing human CEACAM. J Exp Med. 2009;206:2179–2189. doi:10.1084/jem.20090741.
  • Barnich N, Carvalho FA, Glasser AL, Darcha C, Jantscheff P, Allez M, Peeters H, Bommelaer G, Desreumaux P, Colombel J-F. CEACAM6 acts as a receptor for adherent-invasive E. coli, supporting ileal mucosa colonization in Crohn disease. J Clin Invest. 2007;117:1566–1574. doi:10.1172/JCI30504.
  • Schultsz C, Moussa M, van Ketel R, Tytgat GN, Dankert J. Frequency of pathogenic and enteroadherent Escherichia coli in patients with inflammatory bowel disease and controls. J Clin Pathol. 1997;50:573–579. doi:10.1136/jcp.50.7.573.
  • Petersen AM, Nielsen EM, Litrup E, Brynskov J, Mirsepasi H, Krogfelt KA. A phylogenetic group of Escherichia coli associated with active left-sided inflammatory bowel disease. BMC Microbiol. 2009;9:171. doi:10.1186/1471-2180-9-171.
  • Kotlowski R, Bernstein CN, Sepehri S, Krause DO. High prevalence of Escherichia coli belonging to the B2+D phylogenetic group in inflammatory bowel disease. Gut. 2007;56:669–675. doi:10.1136/gut.2006.099796.
  • Jensen SR, Mirsepasi-Lauridsen HC, Thysen AH, Brynskov J, Krogfelt KA, Petersen AM, Pedersen AE, Brix S. Distinct inflammatory and cytopathic characteristics of Escherichia coli isolates from inflammatory bowel disease patients. Int J Med Microbiol. 2015;305:925–936. doi:10.1016/j.ijmm.2015.10.002.
  • Mirsepasi-Lauridsen HC, Du Z, Struve C, Charbon G, Karczewski J, Krogfelt KA, Petersen AM, Wells JM. Secretion of alpha-hemolysin by escherichia coli disrupts tight junctions in ulcerative colitis patients. Clin Transl Gastroenterol. 2016;7:e149. doi:10.1038/ctg.2016.3.
  • Xiao H, Gulen MF, Qin J, Yao J, Bulek K, Kish D, Altuntas CZ, Wald D, Ma C, Zhou H. The Toll-interleukin-1 receptor member SIGIRR regulates colonic epithelial homeostasis, inflammation, and tumorigenesis. Immunity. 2007;26:461–475. doi:10.1016/j.immuni.2007.02.012.
  • Sham HP, Yu EY, Gulen MF, Bhinder G, Stahl M, Chan JM, Brewster L, Morampudi V, Gibson DL, Hughes MR, et al. SIGIRR, a negative regulator of TLR/IL-1R signalling promotes Microbiota dependent resistance to colonization by enteric bacterial pathogens. PLoS Pathog. 2013;9:e1003539. doi:10.1371/journal.ppat.1003539.
  • Stahl M, Ries J, Vermeulen J, Yang H, Sham HP, Crowley SM, Badayeva Y, Turvey SE, Gaynor EC, Li X, et al. A novel mouse model of Campylobacter jejuni gastroenteritis reveals key pro-inflammatory and tissue protective roles for Toll-like receptor signaling during infection. PLoS Pathog. 2014;10:e1004264. doi:10.1371/journal.ppat.1004264.
  • Lauridsen HC, Yang H, Bosman E, Yu H, Wu X, Ma C, Struve C, Petersen AM, Krogfelt KA, Jacobson K, et al. Ulcerative colitis-associated escherichia coli colonize the ileum and cecum of infected mice by adhering to the intestinal epithelium. Gastroenterology. 2015;148(Supplement 1):S–712.
  • Kiesler P, Fuss IJ, Strober W. Experimental models of inflammatory bowel diseases. Cell Mol Gastroenterol Hepatol. 2015;1:154–170. doi:10.1016/j.jcmgh.2015.01.006.
  • Chassaing B, Srinivasan G, Delgado MA, Young AN, Gewirtz AT, Vijay-Kumar M. Fecal lipocalin 2, a sensitive and broadly dynamic non-invasive biomarker for intestinal inflammation. PLoS One. 2012;7:e44328. doi:10.1371/journal.pone.0044328.
  • Bucker R, Schulz E, Gunzel D, Bojarski C, Lee IF, John LJ, Wiegand S, Janßen T, Wieler LH, Dobrindt U, et al. α-Haemolysin of Escherichia coli in IBD: a potentiator of inflammatory activity in the colon. Gut. 2014;63:1893–1901. doi:10.1136/gutjnl-2013-306099.
  • Mirsepasi-Lauridsen HC, Halkjaer SI, Mortensen EM, Lydolph MC, Nordgaard-Lassen I, Krogfelt KA, Petersen AM. Extraintestinal pathogenic Escherichia coli are associated with intestinal inflammation in patients with ulcerative colitis. Sci Rep. 2016;6:31152. doi:10.1038/srep31152.
  • Vejborg RM, Hancock V, Petersen AM, Krogfelt KA, Klemm P. Comparative genomics of Escherichia coli isolated from patients with inflammatory bowel disease. BMC Genomics. 2011;12:316.
  • Mysorekar IU, Mulvey MA, Hultgren SJ, Gordon JI. Molecular regulation of urothelial renewal and host defenses during infection with uropathogenic Escherichia coli. J Biol Chem. 2002;277:7412–7419.
  • Dreux N, Denizot J, Martinez-Medina M, Mellmann A, Billig M, Kisiela D, Chattopadhyay S, Sokurenko E, Neut C, Gower-Rousseau C, et al. Point mutations in FimH adhesin of Crohn’s disease-associated adherent-invasive Escherichia coli enhance intestinal inflammatory response. PLoS Pathog. 2013;9:e1003141.
  • Boudeau J, Barnich N, Darfeuille-Michaud A. Type 1 pili-mediated adherence of Escherichia coli strain LF82 isolated from Crohn’s disease is involved in bacterial invasion of intestinal epithelial cells. Mol Microbiol. 2001;39:1272–1284.
  • Sivignon A, Bouckaert J, Bernard J, Gouin SG, Barnich N. The potential of FimH as a novel therapeutic target for the treatment of Crohn’s disease. Expert Opin Ther Targets. 2017;21:837–847.
  • Sivignon A, Yan X, Alvarez Dorta D, Bonnet R, Bouckaert J, Fleury E, Bernard J, Gouin SG, Darfeuille-Michaud A, Barnich N. Development of heptylmannoside-based glycoconjugate antiadhesive compounds against adherent-invasive escherichia coli bacteria associated with Crohn’s disease. MBio. 2015;6:e01298–15.
  • Spaulding CN, Klein RD, Ruer S, Kau AL, Schreiber HL, Cusumano ZT, Dodson KW, Pinkner JS, Fremont DH, Janetka JW, et al. Selective depletion of uropathogenic E. coli from the gut by a FimH antagonist. Nature. 2017;546:528–532.
  • Alvarez Dorta D, Sivignon A, Chalopin T, Dumych TI, Roos G, Bilyy RO, Deniaud D, Krammer EM, de Ruyck J, Lensink MF, et al. The antiadhesive strategy in Crohn’s disease: orally active mannosides to decolonize pathogenic Escherichia coli from the Gut. Chembiochem. 2016;17:936–952.
  • Bouckaert J, Li Z, Xavier C, Almant M, Caveliers V, Lahoutte T, Kovensky J, Gouin SG. Heptyl alpha-D-mannosides grafted on a beta-cyclodextrin core to interfere with Escherichia coli adhesion: an in vivo multivalent effect. Chemistry. 2013;19:7847–7855.
  • Carvalho FA, Koren O, Goodrich JK, Johansson ME, Nalbantoglu I, Aitken JD, Su Y, Chassaing B, Walters WA, González A, et al. Transient inability to manage proteobacteria promotes chronic gut inflammation in TLR5-deficient mice. Cell Host Microbe. 2012;12:139–152.
  • Chassaing B, Koren O, Carvalho FA, Ley RE, Gewirtz AT. AIEC pathobiont instigates chronic colitis in susceptible hosts by altering microbiota composition. Gut. 2014;63:1069–1080.
  • Roberts IS. The biochemistry and genetics of capsular polysaccharide production in bacteria. Annu Rev Microbiol. 1996;50:285–315.
  • Galan JE, Lara-Tejero M, Marlovits TC, Wagner S. Bacterial type III secretion systems: specialized nanomachines for protein delivery into target cells. Annu Rev Microbiol. 2014;68:415–438.
  • Winter SE, Winter MG, Xavier MN, Thiennimitr P, Poon V, Keestra AM, Laughlin RC, Gomez G, Wu J, Lawhon SD, et al. Host-derived nitrate boosts growth of E. coli in the inflamed gut. Science. 2013;339:708–711.
  • Troeger H, Richter JF, Beutin L, Gunzel D, Dobrindt U, Epple HJ, Gitter AH, Zeitz M, Fromm M, Schulzke JD. Escherichia coli alpha-haemolysin induces focal leaks in colonic epithelium: a novel mechanism of bacterial translocation. Cell Microbiol. 2007;9:2530–2540.
  • Krogfelt KA, Bergmans H, Klemm P. Direct evidence that the FimH protein is the mannose-specific adhesin of Escherichia coli type 1 fimbriae. Infect Immun. 1990;58:1995–1998.
  • Ofek I, Mirelman D, Sharon N. Adherence of Escherichia coli to human mucosal cells mediated by mannose receptors. Nature. 1977;265:623–625.
  • Sokurenko EV, Chesnokova V, Dykhuizen DE, Ofek I, Wu XR, Krogfelt KA, Struve C, Schembri MA, Hasty DL. Pathogenic adaptation of Escherichia coli by natural variation of the FimH adhesin. Proc Natl Acad Sci U S A. 1998;95:8922–8926.
  • Poole NM, Green SI, Rajan A, Vela LE, Zeng XL, Estes MK, Maresso AW. Role for FimH in extraintestinal pathogenic Escherichia coli invasion and translocation through the intestinal epithelium. Infect Immun. 2017;85(11): e00581-17.
  • Schilling JD, Mulvey MA, Hultgren SJ. Structure and function of Escherichia coli type 1 pili: new insight into the pathogenesis of urinary tract infections. J Infect Dis. 2001;183:S36–40.
  • Russell CW, Fleming BA, Jost CA, Tran A, Stenquist AT, Wambaugh MA, Bronner MP, Mulvey MA. Context-dependent requirements for fimh and other canonical virulence factors in Gut colonization by extraintestinal pathogenic Escherichia coli. Infect Immun. 2018;86(3):e00746-17.
  • Kalas V, Hibbing ME, Maddirala AR, Chugani R, Pinkner JS, Mydock-McGrane LK, Conover MS, Janetka JW, Hultgren SJ. Structure-based discovery of glycomimetic FmlH ligands as inhibitors of bacterial adhesion during urinary tract infection. Proc Natl Acad Sci U S A. 2018;115:E2819–E28.
  • Dwyer BE, Newton KL, Kisiela D, Sokurenko EV, Clegg S. Single nucleotide polypmorphisms of fimH associated with adherence and biofilm formation by serovars of Salmonella enterica. Microbiology. 2011;157:3162–3171.
  • Schembri MA, Klemm P. Biofilm formation in a hydrodynamic environment by novel fimh variants and ramifications for virulence. Infect Immun. 2001;69:1322–1328.
  • Liu Y, Memet S, Saban R, Kong X, Aprikian P, Sokurenko E, Sun TT, Wu XR. Dual ligand/receptor interactions activate urothelial defenses against uropathogenic E. Coli Sci Rep. 2015;5:16234.
  • Lee DJ, Bingle LE, Heurlier K, Pallen MJ, Penn CW, Busby SJ, Hobman JL. Gene doctoring: a method for recombineering in laboratory and pathogenic Escherichia coli strains. BMC Microbiol. 2009;9:252.
  • Schembri MA, Christiansen G, Klemm P. FimH-mediated autoaggregation of Escherichia coli. Mol Microbiol. 2001;41:1419–1430.
  • Sham HP, Shames SR, Croxen MA, Ma C, Chan JM, Khan MA, Wickham ME, Deng W, Finlay BB, Vallance BA. Attaching and effacing bacterial effector NleC suppresses epithelial inflammatory responses by inhibiting NF-kappaB and p38 mitogen-activated protein kinase activation. Infect Immun. 2011;79:3552–3562.
  • Ferrieres L, Hemery G, Nham T, Guerout AM, Mazel D, Beloin C, Ghigo JM. Silent mischief: bacteriophage Mu insertions contaminate products of Escherichia coli random mutagenesis performed using suicidal transposon delivery plasmids mobilized by broad-host-range RP4 conjugative machinery. J Bacteriol. 2010;192:6418–6427.
  • Choi KH, Gaynor JB, White KG, Lopez C, Bosio CM, Karkhoff-Schweizer RR, Schweizer HP. A Tn7-based broad-range bacterial cloning and expression system. Nat Methods. 2005;2:443–448.
  • Robinson GM, Tonks KM, Thorn RM, Reynolds DM. Application of bacterial bioluminescence to assess the efficacy of fast-acting biocides. Antimicrob Agents Chemother. 2011;55:5214–5220.
  • Lutz R, Bujard H. Independent and tight regulation of transcriptional units in Escherichia coli via the LacR/O, the TetR/O and AraC/I1-I2 regulatory elements. Nucleic Acids Res. 1997;25:1203–1210.
  • Yu HB, Croxen MA, Marchiando AM, Ferreira RB, Cadwell K, Foster LJ,  Finlay BB. Autophagy facilitates Salmonella replication in HeLa cells. MBio. 2014;5:e00865–14.
  • Bergstrom KS, Kissoon-Singh V, Gibson DL, Ma C, Montero M, Sham HP, Ryz N, Huang T, Velcich A, Finlay BB, et al. Muc2 protects against lethal infectious colitis by disassociating pathogenic and commensal bacteria from the colonic mucosa. PLoS Pathog. 2010;6:e1000902.
  • Stahl M, Tremblay S, Montero M, Vogl W, Xia L, Jacobson K, Menendez A, Vallance BA. The Muc2 mucin coats murine Paneth cell granules and facilitates their content release and dispersion. Am J Physiol Gastrointest Liver Physiol. 2018;315:G195–G205.