Citrobacter rodentium Relies on Commensals for Colonization of the Colonic Mucosa

Cell Reports

Volumn 21, Issue 12, 2017, Pages 3381-3389

  Mullineaux Sanders, Caroline ^a   Collins, James W ^a   Ruano Gallego, David ^a   Levy, Maayan ^b   Pevsner Fischer, Meirav ^b   Glegola Madejska, Izabela T ^a   Sågfors, Agnes M ^a   Wong, Joshua L C ^a   Elinav, Eran ^b   Crepin, Valerie F ^a   Frankel, Gad ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

AMR; antibiotics; C. rodentium; colonization resistance; enteric infection; microbiota

Indexed keywords

CIPROFLOXACIN; KANAMYCIN; METRONIDAZOLE; VANCOMYCIN; ANTIINFECTIVE AGENT; BACTERIAL PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL VIRULENCE; BIOLUMINESCENCE; CECUM MUCOSA; CITROBACTER RODENTIUM; COLON MUCOSA; COMMENSAL; CONTROLLED STUDY; ENTEROBACTERIACEAE INFECTION; FEMALE; GENE EXPRESSION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SINGLE DRUG DOSE; ANIMAL; COLON; DRUG EFFECT; GENETICS; INTESTINE FLORA; INTESTINE MUCOSA; MICROBIOLOGY; PATHOGENICITY; VIRULENCE;

ANIMALS; ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; CITROBACTER RODENTIUM; COLON; GASTROINTESTINAL MICROBIOME; INTESTINAL MUCOSA; KANAMYCIN; METRONIDAZOLE; MICE; VANCOMYCIN; VIRULENCE;

EID: 85039944587     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2017.11.086     Document Type: Article

References (36)

1. Barthel, M., Hapfelmeier, S., Quintanilla-Martínez, L., Kremer, M., Rohde, M., Hogardt, M., Pfeffer, K., Rüssmann, H., Hardt, W.-D., Pretreatment of mice with streptomycin provides a Salmonella enterica serovar Typhimurium colitis model that allows analysis of both pathogen and host. Infect. Immun. 71 (2003), 2839–2858.
2. Berdichevsky, T., Friedberg, D., Nadler, C., Rokney, A., Oppenheim, A., Rosenshine, I., Ler is a negative autoregulator of the LEE1 operon in enteropathogenic Escherichia coli. J. Bacteriol. 187 (2005), 349–357.
3. Berger, C.N., Crepin, V.F., Roumeliotis, T.I., Wright, J.C., Carson, D., Pevsner-Fischer, M., Furniss, R.C.D., Dougan, G., Dori-Bachash, M., Yu, L., et al. Citrobacter rodentium subverts ATP flux and cholesterol homeostasis in intestinal epithelial cells in vivo. Cell Metab. 26 (2017), 738–752.e6.
4. Collins, J.W., Meganck, J.A., Kuo, C., Francis, K.P., Frankel, G., 4D multimodality imaging of Citrobacter rodentium infections in mice. J. Vis. Exp., 78, 2013, e50450.
5. Collins, J.W., Keeney, K.M., Crepin, V.F., Rathinam, V.A., Fitzgerald, K.A., Finlay, B.B., Frankel, G., Citrobacter rodentium: infection, inflammation and the microbiota. Nat. Rev. Microbiol. 12 (2014), 612–623.
6. Crepin, V.F., Girard, F., Schüller, S., Phillips, A.D., Mousnier, A., Frankel, G., Dissecting the role of the Tir:Nck and Tir:IRTKS/IRSp53 signalling pathways in vivo. Mol. Microbiol. 75 (2010), 308–323.
7. Crepin, V.F., Collins, J.W., Habibzay, M., Frankel, G., Citrobacter rodentium mouse model of bacterial infection. Nat. Protoc. 11 (2016), 1851–1876.
8. Curtis, M.M., Hu, Z., Klimko, C., Narayanan, S., Deberardinis, R., Sperandio, V., The gut commensal Bacteroides thetaiotaomicron exacerbates enteric infection through modification of the metabolic landscape. Cell Host Microbe 16 (2014), 759–769.
9. Deng, W., Puente, J.L., Gruenheid, S., Li, Y., Vallance, B.A., Vázquez, A., Barba, J., Ibarra, J.A., O'Donnell, P., Metalnikov, P., et al. Dissecting virulence: systematic and functional analyses of a pathogenicity island. Proc. Natl. Acad. Sci. USA 101 (2004), 3597–3602.
10. DeSantis, T.Z., Hugenholtz, P., Larsen, N., Rojas, M., Brodie, E.L., Keller, K., Huber, T., Dalevi, D., Hu, P., Andersen, G.L., Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl. Environ. Microbiol. 72 (2006), 5069–5072.
11. Elinav, E., Strowig, T., Kau, A.L., Henao-Mejia, J., Thaiss, C.A., Booth, C.J., Peaper, D.R., Bertin, J., Eisenbarth, S.C., Gordon, J.I., Flavell, R.A., NLRP6 inflammasome regulates colonic microbial ecology and risk for colitis. Cell 145 (2011), 745–757.
12. Garmendia, J., Frankel, G., Crepin, V.F., Enteropathogenic and enterohemorrhagic Escherichia coli infections: translocation, translocation, translocation. Infect. Immun. 73 (2005), 2573–2585.
13. Ghosh, S., Dai, C., Brown, K., Rajendiran, E., Makarenko, S., Baker, J., Ma, C., Halder, S., Montero, M., Ionescu, V.-A., et al. Colonic microbiota alters host susceptibility to infectious colitis by modulating inflammation, redox status, and ion transporter gene expression. Am. J. Physiol. Gastrointest. Liver Physiol. 301 (2011), G39–G49.
14. Hecht, G., Bar-Nathan, C., Milite, G., Alon, I., Moshe, Y., Greenfeld, L., Dotsenko, N., Suez, J., Levy, M., Thaiss, C.A., et al. A simple cage-autonomous method for the maintenance of the barrier status of germ-free mice during experimentation. Lab. Anim. 48 (2014), 292–297.
15. Islam, M.S., Bingle, L.E., Pallen, M.J., Busby, S.J., Organization of the LEE1 operon regulatory region of enterohaemorrhagic Escherichia coli O157:H7 and activation by GrlA. Mol. Microbiol. 79 (2011), 468–483.
16. Kamada, N., Kim, Y.-G., Sham, H.P., Vallance, B.A., Puente, J.L., Martens, E.C., Núñez, G., Regulated virulence controls the ability of a pathogen to compete with the gut microbiota. Science 336 (2012), 1325–1329.
17. Kamada, N., Chen, G.Y., Inohara, N., Núñez, G., Control of pathogens and pathobionts by the gut microbiota. Nat. Immunol. 14 (2013), 685–690.
18. Kelly, C.J., Zheng, L., Campbell, E.L., Saeedi, B., Scholz, C.C., Bayless, A.J., Wilson, K.E., Glover, L.E., Kominsky, D.J., Magnuson, A., et al. Crosstalk between microbiota-derived short-chain fatty acids and intestinal epithelial HIF augments tissue barrier function. Cell Host Microbe 17 (2015), 662–671.
19. Kilkenny, C., Browne, W.J., Cuthill, I.C., Emerson, M., Altman, D.G., Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. PLoS Biol., 8, 2010, e1000412.
20. Lio, J.C.-W., Syu, W.-J., Identification of a negative regulator for the pathogenicity island of enterohemorrhagic Escherichia coli O157:H7. J. Biomed. Sci. 11 (2004), 855–863.
21. Lopez, C.A., Miller, B.M., Rivera-Chávez, F., Velazquez, E.M., Byndloss, M.X., Chávez-Arroyo, A., Lokken, K.L., Tsolis, R.M., Winter, S.E., Bäumler, A.J., Virulence factors enhance Citrobacter rodentium expansion through aerobic respiration. Science 353 (2016), 1249–1253.
22. Lupp, C., Robertson, M.L., Wickham, M.E., Sekirov, I., Champion, O.L., Gaynor, E.C., Finlay, B.B., Host-mediated inflammation disrupts the intestinal microbiota and promotes the overgrowth of Enterobacteriaceae. Cell Host Microbe 2 (2007), 119–129.
23. McDaniel, T.K., Jarvis, K.G., Donnenberg, M.S., Kaper, J.B., A genetic locus of enterocyte effacement conserved among diverse enterobacterial pathogens. Proc. Natl. Acad. Sci. USA 92 (1995), 1664–1668.
24. Mellies, J.L., Elliott, S.J., Sperandio, V., Donnenberg, M.S., Kaper, J.B., The Per regulon of enteropathogenic Escherichia coli : identification of a regulatory cascade and a novel transcriptional activator, the locus of enterocyte effacement (LEE)-encoded regulator (Ler). Mol. Microbiol. 33 (1999), 296–306.
25. Nakanishi, N., Tashiro, K., Kuhara, S., Hayashi, T., Sugimoto, N., Tobe, T., Regulation of virulence by butyrate sensing in enterohaemorrhagic Escherichia coli. Microbiology 155 (2009), 521–530.
26. Ng, K.M., Ferreyra, J.A., Higginbottom, S.K., Lynch, J.B., Kashyap, P.C., Gopinath, S., Naidu, N., Choudhury, B., Weimer, B.C., Monack, D.M., Sonnenburg, J.L., Microbiota-liberated host sugars facilitate post-antibiotic expansion of enteric pathogens. Nature 502 (2013), 96–99.
27. Pacheco, A.R., Curtis, M.M., Ritchie, J.M., Munera, D., Waldor, M.K., Moreira, C.G., Sperandio, V., Fucose sensing regulates bacterial intestinal colonization. Nature 492 (2012), 113–117.
28. Rivera-Chávez, F., Zhang, L.F., Faber, F., Lopez, C.A., Byndloss, M.X., Olsan, E.E., Xu, G., Velazquez, E.M., Lebrilla, C.B., Winter, S.E., Bäumler, A.J., Depletion of butyrate-producing Clostridia from the gut microbiota drives an aerobic luminal expansion of Salmonella. Cell Host Microbe 19 (2016), 443–454.
29. Spees, A.M., Wangdi, T., Lopez, C.A., Kingsbury, D.D., Xavier, M.N., Winter, S.E., Tsolis, R.M., Bäumler, A.J., Streptomycin-induced inflammation enhances Escherichia coli gut colonization through nitrate respiration. MBio 4 (2013), e00430–13.
30. Wadolkowski, E.A., Burris, J.A., O'Brien, A.D., Mouse model for colonization and disease caused by enterohemorrhagic Escherichia coli O157:H7. Infect. Immun. 58 (1990), 2438–2445.
31. Wiles, S., Clare, S., Harker, J., Huett, A., Young, D., Dougan, G., Frankel, G., Organ specificity, colonization and clearance dynamics in vivo following oral challenges with the murine pathogen Citrobacter rodentium. Cell. Microbiol. 6 (2004), 963–972.
32. Winter, S.E., Thiennimitr, P., Winter, M.G., Butler, B.P., Huseby, D.L., Crawford, R.W., Russell, J.M., Bevins, C.L., Adams, L.G., Tsolis, R.M., et al. Gut inflammation provides a respiratory electron acceptor for Salmonella. Nature 467 (2010), 426–429.
33. Wlodarska, M., Willing, B., Keeney, K.M., Menendez, A., Bergstrom, K.S., Gill, N., Russell, S.L., Vallance, B.A., Finlay, B.B., Antibiotic treatment alters the colonic mucus layer and predisposes the host to exacerbated Citrobacter rodentium-induced colitis. Infect. Immun. 79 (2011), 1536–1545.
34. Wong, A.R., Pearson, J.S., Bright, M.D., Munera, D., Robinson, K.S., Lee, S.F., Frankel, G., Hartland, E.L., Enteropathogenic and enterohaemorrhagic Escherichia coli: even more subversive elements. Mol. Microbiol. 80 (2011), 1420–1438.
35. Wostmann, B., Bruckner-Kardoss, E., Cecal enlargement in germ-free animals. Nutr. Rev. 18 (1960), 313–314.
36. Zhang, L., Huang, Y., Zhou, Y., Buckley, T., Wang, H.H., Antibiotic administration routes significantly influence the levels of antibiotic resistance in gut microbiota. Antimicrob. Agents Chemother. 57 (2013), 3659–3666.