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Research Paper/Report

Bile salt metabolism is not the only factor contributing to Clostridioides (Clostridium) difficile disease severity in the murine model of disease

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Pages 481-496 | Received 20 Jan 2019, Accepted 26 Sep 2019, Published online: 02 Dec 2019

References

  • Garey KW, Sethi S, Yadav Y, DuPont HL. Meta-analysis to assess risk factors for recurrent Clostridium difficile infection. J Hosp Infect. 2008;70(4):298–304. doi:10.1016/j.jhin.2008.08.012.
  • Farooq PD, Urrunaga NH, Tang DM, Von Rosenvinge EC. Pseudomembranous Colitis HHS public access. Dis Mon. 2015;61(5):181–206. doi:10.1016/j.disamonth.2015.01.006.
  • McFarland LV, Elmer GW, Surawicz CM. Breaking the cycle: treatment strategies for 163 cases of recurrent Clostridium difficile disease. Am J Gastroenterol. 2002;97(7):1769–1775. doi:10.1111/j.1572-0241.2002.05839.x.
  • Kelly CP. Can we identify patients at high risk of recurrent Clostridium difficile infection? Clin Microbiol Infect. 2012;18:21–27. doi:10.1111/1469-0691.12046.
  • Viswanathan VK, Mallozzi MJ, Vedantam G. An overview of the disease and its pathogenesis, epidemiology and interventions Clostridium difficile infection. Gut Microbes. 2010;1(4):234–242. doi:10.4161/gmic.1.4.12706.
  • Chang JY, Antonopoulos DA, Kalra A, Tonelli A, Khalife WT, Schmidt TM, Young VB. Decreased diversity of the fecal microbiome in recurrent Clostridium difficile-associated diarrhea. J Infect Dis. 2008;197(3):435–438. doi:10.1086/525047.
  • Becattini S, Taur Y, Pamer EG. Antibiotic-induced changes in the intestinal microbiota and disease [internet]. Trends in Molecular Medicine. 2016;22:458–478. doi:10.1016/j.molmed.2016.04.003.
  • van Nood E, Vrieze A, Nieuwdorp M, Fuentes S, Zoetendal EG, de Vos WM, Visser CE, Kuijper EJ, Bartelsman JFWM, Tijssen JGP, et al. Duodenal infusion of donor feces for recurrent Clostridium difficile. N Engl J Med. 2013;368(5):407–415. doi:10.1056/NEJMoa1205037.
  • Fuentes S, Van Nood E, Tims S, Heikamp-De Jong I, Jf Ter Braak C, Keller JJ, Zoetendal EG, De Vos WM. Reset of a critically disturbed microbial ecosystem: faecal transplant in recurrent Clostridium difficile infection. Isme J. 2014;8(10):1621–1633. doi:10.1038/ismej.2014.13.
  • Petrof EO, Gloor GB, Vanner SJ, Weese SJ, Carter D, Daigneault MC, Brown EM, Schroeter K, Allen-Vercoe E. Stool substitute transplant therapy for the eradication of Clostridium difficile infection: “RePOOPulating” the gut. Microbiome. 2013;1(1):3. doi:10.1186/2049-2618-1-3.
  • Buffie CG, Bucci V, Stein RR, McKenney PT, Ling L, Gobourne A, No D, Liu H, Kinnebrew M, Viale A, et al. Precision microbiome reconstitution restores bile acid mediated resistance to Clostridium difficile. Nature. 2014;517(7533):205–208. doi:10.1038/nature13828.
  • Khanna S, Pardi DS, Kelly CR, Kraft CS, Dhere T, Henn MR, Lombardo M-J, Vulic M, Ohsumi T, Winkler J, et al. A novel microbiome therapeutic increases gut microbial diversity and prevents recurrent Clostridium difficile infection. J Infect Dis. 2016;214:173–181. doi:10.1093/infdis/jiv766.
  • Ott SJ, Waetzig GH, Rehman A, Moltzau-Anderson J, Bharti R, Grasis JA, Cassidy L, Tholey A, Fickenscher H, Seegert D, et al. Efficacy of sterile fecal filtrate transfer for treating patients with Clostridium difficile infection. Gastroenterology. 2017;152:799–811. doi:10.1053/j.gastro.2016.11.010.
  • Aziz Q, Doré J, Emmanuel A, Guarner F, Quigley EMM. Gut microbiota and gastrointestinal health: current concepts and future directions. Neurogastroenterol Motil. 2013;25(1):4–15. doi:10.1111/nmo.12046.
  • Lawley TD, Clare S, Walker AW, Stares MD, Connor TR, Raisen C, Goulding D, Rad R, Schreiber F, Brandt C, et al. targeted restoration of the intestinal microbiota with a simple, defined bacteriotherapy resolves relapsing Clostridium difficile disease in mice. PLoS Pathog. 2012;8(10):e1002995. doi:10.1371/journal.ppat.1002995.
  • Ridlon JM, Kang D-J, Hylemon PB. Bile salt biotransformations by human intestinal bacteria. J Lipid Res. 2006;47(2):241–259. doi:10.1194/jlr.R500013-JLR200.
  • Lewis BB, Buffie CG, Carter RA, Leiner I, Toussaint NC, Miller LC, Gobourne A, Ling L, Pamer EG. Loss of microbiota-mediated colonization resistance to Clostridium difficile infection with oral vancomycin compared with metronidazole. J Infect Dis. 2015;212(10):1656–1665. doi:10.1093/infdis/jiv256.
  • Allegretti JR, Kearney S, Li N, Bogart E, Bullock K, Gerber GK, Bry L, Clish CB, Alm E, Korzenik JR. Recurrent Clostridium difficile infection associates with distinct bile acid and microbiome profiles. Aliment Pharmacol Ther. 2016;43:1142–1153. doi:10.1111/apt.13616.
  • Sorg JA, Sonenshein AL. Bile salts and glycine as cogerminants for Clostridium difficile spores. J Bacteriol. 2008;190(7):2505–2512. doi:10.1128/JB.01765-07.
  • Sorg JA, Sonenshein AL. Chenodeoxycholate is an inhibitor of Clostridium difficile spore germination. J Bacteriol. 2009;191(3):1115–1117. doi:10.1128/JB.01260-08.
  • Francis MB, Allen CA, Sorg JA. Muricholic acids inhibit Clostridium difficile spore germination and growth. PLoS One. 2013;8(9):e73653. doi:10.1371/journal.pone.0073653.
  • Ridlon JM, Harris SC, Bhowmik S, Kang DJ, Hylemon PB. Consequences of bile salt biotransformations by intestinal bacteria. Gut Microbes. 2016;7(1):22–39. doi:10.1080/19490976.2015.1127483.
  • Mallonee DH, Adams JL, Hylemon PB. The bile acid-inducible baiB gene from Eubacterium sp. strain VPI 12708 encodes a bile acid-coenzyme A ligase. J Bacteriol. 1992;174(7):2065–2071. doi:10.1128/jb.174.7.2065-2071.1992.
  • Antunes LCM, Han J, Ferreira RBR, Lolić P, Borchers CH, Finlay BB. Effect of antibiotic treatment on the intestinal metabolome. Antimicrob Agents Chemother. 2011;55(4):1494–1503. doi:10.1128/AAC.01664-10.
  • Theriot CM, Koenigsknecht MJ, Carlson PE, Hatton GE, Nelson AM, Li B, Huffnagle GB, Z Li J, Young VB. Antibiotic-induced shifts in the mouse gut microbiome and metabolome increase susceptibility to Clostridium difficile infection. Nat Commun. 2014;5:3114. doi:10.1038/ncomms5972.
  • Theriot CM, Bowman AA, Young VB. Antibiotic-induced alterations of the gut microbiota alter secondary bile acid production and allow for Clostridium difficile spore germination and outgrowth in the large intestine. mSphere. 2015;1:e00045–15.
  • Andréasson K, Norin KE, Midtvedt T. Influence of ampicillin, clindamycin or metronidazole upon the 7α-dehydroxylation of bile acids in the human intestine. Curr Microbiol. 1988;16(6):329–331. doi:10.1007/BF01568540.
  • Theriot CM, Young VB. Microbial and metabolic interactions between the gastrointestinal tract and Clostridium difficile infection. Gut Microbes. 2014;5:86–95. doi:10.4161/gmic.27131.
  • Chen X, Katchar K, Goldsmith JD, Nanthakumar N, Cheknis A, Gerding DN, Kelly CP. A mouse model of Clostridium difficile-associated disease. Gastroenterology. 2008;135(6):1984–1992. doi:10.1053/j.gastro.2008.09.002.
  • Abhauer KP, Wemheuer B, Daniel R, Meinicke P. Tax4Fun: predicting functional profiles from metagenomic 16S rRNA data. Bioinformatics. 2015;31(17):2882–2884. doi:10.1093/bioinformatics/btv287.
  • Yoon S, Yu J, McDowell A, Kim SH, You HJ, Ko GP. Bile salt hydrolase-mediated inhibitory effect of bacteroides ovatus on growth of Clostridium difficile. J Microbiol. 2017;55:892–899. doi:10.1007/s12275-017-7340-4.
  • Thanissery R, Winston JA, Theriot CM. Inhibition of spore germination, growth, and toxin activity of clinically relevant C. difficile strains by gut microbiota derived secondary bile acids HHS public access. Anaerobe. 2017;45:86–100. doi:10.1016/j.anaerobe.2017.03.004.
  • Van Eldere J, Celis P, De Pauw G, Lesaffre E, Eyssen H. Tauroconjugation of cholic acid stimulates 7 alpha-dehydroxylation by fecal bacteria. Appl Environ Microbiol. 1996;62:656–661.
  • Gustafsson N, Norin E, Midvedt KI. Effect of clindamycin given alone or with Lactobacillus delbrueckii and Streptococcus thermophilus on 7a-dehydroxylation of bile acids in rats. Clin Microbiol Infect. 1998;4:594–598.
  • Saiful Islam KBM, Fukiya S, Hagio M, Fujii N, Ishizuka S, Ooka T, Ogura Y, Hayashi T, Yokota A. Bile acid is a host factor that regulates the composition of the cecal microbiota in rats. YGAST. 2011;141:1773–1781.
  • Ridlon JM, Alves JM, Hylemon PB, Bajaj JS. Cirrhosis, bile acids and gut microbiota: unraveling a complex relationship. Gut Microbes. 2013;4:382–387. doi:10.4161/gmic.25723.
  • Collins J, Auchtung JM, Schaefer L, Eaton KA, Britton RA. Humanized microbiota mice as a model of recurrent Clostridium difficile disease. Microbiome. 2015;3:35. doi:10.1186/s40168-015-0097-2.
  • Tam J, Beilhartz GL, Auger A, Gupta P, Therien AG, Melnyk RA. Small molecule inhibitors of Clostridium difficile toxin b-induced cellular damage. Chem Biol. 2015;22(2):175–185. doi:10.1016/j.chembiol.2014.12.010.
  • Peniche AG, Savidge TC, Dann SM. Recent insights into Clostridium difficile pathogenesis. Curr Opin Infect Dis. 2013;26(5):447–453. doi:10.1097/01.qco.0000433318.82618.c6.
  • Reeves AE, Theriot CM, Bergin IL, Huffnagle GB, Schloss PD, Young VB. The interplay between microbiome dynamics and pathogen dynamics in a murine model of Clostridium difficile infection. Gut Microbes. 2011;2(3):145–158. doi:10.4161/gmic.2.3.16333.
  • Martens EC, Roth R, Heuser JE, Gordon JI. Coordinate regulation of glycan degradation and polysaccharide capsule biosynthesis by a prominent human gut symbiont. J Biol Chem. 2009;284(27):18445–18457. doi:10.1074/jbc.M109.008094.
  • Engevik MA, Yacyshyn MB, Engevik KA, Wang J, Darien B, Hassett DJ, Yacyshyn BR, Worrell RT. Human Clostridium difficile infection: altered mucus production and composition. Am J Physiol - Gastrointest Liver Physiol. 2015;308(6):G510–24. doi:10.1152/ajpgi.00091.2014.
  • Wlodarska M, Willing B, Keeney KM, Menendez A, Bergstrom KS, Gill N, Russell SL, Vallance BA, Finlay BB. Antibiotic treatment alters the colonic mucus layer and predisposes the host to exacerbated Citrobacter rodentium-induced colitis. Infect Immun. 2011;79(4):1536–1545. doi:10.1128/IAI.01104-10.
  • Curtis MM, 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. 2014;16(6):759–769. doi:10.1016/j.chom.2014.11.005.
  • Ferreyra JA, Wu KJ, Hryckowian AJ, Bouley DM, Weimer BC, Sonnenburg JL. Gut microbiota-produced succinate promotes C. difficile infection after antibiotic treatment or motility disturbance. Cell Host Microbe. 2014;16(6):770–777. doi:10.1016/j.chom.2014.11.003.
  • Ng KM, Ferreyra JA, Higginbottom SK, Lynch JB, Kashyap PC, Gopinath S, Naidu N, Choudhury B, Weimer BC, Monack DM, et al. Microbiota-liberated host sugars facilitate post-antibiotic expansion of enteric pathogens. Nature. 2013;502:906–909. doi:10.1038/nature12503.
  • Wrzosek L, Miquel S, Noordine M-L, Bouet S, Chevalier-Curt MJ, Robert V, Philippe C, Bridonneau C, Cherbuy C, Robbe-Masselot C, et al. Bacteroides thetaiotaomicron and Faecalibacterium prausnitzii influence the production of mucus glycans and the development of goblet cells in the colonic epithelium of a gnotobiotic model rodent. BMC Biol. 2013;11:61. doi:10.1186/1741-7007-11-88.
  • Jakobsson HE, Rodríguez-Piñeiro AM, Schütte A, Ermund A, Boysen P, Bemark M, Sommer F, Bäckhed F, Hansson GC, Johansson ME. The composition of the gut microbiota shapes the colon mucus barrier. EMBO Rep. 2015;16(2):164–177. doi:10.15252/embr.201439263.
  • Rea MC, Alemayehu D, Paul Ross R, Hill C. Gut solutions to a gut problem: bacteriocins, probiotics and bacteriophage for control of Clostridium difficile infection. J Med Microbiol. 2013;62:1369–1378. doi:10.1099/jmm.0.058933-0.
  • Schubert AM, Sinani H, Schloss PD. Antibiotic induced alterations of the murine gut microbiota and subsequent effects on colonisation resistance against Clostridium difficile. mBio. 2015;6:1–10. doi:10.1128/mBio.00974-15.
  • Jenior ML, Leslie JL, Young VB, Schloss PD. Clostridium difficile alters the structure and metabolism of distinct cecal microbiomes during initial infection to promote sustained colonization. mSphere. 2018;23:e00261–18.
  • Buckley AM, Spencer J, Candlish D, Irvine JJ, Douce GR. Infection of hamsters with the UK Clostridium difficile ribotype 027 outbreak strain R20291. J. Med. Micro. 2011;60:1174–1180. doi:10.1099/jmm.0.028514-0.
  • Fischer AH, Jacobson KA, Rose J, Zeller R. Hematoxylin and eosin staining of tissue and cell sections. Cold Spring Harb Protoc. 2008;3:4986–4988.
  • Rose TM, Schultz ER, Henikoff JG, Pietrokovski S, McCallum CM, Henikoff S. Consensus-degenerate hybrid oligonucleotide primers for amplification of distantly related sequences. Nucleic Acids Res. 1998;26(7):1628–1635. doi:10.1093/nar/26.7.1628.
  • Mullish BH, Pechlivanis A, Barker GF, Thursz MR, Marchesi JR, McDonald JAK. Functional microbiomics: evaluation of gut microbiota-bile acid metabolism interactions in health and disease. Methods. 2018;149:49–58. doi:10.1016/j.ymeth.2018.04.028.
  • Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol. 2012;19(5):455–477. doi:10.1089/cmb.2012.0021.
  • Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics. 2014;30(14):2068–2069. doi:10.1093/bioinformatics/btu153.
  • Want EJ, Coen M, Masson P, Keun HC, Pearce JT, Reily MD, Robertson DG, Rohde CM, Holmes E, Lindon JC, et al. Ultra-performance liquid chromatography-mass spectrometry profiling of bile acid metabolites in biofluids: application to experimental toxicology studies. Anal Chem. 2010;82:5282–5289. doi:10.1021/ac1007078.
  • Smith CA, Want EJ, O’Maille G, Abagyan R, Siuzdak G. XCMS: processing mass spectrometry data for metabolite profiling using nonlinear peak alignment,matching, and identification. Anal Chem. 2006;78:779–787. doi:10.1021/ac051437y.