The interplay between microbiome dynamics and pathogen dynamics in a murine model of Clostridium difficile infection

Gut Microbes

Volumn 2, Issue 3, 2011, Pages 145-158

  Reeves, Angela E ^a   Theriot, Casey M ^a   Bergin, Ingrid L ^b   Huffnagle, Gary B ^a   Schloss, Patrick D ^a   Young, Vincent B ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Antibiotic associated diarrhea; C. difficile infection; Clostridium difficile; Colonization resistance; Microbial ecology

Indexed keywords

CEFOPERAZONE; CLINDAMYCIN; COLISTIN; CYTOTOXIN; DRINKING WATER; GENTAMICIN; KANAMYCIN; METRONIDAZOLE; RNA 16S; VANCOMYCIN;

ACTINOBACTERIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL STRAIN; BACTERIUM; BACTEROIDETES; CLOSTRIDIUM DIFFICILE INFECTION; COLITIS; COLONY FORMING UNIT; COMMUNITY DYNAMICS; COMMUNITY STRUCTURE; CONTROLLED STUDY; CRITICAL ILLNESS; DISEASE SEVERITY; DOSE RESPONSE; DYING; FIRMICUTES; HISTOPATHOLOGY; INFECTION SENSITIVITY; INTESTINE FLORA; MICROBIAL COMMUNITY; MOUSE; NONHUMAN; PROTEOBACTERIA; RNA SEQUENCE; VERRUCOMICROBIA; WEIGHT REDUCTION;

ANIMALS; ANTI-BACTERIAL AGENTS; BACTERIA; CLOSTRIDIUM DIFFICILE; CLOSTRIDIUM INFECTIONS; COLITIS; DISEASE MODELS, ANIMAL; GASTROINTESTINAL TRACT; HUMANS; METAGENOME; MICE; MICE, INBRED C57BL;

ANIMALIA; CLOSTRIDIUM DIFFICILE; FIRMICUTES; MURINAE; PROTEOBACTERIA;

EID: 80051717743     PISSN: 19490976     EISSN: 19490984     Source Type: Journal    
DOI: 10.4161/gmic.2.3.16333     Document Type: Article

References (66)

1. Ley RE, Peterson DA, Gordon JI. Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell 2006; 124:837-48.
2. Dethlefsen L, McFall-Ngai M, Relman DA. An ecological and evolutionary perspective on human-microbe mutualism and disease. Nature 2007; 449:811-8.
3. Yap IK, Li JV, Saric J, Martin FP, Davies H, Wang Y, et al. Metabolomic and microbiological analysis of the dynamic effect of vancomycin-induced gut microbiota modification in the mouse. J Proteome Res 2008; 7:3718-28.
4. Stappenbeck TS, Hooper LV, Gordon JI. Developmental regulation of intestinal angiogenesis by indigenous microbes via Paneth cells. Proc Natl Acad Sci USA 2002; 99:15451-5.
5. Hooper LV. Bacterial contributions to mammalian gut development. Trends Microbiol 2004; 12:129-34.
6. Ivanov II, Atarashi K, Manel N, Brodie EL, Shima T, Karaoz U, et al. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 2009; 139:485-98.
7. Ivanov II, Frutos Rde L, Manel N, Yoshinaga K, Rifkin DB, Sartor RB, et al. Specific microbiota direct the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine. Cell Host Microbe 2008; 4:337-49.
8. van der Waaij D, Berghuis JM, Lekkerkerk-van der Wees JEC. Colonization resistance of the digestive tract in conventional and antibiotic-treated mice. J Hyg 1971; 69:405-11.
9. Sekirov I, Finlay BB. The role of the intestinal microbiota in enteric infection. J Physiol 2009; 587:4159-67.
10. Hall I, O'Toole E. Intestinal flora in newborn infants with the description of a new anaerobic pathogen, Bacillus difficilus. Am J Dis Child 1935; 49:390-402.
11. McDonald LC, Killgore GE, Thompson A, Owens RC Jr, Kazakova SV, Sambol SP, et al. An epidemic, toxin gene-variant strain of Clostridium difficile. N Engl J Med 2005; 353:2433-41.
12. Pepin J, Valiquette L, Alary ME, Villemure P, Pelletier A, Forget K, et al. Clostridium difficile-associated diarrhea in a region of Quebec from 1991 to 2003: a changing pattern of disease severity. CMAJ 2004; 171:466-72.
13. Kelly CP, Lamont JT. Clostridium difficile-more difficult than ever. N Engl J Med 2008; 359:1932-40.
14. Paterson DL. ''Collateral damage'' from cephalosporin or quinolone antibiotic therapy. Clin Infect Dis 2004; 38:341-5.
15. Wilson KH. The microecology of Clostridium difficile. Clin Infect Dis 1993; 16:214-8.
16. Maroo S, Lamont JT. Recurrent Clostridium difficile. Gastroenterology 2006; 130:1311-6.
17. Chang JY, Antonopoulos DA, Kalra A, Tonelli A, Khalife WT, Schmidt TM, et al. Decreased diversity of the fecal microbiome in recurrent Clostridium difficileassociated diarrhea. J Infect Dis 2008; 197:435-8.
18. Bartlett JG, Onderdonk AB, Cisneros RL, Kasper DL. Clindamycin-associated colitis due to a toxin-producing species of Clostridium in hamsters. J Infectious Disease 1977; 136:701-5.
19. Onderdonk A, Cisneros RL, Bartlett JG. Clostridium difficile in gnotobiotic mice. Infect Immun 1980; 28:227-82.
20. Wilson KH, Freter R. Interaction of Clostridium difficile and Escherichia coli with microfloras in continuousflow cultures and gnotobiotic mice. Infect Immun 1986; 54:354-8.
21. Pawlowski SW, Calabrese G, Kolling GL, Freire R, AlcantaraWarren C, Liu B, et al. Murine model of Clostridium difficile infection with aged gnotobiotic C57BL/6 mice and a BI/NAP1 strain. J Infect Dis 2010; 202:1708-12.
22. Lawley TD, Clare S, Walker AW, Goulding D, Stabler RA, Croucher N, et al. Antibiotic treatment of Clostridium difficile carrier mice triggers a supershedder state, spore-mediated transmission and severe disease in immunocompromised hosts. Infect Immun 2009; 77:3661-9.
23. Chen X, Katchar K, Goldsmith JD, Nanthakumar N, Cheknis A, Gerding DN, et al. A mouse model of Clostridium difficile-associated disease. Gastroenterology 2008; 135:1984-92.
24. Jarchum I, Liu M, Lipuma L, Pamer EG. Toll-Like receptor 5 stimulation protects mice from acute Clostridium difficile colitis. Infect Immun 2011; 79:1498-503.
25. Voth D, Ballard J. Clostridium difficile toxins, mechanisms of action and role in disease. Clin Microbiol Rev 2005; 18:247-63.
26. Antonopoulos DA, Huse SM, Morrison HG, Schmidt TM, Sogin ML, Young VB. Reproducible community dynamics of the gastrointestinal microbiota following antibiotic perturbation. Infect Immun 2009; 77:2367-75.
27. van der Waaij D, Berghuis-de Vries JM, Lekkerkerk LV. Colonization resistance of the digestive tract in conventional and antibiotic-treated mice. J Hyg (Lond) 1971; 69:405-11.
28. Freter R. In vivo and in vitro antagonism of intestinal bacteria against Shigella flexneri. II. The inhibitory mechanism. J Infect Dis 1962; 110:38-46.
29. Hentges DJ, Freter R. In vivo and in vitro antagonism of intestinal bacteria against Shigella flexneri. I. Correlation between various tests. J Infect Dis 1962; 110:30-7.
30. Robinson CJ, Bohannan BJ, Young VB. From structure to function: the ecology of host-associated microbial communities. Microbiol Mol Biol Rev 2010; 74:453-76.
31. Pultz NJ, Donskey CJ. Effect of antibiotic treatment on growth of and toxin production by Clostridium difficile in the cecal contents of mice. Antimicrob Agents Chemother 2005; 49:3529-32.
32. Wilson KH, Silva J, Fekety FR. Suppression of Clostridium difficile by normal hamster cecal flora and prevention of antibiotic-associated cecitis. Infect Immun 1981; 34:626-8.
33. Blondeau JM. What have we learned about antimicrobial use and the risks for Clostridium difficile-associated diarrhoea? J Antimicrob Chemother 2009; 63:238-42.
34. Jump RL, Li Y, Pultz MJ, Kypriotakis G, Donskey CJ. Tigecycline exhibits inhibitory activity against Clostridium difficile in the colon of mice and does not promote growth or toxin production. Antimicrob Agents Chemother 2011; 55:546-9.
35. Nerandzic MM, Donskey CJ. Effect of ceftobiprole treatment on growth of and toxin production by Clostridium difficile in cecal contents of mice. Antimicrob Agents Chemother 2011; 55:2174-7.
36. Dethlefsen L, Huse S, Sogin ML, Relman DA. The pervasive effects of an antibiotic on the human gut microbiota, as revealed by deep 16S rRNA sequencing. PLoS Biol 2008; 6:280.
37. Dethlefsen L, Relman DA. Incomplete recovery and individualized responses of the human distal gut microbiota to repeated antibiotic perturbation. Proc Natl Acad Sci USA 2011; 108:4554-61.
38. Stecher B, Chaffron S, Kappeli R, Hapfelmeier S, Freedrich S, Weber TC, et al. Like will to like: abundances of closely related species can predict susceptibility to intestinal colonization by pathogenic and commensal bacteria. PLoS Pathog 2010; 6:1000711.
39. Cash HL, Whitham CV, Behrendt CL, Hooper LV. Symbiotic bacteria direct expression of an intestinal bactericidal lectin. Science 2006; 313:1126-30.
40. Lehotzky RE, Partch CL, Mukherjee S, Cash HL, Goldman WE, Gardner KH, et al. Molecular basis for peptidoglycan recognition by a bactericidal lectin. Proc Natl Acad Sci USA 2010; 107:7722-7.
41. Brandl K, Plitas G, Mihu CN, Ubeda C, Jia T, Fleisher M, et al. Vancomycin-resistant enterococci exploit antibiotic-induced innate immune deficits. Nature 2008; 455:804-7.
42. Kyne L, Warny M, Qamar A, Kelly CP. Association between antibody response to toxin A and protection against recurrent Clostridium difficile diarrhoea. Lancet 2001; 357:189-93.
43. Permpoonpattana P, Hong HA, Phetcharaburanin J, Huang JM, Cook J, Fairweather NF, et al. Immunisation with Bacillus spores expressing toxin A peptide repeats protects against infection with toxin A+ B+ strains of Clostridium difficile. Infect Immun 2011.
44. Leav BA, Blair B, Leney M, Knauber M, Reilly C, Lowy I, et al. Serum anti-toxin B antibody correlates with protection from recurrent Clostridium difficile infection (CDI). Vaccine 2010; 28:965-9.
45. Pechine S, Janoir C, Boureau H, Gleizes A, Tsapis N, Hoys S, et al. Diminished intestinal colonization by Clostridium difficile and immune response in mice after mucosal immunization with surface proteins of Clostridium difficile. Vaccine 2007; 25:3946-54.
46. Ghose C, Kalsy A, Sheikh A, Rollenhagen J, John M, Young J, et al. Transcutaneous immunization with Clostridium difficile toxoid A induces systemic and mucosal immune responses and toxin A-neutralizing antibodies in mice. Infect Immun 2007; 75:2826-32.
47. Hasegawa M, Yamazaki T, Kamada N, Tawaratsumida K, Kim YG, Nunez G, et al. Nucleotide-binding oligomerization domain 1 mediates recognition of Clostridium difficile and induces neutrophil recruitment and protection against the pathogen. J Immunol 2011; 186:4872-80.
48. Wlodarska M, Willing B, Keeney KM, Menendez A, Bergstrom KS, Gill N, et al. Antibiotic treatment alters the colonic mucus layer and predisposes the host to exacerbated Citrobacter rodentium-induced colitis. Infect Immun 2011; 79:1536-45.
49. Ghosh S, Dai C, Brown K, Rajendiran E, Makarenko S, Baker J, 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 2011; 301: G39-49.
50. Romick-Rosendale LE, Goodpaster AM, Hanwright PJ, Patel NB, Wheeler ET, Chona DL, et al. NMRbased metabonomics analysis of mouse urine and fecal extracts following oral treatment with the broadspectrum antibiotic enrofloxacin (Baytril). Magn Reson Chem 2009; 47:36-46.
51. Barcenilla A, Pryde SE, Martin JC, Duncan SH, Stewart CS, Henderson C, et al. Phylogenetic relationships of butyrate-producing bacteria from the human gut. Appl Environ Microbiol 2000; 66:1654-61.
52. Pryde SE, Duncan SH, Hold GL, Stewart CS, Flint HJ. The microbiology of butyrate formation in the human colon. FEMS Microbiol Lett 2002; 217:133-9.
53. Wong JM, de Souza R, Kendall CW, Emam A, Jenkins DJ. Colonic health: fermentation and short chain fatty acids. J Clin Gastroenterol 2006; 40:235-43.
54. May T, Mackie RI, Fahey GC Jr, Cremin JC, Garleb KA. Effect of fiber source on short-chain fatty acid production and on the growth and toxin production by Clostridium difficile. Scand J Gastroenterol 1994; 29:916-22.
55. Young VB, Knox KA, Pratt JS, Cortez JS, Mansfield LS, Rogers AB, et al. In vitro and in vivo characterization of Helicobacter hepaticus cytolethal distending toxin mutants. Infect Immun 2004; 72:2521-7.
56. Kelly CP, Becker S, Linevsky JK, Joshi MA, O'Keane JC, Dickey BF, et al. Neutrophil recruitment in Clostridium difficile toxin A enteritis in the rabbit. J Clin Invest 1994; 93:1257-65.
57. Pace N, Stahl D, Lane D, Olsen G. Analyzing natural microbial populations by rRNA sequences. ASM News 1985; 51:4-12.
58. Pace NR. A molecular view of microbial diversity and the biosphere. Science 1997; 276:734-40.
59. Schmidt TM, Relman DA. Phylogenetic identification of uncultured pathogens using ribosomal RNA sequences. Methods Enzymol 1994; 235:205-22.
60. Cole JR, Chai B, Marsh TL, Farris RJ, Wang Q, et al. The Ribosomal Database Project (RDP-II): previewing a new autoaligner that allows regular updates and the new prokaryotic taxonomy. Nucleic Acids Res 2003; 31:442-3.
61. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, et al. Introducing mothur: opensource, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 2009; 75:7537-41.
62. Kumar S, Nei M, Dudley J, Tamura K. MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief Bioinform 2008; 9:299-306.
63. Nadkarni MA, Martin FE, Jacques NA, Hunter N. Determination of bacterial load by real-time PCR using a broad-range (universal) probe and primers set. Microbiology 2002; 148:257-66.
64. Nitsche A, Becker M, Junghahn I, Aumann J, Landt O, Fichtner I, et al. Quantification of human cells in NOD/SCID mice by duplex real-time polymerasechain reaction. Haematologica 2001; 86:693-9.
65. Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 2008; 3:1101-8.
66. Corthier G, Dubos F, Raibaud P. Modulation of cytotoxin production by Clostridium difficile in the intestinal tracts of gnotobiotic mice inoculated with various human intestinal bacteria. Appl Environ Microbiol 1985; 49:250-2.