Muricholic Acids Inhibit Clostridium difficile Spore Germination and Growth

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Francis, Michael B ^a   Allen, Charlotte A ^a   Sorg, Joseph A ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIINFECTIVE AGENT; MURICHOLIC ACID DERIVATIVE; UNCLASSIFIED DRUG;

ANTIBACTERIAL ACTIVITY; ARTICLE; BACTERIAL GROWTH; BACTERIUM ISOLATE; CLOSTRIDIUM DIFFICILE; CONTROLLED STUDY; DRUG STRUCTURE; ENZYME KINETICS; GROWTH INHIBITION; MICHAELIS MENTEN KINETICS; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; OXIDATION; SPORE GERMINATION;

ANIMALS; CHOLIC ACIDS; CLOSTRIDIUM DIFFICILE; ENTEROCOLITIS, PSEUDOMEMBRANOUS; HUMANS; KINETICS; MICE; MICROBIAL SENSITIVITY TESTS; MICROBIAL VIABILITY; MOLECULAR STRUCTURE; SPECIES SPECIFICITY; SPORES, BACTERIAL;

EID: 84883621976     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0073653     Document Type: Article

References (54)

1. Kyne L, Hamel MB, Polavaram R, Kelly CP, (2002) Health care costs and mortality associated with nosocomial diarrhea due to Clostridium difficile. Clin Infect Dis 34: 346-353.
2. O'Brien JA, Lahue BJ, Caro JJ, Davidson DM, (2007) The emerging infectious challenge of Clostridium difficile-associated disease in Massachusetts hospitals: clinical and economic consequences. Infect Control Hosp Epidemiol 28: 1219-1227.
3. Czuprynski CJ, Johnson WJ, Balish E, Wilkins T, (1983) Pseudomembranous colitis in Clostridium difficile-monoassociated rats. Infect Immun 39: 1368-1376.
4. Reeves AE, Koenigsknecht MJ, Bergin IL, Young VB, (2012) Suppression of Clostridium difficile in the gastrointestinal tracts of germfree mice inoculated with a murine isolate from the family Lachnospiraceae. Infect Immun 80: 3786-3794.
5. Pawlowski SW, Calabrese G, Kolling GL, Platts-Mills J, Freire R, et al. (2010) Murine model of Clostridium difficile infection with aged gnotobiotic C57BL/6 mice and a BI/NAP1 strain. J Infect Dis 202: 1708-1712.
6. Steele J, Feng H, Parry N, Tzipori S, (2010) Piglet models of acute or chronic Clostridium difficile illness. J Infect Dis 201: 428-434.
7. Bartlett JG, Chang BJ, Moon N, Onderdonk AB, (1978) Antibiotic-induced lethal entercolitis in hamsters: studies with eleven agents and evidence to support the pathogenic role of toxin-producing Clostridia. Am J Vet Res 39: 1525-1530.
8. Fekety FR, Silva J, Toshniwal R, Allo M, Armstrong J, et al. (1979) Antibiotic-associated colitis: effects of antibiotics on Clostridium difficile and the disease in hamsters. Rev Infect Dis 1: 386-397.
9. Sambol SP, Tang JK, Merrigan MM, Johnson S, Gerding DN, (2001) Infection of hamsters with epidemiologically important strains of Clostridium difficile. J Infect Dis 183: 1760-1766.
10. Kuehne SA, Cartman ST, Heap JT, Kelly ML, Cockayne A, et al. (2010) The role of toxin A and toxin B in Clostridium difficile infection. Nature 467: 711-713.
11. Lyras D, O'Connor JR, Howarth PM, Sambol SP, Carter GP, et al. (2009) Toxin B is essential for virulence of Clostridium difficile. Nature doi:10.1038/nature07822.
12. Borriello SP, Ketley JM, Mitchell TJ, Barclay FE, Welch AR, et al. (1987) Clostridium difficile-a spectrum of virulence and analysis of putative virulence determinants in the hamster model of antibiotic-associated colitis. J Med Microbiol 24: 53-64.
13. Lawley TD, Clare S, Walker AW, Goulding D, Stabler RA, et al. (2009) Antibiotic treatment of Clostridium difficile carrier mice triggers a supershedder state, spore-mediated transmission, and severe disease in immunocompromised hosts. Infect Immun 77: 3661-3669.
14. Chen X, Katchar K, Goldsmith JD, Nanthakumar N, Cheknis A, et al. (2008) A mouse model of Clostridium difficile-associated disease. Gastroenterology 135: 1984-1992.
15. Reeves AE, Theriot CM, Bergin IL, Huffnagle GB, Schloss PD, et al. (2011) The interplay between microbiome dynamics and pathogen dynamics in a murine model of Clostridium difficile Infection. Gut Microbes 2: 145-158.
16. Buffie CG, Jarchum I, Equinda M, Lipuma L, Gobourne A, et al. (2012) Profound alterations of intestinal microbiota following a single dose of clindamycin results in sustained susceptibility to Clostridium difficile-induced colitis. Infect Immun 80: 62-73.
17. Lawley TD, Clare S, Walker AW, Stares MD, Connor TR, et al. (2012) Targeted restoration of the intestinal microbiota with a simple, defined bacteriotherapy resolves relapsing Clostridium difficile disease in mice. PLoS Pathog 8: e1002995.
18. Marsh JW, Arora R, Schlackman JL, Shutt KA, Curry SR, et al. (2012) Recurrent Clostridium difficile Disease: Association of Relapse with BI/NAP1/027. J Clin Microbiol.
19. van Nood E, Vrieze A, Nieuwdorp M, Fuentes S, Zoetendal EG, et al. (2013) Duodenal infusion of donor feces for recurrent Clostridium difficile. N Engl J Med 368: 407-415.
20. Howerton A, Patra M, Abel-Santos E (2013) A new strategy for the prevention of Clostridium difficile infections. J Infect Dis.
21. Jarchum I, Liu M, Lipuma L, Pamer EG, (2011) Toll-like receptor 5 stimulation protects mice from acute Clostridium difficile colitis. Infect Immun 79: 1498-1503.
22. Jarchum I, Liu M, Shi C, Equinda M, Pamer EG, (2012) Critical role for MyD88-mediated neutrophil recruitment during Clostridium difficile colitis. Infect Immun 80: 2989-2996.
23. Antonopoulos DA, Huse SM, Morrison HG, Schmidt TM, Sogin ML, et al. (2009) Reproducible community dynamics of the gastrointestinal microbiota following antibiotic perturbation. Infect Immun 77: 2367-2375.
24. Britton RA, Young VB, (2012) Interaction between the intestinal microbiota and host in Clostridium difficile colonization resistance. Trends Microbiol 20: 313-319.
25. Alnouti Y, Csanaky IL, Klaassen CD, (2008) Quantitative-profiling of bile acids and their conjugates in mouse liver, bile, plasma, and urine using LC-MS/MS. J Chromatogr B Analyt Technol Biomed Life Sci 873: 209-217.
26. Eyssen H, Smets L, Parmentier G, Janssen G, (1977) Sex-linked differences in bile acid metabolism of germfree rats. Life Sci 21: 707-712.
27. Ridlon JM, Kang D, Hylemon PB, (2006) Bile salt biotransformations by human intestinal bacteria. J Lipid Res 47: 241-259.
28. Hong YJ, Turowski M, Lin JT, Yokoyama WH, (2007) Simultaneous characterization of bile acid, sterols, and determination of acylglycerides in feces from soluble cellulose-fed hamsters using HPLC with evaporative light-scattering detection and APCI-MS. J Agric Food Chem 55: 9750-9757.
29. Benson GM, Haskins NJ, Eckers C, Moore PJ, Reid DG, et al. (1993) Polydeoxycholate in human and hamster feces: a major product of cholate metabolism. J Lipid Res 34: 2121-2134.
30. Une M, Yamanaga K, Mosbach EH, Tsujimura K, Hoshita T, (1990) Metabolism of 7 beta-alkyl chenodeoxycholic acid analogs and their effect on cholesterol metabolism in hamsters. J Lipid Res 31: 1015-1021.
31. Sorg JA, Sonenshein AL, (2008) Bile salts and glycine as cogerminants for Clostridium difficile spores. J Bacteriol 190: 2505-2512.
32. Wilson KH, Kennedy MJ, Fekety FR, (1982) Use of sodium taurocholate to enhance spore recovery on a medium selective for Clostridium difficile. J Clin Microbiol 15: 443-446.
33. Sorg JA, Sonenshein AL, (2009) Chenodeoxycholate is an inhibitor of Clostridium difficile spore germination. J Bacteriol 191: 1115-1117.
34. Sorg JA, Sonenshein AL, (2010) Inhibiting the initiation of Clostridium difficile spore germination using analogs of chenodeoxycholic acid, a bile acid. J Bacteriol 192: 4983-4990.
35. Wheeldon LJ, Worthington T, Hilton AC, Elliot TS, Lambert PA, (2008) Physical and chemical factors influencing the germination of Clostridium difficile spores. Journal of Applied Microbiology 105: 2223-2230.
36. Howerton A, Ramirez N, Abel-Santos E, (2011) Mapping interactions between germinants and Clostridium difficile spores. J Bacteriol 193: 274-282.
37. Hofmann AF, (1999) The continuing importance of bile acids in liver and intestinal disease. Arch Intern Med 159: 2647-2658.
38. Francis MB, Allen CA, Shrestha R, Sorg JA, (2013) Bile Acid Recognition by the Clostridium difficile Germinant Receptor, CspC, Is Important for Establishing Infection. PLoS Pathog 9: e1003356.
39. Lawley TD, Croucher NJ, Yu L, Clare S, Sebaihia M, et al. (2009) Proteomic and genomic characterization of highly infectious Clostridium difficile 630 spores. J Bacteriol 191: 5377-5386.
40. Larson HE, Borriello SP, (1990) Quantitative study of antibiotic-induced susceptibility to Clostridium difficile enterocecitis in hamsters. Antimicrob Agents Chemother 34: 1348-1353.
41. Killgore G, Thompson A, Johnson S, Brazier J, Kuijper E, et al. (2008) Comparison of seven techniques for typing international epidemic strains of Clostridium difficile: restriction endonuclease analysis, pulsed-field gel electrophoresis, PCR-ribotyping, multilocus sequence typing, multilocus variable-number tandem-repeat analysis, amplified fragment length polymorphism, and surface layer protein A gene sequence typing. J Clin Microbiol 46: 431-437.
42. Allen CA, Babakhani F, Sears P, Nguyen L, Sorg JA, (2013) Both Fidaxomicin and Vancomycin Inhibit Outgrowth of Clostridium difficile Spores. Antimicrob Agents Chemother 57: 664-667.
43. Drudy D, Harnedy N, Fanning S, O'Mahony R, Kyne L, (2007) Isolation and characterisation of toxin A-negative, toxin B-positive Clostridium difficile in Dublin, Ireland. Clin Microbiol Infect 13: 298-304.
44. Liggins M, Ramirez N, Magnuson N, Abel-Santos E, (2011) Progesterone analogs influence germination of Clostridium sordellii and Clostridium difficile spores in vitro. J Bacteriol 193: 2776-2783.
45. Ramirez N, Liggins M, Abel-Santos E, (2010) Kinetic evidence for the presence of putative germination receptors in Clostridium difficile spores. J Bacteriol 192: 4215-4222.
46. Eyssen H, De Pauw G, Stragier J, Verhulst A, (1983) Cooperative formation of omega-muricholic acid by intestinal microorganisms. Appl Environ Microbiol 45: 141-147.
47. Eyssen HJ, De Pauw G, Van Eldere J, (1999) Formation of hyodeoxycholic acid from muricholic acid and hyocholic acid by an unidentified gram-positive rod termed HDCA-1 isolated from rat intestinal microflora. Appl Environ Microbiol 65: 3158-3163.
48. Akoachere M, Squires RC, Nour AM, Angelov L, Brojatsch J, et al. (2007) Indentification of an in vivo inhibitor of Bacillus anthracis spore germination. J Biol Chem 282: 12112-12118.
49. Ramirez N, Abel-Santos E, (2010) Requirements for germination of Clostridium sordellii spores in vitro. J Bacteriol 192: 418-425.
50. Dodatko T, Akoachere M, Jimenez N, Alvarez Z, Abel-Santos E, (2010) Dissecting interactions between nucleosides and germination receptors in Bacillus cereus 569 spores. Microbiology 156: 1244-1255.
51. Alnouti Y, Csanaky IL, Klaassen CD, (2008) Quantitative-profiling of bile acids and their conjugates in mouse liver, bile, plasma, and urine using LC-MS/MS. Journal of Chromatography B 873: 209-217.
52. Northfield T, McColl I, (1973) Postprandial concentrations of free and conjugated bile acids down the length of the normal human small intestine. Gut 14: 513-518.
53. Hamilton JP, Xie G, Raufman J-P, Hogan S, Griffin TL, et al. (2007) Human cecal bile acids: concentration and spectrum. Am J Physiol Gastrointest Liver Physiol 293: G256-263.
54. Miyata M, Takamatsu Y, Kuribayashi H, Yamazoe Y, (2009) Administration of ampicillin elevates hepatic primary bile acid synthesis through suppression of ileal fibroblast growth factor 15 expression. J Pharmacol Exp Ther 331: 1079-1085.