Lactobacillus acidophilus modulates the virulence of Clostridium difficile

Journal of Dairy Science

Volumn 97, Issue 8, 2014, Pages 4745-4758

  Yun, B ^a   Oh, S ^a   Griffiths, M W ^b  

^a Chonnam National University   (South Korea)

^b UNIVERSITY OF GUELPH   (Canada)

Author keywords

Autoinducer 2; Clostridium difficile ribotype 027; Lactobacillus acidophilus GP1B; Quorum sensing

Indexed keywords

BACTERIAL PROTEIN; BACTERIAL RNA; BACTERIAL TOXIN; ENTEROTOXIN; HOMOSERINE; LACTONE; N-OCTANOYLHOMOSERINE LACTONE; PROBIOTIC AGENT; TCDA PROTEIN, CLOSTRIDIUM DIFFICILE; TOXB PROTEIN, CLOSTRIDIUM DIFFICILE;

ANALOGS AND DERIVATIVES; ANALYSIS; ANIMAL; C57BL MOUSE; DIARRHEA; DOWN REGULATION; FEMALE; FOOD CONTAMINATION; FOOD CONTROL; GASTROINTESTINAL TRACT; GENETICS; HUMAN; LACTOBACILLUS ACIDOPHILUS; METABOLISM; MICROBIOLOGY; MICROFLORA; MOUSE; PATHOGENICITY; PEPTOCLOSTRIDIUM DIFFICILE; PHYSIOLOGY; PREVENTION AND CONTROL; VIRULENCE;

ANIMALS; BACTERIAL PROTEINS; BACTERIAL TOXINS; CLOSTRIDIUM DIFFICILE; DIARRHEA; DOWN-REGULATION; ENTEROTOXINS; FEMALE; FOOD CONTAMINATION; FOOD MICROBIOLOGY; GASTROINTESTINAL TRACT; HOMOSERINE; HUMANS; LACTOBACILLUS ACIDOPHILUS; LACTONES; MICE; MICE, INBRED C57BL; MICROBIOTA; PROBIOTICS; RNA, BACTERIAL; VIRULENCE;

EID: 84904416174     PISSN: 00220302     EISSN: 15253198     Source Type: Journal    
DOI: 10.3168/jds.2014-7921     Document Type: Article

References (69)

1. Asahara T., Shimizu K., Nomoto K., Hamabata T., Ozawa A., Takeda Y. Probiotic bifidobacteria protect mice from lethal infection with Shiga toxin-producing Escherichia coli O157:H7. Infect. Immun. 2004, 72:2240-2247.
2. Bahrami B., Macfarlane S., Macfarlane G.T. Induction of cytokine formation by human intestinal bacteria in gut epithelial cell lines. J. Appl. Microbiol. 2011, 110:353-363.
3. Bai A.J., Rai V.R. Bacterial quorum sensing and food industry. Comp. Rev. Food Sci. Food Safety 2011, 10:183-193. 10.1111/j.1541-4337.2011.00150.x.
4. Bakri M.M., Brown D.J., Butcher J.P., Sutherland A.D. Clostridium difficile in ready-to-eat salads, Scotland. Emerg. Infect. Dis. 2009, 15:817-818.
5. Barbut F., Corthier G., Charpak Y., Cerf M., Monteil H., Fosse T., Trevoux A., De Barbeyrac B., Boussougant Y., Tigaud S. Prevalence and pathogenicity of Clostridium difficile in hospitalized patients: A French multicenter study. Arch. Intern. Med. 1996, 156:1449-1454.
6. Bartlett J.G. Antibiotic-associated diarrhea. N. Engl. J. Med. 2002, 346:334-339.
7. Bartlett J.G. Historical perspectives on studies of Clostridium difficile and C. difficile infection. Clin. Infect. Dis. 2008, 46:S4-S11.
8. Brashears M.M., Reilly S.S., Gilliland S.E. Antagonistic action of cells of Lactobacillus lactis toward Escherichia coli O157:H7 on refrigerated raw chicken meat. J. Food Prot. 1998, 61:166-170.
9. Carey C.M., Kostrzynska M., Ojha S., Thompson S. The effect of probiotics and organic acids on Shiga-toxin 2 gene expression in enterohemorrhagic Escherichia coli O157:H7. J. Microbiol. Methods 2008, 73:125-132.
10. Carter G.P., Purdy D., Williams P., Minton N.P. Quorum sensing in Clostridium difficile: Analysis of a luxS-type signalling system. J. Med. Microbiol. 2005, 54:119-127.
11. Carter G.P., Rood J.I., Lyras D. The role of toxin A and toxin B in the virulence of Clostridium difficile. Trends Microbiol. 2012, 20:21-29.
12. Chapman C.M.C., Gibson G.R., Rowland I. In vitro evaluation of single- and multi-strain probiotics: Inter-species inhibition between probiotic strains, and inhibition of pathogens. Anaerobe 2012, 18:405-413.
13. Chateau N., Castellanos I., Deschamps A.M. Distribution of pathogen inhibition in the Lactobacillus isolates of a commercial probiotic consortium. J. Appl. Bacteriol. 1993, 74:36-40.
14. Chen X., Katchar K., Goldsmith J.D., Nanthakumar N., Cheknis A., Gerding D.N., Kelly C.P. A mouse model of Clostridium difficile-associated disease. Gastroenterology 2008, 135:1984-1992.
15. Davies A.H., Roberts A.K., Shone C.C., Acharya K.R. Super toxins from a super bug: Structure and function of Clostridium difficile toxins. Biochem. J. 2011, 436:517-526.
16. Dethlefsen L., Eckburg P.B., Bik E.M., Relman D.A. Assembly of the human intestinal microbiota. Trends Ecol. Evol. 2006, 21:517-523.
17. Dethlefsen L., Huse S., Sogin M.L., Relman D.A. The pervasive effects of an antibiotic on the human gut microbiota, as revealed by deep 16S rRNA sequencing. PLoS Biol. 2008, 6:e280.
18. Ewaschuk J.B., Dieleman L.A. Probiotics and prebiotics in chronic inflammatory bowel diseases. World J. Gastroenterol. 2006, 12:5941-5950.
19. Fayol-Messaoudi D., Berger C.N., Coconnier-Polter M.H., Liévin-Le Moal V., Servin A.L. pH-, lactic acid-, and non-lactic acid-dependent activities of probiotic lactobacilli against Salmonella enterica serovar Typhimurium. Appl. Environ. Microbiol. 2005, 71:6008-6013.
20. Floch M.H., Walker W.A., Madsen K., Sanders M.E., Macfarlane G.T., Flint H.J., Dieleman L.A., Ringel Y., Guandalini S., Kelly C.P. Recommendations for probiotic use-2011 update. J. Clin. Gastroenterol. 2011, 45:S168-S171.
21. Guglielmetti S., Mora D., Gschwender M., Popp K. Randomised clinical trial: Bifidobacterium bifidum MIMBb75 significantly alleviates irritable bowel syndrome and improves quality of life-A double-blind, placebo-controlled study. Aliment. Pharmacol. Ther. 2011, 33:1123-1132.
22. Han K.-S., Kim Y., Kim S.H., Oh S. Characterization and purification of acidocin 1B, a bacteriocin produced by Lactobacillus acidophilus GP1B. J. Microbiol. Biotechnol. 2007, 17:774-783.
23. Hell M., Bernhofer C., Stalzer P., Kern J.M., Claassen E. Probiotics in Clostridium difficile infection: Reviewing the need for a multistrain probiotic. Benef. Microbes. 2013, 4:39-51.
24. Holzapfel W.H., Geisen R., Schillinger U. Biological preservation of foods with reference to protective cultures, bacteriocins and food-grade enzymes. Int. J. Food Microbiol. 1995, 24:343-362.
25. Jernberg C., Löfmark S., Edlund C., Jansson J.K. Long-term ecological impacts of antibiotic administration on the human intestinal microbiota. ISME J. 2007, 1:56-66.
26. Jöbstl M., Heuberger S., Indra A., Nepf R., Köfer J., Wagner M. Clostridium difficile in raw products of animal origin. Int. J. Food Microbiol. 2010, 138:172-175.
27. Kaper J.B., Sperandio V. Bacterial cell-to-cell signaling in the gastrointestinal tract. Infect. Immun. 2005, 73:3197-3209.
28. Kaplan E.L., Meier P. Nonparametric estimation from incomplete observations. J. Am. Stat. Assoc. 1958, 53:457-481.
29. Katz J.A. Probiotics for the prevention of antibiotic-associated diarrhea and Clostridium difficile diarrhea. J. Clin. Gastroenterol. 2006, 40:249-255.
30. Kim Y., Lee J.W., Kang S.G., Oh S., Griffiths M.W. Bifidobacterium spp. influences the production of autoinducer-2 and biofilm formation by Escherichia coli O157:H7. Anaerobe 2012, 18:539-545.
31. Kuehne S.A., Cartman S.T., Heap J.T., Kelly M.L., Cockayne A., Minton N.P. The role of toxin A and toxin B in Clostridium difficile infection. Nature 2010, 467:711-713.
32. Lee A.S.Y., Song K.P. LuxS/autoinducer-2 quorum sensing molecule regulates transcriptional virulence gene expression in Clostridium difficile. Biochem. Biophys. Res. Commun. 2005, 335:659-666.
33. Lee K.M., Kim W.S., Lim J., Nam S., Youn M., Nam S.W., Kim Y., Kim S.H., Park W., Park S. Antipathogenic properties of green tea polyphenol epigallocatechin gallate at concentrations below the MIC against enterohemorrhagic Escherichia coli O157:H7. J. Food Prot. 2009, 72:325-331.
34. Lenoir-Wijnkoop I., Sanders M.E., Cabana M.D., Caglar E., Corthier G., Rayes N., Sherman P.M., Timmerman H.M., Vaneechoutte M., Loo J.V., Wolvers D.A.W. Probiotic and prebiotic influence beyond the intestinal tract. Nutr. Rev. 2007, 65:469-489.
35. Ley R.E., Peterson D.A., Gordon J.I. Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell 2006, 124:837-848.
36. Limdi J.K., O'Neill C., McLaughlin J. Do probiotics have a therapeutic role in gastroenterology?. World J. Gastroenterol. 2006, 12:5447-5457.
37. Löfmark S., Jernberg C., Jansson J.K., Edlund C. Clindamycin-induced enrichment and long-term persistence of resistant Bacteroides spp. and resistance genes. J. Antimicrob. Chemother. 2006, 58:1160-1167.
38. Mani N., Dupuy B. Regulation of toxin synthesis in Clostridium difficile by an alternative RNA polymerase sigma factor. Proc. Natl. Acad. Sci. USA 2001, 98:5844-5849.
39. Maslowski K.M., Vieira A.T., Ng A., Kranich J., Sierro F., Di Y., Schilter H.C., Rolph M.S., Mackay F., Artis D., Xavier R.J., Teixeira M.M., Mackay C.R. Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature 2009, 461:1282-1286.
40. McDonald L.C., Killgore G.E., Thompson A., Owens R.C., Kazakova S.V., Sambol S.P., Johnson S., Gerding D.N. An epidemic, toxin gene-variant strain of Clostridium difficile. N. Engl. J. Med. 2005, 353:2433-2441.
41. McGroarty J.A., Reid G. Detection of a Lactobacillus substance that inhibits Escherichia coli. Can. J. Microbiol. 1988, 34:974-978.
42. Medellin-Peña M.J., Wang H., Johnson R., Anand S., Griffiths M.W. Probiotics affect virulence-related gene expression in Escherichia coli O157:H7. Appl. Environ. Microbiol. 2007, 73:4259-4267.
43. Mellefont L.A., McMeekin T.A., Ross T. Effect of relative inoculum concentration on Listeria monocytogenes growth in co-culture. Int. J. Food Microbiol. 2008, 121:157-168.
44. Metcalf D., Sharif S., Weese J.S. Evaluation of candidate reference genes in Clostridium difficile for gene expression normalization. Anaerobe 2010, 16:439-443.
45. Meurman J.H., Antila H., Korhonen A., Salminen S. Effect of Lactobacillus rhamnosus strain GG (ATCC 53103) on the growth of Streptococcus sobrinus in vitro. Eur. J. Oral Sci. 1995, 103:253-258.
46. Mundi A., Delcenserine V., Amiri-Jami M., Moorhead S., Griffiths M.W. Cell-free preparation of Lactobacillus acidophilus strain La-5 and Bifidobacterium longum strain NCC2705 affect virulence gene expression in Campylobacter jejuni. J. Food Prot. 2013, 76:1740-1746.
47. Mylonakis E., Ryan E.T., Calderwood S.B. Clostridium difficile-associated diarrhea: A review. Arch. Intern. Med. 2001, 161:525-533.
48. Na X., Kelly C. Probiotics in Clostridium difficile infection. J. Clin. Gastroenterol. 2011, 45:S154-S158.
49. Ogawa M., Shimizu K., Nomoto K., Tanaka R., Hamabata T., Yamasaki S., Takeda T., Takeda Y. Inhibition of in vitro growth of Shiga toxin-producing Escherichia coli O157:H7 by probiotic Lactobacillus strains due to production of lactic acid. Int. J. Food Microbiol. 2001, 68:135-140.
50. Ohtani K., Hayashi H., Shimizu T. The luxS gene is involved in cell-cell signalling for toxin production in Clostridium perfringens. Mol. Microbiol. 2002, 44:171-179.
51. Ouwehand A.C. Antiallergic effects of probiotics. J. Nutr. 2007, 137:794S-797S.
52. Reeves A.E., Theriot C.M., Bergin I.L., Huffnagle G.B., Schloss P.D., Young V.B. The interplay between microbiome dynamics and pathogen dynamics in a murine model of Clostridium difficile infection. Gut Microbes 2011, 2:145-158.
53. Rodriguez C., Avesani V., Van Broeck J., Taminiau B., Delmee M., Daube G. Presence of Clostridium difficile in pigs and cattle intestinal contents and carcass contamination at the slaughterhouse in Belgium. Int. J. Food Microbiol. 2013, 166:256-262.
54. Rodriguez-Palacios A., Staempfli H.R., Duffield T., Weese J.S. Clostridium difficile in retail ground meat, Canada. Emerg. Infect. Dis. 2007, 13:485-487.
55. Rutherford S.T., Bassler B.L. Bacterial quorum sensing: Its role in virulence and possibilities for its control. Cold Spring Harb. Perspect. Med. 2012, 2:a012427.
56. SAS User's Guide: Statistics. SAS Inst 2006, SAS Institute Inc, Inc., Cary, NC.
57. Savard P., Lamarche B., Paradis M.E., Thiboutot H., Laurin É., Roy D. Impact of Bifidobacterium animalis ssp. lactis BB-12 and, Lactobacillus acidophilus LA-5-containing yoghurt, on fecal bacterial counts of healthy adults. Int. J. Food Microbiol. 2011, 149:50-57.
58. Silva M., Jacobus N.V., Deneke C., Gorbach S.L. Antimicrobial substance from a human Lactobacillus strain. Antimicrob. Agents Chemother. 1987, 31:1231-1233.
59. Songer J.G., Trinh H.T., Killgore G.E., Thompson A.D., McDonald L.C., Limbago B.M. Clostridium difficile in retail meat products, USA, 2007. Emerg. Infect. Dis. 2009, 15:819-821.
60. Sperandio V., Mellies J.L., Nguyen W., Shin S., Kaper J.B. Quorum sensing controls expression of the type III secretion gene transcription and protein secretion in enterohemorrhagic and enteropathogenic Escherichia coli. Proc. Natl. Acad. Sci. USA 1999, 96:15196-15201.
61. Surette M.G., Bassler B.L. Quorum sensing in Escherichia coli and Salmonella typhimurium. Proc. Natl. Acad. Sci. USA 1998, 95:7046-7050.
62. Szajewska H., Kotowska M., Mrukowicz J.Z., Armánska M., Mikolajczyk W. Efficacy of Lactobacillus GG in prevention of nosocomial diarrhea in infants. J. Pediatr. 2001, 138:361-365.
63. Tedelind S., Westberg F., Kjerrulf M., Vidal A. Anti-inflammatory properties of the short-chain fatty acids acetate and propionate: A study with relevance to inflammatory bowel disease. World J. Gastroenterol. 2007, 13:2826-2832.
64. Teraguchi S., Uehara M., Ogasa K., Mitsuoka T. Enumeration of bifidobacteria in dairy products. Nippon Saikingaku Zasshi 1978, 33:753-761.
65. Vandenbergh P.A. Lactic acid bacteria, their metabolic products and interference with microbial growth. FEMS Microbiol. Rev. 1993, 12:221-237.
66. Von Abercron S.M., Karlsson F., Wigh G.T., Wierup M., Krovacek K. Low occurrence of Clostridium difficile in retail ground meat in Sweden. J. Food Prot. 2009, 72:1732-1734.
67. Weese J.S., Avery B.P., Rousseau J., Reid-Smith R.J. Detection and enumeration of Clostridium difficile spores in retail beef and pork. Appl. Environ. Microbiol. 2009, 75:5009-5011.
68. Zar F.A., Bakkanagari S.R., Moorthi K., Davis M.B. A comparison of vancomycin and metronidazole for the treatment of Clostridium difficile-associated diarrhea, stratified by disease severity. Clin. Infect. Dis. 2007, 45:302-307.
69. Zeinhom M., Tellez A.M., Delcenserine V., El-kholy A.M., El-Shinawy S.H., Griffiths M.W. Yogurt containing bioactive molecules produced by Lactobacillus acidophilus La-5 exerts a protective effect against enterohemorrhagic Escherichia coli in mice. J. Food Prot. 2012, 75:1796-1805.