Secreted compounds of the probiotic Bacillus clausii strain O/C inhibit the cytotoxic effects induced by Clostridium difficile and Bacillus cereus toxins

Antimicrobial Agents and Chemotherapy

Volumn 60, Issue 6, 2016, Pages 3445-3454

  Ripert, Gabrielle ^a   Racedo, Silvia M ^a   Elie, Anne Marie ^a   Jacquot, Claudine ^a   Bressollier, Philippe ^a   Urdaci, Maria C ^a  

^a UNIVERSITÉ DE BORDEAUX   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL TOXIN; BENZYLSULFONYL FLUORIDE; PROBIOTIC AGENT; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHOB GUANINE NUCLEOTIDE BINDING PROTEIN; CONDITIONED MEDIUM; M-PROTEASE; PROTEINASE INHIBITOR; SUBTILISIN;

ANTIBACTERIAL ACTIVITY; ARTICLE; BACILLUS; BACILLUS CEREUS; BACILLUS CLAUSII; CELL ADHESION; CELL DEATH; CELL PROTECTION; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; CYTOTOXICITY ASSAY; ENZYME ACTIVITY; ENZYME SPECIFICITY; EUKARYOTIC CELL; GENE EXPRESSION; HEMOLYSIS; MOLECULAR WEIGHT; NONHUMAN; NUCLEOTIDE SEQUENCE; PEPTOCLOSTRIDIUM DIFFICILE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; SUPERNATANT; UPREGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; CACO-2 CELL LINE; CELL SURVIVAL; CHLOROCEBUS AETHIOPS; CONDITIONED MEDIUM; DRUG EFFECTS; HUMAN; INTESTINE MUCOSA; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PATHOLOGY; PHARMACOLOGY; TUMOR CELL LINE; VERO CELL LINE;

ANIMALS; BACILLUS CEREUS; BACILLUS CLAUSII; BACTERIAL TOXINS; CACO-2 CELLS; CELL LINE, TUMOR; CELL SURVIVAL; CERCOPITHECUS AETHIOPS; CLOSTRIDIUM DIFFICILE; CULTURE MEDIA, CONDITIONED; HUMANS; INTESTINAL MUCOSA; PHENYLMETHYLSULFONYL FLUORIDE; PROBIOTICS; PROTEASE INHIBITORS; RHOB GTP-BINDING PROTEIN; SUBTILISINS; VERO CELLS;

EID: 84973547906     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.02815-15     Document Type: Article

References (55)

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. http://dx.doi.org/10.1086/338260.
2. Spigaglia P, Barbanti F, Castagnola E, Bandettini R. 2015. Clostridium difficile infection (CDI) in children due to hypervirulent strains PCR-ribotype 027: an emblematic report of two cases. Anaerobe 36:91-93. http://dx.doi.org/10.1016/j.anaerobe.2015.09.004.
3. Yakob L, Riley TV, Paterson DL, Marquess J, Magalhaes RJ, Furuya-Kanamori L, Clements AC. 2015. Mechanisms of hypervirulent Clostridium difficile ribotype 027 displacement of endemic strains: an epidemiological model. Sci Rep 5:12666. http://dx.doi.org/10.1038/srep12666.
4. Vindigni SM, Surawicz CM. 2015. C. difficile infection: changing epidemiology and management paradigms. Clin Transl Gastroenterol 6:e99. http://dx.doi.org/10.1038/ctg.2015.24.
5. Shen A. 2012. Clostridium difficile toxins: mediators of inflammation. J Innate Immun 4:149-158. http://dx.doi.org/10.1159/000332946.
6. Janvilisri T, Scaria J, Chang YF. 2010. Transcriptional profiling of Clostridium difficile and Caco-2 cells during infection. J Infect Dis 202:282-290. http://dx.doi.org/10.1086/653484.
7. Gerhard R, Tatge H, Genth H, Thum T, Borlak J, Fritz G, Just I. 2005. Clostridium difficile toxin A induces expression of the stress-induced early gene product RhoB. J Biol Chem 280:1499-1505. http://dx.doi.org/10.1074/jbc.M406014200.
8. Popoff MR, Geny B. 2009. Multifaceted role of Rho, Rac, Cdc42 and Ras in intercellular junctions, lessons from toxins. Biochim Biophys Acta 1788:797-812. http://dx.doi.org/10.1016/j.bbamem.2009.01.011.
9. Popoff MR, Geny B. 2011. Rho/Ras-GTPase-dependent and -independent activity of clostridial glucosylating toxins. J Med Microbiol 60:1057-1069. http://dx.doi.org/10.1099/jmm.0.029314-0.
10. Aschenbach JR, Seidler T, Ahrens F, Schrödl W, Buchholz I, Garz B, Krüger M, Gäbel G. 2003. Luminal Salmonella endotoxin affects epithelial and mast cell function in the proximal colon of pigs. Scand J Gastroenterol 38(7):719-726. http://dx.doi.org/10.1080/00365520310003129.
11. Madhavan TP, Sakellaris H. 2015. Colonization factors of enterotoxigenic Escherichia coli. Adv Appl Microbiol 90:155-197. http://dx.doi.org/10.1016/bs.aambs.2014.09.003.
12. Gray MD, Lacher DW, Leonard SR, Abbott J, Zhao S, Lampel KA, Prothery E, Gouali M, Weill FX, Maurelli AT. 2015. Prevalence of Shiga toxin-producing Shigella species isolated from French travellers returning from the Caribbean: an emerging pathogen with international implications. Clin Microbiol Infect 21(8):765.e9-765.e14.
13. Granum PE, Brynestad S, Kramer JM. 1993. Analysis of enterotoxin production by Bacillus cereus from dairy products, food poisoning incidents and non-gastrointestinal infections. Int J Food Microbiol 17:269-279. http://dx.doi.org/10.1016/0168-1605(93)90197-O.
14. Ehling-Schulz M, Fricker M, Scherer S. 2004. Bacillus cereus, the causative agent of an emetic type of food-borne illness. Mol Nutr Food Res 48:479-487. http://dx.doi.org/10.1002/mnfr.200400055.
15. Stenfors Arnesen LP, Fagerlund A, Granum PE. 2008. From soil to gut: Bacillus cereus and its food poisoning toxins. FEMS Microbiol Rev 32:579-606. http://dx.doi.org/10.1111/j.1574-6976.2008.00112.x.
16. Beecher DJ, Macmillan JD. 1991. Characterization of the components of hemolysin BL from Bacillus cereus. Infect Immun 59:1778-1784.
17. Beecher DJ, Schoeni JL, Wong AC. 1995. Enterotoxic activity of hemolysin BL from Bacillus cereus. Infect Immun 63:4423-4428.
18. Friedman G. 2012. The role of probiotics in the prevention and treatment of antibiotic-associated diarrhea and Clostridium difficile colitis. Gastroenterol Clin North Am 41:763-779. http://dx.doi.org/10.1016/j.gtc.2012.08.002.
19. Kolling GL, Wu M, Warren CA, Durmaz E, Klaenhammer TR, Guerrant RL. 2012. Lactic acid production by Streptococcus thermophilus alters Clostridium difficile infection and in vitro toxin A production. Gut Microbes 3:523-529. http://dx.doi.org/10.4161/gmic.21757.
20. Food and Agriculture Organization of the United Nations (FAO). 2001. Health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria. FAO, Rome, Italy.
21. Satish Kumar R, Kanmani P, Yuvaraj N, Paari KA, Pattukumar V, Arul V. 2011. Lactobacillus plantarum AS1 binds to cultured human intestinal cell line HT-29 and inhibits cell attachment by enterovirulent bacterium Vibrio parahaemolyticus. Lett Appl Microbiol 53:481-487. http://dx.doi.org/10.1111/j.1472-765X.2011.03136.x.
22. Ng SC, Hart AL, Kamm MA, Stagg AJ, Knight SC. 2009. Mechanisms of action of probiotics: recent advances. Inflamm Bowel Dis 15:300-310. http://dx.doi.org/10.1002/ibd.20602.
23. Kakisu E, Abraham AG, Tironi Farinati C, Ibarra C, De Antoni GL. 2012. Lactobacillus plantarum isolated from kefir protects Vero cells from cytotoxicity by type-II Shiga toxin from Escherichia coli O157:H7. J Dairy Res 80:64-71.
24. Carasi P, Trejo FM, Pérez PF, De Antoni GL, de los Serradell MA. 2012. Surface proteins from Lactobacillus kefir antagonize in vitro cytotoxic effect of Clostridium difficile toxins. Anaerobe 18:135-142. http://dx.doi.org/10.1016/j.anaerobe.2011.11.002.
25. Castagliuolo I, LaMont JT, Nikulasson ST, Pothoulakis C. 1996. Saccharomyces boulardii protease inhibits Clostridium difficile toxin A effects in the rat ileum. Infect Immun 64:5225-5232.
26. Castagliuolo I, Riegler MF, Valenick L, LaMont JT, Pothoulakis C. 1999. Saccharomyces boulardii protease inhibits the effects of Clostridium difficile toxins A and B in human colonic mucosa. Infect Immun 67:302-307.
27. Tasteyre A, Barc MC, Karjalainen T, Bourlioux P, Collignon A. 2002. Inhibition of in vitro cell adherence of Clostridium difficile by Saccharomyces boulardii. Microb Pathog 32:219-225. http://dx.doi.org/10.1006/mpat.2002.0495.
28. Mazza P. 1994. The use of Bacillus subtilis as an antidiarrhoeal microorganism. Boll Chim Farm 133:3-18.
29. Nista EC, Candelli M, Cremonini F, Cazzato IA, Zocco MA, Franceschi F, Cammarota G, Gasbarrini G, Gasbarrini A. 2004. Bacillus clausii therapy to reduce side-effects of anti-Helicobacter pylori treatment: randomized, double-blind, placebo controlled trial. Aliment Pharmacol Ther 20:1181-1188. http://dx.doi.org/10.1111/j.1365-2036.2004.02274.x.
30. Ciprandi G, Vizzaccaro A, Cirillo I, Tosca MA. 2005. Bacillus clausii exerts immuno-modulatory activity in allergic subjects: a pilot study. Eur Ann Allergy Clin Immunol 37:129-134.
31. Urdaci MC, Bressollier P, Pinchuk I. 2004. Bacillus clausii probiotic strains: antimicrobial and immunomodulatory activities. J Clin Gastroenterol 38:S86-S90. http://dx.doi.org/10.1097/01.mcg.0000128925.06662.69.
32. Bouhss A, Al-Dabbagh B, Vincent M, Odaert B, Aumont-Nicaise M, Bressolier P, Desmadril M, Mengin-Lecreulx D, Urdaci MC, Gallay J. 2009. Specific interactions of clausin, a new lantibiotic, with lipid precursors of the bacterial cell wall. Biophysics J 97:1390-1397. http://dx.doi.org/10.1016/j.bpj.2009.06.029.
33. Karlsson S, Burman LG, Akerlund T. 1999. Suppression of toxin production in Clostridium difficile VPI 10463 by amino acids. Microbiology (Reading, Engl) 145(Part 7):1683-1693. http://dx.doi.org/10.1099/13500872-145-7-1683.
34. Ivanova N, Sorokin A, Anderson I, Galleron N, Candelon B, Kapatral V, Bhattacharyya A, Reznik G, Mikhailova N, Lapidus A, Chu L, Mazur M, Goltsman E, Larsen N, D'Souza M, Walunas T, Grechkin Y, Pusch G, Haselkorn R, Fonstein M, Ehrlich SD, Overbeek R, Kyrpides N. 2003. Genome sequence of Bacillus cereus and comparative analysis with Bacillus anthracis. Nature 423:87-91. http://dx.doi.org/10.1038/nature01582.
35. Larsen MD, Kristiansen KR, Hansen TK. 1998. Characterization of the proteolytic activity of starter cultures of Penicillium roqueforti for production of blue veined cheeses. Int J Food Microbiol 43:215-221. http://dx.doi.org/10.1016/S0168-1605(98)00114-7.
36. Minnaard J, Humen M, Pérez PF. 2001. Effect of Bacillus cereus exocellular factors on human intestinal epithelial cells. J Food Prot 64(10):1535-1541.
37. Medrano M, Pérez PF, Abraham AG. 2008. Kefiran antagonizes cytopathic effects of Bacillus cereus extracellular factors. Int J Food Microbiol 122:1-7. http://dx.doi.org/10.1016/j.ijfoodmicro.2007.11.046.
38. Keller MA, Addya S, Vadigepalli R, Banini B, Delgrosso K, Huang H, Surrey S. 2006. Transcriptional regulatory network analysis of developing human erythroid progenitors reveals patterns of coregulation and potential transcriptional regulators. Physiol Genomics 28:114-128. http://dx.doi.org/10.1152/physiolgenomics.00055.2006.
39. Vinogradov SN, Sharma PK. 1994. Preparation and characterization of invertebrate globin complexes. Methods Enzymol 231:112-124. http://dx.doi.org/10.1016/0076-6879(94)31010-6.
40. Sella SR, Vandenberghe LP, Soccol CR. 2014. Life cycle and spore resistance of spore-forming Bacillus atrophaeus. Microbiol Res 169(12):931-939. http://dx.doi.org/10.1016/j.micres.2014.05.001.
41. Collado MC, Meriluoto J, Salminen S. 2007. Role of commercial probiotic strains against human pathogen adhesion to intestinal mucus. Lett Appl Microbiol 45:454-460. http://dx.doi.org/10.1111/j.1472-765X.2007.02212.x.
42. Rai AK, Chattopadhyay K. 2015. Vibrio cholerae cytolysin: structure-function mechanism of an atypical β-barrel pore-forming toxin. Adv Exp Med Biol 842:109-125. http://dx.doi.org/10.1007/978-3-319-11280-0-7.
43. Jeßberger N, Krey VM, Rademacher C, Böhm ME, Mohr AK, Ehling-Schulz M, Scherer S, Märtlbauer E. 2015. From genome to toxicity: a combinatory approach highlights the complexity of enterotoxin production in Bacillus cereus. Front Microbiol 6:560. http://dx.doi.org/10.3389/fmicb.2015.00560.
44. Janoir C. 2016. Virulence factors of Clostridium difficile and their role during infection. Anaerobe 37:13-24. http://dx.doi.org/10.1016/j.anaerobe.2015.10.009.
45. Sánchez B, Urdaci MC, Margolles A. 2010. Extracellular proteins secreted by probiotic bacteria as mediators of effects that promote mucosal-bacteria interactions. Microbiology 156:3232-3242. http://dx.doi.org/10.1099/mic.0.044057-0.
46. Yan F, Cao H, Cover TL, Whitehead R, Washington MK, Polk DB. 2007. Soluble proteins produced by probiotic bacteria regulate intestinal epithelial cell survival and growth. Gastroenterology 132:562-575. http://dx.doi.org/10.1053/j.gastro.2006.11.022.
47. Bressolier P, Brugo MA, Robineau P, Schmitter M, Sofeir M, Urdaci M. April 2007. Peptide compound with biological activity, its preparation and application. WIPO PCT/IB2007/0022003.
48. Pothoulakis C, Kelly CP, Joshi MA, Gao N, O'Keane CJ, Castagliuolo I, Lamont JT. 1993. Saccharomyces boulardii inhibits Clostridium difficile toxin A binding and enterotoxicity in rat ileum. Gastroenterology 104(4):1108-1115.
49. Leslie JL, Huang S, Opp JS, Nagy MS, Kobayashi M, Young VB, Spence JR. 2015. Persistence and toxin production by Clostridium difficile within human intestinal organoids result in disruption of epithelial paracellular barrier function. Infect Immun 83(1):138-145. http://dx.doi.org/10.1128/IAI.02561-14.
50. Davies AH, Roberts AK, Shone CC, Acharya KR. 2011. Super toxins from a super bug: structure and function of Clostridium difficile toxins. Biochem J 436(3):517-526. http://dx.doi.org/10.1042/BJ20110106.
51. Shuyi C, Chunli S, Haiying W, Jufang W. 2015. The Role of Rho GTPases in toxicity of Clostridium difficile toxins. Toxins (Basel) 7(12):5254-5267. http://dx.doi.org/10.3390/toxins7124874.
52. Popoff MR, Geny B. 2011. Rho/Ras-GTPase-dependent and -independent activity of clostridial glucosylating toxins. J Med Microbiol 60(Part 8):1057-1069. http://dx.doi.org/10.1099/jmm.0.029314-0.
53. Jank T, Giesemann T, Aktories K. 2007. Rho-glucosylating Clostridium difficile toxins A and B: new insights into structure and function. Glycobiology 17:15R-22R. http://dx.doi.org/10.1093/glycob/cwm004.
54. Jeßberger N, Dietrich R, Bock S, Didier A, Märtlbauer E. 2014. Bacillus cereus enterotoxins act as major virulence factors and exhibit distinct cytotoxicity to different human cell lines. Toxicon 77:49-57. http://dx.doi.org/10.1016/j.toxicon.2013.10.028.
55. Kazan D, Akin Denizci Astring-name', Kerimak Öner MN, Erarslan A. 2005. Purification and characterization of a serine alkaline protease from Bacillus clausii GMBAE 42. J Ind Microbiol Biotechnol 32:335-344. http://dx.doi.org/10.1007/s10295-005-0260-z.