Evaluation of protective effect of Lactobacillus acidophilus La-5 on toxicity and colonization of Clostridium difficile in human epithelial cells in vitro

Leffler, 2015, Clostridium difficile infection, N. Engl. J. Med., 372, 1539, 10.1056/NEJMra1403772 Kyne, 2002, Health care costs and mortality associated with nosocomial diarrhea due to Clostridium difficile, Clin. Infect. Dis., 34, 346, 10.1086/338260 Shorr, 2016, Mortality and costs in Clostridium difficile infection among the elderly in the United States, Infect. Control Hosp. Epidemiol., 37, 1331, 10.1017/ice.2016.188 Pépin, 2004, Clostridium difficile-associated diarrhea in a region of Quebec from 1991 to 2003: a changing pattern of disease severity, C.M.A.G., 171, 466 Denève, 2009, New trends in Clostridium difficile virulence and pathogenesis, Int. J. Antimicrob. Agents, 33, 24, 10.1016/S0924-8579(09)70012-3 Khanna, 2016, Epidemiology, outcomes, and predictors of mortality in hospitalized adults with Clostridium difficile infection, Intern. Emerg. Med., 20, 657, 10.1007/s11739-015-1366-6 Eveillard, 1993, Identification and characterization of adhesive factors of Clostridium difficile involved in adhesion to human colonic enterocyte-like Caco-2 and mucus-secreting HT29 cells in culture, Mol. Microbiol., 7, 371, 10.1111/j.1365-2958.1993.tb01129.x Naaber, 1996, Inhibition of adhesion of Clostridium difficile to Caco-2 cells, FEMS Immunol. Med. Microbiol., 14, 205, 10.1111/j.1574-695X.1996.tb00288.x Janoir, 2016, Virulence factors of Clostridium difficile and their role during infection, Anaerobe, 37, 13, 10.1016/j.anaerobe.2015.10.009 Lyras, 2009, Toxin B is essential for virulence of Clostridium difficile, Nature, 458, 1176, 10.1038/nature07822 Chen, 2002, Protein kinase C signaling regulates ZO-1 translocation and increased paracellular flux of T84 colonocytes exposed to Clostridium difficile toxin A, J. Biol. Chem., 277, 4247, 10.1074/jbc.M109254200 McCormack, 2013, Cycling around cell-cell adhesion with Rho GTPase regulators, J. Cell Sci., 126, 379, 10.1242/jcs.097923 Fiorentini, 1998, Clostridium difficile toxin B induces apoptosis in intestinal cultured cells, Infect. Immun., 66, 2660, 10.1128/IAI.66.6.2660-2665.1998 Mahida, 1996, Effect of Clostridium difficile toxin A on human intestinal epithelial cells: induction of interleukin 8 production and apoptosis after cell detachment, Gut, 38, 337, 10.1136/gut.38.3.337 Voth, 2005, Clostridium difficile toxins: mechanism of action and role in disease, Clin. Microbiol. Rev., 18, 247, 10.1128/CMR.18.2.247-263.2005 Yakob, 2015, Mechanisms of hypervirulent Clostridium difficile ribotype 027 displacement of endemic strains: an epidemiological model, Sci. Rep., 5, 1, 10.1038/srep12666 Rupnik, 2009, Clostridium difficile infection: new developments in epidemiology and pathogenesis, Nat. Rev. Microbiol., 7, 526, 10.1038/nrmicro2164 Carter, 2012, The role of toxin A and toxin B in the virulence of Clostridium difficile, Trends Microbiol., 20, 21, 10.1016/j.tim.2011.11.003 Shen, 2017, Timely use of probiotics in hospitalized adults prevents Clostridium difficile infection: a systematic review with meta-regression analysis, Gastroenterology, 152, 1889, 10.1053/j.gastro.2017.02.003 Johnson, 2012, Is primary prevention of Clostridium difficile infection possible with specific probiotics?, Int. J. Infect. Dis., 16, e786, 10.1016/j.ijid.2012.06.005 Hickson, 2011, Probiotics in the prevention of antibiotic-associated diarrhoea and Clostridium difficile infection, Therap. Adv. Gastroenterol., 4, 185, 10.1177/1756283X11399115 Kathleen, 2010, Probiotics: preventing antibiotic-associated diarrhea, J. Spec. Pediatr. Nurs. (JSPN), 15, 160, 10.1111/j.1744-6155.2010.00231.x Isakow, 2007, Probiotics for preventing and treating nosocomial infections: review of current evidence and recommendations, Chest, 132, 286, 10.1378/chest.06-2156 Sánchez, 2010, Extracellular proteins secreted by probiotic bacteria as mediators of effects that promote mucosa-bacteria interactions, Microbiol., 156, 3232, 10.1099/mic.0.044057-0 Bayoumi, 2010, Probiotics down-regulate genes in Salmonella enterica serovar typhimurium pathogenicity islands 1 and 2, J. Food Protect., 73, 452, 10.4315/0362-028X-73.3.452 Mundi, 2013, Cell-free preparations of Lactobacillus acidophilus strain La-5 and Bifidobacterium longum strain NCC2705 affect virulence gene expression in Campylobacter jejuni, J. Food Protect., 76, 1740, 10.4315/0362-028X.JFP-13-084 Yun, 2014, Lactobacillus acidophilus modulates the virulence of Clostridium difficile, J. Dairy Sci., 97, 4745, 10.3168/jds.2014-7921 Zeinhom, 2012, Yogurt containing bioactive molecules produced by Lactobacillus acidophilus La-5 exerts a protective effect against enterohemorrhagic Escherichia coli in mice, J. Food Protect., 75, 1796, 10.4315/0362-028X.JFP-11-508 Delcenserie, 2012, Glucose decreases virulence gene expression of Escherichia coli O157:H7, J. Food Protect., 75, 748, 10.4315/0362-028X.JFP-11-384 Nordeste, 2017, Molecules produced by probiotics prevent enteric colibacillosis in pigs, BMC Vet. Res., 13, 335, 10.1186/s12917-017-1246-6 Medellin-Peña, 2007, Probiotics affect virulence-related gene expression in Escherichia coli O157:H7, Appl. Environ. Microbiol., 73, 4259, 10.1128/AEM.00159-07 Houghton, 2007, The sulphorhodamine (SRB) assay and other approaches to testing plant extracts and derived compounds for activities related to reputed anticancer activity, Methods, 42, 377, 10.1016/j.ymeth.2007.01.003 Kelly, 1994, Clostridium difficile colitis, N. Engl. J. Med., 330, 257, 10.1056/NEJM199401273300406 Vichai, 2006, Sulforhodamine B colorimetric assay for cytotoxicity screening, Nat. Protoc., 1, 1112, 10.1038/nprot.2006.179 Skehan, 1990, New colorimetric cytotoxicity assay for anti- cancer-drug screening, J. Natl. Cancer Inst., 82, 1107, 10.1093/jnci/82.13.1107 Dupuy, 2008, Clostridium difficile toxin synthesis is negatively regulated by TcdC, J. Med. Microbiol., 57, 685, 10.1099/jmm.0.47775-0 Hussack, 2011, Neutralization of Clostridium difficile toxin A with single-domain antibodies targeting the cell receptor binding domain, J. Biol. Chem., 286, 8961, 10.1074/jbc.M110.198754 Yang, 2008, In situ growth rates and biofilm development of Pseudomonas aeruginosa populations in chronic lung infections, J. Bacteriol., 190, 2767, 10.1128/JB.01581-07 Denève, 2008, Antibiotics involved in Clostridium difficile-associated disease increase colonization factor gene expression, J. Med. Microbiol., 57, 732, 10.1099/jmm.0.47676-0 Pushpanathan, 2013, Antimicrobial peptides: versatile biological properties, Int. J. Pept., 2013, 1, 10.1155/2013/675391 Tellez, 2011, A peptidic fraction from milk fermented with Lactobacillus helveticus protects mice against Salmonella infection, Int. Dairy J., 21, 607, 10.1016/j.idairyj.2011.03.011 Dingle, 2011, Mutagenic analysis of the Clostridium difficile flagellar proteins, flic and flid, and their contribution to virulence in hamsters, Infect. Immun., 79, 4061, 10.1128/IAI.05305-11 Najarian, 2018 Plummer, 2004, Clostridium difficile pilot study: effects of probiotic supplementation on the incidence of C. difficile diarrhoea, Int. Microbiol., 7, 59 Banerjee, 2009, Lactobacillus delbrueckii ssp. bulgaricus B-30892 can inhibit cytotoxic effects and adhesion of pathogenic Clostridium difficile to Caco-2 cells, Gut Pathog., 1, 1, 10.1186/1757-4749-1-8 Allen, 2015, The potential of probiotics to prevent Clostridium difficile infection, Infect. Dis. Clin., 29, 135, 10.1016/j.idc.2014.11.002 Sharma, 2014 Kos, 2003, Adhesion and aggregation ability of probiotic strain Lactobacillus acidophilus M92, J. Appl. Microbiol., 94, 981, 10.1046/j.1365-2672.2003.01915.x Koo, 2012, Recombinant probiotic expressing Listeria adhesion protein attenuates Listeria monocytogenes virulence in vitro, PLoS One, 7, 10.1371/journal.pone.0029277 Chang, 1979, Ultrastructural changes of cultured human amnion cells by Clostridium difficile toxin, Infect. Immun., 23, 795, 10.1128/IAI.23.3.795-798.1979 Fiorentini, 1990, Interaction of Clostridium difficile toxin A with cultured cells: cytoskeletal changes and nuclear polarization, Infect. Immun., 58, 2329, 10.1128/IAI.58.7.2329-2336.1990 Dailey, 2006, 381 Gratz, 2006, Lactobacillus rhamnosus strain GG modulates intestinal absorption, fecal excretion, and toxicity of aflatoxin B1 in rats, Appl. Environ. Microbiol., 72, 7398, 10.1128/AEM.01348-06 Borriello, 1988, Mucosal association by Clostridium difficile in the hamster gastrointestinal tract, J. Med. Microbiol., 25, 191, 10.1099/00222615-25-3-191 Pérez, 1998, Surface properties of bifidobacterial strains of human origin, Appl. Environ. Microbiol., 64, 21, 10.1128/AEM.64.1.21-26.1998 Rojas, 1996, Colonization by lactobacilli of piglet small intestinal mucus, J. Appl. Microbiol., 81, 474, 10.1111/j.1365-2672.1996.tb01942.x Boris, 1997, Characterization of the aggregation promoting factor from Lactobacillus gasseri, a vaginal isolate, J. Appl. Microbiol., 83, 413, 10.1046/j.1365-2672.1997.00250.x Reid, 1988, Lactobacillus inhibitor production against Escherichia coli and coaggregation ability with uropathogens, Can. J. Microbiol., 34, 344, 10.1139/m88-063 Finlay, 1989, Epithelial cell surfaces induce Salmonella proteins required for bacterial adherence and invasion, Science, 243, 940, 10.1126/science.2919285 Hoepelman, 1992, Consequences of microbial attachment: directing host cell functions with adhesins, Infect. Immun., 60, 1729, 10.1128/IAI.60.5.1729-1733.1992 Johnson-henry, 2007, Surface-layer protein extracts from Lactobacillus helveticus inhibit enterohaemorrhagic Escherichia coli O157:H7 adhesion to epithelial cells, Cell Microbiol., 9, 356, 10.1111/j.1462-5822.2006.00791.x Bergonzelli, 2006, GroEL of Lactobacillus johnsonii La1 (NCC 533) is cell surface associated: potential role in interactions with the host and the gastric pathogen Helicobacter pylori, Infect. Immun., 74, 425, 10.1128/IAI.74.1.425-434.2006 Hennequin, 2001, GroEL (Hsp60) of Clostridium difficile is involved in cell adherence, Microbiol., 147, 87, 10.1099/00221287-147-1-87 Martínez-Maqueda, 2015, HT29 cell line, 113