Impairment of swimming motility by antidiarrheic Lactobacillus acidophilus strain LB retards internalization of Salmonella enterica serovar typhimurium within human enterocyte-like cells

Antimicrobial Agents and Chemotherapy

Volumn 55, Issue 10, 2011, Pages 4810-4820

  Moal, Vanessa Liévin Le ^a,b,c   Amsellem, Raymonde ^a,b   Servin, Alain L ^a,b  

^a INSERM   (France)

^b UNIVERSITÉ PARIS SACLAY   (France)

^c CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; F ACTIN;

ARTICLE; BACTERIAL FLAGELLUM; BACTERIAL VIABILITY; BACTERIUM CULTURE; CELL FREE SYSTEM; CELL MEMBRANE; CELL MOTILITY; CONTROLLED STUDY; DEPOLARIZATION; HUMAN; HUMAN CELL; INTESTINE CELL; LACTOBACILLUS ACIDOPHILUS; MOLECULAR WEIGHT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN STABILITY; SALMONELLA ENTERICA; SALMONELLA TYPHIMURIUM; SEROTYPE; SUPERNATANT; TIME LAPSE IMAGING; WESTERN BLOTTING; WILD TYPE;

ACTINS; BACTERIAL ADHESION; BACTERIAL PROTEINS; CACO-2 CELLS; CELL MEMBRANE; CELLS, CULTURED; ENTEROCYTES; FLAGELLA; HUMANS; LACTOBACILLUS ACIDOPHILUS; MICROBIAL VIABILITY; MOVEMENT; PROBIOTICS; SALMONELLA TYPHIMURIUM; TIME-LAPSE IMAGING;

EID: 80052837387     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.00418-11     Document Type: Article

References (60)

1. Alakomi, H. L., et al. 2000. Lactic acid permeabilizes gram-negative bacteria by disrupting the outer membrane. Appl. Environ. Microbiol. 66:2001-2005.
2. CDC. 2009. National antimicrobial resistance monitoring system for enteric bacteria (NARMS): 2006 human isolates report. U.S. Department of Health and Human Services, Atlanta, GA.
3. CDC. 2008. Salmonella surveillance: annual summary, 2006. U.S. Department of Health and Human Services, Atlanta, GA.
4. Chantret, I., et al. 1994. Differential expression of sucrase-isomaltase in clones isolated from early and late passages of the cell line Caco-2: evidence for glucose-dependent negative regulation. J. Cell Sci. 107:213-225. (Pubitemid 24039048)
5. Chevance, F. F., and K. T. Hughes. 2008. Coordinating assembly of a bacterial macromolecular machine. Nat. Rev. Microbiol. 6:455-465.
6. Coconnier, M. H., M. F. Bernet, G. Chauviere, and A. L. Servin. 1993. Adhering heat-killed human Lactobacillus acidophilus, strain LB, inhibits the process of pathogenicity of diarrhoeagenic bacteria in cultured human intestinal cells. J. Diarrhoeal Dis. Res. 11:235-242.
7. Coconnier, M. H., et al. 1993. Inhibition of adhesion of enteroinvasive pathogens to human intestinal Caco-2 cells by Lactobacillus acidophilus strain LB decreases bacterial invasion. FEMS Microbiol. Lett. 110:299-305.
8. Coconnier, M. H., V. Lievin, M. F. Bernet-Camard, S. Hudault, and A. L. Servin. 1997. Antibacterial effect of the adhering human Lactobacillus acidophilus strain LB. Antimicrob. Agents Chemother. 41:1046-1052.
9. Coconnier, M. H., V. Lievin, M. Lorrot, and A. L. Servin. 2000. Antagonistic activity of Lactobacillus acidophilus LB against intracellular Salmonella enterica serovar Typhimurium infecting human enterocyte-like Caco-2/TC-7 cells. Appl. Environ. Microbiol. 66:1152-1157.
10. Coconnier-Polter, M. H., V. Lievin-Le Moal, and A. L. Servin. 2005. A Lactobacillus acidophilus strain of human gastrointestinal microbiota origin elicits killing of enterovirulent Salmonella enterica serovar Typhimurium by triggering lethal bacterial membrane damage. Appl. Environ. Microbiol. 71:6115-6120.
11. Daefler, S., and M. Russel. 1998. The Salmonella typhimurium InvH protein is an outer membrane lipoprotein required for the proper localization of InvG. Mol. Microbiol. 28:1367-1380.
12. Dibb-Fuller, M. P., E. Allen-Vercoe, C. J. Thorns, and M. J. Woodward. 1999. Fimbriae- and flagella-mediated association with and invasion of cultured epithelial cells by Salmonella enteritidis. Microbiology 145:1023-1031.
13. Eichelberg, K., and J. E. Galan. 2000. The flagellar sigma factor FliA (sigma(28)) regulates the expression of Salmonella genes associated with the centisome 63 type III secretion system. Infect. Immun. 68:2735-2743.
14. FAO/WHO. 2001. Health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria. FAO/WHO, Geneva, Switzerland. http://www.who.int/foodsafety/publications/fs-management/en/ probiotics.pdf.
15. Fayol-Messaoudi, D., et al. 2007. The Lactobacillus plantarum strain ACADC287 isolated from a Greek cheese demonstrates antagonistic activity in vitro and in vivo against Salmonella enterica serovar Typhimurium. J. Appl. Microbiol. 103:657-665. (Pubitemid 47256337)
16. Finlay, B. B., S. Ruschkowski, and S. Dedhar. 1991. Cytoskeletal rearrangements accompanying Salmonella entry into epithelial cells. J. Cell Sci. 99: 283-296.
17. Forbes, S. J., M. Eschmann, and N. J. Mantis. 2008. Inhibition of Salmonella enterica serovar Typhimurium motility and entry into epithelial cells by a protective antilipopolysaccharide monoclonal immunoglobulin A antibody. Infect. Immun. 76:4137-4144.
18. Galán, J. E. 2001. Salmonella interactions with host cells: type III secretion at work. Annu. Rev. Cell Dev. Biol. 17:53-86.
19. Galán, J. E., and H. Wolf-Watz. 2006. Protein delivery into eukaryotic cells by type III secretion machines. Nature 444:567-573. (Pubitemid 44864429)
20. Grassl, G. A., and B. B. Finlay. 2008. Pathogenesis of enteric Salmonella infections. Curr. Opin. Gastroenterol. 24:22-26.
21. Harshey, R. M. 2003. Bacterial motility on a surface: many ways to a common goal. Annu. Rev. Microbiol. 57:249-273.
22. Hautefort, I., M. J. Proenca, and J. C. Hinton. 2003. Single-copy green fluorescent protein gene fusions allow accurate measurement of Salmonella gene expression in vitro and during infection of mammalian cells. Appl. Environ. Microbiol. 69:7480-7491.
23. Higashide, W., S. Dai, V. P. Hombs, and D. Zhou. 2002. Involvement of SipA in modulating actin dynamics during Salmonella invasion into cultured epithelial cells. Cell Microbiol. 4:357-365.
24. Hoiseth, S. K., and B. A. Stocker. 1981. Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines. Nature 291:238-239.
25. Hudault, S., V. Lievin, M. F. Bernet-Camard, and A. L. Servin. 1997. Antagonistic activity exerted in vitro and in vivo by Lactobacillus casei (strain GG) against Salmonella typhimurium C5 infection. Appl. Environ. Microbiol. 63:513-518.
26. Hueck, C. J., et al. 1995. Salmonella typhimurium secreted invasion determinants are homologous to Shigella Ipa proteins. Mol. Microbiol. 18:479-490.
27. Jepson, M. A., B. Kenny, and A. D. Leard. 2001. Role of sipA in the early stages of Salmonella typhimurium entry into epithelial cells. Cell Microbiol. 3:417-426.
28. Jones, B. D., C. A. Lee, and S. Falkow. 1992. Invasion by Salmonella typhimurium is affected by the direction of flagellar rotation. Infect. Immun. 60:2475-2480.
29. Khoramian-Falsafi, T., S. Harayama, K. Kutsukake, and J. C. Pechere. 1990. Effect of motility and chemotaxis on the invasion of Salmonella typhimurium into HeLa cells. Microb. Pathog. 9:47-53.
30. Lebeer, S., J. Vanderleyden, and S. C. De Keersmaecker. 2008. Genes and molecules of lactobacilli supporting probiotic action. Microbiol. Mol. Biol. Rev. 72:728-764.
31. Liévin-Le Moal, V., R. Amsellem, A. L. Servin, and M. H. Coconnier. 2002. Lactobacillus acidophilus (strain LB) from the resident adult human gastrointestinal microflora exerts activity against brush border damage promoted by a diarrhoeagenic Escherichia coli in human enterocyte-like cells. Gut 50:803-811.
32. Liévin-Le Moal, V., L. E. Sarrazin-Davila, and A. L. Servin. 2007. An experimental study and a randomized, double-blind, placebo-controlled clinical trial to evaluate the antisecretory activity of Lactobacillus acidophilus strain LB against nonrotavirus diarrhea. Pediatrics 120:e795-e803.
33. Liévin-Le Moal, V., and A. L. Servin. 2006. The front line of enteric host defense against unwelcome intrusion of harmful microorganisms: mucins, antimicrobial peptides, and microbiota. Clin. Microbiol. Rev. 19:315-337.
34. Liu, S. L., T. Ezaki, H. Miura, K. Matsui, and E. Yabuuchi. 1988. Intact motility as a Salmonella typhi invasion-related factor. Infect. Immun. 56: 1967-1973.
35. Lockman, H. A., and R. Curtiss III. 1990. Salmonella typhimurium mutants lacking flagella or motility remain virulent in BALB/c mice. Infect. Immun. 58:137-143.
36. Macnab, R. M. 2003. How bacteria assemble flagella. Annu. Rev. Microbiol. 57:77-100.
37. Michetti, P., et al. 1994. Monoclonal immunoglobulin A prevents adherence and invasion of polarized epithelial cell monolayers by Salmonella typhimurium. Gastroenterology 107:915-923. (Pubitemid 24294552)
38. Milillo, S. R., E. Martin, A. Muthaiyan, and S. C. Ricke. 2011. Immediate reduction of Salmonella enterica serotype Typhimurium viability via membrane destabilization following exposure to multiple-hurdle treatments with heated, acidified organic acid salt solutions. Appl. Environ. Microbiol. 77: 3765-3772.
39. Minamino, T., K. Imada, and K. Namba. 2008. Molecular motors of the bacterial flagella. Curr. Opin. Struct. Biol. 18:693-701.
40. Minamino, T., Y. Imae, F. Oosawa, Y. Kobayashi, and K. Oosawa. 2003. Effect of intracellular pH on rotational speed of bacterial flagellar motors. J. Bacteriol. 185:1190-1194. (Pubitemid 36176851)
41. Morin, N., et al. 2011. Mechanism of bactericidal activity of microcin L in Escherichia coli and Salmonella enterica. Antimicrob. Agents Chemother. 55:997-1007.
42. Parthasarathy, G., Y. Yao, and K. S. Kim. 2007. Flagella promote Escherichia coli K1 association with and invasion of human brain microvascular endothelial cells. Infect. Immun. 75:2937-2945.
43. Patel, J. C., and J. E. Galan. 2005. Manipulation of the host actin cytoskeleton by Salmonella - all in the name of entry. Curr. Opin. Microbiol. 8:10-15.
44. Perrett, C. A., and M. A. Jepson. 2009. Regulation of Salmonella-induced membrane ruffling by SipA differs in strains lacking other effectors. Cell Microbiol. 11:475-487.
45. Pichon, C., et al. 2009. Uropathogenic Escherichia coli AL511 requires flagellum to enter renal collecting duct cells. Cell Microbiol. 11:616-628.
46. Raffatellu, M., et al. 2005. SipA, SopA, SopB, SopD, and SopE2 contribute to Salmonella enterica serotype Typhimurium invasion of epithelial cells. Infect. Immun. 73:146-154.
47. Salazar-Lindo, E., et al. 2007. Effectiveness and safety of Lactobacillus LB in the treatment of mild acute diarrhea in children. J. Pediatr. Gastroenterol. Nutr. 44:571-576.
48. Sampaio, S. C., et al. 2009. The flagella of an atypical enteropathogenic Escherichia coli strain are required for efficient interaction with and stimulation of interleukin-8 production by enterocytes in vitro. Infect. Immun. 77:4406-4413.
49. Servin, A. L. 2004. Antagonistic activities of lactobacilli and bifidobacteria against microbial pathogens. FEMS Microbiol. Rev. 28:405-440.
50. Sojka, M., A. R. Sayers, and M. J. Woodward. 2001. Analysis of expression of flagella by Salmonella enterica serotype Typhimurium by monoclonal antibodies recognising both phase specific and common epitopes. Vet. Microbiol. 78:61-77.
51. Spengler, G., et al. 2004. Inhibitory action of a new proton pump inhibitor, trifluoromethyl ketone derivative, against the motility of clarithromycinsusceptible and-resistant Helicobacter pylori. Int. J. Antimicrob. Agents 23: 631-633. (Pubitemid 38759680)
52. Stecher, B., et al. 2004. Flagella and chemotaxis are required for efficient induction of Salmonella enterica serovar Typhimurium colitis in streptomycin- pretreated mice. Infect. Immun. 72:4138-4150.
53. Toguchi, A., M. Siano, M. Burkart, and R. M. Harshey. 2000. Genetics of swarming motility in Salmonella enterica serovar typhimurium: critical role for lipopolysaccharide. J. Bacteriol. 182:6308-6321.
54. Turner, L., W. S. Ryu, and H. C. Berg. 2000. Real-time imaging of fluorescent flagellar filaments. J. Bacteriol. 182:2793-2801. (Pubitemid 30246910)
55. Turner, L., R. Zhang, N. C. Darnton, and H. C. Berg. 2010. Visualization of flagella during bacterial swarming. J. Bacteriol. 192:3259-3267.
56. van Asten, F. J., H. G. Hendriks, J. F. Koninkx, and J. E. van Dijk. 2004. Flagella-mediated bacterial motility accelerates but is not required for Salmonella serotype Enteritidis invasion of differentiated Caco-2 cells. Int. J. Med. Microbiol. 294:395-399.
57. Welch, M., Y. Margolin, S. R. Caplan, and M. Eisenbach. 1995. Rotational asymmetry of Escherichia coli flagellar motor in the presence of arsenate. Biochim. Biophys. Acta 1268:81-87.
58. Winter, S. E., et al. 2009. Contribution of flagellin pattern recognition to intestinal inflammation during Salmonella enterica serotype Typhimurium infection. Infect. Immun. 77:1904-1916.
59. Zhang, L., P. Dhillon, H. Yan, S. Farmer, and R. E. Hancock. 2000. Interactions of bacterial cationic peptide antibiotics with outer and cytoplasmic membranes of Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 44:3317-3321.
60. Zhou, D., M. S. Mooseker, and J. E. Galan. 1999. Role of the S. typhimurium actin-binding protein SipA in bacterial internalization. Science 283:2092-2095.