A Lactobacillus plantarum strain isolated from kefir protects against intestinal infection with Yersinia enterocolitica O9 and modulates immunity in mice

Research in Microbiology

Volumn 166, Issue 8, 2015, Pages 626-632

  De Montijo Prieto, Soumi ^a   Moreno, Encarnación ^a   Bergillos Meca, Triana ^a   Lasserrot, Agustín ^b   Ruiz López, María Dolores ^a   Ruiz Bravo, Alfonso ^a   Jiménez Valera, María ^a  

^a UNIVERSITY OF GRANADA   (Spain)

^b Edificio BIC   (Spain)

Author keywords

Cytokines; Immunomodulation; Infection; Lactobacillus plantarum; Probiotic; Yersinia enterocolitica

Indexed keywords

GAMMA INTERFERON; IMMUNOGLOBULIN A; KEFIR; TUMOR NECROSIS FACTOR ALPHA; CYTOKINE; PROBIOTIC AGENT; SECRETORY IMMUNOGLOBULIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL STRAIN; FEMALE; IMMUNOMODULATION; INTESTINE INFECTION; INTESTINE MUCOSA; LACTOBACILLUS PLANTARUM; MOUSE; NONHUMAN; PEYER PATCH; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN SECRETION; YERSINIA ENTEROCOLITICA; ANIMAL; BAGG ALBINO MOUSE; BLOOD; DAIRY PRODUCT; DISEASE MODEL; FECES; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; INTESTINE; ISOLATION AND PURIFICATION; MICROBIOLOGY; PHYSIOLOGY; YERSINIA INFECTIONS;

ANIMALS; CULTURED MILK PRODUCTS; CYTOKINES; DISEASE MODELS, ANIMAL; FECES; FEMALE; IMMUNOGLOBULIN A, SECRETORY; IMMUNOMODULATION; INTERFERON-GAMMA; INTESTINES; LACTOBACILLUS PLANTARUM; MICE, INBRED BALB C; PEYER'S PATCHES; PROBIOTICS; TUMOR NECROSIS FACTOR-ALPHA; YERSINIA ENTEROCOLITICA; YERSINIA INFECTIONS;

EID: 84941880421     PISSN: 09232508     EISSN: 17697123     Source Type: Journal    
DOI: 10.1016/j.resmic.2015.07.010     Document Type: Article

References (48)

1. Hill C., Guarner F., Reid G., Gibson G.R., Merenstein D.J., Pot B., et al. Expert consensus document. The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat Rev Gastroenterol Hepatol 2014, 11:506-514.
2. Van Niel C.W., Feudtner C., Garrison M.M., Christakis D.A. Lactobacillus therapy for acute infectious diarrhea in children: a meta-analysis. Pediatrics 2002, 109:678-684.
3. Servin A.L. Antagonistic activities of lactobacilli and bifidobacteria against microbial pathogens. FEMS Microbiol Rev 2004, 28:405-440.
4. Sazawal S., Hiremath G., Dhingra U., Malik P., Deb S., Black R.E. Efficacy of probiotics in prevention of acute diarrhoea: a meta-analysis of masked, randomised, placebo-controlled trials. Lancet Infect Dis 2006, 6:374-382.
5. Guandalini S. Probiotics for prevention and treatment of diarrhea. J Clin Gastroenterol 2011, 45:S149-S153.
6. Selle K., Klaenhammer T.R. Genomic and phenotypic evidence for probiotic influences of Lactobacillus gasseri on human health. FEMS Microbiol Rev 2013, 37:915-935.
7. Zhang Y., Chen J., Wu J., Chalson H., Merigan L., Mitchell A. Probiotic use in preventing postoperative infection in liver transplant patients. Hepatobiliary Surg Nutr 2013, 2:142-147.
8. Gibson G.R., McCartney A.L., Rastall R.A. Prebiotics and resistance to gastrointestinal infections. Br J Nutr 2005, 93:S31-S34.
9. Ohland C.L., Macnaughton W.K. Probiotic bacteria and intestinal epithelial barrier function. Am J Physiol Gastrointest Liver Physiol 2010, 298:G807-G819.
10. Vinderola G., Perdigon G., Duarte J., Thangavel D., Farnworth E., Matar C. Effects of kefir fractions on innate immunity. Immunobiology 2006, 211:149-156.
11. Bakken J.S. Staggered and tapered antibiotic withdrawal with administration of kefir for recurrent Clostridium difficile infection. Clin Infect Dis 2014, 59:858-861.
12. Bolla P.A., Carasi P., Bolla Mde L., De Antoni G.L., Serradell M.A. Protective effect of a mixture of kefir-isolated lactic acid bacteria and yeasts in a hamster model of Clostridium difficile infection. Anaerobe 2013, 21:28-33.
13. Chen Y.P., Lee T.Y., Hong W.S., Hsieh H.H., Chen M.J. Effects of Lactobacillus kefiranofaciens M1 isolated from kefir grains on enterohemorrhagic Escherichia coli infection using mouse and intestinal cell models. J Dairy Sci 2013, 96:7467-7477.
14. Zheng Y., Lu Y., Wang J., Yang L., Pan C., Huang Y. Probiotic properties of Lactobacillus strains isolated from Tibetan kefir grains. PLoS One 2013, 8:e69868. 10.1371/journal.pone.0069868.
15. Bujalance C., Moreno E., Jiménez-Valera M., Ruiz-Bravo A. A probiotic strain of Lactobacillus plantarum stimulates lymphocyte responses in immunologically intact and immunocompromised mice. Int J Food Microbiol 2007, 113:28-34.
16. Fuentes S., Egert M.G.G., Jimenez-Valera M., Monteoliva-Sanchez M., Ruiz-Bravo A., Smidt H. A strain of Lactobacillus plantarum affects segmented filamentous bacteria in the intestine of immunosupressed mice. FEMS Microbiol Ecol 2008, 63:65-72.
17. Fuentes S., Egert M.G.G., Jimenez-Valera M., Ramos-Cormenzana A., Ruiz-Bravo A., Smidt H., et al. Administration of Lactobacillus casei and Lactobacillus plantarum affects the diversity of murine intestinal lactobacilli, but not the overall bacterial community structure. Res Microbiol 2008, 159:237-243.
18. Puertollano E., Puertollano M., Cruz-Chamorro L., Álvarez de Cienfuegos G., Ruiz-Bravo A., de Pablo M. Orally administered Lactobacillus plantarum reduces pro-inflammatory interleukin secretion in sera from Listeria monocytogenes infected mice. Br J Nutr 2008, 99:819-825.
19. Puertollano E., Puertollano M., Cruz-Chamorro L., Alvarez de Cienfuegos G., Ruiz-Bravo A., de Pablo M. Effects of concentrated supernatants recovered from Lactobacillus plantarum on Escherichia coli growth and on the viability of a human promyelocytic cell line. J Appl Microbiol 2009, 106:1194-1203.
20. Bergillos-Meca T., Costabile A., Walton G., Moreno-Montoro M., Ruiz-Bravo A., Dolores Ruiz-López M. In vitro evaluation of the fermentation properties and potential probiotic activity of Lactobacillus plantarum C4 in batch culture systems. LWT Food Sci Technol 2015, 60:420-426.
21. Galindo C.L., Rosenzweig J.A., Kirtley M.L., Chopra A.K. Pathogenesis of Y. enterocolitica and Y. pseudotuberculosis in human yersiniosis. J Pathog 2011, 2011:182051. 10.4061/2011/182051.
22. Fàbrega A., Vila J. Yersinia enterocolitica: pathogenesis, virulence and antimicrobial resistance. Enferm Infecc Microbiol Clin 2012, 30:24-32.
23. Cornelis G.R., Boland A., Boyd A.P., Geuijen C., Iriarte M., Neyt C., et al. The virulence plasmid of Yersinia, an antihost genome. Microbiol Mol Biol Rev 1998, 62:1315-1352.
24. Grosdent N., Maridonneau-Parini I., Sory M.P., Cornelis G.R. Role of Yops and adhesins in resistance of Yersinia enterocolitica to phagocytosis. Infect Immun 2002, 70:4165-4176.
25. Hoogkamp-Korstanje J.A., de Koning J., Heesemann J. Persistence of Yersinia enterocolitica in man. Infection 1988, 6:81-85.
26. Morris J.G., Prado V., Ferreccio C., Robins-Browne R.M., Bordun A.M., Cayazzo M., et al. Yersinia enterocolitica isolated from two cohorts of young children in Santiago, Chile: incidence of and lack of correlation between illness and proposed virulence factors. J Clin Microbiol 1991, 29:2784-2788.
27. Ruiz-Bravo A., Moreno E., Sampedro A., Jimenez-Valera M. Experimental infection of mice with Yersinia enterocolitica serotype O9 by oral and parenteral routes: spreading and enterotropism of virulent yersiniae. Curr Microbiol 1999, 38:257-263.
28. Schippers A., Mateika S., Prochnow B., Gruber A.D., Müller W., Frischmann U. Susceptibility of four inbred mouse strains to a low-pathogenic isolate of Yersinia enterocolitica. Mamm Genome 2008, 19:279-291.
29. Bergillos-Meca T., Cabrera-Vique C., Artacho R., Moreno-Montoro M., Navarro-Alarcón M., Olalla M., et al. Influence of milk ultrafiltration on Ca, Mg, Zn and P levels in fermented goats' milk. Small Rumin Res 2015, 124:95-100.
30. Bujalance C., Jimenez-Valera M., Moreno E., Ruiz-Bravo A. A selective differential medium for Lactobacillus plantarum. J Microbiol Meth 2006, 66:572-575.
31. Mazigh D., Alonso J.M., Mollaret H.H. Simple method for demonstration of differential colony morphology of plasmid-associated virulent clones of Yersinia enterocolitica. J Clin Microbiol 1983, 17:555-557.
32. Bujalance C., Jiménez-Valera M., Moreno E., Ruiz-López M.D., Lasserrot A., Ruiz-Bravo A. Lack of correlation between in vitro antibiosis and in vivo protection against enteropathogenic bacteria by probiotic lactobacilli. Res Microbiol 2014, 165:14-20.
33. Oellerich M.F., Jacobi C.A., Freund S., Niedung K., Bach A., Heesemann J., et al. Yersinia enterocolitica infection of mice reveals clonal invasion and abscess formation. Infect Immun 2007, 75:3802-3811.
34. Pfeffer K. Biological functions of tumor necrosis factor cytokines and their receptors. Cytokine Growth Factor Rev 2003, 14:185-191.
35. Autenrieth I.B., Heesemann J. In vivo neutralization of tumor necrosis factor-alpha and interferon-gamma abrogates resistance to Yersinia enterocolitica infection in mice. Med Microbiol Immunol 1992, 181:333-338.
36. Autenrieth I.B., Kempf V., Sprinz T., Preger S., Schnell A. Defense mechanisms in Peyer's patches and mesenteric lymph nodes against Yersinia enterocolitica involve integrins and cytokines. Infect Immun 1996, 64:1357-1368.
37. Mege J.L., Meghari S., Honstettre A., Capo C., Raoult D. The two faces of interleukin 10 in human infectious diseases. Lancet Infect Dis 2006, 6:557-569.
38. Lee K.S., Jeong E.S., Heo S.H., Seo J.H., Jeong D.G., Choi Y.K. IL-10 suppresses bactericidal response of macrophages against Salmonella Typhimurium. J Microbiol 2011, 49:1050-1053.
39. Schaake J., Kronshage M., Uliczka F., Rohde M., Knuuti T., Strauch E., et al. Human and animal isolates of Yersinia enterocolitica show significant serotype-specific colonization and host-specific immune defense properties. Infect Immun 2013, 81:4013-4025.
40. Brandtzaeg P. Role of secretory antibodies in the defence against infections. Int J Med Microbiol 2003, 293:3-15.
41. Sugiura Y., Kamdar K., Khakpour S., Young G., Karpus W.J., DePaolo R.W. TLR1-induced chemokine production is critical for mucosal immunity against Yersinia enterocolitica. Mucosal Immunol 2013, 6:1101-1109.
42. Stark G.R., Kerr I.M., Williams B.R., Silverman R.H., Schreiber R.D. How cells respond to interferons. Annu Rev Biochem 1998, 67:227-264.
43. Taylor G.A., Feng C.G., Sher A. Control of IFN-gamma-mediated host resistance to intracellular pathogens by immunity-related GTPases (p47 GTPases). Microbes Infect 2007, 9:1644-1651.
44. Bohn E., Heesemann J., Ehlers S., Autenrieth I.B. Early gamma interferon mRNA expression is associated with resistance of mice against Yersinia enterocolitica. Infect Immun 1994, 62:3027-3032.
45. Autenrieth I.B., Beer M., Bohn E., Kaufmann S.H., Heesemann J. Immune responses to Yersinia enterocolitica in susceptible BALB/c and resistant C57BL/6 mice: an essential role for gamma interferon. Infect Immun 1994, 62:2590-2599.
46. Steinberg R.S., Silva L.C., Souza T.C., Lima M.T., de Oliveira N.L., Vieira L.Q., et al. Safety and protective effectiveness of two strains of Lactobacillus with probiotic features in an experimental model of salmonellosis. Int J Environ Res Public Health 2014, 11(9):8755-8776.
47. Frick J.S., Fink K., Kahl F., Niemiec M.J., Quitadamo M., Schenk K., et al. Identification of commensal bacterial strains that modulate Yersinia enterocolitica and dextran sodium sulfate-induced inflammatory responses: implications for the development of probiotics. Infect Immun 2007, 75:3490-3497.
48. Wittmann A., Autenrieth I.B., Frick J.S. Plasmacytoid dendritic cells are crucial in Bifidobacterium adolescentis-mediated inhibition of Yersinia enterocolitica infection. PLoS One 2013, 8:e71338. 10.1371/journal.pone.0071338.