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Journal of Immunology Research
Volume 2015, Article ID 106743, 10 pages
http://dx.doi.org/10.1155/2015/106743
Research Article

Lactic Acid Bacteria Strains Exert Immunostimulatory Effect on H. pylori-Induced Dendritic Cells

1Collegium Medicum, Nicolaus Copernicus University, M. Sklodowskiej-Curie 9 Street, 85-094 Bydgoszcz, Poland
2Department of Regenerative Medicine and Immune Regulation, Medical University of Białystok, Waszyngtona 13 Street, 15-269 Białystok, Poland
3Faculty of Mechanical Engineering, University of Technology and Sciences in Bydgoszcz, Kaliskiego 7 Street, 85-789 Bydgoszcz, Poland
4The Institute of Technology Fermentation and Microbiology, Faculty of Biotechnology and Food Sciences, Technical University of Lodz, Wólczańska 171/173 Street, 90-924 Łódź, Poland
5Department of Clinical Microbiology and Immunology, Children’s Memorial Hospital, Aleja Dzieci Polskich 20, 04-730 Warsaw, Poland

Received 13 July 2014; Revised 11 September 2014; Accepted 15 September 2014

Academic Editor: Miguel Gueimonde

Copyright © 2015 Małgorzata Wiese et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. T. G. Blanchard, J. C. Eisenberg, and Y. Matsumoto, “Clearance of Helicobacter pylori infection through immunization: the site of T cell activation contributes to vaccine efficacy,” Vaccine, vol. 22, no. 7, pp. 888–897, 2004. View at Publisher · View at Google Scholar · View at Scopus
  2. K. Dzierzanowska-Fangrat, E. Rozynek, D. Celinska-Cedro et al., “Antimicrobial resistance of Helicobacter pylori in Poland: a multicentre study,” International Journal of Antimicrobial Agents, vol. 26, no. 3, pp. 230–234, 2005. View at Publisher · View at Google Scholar · View at Scopus
  3. B.-S. Sheu, H.-C. Cheng, A.-W. Kao et al., “Pretreatment with Lactobacillus- and Bifidobacterium-containing yogurt can improve the efficacy of quadruple therapy in eradicating residual Helicobacter pylori infection after failed triple therapy,” The American Journal of Clinical Nutrition, vol. 83, no. 4, pp. 864–869, 2006. View at Google Scholar · View at Scopus
  4. C. P. Felley, I. Corthésy-Theulaz, J.-L. Blanco Rivero et al., “Favourable effect of an acidified milk (LC-1) on Helicobacter pylori gastritis in man,” European Journal of Gastroenterology and Hepatology, vol. 13, no. 1, pp. 25–29, 2001. View at Publisher · View at Google Scholar · View at Scopus
  5. M. Gotteland, O. Brunser, and S. Cruchet, “Systematic review: are probiotics useful in controlling gastric colonization by Helicobacter pylori?” Alimentary Pharmacology and Therapeutics, vol. 23, no. 8, pp. 1077–1086, 2006. View at Publisher · View at Google Scholar · View at Scopus
  6. K. Stingl, E.-M. Uhlemann, G. Deckers-Hebestreit, R. Schmid, E. P. Bakker, and K. Altendorf, “Prolonged survival and cytoplasmic pH homeostasis of Helicobacter pylori at pH 1,” Infection and Immunity, vol. 69, no. 2, pp. 1178–1181, 2001. View at Publisher · View at Google Scholar · View at Scopus
  7. D. Lesbros-Pantoflickova, I. Corthésy-Theulaz, and A. L. Blum, “Helicobacter pylori and probiotics,” Journal of Nutrition, vol. 137, supplement 2, no. 3, pp. 812S–818S, 2007. View at Google Scholar · View at Scopus
  8. E. Vitiñi, S. Alvarez, M. Medina, M. Medici, M. V. de Budeguer, and G. Perdigón, “Gut mucosal immunostimulation by lactic acid bacteria,” Biocell, vol. 24, no. 3, pp. 223–232, 2000. View at Google Scholar · View at Scopus
  9. D. Sgouras, P. Maragkoudakis, K. Petraki et al., “In vitro and in vivo inhibition of Helicobacter pylori by Lactobacillus casei strain Shirota,” Applied and Environmental Microbiology, vol. 70, no. 1, pp. 518–526, 2004. View at Publisher · View at Google Scholar · View at Scopus
  10. T. von der Weid, C. Bulliard, and E. J. Schiffrin, “Induction by a lactic acid bacterium of a population of CD4+ T cells with low proliferative capacity that produce transforming growth factor β and interleukin-10,” Clinical and Diagnostic Laboratory Immunology, vol. 8, no. 4, pp. 695–701, 2001. View at Publisher · View at Google Scholar · View at Scopus
  11. A. Helmin-Basa, J. Michalkiewicz, L. Gackowska et al., “Pediatric Helicobacter pylori infection and circulating T-lymphocyte activation and differentiation,” Helicobacter, vol. 16, no. 1, pp. 27–35, 2011. View at Publisher · View at Google Scholar · View at Scopus
  12. A. Helmin-Basa, M. Czerwionka-Szaflarska, G. Bala et al., “Expression of adhesion and activation molecules on circulating monocytes in children with Helicobacter pylori infection,” Helicobacter, vol. 17, no. 3, pp. 181–186, 2012. View at Publisher · View at Google Scholar · View at Scopus
  13. S. Kabir, “The role of interleukin-17 in the Helicobacter pylori induced infection and immunity,” Helicobacter, vol. 16, no. 1, pp. 1–8, 2011. View at Publisher · View at Google Scholar · View at Scopus
  14. D. Bimczok, R. H. Clements, K. B. Waites et al., “Human primary gastric dendritic cells induce a Th1 response to H. pylori,” Mucosal Immunology, vol. 3, no. 3, pp. 260–269, 2010. View at Publisher · View at Google Scholar · View at Scopus
  15. P. Mitchell, C. Germain, P. L. Fiori et al., “Chronic exposure to Helicobacter pylori impairs dendritic cell function and inhibits Th1 development,” Infection and Immunity, vol. 75, no. 2, pp. 810–819, 2007. View at Publisher · View at Google Scholar · View at Scopus
  16. R. Karttunen, T. Karttunen, H.-P. T. Ekre, and T. T. MacDonald, “Interferon gamma and interleukin 4 secreting cells in the gastric antrum in Helicobacter pylori positive and negative gastritis,” Gut, vol. 36, no. 3, pp. 341–345, 1995. View at Publisher · View at Google Scholar · View at Scopus
  17. M. Mohammadi, S. Czinn, R. Redline, and J. Nedrud, “Helicobacter-specific cell-mediated immune responses display a predominant Th1 phenotype and promote a delayed-type hypersensitivity response in the stomachs of mice,” Journal of Immunology, vol. 156, no. 12, pp. 4729–4738, 1996. View at Google Scholar · View at Scopus
  18. A. Lundgren, E. Suri-Payer, K. Enarsson, A.-M. Svennerholm, and B. S. Lundin, “Helicobacter pylori-specific CD4+ CD25high regulatory T cells suppress memory T-cell responses to H. pylori in infected individuals,” Infection and Immunity, vol. 71, no. 4, pp. 1755–1762, 2003. View at Publisher · View at Google Scholar · View at Scopus
  19. O. Pabst and A. M. Mowat, “Oral tolerance to food protein,” Mucosal Immunology, vol. 5, no. 3, pp. 232–239, 2012. View at Publisher · View at Google Scholar · View at Scopus
  20. T. W. Spahn and T. Kucharzik, “Modulating the intestinal immune system: the role of lymphotoxin and GALT organs,” Gut, vol. 53, no. 3, pp. 456–465, 2004. View at Publisher · View at Google Scholar · View at Scopus
  21. C. W. Cutler and R. Jotwani, “Dendritic cells at the oral mucosal interface,” Journal of Dental Research, vol. 85, no. 8, pp. 678–689, 2006. View at Publisher · View at Google Scholar · View at Scopus
  22. J. Y. Kao, M. Zhang, M. J. Miller et al., “Helicobacter pylori immune escape is mediated by dendritic cell-induced Treg skewing and Th17 suppression in mice,” Gastroenterology, vol. 138, no. 3, pp. 1046–1054, 2010. View at Publisher · View at Google Scholar · View at Scopus
  23. M. L. Drakes, S. J. Czinn, and T. G. Blanchard, “Regulation of murine dendritic cell immune responses by Helicobacter felis antigen,” Infection and Immunity, vol. 74, no. 8, pp. 4624–4633, 2006. View at Publisher · View at Google Scholar · View at Scopus
  24. J. Y. Kao, S. Rathinavelu, K. A. Eaton et al., “Helicobacter pylori-secreted factors inhibit dendritic cell IL-12 secretion: a mechanism of ineffective host defense,” The American Journal of Physiology—Gastrointestinal and Liver Physiology, vol. 291, no. 1, pp. G73–G81, 2006. View at Publisher · View at Google Scholar · View at Scopus
  25. M. Zhang, B. E. Berndt, K. A. Eaton, S. Rathinavelu, A. Pierzchala, and J. Y. Kao, “Helicobacter pylori-pulsed dendritic cells induce H. pylori-specific immunity in mice,” Helicobacter, vol. 13, no. 3, pp. 200–208, 2008. View at Publisher · View at Google Scholar · View at Scopus
  26. M. Zhang, M. Liu, J. Luther, and J. Y. Kao, “Helicobacter pylori directs tolerogenic programming of dendritic cells,” Gut Microbes, vol. 1, no. 5, pp. 325–329, 2010. View at Publisher · View at Google Scholar · View at Scopus
  27. T. Aleksandrzak-Piekarczyk, A. Koryszewska-Baginska, and J. Bardowski, “Genome sequence of the probiotic strain Lactobacillus rhamnosus (formerly Lactobacillus casei) LOCK900,” Genome Announcements, vol. 1, no. 4, 2013. View at Publisher · View at Google Scholar
  28. M. Strus, “A new method for evaluation of the antagonistic action of bacterial lactic acid (LAB) on selected pathogenic indicator bacteria,” Medycyna Doświadczalna i Mikrobiologia, vol. 50, no. 1-2, pp. 123–130, 1998. View at Google Scholar
  29. H. Braat, E. C. de Jong, J. M. H. van den Brande et al., “Dichotomy between Lactobacillus rhamnosus and Klebsiella pneumoniae on dendritic cell phenotype and function,” Journal of Molecular Medicine, vol. 82, no. 3, pp. 197–205, 2004. View at Publisher · View at Google Scholar · View at Scopus
  30. N. Baba, S. Samson, R. L. Bourdet-Sicard, M. Rubio, and M. Sarfati, “Commensal bacteria trigger a full dendritic cell maturation program that promotes the expansion of non-Tr1 suppressor T cells,” Journal of Leukocyte Biology, vol. 84, no. 2, pp. 468–476, 2008. View at Publisher · View at Google Scholar · View at Scopus
  31. S. Latvala, T. E. Pietilä, V. Veckman et al., “Potentially probiotic bacteria induce efficient maturation but differential cytokine production in human monocyte-derived dendritic cells,” World Journal of Gastroenterology, vol. 14, no. 36, pp. 5570–5583, 2008. View at Publisher · View at Google Scholar · View at Scopus
  32. M. Mohamadzadeh, S. Olson, W. V. Kalina et al., “Lactobacilli active human dendritic cells that skew T cells toward T helper 1 polarization,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 8, pp. 2880–2885, 2005. View at Publisher · View at Google Scholar · View at Scopus
  33. M. Wiese, A. Eljaszewicz, M. Andryszczyk et al., “Immunomodulatory effects of Lactobacillus plantarum and helicobacter pylori CagA+ on the expression of selected superficial molecules on monocyte and lymphocyte and the synthesis of cytokines in whole blood culture,” Journal of Physiology and Pharmacology, vol. 63, no. 3, pp. 217–224, 2012. View at Google Scholar · View at Scopus
  34. M. B. Lutz and G. Schuler, “Immature, semi-mature and fully mature dendritic cells: which signals induce tolerance or immunity?” Trends in Immunology, vol. 23, no. 9, pp. 445–449, 2002. View at Publisher · View at Google Scholar · View at Scopus
  35. M. B. Lutz, “Therapeutic potential of semi-mature dendritic cells for tolerance induction,” Frontiers in Immunology, vol. 3, no. 123, Article ID Article 123, 2012. View at Publisher · View at Google Scholar · View at Scopus
  36. A. M. Dudek, S. Martin, A. D. Garg, and P. Agostinis, “Immature, semi-mature, and fully mature dendritic cells: toward a DC-cancer cells interface that augments anticancer immunity,” Frontiers in Immunology, vol. 4, article 438, 2013. View at Publisher · View at Google Scholar · View at Scopus
  37. F. Sallusto and A. Lanzavecchia, “The instructive role of dendritic cells on T-cell responses,” Arthritis Research, vol. 4, supplement 3, pp. S127–S132, 2002. View at Publisher · View at Google Scholar
  38. R. Rutkowski and T. Moniuszko, “Rola czasteczek kostymulujących B7.1 (CD80) i B7.2 (CD86) w patomechaniźmie odczynu zapalnego,” Alergia Astma Immunologia, vol. 6, no. 2, pp. 87–94, 2001. View at Google Scholar · View at Scopus
  39. N. S. Wilson, D. El-Sukkari, and J. A. Villadangos, “Dendritic cells constitutively present self antigens in their immature state in vivo and regulate antigen presentation by controlling the rates of MHC class II synthesis and endocytosis,” Blood, vol. 103, no. 6, pp. 2187–2195, 2004. View at Publisher · View at Google Scholar · View at Scopus
  40. K. Kranzer, A. Eckhardt, M. Aigner et al., “Induction of maturation and cytokine release of human dendritic cells by Helicobacter pylori,” Infection and Immunity, vol. 72, no. 8, pp. 4416–4423, 2004. View at Publisher · View at Google Scholar · View at Scopus
  41. M. Hubo, B. Trinschek, F. Kryczanowsky, A. Tuettenberg, K. Steinbrink, and H. Jonuleit, “Costimulatory molecules on immunogenic versus tolerogenic human dendritic cells,” Frontiers in Immunology, vol. 4, article 82, 2013. View at Publisher · View at Google Scholar · View at Scopus
  42. B. M. Fu, X. S. He, S. Yu et al., “A tolerogenic semimature dendritic cells induce effector T-cell hyporesponsiveness by activation of antigen-specific CD4+CD25+ T regulatory cells that promotes skin allograft survival in mice,” Cellular Immunology, vol. 261, no. 1, pp. 69–76, 2010. View at Publisher · View at Google Scholar · View at Scopus
  43. C. D. Gimmi, G. J. Freeman, J. G. Gribben, G. Gray, and L. M. Nadler, “Human T-cell clonal anergy is induced by antigen presentation in the absence of B7 costimulation,” Proceedings of the National Academy of Sciences of the United States of America, vol. 90, no. 14, pp. 6586–6590, 1993. View at Publisher · View at Google Scholar · View at Scopus
  44. A. Landi, L. A. Babiuk, and S. van Drunen Littel-van den Hurk, “Dendritic cells matured by a prostaglandin E2-containing cocktail can produce high levels of IL-12p70 and are more mature and Th1-biased than dendritic cells treated with TNF-α or LPS,” Immunobiology, vol. 216, no. 6, pp. 649–662, 2011. View at Publisher · View at Google Scholar · View at Scopus
  45. C. Aerts-Toegaert, C. Heirman, S. Tuyaerts et al., “CD83 expression on dendritic cells and T cells: correlation with effective immune responses,” European Journal of Immunology, vol. 37, no. 3, pp. 686–695, 2007. View at Publisher · View at Google Scholar · View at Scopus
  46. G. Weiss, S. Forster, A. Irving et al., “Helicobacter pylori VacA suppresses Lactobacillus acidophilus-induced interferon beta signaling in macrophages via alterations in the endocytic pathway,” mBio, vol. 4, no. 3, Article ID e00609-12, 2013. View at Publisher · View at Google Scholar · View at Scopus
  47. S. A. Khader, J. E. Pearl, K. Sakamoto et al., “IL-23 compensates for the absence of IL-12p70 and is essential for the IL-17 response during tuberculosis but is dispensable for protection and antigen-specific IFN-γ responses if IL-12p70 is available,” Journal of Immunology, vol. 175, no. 2, pp. 788–795, 2005. View at Publisher · View at Google Scholar · View at Scopus
  48. M. M. Curtis and S. S. Way, “Interleukin-17 in host defence against bacterial, mycobacterial and fungal pathogens,” Immunology, vol. 126, no. 2, pp. 177–185, 2009. View at Publisher · View at Google Scholar · View at Scopus
  49. H. H. Uhlig, B. S. McKenzie, S. Hue et al., “Differential activity of IL-12 and IL-23 in mucosal and systemic innate immune pathology,” Immunity, vol. 25, no. 2, pp. 309–318, 2006. View at Publisher · View at Google Scholar · View at Scopus
  50. M. Menges, S. Rößner, C. Voigtländer et al., “Repetitive injections of dendritic cells matured with tumor necrosis factor α induce antigen-specific protection of mice from autoimmunity,” The Journal of Experimental Medicine, vol. 195, no. 1, pp. 15–21, 2002. View at Publisher · View at Google Scholar · View at Scopus
  51. C. Voigtländer, S. Rössner, E. Cierpka et al., “Dendritic cells matured with TNF can be further activated in vitro and after subcutaneous injection in vivo which converts their tolerogenicity into immunogenicity,” Journal of Immunotherapy, vol. 29, no. 4, pp. 407–415, 2006. View at Publisher · View at Google Scholar · View at Scopus
  52. M. L. Albert, M. Jegathesan, and R. B. Darnell, “Dendritic cell maturation is required for the cross-tolerization of CD8+ T cells,” Nature Immunology, vol. 2, no. 11, pp. 1010–1017, 2001. View at Publisher · View at Google Scholar · View at Scopus
  53. A. Langenkamp, M. Messi, A. Lanzavecchia, and F. Sallusto, “Kinetics of dendritic cell activation: Impact on priming of TH1,TH2 and nonpolarized T cells,” Nature Immunology, vol. 1, no. 4, pp. 311–316, 2000. View at Publisher · View at Google Scholar · View at Scopus
  54. D. J. MacEwan, “TNF receptor subtype signalling: differences and cellular consequences,” Cellular Signalling, vol. 14, no. 6, pp. 477–492, 2002. View at Publisher · View at Google Scholar · View at Scopus
  55. A. Lubecka-Macura and M. Kohut, “TNF superfamily—mechanisms of action, biologic funtions and therapeutic possibilities,” Przeglad Gastroenterologiczny, vol. 5, no. 6, pp. 303–309, 2010. View at Publisher · View at Google Scholar · View at Scopus
  56. J. U. Igietseme, G. A. Ananaba, J. Bolier et al., “Suppression of endogenous IL-10 gene expression in dendritic cells enhances antigen presentation for specific Th1 induction: Potential for cellular vaccine development,” Journal of Immunology, vol. 164, no. 8, pp. 4212–4219, 2000. View at Publisher · View at Google Scholar · View at Scopus
  57. K. Sckäkel, “Dendritic cells—why can they help and hurt us,” Experimental Dermatology, vol. 18, no. 3, pp. 264–273, 2009. View at Publisher · View at Google Scholar · View at Scopus
  58. R. Rad, L. Brenner, S. Bauer et al., “CD25+/Foxp3+ T cells regulate gastric inflammation and Helicobacter pylori colonization in vivo,” Gastroenterology, vol. 131, no. 2, pp. 525–537, 2006. View at Publisher · View at Google Scholar · View at Scopus