Table of Contents Author Guidelines Submit a Manuscript
Journal of Immunology Research
Volume 2016 (2016), Article ID 7402760, 8 pages
http://dx.doi.org/10.1155/2016/7402760
Research Article

Lactobacillus rhamnosus GG Activation of Dendritic Cells and Neutrophils Depends on the Dose and Time of Exposure

1Department of Surgery, Yong Loo Lin School of Medicine, National University of Singapore, Singapore 119228
2Department of Anatomy, Yong Loo Lin School of Medicine, National University of Singapore, Singapore 117594
3Department of Microbiology and Immunology, Yong Loo Lin School of Medicine, National University of Singapore, Singapore 117545

Received 10 March 2016; Revised 9 May 2016; Accepted 19 May 2016

Academic Editor: Lenin Pavón

Copyright © 2016 Shirong Cai 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. Pessi, Y. Sütas, M. Hurme, and E. Isolauri, “Interleukin-10 generation in atopic children following oral lactobacillus rhamnosus GG,” Clinical and Experimental Allergy, vol. 30, no. 12, pp. 1804–1808, 2000. View at Publisher · View at Google Scholar · View at Scopus
  2. J. Sawada, H. Morita, A. Tanaka, S. Salminen, F. He, and H. Matsuda, “Ingestion of heat-treated Lactobacillus rhamnosus GG prevents development of atopic dermatitis in NC/Nga mice,” Clinical and Experimental Allergy, vol. 37, no. 2, pp. 296–303, 2007. View at Publisher · View at Google Scholar · View at Scopus
  3. G. Zuccotti, F. Meneghin, A. Aceti et al., “Probiotics for prevention of atopic diseases in infants: systematic review and meta-analysis,” Allergy, vol. 70, no. 11, pp. 1356–1371, 2015. View at Publisher · View at Google Scholar · View at Scopus
  4. A. Horvath, P. Dziechciarz, and H. Szajewska, “Meta-analysis: Lactobacillus rhamnosus GG for abdominal pain-related functional gastrointestinal disorders in childhood,” Alimentary Pharmacology & Therapeutics, vol. 33, no. 12, pp. 1302–1310, 2011. View at Publisher · View at Google Scholar · View at Scopus
  5. Y. Ohashi, S. Nakai, T. Tsukamoto et al., “Habitual intake of lactic acid bacteria and risk reduction of bladder cancer,” Urologia Internationalis, vol. 68, no. 4, pp. 273–280, 2002. View at Publisher · View at Google Scholar · View at Scopus
  6. B.-K. Lim, R. Mahendran, Y.-K. Lee, and B.-H. Bay, “Chemopreventive effect of Latobacillus rhamnosus on growth of a subcutaneously implanted bladder cancer cell line in the mouse,” Japanese Journal of Cancer Research, vol. 93, no. 1, pp. 36–41, 2002. View at Publisher · View at Google Scholar · View at Scopus
  7. S. W. Seow, S. Cai, J. N. Rahmat et al., “Lactobacillus rhamnosus GG induces tumor regression in mice bearing orthotopic bladder tumors,” Cancer Science, vol. 101, no. 3, pp. 751–758, 2010. View at Publisher · View at Google Scholar · View at Scopus
  8. Z. S. Yuksel, E. Buber, T. Kocagoz, A. Alp, Z. Saribas, and N. L. Acan, “Mycobacterial strains that stimulate the immune system most efficiently as candidates for the treatment of bladder cancer,” Journal of Molecular Microbiology and Biotechnology, vol. 20, no. 1, pp. 24–28, 2011. View at Publisher · View at Google Scholar · View at Scopus
  9. 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
  10. G. Trinchieri, “Interleukin-12: a proinflammatory cytokine with immunoregulatory functions that bridge innate resistance and antigen-specific adaptive immunity,” Annual Review of Immunology, vol. 13, pp. 251–276, 1995. View at Publisher · View at Google Scholar · View at Scopus
  11. S. Miyazaki, F. Ishikawa, T. Fujikawa, S. Nagata, and K. Yamaguchi, “Intraperitoneal injection of lipopolysaccharide induces dynamic migration of Gr-1high polymorphonuclear neutrophils in the murine abdominal cavity,” Clinical and Diagnostic Laboratory Immunology, vol. 11, no. 3, pp. 452–457, 2004. View at Publisher · View at Google Scholar · View at Scopus
  12. C. Morel, E. Badell, V. Abadie et al., “Mycobacterium bovis BCG-infected neutrophils and dendritic cells cooperate to induced specific T cell responses in humans and mice,” European Journal of Immunology, vol. 38, no. 2, pp. 437–447, 2008. View at Publisher · View at Google Scholar · View at Scopus
  13. S. W. Seow, J. N. B. Rahmat, A. A. K. Mohamed, R. Mahendran, Y. K. Lee, and B. H. Bay, “Lactobacillus species is more cytotoxic to human bladder cancer cells than Mycobacterium Bovis (bacillus Calmette-Guerin),” The Journal of Urology, vol. 168, no. 5, pp. 2236–2239, 2002. View at Publisher · View at Google Scholar · View at Scopus
  14. I. Von Ossowski, J. Reunanen, R. Satokari et al., “Mucosal adhesion properties of the probiotic lactobacillus rhamnosus GG SpaCBA and SpaFED pilin subunits,” Applied and Environmental Microbiology, vol. 76, no. 7, pp. 2049–2057, 2010. View at Publisher · View at Google Scholar · View at Scopus
  15. J. N. Rahmat, K. Esuvaranathan, and R. Mahendran, “Bacillus Calmette-Guérin induces cellular reactive oxygen species and lipid peroxidation in cancer cells,” Urology, vol. 79, no. 6, pp. 1411.e15–1411.e20, 2012. View at Publisher · View at Google Scholar · View at Scopus
  16. M. Kandasamy, B.-H. Bay, Y.-K. Lee, and R. Mahendran, “Lactobacilli secreting a tumor antigen and IL15 activates neutrophils and dendritic cells and generates cytotoxic T lymphocytes against cancer cells,” Cellular Immunology, vol. 271, no. 1, pp. 89–96, 2011. View at Publisher · View at Google Scholar · View at Scopus
  17. S. Hedlund, A. Persson, A. Vujic, K. F. Che, O. Stendahl, and M. Larsson, “Dendritic cell activation by sensing Mycobacterium tuberculosis-induced apoptotic neutrophils via DC-SIGN,” Human Immunology, vol. 71, no. 6, pp. 535–540, 2010. View at Publisher · View at Google Scholar · View at Scopus
  18. M. Lanzinger, B. Jürgens, U. Hainz et al., “Ambivalent effects of dendritic cells displaying prostaglandin E2-induced indoleamine 2,3-dioxygenase,” European Journal of Immunology, vol. 42, no. 5, pp. 1117–1128, 2012. View at Publisher · View at Google Scholar · View at Scopus
  19. A. Shimabukuro-Vornhagen, T. M. Liebig, T. Koslowsky, S. Theurich, and M. S. von Bergwelt-Baildon, “The ratio between dendritic cells and T cells determines whether prostaglandin E2 has a stimulatory or inhibitory effect,” Cellular Immunology, vol. 281, no. 1, pp. 62–67, 2013. View at Publisher · View at Google Scholar · View at Scopus
  20. H. Harizi, M. Juzan, V. Pitard, J.-F. Moreau, and N. Gualde, “Cyclooxygenase-2-issued prostaglandin E2 enhances the production of endogenous IL-10, which down-regulates dendritic cell functions,” Journal of Immunology, vol. 168, no. 5, pp. 2255–2263, 2002. View at Publisher · View at Google Scholar · View at Scopus
  21. 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
  22. T. Takahashi, A. Kushiro, K. Nomoto et al., “Antitumor effects of the intravesical instillation of heat killed cells of the lactobacillus casei strain shirota on the murine orthotopic bladder tumor MBT-2,” Journal of Urology, vol. 166, no. 6, pp. 2506–2511, 2001. View at Publisher · View at Google Scholar · View at Scopus
  23. M. Mohamadzadeh, S. Olson, W. V. Kalina et al., “Lactobacilli activate 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
  24. H. R. Christensen, H. Frøkiær, and J. J. Pestka, “Lactobacilli differentially modulate expression of cytokines and maturation surface markers in murine dendritic cells,” The Journal of Immunology, vol. 168, no. 1, pp. 171–178, 2002. View at Publisher · View at Google Scholar · View at Scopus
  25. S. Cai, B. H. Bay, Y. K. Lee, J. Lu, and R. Mahendran, “Live and lyophilized Lactobacillus species elicit differential immunomodulatory effects on immune cells,” FEMS Microbiology Letters, vol. 302, no. 2, pp. 189–196, 2010. View at Publisher · View at Google Scholar · View at Scopus
  26. H. L. Tytgat, N. H. van Teijlingen, R. M. Sullan et al., “Probiotic gut microbiota isolate interacts with dendritic cells via glycosylated heterotrimeric pili,” PLoS One, vol. 11, no. 3, article e0151824, 2016. View at Publisher · View at Google Scholar
  27. T. Shimosato, H. Kitazawa, S. Katoh et al., “Augmentation of TH-1 type response by immunoactive AT oligonucleotide from lactic acid bacteria via Toll-like receptor 9 signaling,” Biochemical and Biophysical Research Communications, vol. 326, no. 4, pp. 782–787, 2005. View at Publisher · View at Google Scholar · View at Scopus
  28. S. Ichikawa, M. Miyake, R. Fujii, and Y. Konishi, “MyD88 associated ROS generation is crucial for Lactobacillus induced IL-12 production in macrophage,” PLoS One, vol. 7, no. 4, article e35880, 2012. View at Publisher · View at Google Scholar · View at Scopus
  29. K. Shida, J. Kiyoshima-Shibata, M. Nagaoka, K. Watanabe, and M. Nanno, “Induction of interleukin-12 by Lactobacillus strains having a rigid cell wall resistant to intracellular digestion,” Journal of Dairy Science, vol. 89, no. 9, pp. 3306–3317, 2006. View at Publisher · View at Google Scholar · View at Scopus
  30. V. Abadie, E. Badell, P. Douillard et al., “Neutrophils rapidly migrate via lymphatics after Mycobacterium bovis BCG intradermal vaccination and shuttle live bacilli to the draining lymph nodes,” Blood, vol. 106, no. 5, pp. 1843–1850, 2005. View at Publisher · View at Google Scholar · View at Scopus
  31. A. M. DeCathelineau and P. M. Henson, “The final step in programmed cell death: phagocytes carry apoptotic cells to the grave,” Essays in Biochemistry, vol. 39, pp. 105–117, 2003. View at Publisher · View at Google Scholar · View at Scopus
  32. C. Alfaro, N. Suarez, C. Oñate et al., “Dendritic cells take up and present antigens from viable and apoptotic polymorphonuclear leukocytes,” PLoS ONE, vol. 6, no. 12, Article ID e29300, 2011. View at Publisher · View at Google Scholar · View at Scopus
  33. L. M. Stuart, M. Lucas, C. Simpson, J. Lamb, J. Savill, and A. Lacy-Hulbert, “Inhibitory effects of apoptotic cell ingestion upon endotoxin-driven myeloid dendritic cell maturation,” Journal of Immunology, vol. 168, no. 4, pp. 1627–1635, 2002. View at Publisher · View at Google Scholar · View at Scopus
  34. A. Camporeale, A. Boni, G. Iezzi et al., “Critical impact of the kinetics of dendritic cells activation on the in vivo induction of tumor-specific T lymphocytes,” Cancer Research, vol. 63, no. 13, pp. 3688–3694, 2003. View at Google Scholar · View at Scopus
  35. K. Steinbrink, M. Wölfl, H. Jonuleit, J. Knop, and A. H. Enk, “Induction of tolerance by IL-10-treated dendritic cells,” The Journal of Immunology, vol. 159, no. 10, pp. 4772–4780, 1997. View at Google Scholar · View at Scopus
  36. D. L. Commeren, P. L. Van Soest, K. Karimi, B. Löwenberg, J. J. Cornelissen, and E. Braakman, “Paradoxical effects of interleukin-10 on the maturation of murine myeloid dendritic cells,” Immunology, vol. 110, no. 2, pp. 188–196, 2003. View at Publisher · View at Google Scholar · View at Scopus
  37. L. Faulkner, G. Buchan, and M. Baird, “Interleukin-10 does not affect phagocytosis of particulate antigen by bone marrow-derived dendritic cells but does impair antigen presentation,” Immunology, vol. 99, no. 4, pp. 523–531, 2000. View at Publisher · View at Google Scholar · View at Scopus
  38. W. L. W. Chang, N. Baumgarth, M. K. Eberhardt et al., “Exposure of myeloid dendritic cells to exogenous or endogenous IL-10 during maturation determines their longevity,” The Journal of Immunology, vol. 178, no. 12, pp. 7794–7804, 2007. View at Publisher · View at Google Scholar · View at Scopus