Table of Contents
ISRN Gastroenterology
Volume 2011, Article ID 892971, 11 pages
http://dx.doi.org/10.5402/2011/892971
Review Article

Importance of IL-10 Modulation by Probiotic Microorganisms in Gastrointestinal Inflammatory Diseases

1Centro de Referencia para Lactobacilos (CERELA-CONICET), Chacabuco 145, San Miguel de Tucumán, T4000ILC Tucumán, Argentina
2Institute of Biological Sciences, Federal University of Minas Gerais (UFMG-ICB), Belo Horizonte, MG, CEP 31270-901, Brazil
3Microbial Genetics Research Unit, Microbiology and the Food Chain Department, INRA Research Centre of Jouy-en-Josas, 78352 Paris, France

Received 18 November 2010; Accepted 23 December 2010

Academic Editors: A. Amedei, J. Clària, J. De Man, and A. Weimann

Copyright © 2011 Alejandra de Moreno de LeBlanc 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. S. Nouaille, L. A. Ribeiro, A. Miyoshi et al., “Heterologous protein production and delivery systems for Lactococcus lactis,” Genetics and Molecular Research, vol. 2, no. 1, pp. 102–111, 2003. View at Google Scholar · View at Scopus
  2. V. Azevedo and A. Miyoshi, “Novas utilizações biotecnológicas e terapêuticas das bactérias do ácido láctico,” 2004.
  3. A. Bolotin, P. Wincker, S. Mauger et al., “The complete genome sequence of the lactic acid bacterium lactococcus lactis ssp. lactis IL1403,” Genome Research, vol. 11, no. 5, pp. 731–753, 2001. View at Publisher · View at Google Scholar · View at Scopus
  4. E. A. Pfeiler and T. R. Klaenhammer, “The genomics of lactic acid bacteria,” Trends in Microbiology, vol. 15, no. 12, pp. 546–553, 2007. View at Publisher · View at Google Scholar · View at Scopus
  5. J. G. LeBlanc, A. de Moreno de LeBlanc, G. Perdigón et al., “Anti-inflammatory properties of lactic acid bacteria: current knowledge, applications and prospects,” Anti-Infective Agents in Medicinal Chemistry, vol. 7, no. 3, pp. 148–154, 2008. View at Publisher · View at Google Scholar · View at Scopus
  6. A. C. Ouwehand, S. Salminen, and E. Isolauri, “Probiotics: an overview of beneficial effects,” Antonie van Leeuwenhoek, vol. 82, no. 1-4, pp. 279–289, 2002. View at Publisher · View at Google Scholar · View at Scopus
  7. “Report of a Joint FAO/WHO Expert Consultation on Evaluation of Health and Nutritional Properties of Probiotics in Food Including Powder Milk with Live Lactic Acid Bacteria,” pp. 2001.
  8. C. Maldonado Galdeano, A. de Moreno de LeBlanc, G. Vinderola, M. E. Bibas Bonet, and G. Perdigón, “Proposed model: mechanisms of immunomodulation induced by probiotic bacteria,” Clinical and Vaccine Immunology, vol. 14, no. 5, pp. 485–492, 2007. View at Publisher · View at Google Scholar · View at Scopus
  9. A. Miyoshi, L. Bermudez-Humaran, M. Pacheco de Azevedo, P. Langella, and V. Azevedo, “Lactic acid bacteria as live vectors: heterologous protein production and delivery systems,” in Biotechnology of Lactic Acid Bacteria Novel Applications, F. Mozzi, R. Raya, and G. Vignolo, Eds., p. 9, Blackwell Publishing, Ames, Iowa, USA, 2010. View at Google Scholar
  10. J. M. Wells, P. W. Wilson, P. M. Norton, M. J. Gasson, and R. W. F. Le Page, “Lactococcus lactis: high-level expression of tetanus toxin fragment C and protection against lethal challenge,” Molecular Microbiology, vol. 8, no. 6, pp. 1155–1162, 1993. View at Google Scholar · View at Scopus
  11. P. M. Norton, R. W. F. Le Page, and J. M. Wells, “Progress in the development of Lactococcus lactis as a recombinant mucosal vaccine delivery system,” Folia Microbiologica, vol. 40, no. 3, pp. 225–230, 1995. View at Publisher · View at Google Scholar · View at Scopus
  12. Y. Le Loir, S. Nouaille, J. Commissaire, L. Brétigny, A. Gruss, and P. Langella, “Signal peptide and propeptide optimization for heterologous protein secretion in Lactococcus lactis,” Applied and Environmental Microbiology, vol. 67, no. 9, pp. 4119–4127, 2001. View at Publisher · View at Google Scholar · View at Scopus
  13. S. Innocentin, V. Guimarães, A. Miyoshi et al., “Lactococcus lactis expressing either Staphylococcus aureus fibronectin-binding protein A or Listeria monocytogenes internalin A can efficiently internalize and deliver DNA in human epithelial cells,” Applied and Environmental Microbiology, vol. 75, no. 14, pp. 4870–4878, 2009. View at Publisher · View at Google Scholar · View at Scopus
  14. K. Asadullah, W. Sterry, and H. D. Volk, “Interleukin-10 therapy—review of a new approach,” Pharmacological Reviews, vol. 55, no. 2, pp. 241–269, 2003. View at Publisher · View at Google Scholar · View at Scopus
  15. I. Lalani, K. Bhol, and A. R. Ahmed, “Interleukin-10: biology, role in inflammation and autoimmunity,” Annals of Allergy, Asthma and Immunology, vol. 79, no. 6, pp. 469–484, 1997. View at Google Scholar · View at Scopus
  16. M. Howard and A. O'Garra, “Biological properties of interleukin 10,” Immunology Today, vol. 13, no. 6, pp. 198–200, 1992. View at Google Scholar · View at Scopus
  17. S. M. Opal, J. C. Wherry, and P. Grint, “Interleukin-10: potential benefits and possible risks in clinical infectious diseases,” Clinical Infectious Diseases, vol. 27, no. 6, pp. 1497–1507, 1998. View at Google Scholar · View at Scopus
  18. K. W. Moore, R. de Waal Malefyt, R. L. Coffman, and A. O'Garra, “Interleukin-10 and the interleukin-10 receptor,” Annual Review of Immunology, vol. 19, pp. 683–765, 2001. View at Publisher · View at Google Scholar · View at Scopus
  19. M. Kamanaka, S. T. Kim, Y. Y. Wan et al., “Expression of interleukin-10 in intestinal lymphocytes detected by an interleukin-10 reporter knockin tiger mouse,” Immunity, vol. 25, no. 6, pp. 941–952, 2006. View at Publisher · View at Google Scholar · View at Scopus
  20. L. M. Williams, G. Ricchetti, U. Sarma, T. Smallie, and B. M. J. Foxwell, “Interleukin-10 suppression of myeloid cell activation—a continuing puzzle,” Immunology, vol. 113, no. 3, pp. 281–292, 2004. View at Publisher · View at Google Scholar · View at Scopus
  21. S. Mocellin, F. Marincola, C. R. Rossi, D. Nitti, and M. Lise, “The multifaceted relationship between IL-10 and adaptive immunity: putting together the pieces of a puzzle,” Cytokine and Growth Factor Reviews, vol. 15, no. 1, pp. 61–76, 2004. View at Publisher · View at Google Scholar · View at Scopus
  22. K. N. Couper, D. G. Blount, and E. M. Riley, “IL-10: the master regulator of immunity to infection,” Journal of Immunology, vol. 180, no. 9, pp. 5771–5777, 2008. View at Google Scholar · View at Scopus
  23. G. Del Prete, M. de Carli, F. Almerigogna, M. G. Giudizi, R. Biagiotti, and S. Romagnani, “Human IL-10 is produced by both type 1 helper (Th1) and type 2 helper (Th2) T cell clones and inhibits their antigen-specific proliferation and cytokine production,” Journal of Immunology, vol. 150, no. 2, pp. 353–360, 1993. View at Google Scholar · View at Scopus
  24. R. de Waal Malefyt, J. Abrams, B. Bennett, C. G. Figdor, and J. E. de Vries, “Interleukin 10(IL-10) inhibits cytokine synthesis by human monocytes: an autoregulatory role of IL-10 produced by monocytes,” Journal of Experimental Medicine, vol. 174, no. 5, pp. 1209–1220, 1991. View at Google Scholar · View at Scopus
  25. P. Allavena, L. Piemonti, D. Longoni et al., “IL-10 prevents the differentiation of monocytes to dendritic cells but promotes their maturation to macrophages,” European Journal of Immunology, vol. 28, no. 1, pp. 359–369, 1998. View at Publisher · View at Google Scholar · View at Scopus
  26. A. S. Morel, S. Quaratino, D. C. Douek, and M. Londei, “Split activity of interleukin-10 on antigen capture and antigen presentation by human dendritic cells: definition of a maturative step,” European Journal of Immunology, vol. 27, no. 1, pp. 26–34, 1997. View at Publisher · View at Google Scholar · View at Scopus
  27. C. Demangel, P. Bertolino, and W. J. Britton, “Autocrine IL-10 impairs dendritic cell (DC)-derived immune responses to mycobacterial infection by suppressing DC trafficking to draining lymph nodes and local IL-12 production,” European Journal of Immunology, vol. 32, no. 4, pp. 994–1002, 2002. View at Publisher · View at Google Scholar · View at Scopus
  28. J. Wang, E. Guan, G. Roderiquez, and M. A. Norcross, “Inhibition of CCR5 expression by IL-12 through induction of β- chemokines in human T lymphocytes,” Journal of Immunology, vol. 163, no. 11, pp. 5763–5769, 1999. View at Google Scholar · View at Scopus
  29. T. H. Flo, O. Halaas, S. Torp et al., “Differential expression of Toll-like receptor 2 in human cells,” Journal of Leukocyte Biology, vol. 69, no. 3, pp. 474–481, 2001. View at Google Scholar · View at Scopus
  30. R. M. Vabulas, S. Braedel, N. Hilf et al., “The endoplasmic reticulum-resident heat shock protein Gp96 activates dendritic cells via the toll-like receptor 2/4 pathway,” Journal of Biological Chemistry, vol. 277, no. 23, pp. 20847–20853, 2002. View at Publisher · View at Google Scholar
  31. Y. Shibata, L. A. Foster, M. Kurimoto et al., “Immunoregulatory roles of IL-10 in innate immunity: IL-10 inhibits macrophage production of IFN-γ-inducing factors but enhances NK cell production of IFN-γ,” Journal of Immunology, vol. 161, no. 8, pp. 4283–4288, 1998. View at Google Scholar · View at Scopus
  32. D. M. Mosser and X. Zhang, “Interleukin-10: new perspectives on an old cytokine,” Immunological Reviews, vol. 226, no. 1, pp. 205–218, 2008. View at Publisher · View at Google Scholar · View at Scopus
  33. H. L. Weiner, P. A. Gonnella, A. Slavin, and R. Maron, “Oral tolerance: cytokine milieu in the gut and modulation of tolerance by cytokines,” Research in Immunology, vol. 148, no. 8-9, pp. 528–533, 1997. View at Publisher · View at Google Scholar · View at Scopus
  34. D. J. O'Sullivan, “Screening of intestinal microflora for effective probiotic bacteria,” Journal of Agricultural and Food Chemistry, vol. 49, no. 4, pp. 1751–1760, 2001. View at Publisher · View at Google Scholar · View at Scopus
  35. M. J. Ruddy, G. C. Wong, X. K. Liu et al., “Functional cooperation between interleukin-17 and tumor necrosis factor-α is mediated by CCAAT/enhancer-binding protein family members,” Journal of Biological Chemistry, vol. 279, no. 4, pp. 2559–2567, 2004. View at Publisher · View at Google Scholar · View at Scopus
  36. F. Leon, L. E. Smythies, P. D. Smith, and B. L. Kelsall, “Involvement of dendritic cells in the pathogenesis of inflammatory bowel disease,” Advances in Experimental Medicine and Biology, vol. 579, pp. 117–132, 2006. View at Publisher · View at Google Scholar · View at Scopus
  37. M. F. Neurath, I. Fuss, B. L. Kelsall, D. H. Presky, W. Waegell, and W. Strober, “Experimental granulomatous colitis in mice is abrogated by induction of TGF-β-mediated oral tolerance,” Journal of Experimental Medicine, vol. 183, no. 6, pp. 2605–2616, 1996. View at Publisher · View at Google Scholar · View at Scopus
  38. H. Jonuleit, E. Schmitt, M. Stassen, A. Tuettenberg, J. Knop, and A. H. Enk, “Identification and functional characterization of human CD4(+)CD25(+) T cells with regulatory properties isolated from peripheral blood,” Journal of Experimental Medicine, vol. 193, no. 11, pp. 1285–1294, 2001. View at Publisher · View at Google Scholar · View at Scopus
  39. Y. Cong, C. T. Weaver, A. Lazenby, and C. O. Elson, “Bacterial-reactive T regulatory cells inhibit pathogenic immune responses to the enteric flora,” Journal of Immunology, vol. 169, no. 11, pp. 6112–6119, 2002. View at Google Scholar · View at Scopus
  40. D. K. Podolsky, “Inflammatory bowel disease,” New England Journal of Medicine, vol. 347, no. 6, pp. 417–429, 2002. View at Publisher · View at Google Scholar · View at Scopus
  41. S. Brand, “Crohn's disease: Th1, Th17 or both? The change of a paradigm: new immunological and genetic insights implicate Th17 cells in the pathogenesis of Crohn's disease,” Gut, vol. 58, no. 8, pp. 1152–1167, 2009. View at Publisher · View at Google Scholar · View at Scopus
  42. A. Kappeler and C. Mueller, “The role of activated cytotoxic T cells in inflammatory bowel disease,” Histology and Histopathology, vol. 15, no. 1, pp. 167–172, 2000. View at Google Scholar · View at Scopus
  43. G. Perdigon, M. Medina, E. Vintini, and J. C. Valdez, “Intestinal pathway of internalisation of lactic acid bacteria and gut mucosal immunostimulation,” International Journal of Immunopathology and Pharmacology, vol. 13, no. 3, pp. 141–150, 2000. View at Google Scholar · View at Scopus
  44. 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
  45. P. Gupta, H. Andrew, B. S. Kirschner, and S. Guandalini, “Is Lactobacillus GG helpful in children with Crohn's disease? Results of a preliminary, open-label study,” Journal of Pediatric Gastroenterology and Nutrition, vol. 31, no. 4, pp. 453–457, 2000. View at Publisher · View at Google Scholar · View at Scopus
  46. A. de Moreno de LeBlanc, S. Chaves, and G. Perdigón, “Effect of yoghurt on the cytokine profile using a murine model of intestinal inflammation,” European Journal of Inflammation, vol. 7, no. 2, pp. 97–109, 2009. View at Google Scholar · View at Scopus
  47. C. M. Galdeano, A. de Moreno de LeBlanc, E. Carmuega, R. Weill, and G. Perdigón, “Mechanisms involved in the immunostimulation by probiotic fermented milk,” Journal of Dairy Research, vol. 76, no. 4, pp. 446–454, 2009. View at Publisher · View at Google Scholar · View at Scopus
  48. M. G. Vizoso Pinto, M. Rodriguez Gómez, S. Seifert, B. Watzl, W. H. Holzapfel, and C. M. A. P. Franz, “Lactobacilli stimulate the innate immune response and modulate the TLR expression of HT29 intestinal epithelial cells in vitro,” International Journal of Food Microbiology, vol. 133, no. 1-2, pp. 86–93, 2009. View at Publisher · View at Google Scholar · View at Scopus
  49. S. Ishihara, M. A. K. Rumi, C. F. Ortega-Cava et al., “Therapeutic targeting of toll-like receptors in gastrointestinal inflammation,” Current Pharmaceutical Design, vol. 12, no. 32, pp. 4215–4228, 2006. View at Publisher · View at Google Scholar · View at Scopus
  50. P. Pimentel-Nunes, J. B. Soares, R. Roncon-Albuquerque, M. Dinis-Ribeiro, and A. F. Leite-Moreira, “Toll-like receptors as therapeutic targets in gastrointestinal diseases,” Expert Opinion on Therapeutic Targets, vol. 14, no. 4, pp. 347–368, 2010. View at Publisher · View at Google Scholar · View at Scopus
  51. M. Schultz and A. L. Lindström, “Rationale for probiotic treatment strategies in inflammatory bowel disease,” Expert Review of Gastroenterology and Hepatology, vol. 2, no. 3, pp. 337–355, 2008. View at Publisher · View at Google Scholar · View at Scopus
  52. M. Fukata and M. T. Abreu, “TLR4 signalling in the intestine in health and disease,” Biochemical Society Transactions, vol. 35, no. 6, pp. 1473–1478, 2007. View at Publisher · View at Google Scholar · View at Scopus
  53. C. A. Dogi, C. M. Galdeano, and G. Perdigón, “Gut immune stimulation by non pathogenic Gram(+) and Gram(-) bacteria. Comparison with a probiotic strain,” Cytokine, vol. 41, no. 3, pp. 223–231, 2008. View at Publisher · View at Google Scholar · View at Scopus
  54. Y. W. Chung, J. H. Choi, T. Y. Oh, C. S. Eun, and D. S. Han, “Lactobacillus casei prevents the development of dextran sulphate sodium-induced colitis in Toll-like receptor 4 mutant mice,” Clinical and Experimental Immunology, vol. 151, no. 1, pp. 182–189, 2008. View at Publisher · View at Google Scholar · View at Scopus
  55. D. Rachmilewitz, F. Karmeli, K. Takabayashi et al., “Immunostimulatory DNA ameliorates experimental and spontaneous murine colitis,” Gastroenterology, vol. 122, no. 5, pp. 1428–1441, 2002. View at Google Scholar · View at Scopus
  56. F. Obermeier, N. Dunger, U. G. Strauch et al., “CpG motifs of bacterial DNA essentially contribute to the perpetuation of chronic intestinal inflammation,” Gastroenterology, vol. 129, no. 3, pp. 913–927, 2005. View at Publisher · View at Google Scholar · View at Scopus
  57. M. Akhtar, J. L. Watson, A. Nazli, and D. M. McKay, “Bacterial DNA evokes epithelial IL-8 production by a MAPK-dependent, NF-kappaB-independent pathway,” The FASEB Journal, vol. 17, no. 10, pp. 1319–1321, 2003. View at Google Scholar · View at Scopus
  58. J. Lee, D. Rachmilewitz, and E. Raz, “Homeostatic effects of TLR9 signaling in experimental colitis,” Annals of the New York Academy of Sciences, vol. 1072, pp. 351–355, 2006. View at Publisher · View at Google Scholar · View at Scopus
  59. D. Rachmilewitz, K. Katakura, F. Karmeli et al., “Toll-like receptor 9 signaling mediates the anti-inflammatory effects of probiotics in murine experimental colitis,” Gastroenterology, vol. 126, no. 2, pp. 520–528, 2004. View at Publisher · View at Google Scholar · View at Scopus
  60. D. Rachmilewitz, F. Karmeli, S. Shteingart, J. Lee, K. Takabayashi, and E. Raz, “Immunostimulatory oligonucleotides inhibit colonic proinflammatory cytokine production in ulcerative colitis,” Inflammatory Bowel Diseases, vol. 12, no. 5, pp. 339–345, 2006. View at Publisher · View at Google Scholar · View at Scopus
  61. N. Kamada, N. Inoue, T. Hisamatsu et al., “Nonpathogenic Escherichia coli strain Nissle 1917 prevents murine acute and chronic colitis,” Inflammatory Bowel Diseases, vol. 11, no. 5, pp. 455–463, 2005. View at Publisher · View at Google Scholar · View at Scopus
  62. R. Kuhn, J. Lohler, D. Rennick, K. Rajewsky, and W. Muller, “Interleukin-10-deficient mice develop chronic enterocolitis,” Cell, vol. 75, no. 2, pp. 263–274, 1993. View at Publisher · View at Google Scholar · View at Scopus
  63. H. Tilg, C. Van Montfrans, A. Van den Ende et al., “Treatment of Crohn's disease with recombinant human interleukin 10 induces the proinflammatory cytokine interferon γ,” Gut, vol. 50, no. 2, pp. 191–195, 2002. View at Publisher · View at Google Scholar · View at Scopus
  64. H. H. Uhlig, J. Coombes, C. Mottet et al., “Characterization of Foxp3+ CD4+ CD25+ and IL-10-secreting CD4+ CD25+ T cells during cure of colitis,” Journal of Immunology, vol. 177, no. 9, pp. 5852–5860, 2006. View at Google Scholar · View at Scopus
  65. H. H. Cui, C. L. Chen, JI. D. Wang et al., “Effects of probiotic on intestinal mucosa of patients with ulcerative colitis,” World Journal of Gastroenterology, vol. 10, no. 10, pp. 1521–1525, 2004. View at Google Scholar · View at Scopus
  66. F. Calcinaro, S. Dionisi, M. Marinaro et al., “Oral probiotic administration induces interleukin-10 production and prevents spontaneous autoimmune diabetes in the non-obese diabetic mouse,” Diabetologia, vol. 48, no. 8, pp. 1565–1575, 2005. View at Publisher · View at Google Scholar · View at Scopus
  67. G. Mastrangeli, S. Corinti, C. Butteroni et al., “Effects of live and inactivated VSL#3 probiotic preparations in the modulation of in vitro and in vivo allergen-induced Th2 responses,” International Archives of Allergy and Immunology, vol. 150, no. 2, pp. 133–143, 2009. View at Publisher · View at Google Scholar · View at Scopus
  68. C. Di Giacinto, M. Marinaro, M. Sanchez, W. Strober, and M. Boirivant, “Probiotics ameliorate recurrent Th1-mediated murine colitis by inducing IL-10 and IL-10-dependent TGF-β-bearing regulatory cells,” Journal of Immunology, vol. 174, no. 6, pp. 3237–3246, 2005. View at Google Scholar · View at Scopus
  69. S. Lavasani, B. Dzhambazov, M. Nouri et al., “A novel probiotic mixture exerts a therapeutic effect on experimental autoimmune encephalomyelitis mediated by IL-10 producing regulatory T cells,” PLoS ONE, vol. 5, no. 2, Article ID e9009, 2010. View at Publisher · View at Google Scholar · View at Scopus
  70. A. de Moreno de LeBlanc and G. Perdigón, “The application of probiotic fermented milks in cancer and intestinal inflammation,” Proceedings of the Nutrition Society, vol. 69, pp. 421–428, 2010. View at Publisher · View at Google Scholar · View at Scopus
  71. B. G. Jung, S. J. Cho, H. B. Koh, D. U. Han, and B. J. Lee, “Fermented Maesil (Prunus mume) with probiotics inhibits development of atopic dermatitis-like skin lesions in NC/Nga mice,” Veterinary Dermatology, vol. 21, no. 2, pp. 184–191, 2010. View at Publisher · View at Google Scholar · View at Scopus
  72. R. D'Incà, M. Barollo, M. Scarpa et al., “Rectal administration of Lactobacillus casei DG modifies flora composition and Toll-Like receptor expression in colonic mucosa of patients with mild ulcerative colitis,” Digestive Diseases and Sciences. In press. View at Publisher · View at Google Scholar
  73. J. Villena, N. Barbieri, S. Salva, M. Herrera, and S. Alvarez, “Enhanced immune response to pneumococcal infection in malnourished mice nasally treated with heat-killed Lactobacillus casei,” Microbiology and Immunology, vol. 53, no. 11, pp. 636–646, 2009. View at Publisher · View at Google Scholar · View at Scopus
  74. N. Li, W. M. Russell, M. Douglas-Escobar, N. Hauser, M. Lopez, and J. Neu, “Live and heat-killed lactobacillus rhamnosus GG: effects on proinflammatory and anti-inflammatory cytokines/chemokines in gastrostomy-fed infant rats,” Pediatric Research, vol. 66, no. 2, pp. 203–207, 2009. View at Publisher · View at Google Scholar · View at Scopus
  75. B. Foligne, S. Nutten, C. Grangette et al., “Correlation between in vitro and in vivo immunomodulatory properties of lactic acid bacteria,” World Journal of Gastroenterology, vol. 13, no. 2, pp. 236–243, 2007. View at Google Scholar · View at Scopus
  76. L. M. dos Santos, M. M. Santos, H. P. de Souza Silva, R. M.E. Arantes, J. R. Nicoli, and L. Q. Vieira, “Monoassociation with probiotic Lactobacillus delbrueckii UFV-H2b20 stimulates the immune system and protects germfree mice against Listeria monocytogenes infection,” Medical Microbiology and Immunology, vol. 200, no. 1, pp. 29–38, 2011. View at Publisher · View at Google Scholar
  77. S. Sierra, F. Lara-Villoslada, L. Sempere, M. Olivares, J. Boza, and J. Xaus, “Intestinal and immunological effects of daily oral administration of Lactobacillus salivarius CECT5713 to healthy adults,” Anaerobe, vol. 16, no. 3, pp. 195–200, 2010. View at Publisher · View at Google Scholar · View at Scopus
  78. S. V. Generoso, M. Viana, R. Santos et al., “Saccharomyces cerevisiae strain UFMG 905 protects against bacterial translocation, preserves gut barrier integrity and stimulates the immune system in a murine intestinal obstruction model,” Archives of Microbiology, vol. 192, no. 6, pp. 477–484, 2010. View at Publisher · View at Google Scholar · View at Scopus
  79. C. Grangette, S. Nutten, E. Palumbo et al., “Enhanced antiinflammatory capacity of a Lactobacillus plantarum mutant synthesizing modified teichoic acids,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 29, pp. 10321–10326, 2005. View at Publisher · View at Google Scholar · View at Scopus
  80. F. A.V. Marinho, L. G.G. Pacífico, A. Miyoshi et al., “An intranasal administration of Lactococcus lactis strains expressing recombinant interleukin-10 modulates acute allergic airway inflammation in a murine model,” Clinical and Experimental Allergy, vol. 40, no. 10, pp. 1541–1551, 2010. View at Publisher · View at Google Scholar
  81. L. Steidler, W. Hans, L. Schotte et al., “Treatment of murine colitis by Lactococcus lactis secreting interleukin-10,” Science, vol. 289, no. 5483, pp. 1352–1355, 2000. View at Publisher · View at Google Scholar · View at Scopus
  82. M. Roselli, A. Finamore, S. Nuccitelli et al., “Prevention of TNBS-induced colitis by different Lactobacillus and Bifidobacterium strains is associated with an expansion of γδT and regulatory T cells of intestinal intraepithelial lymphocytes,” Inflammatory Bowel Diseases, vol. 15, no. 10, pp. 1526–1536, 2009. View at Publisher · View at Google Scholar
  83. E. Mengheri, “Health, probiotics, and inflammation,” Journal of clinical gastroenterology, vol. 42, pp. S177–178, 2008. View at Google Scholar · View at Scopus
  84. W. Sybesma, J. Hugenholtz, W. M. de Vos, and E. J. Smid, “Safe use of genetically modified lactic acid bacteria in food. Bridging the gap between consumers, green groups, and industry,” Electronic Journal of Biotechnology, vol. 9, no. 4, pp. 1–25, 2006. View at Publisher · View at Google Scholar · View at Scopus
  85. L. Schotte, L. Steidler, J. Vandekerckhove, and E. Remaut, “Secretion of biologically active murine interleukin-10 by Lactococcus lactis,” Enzyme and Microbial Technology, vol. 27, no. 10, pp. 761–765, 2000. View at Publisher · View at Google Scholar · View at Scopus
  86. K. G. Tournoy, J. C. Kips, and R. A. Pauwels, “Endogenous interleukin-10 suppresses allergen-induced airway inflammation and nonspecific airway responsiveness,” Clinical and Experimental Allergy, vol. 30, no. 6, pp. 775–783, 2000. View at Publisher · View at Google Scholar · View at Scopus
  87. C. P. Frossard, L. Steidler, and P. A. Eigenmann, “Oral administration of an IL-10-secreting Lactococcus lactis strain prevents food-induced IgE sensitization,” Journal of Allergy and Clinical Immunology, vol. 119, no. 4, pp. 952–959, 2007. View at Publisher · View at Google Scholar · View at Scopus
  88. A. Waeytens, L. Ferdinande, S. Neirynck et al., “Paracellular entry of interleukin-10 producing Lactococcus lactis in inflamed intestinal mucosa in mice,” Inflammatory Bowel Diseases, vol. 14, no. 4, pp. 471–479, 2008. View at Publisher · View at Google Scholar · View at Scopus
  89. M. Loos, E. Remaut, P. Rottiers, and A. de Creus, “Genetically engineered Lactococcus lactis secreting murine IL-10 modulates the functions of bone marrow-derived dendritic cells in the presence of LPS,” Scandinavian Journal of Immunology, vol. 69, no. 2, pp. 130–139, 2009. View at Publisher · View at Google Scholar · View at Scopus
  90. L. Steidler, S. Neirynck, N. Huyghebaert et al., “Biological containment of genetically modified Lactococcus lactis for intestinal delivery of human interleukin 10,” Nature Biotechnology, vol. 21, no. 7, pp. 785–789, 2003. View at Publisher · View at Google Scholar · View at Scopus
  91. H. Braat, P. Rottiers, D. W. Hommes et al., “A phase I trial with transgenic bacteria expressing interleukin-10 in Crohn's disease,” Clinical Gastroenterology and Hepatology, vol. 4, no. 6, pp. 754–759, 2006. View at Publisher · View at Google Scholar · View at Scopus
  92. S. Termont, K. Vandenbroucke, D. Iserentant et al., “Intracellular accumulation of trehalose protects Lactococcus lactis from freeze-drying damage and bile toxicity and increases gastric acid resistance,” Applied and Environmental Microbiology, vol. 72, no. 12, pp. 7694–7700, 2006. View at Publisher · View at Google Scholar · View at Scopus
  93. N. Huyghebaert, AN. Vermeire, S. Neirynck, L. Steidler, E. Remaut, and J. P. Remon, “Development of an enteric-coated formulation containing freeze-dried, viable recombinant Lactococcus lactis for the ileal mucosal delivery of human interleukin-10,” European Journal of Pharmaceutics and Biopharmaceutics, vol. 60, no. 3, pp. 349–359, 2005. View at Publisher · View at Google Scholar · View at Scopus
  94. N. Huyghebaert, A. N. Vermeire, S. Neirynck, L. Steidler, E. Remaut, and J. P. Remon, “Evaluation of extrusion/spheronisation, layering and compaction for the preparation of an oral, multi-particulate formulation of viable, hIL-10 producing Lactococcus lactis,” European Journal of Pharmaceutics and Biopharmaceutics, vol. 59, no. 1, pp. 9–15, 2005. View at Publisher · View at Google Scholar · View at Scopus
  95. S. del Carmen, A. de Moreno de LeBlanc, A. Miyoshi, C. Santos Rochat, V. Azevedo, and J. G. LeBlanc, “Application of probiotics in the prevention and treatment of ulcerative colitis and other inflammatory bowel diseases,” Ulcers, vol. 2011, Article ID 841651, 13 pages, 2011. View at Publisher · View at Google Scholar
  96. J. G. LeBlanc, S. del Carmen, A. Miyoshi et al., “Use of superoxide dismutase and catalase expressing lactic acid bacteria to attenuate TNBS induced Crohn’s disease in mice,” Journal of Biotechnology, vol. 151, no. 3, pp. 287–293, 2011. View at Publisher · View at Google Scholar
  97. J. G. LeBlanc, D. van Sinderen, J. Hugenholtz, J.-C. Piard, F. Sesma, and G. Savoy de Giori, “Risk assessment of genetically modified lactic acid bacteria using the concept of substantial equivalence,” Current Microbiology, vol. 61, no. 6, pp. 590–595, 2010. View at Google Scholar