Gastroenterology
Volume 133, Issue 2 , Pages 517-528 , August 2007

Induction of Ovalbumin-Specific Tolerance by Oral Administration of Lactococcus lactis Secreting Ovalbumin

  • Inge L. Huibregtse

      Affiliations

    • Center for Experimental and Molecular Medicine, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands
    • I.L. Huibregtse, and V. Snoeck contributed equally to this manuscript.
    • ,
  • Veerle Snoeck

      Affiliations

    • Department for Molecular Biomedical Research, Flanders Interuniversity Institute for Biotechnology, Ghent, Belgium
    • Department of Molecular Biology, Ghent University, Ghent, Belgium
    • I.L. Huibregtse, and V. Snoeck contributed equally to this manuscript.
    • ,
  • An de Creus

      Affiliations

    • Department for Molecular Biomedical Research, Flanders Interuniversity Institute for Biotechnology, Ghent, Belgium
    • Department of Molecular Biology, Ghent University, Ghent, Belgium
    • ,
  • Henri Braat

      Affiliations

    • Center for Experimental and Molecular Medicine, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands
    • ,
  • Ester C. de Jong

      Affiliations

    • Department of Cell Biology and Histology, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands
    • ,
  • Sander J.H. van Deventer

      Affiliations

    • Center for Experimental and Molecular Medicine, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands
    • ,
  • Pieter Rottiers

      Affiliations

    • Department for Molecular Biomedical Research, Flanders Interuniversity Institute for Biotechnology, Ghent, Belgium
    • Department of Molecular Biology, Ghent University, Ghent, Belgium
    • Corresponding Author InformationAddress requests for reprints to: Pieter Rottiers, PhD, Technologiepark 4 B-9052 Zwijnaarde, Ghent, Belgium. fax: (32) 9 2610619.

Received 22 January 2007 ,Accepted 19 April 2007.

References 

  1. Abreu-Martin MT, Targan SR. Regulation of immune responses of the intestinal mucosa. Crit Rev Immunol. 1996;16:277–309
  2. Faria AM, Weiner HL. Oral tolerance. Immunol Rev. 2005;206:232–259
  3. Kraus TA, Mayer L. Oral tolerance and inflammatory bowel disease. Curr Opin Gastroenterol. 2005;21:692–696
  4. Weiner HL. Current issues in the treatment of human diseases by mucosal tolerance. Ann N Y Acad Sci. 2004;1029:211–224
  5. Friedman A, Weiner HL. Induction of anergy or active suppression following oral tolerance is determined by antigen dosage. Proc Natl Acad Sci U S A. 1994;91:6688–6692
  6. Mowat AM, Strobel S, Drummond HE, Ferguson A. Immunological responses to fed protein antigens in mice (I. Reversal of oral tolerance to ovalbumin by cyclophosphamide). Immunology. 1982;45:105–113
  7. Yoshida T, Hachimura S, Kaminogawa S. The oral administration of low-dose antigen induces activation followed by tolerization, while high-dose antigen induces tolerance without activation. Clin Immunol Immunopathol. 1997;82:207–215
  8. Sun J, Alison SM, Thompson KL, Fisher VH. Cell cycle block in anergic T cells during tolerance induction. Cell Immunol. 2003;225:33–41
  9. Huibregtse IL, van Lent AU, van Deventer SJ. Immunopathogenesis of IBD: insufficient suppressor function in the gut?. Gut. 2007;56:584–592
  10. Steidler L, Hans W, Schotte L, Neirynck S, Obermeier F, Falk W, et al. Treatment of murine colitis by Lactococcus lactis secreting interleukin-10. Science. 2000;289:1352–1355
  11. Vandenbroucke K, Hans W, Van Huysse J, Neirynck S, Demetter P, Remaut E, et al. Active delivery of trefoil factors by genetically modified Lactococcus lactis prevents and heals acute colitis in mice. Gastroenterology. 2004;127:502–513
  12. Steidler L, Neirynck S, Huyghebaert N, Snoeck V, Vermeire A, Goddeeris B, et al. Biological containment of genetically modified Lactococcus lactis for intestinal delivery of human interleukin 10. Nat Biotechnol. 2003;21:785–789
  13. Braat H, Rottiers P, Hommes DW, Huyghebaert N, Remaut E, Remon JP, et al. A phase I trial with transgenic bacteria expressing interleukin-10 in Crohn’s disease. Clin Gastroenterol Hepatol. 2006;4:754–759
  14. Gasson MJ. Plasmid complements of Streptococcus lactis NCDO 712 and other lactic streptococci after protoplast-induced curing. J Bacteriol. 1983;154:1–9
  15. McReynolds L, O’Malley BW, Nisbet AD, Fothergill JE, Givol D, Fields S, et al. Sequence of chicken ovalbumin mRNA. Nature. 1978;273:723–728
  16. van Asseldonk M, Rutten G, Oteman M, Siezen RJ, de Vos WM, Simons G. Cloning of usp45, a gene encoding a secreted protein from Lactococcus lactis subsp. lactis MG1363. Gene. 1990;95:155–160
  17. Waterfield NR, Le Page RW, Wilson PW, Wells JM. The isolation of lactococcal promoters and their use in investigating bacterial luciferase synthesis in Lactococcus lactis. Gene. 1995;165:9–15
  18. Tobagus IT, Thomas WR, Holt PG. Adjuvant costimulation during secondary antigen challenge directs qualitative aspects of oral tolerance induction, particularly during the neonatal period. J Immunol. 2004;172:2274–2285
  19. Morelli AE, Zahorchak AF, Larregina AT, Colvin BL, Logar AJ, Takayama T, et al. Cytokine production by mouse myeloid dendritic cells in relation to differentiation and terminal maturation induced by lipopolysaccharide or CD40 ligation. Blood. 2001;98:1512–1523
  20. Hauet-Broere F, Unger WW, Garssen J, Hoijer MA, Kraal G, Samsom JN. Functional CD25− and CD25+ mucosal regulatory T cells are induced in gut-draining lymphoid tissue within 48h after oral antigen application. Eur J Immunol. 2003;33:2801–2810
  21. Unger WW, Hauet-Broere F, Jansen W, van Berkel LA, Kraal G, Samsom JN. Early events in peripheral regulatory T-cell induction via the nasal mucosa. J Immunol. 2003;171:4592–4603
  22. Drouault S, Corthier G, Ehrlich SD, Renault P. Survival, physiology, and lysis of Lactococcus lactis in the digestive tract. Appl Environ Microbiol. 1999;65:4881–4886
  23. Rescigno M, Urbano M, Valzasina B, Francolini M, Rotta G, Bonasio R, et al. Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat Immunol. 2001;2:361–367
  24. Niess JH, Brand S, Gu X, Landsman L, Jung S, McCormick BA, et al. CX3CR1-mediated dendritic cell access to the intestinal lumen and bacterial clearance. Science. 2005;307:254–258
  25. Niess JH, Reinecker HC. Dendritic cells: the commanders-in-chief of mucosal immune defenses. Curr Opin Gastroenterol. 2006;22:354–360
  26. Kapsenberg ML. Dendritic-cell control of pathogen-driven T-cell polarization. Nat Rev Immunol. 2003;3:984–993
  27. Kelsall BL, Leon F. Involvement of intestinal dendritic cells in oral tolerance, immunity to pathogens, and inflammatory bowel disease. Immunol Rev. 2005;206:132–148
  28. Read S, Powrie F. CD4(+) regulatory T cells. Curr Opin Immunol. 2001;13:644–649
  29. Sakaguchi S, Sakaguchi N, Asano M, Itoh M, Toda M. Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor α-chains (CD25) (Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases). J Immunol. 1995;155:1151–1164
  30. Steinman RM, Hawiger D, Nussenzweig MC. Tolerogenic dendritic cells. Annu Rev Immunol. 2003;21:685–711119:952–959
  31. Frossard CP, Steidler L, Eigenmann PA. Oral administration of an IL-10-secreting Lactococcus lactis strain prevents food-induced IgE sensitization. J Allergy Clin Immunol. 2007;
  32. Daniel C, Repa A, Wild C, Pollak A, Pot B, Breiteneder H, et al. Modulation of allergic immune responses by mucosal application of recombinant lactic acid bacteria producing the major birch pollen allergen Bet v 1. Allergy. 2006;61:812–819
  33. del-Patient K, Ah-Leung S, Creminon C, Nouaille S, Chatel JM, Langella P, et al. Oral administration of recombinant Lactococcus lactis expressing bovine β-lactoglobulin partially prevents mice from sensitization. Clin Exp Allergy. 2005;35:539–546
  34. Repa A, Grangette C, Daniel C, Hochreiter R, Hoffmann-Sommergruber K, Thalhamer J, et al. Mucosal co-application of lactic acid bacteria and allergen induces counter-regulatory immune responses in a murine model of birch pollen allergy. Vaccine. 2003;22:87–95
  35. Lider O, Santos LM, Lee CS, Higgins PJ, Weiner HL. Suppression of experimental autoimmune encephalomyelitis by oral administration of myelin basic protein (II. Suppression of disease and in vitro immune responses is mediated by antigen-specific CD8+ T lymphocytes). J Immunol. 1989;142:748–752
  36. Zhang X, Izikson L, Liu L, Weiner HL. Activation of CD25(+)CD4(+) regulatory T cells by oral antigen administration. J Immunol. 2001;167:4245–4253
  37. Chen Y, Kuchroo VK, Inobe J, Hafler DA, Weiner HL. Regulatory T-cell clones induced by oral tolerance: suppression of autoimmune encephalomyelitis. Science. 1994;265:1237–1240
  38. Faria AM, Weiner HL. Oral tolerance and TGF-β-producing cells. Inflamm Allergy Drug Targets. 2006;5:179–190
  39. Miller A, Lider O, Roberts AB, Sporn MB, Weiner HL. Suppressor T cells generated by oral tolerization to myelin basic protein suppress both in vitro and in vivo immune responses by the release of transforming growth factor β after antigen-specific triggering. Proc Natl Acad Sci U S A. 1992;89:421–425
  40. Nakamura K, Kitani A, Strober W. Cell contact-dependent immunosuppression by CD4(+)CD25(+) regulatory T cells is mediated by cell surface-bound transforming growth factor β. J Exp Med. 2001;194:629–644
  41. Nakamura K, Kitani A, Fuss I, Pedersen A, Harada N, Nawata H, et al. TGF-β 1 plays an important role in the mechanism of CD4+CD25+ regulatory T cell activity in both humans and mice. J Immunol. 2004;172:834–842
  42. Chung Y, Lee SH, Kim DH, Kang CY. Complementary role of CD4+CD25+ regulatory T cells and TGF-β in oral tolerance. J Leukoc Biol. 2005;77:906–913
  43. Carrier Y, Yuan J, Kuchroo VK, Weiner HL. Th3 cells in peripheral tolerance (I. Induction of Foxp3-positive regulatory T cells by Th3 cells derived from TGF-β T-cell-transgenic mice). J Immunol. 2007;178:179–185
  44. Ochi H, Abraham M, Ishikawa H, Frenkel D, Yang K, Basso AS, et al. Oral CD3-specific antibody suppresses autoimmune encephalomyelitis by inducing CD4+. Nat Med. 2006;12:627–635
  45. Oida T, Zhang X, Goto M, Hachimura S, Totsuka M, Kaminogawa S, et al. CD4+CD25- T cells that express latency-associated peptide on the surface suppress CD4+CD45RBhigh-induced colitis by a TGF-beta-dependent mechanism. J Immunol. 2003;170:2516–2522
  46. Coombes JL, Robinson NJ, Maloy KJ, Uhlig HH, Powrie F. Regulatory T cells and intestinal homeostasis. Immunol Rev. 2005;204:184–194
  47. Fuss IJ, Boirivant M, Lacy B, Strober W. The interrelated roles of TGF-β and IL-10 in the regulation of experimental colitis. J Immunol. 2002;168:900–908
  48. Kitani A, Fuss I, Nakamura K, Kumaki F, Usui T, Strober W. Transforming growth factor (TGF)-β1-producing regulatory T cells induce Smad-mediated interleukin 10 secretion that facilitates coordinated immunoregulatory activity and amelioration of TGF-β1-mediated fibrosis. J Exp Med. 2003;198:1179–1188
  49. Carrier Y, Yuan J, Kuchroo VK, Weiner HL. Th3 cells in peripheral tolerance (II. TGF-β-transgenic Th3 cells rescue IL-2-deficient mice from autoimmunity). J Immunol. 2007;178:172–178
  50. Chen W, Jin W, Hardegen N, Lei KJ, Li L, Marinos N, et al. Conversion of peripheral CD4+. J Exp Med. 2003;198:1875–1886
  51. Tang Q, Henriksen KJ, Bi M, Finger EB, Szot G, Ye J, et al. In vitro-expanded antigen-specific regulatory T cells suppress autoimmune diabetes. J Exp Med. 2004;199:1455–1465
  52. Tang Q, Bluestone JA. Regulatory T-cell physiology and application to treat autoimmunity. Immunol Rev. 2006;212:217–237

 Supported by the Research Fund of Ghent University (GOA, 01G01205).

 No conflict of interest to disclose.

PII: S0016-5085(07)00931-6

doi: 10.1053/j.gastro.2007.04.073

Gastroenterology
Volume 133, Issue 2 , Pages 517-528 , August 2007

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