Gastroenterology
Volume 135, Issue 3 , Pages 917-925 , September 2008

Ovalbumin-Protein σ1 M-Cell Targeting Facilitates Oral Tolerance With Reduction of Antigen-Specific CD4+ T Cells

  • Hideaki Suzuki

      Affiliations

    • The Immunobiology Vaccine Center, Departments of Pediatric Dentistry and Microbiology, The University of Alabama at Birmingham, Birmingham, Alabama
    • ,
  • Shinichi Sekine

      Affiliations

    • The Immunobiology Vaccine Center, Departments of Pediatric Dentistry and Microbiology, The University of Alabama at Birmingham, Birmingham, Alabama
    • ,
  • Kosuke Kataoka

      Affiliations

    • The Immunobiology Vaccine Center, Departments of Pediatric Dentistry and Microbiology, The University of Alabama at Birmingham, Birmingham, Alabama
    • Department of Preventive Dentistry, Institute of Health Biosciences, The University of Tokushima, Tokushima-City, Tokushima, Japan
    • ,
  • David W. Pascual

      Affiliations

    • Veterinary Molecular Biology, Montana State University, Bozeman, Montana
    • ,
  • Massimo Maddaloni

      Affiliations

    • Veterinary Molecular Biology, Montana State University, Bozeman, Montana
    • ,
  • Ryoki Kobayashi

      Affiliations

    • The Immunobiology Vaccine Center, Departments of Pediatric Dentistry and Microbiology, The University of Alabama at Birmingham, Birmingham, Alabama
    • ,
  • Keiko Fujihashi

      Affiliations

    • The Immunobiology Vaccine Center, Departments of Pediatric Dentistry and Microbiology, The University of Alabama at Birmingham, Birmingham, Alabama
    • ,
  • Haruo Kozono

      Affiliations

    • Research Institute for Biological Sciences, Tokyo University of Science, Noda, Chiba, Japan
    • ,
  • Jerry R. McGhee

      Affiliations

    • The Immunobiology Vaccine Center, Departments of Pediatric Dentistry and Microbiology, The University of Alabama at Birmingham, Birmingham, Alabama
    • ,
  • Kohtaro Fujihashi

      Affiliations

    • The Immunobiology Vaccine Center, Departments of Pediatric Dentistry and Microbiology, The University of Alabama at Birmingham, Birmingham, Alabama
    • Corresponding Author InformationAddress requests for reprints to: Kohtaro Fujihashi, The Department of Pediatric Dentistry, The Immunobiology Vaccine Center, The University of Alabama at Birmingham, 801A1 School of Dentistry Building, 1919 7th Avenue South, Birmingham, AL 35294-0007. fax: (205) 975-4431

Received 7 September 2007 ,Accepted 8 May 2008.

References 

  1. Challacombe SJ, Tomasi TB. Systemic tolerance and secretory immunity after oral immunization. J Exp Med. 1980;152:1459–1472
  2. Mestecky J, Blumberg RS, Kiyono H, McGhee JR. The mucosal immune system. In:  Paul WE editors. Fundamental immunology. Philadelphia, PA: Lippincott Williams & Wilkins; 2003;p. 965–1020
  3. Tomasi TB. Oral tolerance. Transplantation. 1980;29:353–356
  4. Kato H, Fujihashi K, Kato R, Yuki Y, McGhee JR. Oral tolerance revisited: prior oral tolerization abrogates cholera toxin-induced mucosal IgA responses. J Immunol. 2001;166:3114–3121
  5. Garside P, Mowat AM, Khoruts A. Oral tolerance in disease. Gut. 1999;44:137–142
  6. Strobel S, Mowat AM. Immune responses to dietary antigens: oral tolerance. Immunol Today. 1998;19:173–181
  7. Strober W, Kelsall B, Marth T. Oral tolerance. J Clin Immunol. 1998;18:1–30
  8. Wardrop RM, Whitacre CC. Oral tolerance in the treatment of inflammatory autoimmune diseases. Inflamm Res. 1999;48:106–119
  9. Mowat AM. Anatomical basis of tolerance and immunity to intestinal antigens. Nat Rev Immunol. 2003;3:331–341
  10. Nagler-Anderson C, Shi HN. Peripheral nonresponsiveness to orally administered soluble protein antigens. Crit Rev Immunol. 2001;21:121–131
  11. Viney JL, Mowat AM, O'Malley JM, Williamson E, Fanger NA. Expanding dendritic cells in vivo enhances the induction of oral tolerance. J Immunol. 1998;160:5815–5825
  12. Weiner HL. Induction and mechanism of action of transforming growth factor-beta-secreting Th3 regulatory cells. Immunol Rev. 2001;182:207–214
  13. 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
  14. Melamed D, Friedman A. Direct evidence for anergy in T lymphocytes tolerized by oral administration of ovalbumin. Eur J Immunol. 1993;23:935–942
  15. Whitacre CC, Gienapp IE, Orosz CG, Bitar DM. Oral tolerance in experimental autoimmune encephalomyelitis (III. Evidence for clonal anergy). J Immunol. 1991;147:2155–2163
  16. Chen Y, Inobe J, Marks R, Gonnella P, Kuchroo VK, Weiner HL. Peripheral deletion of antigen-reactive T cells in oral tolerance. Nature. 1995;376:177–180
  17. 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
  18. Groux H, O'Garra A, Bigler M, et al. A CD4+ T-cell subset inhibits antigen-specific T-cell responses and prevents colitis. Nature. 1997;389:737–742
  19. Nagler-Anderson C, Bhan AK, Podolsky DK, Terhorst C. Control freaks immune regulatory cells. Nat Immunol. 2004;5:119–122
  20. Cottrez F, Groux H. Specialization in tolerance: innate CD4+ CD25+ versus acquired Tr1 and Th3 regulatory T cells. Transplantation. 2004;77(1 suppl):S12–S15
  21. Dieckmann D, Bruett CH, Ploettner H, Lutz MB, Schuler G. Human CD4+ CD25+ regulatory, contact-dependent T cells induce interleukin 10-producing, contact-independent type 1-like regulatory T cells [corrected]. J Exp Med. 2002;196:247–253
  22. Wu Y, Boysun MJ, Csencsits KL, Pascual DW. Gene transfer facilitated by a cellular targeting molecule, reovirus protein sigma1. Gene Ther. 2000;7:61–69
  23. Wu Y, Wang X, Csencsits KL, Haddad A, Walters N, Pascual DW. M cell-targeted DNA vaccination. Proc Natl Acad Sci U S A. 2001;98:9318–9323
  24. Rubas W, Banerjea AC, Gallati H, Speiser PP, Joklik WK. Incorporation of the reovirus M cell attachment protein into small unilamellar vesicles: incorporation efficiency and binding capability to L929 cells in vitro. J Microencapsul. 1990;7:385–395
  25. Rynda A, Maddaloni M, Mierzejewska D, et al. Low-dose tolerance is mediated by the microfold cell ligand, reovirus protein sigma1. J Immunol. 2008;180:5187–5200
  26. Fujihashi K, Dohi T, Rennert PD, et al. Peyer's patches are required for oral tolerance to proteins. Proc Natl Acad Sci U S A. 2001;98:3310–3315
  27. Kataoka K, McGhee JR, Kobayashi R, Fujihashi K, Shizukuishi S, Fujihashi K. Nasal Flt3 ligand cDNA elicits CD11c+ CD8+ dendritic cells for enhanced mucosal immunity. J Immunol. 2004;172:3612–3619
  28. Fujihashi K, McGhee JR, Kweon MN, et al. γ/δ T cell-deficient mice have impaired mucosal immunoglobulin A responses. J Exp Med. 1996;183:1929–1935
  29. Kato H, Fujihashi K, Kato R, et al. Lack of oral tolerance in aging is due to sequential loss of Peyer's patch cell interactions. Int Immunol. 2003;15:145–158
  30. Fujihashi K, Kato H, van Ginkel FW, et al. A revisit of mucosal IgA immunity and oral tolerance. Acta Odontol Scand. 2001;59:301–308
  31. Hagiwara Y, McGhee JR, Fujihashi K, et al. Protective mucosal immunity in aging is associated with functional CD4+ T cells in nasopharyngeal-associated lymphoreticular tissue. J Immunol. 2003;170:1754–1762
  32. Ermak TH, Dougherty EP, Bhagat HR, Kabok Z, Pappo J. Uptake and transport of copolymer biodegradable microspheres by rabbit Peyer's patch M cells. Cell Tissue Res. 1995;279:433–436
  33. Neutra MR, Frey A, Kraehenbuhl JP. Epithelial M cells: gateways for mucosal infection and immunization. Cell. 1996;86:345–348
  34. Gebert A, Rothkotter HJ, Pabst R. M cells in Peyer's patches of the intestine. Int Rev Cytol. 1996;167:91–159
  35. Wolf JL, Bye WA. The membranous epithelial (M) cell and the mucosal immune system. Annu Rev Med. 1984;35:95–112
  36. Allan CH, Mendrick DL, Trier JS. Rat intestinal M cells contain acidic endosomal-lysosomal compartments and express class II major histocompatibility complex determinants. Gastroenterology. 1993;104:698–708
  37. Jones BD, Ghori N, Falkow S. Salmonella typhimurium initiates murine infection by penetrating and destroying the specialized epithelial M cells of the Peyer's patches. J Exp Med. 1994;180:15–23
  38. Krug A, French AR, Barchet W, et al. TLR9-dependent recognition of MCMV by IPC and DC generates coordinated cytokine responses that activate antiviral NK cell function. Immunity. 2004;21:107–119
  39. Gutgemann I, Fahrer AM, Altman JD, Davis MM, Chien YH. Induction of rapid T cell activation and tolerance by systemic presentation of an orally administered antigen. Immunity. 1998;8:667–673
  40. Sun JB, Raghavan S, Sjoling A, Lundin S, Holmgren J. Oral tolerance induction with antigen conjugated to cholera toxin B subunit generates both Foxp3+CD25+ and Foxp3−CD25− CD4+ regulatory T cells. J Immunol. 2006;177:7634–7644
  41. Tsuji NM, Mizumachi K, Kurisaki J. Antigen-specific, CD4+ CD25+ regulatory T cell clones induced in Peyer's patches. Int Immunol. 2003;15:525–534

 Supported by grants from the US Public Health Service (AI 18958, DE 12242, AG 025873, and DE 13812).

 All authors declare that they have no conflict of interest to disclose.

PII: S0016-5085(08)00857-3

doi: 10.1053/j.gastro.2008.05.037

Gastroenterology
Volume 135, Issue 3 , Pages 917-925 , September 2008

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