Gastroenterology
Volume 131, Issue 1 , Pages 47-58 , July 2006

Transcytosis of IgE–Antigen Complexes by CD23a in Human Intestinal Epithelial Cells and Its Role in Food Allergy

  • Hongxing Li

      Affiliations

    • Department of Medicine/Division of Clinical Immunology, Mount Sinai School of Medicine, New York, New York, USA
    • Immunobiology Center, Mount Sinai School of Medicine, New York, New York, USA
    • ,
  • Anna Nowak–Wegrzyn

      Affiliations

    • Department of Pediatrics, Mount Sinai School of Medicine, New York, New York
    • ,
  • Zachary Charlop–Powers

      Affiliations

    • Department of Pediatrics, Mount Sinai School of Medicine, New York, New York
    • ,
  • Wayne Shreffler

      Affiliations

    • Department of Pediatrics, Mount Sinai School of Medicine, New York, New York
    • ,
  • Mirna Chehade

      Affiliations

    • Department of Pediatrics, Mount Sinai School of Medicine, New York, New York
    • ,
  • Sunil Thomas

      Affiliations

    • Department of Medicine/Division of Clinical Immunology, Mount Sinai School of Medicine, New York, New York, USA
    • ,
  • Giulia Roda

      Affiliations

    • Department of Medicine/Division of Clinical Immunology, Mount Sinai School of Medicine, New York, New York, USA
    • ,
  • Stephanie Dahan

      Affiliations

    • Department of Medicine/Division of Clinical Immunology, Mount Sinai School of Medicine, New York, New York, USA
    • ,
  • Kirk Sperber

      Affiliations

    • Department of Medicine/Division of Clinical Immunology, Mount Sinai School of Medicine, New York, New York, USA
    • Immunobiology Center, Mount Sinai School of Medicine, New York, New York, USA
    • ,
  • M. Cecilia Berin

      Affiliations

    • Department of Pediatrics, Mount Sinai School of Medicine, New York, New York
    • Corresponding Author InformationAddress requests for reprints to: M. Cecilia Berin, PhD, Pediatric Allergy and Immunology, Box 1198, Mount Sinai School of Medicine, One Gustave L. Levy Place, New York, New York 10029.

Received 19 September 2005 ,Accepted 23 March 2006.

References 

  1. Belut D , Moneret-Vautrin DA , Nicolas JP , Grilliat JP . IgE levels in intestinal juice . Dig Dis Sci . 1980;25:323–332
  2. Negrao-Correa D , Adams LS , Bell RG . Intestinal transport and catabolism of IgE (a major blood-independent pathway of IgE dissemination during a Trichinella spiralis infection of rats) . J Immunol . 1996;157:4037–4044
  3. Ramaswamy K , Hakimi J , Bell RG . Evidence for an interleukin 4-inducible immunoglobulin E uptake and transport mechanism in the intestine . J Exp Med . 1994;180:1793–1803
  4. Yang PC , Berin MC , Yu LC , Conrad DH , Perdue MH . Enhanced intestinal transepithelial antigen transport in allergic rats is mediated by IgE and CD23 (FcepsilonRII) . J Clin Invest . 2000;106:879–886
  5. Yu LC, Yang PC, Berin MC, Di Leo V, Conrad DH, McKay DM, et al. Enhanced transepithelial antigen transport in intestine of allergic mice is mediated by IgE/CD23 and regulated by interleukin-4 . Gastroenterology . 2001;121:370–381
  6. Beavil AJ , Edmeades RL , Gould HJ , Sutton BJ . Alpha-helical coiled-coil stalks in the low-affinity receptor for IgE (Fc epsilon RII/CD23) and related C-type lectins . Proc Natl Acad Sci U S A . 1992;89:753–757
  7. Dierks SE , Bartlett WC , Edmeades RL , Gould HJ , Rao M , Conrad DH . The oligomeric nature of the murine Fc epsilon RII/CD23. Implications for function . J Immunol . 1993;150:2372–2382
  8. Gould H , Sutton B , Edmeades R , Beavil A . CD23/Fc epsilon RII (C-type lectin membrane protein with a split personality?) . Monogr Allergy . 1991;29:28–49
  9. Yokota A, Kikutani H, Tanaka T, Sato R, Barsumian EL, Suemura M, et al. Two species of human Fc epsilon receptor II (Fc epsilon RII/CD23) (tissue-specific and IL-4-specific regulation of gene expression) . Cell . 1988;55:611–618
  10. Kikutani H, Inui S, Sato R, Barsumian EL, Owaki H, Yamasaki K, et al  Molecular structure of human lymphocyte receptor for immunoglobulin E . Cell . 1986;47:657–665
  11. Yokota A, Yukawa K, Yamamoto A, Sugiyama K, Suemura M, Tashiro Y, et al. Two forms of the low-affinity Fc receptor for IgE differentially mediate endocytosis and phagocytosis (identification of the critical cytoplasmic domains) . Proc Natl Acad Sci U S A . 1992;89:5030–5034
  12. Yu LC , Montagnac G , Yang PC , Conrad DH , Benmerah A , Perdue MH . Intestinal epithelial CD23 mediates enhanced antigen transport in allergy (evidence for novel splice forms) . Am J Physiol . 2003;285:G223–G234
  13. Montagnac G, Yu LC, Bevilacqua C, Heyman M, Conrad DH, Perdue MH, et al. Differential role for CD23 splice forms in apical to basolateral transcytosis of IgE/allergen complexes . Traffic . 2005;6:230–242
  14. Payet M , Conrad DH . IgE regulation in CD23 knockout and transgenic mice . Allergy . 1999;54:1125–1129
  15. Payet ME , Woodward EC , Conrad DH . Humoral response suppression observed with CD23 transgenics . J Immunol . 1999;163:217–223
  16. Texido G , Eibel H , Le Gros G , van der Putten H . Transgene CD23 expression on lymphoid cells modulates IgE and IgG1 responses . J Immunol . 1994;153:3028–3042
  17. Yu P , Kosco-Vilbois M , Richards M , Kohler G , Lamers MC . Negative feedback regulation of IgE synthesis by murine CD23 . Nature . 1994;369:753–756
  18. Flores-Romo L, Shields J, Humbert Y, Graber P, Aubry JP, Gauchat JF, et al  Inhibition of an in vivo antigen-specific IgE response by antibodies to CD23 . Science . 1993;261:1038–1041
  19. Getahun A , Hjelm F , Heyman B . IgE enhances antibody and T cell responses in vivo via CD23+ B cells . J Immunol . 2005;175:1473–1482
  20. Kaiserlian D , Lachaux A , Grosjean I , Graber P , Bonnefoy JY . Intestinal epithelial cells express the CD23/Fc epsilon RII molecule (enhanced expression in enteropathies) . Immunology . 1993;80:90–95
  21. Mayer L , Shlien R . Evidence for function of Ia molecules on gut epithelial cells in man . J Exp Med . 1987;166:1471–1483
  22. Sicherer SH . Food allergy (when and how to perform oral food challenges) . Pediatr Allergy Immunol . 1999;10:226–234
  23. Sampson HA . Update on food allergy . J Allergy Clin Immunol . 2004;113:805–820
  24. Beyer K , Castro R , Birnbaum A , Benkov K , Pittman N , Sampson HA . Human milk-specific mucosal lymphocytes of the gastrointestinal tract display a TH2 cytokine profile . J Allergy Clin Immunol . 2002;109:707–713
  25. Punnonen J , Aversa G , Cocks BG , de Vries JE . Role of interleukin-4 and interleukin-13 in synthesis of IgE and expression of CD23 by human B cells . Allergy . 1994;49:576–586
  26. Brown WR , Borthistle BK , Chen ST . Immunoglobulin E (IgE) and IgE-containing cells in human gastrointestinal fluids and tissues . Clin Exp Immunol . 1975;20:227–237
  27. Montagnac G, Molla-Herman A, Bouchet J, Yu LC, Conrad DH, Perdue MH, et al. Intracellular trafficking of CD23 (differential regulation in humans and mice by both extracellular and intracellular exons) . J Immunol . 2005;174:5562–5572
  28. Tu Y, Salim S, Bourgeois J, Di Leo V, Irvine EJ, Marshall JK, et al. CD23-mediated IgE transport across human intestinal epithelium (inhibition by blocking sites of translation or binding) . Gastroenterology . 2005;129:928–940
  29. Tinnell SB , Jacobs-Helber SM , Sterneck E , Sawyer ST , Conrad DH . STAT6, NF-κB and C/EBP in CD23 expression and IgE production . Int Immunol . 1998;10:1529–1538
  30. Heyman M, Darmon N, Dupont C, Dugas B, Hirribaren A, Blaton MA, et al. Mononuclear cells from infants allergic to cow’s milk secrete tumor necrosis factor alpha, altering intestinal function . Gastroenterology . 1994;106:1514–1523
  31. Rojas R , Apodaca G . Immunoglobulin transport across polarized epithelial cells . Nat Rev Mol Cell Biol . 2002;3:944–955

 Supported by National Institutes of Health grants AI-44236 and AI-45343 (K.S.) and DK-071576 (M.C.B.).

PII: S0016-5085(06)00711-6

doi: 10.1053/j.gastro.2006.03.044

Gastroenterology
Volume 131, Issue 1 , Pages 47-58 , July 2006

Article Tools

* Image Usage & Resolution