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Immunoglobulin E: Pathogenic Relevance in Immediate Contact Reactions

  • Maria Estela Martinez-Escala
  • Leah Ariella Kaplan
  • Ana M. Giménez-Arnau
Chapter
Part of the Updates in Clinical Dermatology book series (UCD)

Abstract

Contact urticaria syndrome, contact urticaria, and protein contact dermatitis are a heterogeneous group of immediate skin reactions clinically characterized by the presence of wheals, or eczema, or both, commonly limited to the exposed skin. Two pathogenic pathways have been described, which include a nonimmune-mediated mechanism and an immune-mediated mechanism. In the nonimmune-mediated mechanism, the agent directly causes skin reaction through vasogenic mediators, and therefore prior sensitization is not required to develop a skin reaction. Conversely, the immune-mediated mechanism consists of an IgE-mediated type I hypersensitivity reaction. This type of hypersensitivity requires an initial exposure to the antigen to induce a sensitization, causing the production of antigen-specific IgE that will induce mast cell degranulation after future exposures with the same antigen. Additionally, studies in vitro, as well as in vivo, have demonstrated supplementary roles of IgE beyond the immediate immune response subjected to the presence of a specific antigen. These antigen-independent roles of IgE have been shown to provide and prepare the perfect environment to induce the allergic response from the sensitization phase to amplification and perpetuation of this immune response. Herein, the roles of IgE in the immediate contact response, as well as those favoring its development, are reviewed.

Keywords

Allergy CD23, contact immune reaction Contact urticaria FcεRI Immunoglobulin E Protein contact disease Pathogenesis Type I hypersensitivity Sensitization 

References

  1. 1.
    Gimenez-Arnau A, Maurer M, De La Cuadra J, Maibach H. Immediate contact skin reactions, an update of contact urticaria, contact urticaria syndrome and protein contact dermatitis– “A Never Ending Story”. Eur J Dermatol. 2010;20(5):552–62. PubMed PMID: 20732848.PubMedGoogle Scholar
  2. 2.
    Levin C, Warshaw E. Protein contact dermatitis: allergens, pathogenesis, and management. Dermatitis. 2008;19(5):241–51. PubMed PMID: 18845114.PubMedGoogle Scholar
  3. 3.
    Janssens V, Morren M, Dooms-Goossens A, Degreef H. Protein contact dermatitis: myth or reality? Br J Dermatol. 1995;132(1):1–6. PubMed PMID: 7756118.CrossRefPubMedGoogle Scholar
  4. 4.
    Amaro C, Goossens A. Immunological occupational contact urticaria and contact dermatitis from proteins: a review. Contact Dermatitis. 2008;58(2):67–75. PubMed PMID: 18186738.CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Hjorth N, Roed-Petersen J. Occupational protein contact dermatitis in food handlers. Contact Dermatitis. 1976;2(1):28–42. PubMed PMID: 145923.CrossRefPubMedGoogle Scholar
  6. 6.
    Jones HE, Reinhardt JH, Rinaldi MG. Immunologic susceptibility to chronic dermatophytosis. Arch Dermatol. 1974;110(2):213–20. PubMed PMID: 4852361.CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Conde-Salazar L, Gonzalez MA, Guimaraens D. Type I and Type IV sensitization to Anisakis simplex in 2 patients with hand eczema. Contact Dermatitis. 2002;46(6):361. PubMed PMID: 12190630.CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Jappe U, Bonnekoh B, Hausen BM, Gollnick H. Garlic-related dermatoses: case report and review of the literature. Am J Contact Dermat. 1999;10(1):37–9. PubMed PMID: 10072338.CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Jeannet-Peter N, Piletta-Zanin PA, Hauser C. Facial dermatitis, contact urticaria, rhinoconjunctivitis, and asthma induced by potato. Am J Contact Dermat. 1999;10(1):40–2. PubMed PMID: 10072339.CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Kanerva L, Estlander T. Immediate and delayed skin allergy from cow dander. Am J Contact Dermat. 1997;8(3):167–9. PubMed PMID: 9249287.PubMedGoogle Scholar
  11. 11.
    Scharer L, Hafner J, Wuthrich B, Bucher C. Occupational protein contact dermatitis from shrimps. a new presentation of the crustacean-mite syndrome. Contact Dermatitis. 2002;46(3):181–2. PubMed PMID: 12000333.CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Saloga J, Knop J. Does sensitization through the skin occur? Allergy. 2000;55(10):905–9. PubMed PMID: 11030369.CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Hamilton RG. Science behind the discovery of IgE. J Allergy Clin Immunol. 2005;115(3):648–52. PubMed PMID: 15753924.CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Stanworth DR. The discovery of IgE. Allergy. 1993;48(2):67–71. PubMed PMID: 8457034.CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Taylor AI, Fabiane SM, Sutton BJ, Calvert RA. The crystal structure of an avian IgY-fc fragment reveals conservation with both mammalian IgG and IgE. Biochemistry. 2009;48(3):558–62. PubMed PMID: 19115948.CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    McDonnell JM, Calvert R, Beavil RL, Beavil AJ, Henry AJ, Sutton BJ, et al. The structure of the IgE Cepsilon2 domain and its role in stabilizing the complex with its high-affinity receptor FcepsilonRIalpha. Nat Struct Biol. 2001;8(5):437–41. PubMed PMID: 11323720.CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Gergen PJ, Arbes SJ Jr, Calatroni A, Mitchell HE, Zeldin DC. Total IgE levels and asthma prevalence in the US population: results from the National Health and Nutrition Examination Survey 2005-2006. J Allergy Clin Immunol. 2009;124(3):447–53. PubMed Pubmed Central PMCID: 2758573.CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Gould HJ, Sutton BJ. IgE in allergy and asthma today. Nat Rev Immunol. 2008;8(3):205–17. PubMed PMID: 18301424.CrossRefPubMedGoogle Scholar
  19. 19.
    MacGlashan DW Jr, Bochner BS, Adelman DC, Jardieu PM, Togias A, Lichtenstein LM. Serum IgE level drives basophil and mast cell IgE receptor display. Int Arch Allergy Immunol. 1997;113(1–3):45–7. PubMed PMID: 9130480.CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Saavedra MC, Sur S. Down regulation of the high-affinity IgE receptor associated with successful treatment of chronic idiopathic urticaria with omalizumab. Clin Mol Allergy. 2011;9(1):2. PubMed PMID: 21247438. Pubmed Central PMCID: 3031269.CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Saini SS, MacGlashan DW Jr, Sterbinsky SA, Togias A, Adelman DC, Lichtenstein LM, et al. Down-regulation of human basophil IgE and FC epsilon RI alpha surface densities and mediator release by anti-IgE-infusions is reversible in vitro and in vivo. J Immunol. 1999;162(9):5624–30. PubMed PMID: 10228046.PubMedGoogle Scholar
  22. 22.
    Malveaux FJ, Conroy MC, Adkinson NF Jr, Lichtenstein LM. IgE receptors on human basophils. relationship to serum IgE concentration. J Clin Invest. 1978;62(1):176–81. PubMed PMID: 659631. Pubmed Central PMCID: 371751.CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Jardieu P. Anti-IgE therapy. Curr Opin Immunol. 1995;7(6):779–82. PubMed PMID: 8679119.CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Lantz CS, Yamaguchi M, Oettgen HC, Katona IM, Miyajima I, Kinet JP, et al. IgE regulates mouse basophil Fc epsilon RI expression in vivo. J Immunol. 1997;158(6):2517–21. PubMed PMID: 9058781.PubMedGoogle Scholar
  25. 25.
    Burton OT, Oettgen HC. Beyond immediate hypersensitivity: evolving roles for IgE antibodies in immune homeostasis and allergic diseases. Immunol Rev. 2011;242(1):128–43. PubMed Pubmed Central PMCID: 3122143.CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Conrad DH, Ford JW, Sturgill JL, Gibb DR. CD23: an overlooked regulator of allergic disease. Curr Allergy Asthma Rep. 2007;7(5):331–7. PubMed PMID: 17697638.CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Shiung YY, Chiang CY, Chen JB, Wu PC, Hung AF, Lu DC, et al. An anti-IgE monoclonal antibody that binds to IgE on CD23 but not on high-affinity IgE.Fc receptors. Immunobiology. 2012;217(7):676–83. PubMed PMID: 22226669.CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Bonnefoy JY, Gauchat JF, Lecoanet-Henchoz S, Graber P, Aubry JP. Regulation of human IgE synthesis. Ann N Y Acad Sci. 1996;796:59–71. PubMed PMID: 8906212.CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Getahun A, Hjelm F, Heyman B. IgE enhances antibody and T cell responses in vivo via CD23+ B cells. J Immunol. 2005;175(3):1473–82. PubMed PMID: 16034084.CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Hjelm F, Karlsson MC, Heyman B. A novel B cell-mediated transport of IgE-immune complexes to the follicle of the spleen. J Immunol. 2008;180(10):6604–10. PubMed PMID: 18453579.CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Lemieux GA, Blumenkron F, Yeung N, Zhou P, Williams J, Grammer AC, et al. The low affinity IgE receptor (CD23) is cleaved by the metalloproteinase ADAM10. J Biol Chem. 2007;282(20):14836–44. PubMed PMID: 17389606. Pubmed Central PMCID: 2582392.CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Marolewski AE, Buckle DR, Christie G, Earnshaw DL, Flamberg PL, Marshall LA, et al. CD23 (FcepsilonRII) release from cell membranes is mediated by a membrane-bound metalloprotease. Biochem J. 1998;333(Pt 3):573–9. PubMed Pubmed Central PMCID: 1219619.CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Weskamp G, Ford JW, Sturgill J, Martin S, Docherty AJ, Swendeman S, et al. ADAM10 is a principal ‘sheddase’ of the low-affinity immunoglobulin E receptor CD23. Nat Immunol. 2006;7(12):1293–8. PubMed PMID: 17072319.CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Liu YJ, Zhang J, Lane PJ, Chan EY, MacLennan IC. Sites of specific B cell activation in primary and secondary responses to T cell-dependent and T cell-independent antigens. Eur J Immunol. 1991;21(12):2951–62. PubMed PMID: 1748148.CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Frigeri LG, Liu FT. Surface expression of functional IgE binding protein, an endogenous lectin, on mast cells and macrophages. J Immunol. 1992;148(3):861–7. PubMed PMID: 1730878.PubMedGoogle Scholar
  36. 36.
    Frigeri LG, Zuberi RI, Liu FT. Epsilon BP, a beta-galactoside-binding animal lectin, recognizes IgE receptor (Fc epsilon RI) and activates mast cells. Biochemistry. 1993;32(30):7644–9. PubMed PMID: 8347574.CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Hirano M, Davis RS, Fine WD, Nakamura S, Shimizu K, Yagi H, et al. IgEb immune complexes activate macrophages through FcgammaRIV binding. Nat Immunol. 2007;8(7):762–71. PubMed PMID: 17558411.CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Mancardi DA, Iannascoli B, Hoos S, England P, Daeron M, Bruhns P. FcgammaRIV is a mouse IgE receptor that resembles macrophage FcepsilonRI in humans and promotes IgE-induced lung inflammation. J Clin Invest. 2008;118(11):3738–50. PubMed PMID: 18949059. Pubmed Central PMCID: 2571035.CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Rajan TV. The Gell-Coombs classification of hypersensitivity reactions: a re-interpretation. Trends Immunol. 2003;24(7):376–9. PubMed PMID: 12860528.CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Tedeschi A, Lorini M, Asero R. Anti-thyroid peroxidase IgE in patients with chronic urticaria. J Allergy Clin Immunol. 2001;108(3):467–8. PubMed PMID: 11544471.CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Murphy K, Travers P, Walport M, Janeway C. Janeway’s immunobiology, vol. xix. 8th ed. New York: Garland Science; 2012. p. 868.Google Scholar
  42. 42.
    van Ree R, Hummelshoj L, Plantinga M, Poulsen LK, Swindle E. Allergic sensitization: host-immune factors. Clin Transl Allergy. 2014;4(1):12. PubMed PMID: 24735802. Pubmed Central PMCID: 3989850.CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Ovary Z. Passive cutaneous anaphylaxis. Methods Med Res. 1964;10:158–62. PubMed PMID: 14284910.PubMedGoogle Scholar
  44. 44.
    Feuser K, Feilhauer K, Staib L, Bischoff SC, Lorentz A. Akt cross-links IL-4 priming, stem cell factor signaling, and IgE-dependent activation in mature human mast cells. Mol Immunol. 2011;48(4):546–52. PubMed PMID: 21106245.CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Lorentz A, Schwengberg S, Sellge G, Manns MP, Bischoff SC. Human intestinal mast cells are capable of producing different cytokine profiles: role of IgE receptor cross-linking and IL-4. J Immunol. 2000;164(1):43–8. PubMed PMID: 10604991.CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Miescher SM, Vogel M. Molecular aspects of allergy. Mol Asp Med. 2002;23(6):413–62. PubMed PMID: 12385747.CrossRefGoogle Scholar
  47. 47.
    Pawankar R, Okuda M, Yssel H, Okumura K, Ra C. Nasal mast cells in perennial allergic rhinitics exhibit increased expression of the Fc epsilonRI, CD40L, IL-4, and IL-13, and can induce IgE synthesis in B cells. J Clin Invest. 1997;99(7):1492–9. PubMed Pubmed Central PMCID: 507968.CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Shelburne CP, Ryan JJ. The role of Th2 cytokines in mast cell homeostasis. Immunol Rev. 2001;179:82–93. PubMed PMID: 11292031.CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Yamaguchi M, Sayama K, Yano K, Lantz CS, Noben-Trauth N, Ra C, et al. IgE enhances Fc epsilon receptor I expression and IgE-dependent release of histamine and lipid mediators from human umbilical cord blood-derived mast cells: synergistic effect of IL-4 and IgE on human mast cell Fc epsilon receptor I expression and mediator release. J Immunol. 1999;162(9):5455–65. PubMed PMID: 10228025.PubMedGoogle Scholar
  50. 50.
    Sutton JK, Brunso-Bechtold JK. Dendritic development in the dorsal lateral geniculate nucleus of ferrets in the postnatal absence of retinal input: a Golgi study. J Neurobiol. 1993;24(3):317–34. PubMed PMID: 8492109.CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Novak N, Bieber T, Kraft S. Immunoglobulin E-bearing antigen-presenting cells in atopic dermatitis. Curr Allergy Asthma Rep. 2004;4(4):263–9. PubMed PMID: 15175139.CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Bieber T. Fc epsilon RI-expressing antigen-presenting cells: new players in the atopic game. Immunol Today. 1997;18(7):311–3. PubMed PMID: 9238831.CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Stingl G, Maurer D. IgE-mediated allergen presentation via Fc epsilon RI on antigen-presenting cells. Int Arch Allergy Immunol. 1997;113(1–3):24–9. PubMed PMID: 9130475.CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Karagiannis SN, Warrack JK, Jennings KH, Murdock PR, Christie G, Moulder K, et al. Endocytosis and recycling of the complex between CD23 and HLA-DR in human B cells. Immunology. 2001;103(3):319–31. PubMed PMID: 11454061. Pubmed Central PMCID: 1783243.CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Carlsson F, Hjelm F, Conrad DH, Heyman B. IgE enhances specific antibody and T-cell responses in mice overexpressing CD23. Scand J Immunol. 2007;66(2–3):261–70. PubMed PMID: 17635803.CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Bryce PJ, Miller ML, Miyajima I, Tsai M, Galli SJ, Oettgen HC. Immune sensitization in the skin is enhanced by antigen-independent effects of IgE. Immunity. 2004;20(4):381–92. PubMed PMID: 15084268.CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Kawakami T, Galli SJ. Regulation of mast-cell and basophil function and survival by IgE. Nat Rev Immunol. 2002;2(10):773–86. PubMed PMID: 12360215.CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Oettgen HC, Martin TR, Wynshaw-Boris A, Deng C, Drazen JM, Leder P. Active anaphylaxis in IgE-deficient mice. Nature. 1994;370(6488):367–70. PubMed PMID: 8047141.CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Asai K, Kitaura J, Kawakami Y, Yamagata N, Tsai M, Carbone DP, et al. Regulation of mast cell survival by IgE. Immunity. 2001;14(6):791–800. PubMed PMID: 11420048.CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Kalesnikoff J, Huber M, Lam V, Damen JE, Zhang J, Siraganian RP, et al. Monomeric IgE stimulates signaling pathways in mast cells that lead to cytokine production and cell survival. Immunity. 2001;14(6):801–11. PubMed PMID: 11420049.CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Bryce PJ, Oettgen HC. Antigen-independent effects of immunoglobulin E. Curr Allergy Asthma Rep. 2005;5(3):186–90. PubMed PMID: 15842955.CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    Kitaura J, Song J, Tsai M, Asai K, Maeda-Yamamoto M, Mocsai A, et al. Evidence that IgE molecules mediate a spectrum of effects on mast cell survival and activation via aggregation of the FcepsilonRI. Proc Natl Acad Sci U S A. 2003;100(22):12911–6. PubMed PMID: 14569021. Pubmed Central PMCID: 240718.CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Kashiwakura J, Xiao W, Kitaura J, Kawakami Y, Maeda-Yamamoto M, Pfeiffer JR, et al. Pivotal advance: IgE accelerates in vitro development of mast cells and modifies their phenotype. J Leukoc Biol. 2008;84(2):357–67. PubMed Pubmed Central PMCID: 2516357.CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    Kitaura J, Kinoshita T, Matsumoto M, Chung S, Kawakami Y, Leitges M, et al. IgE- and IgE+Ag-mediated mast cell migration in an autocrine/paracrine fashion. Blood. 2005;105(8):3222–9. PubMed Pubmed Central PMCID: 1464406.CrossRefPubMedPubMedCentralGoogle Scholar
  65. 65.
    Lam V, Kalesnikoff J, Lee CW, Hernandez-Hansen V, Wilson BS, Oliver JM, et al. IgE alone stimulates mast cell adhesion to fibronectin via pathways similar to those used by IgE + antigen but distinct from those used by steel factor. Blood. 2003;102(4):1405–13. PubMed PMID: 12702510.CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Kitagaki H, Ono N, Hayakawa K, Kitazawa T, Watanabe K, Shiohara T. Repeated elicitation of contact hypersensitivity induces a shift in cutaneous cytokine milieu from a T helper cell type 1 to a T helper cell type 2 profile. J Immunol. 1997;159(5):2484–91. PubMed PMID: 9278342.PubMedGoogle Scholar
  67. 67.
    Natsuaki M, Yano N, Yamaya K, Kitano Y. Immediate contact hypersensitivity induced by repeated hapten challenge in mice. Contact Dermatitis. 2000;43(5):267–72. PubMed PMID: 11016667.CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Kitagaki H, Fujisawa S, Watanabe K, Hayakawa K, Shiohara T. Immediate-type hypersensitivity response followed by a late reaction is induced by repeated epicutaneous application of contact sensitizing agents in mice. J Invest Dermatol. 1995;105(6):749–55. PubMed PMID: 7490467.CrossRefPubMedPubMedCentralGoogle Scholar

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© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Maria Estela Martinez-Escala
    • 1
  • Leah Ariella Kaplan
    • 2
  • Ana M. Giménez-Arnau
    • 3
  1. 1.Department of DermatologyNorthwestern University, Feinberg School of MedicineChicagoUSA
  2. 2.Tulane UniversityNew OrleansUSA
  3. 3.Department of DermatologyHospital del Mar - Institut Mar d’Investigacions Mediques, Universitat Autònoma de Barcelona (UAB)BarcelonaSpain

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