Skin as a novel route for allergen-specific immunotherapy

Current Pharmaceutical Design

Volumn 20, Issue 6, 2014, Pages 886-891

  Li, Wei ^a   Zhang, Zhuo ^a,b   Tian, Rong ^a,c   Zhang, Ke ^d  

^a FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^b FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^c AIR FORCE GENERAL HOSPITAL   (China)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Epicutaneous; Food allergy; Immunization; Immunotherapy; Langerhans cells; Peanut; Skin; Tolerance

Indexed keywords

ALLERGEN;

ALLERGY; ARTICLE; HUMAN; IMMUNE RESPONSE; IMMUNIZATION; IMMUNOLOGICAL TOLERANCE; IMMUNOTHERAPY; LANGERHANS CELL; NONHUMAN; PRIORITY JOURNAL; SENSITIZATION; SKIN;

ALLERGENS; ANIMALS; DESENSITIZATION, IMMUNOLOGIC; FOOD HYPERSENSITIVITY; HUMANS; HYPERSENSITIVITY; IMMUNE TOLERANCE; IMMUNOGLOBULIN E; IMMUNOTHERAPY; MICE; SKIN;

EID: 84895165632     PISSN: 13816128     EISSN: 18734286     Source Type: Journal    
DOI: 10.2174/13816128113199990051     Document Type: Article

References (86)

1. Sicherer SH, Munoz-Furlong A, Sampson HA. Prevalence of peanut and tree nut allergy in the United States determined by means of a random digit dial telephone survey: a 5-year follow-up study. J Allergy Clin Immunol 2003; 112: 1203-7.
2. Osterballe M, Hansen TK, Mortz CG, et al. The prevalence of food hypersensitivity in an unselected population of children and adults. Pediatr Allergy Immunol 2005; 16: 567-73.
3. Sicherer SH, Leung DY. Advances in allergic skin disease, anaphylaxis, and hypersensitivity reactions to foods, drugs, and insects. J Allergy Clin Immunol 2006; 118: 170-7.
4. Sicherer SH, Sampson HA. Food allergy. J Allergy Clin Immunol 2006; 117: S470-5.
5. Palmer K, and Burks AW. Current developments in peanut allergy. Curr Opin Allergy Clin Immunol 2006; 6: 202-6.
6. Leung DY, Sampson HA, Yunginger JW, et al. Effect of anti-IgE-therapy in patients with peanut allergy. N Engl J Med 2003; 348: 986-93.
7. Glaspole IN, De Leon MP, Rolland JM, O'Hehir RE. Characterization of the T-cell epitopes of a major peanut allergen, Ara h 2. Allergy 2005; 60: 35-40.
8. Hong SJ, Michael JG, Fehringer A, Leung DY. Pepsin-digested peanut contains T-cell epitopes but no IgE epitopes. J Allergy Clin Immunol 1999; 104: 473-8.
9. Buchanan AD, Green TD, Jones SM, et al. Egg oral immunotherapy in nonanaphylactic children with egg allergy. J Allergy Clin Immunol 2007; 119: 199-205.
10. Burks AW, Cockrell G, Stanley JS, et al. Recombinant peanut allergen Ara h 1 expression and IgE binding in patients with peanut hypersensitivity. J Clin Invest 1995; 96: 1715-21.
11. Stanley JS, King N, Burks AW, et al. Identification and mutational analysis of the immunodominant IgE binding epitopes of the major peanut allergen Ara h 2. Arch Biochem Biophys 1997; 342: 244-53.
12. Burks AW, King N, Bannon GA. Modification of a major peanut allergen leads to loss of IgE binding. Int Arch Allergy Immunol 1999; 118: 313-4.
13. Bolhaar ST, Tiemessen MM, Zuidmeer L, et al. Efficacy of birch-pollen immunotherapy on cross-reactive food allergy confirmed by skin tests and double-blind food challenges. Clin Exp Allergy 2004; 34: 761-9.
14. Roman M, Martin-Orozco E, Goodman JS, et al. Immunostimula-tory DNA sequences function as T helper-1-promoting adjuvants. Nat Med 1997; 3: 849-54.
15. Li XM, Zhang TF, Huang CK, et al. Food Allergy Herbal Formula-1 (FAHF-1) blocks peanut-induced anaphylaxis in a murine model. J. Allergy Clin Immunol 2001; 108: 639-46.
16. Srivastava KD, Kattan JD, Zou ZM, et al. The Chinese herbal medicine formula FAHF-2 completely blocks anaphylactic reactions in a murine model of peanut allergy. J Allergy Clin Immunol 2005; 115: 171-8.
17. Raz E, Tighe H, Sato Y, et al. Preferential induction of a Th1 immune response and inhibition of specific IgE antibody formation by plasmid DNA immunization, Proc Natl Acad Sci USA 1996; 93: 5141-5.
18. Streilein J. W. Skin-associated lymphoid tissues (SALT): origins and functions. J. Invest. Dermatol 1983; 80: 12s-16s.
19. Glenn GM, Rao M, Matyas GR, Alving CR. Skin immunization made possible by cholera toxin. Nature 1998; 391: 851.
20. Stoitzner P, Green LK, Jung JY, et al. Tumor immunotherapy by epicutaneous immunization requires langerhans cells. J Immunol. 2008; 180: 1991-8.
21. Glenn GM, Scharton-Kersten T, Vassell R, et al. Transcutaneous immunization with bacterial ADP-ribosylating exotoxins as anti-gens and adjuvants. Infect Immun 1999; 67: 1100-6.
22. Glenn GM, Scharton-Kersten T, Vassell R, et al. Transcutaneous immunization with cholera toxin protects mice against lethal mucosal toxin challenge. J Immunol 1998; 161: 3211-4.
23. Berry LJ, Hickey DK, Skelding KA, et al. Transcutaneous immunization with combined cholera toxin and CpG adjuvant protects against Chlamydia muridarum genital tract infection. Infect. Immun 2004; 72: 1019-28.
24. Yu J, Cassels F, Scharton-Kersten T, et al. Transcutaneous immunization using colonization factor and heat-labile enterotoxininduces correlates of protective immunity for enterotoxigenic Escherichia coli.et al. Infect Immun 2002; 70: 1056-68.
25. Nicolas JF, Guy B. Intradermal, epidermal and transcutaneous vaccination: from immunology to clinical practice. Expert Rev Vaccines 2008; 8: 1201-14.
26. Partidos CD and Muller S. Decision-making at the surface of the intact or barrier disrupted skin: potential applications for vaccination or therapy. Cell Mol Life Sci 2005; 62: 1418-24.
27. Williams IR, Kupper TS. Immunity at the surface: homeostatic mechanisms of the skin immune system. Life Sci 1996. 58: 1485-507.
28. Wood LC, Jackson SM, Elias P M, et al. Cutaneous barrier perturbation stimulates cytokine production in the epidermis of mice. J Clin Invest 1992; 90: 482-7.
29. Cumberbatch M, Dearman RJ. and Kimber I. Langerhans cells require signals from both tumour necrosis factoralpha and interleukin-1 beta for migration. Immunology 1997; 92: 388-95.
30. Schwarzenberger K, Udey MC. Contact allergens and epidermal proinflammatory cytokines modulate Langerhans cell E-cadherin expression in situ. J Invest Dermatol 1996; 106: 553-8.
31. Price AA, Cumberbatch M, Kimber I, Ager A. Alpha 6 integrins are required for Langerhans cell migration from the epidermis. J Exp Med 1997; 186: 1725-35.
32. Sozzani S, Allavena P, D'Amico G, et al. Differential regulation of chemokine receptors during dendritic cell maturation: a model for their trafficking properties. J Immunol 1998; 161: 1083-6.
33. Ring J, Möhrenschlager M. Allergy to peanut oil--clinically relevant? J Eur Acad Dermatol Venereol 2007; 21: 452-5.
34. Lack G, Fox D, Northstone K, et al. Factors associated with the development of peanut allergy in childhood. N Engl J Med. 2003; 348: 977-85.
35. Wang LF, Lin JY, Hsieh KH, Lin RH. Epicutaneous exposure of protein antigen induces a predominant Th2-like response with high IgE production in mice. J Immunol 1996; 156: 4077-82.
36. Wang LF, Wu JT, Sun CC. Local but not systemic administration of IFN-gamma during the sensitization phase of protein antigen immunization suppress Th2 development in a murine model of atopic dermatitis. Cytokine 2002; 19: 147-52.
37. He R, Oyoshi MK, Jin H, Geha RS. Epicutaneous antigen exposure induces a Th17 response that drives airway inflammation after inhalation challenge. Proc Natl Acad Sci USA 2007; 104: 15817-22.
38. Jin H, Oyoshi MK, Le Y, et al. IL-21R is essential for epicutaneous sensitization and allergic skin inflammation in humans and mice. J Clin Invest 2009; 119: 47-60.
39. Strid J, Hourihanew J, Kimberz I, et al. Epicutaneous exposure to peanut protein prevents oral tolerance and enhances allergic sensitization. Clin Exp Allergy 2005; 35: 757-66.
40. Novak N, Bieber T. Dendritic cells as regulators of immunity and tolerance. J Allergy Clin Immunol 2008; 121: S370-4.
41. Li M, Hener P, Zhang Z, et al. Topical vitamin D3 and low-calcemic analogs induce thymic stromal lymphopoietin in mouse keratinocytes and trigger an atopic dermatitis. Proc Natl Acad Sci U S A. 2006; 103: 11736-41.
42. Szczepanik M. Skin-induced tolerance and its reversal by Toll-like receptor ligands. Arch Immunol Ther Exp 2007; 55: 161-72.
43. Ptak W, Szczepanik M, Bryniarski K, et al. Epicutaneous application of protein antigens incorporated into cosmetic cream induces antigen-nonspecific unresponsiveness in mice and affects the cell-mediated immune response. Int Arch Allergy Immunol 2002. 128: 8-14.
44. Szczepanik M, Tutaj M, Bryniarski K, Dittel BN. Epicutaneously induced TGF- -dependent tolerance inhibits experimental autoimmune encephalomyelitis. J Neuroimmunol 2005. 164: 105-14.
45. Tutaj M, Szczepanik, M. Epicutaneous (EC+) imm+unizat+on with myelin basic protein (MBP) induces TCR CD4 CD8 double positive suppressor cells that protect from experimental autoimmune encephalomyelitis (EAE). J Autoimmun 2007; 28: 208-15.
46. Szczepanik M, Bryniarski K, Tutaj M, et al. Epicutaneous immunization induces alphabeta T-cell receptor CD4 CD8 double-positive non-specific suppressor T cells that inhibit contact sensitivity via transforming growth factor-beta. Immunology 2005; 115: 42-54.
47. Majewska M, Zajac K, Kubera M, et al. Effects of ovalbumin on survival of H-Y incompatible skin graft in C57BL/6 mice. Pharmacol Rap 2006; 58: 439-42.
48. Majewska-Szczepanik M, Góralska M, Marcińska K, et al. Epicu-taneous immunization with protein antigen TNP-Ig alleviates TNBS-induced colitis in mice. Pharmacol Rep. 2012; 64: 1497-1504
49. Majewska-Szczepanik M, Zemelka-Wia̧cek M, Ptak W, Wen L, Szczepanik M. Epicutaneous immunization with DNP-BSA induces CD4+CD25+ Treg cells that inhibit Tc1-mediated CS. Immunol Cell Biol. 2012; 90: 784-95.
50. Zemelka-Wia̧cek M, Majewska-Szczepanik M, Ptak W, Szcze-panik M. Epicutaneous immunization with protein antigen induces antigen-non-specific suppression of CD8 T cell mediated contact sensitivity. Pharmacol Rep. 2012; 64: 1485-96
51. Ghoreishi M, and Dutz JP. Tolerance induction by transcutaneous immunization through ultraviolet-irradiated skin is transferable through CD4+CD25+ T regulatory cells and is dependent on host- derived IL-10. J Immunol 2006; 176: 2635-44.
52. Ptak W, Bryniarski K, Ptak M, et al. Toll-like receptor (TLR) ligands reverse suppression of contact hypersensitivity (CS) reactions induced by epicutaneous (EC) immunization with protein antigen. Int. Arch. Allergy Immunol 2006; 139: 188-200.
53. Ptak W, Majewska M, Bryniarski K, et al. Epicutaneous immunization with protein antigen in the presence of TLR4 ligand induces TCR alpha beta+CD4+ T contrasuppressor cells that reverse skin-induced suppression of Th1-mediated contact sensitivity. J Immunol 2009. 182: 837-50.
54. Paust S, Gill HS, Wang BZ, Flynn MP, et al. Critical role for the chemokine receptor CXCR6 in NK cell-mediated antigen-specific memory of haptens and viruses. Nat Immunol. 2010; 11: 1127-35.
55. Majewska-Szczepanik M, Strzȩpa A, Droyska I, et al. Epicuta-neous immunization with hapten-conjugated protein antigen alleviates contact sensitivity mediated by three different types of effector cells. Pharmacol Rep. 2012; 64: 919-26.
56. Juryńczyk M, Walczak A, Jurewicz A, et al. Immune regulation of multiple sclerosis by transdermally applied myelin peptides. Ann Neurol. 2010; 68: 593-601.
57. Li W, Zhang Z, Saxon A, Zhang K. Prevention of oral peanut allergy sensitization via skin application of peanut allergen in a murine model. Allergy 2012; 67: 622-9
58. Spergel JM, Mizoguchi E, Brewer JP, et al. Epicutaneous sensitization with protein antigen induces localized allergic dermatitis and hyperresponsiveness to methacholine after single exposure to aerosolized antigen in mice. J Clin Invest. 1998; 101: 1614-22.
59. Spergel JM, Mizoguchi E, Oettgen H, Bhan AK, Geha RS. Roles of TH1 and TH2 cytokines in a murine model of allergic dermatitis. J Clin Invest. 1999; 103(8): 1103-11.
60. Herrick CA, MacLeod H, Glusac E, Tigelaar RE, Bottomly K. Th2 responses induced by epicutaneous or inhalational protein exposure are differentially dependent on IL-4. J Clin Invest. 2000; 105: 765-75.
61. Akei HS, Mishra A, Blanchard C, Rothenberg ME. Epicutaneous antigen exposure primes for experimental eosinophilic esophagitis in mice. Gastroenterology. 2005; 129: 985-94.
62. Hsieh KY, Tsai CC, Wu CH, Lin RH. Epicutaneous exposure to protein antigen and food allergy. Clin Exp Allergy. 2003; 33: 1067-75.
63. Blamoutier P, Blamoutier J, Guibert L. Treatment of pollinosis with pollen extracts by the method of cutaneous quadrille ruling [in French]. Presse Med 1959; 67: 2299-301.
64. Senti G, Graf N, Haug S, R€uedi N, von Moos S, Sonderegger T, et al. Epicutaneous allergen administration as a novel method of allergen-specific immunotherapy. J Allergy Clin Immunol 2009; 124: 997-1002.
65. Wang B, Feliciani C, Howell BG, et al. Contribution of Langerhans cell-derived IL-18 to contact hypersensitivity. J Immunol 2002; 168: 3303-8.
66. Hauser C, Saurat JH, Schmitt A, et al. Interleukin 1 is present in normal human epidermis. J Immunol 1986; 136: 3317-3323.
67. Camp R, Fincham N, Ross J, et al. Potent inflammatory properties in human skin of interleukin-1 alpha-like material isolated from normal skin. J Invest Dermatol 1990; 94: 735-41.
68. Corsini E, Galli CL. Epidermal cytokines in experimental contact dermatitis. Toxicology 2000; 142: 203-11.
69. Inoue J, Yotsumoto S, Sakamoto T, et al. Changes in immune responses to antigen applied to tape-stripped skin with CpG- oligodeoxynucleotide in mice. J Control Release 2005; 108: 294-305.
70. Strid J, Hourihane J, Kimber I, et al. Disruption of the stratum corneum allows potent epicutaneous immunization with protein an- tigens resulting in a dominant systemic Th2 response. Eur J Immu- nol 2004; 34: 2100-9.
71. Inoue J, Aramaki Y. Toll-like receptor-9 expression induced by tape-stripping triggers on effective immune response with CpGoligodeoxynucleotides. Vaccine 2007; 25: 1007-13.
72. Cumberbatch M, Dearman RJ, Antonopoulos C, et al. Interleukin (IL)-18 induces Langerhans cell migration by a tumour necrosis factor-alpha- and IL-1beta-dependent mechanism. Immunology 2001; 102: 323-30.
73. Senti G, von Moos S, Tay F, et al. Epicutaneous allergen-specific immunotherapy ameliorates grass pollen-induced rhinoconjunctivitis: A double-blind, placebo-controlled dose escalation study. J Allergy Clin Immunol. 2012; 129: 128-35.
74. von Moos S, Johansen P, Waeckerle-Men Y, et al. The contact sensitizer diphenylcyclopropenone has adjuvant properties in mice and potential application in epicutaneous immunotherapy. Allergy. 2012; 67: 638-46.
75. Dupont C, Kalach N, Soulaines P, et al. Cow's milk epicutaneous immunotherapy in children: a pilot trial of safety, acceptability, and impact on allergic reactivity. J Allergy Clin Immunol 2010; 125: 1165-7.
76. Mondoulet L, Dioszeghy V, Ligouis M, et al. Epicutaneous immunotherapy on intact skin using a new delivery system in a murine model of allergy. Clin Exp Allergy 2010; 40: 659-67.
77. Mondoulet L, Dioszeghy V, Vanoirbeek JA, et al. Epicutaneous immunotherapy using a new epicutaneous delivery system in mice sensitized to peanuts. Int Arch Allergy Immunol 2011; 154: 299-309.
78. Soury D, Barratt G, Ah-Leung S, et al. Skin localization of cow's milk proteins delivered by a new ready-to-use atopy patch test. Pharm Res 2005; 22: 1530-6.
79. Dioszeghy V, Mondoulet L, Dhelft V, et al. Epicutaneous Immuno-therapy Results in Allergen-Specific Response in Sensitized Mice through Intact Skin and Downregulates the Rapid Allergen Uptake by Dendritic Cells. J Immunol 2011; 186: 5629-37.
80. Chen Y, Inobe J, Kuchroo VK, et al. Oral tolerance in myelin basic protein T-cell receptor transgenic mice: suppression of autoimmune encephalomyelitis and dose-dependent induction of regulatory cells. Proc Natl Acad Sci USA 1996; 93, 388-91.
81. Weiner HL, Friedman A, Miller A, et al. Oral tolerance: immunologic mechanisms and treatment of animal and human organ- specific autoimmune diseases by oral administration of autoantigens. Annu Rev Immunol 1994; 12: 809-37.
82. Xiao BG, Link H. Mucosal tolerance: a two--edged sword to pre-vent and treat autoimmune diseases. Clin Immunol Immunopathol 1997; 85: 119-28.
83. Faria AM, Weiner HL. Oral tolerance. Immunol Rev 2005; 206: 232-59.
84. Weiner HL. The mucosal milieu creates tolerogenic dendritic cells and T(R)1 and T(H)3 regulatory cells. Nat Immunol 2001; 2: 671-2.
85. Butcher EC, Picker LJ. Lymphocyte homing and homeostasis. Science 1996; 272: 60-66.
86. Belyakov IM, Hammond SA, Ahlers JD, et al. Transcutaneous immunization induces mucosal CTLs and protective immunity by migration of primed skin dendritic cells. J Clin Invest 2004; 113: 998-1007.