Skin-infiltrating T cells and cytokine expression in Icelandic horses affected with insect bite hypersensitivity: A possible role for regulatory T cells

Veterinary Immunology and Immunopathology

Volumn 140, Issue 1-2, 2011, Pages 63-74

  Heimann, Mareike ^a   Janda, Jozef ^b   Sigurdardottir, Olöf G ^a   Svansson, Vilhjalmur ^a   Klukowska, Jolanta ^b   von Tscharner, Claudia ^b   Doherr, Marcus ^b   Broström, Hans ^c   Andersson, Lisa S ^c   Einarsson, Sigurjón ^c   Marti, Eliane ^b   Torsteinsdottir, Sigurbjörg ^a  

^a UNIVERSITY OF ICELAND   (Iceland)

^b UNIVERSITY OF BERN   (Switzerland)

^c SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

Author keywords

Cytokines; Equine; FoxP3; Immunohistochemistry; Insect bite hypersensitivity; Treg cells

Indexed keywords

INTERLEUKIN 13; TRANSCRIPTION FACTOR FOXP3; CD4 ANTIGEN; CD8 ANTIGEN; CYTOKINE; FORKHEAD TRANSCRIPTION FACTOR; IMMUNOGLOBULIN E;

ARTICLE; CULICOIDES; CYTOKINE RELEASE; HORSE; HORSE DISEASE; HYPERSENSITIVITY; INSECT BITE; INSECT BITE HYPERSENSITIVITY; NONHUMAN; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE SUBPOPULATION; TH1 CELL; TH1 TH2 BALANCE; TH2 CELL; ANIMAL; ANIMAL DISEASE; BIOPSY; BIOSYNTHESIS; BLOOD; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CERATOPOGONIDAE; ENZYME LINKED IMMUNOSORBENT ASSAY; IMMEDIATE TYPE HYPERSENSITIVITY; IMMUNOLOGY; LYMPHOCYTE COUNT; METABOLISM; PATHOLOGY; PRURITUS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SKIN;

CULICOIDES NUBECULOSUS; EQUIDAE; HEXAPODA;

ANIMALS; ANTIGENS, CD4; ANTIGENS, CD8; BIOPSY; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CERATOPOGONIDAE; CYTOKINES; ENZYME-LINKED IMMUNOSORBENT ASSAY; FORKHEAD TRANSCRIPTION FACTORS; HORSES; HYPERSENSITIVITY, IMMEDIATE; IMMUNOGLOBULIN E; INSECT BITES AND STINGS; INTERLEUKIN-13; LYMPHOCYTE COUNT; PRURITUS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SKIN; T-LYMPHOCYTES, REGULATORY;

EID: 79961008673     PISSN: 01652427     EISSN: 18732534     Source Type: Journal    
DOI: 10.1016/j.vetimm.2010.11.016     Document Type: Article

References (63)

1. Akdis C.A., Blesken T., Akdis M., Wuthrich B., Blaser K. Role of interleukin 10 in specific immunotherapy. J. Clin. Invest. 1998, 102:98-106.
2. Akdis C.A., Akdis M., Simon D., Dibbert B., Weber M., Gratzl S., Kreyden O., Disch R., Wuthrich B., Blaser K., Simon H.U. T cells and T cell-derived cytokines as pathogenic factors in the nonallergic form of atopic dermatitis. J. Invest. Dermatol. 1999, 113:628-634.
3. Akdis M., Verhagen J., Taylor A., Karamloo F., Karagiannidis C., Crameri R., Thunberg S., Deniz G., Valenta R., Fiebig H., Kegel C., Disch R., Schmidt-Weber C.B., Blaser K., Akdis C.A. Immune responses in healthy and allergic individuals are characterized by a fine balance between allergen-specific T regulatory 1 and T helper 2 cells. J. Exp. Med. 2004, 199:1567-1575.
4. Anderton S.M., Liblau R.S. Regulatory T cells in the control of inflammatory demyelinating diseases of the central nervous system. Curr. Opin. Neurol. 2008, 21:248-254.
5. Baker K.P., Quinn P.J. A report on clinical aspects and histopathology of sweet itch. Equine Vet. J. 1978, 10:243-248.
6. Belkaid Y. Regulatory T cells and infection: a dangerous necessity. Nat. Rev. Immunol. 2007, 7:875-888.
7. Bellinghausen I., Klostermann B., Knop J., Saloga J. Human CD4+ CD25+ T cells derived from the majority of atopic donors are able to suppress TH1 and TH2 cytokine production. J. Allergy Clin. Immunol. 2003, 111:862-868.
8. Biedermann T., Rocken M., Carballido J.M. TH1 and TH2 lymphocyte development and regulation of TH cell-mediated immune responses of the skin. J. Invest. Dermatol. Symp. Proc. 2004, 9:5-14.
9. Bjornsdottir S., Sigvaldadottir J., Brostrom H., Langvad B., Sigurdsson A. Summer eczema in exported Icelandic horses: influence of environmental and genetic factors. Acta Vet. Scand. 2006, 48:3.
10. Brostrom H., Larsson A., Troedsson M. Allergic dermatitis (sweet itch) of Icelandic horses in Sweden: an epidemiological study. Equine Vet. J. 1987, 19:229-236.
11. Cao D., Malmstrom V., Baecher-Allan C., Hafler D., Klareskog L., Trollmo C. Isolation and functional characterization of regulatory CD25brightCD4+ T cells from the target organ of patients with rheumatoid arthritis. Eur. J. Immunol. 2003, 33:215-223.
12. Corry D.B. IL-13 in allergy: home at last. Curr. Opin. Immunol. 1999, 11:610-614.
13. Fadok V.A., Greiner E.C. Equine insect hypersensitivity: skin test and biopsy results correlated with clinical data. Equine Vet. J. 1990, 22:236-240.
14. Fontenot J.D., Rudensky A.Y. A well adapted regulatory contrivance: regulatory T cell development and the forkhead family transcription factor Foxp3. Nat. Immunol. 2005, 6:331-337.
15. Franz B., Fritzsching B., Riehl A., Oberle N., Klemke C.D., Sykora J., Quick S., Stumpf C., Hartmann M., Enk A., Ruzicka T., Krammer P.H., Suri-Payer E., Kuhn A. Low number of regulatory T cells in skin lesions of patients with cutaneous lupus erythematosus. Arthritis Rheum. 2007, 56:1910-1920.
16. Grewe M., Walther S., Gyufko K., Czech W., Schopf E., Krutmann J. Analysis of the cytokine pattern expressed in situ in inhalant allergen patch test reactions of atopic dermatitis patients. J. Invest. Dermatol. 1995, 105:407-410.
17. Grindebacke H., Wing K., Andersson A.C., Suri-Payer E., Rak S., Rudin A. Defective suppression of Th2 cytokines by CD4CD25 regulatory T cells in birch allergics during birch pollen season. Clin. Exp. Allergy 2004, 34:1364-1372.
18. Halldorsdottir S., Larsen H.J. An epidemiological study of summer eczema in Icelandic horses in Norway. Equine Vet. J. 1991, 23:296-299.
19. Hamid Q., Boguniewicz M., Leung D.Y. Differential in situ cytokine gene expression in acute versus chronic atopic dermatitis. J. Clin. Invest. 1994, 94:870-876.
20. Hamid Q., Naseer T., Minshall E.M., Song Y.L., Boguniewicz M., Leung D.Y. In vivo expression of IL-12 and IL-13 in atopic dermatitis. J. Allergy Clin. Immunol. 1996, 98:225-231.
21. Hamza E., Doherr M.G., Bertoni G., Jungi T.W., Marti E. Modulation of allergy incidence in icelandic horses is associated with a change in IL-4-producing T cells. Int. Arch. Allergy Immunol. 2007, 144:325-337.
22. Hamza E., Wagner B., Jungi T.W., Mirkovitch J., Marti E. Reduced incidence of insect-bite hypersensitivity in Icelandic horses is associated with a down-regulation of interleukin-4 by interleukin-10 and transforming growth factor-beta1. Vet. Immunol. Immunopathol. 2008, 122:65-75.
23. Hamza E., Torsteinsdottir S., Eydal M., Frey C.F., Mirkovitch J., Brcic M., Wagner B., Wilson A.D., Jungi T.W., Marti E. Increased IL-4 and decreased regulatory cytokine production following relocation of Icelandic horses from a high to low endoparasite environment. Vet. Immunol. Immunopathol. 2010, 133:40-50.
24. Hawrylowicz C.M., O'Garra A. Potential role of interleukin-10-secreting regulatory T cells in allergy and asthma. Nat. Rev. Immunol. 2005, 5:271-283.
25. Hellberg W., Wilson A.D., Mellor P., Doherr M.G., Torsteinsdottir S., Zurbriggen A., Jungi T., Marti E. Equine insect bite hypersensitivity: immunoblot analysis of IgE and IgG subclass responses to Culicoides nubeculosus salivary gland extract. Vet. Immunol. Immunopathol. 2006, 113:99-112.
26. Hori S., Nomura T., Sakaguchi S. Control of regulatory T cell development by the transcription factor Foxp3. Science 2003, 299:1057-1061.
27. Horwitz D.A. Regulatory T cells in systemic lupus erythematosus: past, present and future. Arthritis Res. Ther. 2008, 10:227.
28. Hrafnsdottir T. Diptera 2 (Chironomidae). Zool. Iceland III 2005, 48b:116.
29. Khalil N., Parekh T.V., O'Connor R., Antman N., Kepron W., Yehaulaeshet T., Xu Y.D., Gold L.I. Regulation of the effects of TGF-beta 1 by activation of latent TGF-beta 1 and differential expression of TGF-beta receptors (T beta R-I and T beta R-II) in idiopathic pulmonary fibrosis. Thorax 2001, 56:907-915.
30. Kurotaki T., Narayama K., Oyamada T., Yoshikawa H., Yoshikawa T. Immunopathological study on equine insect hypersensitivity ("kasen") in Japan. J. Comp. Pathol. 1994, 110:145-152.
31. Langner K.F., Jarvis D.L., Nimtz M., Heselhaus J.E., McHolland L.E., Leibold W., Drolet B.S. Identification, expression and characterisation of a major salivary allergen (Culs 1) of the biting midge Culicoides sonorensis relevant for summer eczema in horses. Int. J. Parasitol. 2009, 39:243-250.
32. Larche M. Regulatory T cells in allergy and asthma. Chest 2007, 132:1007-1014.
33. Leung D.Y., Bieber T. Atopic dermatitis. Lancet 2003, 361:151-160.
34. Leung D.Y., Boguniewicz M., Howell M.D., Nomura I., Hamid Q.A. New insights into atopic dermatitis. J. Clin. Invest. 2004, 113:651-657.
35. Ling E.M., Smith T., Nguyen X.D., Pridgeon C., Dallman M., Arbery J., Carr V.A., Robinson D.S. Relation of CD4+ CD25+ regulatory T-cell suppression of allergen-driven T-cell activation to atopic status and expression of allergic disease. Lancet 2004, 363:608-615.
36. Marti E., Urwyler A., Neuenschwander M., Eicher R., Meier D., de Weck A.L., Gerber H., Lazary S., Dahinden C.A. Sulfidoleukotriene generation from peripheral blood leukocytes of horses affected with insect bite dermal hypersensitivity. Vet. Immunol. Immunopathol. 1999, 71:307-320.
37. McKelvie J., Foster A.P., Cunningham F.M., Hamblin A.S. Characterisation of lymphocyte subpopulations in the skin and circulation of horses with sweet itch (Culicoides hypersensitivity). Equine Vet. J. 1999, 31:466-472.
38. Mosmann, Sad The expanding universe of T cell subsets: Th1, Th2, and more. Immunol. Today 1996, 17:138-141.
39. Obara W., Kawa Y., Ra C., Nishioka K., Soma Y., Mizoguchi M. T cells and mast cells as a major source of interleukin-13 in atopic dermatitis. Dermatology 2002, 205:11-17.
40. Pfeffer A., Wilson J.A., Pernthaner A. Changes in morphology and key cytokine gene expression after intradermal injection of louse (Bovicola ovis) antigen in sheep with naturally occurring atopic dermatitis. J. Comp. Pathol. 2007, 136:36-48.
41. Provoost S., Maes T., van Durme Y.M., Gevaert P., Bachert C., Schmidt-Weber C.B., Brusselle G.G., Joos G.F., Tournoy K.G. Decreased FOXP3 protein expression in patients with asthma. Allergy 2009, 64:1539-1546.
42. Rees C.A. Canine and feline atopic dermatitis: a review of the diagnostic options. Clin. Tech. Small Anim. Pract. 2001, 16:230-232.
43. Rho N.K., Kim W.S., Lee D.Y., Lee J.H., Lee E.S., Yang J.M. Immunophenotyping of inflammatory cells in lesional skin of the extrinsic and intrinsic types of atopic dermatitis. Br. J. Dermatol. 2004, 151:119-125.
44. Robinson D.S., Larche M., Durham S.R. Tregs and allergic disease. J. Clin. Invest. 2004, 114:1389-1397.
45. Roncarolo M.G., Bacchetta R., Bordignon C., Narula S., Levings M.K. Type 1 T regulatory cells. Immunol. Rev. 2001, 182:68-79.
46. Roosje P.J., van Kooten P.J., Thepen T., Bihari I.C., Rutten V.P., Koeman J.P., Willemse T. Increased numbers of CD4+ and CD8+ T cells in lesional skin of cats with allergic dermatitis. Vet. Pathol. 1998, 35:268-273.
47. Schaffartzik, A., Marti, E., Torsteinsdottir, S., Mellor, P.S., Crameri, R., Rhyner, C., 2010. Selective cloning, characterization, and production of the Culicoides nubeculosus salivary gland allergen repertoire associated with equine insect bite hypersensitivity. Vet. Immunol. Immunopathol., doi:10.1016/j.vetimm2010.10.015.
48. Scott D.W. Histopathologie cutatnée de l'hypersensibilité aux piqures de Culicoides chez le cheval. Point Vét. 1990, 22.
49. Scott D.W., Millier W.H. Equine Dermatology 2003, Elsevier Sciences, St. Louis, 10 p.
50. Solomon G.J., Magro C.M. Foxp3 expression in cutaneous T-cell lymphocytic infiltrates. J. Cutan. Pathol. 2008, 35:1032-1039.
51. Steinbach F., Bischoff S., Freund H., Metzner-Flemisch S., Ibrahim S., Walter J., Wilke I., Mauel S. Clinical application of dendritic cells and interleukin-2 and tools to study activated T cells in horses - first results and implications for quality control. Vet. Immunol. Immunopathol. 2009, 128:16-23.
52. Taylor A., Verhagen J., Blaser K., Akdis M., Akdis C.A. Mechanisms of immune suppression by interleukin-10 and transforming growth factor-beta: the role of T regulatory cells. Immunology 2006, 117:433-442.
53. Tazawa T., Sugiura H., Sugiura Y., Uehara M. Relative importance of IL-4 and IL-13 in lesional skin of atopic dermatitis. Arch. Dermatol. Res. 2004, 295:459-464.
54. Thepen T., Langeveld-Wildschut E.G., Bihari I.C., van Wichen D.F., van Reijsen F.C., Mudde G.C., Bruijnzeel-Koomen C.A. Biphasic response against aeroallergen in atopic dermatitis showing a switch from an initial TH2 response to a TH1 response in situ: an immunocytochemical study. J. Allergy Clin. Immunol. 1996, 97:828-837.
55. Till S.J., Francis J.N., Nouri-Aria K., Durham S.R. Mechanisms of immunotherapy. J. Allergy Clin. Immunol. 2004, 113:1025-1034. quiz 1035.
56. van der Haegen A., Griot-Wenk M., Welle M., Busato A., von Tscharner C., Zurbriggen A., Marti E. Immunoglobulin-E-bearing cells in skin biopsies of horses with insect bite hypersensitivity. Equine Vet. J. 2001, 33:699-706.
57. van Grevenhof E.M., Ducro B., Heuven H.C., Bijma P. Identification of environmental factors affecting the prevalence of insect bite hypersensitivity in Shetland ponies and Friesian horses in The Netherlands. Equine Vet. J. 2007, 39:69-73.
58. Wagner B., Miller W.H., Morgan E.E., Hillegas J.M., Erb H.N., Leibold W., Antczak D.F. IgE and IgG antibodies in skin allergy of the horse. Vet. Res. 2006, 37:813-825.
59. Wagner B., Hillegas J.M., Brinker D.R., Horohov D.W., Antczak D.F. Characterization of monoclonal antibodies to equine interleukin-10 and detection of T regulatory 1 cells in horses. Vet. Immunol. Immunopathol. 2008, 122:57-64.
60. Wan Y.Y., Flavell R.A. Regulatory T-cell functions are subverted and converted owing to attenuated Foxp3 expression. Nature 2007, 445:766-770.
61. Wilson A.D., Harwood L., Torsteinsdottir S., Marti E. Production of monoclonal antibodies specific for native equine IgE and their application to monitor total serum IgE responses in Icelandic and non-Icelandic horses with insect bite dermal hypersensitivity. Vet. Immunol. Immunopathol. 2006, 112:156-170.
62. Wilson A.D., Heesom K.J., Mawby W.J., Mellor P.S., Russell C.L. Identification of abundant proteins and potential allergens in Culicoides nubeculosus salivary glands. Vet. Immunol. Immunopathol. 2008, 122:94-103.
63. Zhang B., Zhang X., Tang F., Zhu L., Liu Y. Reduction of forkhead box P3 levels in CD4+ CD25high T cells in patients with new-onset systemic lupus erythematosus. Clin. Exp. Immunol. 2008, 153:182-187.