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Ige and Igg Antibodies in Skin Allergy of the Horse Bettina Wagner, William Miller, Erin Morgan, Julia Hillegas, Hollis Erb, Wolfgang Leibold, Douglas Antczak

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Ige and Igg Antibodies in Skin Allergy of the Horse Bettina Wagner, William Miller, Erin Morgan, Julia Hillegas, Hollis Erb, Wolfgang Leibold, Douglas Antczak IgE and IgG antibodies in skin allergy of the horse Bettina Wagner, William Miller, Erin Morgan, Julia Hillegas, Hollis Erb, Wolfgang Leibold, Douglas Antczak To cite this version: Bettina Wagner, William Miller, Erin Morgan, Julia Hillegas, Hollis Erb, et al.. IgE and IgG anti- bodies in skin allergy of the horse. Veterinary Research, BioMed Central, 2006, 37 (6), pp.813-825. 10.1051/vetres:2006039. hal-00903061 HAL Id: hal-00903061 https://hal.archives-ouvertes.fr/hal-00903061 Submitted on 1 Jan 2006 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Vet. Res. 37 (2006) 813–825 813 c INRA, EDP Sciences, 2006 DOI: 10.1051/vetres:2006039 Original article IgE and IgG antibodies in skin allergy of the horse Bettina Wa*, William H. Mb,ErinE.Ma, Julia M. Ha, Hollis N. Ec,WolfgangLd, Douglas F. Aa a Baker Institute for Animal Health, College of Veterinary Medicine, Cornell University, Ithaca, NY 14853, USA b Department of Clinical Sciences, College of Veterinary Medicine, Cornell University, Ithaca, NY 14853, USA c Department of Population Medicine and Diagnostic Sciences, College of Veterinary Medicine, Cornell University, Ithaca, NY 14853, USA d Institute of Immunology, University of Veterinary Medicine, 30173 Hannover, Germany (Received 15 March 2006; accepted 5 June 2006) Abstract – In horses, allergies have been characterized by clinical signs and/or intradermal (i.d.) allergen testing. Our aim was to find the first direct evidence that immunoglobulin E (IgE) mediates equine allergy. In addition, we tested the hypothesis that immediate skin reactions in horses can also be mediated by IgG. Anti-IgE affinity columns were used to purify IgE from serum of one healthy horse and three horses affected with summer eczema, an allergic dermatitis which is believed to be induced by Culicoides midges. A modified Prausnitz-Küstner experiment was performed in four clinical healthy horses by i.d. injection of the purified serum IgE antibodies. The following day, Culicoides allergen was injected at the same sites. Skin reactions were not observed in response to allergen alone, and in two horses after stimulation at any previous IgE injection site. However, the other two horses showed an immediate skin reaction at the previous injection sites of IgE obtained from allergic horses. In addition, purified monoclonal antibodies to various equine immunoglobu- lin isotypes were injected i.d. into six healthy horses. Immediate skin reactions were observed in response to anti-IgE (6/6 horses) and anti-IgG(T) injections (5/6 horses). The specificities of both antibodies for IgE and IgG(T), respectively, were confirmed by enzyme linked immunosorbent as- says. The results provide the first direct evidence that IgE mediates classical Type-I allergy in horses and plays a major role in the pathogenesis of summer eczema. The data also suggest that IgG(T) can bind to skin mast cells and might contribute to clinical allergy. horse / allergy / summer eczema / IgE / IgG 1. INTRODUCTION [19]. These include skin hypersensitiv- ities [4, 13, 27], urticaria [17], chronic obstructive pulmonary disease (recurrent Based on clinical signs and intrader- airway obstruction) [20, 24], and head- mal (i.d.) skin testing, several diseases shaking [17]. Epidemiological data about have been associated with Immunoglob- allergy in horses are rare. This most likely ulin E (IgE) mediated allergy in horses reflects the existing difficulties in pre- cisely diagnosing the presence of allergy. * Corresponding author: [email protected] Article available at http://www.edpsciences.org/vetres or http://dx.doi.org/10.1051/vetres:2006039 814 B. Wagner et al. Currently, the best allergy test available IgE antibodies. These antibodies are sub- is intradermal skin testing with allergen sequently bound by high-affinity FcεRI extracts. However, this procedure requires on cell membranes of mast cells and ba- expertise in technical performance and sophils, a process which is called “sen- interpretation of the results. Thus, it is sitization”. The IgE sensitized cells can mainly performed in some larger clinics be stimulated at each successive contact or university hospitals [14]. Because of with allergen, resulting in release of pre- economic, scheduling, or transportation is- formed inflammatory mediators, such as sues, allergies in the field are often diag- histamine, and induction of synthesis and nosed by clinical signs only. These horses release of leukotrienes, prostaglandins and generally do not contribute to statistical cytokines, all of which together initiate the analysis about the prevalence of allergy. inflammatory response and maintain the The most common skin hypersensitiv- production of allergen-specific IgE [11]. ity in horses is called “summer eczema” Although a role for IgE-mediated mast or “sweet itch”. This is a recurrent al- cell degranulation in summer eczema has lergic dermatitis that has been described been hypothesized by inducing immediate frequently in Icelandic horses, but it also skin reactions after intradermal Culicoides occurs in many other horse breeds, in- allergen exposure in affected horses [2, 4, cluding Thoroughbreds, Arabians, Warm- 13], the direct involvement of IgE has not bloods, Draft horses, Quarter horses and yet been demonstrated. Our aim was to ponies. Summer eczema has been found all provide the first formal evidence that IgE over the world and is believed to be in- mediates allergy in horses. We performed duced by allergens from the saliva of biting two experiments. First, we used a previ- midges of Culicoides spp. [2,4,8,9,13,15]. ously described method to purify IgE from The prevalence of the disease varies be- serum [30] and performed a Prausnitz- tween 3–72% [5,10,12]. Similar to human Küstner (P-K) experiment by transferring atopic dermatitis, summer eczema is not the allergic reaction to healthy animals life-threatening, but it induces high levels using IgE from horses affected with sum- of discomfort and massive scratching fol- mer eczema. Second, to determine the im- lowed by loss of hair and severe skin irrita- munoglobulin isotypes which can mediate tions. Current treatments include allergen mast cell degranulation in horses, we tested avoidance, anti-allergic medications, and monoclonal antibodies (mabs) to equine immunotherapy, also known as “hypo-” or IgE and IgG isotypes for their potential to “desensitization” [3]. The current therapies induce an immediate skin reaction in vivo. reduce clinical signs but do not cure the al- lergic disease. 2. MATERIALS AND METHODS IgE has a natural protective function as a defense against parasites. However, 2.1. Horses IgE can also mediate pathological reac- tions which manifest as allergy. IgE binds The recipient horses for the P-K ex- to high-affinity IgE-receptors (FcεRI) on periment and for intradermal (i.d.) injec- mast cells. This interaction between IgE tion of anti-equine IgE or IgG mabs were and the FcεRI plays a key role in allergic clinical healthy, adult horses (10–19 years inflammatory responses induced by mast of age) from the experimental herd at cell degranulation. Type-I hypersensitivi- the Baker Institute for Animal Health. ties are characterized by an initial contact Two geldings and four mares of different to the allergen, resulting in activation of breeds (Thoroughbred, Warmblood, Quar- B-cells and production of allergen-specific ter Horse) were used. The serum donors Skin allergy in horses 815 for the P-K experiment and the periph- run under non-reducing conditions. The eral blood donors for the histamine release proteins were either stained in the gel us- assay were adult female Icelandic horses ing Coomassie Brilliant Blue or blotted with or without clinical signs of summer to PVDF membranes (Bio-Rad, Hercules, eczema. All experimental procedures were CA, USA). The membranes were incu- approved by the Animal Care Committee bated with the following monoclonal anti- of Cornell University and were in accor- bodies to equine IgG: anti-IgGa (CVS45), dance with the guidelines established by anti-IgGb (CVS39), anti-IgGc (CVS52), the NIH. and anti-IgG(T) (CVS40) [16, 26]. The CVS antibodies were kindly provided by Dr P. Lunn (Colorado State University, 2.2. Purification of IgE and IgG from Fort Collins, CO, USA). serum IgE and IgG were purified from equine 2.4. Prausnitz-Küstner (P-K) serum as previously described [30]. In experiment brief, the purification was performed using an ÄKTA FPLC instrument (Amersham Biosciences, Piscataway, NJ, USA) and The horses used as recipients in this ex- two affinity columns. First, a Protein G periment showed no clinical signs of skin affinity column (HiTrap Protein G, Amer- hypersensitivity over the past two sum- sham Biosciences, Piscataway, NJ, USA) mers, nor reaction to Culicoides allergen was used to deplete IgG from serum. Sec- when skin testing was performed. An area ond, the IgG depleted serum was passed at the lateral side of the neck was prepared over an anti-equine IgE affinity column for i.d. injection by clipping. A total of generated by coupling of anti-IgE134 mab 100 µL purified IgE (50 µg/mL) and IgG 1 to CNBr-activated sepharose 4B. Both the (300 µg/mL) were injected i.d. to four an- Protein G and anti-IgE columns were imals. The next day, allergen (Culicoides eluted using 0.1M glycine (pH 3.0) and extract; 1000 pnu/mL; Greer Laboratories, the eluates were subsequently neutralized Lenoir, NC, USA) was injected at the same in 1M Tris buffer (pH 8.0).
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