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Characterisation of Potential Novel Allergens in the Fish e u pa open proteomics 4 (2014) 140–155 View metadata, citation and similar papers at core.ac.uk brought to you by CORE Available online at www.sciencedirect.com provided by Elsevier - Publisher Connector ScienceDirect journal homepage: http://www.elsevier.com/locate/euprot Characterisation of potential novel allergens in the fish parasite Anisakis simplex Christiane Kruse Fæste a,∗, Karen R. Jonscher b, Maaike M.W.B. Dooper a, Wolfgang Egge-Jacobsen c, Anders Moen c, Alvaro Daschner d, Eliann Egaas a, Uwe Christians b a Norwegian Veterinary Institute, Oslo, Norway b University of Colorado Denver, Aurora, CO, USA c University of Oslo, Oslo, Norway d Instituto de Investigación Sanitaria-Hospital Universitario de La Princesa, Madrid, Spain article info abstract Article history: The parasitic nematode Anisakis simplex occurs in fish stocks in temperate seas. A. sim- Received 25 November 2013 plex contamination of fish products is unsavoury and a health concern considering human Received in revised form infection with live larvae (anisakiasis) and allergic reactions to anisakid proteins in seafood. 25 June 2014 Protein extracts of A. simplex produce complex band patterns in gel electrophoresis and IgE- Accepted 26 June 2014 immunostaining. In the present study potential allergens have been characterised using Available online 5 July 2014 sera from A. simplex-sensitised patients and proteome data obtained by mass spectrometry. A. simplex proteins were homologous to allergens in other nematodes, insects, and shellfish Keywords: indicating cross-reactivity. Characteristic marker peptides for relevant A. simplex proteins Allergenicity were described. Anisakis simplex © 2014 The Authors. Published by Elsevier B.V. on behalf of European Proteomics Cross-reactivity Association (EuPA). This is an open access article under the CC BY-NC-ND license Immunoblotting (http://creativecommons.org/licenses/by-nc-nd/3.0/). Mass spectrometry Proteomic analysis by antigens from dead larvae can also occur [3–6]. Four clini- 1. Introduction cal allergic manifestations, i.e. gastric, intestinal, ectopic, and systemic, have been associated with A. simplex, and responses Anisakis simplex (herring or whale worm) is the only known might depend on the route of sensitisation [7]. More than 90% fishery product-contaminating parasite eliciting clinical aller- of the anisakiasis cases resulted from infection with a single gic responses [1]. In gastro-allergic anisakiasis allergic larva [2]. The seafood-transmitted zoonotic disease is caused symptoms can arise as secondary immune response after a by the accidental ingestion of third-stage larvae lying encap- previous infestation by live larvae [2]. There is, however, an sulated in the edible tissues of infected fish that is eaten raw on-going discussion regarding whether primary sensitisation or under-cooked [8]. Allergic incidents can, however, also be Abbreviations: A. simplex, Anisakis simplex; m/z, mass-to-charge ratio; NanoLC ESI-MS/MS, nano-liquid chromatography electrospray ionisation tandem mass spectrometry; OD, optical density. ∗ Corresponding author at: Norwegian Veterinary Institute, PO Box 750 Sentrum, N-0106 Oslo, Norway. Tel.: +47 23216232; fax: +47 23216201. E-mail address: [email protected] (C.K. Fæste). http://dx.doi.org/10.1016/j.euprot.2014.06.006 2212-9685/© 2014 The Authors. Published by Elsevier B.V. on behalf of European Proteomics Association (EuPA). This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/3.0/). e u pa open proteomics 4 (2014) 140–155 141 elicited by hidden allergens in processed fish and products allergenicity appeared to be allocated to sequential epitopes thereof [9],byA. simplex protein transmission through the and independent from glycosylation [22]. food chain [7], and by occupational exposure to aerosols [4,10]. Three different groups of potential allergenic proteins orig- Recently, the European Food Safety Authority has concluded inate from A. simplex. Excretory/secretory (ES) proteins are that A. simplex larvae have a considerable allergic potential, expressed by the larvae in high amounts during host infesta- emphasising the need for routine testing of fishery products tion, somatic proteins are constituents of the larvae body, and [6]. cuticular proteins on the larvae’s surface serve as protection The occurrence of anisakid nematodes has been reported from digestion [1]. Together with the different routes of sensi- from all major oceans and seas [11]. The A. simplex life cycle tisation (ingestion, inhalation, mucosal, or cutaneous contact) is complex involving planktonic crustaceans, fish and marine this diverse immunogenic composition is likely a major cause mammals. In fish, the larvae are mainly situated in the vis- for the development of differential clinical responses. ceral cavity; however, a minor proportion may migrate deeply A. simplex protein extracts produce complex band pat- into the fillets [12]. In recent years, an increasing number of terns in gel electrophoresis [23,24]. A number of proteins have anisakiasis cases have been observed [13], and this develop- been recognised as allergens and are registered in the Aller- ment has been connected to the increase of marine mammal gome database [25]. Among these are known proteins such populations, a more globalised cuisine, faster cooking prac- as secreted proteinase inhibitors (Ani s1, Ani s 4) and somatic tices (e.g. microwaving), the trend to avoid overcooked food paramyosin (Ani s 2) and tropomyosin (Ani s 3), but also a num- for vitamin preservation, and a generally higher consumption ber of un-characterised proteins, whose functions have not yet of fish for health reasons [1]. Over 90% of the anisakiasis cases been established (Ani s 7, Ani s 10–12, Ani s 24) (Table 1). world-wide are reported from Japan, and most others occur in The complex binding pattern of A. simplex proteins Spain, Italy, the USA (Hawaii), the Netherlands, and Germany observed in IgE immunoblots suggests that the description of in regions, where traditionally raw or undercooked fish dishes allergens is incomplete. Indeed, several new allergens have such as sushi and sashimi, pickled anchovies, lomi-lomi, and been detected by using high-resolution protein purification salted herring are consumed [5]. methods and immunoscreening of protein-expressing cDNA In Norway, a country with proportionally high per-capita libraries or phage display systems constructed from A. simplex fish consumption, the number of anisakiasis incidents is larvae [26]. low, possibly because mainly cooked or fried fish prod- In the present study a different approach using mass ucts are eaten [14]. The demographic IgE sensitisation spectrometry-based proteomic analysis was attempted to to A. simplex proteins is less than 2%, a relatively low characterise A. simplex proteins and to identify potential novel value as compared to about 12% in Japan and Spain. allergens. Immunoblot analyses using crude A. simplex extracts have shown very heterogeneous and individually different IgE compositions between patients and populations [15–17], and 2. Materials and methods genetic predisposition is thought to be a possible cause for the observed differences in disease susceptibility [18]. The 2.1. Patients prevalence of anti-A. simplex IgE in a population may also result from subclinical and undiagnosed anisakiasis, cross- Sera from two different patient populations were obtained reactivity with other nematodes or insects due to homol- including 14 Norwegian and 13 Spanish patients with IgE ogous allergens, or cross-reactions with carbohydrate- and against A. simplex and positive skin prick tests (Table 2). The phosphorylcholine-groups on post-translationally modified Norwegian patients were originally recruited by newspaper proteins [19]. advertisements for a study on shellfish allergy; however, they Since positive IgE values are not a reliable marker for aller- were also tested for cross-reactivity to A. simplex and mite. gic reactivity, the discrimination between symptomatic and Skin prick testing (SPT) was performed with total PBS extract asymptomatic individuals by other than serodiagnostic analy- of A. simplex 3rd stage larvae retrieved from contaminated ses is important for the determination of A. simplex allergy [15]. Blue Withing (Micromesistius poutassou) caught in the Nor- Established methods include skin prick testing (SPT), basophil wegian Sea. Positive responders were studied further using activation (BAT) measurement, and oral challenge. How- a basophile activation test, ImmunoCapTM (Phadia, Uppsala, ever, even the outcome of double-blind placebo-controlled Sweden) analyses, and immunoblotting. Specific IgE levels to food challenges (DBPCFC) is influenced by patient recruit- A. simplex (p4, Anisakis spp.), shrimp (f24, Pandalus borealis, ment and choice of the A. simplex challenge material [5,20]. Penaeus monodon, Metapenaeopsis barbata, Metapenaus joyneri), Whereas some studies reported that sensitised patients tol- and mite (d1, Dermatophagoides pteronyssinus) were measured. erated deep-frozen or well-cooked fish with anisakid larvae, The sera were stored in conformity with Norwegian law in a others have described patients getting allergic symptoms from registered diagnostic bio-bank. heat-processed contaminated fish. The Spanish patients were admitted to clinical treat- In addition to the great variability in responsiveness ment either because of anisakiasis or allergy to A. simplex between individuals, differences
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