Abstract
Sarcoplasmic calcium-binding protein (SCP) is an EF-hand Ca2+-binding protein recently identified as a new crustacean allergen. Some EF-hand Ca2+-binding allergens, such as parvalbumin (fish allergen) and Bet v 4 (birch pollen allergen), have been shown to contain conformational-type IgE epitopes associated with the Ca2+-chelating. This study was performed to clarify the relationships between IgE reactivity and structure of the black tiger shrimp SCP. When analyzed by ELISA in the absence and presence of EGTA, the IgE reactivity of the black tiger shrimp SCP was found to be considerably reduced by Ca2+-depletion. Furthermore, circular dichroism spectral data showed a conformational difference between Ca2+-bound and Ca2+-depleted forms of the black tiger shrimp SCP. On the other hand, the synthetic 18 peptides spanning the entire amino acid sequence of the black tiger shrimp SCP were all assessed to have little IgE-binding ability by ELISA. Our results demonstrate that the IgE reactivity of the black tiger shrimp SCP is attributable mostly to conformational-type IgE epitopes, at least part of which is maintained by Ca2+-chelating.
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Shanti KN, Martin BM, Nagpal S, Metcalfe DD, Subba Rao PV (1993) Identification of tropomyosin as the major shrimp allergen and characterization of its IgE-binding epitopes. J Immunol 151:5354–5363
Daul CB, Slattery M, Reese G, Lehrer SB (1994) Identification of the major brown shrimp (Penaeus aztecus) allergen as the muscle protein tropomyosin. Int Arch Allergy Immunol 105:49–55
Leung PSC, Chu KH, Chow WK, Ansari A, Bandea CI, Kwan HS, Nagy SM, Gershwin ME (1994) Cloning, expression, and primary structure of Metapenaeus ensis tropomyosin, the major heat-stable shrimp allergen. J Allergy Clin Immunol 94:882–890
Motoyama K, Suma Y, Ishizaki S, Nagashima Y, Shiomi K (2007) Molecular cloning of tropomyosins identified as allergens in six species of crustaceans. J Agric Food Chem 55:985–991
Leung PSC, Chen YS, Mykles DL, Chow WK, Li CP, Chu KH (1998) Molecular identification of the lobster muscle protein tropomyosin, as a seafood allergen. Mol Mar Biol Biotechnol 7:12–20
Leung PSC, Chen YS, Gershwin ME, Wong SH, Kwan HS, Chu KH (1998) Identification and molecular characterization of Charybdis feriatus tropomyosin, the major crab allergen. J Allergy Clin Immunol 102:847–852
Suma Y, Ishizaki S, Nagashima Y, Lu Y, Ushio H, Shiomi K (2007) Comparative analysis of barnacle tropomyosin: divergence from decapod tropomyosins and role as a potential allergen. Comp Biochem Physiol B 147:230–236
Motoyama K, Suma Y, Ishizaki S, Nagashima Y, Lu Y, Ushio H, Shiomi K (2008) Identification of tropomyosins as major allergens in Antarctic krill and mantis shrimp and their amino acid sequence characteristics. Mar Biotechnol 10:709–718
Nakano S, Yoshimura T, Yamada T (2008) Reactivity of shrimp allergy-related IgE antibodies to krill tropomyosin. Int Arch Allergy Immunol 145:175–181
Yu CJ, Lin YF, Chiang BL, Chow LP (2003) Proteomics and immunological analysis of a novel shrimp allergen, Pen m 2. J Immunol 170:445–453
García-Orozco KD, Aispuro-Hernández E, Yepiz-Plascencia G, Calderón-de-la-Barca AM, Sotelo-Mundo RR (2007) Molecular characterization of arginine kinase, an allergen from the shrimp Litopenaeus vannamei. Int Arch Allergy Immunol 144:23–28
Shen Y, Cao MJ, Cai QF, Su WJ, Yu HL, Ruan WW, Liu GM (2011) Purification, cloning, expression and immunological analysis of Scylla serrata arginine kinase, the crab allergen. J Sci Food Agric 91:1326–1335
Shiomi K, Sato Y, Hamamoto S, Mita H, Shimakura K (2008) Sarcoplasmic calcium-binding protein: identification as a new allergen of the black tiger shrimp Penaeus monodon. Int Arch Allergy Immunol 146:91–98
Ayuso R, Grishina G, Ibáñez MD, Blanco C, Carrillo T, Bencharitiwong R, Sánchez S, Nowak-Wegrzyn A, Sampson HA (2009) Sarcoplasmic calcium-binding protein is an EF-hand-type protein identified as a new shrimp allergen. J Allergy Clin Immunol 124:114–120
Ayuso R, Grishina G, Bardina L, Carrillo T, Blanco C, Ibáñez MD, Sampson HA, Beyer K (2008) Myosin light chain is a novel shrimp allergen, Lit v 3. J Allergy Clin Immunol 122:795–802
Piboonpocanun S, Jirapongsananuruk O, Tipayanon T, Boonchoo S, Goodman RE (2011) Identification of hemocyanin as a novel non-cross-reactive allergen from the giant freshwater shrimp Macrobrachium rosenbergii. Mol Nutr Food Res 55:1492–1498
Lehrer SB, Ayuso R, Reese G (2003) Seafood allergy and allergens: a review. Mar Biotechnol 5:339–348
Wild LG, Lehrer SB (2005) Fish and shellfish allergy. Curr Allergy Asthma Rep 5:74–79
Gao Y, Gillen CM, Wheatly MG (2006) Molecular characterization of the sarcoplasmic calcium-binding protein (SCP) from crayfish Procambarus clarkii. Comp Biochem Physiol B 144:478–487
Cook WJ, Ealick SE, Babu YS, Cox JA, Vijay-Kumar S (1991) Three-dimensional structure of a sarcoplasmic calcium-binding protein from Nereis diversicolor. J Biol Chem 266:652–656
Hermann A, Cox JA (1995) Sarcoplasmic calcium-binding protein. Comp Biochem Physiol B 111:337–345
Swoboda I, Bugajska-Schretter A, Verdino P, Keller W, Sperr WR, Valent P, Valenta R, Spitzauer S (2002) Recombinant carp parvalbumin, the major cross-reactive fish allergen: a tool for diagnosis and therapy of fish allergy. J Immunol 168:4576–4584
Tomura S, Ishizaki S, Nagashima Y, Shiomi K (2008) Reduction in the IgE reactivity of Pacific mackerel parvalbumin by mutations at Ca2+-binding sites. Fish Sci 74:411–417
Ma Y, Griesmeier U, Susani M, Radauer C, Briza P, Erler A, Bublin M, Alessandri S, Himly M, Vàzquez-Cortés S, De Arellano IRR, Vassilopoulou E, Saxoni-Papageorgiou P, Knulst AC, Fernández-Rivas M, Hoffmann-Sommergruber K, Breiteneder H (2008) Comparison of natural and recombinant forms of the major fish allergen parvalbumin from cod and carp. Mol Nutr Food Res 52:S196–S207
Elsayed S, Apold J (1983) Immunochemical analysis of cod fish allergen M: locations of the immunoglobulin binding sites as demonstrated by the native and synthetic peptides. Allergy 38:449–459
Yoshida S, Ichimura A, Shiomi K (2008) Elucidation of a major IgE epitope of Pacific mackerel parvalbumin. Food Chem 111:857–861
Lowry OH, Rosebrough AL, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275
Hamada Y, Tanaka H, Sato A, Ishizaki S, Nagashima Y, Shiomi K (2004) Expression and evaluation of IgE-binding capacity of recombinant Pacific mackerel parvalbumin. Allergol Int 53:271–278
Engel E, Richter K, Obermeyer G, Briza P, Kungl AJ, Simon B, Auer M, Ebner C, Rheinberger HJ, Breitenbach M, Ferreira F (1997) Immunological and biological properties of Bet v 4, a novel birch pollen allergen with two EF-hand calcium-binding domains. J Biol Chem 272:28630–28637
Suphioglu C, Ferreira F, Knox RB (1997) Molecular cloning and immunological characterisation of Cyn d 7, a novel calcium-binding allergen from Bermuda grass pollen. FEBS Lett 402:167–172
Ledesma A, Gonzalez E, Pascual CY, Quiralte J, Villalba M, Rodriguez R (2002) Are Ca2+-binding motifs involved in the immunoglobin E-binding of allergens? Olive pollen allergens as model of study. Clin Exp Allergy 32:1476–1483
Kretsinger RH, Nockolds CE (1973) Carp muscle calcium-binding protein. II. Structure determination and general description. J Biol Chem 248:3313–3326
Declercq JP, Tinant B, Parello J, Rambaud J (1991) Ionic interactions with parvalbumins. Crystal structure determination of pike 4.10 parvalbumin in four different ionic environments. J Mol Biol 220:1017–1039
Swoboda I, Bugajska-Schretter A, Linhart B, Verdino P, Keller W, Schulmeister U, Sperr WR, Valent P, Peltre G, Quirce S, Douladiris N, Papadopoulos NG, Valenta R, Spitzauer S (2007) A recombinant hypoallergenic parvalbumin mutant for immunotherapy of IgE-mediated fish allergy. J Immunol 178:6290–6296
Hulo N, Bairoch A, Bulliard V, Cerutti L, De Castro E, Langendijk-Genevaux PS, Pagni M, Sigrist CJA (2006) The PROSITE database. Nucleic Acids Res 34:D227–D230
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This study was partly supported by a Grant-in-Aid for Scientific Research from the Ministry of Education, Science, Sports and Culture of Japan and a grant from the Ministry of Health, Labour and Welfare of Japan.
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Morii, A., Mita, H., Ishizaki, S. et al. Importance of conformation for the IgE reactivity of sarcoplasmic calcium-binding protein from the black tiger shrimp Penaeus monodon . Eur Food Res Technol 236, 165–170 (2013). https://doi.org/10.1007/s00217-012-1867-8
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DOI: https://doi.org/10.1007/s00217-012-1867-8