Effect of acid and in vitro digestion on conformation and IgE-binding capacity of major oyster allergen Cra g 1 (tropomyosin)

Main Article Content

Jiangtao Zhang
Wenying Liu
Lei Fang
Ruizeng Gu
Jun Lu
Guoming Li

Keywords

Cra g1, Acid, SGF, SIF, Conformation, IgE-binding

Abstract

Introduction and Objectives: The production and consumption of oysters is increasing annually because it can provide essential nutrients and benefit for human health, leading to frequent occurrence of severe allergic reactions observed in sensitized individuals. The aim of the present study was to investigate the effects of acid and protease treatment on the conformation and IgE-binding capacity of recombinant Crassostrea gigas tropomyosin (Cra g 1).


Results: Under acidic conditions, Cra g 1 did not undergo degradation, however, the changes obvious in the intensity of CD signal and ANS-binding fluorescence were observed, which was associated with a decrease in antibody reactivity. In simulated gastrointestinal fluid (SGF) and simulated intestinal fluid (SIF) digestion system, acid-treated Cra g 1 was relatively resistant to digestion, but the degradative patterns were very different. Moreover, owing to alterations of secondary structure and hydrophobic surface of the protein during digestive processing, antigenicity of acid-induced Cra g 1 reduced in SGF while it increased significantly in SIF.


Conclusion: To our knowledge, this is the first study reporting that antigenicity of acid-treated oyster tropomyosin increased after SIF digestion. These results revealed that treatment with acid and pepsin, rather than trypsin, was an effective way of reducing IgE-binding capacity of tropomyosin from oyster.

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References

1. Dalal I, Binson I, Reifen R, Amitai Z, Shohat T, Rahmani S, et al. Food allergy is a matter of geography after all: sesame as a major cause of severe IgE-mediated food allergic reactions among infants and young children in Israel. Allergy. 2002;57:362-5.

2. Kubota H, Kobayashi A, Kobayashi Y, Shiomi K, Hamada-Sato N. Reduction in IgE reactivity of Pacific mackerel parvalbumin by heat treatment. Food Chem. 2016;206:78-84.

3. Leung PSC, Chu KH. cDNA cloning and molecular identification of the major oyster allergen from the Pacific oyster Crassostrea gigas. Clin Exp Allergy. 2001;31:1287-94.

4. Ai E, Shoichiro I, Kazuo S. Tropomyosins in gastropods and bivalves: identification as major allergens and amino acid sequence features. Food Chem. 2009;114:634-41.

5. Bauermeister K, Wangorsch A, Garoffo LP, Reuter A, Conti A, Taylor SL, et al. Generation of a comprehensive panel of crustacean allergens from the North Sea Shrimp Crangon crangon. Mol Immunol. 2011;48:1983-92.

6. Lopata AL, Kleine-Tebbe J, Kamath SD. Allergens and molecular diagnostics of shellfish allergy. Allergo J Int. 2016;25:24-32.

7. Faber MA, Pascal M, Kharbouchi OE, Sabato V, Hagendorens MM, Decuyper II, et al. Shellfish allergens: tropomyosin and beyond. Allergy. 2017;72:842.

8. Long F, Yang X, Wang R, Hu X, Chen F. Effects of combined high pressure and thermal treatments on the allergenic potential of shrimp (Litopenaeus vannamei) tropomyosin in a mouse model of allergy. Innovative Food Sci Emerg Technol. 2015;29:119-24.

9. Sano T, Ohno T, Otsukafuchino H, Matsumoto JJ, Tsuchiya T. Carp natural actomyosin: thermal denaturation mechanism. Journal of Food Science. 2010;59:1002-8.

10. Chu KH, Wong SH, Leung PS. Tropomyosin is the major mollusk allergen: reverse transcriptase polymerase chain reaction, expression and IgE reactivity. Marine Biotechnol. 2000;2:499.

11. Leung NYH, Wai CYY, Shu SA, Wang J, Kenny TP, Chu KH, et al. Current immunological and molecular biological perspectives on seafood allergy: a comprehensive review. Clin Rev Allergy Immunol. 2014;46:180-97.

12. Ishikawa M, Shimakura K, Nagashima Y, Shiomi K. Isolation and properties of allergenic proteins in the oyster Crassostrea gigas. Fisheries Sci. 2011;63:610-4.

13. Yadzir ZHM, Misnan R, Bakhtiar F, Abdullah N, Murad S. Tropomyosin, the major tropical oyster Crassostrea belcheri allergen and effect of cooking on its allergenicity. Allergy Asthma Clin Immunol. 2015;11:30.

14. Foh MBK, Xia W, Amadou I, Jiang Q. Influence of pH shift on functional properties of protein isolated of tilapia (Oreochromis niloticus) muscles and of soy protein isolate. Food Bioprocess Technol. 2012;5:2192-200.

15. Bernardi ML, Picone D, Tuppo L, Giangrieco I, Petrella G, Palazzo P, et al. Physico-chemical features of the environment affect the protein conformation and the immunoglobulin E reactivity of kiwellin (Act d 5). Clin Exp Allergy J Br Soc Allergy Clin Immunol. 2010;40:1819-26.

16. Nolsøe H, Undeland I. The acid and alkaline solubilization process for the isolation of muscle proteins: state of the art. Food
Bioprocess Technol. 2009;2:1-27.

17. Lasekan A, Cao H, Maleki S, Nayak B. Shrimp tropomyosin retains antibody reactivity after exposure to acidic condition. J Sci Food Agric. 2017;97.

18. Fujita S, Shimizu Y, Kishimura H, Watanabe K, Hara A, Saekia H. In vitro digestion of major allergen in salmon roe and its peptide portion with proteolytic resistance. Food Chem. 2012;130:644-50.

19. Astwood JD, Leach JN, Fuchs RL. Stability of food allergens to digestion in vitro. Nat Biotechnol. 1996;14:1269-73.

20. Tong-Jen FU. Digestion stability as a criterion for protein allergenicity assessment. Ann NY Acad Sci. 2010;964:99-110.

21. Yagami T, Haishima Y, Nakamura A, Osuna H, Ikezawa Z. Digestibility of allergens extracted from natural rubber latex and vegetable foods. J Allergy Clin Immunol. 2000;106:752-62.

22. B. o. Trustees, Simulated gastric fluid, TS and simulated intestinal fluid, TS. The United States Pharmacopeia 23, The National Formulary 18 2053, (1995); published online Epub1995.

23. Zhou NE, Kay CM, Hodges RS. Synthetic model proteins. Positional effects of interchain hydrophobic interactions on stability of two-stranded alpha-helical coiled-coils. J Biol Chem. 1992;267:2664-70.

24. Lin H, Li Z, Lin H, Song Y, Lv L, Hao Z. Effect of pH shifts on IgEbinding capacity and conformational structure of tropomyosin from short-neck clam (Ruditapes philippinarum). Food Chem. 2015;188:248-55.

25. Mikita CP, Padlan EA. Why is there a greater incidence of allergy to the tropomyosin of certain animals than to that of others? Med Hypotheses. 2007;69:1070-3.

26. Huang YY, Liu GM, Cai QF, Weng WY, Maleki SJ, Su WJ, et al. Stability of major allergen tropomyosin and other food proteins of mud crab (Scylla serrata) by in vitro gastrointestinal digestion. Food Chem Toxicol. 2010;48:1196-201.

27. J. F. Kennedy, M. M. He, A.J. Barrett, N.D. Rawlings, J.F.Woessner (Eds.), Handbook of Proteolytic Enzymes, Second Edition (2 Volumes) Elsevier Academic Press, London, UK, 2004(xxxv+2140 pp., £274.95, ISBN 0-12-079610-4). Carbohydrate Polymers 60, 127-127 (2005).

28. Fang L, Li G, Gu R, et al. Influence of thermal treatment on the characteristics of major oyster allergen Cra g 1 (Tropomyosin). J Sci Food Agric. 2018;98(14):5322-8.

29. Lv L, Lin H, Li Z, Ahmed I, Chen G. Determining the effect of malondialdehyde on the IgE-binding capacity of shrimp tropomyosin upon in vitro digestion. J Sci Food Agric. 2017;97:4588.