Skip to main content
SpringerLink
Log in

Allergenicity of tropomyosin of shrimp (Litopenaeus vannamei) and clam (Ruditapes philippinarum) is higher than that of fish (Larimichthys crocea) via in vitro and in vivo assessment

  • Original Paper
  • Published:
European Food Research and Technology Aims and scope Submit manuscript

Abstract

Tropomyosin (TM), acting as heat-stable protein, has a high homology of amino acid sequences with different sensitizations. Fish belongs to vertebrate and its TM owns less allergenicity, whereas shrimp and clam belong to invertebrate and their TM are major allergens. Moreover, the allergenicity of TM might be altered during food processing. Therefore, shrimp-TM was administered intraperitoneally to BALB/c mice to establish an allergic mouse model, to evaluate the elicitation ability of these three proteins, while a mediator-releasing RBL cell line was used to estimate the variation in the stimulation abilities. The results showed that shrimp-TM owned stronger ability in the elicitation of the anaphylactic reactivity as well as in the IgE-mediated the RBL cell line. In comparison with shrimp-TM, clam-TM showed a similar allergic reaction and T-helper 2 (Th2)-based responses from spleen cells and mediums produced by RBL cell line, while fish-TM exhibited a weaker anaphylactic reactivity based on a mouse model and produced fewer active mediums based on cell model. Furthermore, raw and boiled TM did not exhibit a significant difference in allergic reactions and the capacity of degranulation. These results indicated that shrimp-TM owned stronger stimulation ability based on allergic mouse compared with fish-TM and clam-TM, which could supply information for clinical and anaphylaxis of TM in the stages of sensitization and simulation deserve further consideration.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Unterberger C, Luber F, Demmel A, Grunwald K, Huber I, Engel KH, Busch U (2014) Simultaneous detection of allergenic fish, cephalopods and shellfish in food by multiplex ligation-dependent probe amplification. Eur Food Res Technol 239:559–566

    Article  CAS  Google Scholar 

  2. Lu M, Jin Y, Cerny R, Ballmer-Weber B, Goodman RE (2018) Combining 2-DE immunoblots and mass spectrometry to identify putative soybean (Glycine max) allergens. Food Chem Toxicol 116:207–215

    Article  CAS  Google Scholar 

  3. Shiomi K (2010) Current knowledge on molecular features of seafood allergens. Shokuhin Eiseigaku Zasshi 51:139–152

    Article  CAS  Google Scholar 

  4. Rolland JM, Varese NP, Abramovitch JB, Anania J, Nugraha R, Kamath S, Hazard A, Lopata AL, O’Hehir RE (2018) Effect of heat processing on IgE reactivity and cross-reactivity of tropomyosin and other allergens of asia-pacific mollusc species: identification of novel sydney rock oyster tropomyosin Sac g 1. Mol Nutr Food Res. https://doi.org/10.1002/mnfr.201800148

    Article  PubMed  PubMed Central  Google Scholar 

  5. Faber MA, Pascal M, El Kharbouchi O, Sabato V, Hagendorens MM, Decuyper II, Bridts CH, Ebo DG (2017) Shellfish allergens: tropomyosin and beyond. Allergy 72:842–848

    Article  CAS  Google Scholar 

  6. Hu MJ, Liu GY, Yang Y, Pan TM, Liu YX, Sun LC, Cao MJ, Liu GM (2017) Cloning, expression, and the effects of processing on sarcoplasmic-calcium-binding protein: an important allergen in mud crab. J Agric Food Chem 65:6247–6257

    Article  CAS  Google Scholar 

  7. Peixoto S, Monteiro T, Carvalho M, Santos M, Matos C, Bartolome B, Barahona A, Labrador-Horrillo M, Quaresma M (2017) Tropomyosin from vertebrates as an allergen: case report. Allergy 72:534

    Article  Google Scholar 

  8. Abramovitch J, Kamath S, Varese N, Zubrinich C, Lopata A, O’Hehir R, Rolland J (2014) Characterisation of IgE cross-reactivity between Australasian crustacean species in shellfish-allergic patients. Allergy 69:379–380

    Google Scholar 

  9. Joana Cosme ASS, Manuel PB (2016) Tropomyosin as a panallegen: review. Rev Por t Im unoalerg ologia 24:143–153

    Google Scholar 

  10. Liu GM, Cheng H, Nesbit JB, Su WJ, Cao MJ, Maleki SJ (2010) Effects of boiling on the IgE-binding properties of tropomyosin of shrimp (Litopenaeus vannamei). J Food Sci 75:T1–T5

    Article  CAS  Google Scholar 

  11. Mattison CP, Desormeaux WA, Wasserman RL, Yoshioka-Tarver M, Condon B, Grimm CC (2014) Decreased immunoglobulin E (IgE) binding to cashew allergens following sodium sulfite treatment and heating. J Agric Food Chem 62:6746–6755

    Article  CAS  Google Scholar 

  12. Fu TJ, Maks N (2013) Impact of thermal processing on ELISA detection of peanut allergens. J Agric Food Chem 61:5649–5658

    Article  CAS  Google Scholar 

  13. Cai Q, Zhang WJ, Zhu QQ, Chen Q (2016) Influence of heat treatment on the structure and core IgE-binding epitopes of rAra h 2.02. Food Chem 202:404–408

    Article  CAS  Google Scholar 

  14. Kamath SD, Thomassen M, Nugraha R, Aasmoe L, Bang BE, Lopata AL (2016) IgE sensitization to crab allergens among processing workers due to inhalational exposure: an allergenomic approach. Allergy 71:15–16

    Article  Google Scholar 

  15. Misnan R, Salahudin Abd Aziz N, Mohamad Yadzir ZH, Bakhtiar F, Abdullah N, Murad S (2016) Impacts of thermal treatments on major and minor allergens of sea snail, Cerithidea obtusa (Obtuse Horn Shell). Iran J Allergy Asthma Immunol 15:309–316

    PubMed  Google Scholar 

  16. Kamath SD, Abdel Rahman AM, Komoda T, Lopata AL (2013) Impact of heat processing on the detection of the major shellfish allergen tropomyosin in crustaceans and molluscs using specific monoclonal antibodies. Food Chem 141:4031–4039

    Article  CAS  Google Scholar 

  17. Zhang W, Zhu Q, Zhang T, Cai Q, Chen Q (2016) Thermal processing effects on peanut allergen Ara h 2 allergenicity in mice and its antigenic epitope structure. Food Chem 212:657–662

    Article  Google Scholar 

  18. Fang L, Li G, Gu R, Cai M, Lu J (2018) Influence of thermal treatment on the characteristics of major oyster allergen Cra g 1 (tropomyosin). J Sci Food Agric 98:5322–5328

    Article  CAS  Google Scholar 

  19. Carnes J, Ferrer A, Huertas AJ, Andreu C, Larramendi CH, Fernandez-Caldas E (2007) The use of raw or boiled crustacean extracts for the diagnosis of seafood allergic individuals. Ann Allerg Asthma Im 98:349–354

    Article  CAS  Google Scholar 

  20. Prester L (2016) Seafood allergy, toxicity, and intolerance: a review. J Am Coll Nutr 35:271–283

    Article  CAS  Google Scholar 

  21. Charcosset A, Adel-Patient K, Dupont C, Bernard H (2016) Assessment of IgE and IgG4 binding capacities of cow’s milk proteins selectively altered by proteases. J Agric Food Chem 64:3394–3404

    Article  CAS  Google Scholar 

  22. Sicherer SH, Sampson HA (2018) Food allergy: a review and update on epidemiology, pathogenesis, diagnosis, prevention, and management. J Allergy Clin Immunol 141:41–58

    Article  CAS  Google Scholar 

  23. Lv L, Lin H, Li Z, Yuan F, Gao Q, Ma J (2016) Effect of 4-hydroxy-2-nonenal treatment on the IgE binding capacity and structure of shrimp (Metapenaeus ensis) tropomyosin. Food Chem 212:313–322

    Article  CAS  Google Scholar 

  24. Pablos-Tanarro A, Lozano-Ojalvo D, Molina E, Lopez-Fandino R (2018) Assessment of the allergenic potential of the main egg white proteins in BALB/c mice. J Agric Food Chem 66:2970–2976

    Article  CAS  Google Scholar 

  25. Lv L, Lin H, Li Z, Ahmed I, Mi N, Chen G (2018) Allergenicity of acrolein-treated shrimp tropomyosin evaluated using RBL-2H3 cell and mouse model. J Sci Food Agr 98:4374–4378

    Article  CAS  Google Scholar 

  26. Katayama S, Yamaguchi D, Suzuki Y, Athamneh AMA, Mitani T, Satoh R, Teshima R, Mine Y, Nakamura S (2018) Oral immunotherapy with a phosphorylated hypoallergenic allergen ameliorates allergic responses more effectively than intact allergen in a murine model of buckwheat allergy. Mol Nutr Food Res 62:e1800303

    Article  Google Scholar 

  27. Liu G, Hu M, Sun LC, Han X, Liu Q, Alcocer M, Fei D, Cao MJ, Liu GM (2017) Allergenicity and oral tolerance of enzymatic cross-linked tropomyosin evaluated using cell and mouse models. J Agric Food Chem 65:2205–2213

    Article  CAS  Google Scholar 

  28. Rupa P, Schnarr L, Mine Y (2015) Effect of heat denaturation of egg white proteins ovalbumin and ovomucoid on CD4(+) T cell cytokine production and human mast cell histamine production. J Funct Foods 18:28–34

    Article  CAS  Google Scholar 

  29. Song Y, Li Z, Gao Q, Pavase TR, Lin H (2016) Effect of malonaldehyde cross-linking on the ability of shrimp tropomyosin to elicit the release of inflammatory mediators and cytokines from activated RBL-2H3 cells. J Sci Food Agric 96:4263–4267

    Article  CAS  Google Scholar 

  30. Kumar S, Sharma A, Gupta RK, Verma AK, Dwivedi PD (2018) Allergenicity assessment of Buchanania lanzan protein extract in Balb/c mice. Int Immunopharmacol 63:170–182

    Article  CAS  Google Scholar 

  31. Wu W, Wu XJ, Hu YF (2010) Structural modification of soy protein by the lipid peroxidation product acrolein. Food Sci Technol 43:133–140

    CAS  Google Scholar 

  32. Tao B, Bernardo K, Eldi P, Chegeni N, Wiese M, Colella A, Kral A, Hayball J, Smith W, Forsyth K, Chataway T (2016) Extended boiling of peanut progressively reduces IgE allergenicity while retaining T cell reactivity. Clin Exp Allergy 46:1004–1014

    Article  CAS  Google Scholar 

  33. Han XY, Yang H, Rao ST, Liu GY, Hu MJ, Zeng BC, Cao MJ, Liu GM (2018) The Maillard Reaction Reduced the Sensitization of Tropomyosin and Arginine Kinase from Scylla paramamosain, Simultaneously. J Agric Food Chem 66:2934–2943

    Article  CAS  Google Scholar 

  34. Long FY, Yang X, Wang RR, Hu XS, Chen F (2015) Effects of combined high pressure and thermal treatments on the allergenic potential of shrimp (Litopenaeus vannamei) tropomyosin in a mouse model of allergy. Innov Food Sci Emerg 29:119–124

    Article  CAS  Google Scholar 

  35. Wai CY, Leung NY, Leung PS, Chu KH (2016) T cell epitope immunotherapy ameliorates allergic responses in a murine model of shrimp allergy. Clin Exp Allergy 46:491–503

    Article  CAS  Google Scholar 

  36. Larsen JM, Bogh KL (2018) Animal models of allergen-specific immunotherapy in food allergy: overview and opportunities. Clin Exp Allergy 48:1255–1274

    Article  Google Scholar 

Download references

Acknowledgements

The authors would like to express their sincere thanks to the National Natural Science Foundation of China (31771892) and Fundamental Research Funds for the Central Universities (201762004) for supporting the research study.

Author information

Authors and Affiliations

  1. Food Safety Lab, College of Food Science and Engineering, Ocean University of China, No. 5, Yushan Road, Qingdao, 266003, Shandong, People’s Republic of China

    Lili Xu, Lirui Sun, Hong Lin, Ahmed Ishfaq & Zhenxing Li

Authors
  1. Lili Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lirui Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hong Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ahmed Ishfaq
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Zhenxing Li
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zhenxing Li.

Ethics declarations

Conflict of interest

The authors declare that there is no conflict of interest related to this paper.

Compliance with ethics requirements

All experiments conformed to the established guidelines for the Ethical Committee of Experimental Animal Care at the Ocean University of China.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Xu, L., Sun, L., Lin, H. et al. Allergenicity of tropomyosin of shrimp (Litopenaeus vannamei) and clam (Ruditapes philippinarum) is higher than that of fish (Larimichthys crocea) via in vitro and in vivo assessment. Eur Food Res Technol 246, 103–112 (2020). https://doi.org/10.1007/s00217-019-03402-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00217-019-03402-0

Keywords

Search

Navigation