journal article·2024-12-25Open access

Identification of Allergenic Tropomyosins with Known and Unknown Sequences in Seafood Products

Marta Godlewska, Piotr Minkiewicz, Małgorzata Darewicz, Anna Iwaniak

Applied Sciences· Volume 15· Issue 1

Abstract

Invertebrate tropomyosins belong to the key food allergens. Several peptides likely to be released during proteolysis can be found in many sequences of proteins from this family. The aim of the present study was to evaluate the possibility of identifying tropomyosins with known and unknown amino acid sequences in unheated, boiled and fried seafoods. The workflow included in silico proteolysis simulation of tropomyosin sequences and analysis of the distribution of resulting peptides among proteins. The experiment entailed the proteolysis of unheated, boiled and fried products, containing crustaceans or mollusks, and the identification of resulting peptides using LC-MS/MS. Finally, taxonomic lineages of identified peptides were determined. Predicted peptides were identified in unheated samples. The boiling of seafoods resulted in an increase in the length of peptides containing predicted sequences. Some peptides from the boiled samples contained entire linear epitopes. The prediction of tropomyosin cleavage sites failed in the case of fried products. Peptides from the unheated and boiled samples were attributed to crustacean, arthropod or molluscan tropomyosins. In turn, peptides from the fried samples possessed inconclusive taxonomic lineages. Our results show that bioinformatics analysis (especially using Unipept program) may be a viable tool supporting LC-MS/MS experiments aimed at the detection of allergens.
Source: crossref · Quality: baseline

Research context

OpenAlex topics: Identification and Quantification in Food · Meat and Animal Product Quality · Food Allergy and Anaphylaxis Research

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

Affiliations

Department of Food Biochemistry, University of Warmia and Mazury in Olsztyn, Plac Cieszyński 1, 10-726 Olsztyn, Poland

Funding

Minister of Science under the Regional Initiative of Excellence Program

References (96)

Show source-provided references
1. Seafood allergy: A comprehensive review of fish and shellfish allergens10.1016/j.molimm.2018.04.008 ↗
2. An overview of tropomyosin as an important seafood allergen: Structure, cross-reactivity, epitopes, allergenicity, and processing modifications10.1111/1541-4337.12889 ↗
3. Giannetti, A., Pession, A., Bettini, I., Ricci, G., Giannì, G., and Caffarelli, C. (2023). IgE mediated shellfish allergy in children—A review. Nutrients, 15.10.3390/nu15143112 ↗
4. Giovannini, M., Beken, B., Buyuktiryaki, B., Barni, S., Liccioli, G., Sarti, L., Lodi, L., Pontone, M., Bartha, I., and Mori, F. (2023). IgE-mediated shellfish allergy in children. Nutrients, 15.10.3390/nu15122714 ↗
5. Mollusk allergy: Not simply cross-reactivity with crustacean allergens10.1111/all.15377 ↗
6. Food allergen families common to different arthropods (mites, insects, crustaceans), mollusks and nematods: Cross-reactivity and potential cross-allergenicity10.1016/j.reval.2018.10.008 ↗
7. Packi, K., Rudek, A., Matysiak, J., Klimczak, S., Matuszewska, E., Rzetecka, N., and Matysiak, J. (2023). Food allergies and parasites in children. Foods, 12.10.3390/foods12132465 ↗
8. Assessment of crustacean allergen detection methods: Cross reactivity with edible insect samples10.1080/19440049.2023.2283770 ↗
9. Shellfish allergens: Tropomyosin and beyond10.1111/all.13115 ↗
10. Comprehending the allergen repertoire of shrimp for precision molecular diagnosis of shrimp allergy10.1111/all.15370 ↗
11. Commercial shellfish skin prick test extracts show critical variability in allergen repertoire10.1111/all.15853 ↗
12. The occurrence of sequences identical with epitopes from the allergen Pen a 1.0102 among food and non-food proteins10.1515/pjfns-2015-0002 ↗
13. Cross-reactive epitopes and their role in food allergy10.1016/j.jaci.2022.12.827 ↗
14. Characterization of physicochemical and immunogenic properties of allergenic proteins altered by food processing: A review10.26599/FSHW.2022.9250095 ↗
15. Isolation and characterization of heat-stable allergens from shrimp (Penaeus indicus)10.1016/0091-6749(89)90474-0 ↗
16. Cloning, expression, and primary structure of Metapenaeus ensis tropomyosin, the major heat-stable shrimp allergen10.1016/0091-6749(94)90156-2 ↗
17. Contribution of structural reversibility to the heat stability of the tropomyosin shrimp allergen10.1271/bbb.120887 ↗
18. Thermal induced the structural alterations, increased IgG/IgE binding capacity and reduced immunodetection recovery of tropomyosin from shrimp (Litopenaeus vannamei)10.1016/j.foodchem.2022.133215 ↗
19. Major shrimp allergen peptidomics signatures and potential biomarkers of heat processing10.1016/j.foodchem.2022.132567 ↗
20. Influence of thermal treatment on the characteristics of major oyster allergen Cra g 1 (tropomyosin)10.1002/jsfa.9071 ↗
21. Effects of selected processing treatments on antigenicity of banana prawn (Fenneropenaeus merguiensis) tropomyosin10.1111/ijfs.13922 ↗
22. EAACI Molecular Allergology User’s Guide 2.010.1111/pai.13854 ↗
23. Quality control of allergen products with mass spectrometry part I: Positioning within the EU regulatory framework10.1111/all.16080 ↗
24. Targeted proteomics: Current status and future perspectives for quantification of food allergens10.1016/j.jprot.2016.04.018 ↗
25. Authentication of shrimp muscle in complex foodstuff by in-solution digestion and high-resolution mass spectrometry10.1039/C7RA04967F ↗
26. Leni, G., Tedeschi, T., Faccini, A., Pratesi, F., Folli, C., Puxeddu, I., Migliorini, P., Gianotten, N., Jacobs, J., and Depraetere, S. (2020). Shotgun proteomics, in-silico evaluation and immunoblotting assays for allergenicity assessment of lesser mealworm, black soldier fly and their protein hydrolysates. Sci. Rep., 10.10.1038/s41598-020-57863-5 ↗
27. Liquid chromatography coupled to tandem mass spectrometry for comprehensive quantification of crustacean tropomyosin and arginine kinase in food matrix10.1016/j.foodcont.2022.109137 ↗
28. A SILAC-based accurate quantification of shrimp allergen tropomyosin in complex food matrices using UPLC-MS/MS10.1016/j.foodchem.2023.138170 ↗
29. Current perspectives and recommendations for the development of mass spectrometry methods for the determination of allergens in foods10.1093/jaoac/94.4.1026 ↗
30. Charting the proteomes of organisms with unsequenced genomes by MALDI-quadrupole time-of-flight mass spectrometry and BLAST homology searching10.1021/ac0013709 ↗
31. Tools for exploring the proteomosphere10.1016/j.jprot.2009.01.012 ↗
32. Common amino acid subsequences in a universal proteome-relevance for food science10.3390/ijms160920748 ↗
33. The use of peptide markers of carp and herring allergens as an example of detection of sequenced and non-sequenced proteins10.17113/ftb.54.03.16.4244 ↗
34. Identification of cross-species marker peptides for the detection of mammalian and poultry meat in vegan and vegetarian foods10.1021/acs.jafc.3c01100 ↗
35. Unveiling the potential of proteomics in addressing food and feed safety challenges10.2903/j.efsa.2023.e211013 ↗
36. The UniProt Consortium (2023). UniProt: The Universal Protein Knowledgebase in 2023. Nucleic Acids Res., 51, D523–D531.10.1093/nar/gkac1052 ↗
37. Minkiewicz, P., Iwaniak, A., and Darewicz, M. (2019). BIOPEP-UWM database of bioactive peptides: Current opportunities. Int. J. Mol. Sci., 20.10.3390/ijms20235978 ↗
38. BIOPEP-UWM database—Present and future10.1016/j.cofs.2023.101108 ↗
39. NCBI Taxonomy: A comprehensive update on curation, resources and tools10.1093/database/baaa062 ↗
40. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs10.1093/nar/25.17.3389 ↗
41. Epitopic hexapeptide sequences from Baltic cod parvalbumin beta (allergen Gad c 1) are common in the universal proteome10.1016/j.peptides.2012.08.011 ↗
42. InterPro in 202210.1093/nar/gkac993 ↗
43. Unipept 4.0: Functional analysis of metaproteome data10.1021/acs.jproteome.8b00716 ↗
44. The Immune Epitope Database (IEDB): 2018 update10.1093/nar/gky1006 ↗
45. Peptides, specific proteolysis products, as molecular markers of allergenic proteins—In silico studies
46. Heatmapper: Web-enabled heat mapping for all10.1093/nar/gkw419 ↗
47. Effect of heat processing on antibody reactivity to allergen variants and fragments of black tiger prawn: A comprehensive allergenomic approach10.1002/mnfr.201300584 ↗
48. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding10.1016/0003-2697(76)90527-3 ↗
49. Kinter, M., and Sherman, N. (2000). The Prepraration of Protein Digests for Mass Spectrometric Sequencing Experiments, John Wiley and Sons.
50. Development of a method for crustacean allergens using liquid chromatography/tandem mass spectrometry10.5740/jaoacint.14-248 ↗
51. Cleavage of structural proteins during the assembly of the head of bacteriophage T410.1038/227680a0 ↗
52. Darewicz, M., Pliszka, M., Borawska-Dziadkiewicz, J., Minkiewicz, P., and Iwaniak, A. (2022). Multi-bioactivity of protein digests and peptides from oat (Avena sativa L.) kernels in the prevention of the cardiometabolic syndrome. Molecules, 27.10.3390/molecules27227907 ↗
53. Smoothing and differentiation of data by simplified least squares procedures10.1021/ac60214a047 ↗
54. PEAKS DB: De novo sequencing assisted database search for sensitive and accurate peptide identification10.1074/mcp.M111.010587 ↗
55. Defining specific allergens for improved component-resolved diagnosis of shrimp allergy in adults10.1016/j.molimm.2019.05.006 ↗
56. Shellfish tropomyosin IgE cross-reactivity differs among edible insect species10.1002/mnfr.201900923 ↗
57. Fragmentation pathways of protonated peptides10.1002/mas.20024 ↗
58. Lessons in de novo peptide sequencing by tandem mass spectrometry10.1002/mas.21406 ↗
59. Antibody-free enrichment method for proteome-wide analysis of endogenous SUMOylation sites10.1016/j.aca.2021.338324 ↗
60. Song, Y., Wang, Z., Ji, H., Jiang, Z., Li, X., Du, Z., Wei, S., and Sun, Y. (2024). Fatty acid modification of casein bioactive peptides nano-assemblies, synthesis, characterization and anticarcinogenic effect. Int. J. Biol. Macromol., 254.10.1016/j.ijbiomac.2023.127718 ↗
61. GeLC-FAIMS-MS workflow for in-depth middle-down proteomics10.1002/pmic.202200431 ↗
62. Roepstorff, P., and Fohlman, J. (1984). Proposal for a common nomenclature for sequence ions in mass spectra of peptides. Biomed. Mass Spectrom., 11.10.1002/bms.1200111109 ↗
63. Multi-parameter evaluation of the effect of processing conditions on meat protein modification10.1016/j.heliyon.2020.e04185 ↗
64. Kilka uwag o testowaniu istotności współczynnika korelacji
65. Unpacking the proteome and metaproteome of the black soldier fly larvae: Efficacy and complementarity of multiple protein extraction protocols10.1021/acsomega.2c04462 ↗
66. Transcriptomic-proteomic integration: A powerful synergy to elucidate the mechanisms of meat spoilage in the cold chain10.1016/j.tifs.2021.02.051 ↗
67. Current progress and critical challenges to overcome in the bioinformatics of mass spectrometry-based metaproteomics10.1016/j.csbj.2023.01.015 ↗
68. Exploiting structural classifications for function prediction: Towards a domain grammar for protein function10.1016/j.sbi.2009.03.009 ↗
69. The language of the protein universe10.1016/j.gde.2015.08.010 ↗
70. Nucleation, rapid folding, and globular intrachain regions in proteins10.1073/pnas.70.3.697 ↗
71. Edible insects as ingredients in food products: Nutrition, functional properties, allergenicity of insect proteins, and processing modifications10.1080/10408398.2023.2223644 ↗
72. Zhang, Z.-Q., Chen, S.-C., Xiao, J.-H., and Huang, D.-W. (2024). State-of-the-art review of edible insect: From bioactives, pretreatment to enrichment. Food Biosci., 59.10.1016/j.fbio.2024.103879 ↗
73. Medeiros, F., Aleman, R.S., Gabríny, L., You, S.W., Hoskin, R.T., and Moncada, M. (2024). Current status and economic prospects of alternative protein sources for the food industry. Appl. Sci., 14.10.3390/app14093733 ↗
74. Review on proteomics for food authentication10.1016/j.jprot.2016.06.033 ↗
75. Is food allergen analysis flawed? Health and supply chain risks and a proposed framework to address urgent analytical needs10.1039/C5AN01457C ↗
76. Quantification of crustacean tropomyosin in foods using high-performance liquid chromatography–tandem mass spectrometry method10.1002/jsfa.11177 ↗
77. Development and validation of mass spectrometry-based method for detecting shrimp allergen tropomyosin10.1016/j.lwt.2021.112367 ↗
78. Identification of commercial hake and grenadier species by proteomic analysis of the parvalbumin fraction10.1002/pmic.200500899 ↗
79. Carrera, M., Pazos, M., and Gasset, M. (2020). Proteomics-based methodologies for the detection and quantification of seafood allergens. Foods, 9.10.20944/preprints202007.0523.v1 ↗
80. An enzyme-linked immunosorbent assay (ELISA) for the major crustacean allergen, tropomyosin, in food10.1080/09540100600572651 ↗
81. A group-specific, quantitative real-time PCR assay for detection of crab, a crustacean shellfish allergen, in complex food matrices10.1016/j.foodchem.2017.10.045 ↗
82. Comparison of real-time PCR and ELISA for the detection of crustacean shellfish allergens10.1080/19440049.2021.1874061 ↗
83. Food allergen control: Tropomyosin analysis through electrochemical immunosensing10.1016/j.foodchem.2022.133659 ↗
84. A sandwich ELISA for the detection of mollusks and mollusk products10.1016/j.foodchem.2023.136732 ↗
85. Lateral flow immunochromatographic assay for competitive detection of crustacean allergen tropomyosin using phage-displayed shark single-domain antibody10.1021/acs.jafc.3c07569 ↗
86. Development of a fluorescent multiplexed lateral flow immunoassay for the simultaneous detection of crustacean allergen tropomyosin, sarcoplasmic calcium binding protein and egg allergen ovalbumin in different matrices and commercial foods10.1016/j.foodchem.2023.138275 ↗
87. Frying process: From conventional to air frying technology10.1080/87559129.2019.1600541 ↗
88. Metaproteomics revealing microbial diversity and activity in the spontaneous fermentation of maize dough10.1016/j.foodchem.2023.137457 ↗
89. What makes a food protein an allergen?10.1007/s11882-004-0042-0 ↗
90. Lockey, R.F., and Ledford, D.K. (2014). Allergen nomenclature. Allergens and Allergen Immunotherapy, CRC Press. [5th ed.].10.1201/b16539 ↗
91. 2024, Precision engineering for localization, validation, and modification of allergenic epitopes10.1016/j.jaci.2023.12.017 ↗
92. Campelo, F., and Lobo, F.P. (2024). The rise of taxon-specific epitope predictors. Brief. Bioinform., 25.10.1093/bib/bbae092 ↗
93. Contemporary bioinformatics and cheminformatics support for food peptidomics10.1016/j.cofs.2024.101125 ↗
94. The EMBL-EBI Job Dispatcher sequence analysis tools framework in 202410.1093/nar/gkae241 ↗
95. Food allergen detection by mass spectrometry: From common to novel protein ingredients10.1002/pmic.202200427 ↗
96. Periodic Table of Food Initiative for generating biomolecular knowledge of edible biodiversity10.1038/s43016-024-00941-y ↗