CHARACTERIZATION THE ALLERGENICITY AND STABILITY OF ALLERGENS OF FRESHWATER SNAIL, Pomacea canaliculata

Authors

  • Rosmilah Misnan Department of Biology, Faculty of Science and Mathematics, Universiti Pendidikan Sultan Idris, 35900 Tanjong Malim, Perak, Malaysia https://orcid.org/0000-0002-1349-2193
  • Norazlin Salahudin Abd Aziz ᵃDepartment of Biology, Faculty of Science and Mathematics, Universiti Pendidikan Sultan Idris, 35900 Tanjong Malim, Perak, Malaysia ᵇSekolah Menengah Jenis Kebangsaan Notre Dame Convent, 265 Jalan Gajah Berang, 75200 Melaka, Malaysia
  • Komathi Sockalingam ᵃDepartment of Biology, Faculty of Science and Mathematics, Universiti Pendidikan Sultan Idris, 35900 Tanjong Malim, Perak, Malaysia ᶜSekolah Menengah Kebangsaan Pasir Putih, Jalan Selasih 4, Taman Pasir Putih, 81700 Pasir Gudang, Johor, Malaysia
  • Noor Asyikin Kamarazaman ᵃDepartment of Biology, Faculty of Science and Mathematics, Universiti Pendidikan Sultan Idris, 35900 Tanjong Malim, Perak, Malaysia ᵈHonsbridge International, Jalan PJU 5/7 Dataran Sunway, Kota Damansara, 47810 Petaling Jaya, Selangor, Malaysia
  • Zailatul Hani Mohamad Yadzir Disease Control Division, Ministry of Health Malaysia, 62590 Putrajaya, Malaysia
  • Noormalin Abdullah Allergy and Immunology Research Centre, Institute for Medical Research, 50588 Kuala Lumpur, Malaysia
  • Faizal Bakhtiar Allergy and Immunology Research Centre, Institute for Medical Research, 50588 Kuala Lumpur, Malaysia

DOI:

https://doi.org/10.11113/jurnalteknologi.v86.18236

Keywords:

Pomacea canaliculata, freshwater snail, tropomyosin, actin, proteomics

Abstract

 

Snail allergy is considered a serious form of food allergy with prevalence of 1.4 to 22% worldwide. However, allergy to Pomacea canaliculata, a commonly consumed local snail has not been well-described. Hence, this study aimed to characterize the allergenicity and stability of the allergenic proteins of P. canaliculata by proteomics approach. Snail flesh was treated with several thermal and non-thermal treatments prior to overnight protein extraction. The snail proteins were then subjected to SDS-PAGE, followed by immunoblotting, two-dimensional electrophoresis (2-DE), 2-DE immunoblotting and mass-spectrometry analysis. Raw snail demonstrated 31 protein bands between 10 to 250 kDa, with fewer protein bands in treated snails. Boiled snails had the most protein bands among thermally treated snails, while salted and dried snails showed more bands than pickled snails among non-thermal treatments. Immunoblotting of raw extract demonstrated 16 IgE-binding bands, with the 33 and 42 kDa protein bands were identified as the major. The 33 kDa allergen was highly stable to all treatments applied, while the 42 kDa was sensitive to thermal and pickling treatments. Fewer allergenic bands were present in treated snails, with allergenicity ranked as raw > boiled > roasted > fried for thermal treatments, and raw > salted > dried > pickled for non-thermal treatments. Mass spectrometry identified the 33 kDa and 42 kDa allergens as tropomyosin and actin, respectively. In conclusion, P. canaliculata has numerous allergenic proteins with varying stability. 

 

References

Norazlin, S. A. A., Rosmilah M., Zailatul H. M. Y., Faizal, B., Noormalin, A. and Shahnaz, M. 2016. Immediate Hypersensitivity to Marine Snail (Cerithidea obtusa) Allergen among Local Patients with Atopic Diseases. EDUCATUM Journal of Science, Mathematics and Technology. 3(2): 22-30.

Moneret-Vautrin, D. A., Kanny, G., Morisset, M., Rance, F., Fardeau, M. F. & Beaudouin, E. 2004. Severe Food Anaphylaxis: 107 Cases Registered in 2002 by the Allergy Vigilance Network. European Annals of Allergy and Clinical Immunology. 36(2): 46-51.

Vuitton, D. A., Ranc, E. F., Paquin, M. L., Adessi, B., Vigan, M., Gomot, A., et al. 1998. Cross-reactivity between Terrestrial Snails (Helix species) an House-dust Mite (Dermatophagoides pteronyssinus). Allergy. 53(2): 144-150. Doi: http://dx.doi.org/10.1111/j.1398-9995.1998.tb03862.x.

Eriksson, N. E., Moller, C., Werner, S., Magnusson, J., Bengtsson, U. & Zolubas, M. 2004. Self-reported Food Hypersensitivity in Sweden, Denmark, Estonia, Lithuania, and Russia. Journal of Investigational Allergology and Clinical Immunology. 14(1): 70-79.

Boye, J. I. 2012. Food Allergies in Developing and Emerging Economies: Need for Comprehensive Data on Prevalence Rates. Clinical and Translational Allergy. 2(25): 1-9. Doi: http://dx.doi.org/10.1186/2045-7022-2-25.

Wong, L., Tham, E. H. and Lee, B. W. 2019. An Update of Shellfish Allergy. Current Opinion of Allergy and Clinical Immunology. 19(3): 236-242.

Doi: http://dx.doi.org/10.1097/ACI.0000000000000532.

Taylor, S. L. 2008. Molluscan Shellfish Allergy. Advances in Food and Nutrition Research. 54: 140-177.

Doi: http://dx.doi.org/10.1016/S1043-4526(07)00004-6.

Bedolla-Barajas, M., Bedolla-Pulido, T. R., Macriz-Romero, N., Morales-Romero, J., and Robles-Figueroa, M. 2015. Prevalence of Peanut, Tree Nut, Sesame, and Seafood Allergy in Mexican Adults. Revista de investigacion clinica. 67(6): 379-386.

Emons, J. A. M. and Gerth van Wijk, R. 2018. Food Allergy and Asthma: Is There a Link? Current Treatment Options in Allergy. 5(4): 436-444.

Doi: http://dx.doi.org/10.1007/s40521-018-0185-1.

Miller, J. D. 2019. The Role of Dust Mites in Allergy. Clinical Reviews in Allergy and Immunology. 57(3): 312-329.

Doi: http://dx.doi.org/10.1007/s12016-018-8693-0.

Van Ree, R., Antonicelli, L., Akkerdaas, J. H. Pajno, G. B., Barberio, G., Corbetta, L., Ferro, G., Zambito, M., Garritani, M. S., Aalberse, R. C. and Bonifazi, F. 1996. Asthma after Consumption of Snails in House-dust-mite-allergic Patients: A Case of IgE Cross-reactivity. Allergy. 51: 387-93.

Tsapis, M., Chabane, H., Teychene, A. M., Laurent, M., Roland, P. N. and de Pontual, L. 2013. Fatal Anaphylaxis after Snail Ingestion in a Child after 3 Years of House Dust Mite Immunotherapy. Revue française d’allergologie. 53: 436-438.

Ishikawa, M., Ishida, M., Shimakura, K., Nagashima, Y. and Shiomi, K. 1998. Purification and IgE-binding Epitopes of a Major Allergen in the Gastropod Turbo cornutus. Bioscience, Biotechnology, and Biochemistry. 62(7): 1337-1343.

Doi: http://dx.doi.org/10.1271/bbb.62.1337.

Asturias, J. A., Eraso, E., Arilla, M. C., Gomez-Bayon, N., Inacio, F. and Martinez, A. 2002. Cloning, isolation and IgE-binding Properties of Helix aspersa (Brown Garden Snail) tropomyosin. International Achieves of Allergy and Immunology. 128: 90-96.

Doi: http://dx.doi.org/10.1159/000059398.

Misnan, R., Salahudin, A. A. N; Yadzir, Z. H. M., Bakhtiar, F., Abdullah, N. and Murad, S. 2016. Impacts of thermal treatments on major and minor allergens of sea snail, Cerithidea obtusa (obtuse horn shell). Iranian Journal of Allergy, Asthma and Immunology. 15(4): 309-316.

Rosmilah, M., Norazlin, S. A. A., Zailatul, H. M. Y., Noormalin, A., Faizal, B. and Shahnaz, M. 2016. Comparison of Allergenic Proteins of Sea Snail (Cerithidea obtusa) and Freshwater Snail (Pomacea canaliculata). Jurnal Teknologi. 78(11): 113-119.

Martins, L., Pires E. and Ináicio, F. 2009. CD4 T-Cell Cytokine Response to Mite Recombinant Tropomyosin in Mite, Snail and Shrimp Allergic Patients. Internet Journal of Asthma, Allergy and Immunology. 7(1): 1-22.

Bessot, J. C., Metz-Favre, C., Rame, J. M., De Blay, F. and Pauli, G. 2010. Tropomyosin or Not Tropomyosin, What is the Relevant Allergen in House Dust Mite and Snail Cross Allergies? European Annals of Allergy and Clinical Immunology. 42(1): 3-10.

Martins, L. M., Peltre, G., da Costa Faro, C. J., Pires, E. M. and da Cruz Inácio, F. F. 2005. The Helix aspersa (Brown Garden Snail) Allergen Repertoire. International Archives of Allergy and Immunology. 136(1): 7-15.

Doi: http://dx.doi.org/10.1159/000082579.

Matsuo, H., Yokooji, T. and Taogoshi, T. 2015. Common Food Allergens and Their IgE-binding Epitopes. Allergolology International. 64(4): 332-343.

Doi: http://dx.doi.org/10.1016/j.alit.2015.06.009.

Zailatul, H. M. Y., Rosmilah, M., Faizal, B., Noormalin, A. and Shahnaz, M. 2015. Malaysian Cockle (Anadara granosa) Allergy: Identification of IgE-binding Proteins and Effects of Different Cooking Methods. Tropical Biomedicine. 32(2): 323-334.

Rosmilah, M., Komathi, S., Zailatul, H. M. Y., Noormalin, A., Faizal, B. and Shahnaz, M. 2019. Characterization of Major Allergens of Macrobrachium rosenbergii and Their Thermostability in Different Cooking Methods. Jurnal Teknologi. 81(1): 163-170.

Wai, C. Y. Y., Leung, N. Y. H., Chu, K. H., Leung, P. S. C., Leung, A. S. Y., Wong, G. W. K. and Leung, T. F. 2020. Overcoming Shellfish Allergy: How Far Have We Come? International Journal of Molecular Sciences. 21(6).

Doi: http://dx.doi.org/10.3390/ijms21062234.

Palmer, L. K., Marsh, J. T., Lu, M., Goodman, R. E., Zeece, M. G. and Johnson, P. E. 2020. Shellfish Tropomyosin IgE Cross-Reactivity Differs Among Edible Insect Species. Molecular Nutrition and Food Research. 18: e1900923.

Doi: http://dx.doi.org/10.1002/mnfr.201900923.

Nugraha, R., Kamath, S. D., Johnston, E., Karnaneedi, S., Ruethers, T. and Lopata, A. L. 2019. Conservation Analysis of B-Cell Allergen Epitopes to Predict Clinical Cross-Reactivity between Shellfish and Inhalant Invertebrate Allergens. Frontiers Immunology. 10: 2676.

Doi: http://dx.doi.org/10.3389/fimmu.2019.02676.

Kamath, S. D., Abdel Rahman, A. M., Komoda, T. and Lopata, A. L. 2013. Impact of Heat Processing on the Detection of the Major Shellfish Allergen in Crustaceans and Mollusks Using Specific Monoclonal Antibodies. Food Chemistry. 41(4): 4031-4039.

Doi: http://dx.doi.org/10.1016/j.foodchem.2013.06.105.

Samson, K. T., Chen, F. H., Miura, K., Odajima, Y., Iikura, Y., Naval Rivas, M., Minoguchi, K. and Adachi, M. 2004. IgE Binding to Raw and Boiled Shrimp Proteins in Atopic and Nonatopic Patients with Adverse Reactions to Shrimp. International Archives of Allergy and Immunology. 133(3): 225-232.

Doi: http://dx.doi.org/10.1159/000076828.

Davis, P. J. and Williams, S. C. 1998. Protein Modification by Thermal Processing. Allergy. 53(46 Suppl): 102-105.

Doi: http://dx.doi.org/10.1111/j.1398-9995.1998.tb04975.x.

Yadzir, Z. H., Misnan, R., Abdullah, N., Bakhtiar, F., Arip M. and Murad, S. 2010. Identification of IgE-binding Proteins of Raw and Cooked Extracts of Loligo edulis (white squid). Southeast Asian Journal of Tropical Medicine and Public Health. 41(3): 653-659.

Kamath, S. D., Rahman, A. M., Voskamp, A., Komoda, T., Rolland, J. M., O’Hehir, R. E. and Lopata, A. L. 2014. Effect of Heat Processing on Antibody Reactivity to Allergen Variants and Fragments of Black Tiger Prawn: A Comprehensive Allergenomic Approach. Molecular Nutrition and Food Research. 58(5): 1144-1155.

Doi: http://dx.doi.org/10.1002/mnfr.201300584.

Nakamura, A., Watanabe, K., Ojima, T., Ahn, D. H. and Saeki, H. 2005. Effect of Maillard Reaction on Allergenicity of Scallop Tropomyosin. Journal of Agriculture and Food Chemistry. 53(19): 7559-7564.

Doi: http://dx.doi.org/10.1021/jf0502045.

Nakamura, A., Sasaki, F., Watanabe, K., Ojima, T., Ahn, D. H. and Saeki, H. 2006. Changes in Allergenicity and Digestibility of Squid Tropomyosin during the Maillard Reaction with Ribose. Journal of Agriculture and Food Chemistry. 54(25): 9529-9533.

Doi: http://dx.doi.org/10.1021/jf061070d.

Misnan, R., Kamarazaman, N. A., Sockalingam, K., Yadzir, Z. H. M., Bakhtiar, F., Abdullah, N. and Arip, M. 2023. Identification of Major and Cross-reactive Allergens of Local Freshwater Snail (Pila polita) and the Impact of Thermal and Non-thermal Food Processing on Allergen Stability. Journal of Science of Food and Agriculture. 103(12): 5819-5830. Doi: http://dx.doi.org/10.1002/jsfa.12659.

Bu, G., Luo, Y., Chen, F., Liu, K. and Zhu, T. 2013. Milk Processing as a Tool to Reduce Cow’s Milk Allergenicity: A Mini-review. Dairy Science Technology. 93: 211-223.

Doi: http://dx.doi.org/10.1007/s13594-013-0113-x.

Zhang, T., Shi, Y., Zhao, Y., Wang, J., Wang, M., Niu, B. and Chen, Q. 2019. Different Thermal Processing Effects on Peanut Allergenicity. Journal of Science of Food and Agriculture. 99(5): 2321-2328.

Doi: http://dx.doi.org/10.1002/jsfa.9430.

Abramovitch, J. B., Kamath, S., Varese, N., Zubrinich, C., Lopata, A. L., O’Hehir, R. E., et al. 2013. IgE Reactivity of Blue Swimmer Crab (Portunus pelagicus) Tropomyosin, Por p 1, and Other Allergens; Cross-reactivity with Black Tiger Prawn and Effects of Heating. PLoS One. 8(6): e67487.

Doi: http://dx.doi.org/10.1371/journal.pone.0067487.

Bu, G. H., Luo, Y. K., Zheng, Z. and Zheng, H. 2009. Effect of Heat Treatment on the Antigenicity of Bovine α-lactalbumin and β-lactoglobulin in Whey Protein Isolate. Food and Agricultural Immunology. 20: 195-206.

Netting, M., Donato, A., Makrides, M., Gold, M., Quinn, P. and Penttila, I. 2015. Allergenicity of Pasteurized Whole Raw Hen’s Egg Compared with Fresh Whole Raw Hen’s Egg. Pediatric Allergy and Immunology. 26(3): 234-238.

Doi: http://dx.doi.org/10.1111/pai.12365.

Martínez-Alvarez, O. and Gόmez-Guillén, M. C. 2006. Effect of Brine Salting at Different pHs on the Functional Properties of Cod Muscle Proteins after Subsequent Dry Salting. Food Chemistry. 94: 123-129.

Martínez-Alvarez, O. and Gόmez-Guillén, M. C. 2005. The Effect of Brine Composition and Ph on the Yield and Nature of Water-soluble Proteins Extractable from Brined Muscle of Cod (Gadus morhua). Food Chemistry. 92: 71-77.

Ünlüsayin, M., Erdilal, R., Gümüş, B. and Gülyavuz, H. 2010. The effects of different salting methods on extract loss from rainbow trout. Pakistan Veterinary Journal. 30(3): 131-134.

Kobayashi, M., Hashimoto, Y., Taniuchi, S. and Tanabe, S. 2004. Degradation of Wheat Allergen in Japanese Soy Sauce. International Journal of Molecular Medicine. 13(6): 821-827.

Doi: http://dx.doi.org/10.3892/mmr.2017.6815.

Magishi, N., Yuikawa, N., Kobayashi, M. and Taniuchi, S. 2017. Degradation and Removal of Soybean Allergen in Japanese Soy Sauce. Molecular Medicine Reports. 16(2): 2264-2268.

Doi: http://dx.doi.org/10.3892/mmr.2017.6815.

Prachayawarakorn, S., Soponronnarit, S., Wetchacama, S. and Jaısut, D. 2002. Desorption Isotherms and Drying Characteristics of Shrimp in Superheated Steam and Hot Air. Drying Technology. 20(3): 669-684.

Yang, S., Tu, Z. C., Wang, H. and Huang, T. 2020. The Reduction in the Immunoglobulin G and Immunoglobulin E Binding Capacity of β-lactoglobulin via Spray-drying Technology. Journal of Dairy Science. 103(4): 2993-3001.

Doi: http://dx.doi.org/10.3168/jds.2019-17322.

Lasekan, A., Cao, H., Maleki, S. and Nayak, B. B. 2017. Shrimp Tropomyosin Retains Antibody Reactivity after Exposure to Acidic Condition. Journal of the Science of Food and Agriculture. 97(11): 3623-3630.

Doi: http://dx.doi.org/10.1002/jsfa.8221.

Armentia, A., Dueñas-Laita, A., Pineda, F., Herrero, M. and Martín, B. 2010. Vinegar Decreases Allergenic Response in Lentil and Egg Food Allergy, Allergologia et Immunopathologia. 38 (2): 74-77.

Doi: http://dx.doi.org/10.1016/j.aller.2009.08.003.

Perez-Macalalag, E., Sumpaico, M. and Agbayani, B. 2007. Shrimp Allergy Effect of Vinegar Soaking on Allergenicity. The World Allergy Organization Journal. S317.

Lee, J. O., Sung, D., Park, S. H., Lee, J., Kim, J., Shon, D. H., Ahn, K. and Han, Y. 2017. Effect of Acid Treatment on Allergenicity of Peanut and Egg. Journal of the Science of Food and Agriculture. 97(7): 2116-2121.

Doi: http://dx.doi.org/10.1002/jsfa.8017.

Kim, J., Lee, J., Seo, W. H., Han, Y., Ahn, K. and Lee, S. I. 2011. Changes in Major Peanut Allergens under Different pH Conditions. Allergy, Asthma and Immunology Research. 4(3): 157-60.

Doi: http://dx.doi.org/10.4168/aair.2012.4.3.157.

Noor, H. M. S., Arbain, D., Mohamed, Z. M., Pilus, N. and Nawi, R. 2012. Distribution and Management of Pomacea canaliculata in the Northern Region of Malaysia: Mini Review. APCBEE Procedia. 2: 129-134.

Doi: http://dx.doi.org/10.1016/j.apcbee.2012.06.024.

Arfan, A. G., Muhamad, R., Omar, D., Nor Azwady, A. A. and Manjeri, G. 2014. Distribution of two Pomacea spp. In Rice Fields of Peninsular Malaysia. Annual Research and Review in Biology. 4(24): 4123-4136.

Doi: http://dx.doi.org/10.9734/ARRB/2014/11398.

Kannan, A., Rama Rao, S., Ratnayeke, S. and Yow, Y. Y. 2020. The Efficiency of Universal Mitochondrial DNA Barcodes for Species Discrimination of Pomacea canaliculata and Pomacea maculata. Peer Journal. 8: e8755.

Doi: http://dx.doi.org/10.7717/peerj.8755.

Rama Rao, S, Liew, T. S, Yow, Y. Y. and Ratnayeke, S. 2018. Cryptic Diversity: Two Morphologically Similar Species of Invasive Apple Snail in Peninsular Malaysia. PLoS One. 13(5): e0196582.

Doi: http://dx.doi.org/10.1371/journal.pone.0196582.

Khanaruksombat, S., Srisomsap, C., Chokchaichamnankit, D., Punyarit, P. and Phiriyangkul, P. 2014. Identification of a Novel Allergen from Muscle and Various Organs in Banana Shrimp (Fenneropenaeus merguiensis). Annals of Allergy, Asthma and Immunology. 113(3): 301-306.

Doi: http://dx.doi.org/10.1016/j.anai.2014.06.002.

Reisler, E. and Egelman, E. H. 2007. Actin Structure and Function: What We Still Do Not Understand. The Journal of Biology Chemistry. 282(50): 36133–36137.

Doi: http://dx.doi.org/10.1074/jbc.R700030200.

Zailatul, H. M. Y., Rosmilah, M., Faizal, B., Noormalin, A. and Shahnaz, M. 2015. Tropomyosin and Actin Identified as Major Allergens of the Carpet Clam (Paphia textile) and the Effect of Cooking on Their Allergenicity. BioMed Research International. 2015: 254152.

Doi: http://dx.doi.org/10.1155/2015/254152.

González-Mancebo, E., Trujillo-Trujillo, M. J., Gandolfo-Cano, M., Mohedano-Vicente, E., Cuesta-Herranz, J., Bartolome, B. and Pastor-Vargas, C. 2019. Actin Allergen of Common Periwinkle Sea Snail (Littorina littorea). J Investig Allergol Clin Immunol. 29(2): 150-152.

Doi: http://dx.doi.org/10.18176/jiaci.0356.

Ma, H., Xu, W., Mai, K., Liufu, Z. and Chen, H. 2004. Cloning and Characterization of an Abalone (Haliotis discus hannai) Actin Gene. Journal of Ocean University of China. 3(2): 145-149.

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2024-09-17

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Science and Engineering

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CHARACTERIZATION THE ALLERGENICITY AND STABILITY OF ALLERGENS OF FRESHWATER SNAIL, Pomacea canaliculata. (2024). Jurnal Teknologi (Sciences & Engineering), 86(6), 1-9. https://doi.org/10.11113/jurnalteknologi.v86.18236