Abstract
Common carp (Cyprinus carpio) is an important and popular fish in Asia, but due to the short length and low cross-linking degree, fish myofibrillar protein is easy to break and deteriorate, which shows some negative impacts on the quality of fish meat. In present study, the cross-linking modifications of different phenolic compounds on myofibrillar protein of common carp were investigated, and their action mechanism was further explored. Phenolic compounds including gallic acid (GA), chlorogenic acid (CA), epigallocatechin (EGC), epigallocatechin gallate (EGCG), and tannic acid (TA) could increase the average particle size of myofibrillar protein from 61 to 65, 102, 97, 118, and 127 μm individually, and the solubility decreased by 7.7, 16.1, 13.6, 21.1, and 19.2%. The increased particle size and decreased solubility could promote the aggregation of myofibrillar protein, which indicated phenolic compounds exhibited the cross-linking effects on fish myofibrillar protein. Then, hydrogen bonds were found to be the main molecular force for the cross-linking effects. Meanwhile, the contents of sulfhydryl decreased by 13.5, 18.9, 29.7, 35.1, and 40.5%, and the disulfide bonds in myofibrillar protein decreased by 12.9, 11.9, 14.4, 22.3, and 26.7% when treated with GA, CA, EGC, EGCG, and TA, respectively. In addition, the secondary and tertiary structures of myofibrillar protein were both changed with phenolic compounds, which indicated that its spatial structure was changed to be loose. Furthermore, the thermal stability and gel properties of myofibrillar protein were improved with phenolic compounds. Different phenolic compounds showed various cross-linking effects on fish myofibrillar protein, which was due to the content and reactivity of hydroxyl groups in phenolic compounds. All results suggested that phenolic compounds had potential value to modify the length and cross-linking degree of fish myofibrillar protein, so as to improve the quality of fish meat in the food industry.
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References
Balange, A. K., & Benjakul, S. (2009). Effect of oxidised tannic acid on the gel properties of mackerel (Rastrelliger kanagurta) mince and surimi prepared by different washing processes. Food Hydrocolloids, 23, 1693–1701. https://doi.org/10.1016/j.foodhyd.2009.01.007
Barakat, A. Z., Bassuiny, R. I., Abdel-Aty, A. M., & Mohamed, S. A. (2020a). Diabetic complications and oxidative stress: The role of phenolic-rich extracts of saw palmetto and date palm seeds. Journal of Food Biochemistry, 44, e13416. https://doi.org/10.1111/jfbc.13416
Barakat, A. Z., Hamed, A. R., Bassuiny, R. I., Abdel-Aty, A. M., & Mohamed, S. A. (2020b). Date palm and saw palmetto seeds functional properties: Antioxidant, anti-inflammatory and antimicrobial activities. Journal of Food Measurement and Characterization, 14, 1064–1072. https://doi.org/10.1007/s11694-019-00356-5
Beveridge, T., Toma, S. J., & Nakai, S. (1974). Determination of SH-groups and SS-groups in some food proteins using Ellmans reagent. Journal of Food Science, 39, 49–51. https://doi.org/10.1111/j.1365-2621.1974.tb00984.x
Buamard, N., & Benjakul, S. (2018). Combination effect of high pressure treatment and ethanolic extract from coconut husk on gel properties of sardine surimi. LWT-Food Science and Technology, 91, 361–367. https://doi.org/10.1016/j.lwt.2018.01.074
Chanphai, P., & Tajmir-Riahi, H. A. (2019). Tea polyphenols bind serum albumins: A potential application for polyphenol delivery. Food Hydrocolloids, 89, 461–467. https://doi.org/10.1016/j.foodhyd.2018.11.008
Collar, C., Villanueva, M., & Ronda, F. (2020). Structuring diluted wheat matrices: Impact of heat-moisture treatment on protein aggregation and viscoelasticity of hydrated composite flours. Food and Bioprocess Technology, 13, 475–487. https://doi.org/10.1007/s11947-020-02406-z
Cheng, J. R., Zhu, M. J., & Liu, X. M. (2020). Insight into the conformational and functional properties of myofibrillar protein modified by mulberry polyphenols. Food Chemistry, 308, 125592. https://doi.org/10.1016/j.foodchem.2019.125592
Dai, Y., Zhang, Q. N., Wang, L., Liu, Y., Li, X. M., & Dai, R. T. (2014). Changes in shear parameters, protein degradation and ultrastructure of pork following water bath and ohmic cooking. Food and Bioprocess Technology, 7, 1393–1403. https://doi.org/10.1007/s11947-013-1145-1
Debelo, H., Li, M., & Ferruzzi, M. G. (2020). Processing influences on food polyphenol profiles and biological activity. Current Opinion in Food Science, 32, 90–102. https://doi.org/10.1016/j.cofs.2020.03.001
Dong, S. L., Dong, Y. W., Cao, L., Verreth, J., Olsen, Y., Liu, W. J., Fang, Q. Z., Zhou, Y. G., Li, L., Li, J. Y., & Sorgeloos, P. (2022). Optimization of aquaculture sustainability through ecological intensification in China. Reviews in Aquaculture, 14, 1249–1259. https://doi.org/10.1111/raq.12648
Ellman, G. L. (1959). Tissue sulfhydryl groups. Archives of Biochemistry and Biophysics, 82, 70–77. https://doi.org/10.1016/0003-9861(59)90090-6
Estévez, M., Kylli, P., Puolanne, E., Kivikari, R., & Heinonen, M. (2008). Oxidation of Skeletal muscle myofibrillar proteins in oil-in-water emulsions: Interaction with lipids and effect of selected phenolic compounds. Journal of Agricultural and Food Chemistry, 56, 10933–10940. https://doi.org/10.1021/jf801784h
Fang, M. X., Xiong, S. B., Yin, T., Hu, Y., Liu, R., Du, H. Y., Liu, Y. M., & You, J. (2021). In vivo digestion and absorption characteristics of surimi gels with different degrees of cross-linking induced by transglutaminase (TGase). Food Hydrocolloids, 121, 107007. https://doi.org/10.1016/j.foodhyd.2021.107007
Feng, X., Ng, V. K., Mikš-Krajnik, M., & Yang, H. S. (2016). Effects of fish gelatin and tea polyphenol coating on the spoilage and degradation of myofibril in fish fillet during cold storage. Food and Bioprocess Technology, 10, 89–102. https://doi.org/10.1007/s11947-016-1798-7
Gao, M. R., Xu, Q. D., & Zeng, W. C. (2020). Effect of tea polyphenols on the tenderness of yak meat. Journal of Food Processing and Preservation, 44, e14433. https://doi.org/10.1111/jfpp.14433
Gomez-Guillen, M. C., Montero, P., Solas, M. T., & Borderias, A. J. (1998). Thermally induced aggregation of giant squid (Dosidicus gigas) mantle proteins. Physicochemical contribution of added ingredients. Journal of Agricultural and Food Chemistry, 46, 3440–3446. https://doi.org/10.1021/jf9801116
Grosso, G. (2018). Effects of polyphenol-rich foods on human health. Nutrients, 10, 1089. https://doi.org/10.3390/nu10081089
Guo, A., Jiang, J., True, A. D., & Xiong, Y. L. (2021). Myofibrillar protein cross-linking and gelling behavior modified by structurally relevant phenolic compounds. Journal of Agricultural and Food Chemistry, 69, 1308–1317. https://doi.org/10.1021/acs.jafc.0c04365
Huang, Y., Du, H. Y., Kamal, G. M., Cao, Q. J., Liu, C., Xiong, S. B., Manyande, A., & Huang, Q. (2020). Studies on the binding interactions of grass carp (Ctenopharyngodon idella) myosin with chlorogenic acid and rosmarinic acid. Food and Bioprocess Technology, 13, 1421–1434. https://doi.org/10.1007/s11947-020-02483-0
Jiang, L. F., & Wu, S. J. (2018). Pullulan suppresses the denaturation of myofibrillar protein of grass carp (Ctenopharyngodon idella) during frozen storage. International Journal of Biological Macromolecules, 112, 1171–1174. https://doi.org/10.1016/j.ijbiomac.2018.02.094
Karagozlu, M., Ocak, B., & Özdestan-Ocak, Ö. (2021). Effect of tannic acid concentration on the physicochemical, thermal, and antioxidant properties of gelatin/gum Arabic–walled microcapsules containing Origanum onites L. essential oil. Food and Bioprocess Technology, 14, 1231–1243. https://doi.org/10.1007/s11947-021-02633-y
Li, L., Shao, J. H., Zhu, X. D., Zhou, G. H., & Xu, X. L. (2013). Effect of plant polyphenols and ascorbic acid on lipid oxidation, residual nitrite and N-nitrosamines formation in dry-cured sausage. International Journal of Food Science & Technology, 48, 1157–1164. https://doi.org/10.1111/ijfs.12069
Li, L. Y., Zhao, X., & Xu, X. L. (2022). Trace the difference driven by unfolding-refolding pathway of myofibrillar protein: Emphasizing the changes on structural and emulsion properties. Food Chemistry, 367, 130688. https://doi.org/10.1016/j.foodchem.2021.130688
Lin, W. L., Zeng, Q. X., Zhu, Z. W., & Song, G. S. (2012). Relation between protein characteristics and TPA texture characteristics of crisp grass carp (Ctenopharyngodon Idellus C. Et V) and grass carp (Ctenopharyngodon Idellus). Journal of Texture Studies, 43, 1–11. https://doi.org/10.1111/j.1745-4603.2011.00311.x
Mahboob, S., Al-Ghanim, K. A., Al-Balawi, H. F. A., Al-Misned, F., & Ahmed, Z. (2019). Study on assessment of proximate composition and meat quality of fresh and stored Clarias gariepinus and Cyprinus carpio. Brazilian Journal of Biology, 79, 651–658. https://doi.org/10.1590/1519-6984.187647
Martucci, J. F., Espinosa, J. P., & Ruseckaite, R. A. (2015). Physicochemical properties of films based on bovine gelatin cross-linked with 1,4-butanediol diglycidyl ether. Food and Bioprocess Technology, 8, 1645–1656. https://doi.org/10.1007/s11947-015-1524-x
Ojha, H., Mishra, K., Hassan, M. I., & Chaudhury, N. K. (2012). Spectroscopic and isothermal titration calorimetry studies of binding interaction of ferulic acid with bovine serum albumin. Thermochimica Acta, 548, 56–64. https://doi.org/10.1016/j.tca.2012.08.016
Onwulata, C. I., & Tomasula, P. M. (2008). Gelling properties of tyrosinase-treated dairy proteins. Food and Bioprocess Technology, 3, 554–560. https://doi.org/10.1007/s11947-008-0124-4
Ozdal, T., Capanoglu, E., & Altay, F. (2013). A review on protein-phenolic interactions and associated changes. Food Research International, 51, 954–970. https://doi.org/10.1016/j.foodres.2013.02.009
Peng, N., Gu, L. P., Li, J. H., Chang, C. H., Li, X., Su, Y. J., & Yang, Y. J. (2017). Films based on egg white protein and succinylated casein cross-linked with transglutaminase. Food and Bioprocess Technology, 10, 1422–1430. https://doi.org/10.1007/s11947-017-1901-8
Prodpran, T., Benjakul, S., & Phatcharat, S. (2012). Effect of phenolic compounds on protein cross-linking and properties of film from fish myofibrillar protein. International Journal of Biological Macromolecules, 51, 774–782. https://doi.org/10.1016/j.ijbiomac.2012.07.010
Quan, T. H., Benjakul, S., Sae-leaw, T., Balange, A. K., & Maqsood, S. (2019). Protein–polyphenol conjugates: Antioxidant property, functionalities and their applications. Trends in Food Science & Technology, 91, 507–517. https://doi.org/10.1016/j.tifs.2019.07.049
Raak, N., Rohm, H., & Jaros, D. (2020). Enzymatically cross-Linked sodium caseinate as techno-functional ingredient in acid-induced milk gels. Food and Bioprocess Technology, 13, 1857–1865. https://doi.org/10.1007/s11947-020-02527-5
Rawel, H. A., Meidtner, K., & Kroll, J. (2005). Binding of selected phenolic compounds to proteins. Journal of Agricultural and Food Chemistry, 53, 4228–4235. https://doi.org/10.1021/jf0480290
Rawel, H. M., Czajka, D., Rohn, S., & Kroll, J. (2002). Interactions of different phenolic acids and flavonoids with soy proteins. International Journal of Biological Macromolecules, 30, 137–150. https://doi.org/10.1016/s0141-8130(02)00016-8
Roy, A. S., Dinda, A. K., Chaudhury, S., & Dasgupta, S. (2014). Binding of antioxidant flavonol morin to the native state of bovine serum albumin: Effects of urea and metal ions on the binding. Journal of Luminescence, 145, 741–751. https://doi.org/10.1016/j.jlumin.2013.08.054
Smith, P. K., Krohn, R. I., Hermanson, G. T., Mallia, A. K., Gartner, F. H., Provenzano, M. D., Fujimoto, E. K., Goke, N. M., Olson, B. J & Klenk, D. C. (1985). Measurement of protein using bicinchonic acid. Analytical Biochemistry, 150, 76-85. https://doi.org/10.1016/0003-2697(85)90442-7
Tang, C. H., Sun, X., Yin, S. W., & Ma, C. Y. (2008). Transglutaminase-induced cross-linking of vicilin-rich kidney protein isolate: Influence on the functional properties and in vitro digestibility. Food Research International, 41, 941–947. https://doi.org/10.1016/j.foodres.2008.07.015
Tatjana, R., Smiljana, R., & Vesna, N. (2002). Bighead carp myosin stability to heat and frozen storage. Acta Veterinaria-Beograd, 52, 151–161. https://doi.org/10.2298/avb0203151r
Tavares, L., Barros, H. L. B., Vaghetti, J. C. P., & Noreña, C. P. Z. (2019). Microencapsulation of garlic extract by complex coacervation using whey protein isolate/chitosan and gum arabic/chitosan as wall materials: Influence of anionic biopolymers on the physicochemical and structural properties of microparticles. Food and Bioprocess Technology, 12, 2093–2106. https://doi.org/10.1007/s11947-019-02375-y
Tavassoli, K. E., Goli, S. A. H., & Fathi, M. (2017). Encapsulation of orange essential oil using cross-linked electrospun gelatin nanofibers. Food and Bioprocess Technology, 11, 427–434. https://doi.org/10.1007/s11947-017-2026-9
Tironi, V. A., Tomas, M. C., & Anon, M. C. (2002). Structural and functional changes in myofibrillar proteins of sea salmon (Pseudopercis semifasciata) by interaction with malonaldehyde (RI). Journal of Food Science, 67, 930–935. https://doi.org/10.1111/j.1365-2621.2002.tb09430.x
Utrera, M., Morcuende, D., Ganhão, R., & Estévez, M. (2014). Role of phenolics extracting from Rosa canina L. on meat protein oxidation during frozen storage and beef patties processing. Food and Bioprocess Technology, 8, 854–864. https://doi.org/10.1007/s11947-014-1450-3
Wang, H., Luo, Y. K., & Shen, H. X. (2013). Effect of frozen storage on thermal stability of sarcoplasmic protein and myofibrillar protein from common carp (Cyprinus carpio) muscle. International Journal of Food Science & Technology, 48, 1962–1969. https://doi.org/10.1111/ijfs.12177
Xia, X. F., Kong, B. H., Xiong, Y. L., & Ren, Y. M. (2010). Decreased gelling and emulsifying properties of myofibrillar protein from repeatedly frozen-thawed porcine longissimus muscle are due to protein denaturation and susceptibility to aggregation. Meat Science, 85, 481–486. https://doi.org/10.1016/j.meatsci.2010.02.019
Xie, W. L., Huang, Y., Xiang, Y. Z., Xiong, S. B., Manyande, A., & Du, H. Y. (2020). Insights into the binding mechanism of polyphenols and fish myofibrillar proteins explored using multi-spectroscopic methods. Food and Bioprocess Technology, 13, 797–806. https://doi.org/10.1007/s11947-020-02439-4
Xiong, Y., Li, Q. R., Miao, S., Zhang, Y., Zheng, B. D., & Zhang, L. T. (2019). Effect of ultrasound on physicochemical properties of emulsion stabilized by fish myofibrillar protein and xanthan gum. Innovative Food Science & Emerging Technologies, 54, 225–234. https://doi.org/10.1016/j.ifset.2019.04.013
Xu, M. F., Sun, M. F., Lu, C. R., Han, Y. T., Yao, X., Niu, X. Y., Xu, M. J., & Zhu, Q. (2020). Influence of epicatechin on oxidation-induced physicochemical and digestibility changes in porcine myofibrillar proteins during refrigerated storage. Journal of the Science of Food and Agriculture, 101, 746–753. https://doi.org/10.1002/jsfa.10687
Xu, Q. D., Yu, Z. L., & Zeng, W. C. (2021). Structural and functional modifications of myofibrillar protein by natural phenolic compounds and their application in pork meatball. Food Research International, 148, 110593. https://doi.org/10.1016/j.foodres.2021.110593
Yang, F., Jia, S. N., Liu, J. X., Gao, P., Yu, D. W., Jiang, Q. X., Xu, Y. S., Yu, P. P., Xia, W. S., & Zhan, X. (2019). The relationship between degradation of myofibrillar structural proteins and texture of superchilled grass carp (Ctenopharyngodon idella) fillet. Food Chemistry, 301, 125278. https://doi.org/10.1016/j.foodchem.2019.125278
Yavari Maroufi, L., Ghorbani, M., & Tabibiazar, M. (2020). A gelatin-based film reinforced by covalent interaction with oxidized guar gum containing green tea extract as an active food packaging system. Food and Bioprocess Technology, 13, 1633–1644. https://doi.org/10.1007/s11947-020-02509-7
Zeng, W. C., Zhang, Z., Gao, H., Jia, L. R., & Chen, W. Y. (2012). Characterization of antioxidant polysaccharides from Auricularia auricular using microwave-assisted extraction. Carbohydrate Polymers, 89, 694–700. https://doi.org/10.1016/j.carbpol.2012.03.078
Zeng, W. C., Zhang, Z., & Jia, L. R. (2014). Antioxidant activity and characterization of antioxidant polysaccharides from pine needle (Cedrus deodara). Carbohydrate Polymers, 108, 58–64. https://doi.org/10.1016/j.carbpol.2014.03.022
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This work was financially supported by the National Natural Science Foundation of China [Grant No. 31801548], Sichuan Science and Technology Program [Grant No. 2021YFH0072], and the Fundamental Research Funds for the Central Universities of China [Grant No. 2021CDLZ-21].
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Chong Tan: data curation, methodology, software, investigation, writing—original draft. Qian-Da Xu: validation, software, formal analysis. Nan Chen: methodology, software, data curation, validation. Qiang He: resources, funding acquisition, supervision. Wei-Cai Zeng: conceptualization, formal analysis, investigation, project administration, resources, software, writing—review and editing.
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Tan, C., Xu, QD., Chen, N. et al. Cross-Linking Modifications of Different Phenolic Compounds on Myofibrillar Protein of Common Carp. Food Bioprocess Technol 16, 627–638 (2023). https://doi.org/10.1007/s11947-022-02958-2
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DOI: https://doi.org/10.1007/s11947-022-02958-2