Insights into the Binding Mechanism of Polyphenols and Fish Myofibrillar Proteins Explored Using Multi-spectroscopic Methods

Abstract

As the most abundant protein existing in fish, myofibrillar protein (MP) is likely to hydrolyze which affects the quality of fish during preservation. Polyphenols, which are some of the most popular antioxidants and antimicrobials, have been widely used in freshwater fish preservation and storage to prevent protein degradation. However, their binding behavior and mechanism is still unclear. In this study, the binding mechanisms of two types of polyphenols (chlorogenic acid (CGA); quercetin (QUE)) and MP extracted from grass carp were investigated through multi-spectroscopic methods. Different spectroscopic methods (fluorescence spectroscopy and synchronous fluorescence spectroscopy) were used to explore the interaction modes between polyphenols and fish-extracted MP. In addition, circular dichroism spectroscopy was used to detect microstructure changes of MP under different preservation approaches. Results showed that nanocomposites were generated when MP interacted with either CGA or QUE. The addition of CGA did not affect the α-helix content of MP, whereas QUE diffused the β-turns of myofibrillar proteins and promoted the formation of α-helices. At the same time, the fluorescence-quenching effect of CGA/QUE on MP was static quenching, and the binding constants, number of binding sites, and corresponding thermodynamic parameters of MP were calculated. It was concluded that the binding of CGA to MP depends on Van der Waals forces and hydrogen bonds, while QUE binds to MPs on the basis of electrostatic interactions. In addition, the fluorescence quenching of MPs with CGA is related to tryptophan and tyrosine residues, while the fluorescence-quenching effect of QUE on MPs is related only to tryptophan residues.

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References

  1. Ashie, I. N., Smith, J. P., & Simpson, B. K. (1996). Spoilage and shelf-life extension of fresh fish and shellfish. Critical Reviews in Food Science & Nutrition, 36(1–2), 87–121.

  2. Bouletis, A. D., Arvanitoyannis, I. S., & Hadjichristodoulou, C. (2017). Application of modified atmosphere packaging on aquacultured fish and fish products: A review. Critical Reviews in Food Science & Nutrition, 57(11), 2263–2285.

  3. Brvar, M., Perdih, A., Oblak, M., Mašič, L. P., & Solmajer, T. (2010). In silico discovery of 2-amino-4-(2,4-dihydroxyphenyl)thiazoles as novel inhibitors of DNA gyrase B. Bioorganic & Medicinal Chemistry Letters, 20(3), 958–962.

  4. Bu, T., Jin, Y., Li, X., Zhang, J., Xu, D., Yang, W., & Lou, Q. (2017). Effect of electron irradiation and bayberry polyphenols on the quality change of yellowfin tuna fillets during refrigerated storage. Radiation Physics and Chemistry, 138, 67–71.

  5. Buddanavar, A. T., & Nandibewoor, S. T. (2017). Multi-spectroscopic characterization of bovine serum albumin upon interaction with atomoxetine. Journal of Pharmaceutical Analysis, 7(3), 148–155.

  6. Cao, Q., Du, H., Huang, Y., Hu, Y., You, J., Liu, R., Xiong, S., & Manyande, A. (2019). The inhibitory effect of chlorogenic acid on lipid oxidation of grass carp (Ctenopharyngodon idellus) during chilled storage. Food and Bioprocess Technology, 12, 2050–2061.

  7. Cao, X. H., Islam, M. N., Chitrakar, B., Duan, Z. H., Xu, W. X., & Zhong, S. Y. (2020). Effect of combined chlorogenic acid and chitosan coating on antioxidant, antimicrobial, and sensory properties of snakehead fish in cold storage. Food Science & Nutrition.

  8. Fidalgo, L. G., Castro, R., Trigo, M., Aubourg, S. P., Delgadillo, I., & Saraiva, J. A. (2019). Quality of fresh Atlantic Salmon (Salmo salar) under hyperbaric storage at low temperature by evaluation of microbial and physicochemical quality indicators. Food and Bioprocess Technology, 12(11), 1895–1906.

  9. Gao, H., Lei, L., Liu, J., Kong, Q., Chen, X., & Hu, Z. (2004). The study on the interaction between human serum albumin and a new reagent with antitumour activity by spectrophotometric methods. Journal of Photochemistry and Photobiology A: Chemistry, 167(2), 213–221.

  10. Gao, W., Li, N., Chen, Y., Xu, Y., Lin, Y., Yin, Y., & Hu, Z. (2010). Study of interaction between syringin and human serum albumin by multi-spectroscopic method and atomic force microscopy. Journal of Molecular Structure, 983(1), 133–140.

  11. García, M. R., Cabo, M. L., Herrera, J. R., Ramilo-Fernández, G., Alonso, A. A., & Balsa-Canto, E. (2017). Smart sensor to predict retail fresh fish quality under ice storage. Journal of Food Engineering, 197, 87–97.

  12. Ge, L., Xu, Y., Xia, W., & Jiang, Q. (2018). Synergistic action of cathepsin B, L, D and calpain in disassembly and degradation of myofibrillar protein of grass carp. Food Research International, 109, 481–488.

  13. Ghaly, A. E., Dave, D., Budge, S., & Brooks, M. S. (2010). Fish spoilage mechanisms and preservation techniques: Review. American Journal of Applied Sciences, 7(7), 859–877.

  14. Guan, W., Ren, X., Li, Y., & Mao, L. (2019). The beneficial effects of grape seed, sage and oregano extracts on the quality and volatile flavor component of hairtail fish balls during cold storage at 4 °C. LWT, 101, 25–31.

  15. Guo, X. Y., Chen, S. N., Cao, J. Y., Zhou, J. Y., Chen, Y. Z., Jamali, M. A., & Zhang, Y. W. (2019). Hydrolysis and oxidation of protein and lipids in dry-salted grass carp (Ctenopharyngodon idella) as affected by partial substitution of NaCl with KCl and amino acids. Rsc Advances, 9(68), 39545–39560.

  16. Hultmann, L., & Rustad, T. (2004). Iced storage of Atlantic salmon (Salmo salar): Effects on endogenous enzymes and their impact on muscle proteins and texture. Food Chemistry, 87(1), 31–41.

  17. Jiang, L., Belwal, T., Huang, H., Ge, Z., Limwachiranon, J., Zhao, Y., Li, L., Ren, G., & Luo, Z. (2019). Extraction and characterization of phenolic compounds from bamboo shoot shell under optimized ultrasonic-assisted conditions: A potential source of nutraceutical compounds. Food and Bioprocess Technology, 12(10), 1741–1755.

  18. Lakowicz, J. R., & Masters, B. R. (1991). Principles of fluorescence spectroscopy, third edition. Die Naturwissenschaften, 78(10), 456.

  19. Li, T., Hu, W., Li, J., Zhang, X., Zhu, J., & Li, X. (2012). Coating effects of tea polyphenol and rosemary extract combined with chitosan on the storage quality of large yellow croaker (Pseudosciaena crocea). Food Control, 25(1), 101–106.

  20. Liu, J., Tian, J. N., Zhang, J., Hu, Z., & Chen, X. (2003). Interaction of magnolol with bovine serum albumin: A fluorescence-quenching study. Analytical & Bioanalytical Chemistry, 376(6), 864–867.

  21. López-García, M. M., Ramil-Novo, L. A., Vázquez-Odériz, M. L., & Romero-Rodríguez, M. A. (2014). Development of a quality index method for freshness assessment of thawed Greenland halibut (Reinhardtius hippoglossoides) stored at chilling temperature. Food and Bioprocess Technology, 7(6), 1847–1852.

  22. Lowry, O. H., Rosebrough, N. J., Farr, A. L., & Randall, R. J. (1951). Protein measurement with the Folin phenol reagent. Journal of Biological Chemistry, 193(1), 265–275.

  23. Lu, H., Zhang, L., Li, Q., & Luo, Y. (2017). Comparison of gel properties and biochemical characteristics of myofibrillar protein from bighead carp (Aristichthys nobilis) affected by frozen storage and a hydroxyl radical-generation oxidizing system. Food Chemistry, 223, 96–103.

  24. Mahdieh, M., Malihe, P., Mohammad Reza, S., Maryam, G., & Jamshidkhan, C. (2013). Investigation on the interaction between cyclophosphamide and lysozyme in the presence of three different kind of cyclodextrins: Determination of the binding mechanism by spectroscopic and molecular modeling techniques. Molecules, 18(1), 789–813.

  25. Mansouri, A., Mousavi, M., Attar, F., Saboury, A. A., & Falahati, M. (2018). Interaction of manganese nanoparticle with cytochrome c: A multi-spectroscopic study. International Journal of Biological Macromolecules, 106, 78–86.

  26. Mariutti, L. R. B., & Bragagnolo, N. (2017). Influence of salt on lipid oxidation in meat and seafood products: A review. Food Research International, 94, 90–100.

  27. Nie, X., Wang, L., Wang, Q., Lei, J., Hong, W., Huang, B., & Zhang, C. (2018). Effect of a sodium alginate coating infused with tea polyphenols on the quality of fresh Japanese sea bass (Lateolabrax japonicas) fillets. Journal of Food Science, 83(6), 1695–1700.

  28. Niu, Y., Xia, Q., Jung, W., & Yu, L. (2019). Polysaccharides-protein interaction of psyllium and whey protein with their texture and bile acid binding activity. International Journal of Biological Macromolecules, 126, 215–220.

  29. Norton, T., & Sun, D.-W. (2008). Recent advances in the use of high pressure as an effective processing technique in the food industry. Food and Bioprocess Technology, 1(1), 2–34.

  30. Ozogul, Y., & Uçar, Y. (2013). The effects of natural extracts on the quality changes of frozen chub mackerel (Scomber japonicus) burgers. Food and Bioprocess Technology, 6(6), 1550–1560.

  31. Paari, A., Naidu, H. K., Kanmani, P., Satishkumar, R., Yuvaraj, N., Pattukumar, V., & Arul, V. (2012). Evaluation of irradiation and heat treatment on antioxidant properties of fruit peel extracts and its potential application during preservation of goat fish Parupenaeus indicus. Food and Bioprocess Technology, 5(5), 1860–1870.

  32. Papuc, C., Goran, G. V., Predescu, C. N., Nicorescu, V., & Stefan, G. (2017). Plant polyphenols as antioxidant and antibacterial agents for shelf-life extension of meat and meat products: Classification, structures, sources, and action mechanisms. Comprehensive Reviews in Food Science and Food Safety, 16(6), 1243–1268.

  33. Peng, X., Wang, X., Qi, W., Su, R., & He, Z. (2016). Affinity of rosmarinic acid to human serum albumin and its effect on protein conformation stability. Food Chemistry, 192, 178–187.

  34. Prasad, V. G. N. V., Krishna, B. V., Swamy, P. L., Rao, T. S., & Rao, G. S. (2014). Antibacterial synergy between quercetin and polyphenolic acids against bacterial pathogens of fish. Asian Pacific Journal of Tropical Disease, 4, S326–S329.

    CAS  Article  Google Scholar 

  35. Qian, Y.-F., Xie, J., Yang, S.-P., Huang, S., Wu, W.-H., & Li, L. (2015). Inhibitory effect of a quercetin-based soaking formulation and modified atmospheric packaging (MAP) on muscle degradation of Pacific white shrimp (Litopenaeus vannamei). LWT - Food Science and Technology, 63(2), 1339–1346.

    CAS  Article  Google Scholar 

  36. Sampels, S. (2015). The effects of storage and preservation technologies on the quality of fish products: A review. Journal of Food Processing & Preservation, 39(6), 1206–1215.

    CAS  Article  Google Scholar 

  37. Sánchez-Zapata, E., Díaz-Vela, J., Pérez-Chabela, M. L., Pérez-Alvarez, J. A., & Fernández-López, J. (2013). Evaluation of the effect of Tiger nut fibre as a carrier of unsaturated fatty acids rich oil on the quality of dry-cured sausages. Food and Bioprocess Technology, 6(5), 1181–1190.

    Article  Google Scholar 

  38. Souilem, S., Fki, I., Kobayashi, I., Khalid, N., Neves, M. A., Isoda, H., Sayadi, S., & Nakajima, M. (2017). Emerging technologies for recovery of value-added components from olive leaves and their applications in food/feed industries. Food and Bioprocess Technology, 10(2), 229–248.

    CAS  Article  Google Scholar 

  39. Subbaiah, K., Majumdar, R. K., Choudhury, J., Priyadarshini, B. M., Dhar, B., Roy, D., Saha, A., & Maurya, P. (2015). Protein degradation and instrumental textural changes in fresh Nile Tilapia (Oreochromis niloticus) during frozen storage. Journal of Food Processing & Preservation, 39(6).

  40. Sun, F., Huang, Q., Hu, T., Xiong, S., & Zhao, S. (2014). Effects and mechanism of modified starches on the gel properties of myofibrillar protein from grass carp. International Journal of Biological Macromolecules, 64(2), 17–24.

    CAS  Article  Google Scholar 

  41. Tolstorebrov, I., Eikevik, T. M., & Bantle, M. (2016a). Effect of low and ultra-low temperature applications during freezing and frozen storage on quality parameters for fish. International Journal of Refrigeration, 63, 37–47.

    CAS  Article  Google Scholar 

  42. Tolstorebrov, I., Eikevik, T. M., & Bantle, T. (2016b). Review: Effect of low and ultra-low temperature applications during freezing and frozen storage on quality parameters for fish. International Journal of Refrigeration, 63, 37–47.

    CAS  Article  Google Scholar 

  43. Wu, H., Zeng, W., Chen, G., Guo, Y., Yao, C., Li, J., & Liang, Z. (2019). Spectroscopic techniques investigation on the interaction of glucoamylase with 1-deoxynojirimycin: Mechanistic and conformational study. Spectrochimica Acta Part A: Molecular and Biomolecular Spectroscopy, 206, 613–621.

    CAS  Article  Google Scholar 

  44. Yang, J. T., Wu, C. S., & Martinez, H. M. (1986). Calculation of protein conformation from circular dichroism. Methods in Enzymology, 130(4), 208–269.

    CAS  Article  Google Scholar 

  45. Yang, F., Jia, S., Liu, J., Gao, P., Yu, D., Jiang, Q., Xu, Y., Yu, P., Xia, W., & Zhan, X. (2019). The relationship between degradation of myofibrillar structural proteins and texture of superchilled grass carp (Ctenopharyngodon idella) fillet. Food Chemistry, 301, 125278.

    CAS  Article  Google Scholar 

  46. Yin Y, Xie M, Wu H, Jiang M, Zheng J & Wei Q (2009) Interaction of calcineurin with its activator, chlorogenic acid revealed by spectroscopic methods. Biochimie, 91(7),820–825.

  47. Zhao, X., Wu, J., Chen, L., & Yang, H. (2019). Effect of vacuum impregnated fish gelatin and grape seed extract on metabolite profiles of tilapia (Oreochromis niloticus) fillets during storage. Food Chemistry, 293, 418–428.

    CAS  Article  Google Scholar 

  48. Zheng, P., Hao, G., Weng, W., & Ren, H. (2019). Antioxidant activities of Hydrolysates from abalone viscera using subcritical water-assisted enzymatic hydrolysis. Food and Bioprocess Technology, 12(6), 910–918.

    CAS  Article  Google Scholar 

  49. Zhou, X., Zhou, D.-Y., Liu, Z.-Y., Yin, F.-W., Liu, Z.-Q., Li, D.-Y., & Shahidi, F. (2019). Hydrolysis and oxidation of lipids in mussel Mytilus edulis during cold storage. Food Chemistry, 272, 109–116.

    CAS  Article  Google Scholar 

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Funding

Financial support of this work was provided by the National Nature Science Foundation of China (Grant No. 31772047), the Fundamental Research Funds for the Central universities (No. 2662019PY031), and the China Agriculture Research System (CARS-45-27).

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Correspondence to Hongying Du.

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Xie, W., Huang, Y., Xiang, Y. et al. Insights into the Binding Mechanism of Polyphenols and Fish Myofibrillar Proteins Explored Using Multi-spectroscopic Methods. Food Bioprocess Technol 13, 797–806 (2020). https://doi.org/10.1007/s11947-020-02439-4

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Keywords

  • Myofibrillar protein
  • Polyphenols
  • Interaction
  • Fluorescence
  • Circular dichroism