Skip to main content
SpringerLink
Log in

The non-covalent interacting forces and scavenging activities to three free radicals involved in the caseinate–flavonol (kaempferol and quercetin) complexes

  • Original Paper
  • Published:
Journal of Food Measurement and Characterization Aims and scope Submit manuscript

Abstract

Polyphenolic substances kaempferol and quercetin are major flavonols found in plant foods, while caseins are major protein fractions in milk. In this study, the non-covalent interactions involved in the formation of caseinate–flavonol complexes as well as the resultant scavenging activities to three free radicals were assessed by multi-spectroscopic, molecular docking, and chemical assays. The results revealed that the binding of kaempferol/quercetin to caseinate was through a mode of energy transfer, resulting in fluorescence quenching of caseinate; meanwhile, both hydrophobic interaction and H-bonds were the forces involved in the resultant non-covalent caseinate–flavonol interactions. The results from UV-absorption and three-dimensional fluorescence spectra indicated that the two flavonols induced conformational change of caseinate. Moreover, quercetin with two hydroxyl groups at the carbon-4ʹ and -5ʹ positions of the B-ring exerted higher affinity to caseinate than kaempferol with one hydroxyl group at the carbon 4ʹ-position of the B-ring. In addition, the caseinate–quercetin complexes had higher scavenging activities against the DPPH, ABTS, and hydroxyl radicals than the caseinate–kaempferol complexes. In conclusion, both chemical structures and especially hydroxyl group numbers of flavonols are critical to the non-covalent casein–flavonol interactions and radical scavenging activities of the resultant complexes.

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
Fig. 6

Similar content being viewed by others

References

  1. E. Middleton, C. Kandaswami, T.C. Theoharides, The effects of plant flavonoids on mammalian cells: implications for inflammation, heart disease, and cancer. Pharmacol. Rev. 52, 673–751 (2000). https://doi.org/10.1006/phrs.2000.0734

    Article  CAS  PubMed  Google Scholar 

  2. O.L. Woodman, E.C. Chan, Vascular and anti-oxidant actions of flavonols and flavones. Clin. Exp. Pharmacol. P. 31, 786–790 (2004). https://doi.org/10.1111/j.1440-1681.2004.04072.x

    Article  CAS  Google Scholar 

  3. P. Knekt, J. Kumpulainen, R. Järvinen, H. Rissanen, M. Heliövaara, A. Reunanen, T. Hakulinen, A. Aromaa, Flavonoid intake and risk of chronic diseases. Am. J. Clin. Nutr. 76, 560–568 (2002). https://doi.org/10.1093/ajcn/76.3.560

    Article  CAS  PubMed  Google Scholar 

  4. A. Scalbert, G. Williamson, Dietary intake and bioavailability of polyphenols. J. Nutr. 130, 2073S-2085S (2000). https://doi.org/10.1093/jn/130.8.2073S

    Article  CAS  PubMed  Google Scholar 

  5. A. Crozier, I.B. Jaganath, M.N. Clifford, Dietary phenolics: chemistry, bioavailability and effects on health. Nat. Prod. Rep. 26, 1001 (2009). https://doi.org/10.1039/b802662a

    Article  CAS  PubMed  Google Scholar 

  6. F. Perez-Vizcaino, J. Duarte, Flavonlos and cardiovascular disease. Mol. Aspects Med. 31, 478–494 (2010). https://doi.org/10.1016/j.mam.2010.09.002

    Article  CAS  PubMed  Google Scholar 

  7. J.M. Calderón-Montaño, E. Burgos-Morón, C. Pérez-Guerrero, M. López-Lázaro, A review on the dietary flavonoid kaempferol. Mini-Rev. Med. Chem. 11, 298–344 (2011). https://doi.org/10.2174/138955711795305335

    Article  PubMed  Google Scholar 

  8. A.W. Boots, G.R.M.M. Haenen, A. Bast, Health effects of quercetin: from antioxidant to nutraceutical. Eur. J. Pharmacol. 585, 325–337 (2008). https://doi.org/10.1016/j.ejphar.2008.03.008

    Article  CAS  PubMed  Google Scholar 

  9. S. Burda, W. Oleszek, Antioxidant and antiradical activities of flavonoids. J. Agric. Food Chem. 49, 2774–2779 (2001). https://doi.org/10.1021/jf001413m

    Article  CAS  PubMed  Google Scholar 

  10. M. Rogozinska, M. Biesaga, Decomposition of flavonols in the presence of saliva. Appl. Sci.—Basel 10, e7511 (2020). https://doi.org/10.3390/app10217511

    Article  CAS  Google Scholar 

  11. Z. Allahdad, M. Varidi, R. Zadmard, A.A. Saboury, Spectroscopic and docking studies on the interaction between caseins and β-carotene. Food Chem. 255, 187–196 (2018). https://doi.org/10.1016/j.foodchem.2018.01.143

    Article  CAS  PubMed  Google Scholar 

  12. C.S. Ranadheera, W.S. Liyanaarachchi, J. Chandrapala, M. Dissanayake, T. Vasiljevic, Utilizing unique properties of caseins and the casein micelle for delivery of sensitive food ingredients and bioactives. Trends Food Sci. Technol. 57, 178–187 (2016). https://doi.org/10.1016/j.tifs.2016.10.005

    Article  CAS  Google Scholar 

  13. T.H. Quan, S. Benjakul, T. Sae-leaw, A.K. Balange, S. Maqsood, Protein-polyphenol conjugates: antioxidant property, functionalities and their applications. Trends Food Sci. Technol. 91, 507–517 (2019). https://doi.org/10.1016/j.tifs.2019.07.049

    Article  CAS  Google Scholar 

  14. T. Ozdal, E. Capanoglu, F. Altay, A review on protein-phenolic interactions and associated changes. Food Res. Int. 51, 954–970 (2013). https://doi.org/10.1016/j.foodres.2013.02.009

    Article  CAS  Google Scholar 

  15. J. Jiang, Z. Zhang, J. Zhao, Y. Liu, The effect of non-covalent interaction of chlorogenic acid with whey protein and casein on physicochemical and radical-scavenging activity of in vitro protein digests. Food Chem. 268, 334–341 (2018). https://doi.org/10.1016/j.foodchem.2018.06.015

    Article  CAS  PubMed  Google Scholar 

  16. Y.F. Wang, X.Y. Wang, Binding, stability, and antioxidant activity of quercetin with soy protein isolate particles. Food Chem. 188, 24–29 (2015). https://doi.org/10.1016/j.foodchem.2015.04.127

    Article  CAS  PubMed  Google Scholar 

  17. S. Dubeau, G. Samson, H.A. Tajmir-Riahi, Dual effect of milk on the antioxidant capacity of green, Darjeeling and English breakfast teas. Food Chem. 122, 539–545 (2010). https://doi.org/10.1016/j.foodchem.2010.03.005

    Article  CAS  Google Scholar 

  18. M.J.T.J. Arts, G.R.M.M. Haenen, L.C. Wilms, S.A.J.N. Beetstra, C.G.M. Heijnen, H.P. Voss, A. Bast, Interactions between flavonoids and proteins: effects on the total antioxidant capacity. J. Agric. Food Chem. 50, 1184–1187 (2002). https://doi.org/10.1021/jf010855a

    Article  CAS  PubMed  Google Scholar 

  19. S. Poungchawanwong, W. Klaypradit, Q.Q. Li, J. Wang, H. Hou, Interaction effect of phenolic compounds on Alaska Pollock skin gelatin and associated changes. LWT-Food Sci. Technol. 133, e110018 (2020). https://doi.org/10.1016/j.lwt.2020.110018

    Article  CAS  Google Scholar 

  20. G.Y. Ren, H. Sun, J.Y. Guo, J.L. Fan, G. Li, S.W. Xu, Molecular mechanism of interaction between resveratrol and trypsin by spectroscopy and molecular docking. Food Funct. 10, 3291–3302 (2019). https://doi.org/10.1039/c9fo00183b

    Article  CAS  PubMed  Google Scholar 

  21. F. Mehranfar, A.K. Bordbar, H. Parastar, A combined spectroscopic, molecular docking and molecular dynamic simulation study on the interaction of quercetin with β–casein nanoparticles. J. Photoch. Photobio. B. 127, 100–107 (2013). https://doi.org/10.1016/j.jphotobiol.2013.07.019

    Article  CAS  Google Scholar 

  22. X.Y. Gao, Y.L. He, Y.C. Kong, X.Y. Mei, Y.P. Huo, Y. He, J.L. Liu, Elucidating the interaction mechanism of eriocitrin with β-casein by multi-spectroscopic and molecular simulation methods. Food Hydrocoll. 94, 63–70 (2019). https://doi.org/10.1016/j.foodhyd.2019.03.006

    Article  CAS  Google Scholar 

  23. W. Brandwilliams, M.E. Cuveller, C. Berset, Use of a free radical method to evaluate antioxidant activity. LWT—Food Sci. Technol. 28, 25–30 (1995). https://doi.org/10.1016/s0023-6438(95)80008-5

    Article  CAS  Google Scholar 

  24. R. Re, N. Pellegrini, A. Proteggente, A. Pannala, M. Yang, C. Rice-Evans, Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radical Biol. Med. 26, 1231–1237 (1999). https://doi.org/10.1016/s0891-5849(98)00315-3

    Article  CAS  Google Scholar 

  25. N. Smirnoff, Q.J. Cumbes, Hydroxyl radical scavenging activity of compatible solutes. Phytochemistry 28, 1057–1060 (1989). https://doi.org/10.1016/0031-9422(89)80182-7

    Article  CAS  Google Scholar 

  26. H. Bi, L. Tang, X. Gao, J. Jia, H. Lv, Spectroscopic analysis on the binding interaction between tetracycline hydrochloride and bovine proteins β-casein, α-lactalbumin. J. Lumin. 178, 72–83 (2016). https://doi.org/10.1016/j.jlumin.2016.05.048

    Article  CAS  Google Scholar 

  27. F. Mohanmmadi, M. Moeeni, Analysis of binding interaction of genistein and kaempferol with bovine alpha-lactalbumin. J. Funct. Foods 12, 458–467 (2015). https://doi.org/10.1016/j.jff.2014.12.012

    Article  CAS  Google Scholar 

  28. S.C. Lei, D.L. Xu, M. Saeeduddin, A. Riaz, X.X. Zeng, Characterization of molecular structures of theaflavins and the iteractions with bovine serum albumin. J. Food Sci. Tech. 54, 3421–3432 (2017). https://doi.org/10.1007/s13197-017-2791-5

    Article  CAS  Google Scholar 

  29. Y. Lang, E. Li, X. Meng, J. Tian, X. Ran, Y. Zhang, Z.H. Zang, W.S. Wang, B. Li, Protective effects of bovine serum albumin on blueberry anthocyanins under illumination conditions and their mechanism analysis. Food Res. Int. 122, 487–495 (2019). https://doi.org/10.1016/j.foodres.2019.05.021

    Article  CAS  PubMed  Google Scholar 

  30. N. Tayeh, T. Rungassamy, J.R. Albani, Fluorescence spectral resolution of tryptophan residues in bovine and human serum albumins. J. Pharmaceut. Biomed. 50, 107–116 (2009). https://doi.org/10.1016/j.jpba.2009.03.015

    Article  CAS  Google Scholar 

  31. I.J. Arroyo-Maya, J. Campos-Terán, A. Hernández-Arana, D.J. McClements, Characterization of flavonoid-protein interactions using fluorescence spectroscopy: binding of pelargonidin to dairy proteins. Food Chem. 213, 431–439 (2016). https://doi.org/10.1016/j.foodchem.2016.06.105

    Article  CAS  PubMed  Google Scholar 

  32. Z.H. Zang, S.R. Chou, J.L. Tian, Y.X. Lang, Y.X. Shen, X.L. Ran, N.X. Gao, B. Li, Effect of whey protein isolate on the stability and antioxidant capacity of blueberry anthocyanins: a mechanistic and in vitro simulation study. Food Chem. 336, e127700 (2021). https://doi.org/10.1016/j.foodchem.2020.127700

    Article  CAS  Google Scholar 

  33. C.D. Kanakis, I. Hasni, P. Bourassa, P.A. Tarantilis, M.G. Polissiou, H. Tajmir-Riahi, Milk β-lactoglobulin complexes with tea polyphenols. Food Chem. 127, 1046–1055 (2011). https://doi.org/10.1016/j.foodchem.2011.01.079

    Article  CAS  PubMed  Google Scholar 

  34. H. Ojha, K. Mishra, M.I. Hassan, N.K. Chaudhury, Spectroscopic and isothermal titration calorimetry studies of binding interaction of ferulic acid with bovine serum albumin. Thermochim. Acta 548, 56–64 (2012). https://doi.org/10.1016/j.tca.2012.08.016

    Article  CAS  Google Scholar 

  35. Z. Yuksel, E. Avci, Y.K. Erdem, Characterization of binding interactions between green tea flavonoids and milk proteins. Food Chem. 121, 450–456 (2010). https://doi.org/10.1016/j.foodchem.2009.12.064

    Article  CAS  Google Scholar 

  36. T. Li, P. Hu, T.T. Dai, P.Y. Li, X.Q. Ye, J. Chen, C.M. Liu, Comparing the binding interaction between β-lactoglobulin and flavonoids with different structure by multi-spectroscopy analysis and molecular docking. Spectrochim. Acta. A. 201, 197–206 (2018). https://doi.org/10.1016/j.saa.2018.05.011

    Article  CAS  Google Scholar 

  37. D.P. Acharya, L. Sanguansri, M.A. Augustin, Binding of resveratrol with sodium caseinate in aqueous solutions. Food Chem. 141, 1050–1054 (2013). https://doi.org/10.1016/j.foodchem.2013.03.037

    Article  CAS  PubMed  Google Scholar 

  38. M.C.S. Sastry, M.S.N. Rao, Binding of chlorogenic acid by the isolated polyphenol-free 11 S protein of sunflower (Helianthus annuus) seed. J. Agric. Food Chem. 38, 2103–2110 (1990). https://doi.org/10.1021/jf00102a001

    Article  CAS  Google Scholar 

  39. J. Wang, X.H. Zhao, Degradation kinetics of fisetin and quercetin in solutions affected by medium pH, temperature and coexisted proteins. J. Serb. Chem. Soc. 81, 243–253 (2016). https://doi.org/10.2298/JSC150706092W

    Article  CAS  Google Scholar 

  40. L. Jakobek, Interactions of polyphenols with carbohydrates, lipids and proteins. Food Chem. 175, 556–567 (2015). https://doi.org/10.1016/j.foodchem.2014.12.013

    Article  CAS  PubMed  Google Scholar 

  41. J.B. Xiao, F.F. Mao, F. Yang, Y.L. Zhao, C. Zhang, K. Yamamoto, Interaction of dietary polyphenols with bovine milk proteins: molecular structure affinity relationship and influencing bioactivity aspects. Mol. Nutr. Food Res. 55, 1637–1645 (2011). https://doi.org/10.1002/mnfr.201100280

    Article  CAS  PubMed  Google Scholar 

  42. I. Hasni, P. Bourassa, S. Hamdani, G. Samson, R. Carpentier, H.A. Tajmir-Riahi, Interaction of milk α- and β-caseins with tea polyphenols. Food Chem. 126, 630–639 (2011). https://doi.org/10.1016/j.foodchem.2010.11.087

    Article  CAS  Google Scholar 

  43. C.M. Ma, X.H. Zhao, Depicting the non-covalent interaction of whey proteins with galangin or genistein using the multi-spectroscopic techniques and molecular docking. Foods 8, e360 (2019). https://doi.org/10.3390/foods8090360

    Article  CAS  PubMed  Google Scholar 

  44. F. Liu, C. Sun, W. Yang, F. Yuan, Y. Gao, Structural characterization and functional evaluation of lactoferrin-polyphenol conjugates formed by free-radical graft copolymerization. RSC Adv. 5, 15641–15651 (2015). https://doi.org/10.1039/c4ra10802g

    Article  CAS  Google Scholar 

  45. S.D. Zhou, Y.F. Lin, X. Xu, L. Meng, M.S. Dong, Effect of non-covalent and covalent complexation of (-)-epigallocatechin gallate with soybean protein isolate on protein structure and in vitro digestion characteristics. Food Chem. 309, e125718 (2019). https://doi.org/10.1016/j.foodchem.2019.125718

    Article  CAS  Google Scholar 

  46. M. Joyeux, A. Lobstein, R. Anton, F. Mortier, Comparative antilipoperoxidant, antinecrotic and scavenging properties of terpenes and biflavones from Ginkgo and some flavonoids. Planta Med. 61, 126–129 (1995). https://doi.org/10.1055/s-2006-958030

    Article  CAS  PubMed  Google Scholar 

  47. C.D. Kanakis, P.A. Tarantilis, M.G. Polissiou, H.A. Tajmir-Riahi, Probing the binding sites of resveratrol, genistein, and curcumin with milk β-lactoglobulin. J. Biomol. Struct. Dyn. 31, 1455–1466 (2013). https://doi.org/10.1080/07391102.2012.742461

    Article  CAS  PubMed  Google Scholar 

  48. H.M. Rawel, D. Czjka, S. Rohn, J. Kroll, Interactions of different phenolic acids and flavonoids with soy proteins. In. J. Biol. Macromol. 30, 137–150 (2002). https://doi.org/10.1016/S0141-8130(02)00016-8

    Article  CAS  Google Scholar 

  49. S.V.E. Prigent, A.G.J. Voragen, G.A. van Koningsveld, A. Baron, C.M.G.C. Renard, H. Gruppen, Interactions between globular proteins and procyanidins of different degrees of polymerization. J. Dairy Sci. 92, 5843–5853 (2009). https://doi.org/10.3168/jds.2009-2261

    Article  CAS  PubMed  Google Scholar 

  50. Q. Zhao, X.J. Yu, C.S. Zhou, A.E.A. Yagoub, H.L. Ma, Effects of collagen and casein with phenolic compounds interactions on protein in vitro digestion and antioxidation. LWT—Food Sci. Technol. 124, e109192 (2020). https://doi.org/10.1016/j.lwt.2020.109192

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This study was funded by the Scientific Research Foundation of Guangdong University of Petrochemical Technology (Project No. 2020rc026), National High Technology Research and Development Program (“863” Program) of China (Project No. 2013AA102205), and Natural Science Foundation of Guangdong Province (Project No. 2016A030307027). The authors thank the anonymous reviewers for their valuable advice

Author information

Authors and Affiliations

  1. School of Biology and Food Engineering, Guangdong University of Petrochemical Technology, Maoming, 525000, People’s Republic of China

    Chun-Min Ma, Jun-Ren Zhao, Fei-Fei Wu, Qiang Zhang & Xin-Huai Zhao

  2. College of Food Science, Northeast Agricultural University, Harbin, 150030, People’s Republic of China

    Chun-Min Ma

  3. Research Centre of Food Nutrition and Human Healthcare, Guangdong University of Petrochemical Technology, Maoming, 525000, People’s Republic of China

    Jun-Ren Zhao, Fei-Fei Wu, Qiang Zhang & Xin-Huai Zhao

  4. Maoming Branch, Guangdong Laboratory for Lingnan Modern Agriculture, Guangdong University of Petrochemical Technology, Maoming, 525000, Guangdong, People’s Republic of China

    Xin-Huai Zhao

Authors
  1. Chun-Min Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jun-Ren Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Fei-Fei Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Qiang Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xin-Huai Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Xin-Huai Zhao.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

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

Ma, CM., Zhao, JR., Wu, FF. et al. The non-covalent interacting forces and scavenging activities to three free radicals involved in the caseinate–flavonol (kaempferol and quercetin) complexes. Food Measure 16, 114–125 (2022). https://doi.org/10.1007/s11694-021-01157-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11694-021-01157-5

Keywords

Search

Navigation