Size and molecular flexibility affect the binding of ellagitannins to bovine serum albumin

Journal of Agricultural and Food Chemistry

Volumn 62, Issue 37, 2014, Pages 9186-9194

  Dobreva, Marina A ^a   Green, Rebecca J ^a   Mueller Harvey, Irene ^a   Salminen, Juha Pekka ^b   Howlin, Brendan J ^c   Frazier, Richard A ^a  

^a UNIVERSITY OF READING   (United Kingdom)

^b UNIVERSITY OF TURKU   (Finland)

^c UNIVERSITY OF SURREY   (United Kingdom)

Author keywords

Ellagitannins; Fluorescence; Hydrophobic accessible surface area; Isothermal titration calorimetry; Molecular flexibility; Molecular size

Indexed keywords

BODY FLUIDS; CALORIMETERS; CALORIMETRY; FLAVONOIDS; FLUORESCENCE; FLUORESCENCE SPECTROSCOPY; HYDROPHOBICITY; ISOTHERMS; MAMMALS; QUENCHING; STOICHIOMETRY; SURFACE PLASMON RESONANCE; TANNINS; TITRATION;

ACCESSIBLE SURFACE AREAS; ELLAGITANNINS; ISOTHERMAL TITRATION CALORIMETRY; MOLECULAR FLEXIBILITY; MOLECULAR SIZE;

BINDING SITES;

BOVINAE;

BOVINE SERUM ALBUMIN; PROTEIN BINDING; TANNIN; TANNIN DERIVATIVE;

BINDING SITE; CALORIMETRY; CHEMICAL PHENOMENA; CHEMICAL STRUCTURE; CHEMISTRY; ENTROPY; METABOLISM; SPECTROFLUOROMETRY;

BINDING SITES; CALORIMETRY; ENTROPY; HYDROLYZABLE TANNINS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MOLECULAR STRUCTURE; PROTEIN BINDING; SERUM ALBUMIN, BOVINE; SPECTROMETRY, FLUORESCENCE; TANNINS;

EID: 84924241117     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/jf502174r     Document Type: Article

References (55)

1. Okuda, T.; Ito, H. Tannins of constant structure in medicinal and food plants - hydrolysable tannins and polyphenols related to tannins. Molecules 2011, 16, 2191-2217.
2. Vrhovsek, U.; Guella, G.; Gasperotti, M.; Pojer, E.; Zancato, M.; Mattivi, F. Clarifying the identity of the main ellagitannins in the fruit of the strawberry, Fragaria vesca and Fragaria ananassa Duch. J. Agric. Food Chem. 2012, 60, 2507-2516.
3. Larrosa, M.; Garcia-Conesa, M. T.; Espin, J. C.; Tomas-Barberan, F. A. Ellagitannins, ellagic acid and vascular health. Mol. Aspects Med. 2010, 31, 513-539.
4. Quideau, S.; Genot, E.; Saltel, F.; Douat-Casassus, C.; Delannoy Lopez, D. M. C-glucosidic ellagitannin compounds for use for altering the supra molecular arrangement of actin and for the treatment of osteoporosis, cancer, bacterial infection and viral infection. Int. Patent Appl. WO 2012/113835 A1 (PCT/EP2012/053017), 2012.
5. Quideau, S.; Deffieux, D.; Douat-Casassus, C.; Pouységu, L. Plant polyphenols: chemical properties, biological activities, and synthesis. Angew. Chem., Int. Ed. 2011, 50, 5099-5104.
6. Scalbert, A.; Andres-Lacueva, C.; Arita, M.; Kroon, P.; Manach, C.; Urpi-Sarda, M.; Wishart, D. Databases on food phytochemicals and their health-promoting effects. J. Agric. Food Chem. 2011, 59, 4331- 4348.
7. Rothwell, J. A.; Urpi-Sarda, M.; Boto-Ordonez, M.; Knox, C.; Llorach, R.; Eisner, R.; Cruz, J.; Neveu, V.; Wishart, D.; Manach, C.; Andres-Lacueva, C.; Scalbert, A. Phenol-Explorer 2.0: a major update of the Phenol-Explorer database integrating data on polyphenol metabolism and pharmacokinetics in humans and experimental animals. Database 2012, DOI: 10.1093/database/bas031.
8. Fotschki, B.; Milala, J.; Jurgonski, A.; Karlińska, E.; Zdunczyk, Z.; Juskiewicz, J. Strawberry ellagitannins the positive effects of dietary fructooligosaccharides in rat cecum. J. Agric. Food Chem. 2012, 62, 5871-5880.
9. Salminen, J. P.; Karonen, M.; Sinkkonen, J. Chemical ecology of tannins: recent developments in tannin chemistry reveal new structures and structure-activity patterns. Chem.-Eur. J. 2011, 17, 2806-2816.
10. Quideau, S.; Douat-Casassus, C.; Delannoy López, D. M.; Di Primo, C.; Chassain, S.; Jacquet, R.; Saltel, F.; Genot, E. Binding of filamentous actin and winding into fibrillar aggregates by the polyphenolic C-glucosidic ellgitannin vescalagin. Angew. Chem., Int. Ed. 2011, 50, 5099-5104.
11. Okuda, T. Systematics and health effects of chemically distinct tannins in medicinal plants. Phytochemistry 2005, 66, 2012-2031.
12. Kashiwada, Y.; Nonaka, G.-I.; Nishioka, I.; Lee, K. J.-H.; Bori, I.; Fukushima, Y.; Bastow, K. F.; Lee, K.-H. Tannins as potent inhibitors of DNA topoisomerase-II in vitro. J. Pharm. Sci. 1993, 82, 487-492.
13. Quideau, S.; Jourdes, M.; Saucier, C.; Glories, Y.; Pardon, P.; Baudry, C. DNA topoisomerase inhibitor acutissimin A and other flavano-ellagitannins in red wine. Angew. Chem., Int. Ed. 2003, 42, 6012-6014.
14. Auzanneau, C.; Montaudon, D.; Jacquet, R.; Puyo, S.; Pouységu, L.; Deffieux, D.; Elkaoukabi-Chaibi, A.; De Giorgi, F.; Ichas, F.; Quideau, S.; Pourquier, P. The polyphenolic ellagitannin vescalagin acts as a preferential catalytic inhibitor of the α isoform of human DNA topoisomerase II. Mol. Pharmacol. 2012, 82, 124-141.
15. Kiss, A. K.; Granica, S.; Stolarczyk, M.; Melzig, M. F. Epigenetic modulation of mechanisms involved in inflammation: influence of selected polyphenolic substances on histone acetylation state. Food Chem. 2012, 131, 1015-1020.
16. Cala, O.; Dufourc, E. J.; Fouquet, E.; Manigand, C.; Laguerre, M.; Pianet, I. The colloidal state of tannins impacts the nature of their interaction with proteins: the case of salivary proline-rich protein/procyanidins binding. Langmuir 2012, 28, 17410-17418.
17. Fraga, C. G.; Galleano, M.; Verstraeten, S. V.; Oteiza, P. I. Basic biochemical mechanisms behind the health benefits of polyphenols. Mol. Aspects Med. 2010, 31, 435-445.
18. Bacon, J. R.; Rhodes, M. J. C. Binding affinity of hydrolyzable tannins to parotid saliva and to proline-rich proteins derived from it. J. Agric. Food Chem. 2000, 48, 838-843.
19. Frazier, R. A.; Deaville, E. R.; Green, R. J.; Willoughby, I.; Stringano, E.; Plant, J.; Mueller-Harvey, I. Interactions of tea tannins and condensed tannins with proteins. J. Pharm. Biomed. Anal. 2010, 51, 490-495.
20. Canon, F.; Ballivian, R.; Chirot, F.; Antoine, R.; Sarni- Manchado, P.; Lemoine, J.; Dugourd, P. Folding of a salivary intrinsically disordered protein upon binding to tannins. J. Am. Chem. Soc. 2011, 133, 7847-7852.
21. Delannoy, D.; Deffieux, D.; Di Primo, C.; Quideau, S. Study in real time of polyphenol-protein interactions by surface plasmon resonance. Polyphenols Commun. 2012, 1, 59-60.
22. Simon, C.; Barathieu, K.; Laguerre, M.; Schmitter, J.-M.; Fouquet, E.; Pianet, I.; Dufourc, E. J. Three-dimensional structure and dynamics of wine tannin-saliva protein complexes. A multi technique approach. Biochemistry 2003, 42, 10385-10395.
23. Hagerman, A. E. Chapter 3. Fifty years of polyphenol-protein complexes. In Recent Advances in Polyphenol Research; Cheynier, V., Sarni-Manchado, P., Quideau, S., Eds.; Wiley: Oxford, UK, 2012; Vol. 3, pp 71-97.
24. Deaville, E. R.; Green, R. J.; Mueller-Harvey, I.; Willoughby, I.; Frazier, R. A. Hydrolysable tannin structures influence relative binding strengths to globular or random coil proteins. J. Agric. Food Chem. 2007, 55, 4554-4561.
25. Hagerman, A. E.; Butler, L. G. The specificity of proanthocyanidin-protein interactions. J. Biol. Chem. 1981, 256, 4494-4497.
26. Bazylko, A.; Kiss, K. K.; Kowalski, J. High-performance thinlayer chromatography method for quantitative determination of oenothein B and quercetin glucuronide in aqueous extract of Epilobii angustifolii herba. J. Chromatogr., A 2007, 1173, 146-150.
27. Giner-Chavez, B.-I.; Van Soest, P. J.; Robertson, J. B.; Lascano, C.; Pell, A. N. Comparison of the precipitation of alfalfa leaf protein and bovine serum albumin by tannins in the radial diffusion method. J. Sci. Food Agric. 1997, 74, 513-523.
28. Dobreva, M. A.; Frazier, R. A.; Mueller-Harvey, I.; Clifton, L. A.; Gea, A.; Green, R. J. Binding of pentagalloyl glucose to two globular proteins occurs via multiple surface sites. Bio macromolecules 2011, 12, 710-715.
29. Hofmann, T.; Glabasnia, A.; Schwarz, B.; Wisman, K. N.; Gangwer, K. A.; Hagerman, A. E. Protein binding and astringent taste of a polymeric procyanidin, 1, 2, 3, 4, 6-penta-O-galloyl-β-D-glucopyranose, castalagin, and grandinin. J. Agric. Food Chem. 2006, 54, 9503- 9509.
30. Li, M.; Jia, X.; Yang, J.; Deng, J.; Zhao, G. Effect of tannic acid on properties of soybean (Glycine max) seed ferritin: a model for interaction between naturally-occurring components in foodstuffs. Food Chem. 2012, 133, 410-415.
31. Stojadinovic, M.; Radosavljevic, J.; Ognjenovic, J.; Vesic, J.; Prodic, I.; Stanic-Vucinic, D.; Cirkovic Velickovic, T. Binding affinity between dietary polyphenols and β-lactoglobulin negatively correlates with the protein susceptibility to digestion and total antioxidant activity of complexes formed. Food Chem. 2013, 136, 1263-1271.
32. Dufour, C.; Dangles, O. Flavonoid-serum albumin complexation: determination of binding constants and binding sites by fluorescence spectroscopy. Bio chim. Bio phys. Acta 2005, 1721, 164- 173.
33. Skrt, M.; Benedik, E.; Podlipnik, C.; Ulrih, N. P. Interactions of different polyphenols with bovine serum albumin using fluorescence quenching and molecular docking. Food Chem. 2012, 135, 2418-2424.
34. Li, M.; Hagerman, A. E. Interactions between plasma proteins and naturally occurring polyphenols. Curr. Drug Metab. 2013, 14, 432-445.
35. Zhang, Y.; Shi, S.; Chen, X.; Zhang, W.; Huang, K.; Peng, M. Investigation on the interaction between Ilaprazole and bovine serum albumin without or with different C-ring flavonoids from the viewpoint of food-drug interference. J. Agric. Food Chem. 2011, 59, 8499-8506.
36. Huang, B. X.; Kim, H.-H.; Dass, C. Probing three-dimensional structure of bovine serum albumin by chemical cross-linking and mass spectrometry. J. Am. Soc. Mass Spectrom. 2004, 15, 1237-1247.
37. Moilanen, J.; Salminen, J.-P. Ecologically neglected tannins and their biologically relevant activity: chemical structures of plant ellagitannins reveal their in vitro oxidative activity at high pH. Chemoecology 2008, 18, 73-83.
38. O'Brien, R.; Ladbury, J. E.; Chowdhry, B. Z. Isothermal titration calorimetry of bio molecules. In Protein-Ligand Interactions: Hydrodynamics and Calorimetry; Harding, S. E., Chowdhry, B. Z., Eds.; Oxford University Press: Oxford, UK, 2001; pp 263-286.
39. Frazier, R. A.; Papadopoulou, A.; Mueller-Harvey, I.; Kissoon, D.; Green, R. J. Probing protein-tannin interactions by isothermal titration micro calorimetry. J. Agric. Food Chem. 2003, 51, 5189-5195.
40. Freire, E.; Mayorga, O. L.; Straume, M. Isothermal titration calorimetry. Anal. Chem. 1990, 62, A950-A959.
41. Chi, Z.; Liu, R.; Zhang, H. Noncovalent interaction of oxytetracycline with the enzyme trypsin. Bio macromolecules 2010, 11, 2454-2459.
42. Lakowicz, J. R. Principles of Fluorescence Spectroscopy, 2nd ed.; Kluwer Academic/Plenum Publishers: New York, 1999; p 698.
43. Vivas, N.; Laguerre, M.; Pianet de Boissel, I.; Vivas de Gaulejac, N.; Nonier, M.-F. Conformational interpretation of vescalagin and castalagin physicochemical properties. J. Agric. Food Chem. 2004, 52, 2073-2078.
44. McManus, J. P.; Davis, K. G.; Beart, J. E.; Gaffney, S. H.; Lilley, T. H.; Haslam, E. Polyphenol interactions. Part I. Introduction: some observations on the reversible complexation of polyphenols with proteins and polysaccharides. J. Chem. Soc., Perkin Trans. 2 1985, 1429-1438.
45. Charlton, A. J.; Baxter, N. J.; Khan, M. L.; Moir, A. J. G.; Haslam, E.; Davies, A. P.; Williamson, M. P. Polyphenol/peptide binding and precipitation. J. Agric. Food Chem. 2002, 50, 1593-1601.
46. Mishra, B.; Barik, A.; Priyadarsini, K. I.; Mohan, H. Fluorescence spectroscopy studies on binding of a flavanoid antioxidant quercetin to serum albumins. J. Chem. Sci. 2005, 117, 641-647.
47. Tian, J.; Liu, J.; Tina, X.; Hu, Z.; Chen, X. G. Study of the interaction of kaemp ferol with bovine serum albumin. J. Mol. Struct. 2004, 691, 197-202.
48. Tian, J.; Liu, J.; Hu, Z.; Chen, X. G. Interaction of wogonin with bovine serum albumin. Bioorg. Med. Chem. 2005, 13, 4124-4129.
49. Lorrain, B.; Dangles, O.; Genot, C.; Dufour, C. Chemical modeling of heme-induced lipid oxidation in gastric conditions and inhibition by dietary polyphenols. J. Agric. Food Chem. 2010, 58, 676- 683.
50. Maiti, T. K.; Gosh, K. S.; Dasgupta, S. Interaction of (-)-epigallocatchin-3-gallate with human serum albumin: fluorescence, Fourier transform infrared, circular dichroism, and docking studies. Protein Struct. Funct. Genet. 2006, 64, 355-362.
51. Zhang, G.; Wang, L.; Pan, J. Probing the binding of the flavonoid diosmetin to human serum albumin by multi spectroscopic techniques. J. Agric. Food Chem. 2012, 60, 2721-2729.
52. Xiao, J.; Zhao, Y.; Wang, H.; Yuan, Y.; Yang, F.; Zhang, C.; Yamamoto, K. Non covalent interaction of dietary polyphenols with common human plasma proteins. J. Agric. Food Chem. 2011, 59, 10747-10754.
53. Zhu, M. J.; Phillipson, J. D.; Greengrass, P. M.; Bowery, N. E.; Cai, Y. Plant polyphenols: biologically active molecules or nonselective binders to protein? Phytochemistry 1997, 44, 441-447.
54. Chandler, D. Interfaces and the driving force of hydrophobic assembly. Nature 2005, 437, 640-647.
55. Butler, L. G.; Riedl, D. J.; Lebryk, D. G.; Blytt, H. J. Interaction of proteins with sorghum tannin: mechanisms, specificity and significance. J. Am. Oil Chem. Soc. 1984, 61, 916-920.