Journal of Agricultural and Food Chemistry
ARTICLE
In conclusion, all tested carbohydrates are capable of disrupt-
ing aggregates formed between procyanidin B3 and trypsin by a
competition mechanism in which the ionic character of carbohy-
drates and their ability to encapsulate procyanidins account for
the quantitative differences observed among them. From a food
industry and nutrition perspective, these effects may be relevant
since food polyphenols are usually ingested together with food
carbohydrates. These effects may contribute to the reduction of
the antinutritional effects ascribed to procyanidins during diges-
tion involving enzymes such as trypsin and others.
(8) Frazier, R. A.; Papadopoulou, A.; Green, R. J. Isothermal titration
calorimetry study of epicatechin binding to serum albumin. J. Pharm.
Biomed. Anal. 2006, 41, 1602–1605.
(9) Pascal, C.; Poncet-Legrand, C.; Imberty, A.; Gautier, C.; Sarni-
Manchado, P.; Cheynier, V.; Vernhet, A. Interactions between a non
glycosylated human proline-rich protein and flavan-3-ols are affected by
protein concentration and polyphenol/protein ratio. J. Agric. Food Chem.
2
007, 55, 4895–4901.
10) Simon, C.; Barathieu, K.; Laguerre, M.; Schmitter, J.-M.;
(
Fouquet, E.; Pianet, I.; Dufourc, E. J. Three-dimensional structure and
dynamics of wine tanninꢀsaliva protein complexes. A multitechnique
approach. Biochemistry 2003, 42, 10385–10395.
(11) Jobstl, E.; O’Connell, J.; Fairclough, J. P. A.; Williamson, M. P.
’
ASSOCIATED CONTENT
Molecular model for astringency produced by polyphenol/protein
interactions. Biomacromolecules 2004, 5, 942–949.
(12) Baxter, N. J.; Lilley, T. H.; Haslam, E.; Williamson, M. P.
Multiple interactions between polyphenols and a salivary proline-rich
protein repeat result in complexation and precipitation. Biochemistry
S
Supporting Information. Classic proton and corre-
b
sponding STD-NMR spectra of a solution of PPT and procya-
nidin B3 with 5 mM glucose in an external capillary. This material
is available free of charge via the Internet at http://pubs.acs.org.
1
997, 36, 5566–5577.
13) Charlton, A. J.; Baxter, N. J.; Lilley, T. H.; Haslam, E.;
(
McDonald, C. J.; Williamson, M. P. Tannin interactions with a full-
length human salivary proline-rich protein display a stronger affinity
than with single proline-rich repeats. FEBS Lett. 1996, 382, 289–92.
’
AUTHOR INFORMATION
Corresponding Author
(14) Luck, G.; Liao, H.; Murray, N. J.; Grimmer, H. R.; Warminski,
*Phone: +351 226 082 858. Fax: +351 226 082 959. E-mail:
E. E.; Williamson, M. P.; Lilley, T. H.; Haslam, E. Polyphenols,
astringency and proline-rich proteins. Phytochemistry 1994, 37,
vfreitas@fc.up.pt.
3
57–371.
15) Pascal, C.; Pat ꢁe , F.; Cheynier, V.; Delsuc, M.-A. Study of the
Funding Sources
This research was supported by the research project grant
(
interactions between a proline-rich protein and a flavan-3-ol by NMR:
Residual structures in the natively unfolded protein provides anchorage
points for the ligands. Biopolymers 2009, 91, 745–756.
(PTDC/AGR-ALI/67579/2006) funding from FCT (Funda c- ~a o
para a Ci ^e ncia e Tecnologia) of Portugal. The authors would like
to thank the NMR Lab at CEMUP (Centro de Materiais da
Universidade do Porto) supported by the grant REDE/1517/
RMN/2005. R. G. would like to acknowledge a PhD grant from
FCT (SFRH/BD/38814/2007).
(16) DeMiglio, P.; Pickering, G. J.; Reynolds, A. G. In Astringent Sub-
Qualities Elicited by Red Wine: The Role of Ethanol and pH, Proceedings of
the International Bacchus to the Future Conference, Ontario, Canada,
May 23ꢀ25, 2002; DeMiglio, P., Pickering, G. J.; Reynolds, A. G., Eds.;
Ontario, 2002; pp 31ꢀ52.
(17) Leung, D.; Abbenante, G.; Fairlie, D. P. Protease inhibitors:
Current status and future prospects. J. Med. Chem. 2000, 43, 305–341.
(18) Weiss, F. U.; Halangk, W.; Lerch, M. M. New advances in
pancreatic cell physiology and pathophysiology. Best Pract. Res., Clin.
Gastroenterol. 2008, 22, 3–15.
’
ACKNOWLEDGMENT
We thank Professor Eurico J. Cabrita and Dr. Mariana
Andrade for the help in setting up and conducting the STD-
NMR experiments.
(
19) Maliar, T.; Jedin ꢁa k, A.; Kadrabov ꢁa , J.; Sturdík, E. Structural
aspects of flavonoids as trypsin inhibitors. Eur. J. Med. Chem. 2004,
9, 241–248.
20) He, Q.; Lu, Y.; Yao, K. Effects of tea polyphenols on the
3
(
’
REFERENCES
activities of α-amylase, pepsin, trypsin and lipase. Food Chem. 2007,
101, 1178–1182.
(
1) Scalbert, A.; Williamson, G. Dietary intake and bioavailability of
polyphenols. J. Nutr. 2000, 130, 2073–2085.
2) Santos-Buelga, C.; Scalbert, A. Proanthocyanidins and tannin-
(21) Huang, H.; Zhao, M. Changes of trypsin in activity and
secondary structure induced by complex with trypsin inhibitors and
tea polyphenol. Eur. Food Res. Technol. 2008, 227, 361–365.
(22) Gon c- alves, R.; Soares, S.; Mateus, N.; de Freitas, V. Inhibition
of trypsin by condensed tannins and wine. J. Agric. Food Chem. 2007,
55, 7596–7601.
(23) Gon c- alves, R.; Mateus, N.; de Freitas, V. Biological relevance of
the interaction between procyanidins and trypsin: A multitechnique
approach. J. Agric. Food Chem. 2010, 58, 11924–11931.
(24) Ariga, T.; Hamano, M. Radical scavenging action and its mode
in procyanidin-b-1 and procyanidin-b-3 from azuki-beans to peroxyl
radicals. Agric. Biol. Chem. 1990, 54, 2499–2504.
(
like compounds: Nature, occurrence, dietary intake and effects on
nutrition and health. J. Sci. Food Agric. 2000, 80, 1094–1117.
(
3) de Freitas, V.; Carvalho, E.; Mateus, N. Study of carbohidrate
influence on protein-tannin aggregation by nephelometry. Food Chem.
003, 81, 503–509.
4) Mateus, N.; Carvalho, E.; de Freitas, V. Influence of the tannin
2
(
structure on the disruption effect of carbohydrates on protein-tannin
aggregates. Anal. Chim. Acta 2003, 1, 135–140.
(
flavonoids with bovine serum albumin: A fluorescence quenching study.
J. Agric. Food Chem. 2005, 53, 158–163.
(
5) Papadopoulou, A.; Green, R. J.; Frazier, R. A. Interaction of
(25) Geissman, T. A.; Yoshimura, N. N. Synthetic proanthocyanidin.
Tetrahedron Lett. 1966, 7, 2669–2673.
6) Soares, S. I.; Gon c- alves, R. M.; Fernandes, I.; Mateus, N.; de
Freitas, V. Mechanistic approach by which polysaccharides inhibit
α-amylase/procyanidin aggregation. J. Agric. Food Chem. 2009, 57,
(26) Delcour, J. A.; Ferreira, D.; Roux, D. G. Synthesis of condensed
tannins. Part 9. The condensation sequence of leucocyanidin with (+)-
catechin and with the resultant procyanidins. J. Chem. Soc., Perkin Trans.
1 1983, 1711–1717.
4
352–4358.
(
7) Poncet-Legrand, C.; Edelmann, A.; Putaux, J. L.; Cartalade, D.;
Sarni-Manchado, P.; Vernhet, A. Poly(l-proline) interactions with
flavan-3-ols units: Influence of the molecular structure and the
polyphenol/protein ratio. Food Hydrocolloids 2006, 20, 687–697.
(27) Coimbra, M. A.; Waldron, K. W.; Selvendran, R. R. Isolation and
characterisation of cell wall polymers from olive pulp (olea europaea l.).
Carbohydr. Res. 1994, 252, 245–262.
1
1801
dx.doi.org/10.1021/jf203060s |J. Agric. Food Chem. 2011, 59, 11794–11802