Protein precipitation behavior of condensed tannins from Lotus pedunculatus and Trifolium repens with different mean degrees of polymerization

Journal of Agricultural and Food Chemistry

Volumn 63, Issue 4, 2015, Pages 1160-1168

  Zeller, Wayne E ^a   Sullivan, Michael L ^a   Mueller Harvey, Irene ^b   Grabber, John H ^a   Ramsay, Aina ^b   Drake, Chris ^b   Brown, Ronald H ^b  

^a U S DAIRY FORAGE RESEARCH CENTER   (United States)

^b UNIVERSITY OF READING   (United Kingdom)

Author keywords

condensed tannin; NMR; nuclear magnetic resonance spectroscopy; proanthocyanidin; protein precipitation; tannin protein complexes; thiolysis

Indexed keywords

BODY FLUIDS; FLAVONOIDS; MAGNETIC RESONANCE SPECTROSCOPY; NUCLEAR MAGNETIC RESONANCE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; POLYMERIZATION; TANNINS;

CONDENSED TANNINS; PROANTHOCYANIDINS; PROTEIN COMPLEXES; PROTEIN PRECIPITATION; THIOLYSIS;

PROTEINS;

BOVINAE; LOTUS PEDUNCULATUS; LOTUS ULIGINOSUS; MEDICAGO SATIVA; TRIFOLIUM REPENS;

EID: 84922454342     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/jf504715p     Document Type: Article

References (58)

1. Hagerman, A. E. Tannin Handbook; Miami University: Oxford, OH, USA, 2002; available at http://www.users.muohio.edu/hagermae/.
2. Schofield, P.; Mbugua, D. M.; Pell, A. N. Analysis of condensed tannins: a review Anim. Feed Sci. Technol. 2001, 91, 21-40
3. Gea, A.; Stringano, E.; Brown, R. H.; Mueller-Harvey, I. In situ analysis and structural elucidation of sainfoin (Onobrychis viciifolia) tannins for high-throughput germplasm screening J. Agric. Food Chem. 2011, 59, 495-503
4. Le Bourvellec, C.; Renard, C. M. G. C. Interactions between polyphenols and macromolecules: quantification methods and mechanisms Crit. Rev. Food Sci. Nutr. 2012, 52, 213-248
5. Hagerman, A. E. Tannin-protein interactions. In Phenolic Compounds in Foods and Health; Ho, C. T., Ed.; American Chemical Society: Washington, DC, USA, 1992; pp 236-247.
6. Asquith, T. N.; Butler, L. G. Interactions of condensed tannins with selected proteins Phytochemistry 1986, 25, 1591-1593
7. Albrecht, K. A.; Muck, R. E. Proteolysis in ensiled forage legumes that vary in tannin concentration Crop Sci. 1991, 31, 464-469
8. Min, B. R.; Barry, T. N.; Attwood, G. T.; McNabb, W. C. The effect of condensed tannins on the nutrition and health of ruminants fed fresh temperate forages: a review Anim. Feed Sci. Technol. 2003, 106, 3-19
9. Waghorn, G. C.; Douglas, G. B.; Niezen, J. H.; McNabb, W. C.; Foote, A. G. Forages with condensed tannins-their management and nutritive value for ruminants Proc. N. Z. Grassl. Assoc. 1998, 60, 89-98
10. Barry, T. N.; McNabb, W. C. The implications of condensed tannins on the nutritive value of temperate forages fed to ruminants Br. J. Nutr. 1999, 81, 263-272
11. Patra, A. K.; Saxena, J. A new perspective on the use of plant secondary metabolites to inhibit methanogenesis in the rumen Phytochemistry 2010, 71, 1198-1222
12. 4 production using an automated pressure evaluation system (APES) Anim. Feed Sci. Technol. 2011, 166-167, 377-390
13. Aguerre, M. J.; Wattiaux, M. A.; Capozzolo, M. C.; Lencioni, P.; Cabral, C. Effect of quebracho-chestnut tannin extracts at two dietary crude protein levels on nitrogen partitioning in lactating dairy cows J. Dairy Sci. 2010, 93 (E-Suppl. 1) 446 (Abstr.)
14. McMahon, L. R.; McAllister, T. A.; Berg, B. P.; Majak, W.; Acharya, S. N.; Popp, J. D.; Coulman, B. E.; Wang, Y.; Cheng, K.-J. A review of the effects of forage condensed tannins on ruminal fermentation and bloat in grazing cattle Can. J. Plant. Sci. 2000, 80, 469-485
15. Hoste, H.; Jackson, F.; Athanasiadou, S.; Thamsborg, S. M.; Hoskin, S. O. The effects of tannin-rich plants on parasitic nematodes in ruminants Trends Parasitol. 2006, 22, 253-261
16. Hagerman, A. E. Fifty years of polyphenol-protein complexes. In Recent Advances in Polyphenol Research, 1st ed.; Cheynier, V.; Sarni-Manchado, P.; Quideau, S., Eds.; Wiley: Hoboken, NJ, USA, 2012; Vol. 3, pp 71-97.
17. Naumann, H. D.; Muir, J. P.; Lambert, B. D.; Tedeschi, L. O.; Kothmann, M. M. Condensed tannins in the ruminant environment: a perspective on biological activity J. Agric. Sci. 2013, 1, 8-20
18. Mueller-Harvey, I. Unravelling the conundrum of tannins in animal nutrition and health J. Sci. Food Agric. 2006, 86, 2010-2037
19. Barbehenn, R. V.; Constabel, C. P. Tannins in plant-herbivore interactions Phytochemistry 2011, 72, 1551-1565
20. Poncet-Legrand, C.; Edelmann, A.; Putaux, J.-L.; Cartalade, D.; Sarni-Manchado, P.; Vernhet, A. Poly(-proline) interactions with flavan-3-ols units: influence of the molecular structure and the polyphenol/protein ratio Food Hydrocolloids 2006, 20, 687-697
21. Lorenz, M. M.; Alkhafadji, L.; Stringano, E.; Nilsson, S.; Mueller-Harvey, I.; Udén, P. Relationship between condensed tannin structures and their ability to precipitate feed proteins in the rumen J. Sci. Food Agric. 2014, 94, 963-968
22. De Freitas, V.; Mateus, N. Nephelometric study of salivary protein-tannin aggregates J. Sci. Food Agric. 2002, 82, 113-119
23. Hagerman, A. E.; Robbins, C. T. Specificity of tannin-binding salivary proteins relative to diet selection by mammals Can. J. Zool. 1993, 71, 628-633
24. McNabb, W. C.; Peters, J. S.; Foo, L. Y.; Waghorn, G. C.; Jackson, F. S. Effect of condensed tannins prepared from several forages on the in vitro precipitation of ribulose-1,5- bis phosphate carboxylase (Rubisco) protein and its digestion by trypsin (EC 2.4.21.4) and chymotrypsin (EC 2.4.21.1) J. Sci. Food Agric. 1998, 77, 201-212
25. Hagerman, A. E.; Butler, L. G. The specificity of proanthocyanidin-protein interactions J. Biol. Chem. 1981, 256, 4494-4497
26. 16 (4-8) catechin (procyanidin) J. Agric. Food Chem. 1998, 46, 2590-2595
27. 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
28. Adamczyk, B.; Salminen, J.-P.; Smolander, A.; Kitunen, V. Precipitation of proteins by tannins: effects of concentration, protein/tannin ratio and pH Int. J. Food Sci. Technol. 2012, 47, 875-878
29. Bate-Smith, E. C. Haemanalysis of tannins: the concept of relative astringency Phytochemistry 1973, 12, 907-912
30. 4 production Anim. Feed Sci. Technol. 2011, 166-167, 373-376
31. Huang, X. D.; Liang, J. B.; Tan, H. Y.; Yahya, R.; Long, R.; Ho, Y. W. Protein-binding affinity of Leucaena condensed tannins of differing molecular weights J. Agric. Food Chem. 2011, 59, 10677-10682
32. Huang, X. D.; Liang, J. B.; Tan, H. Y.; Yahya, R.; Khamseekhiew, B.; Ho, Y. W. Molecular weight and protein binding affinity of Leucaena condensed tannins and their effects on in vitro fermentation parameters Anim. Feed Sci. Technol. 2010, 159, 81-87
33. Osborne, N. J. T.; McNeill, D. M. Characterisation of Leucaena condensed tannins by size and protein precipitation capacity J. Sci. Food Agric. 2001, 81, 1113-1119
34. Naumann, H. D.; Tedeschi, L. O.; Muir, J. P.; Lambert, B. D.; Kothmann, M. M. Effect of molecular weight of condensed tannins from warm-season perennial legumes on ruminal methane production in vitro Biochem. Syst. Ecol. 2013, 50, 154-162
35. Naumann, H. D.; Hagerman, A. E.; Lambert, B. D.; Muir, J. P.; Tedeschi, L. O.; Kothmann, M. M. Molecular weight and protein-precipitating ability of condensed tannins from warm-season perennial legumes J. Plant Interact. 2014, 9, 212-219
36. Harbertson, J. F.; Kilmister, R. L.; Kelm, M. A.; Downey, M. O. Impact of condensed tannin size as individual and mixed polymers on bovine serum albumin precipitation Food Chem. 2014, 160, 16-21
37. Gu, L.; Kelm, M.; Hammerstone, J. F.; Beecher, G.; Cunningham, D.; Vannozzi, S.; Prior, R. L. Fractionation of polymeric procyanidins from lowbush blueberry and quantification of procyanidins in selected foods with an optimized normal-phase HPLC-MS fluorescent detection method J. Agric. Food Chem. 2002, 50, 4852-4860
38. Kelm, M. A.; Johnson, J. C.; Robbins, R. J.; Hammerstone, J. F.; Schmitz, H. H. High-performance liquid chromatography separation and purification of cacao (Theobroma cacao L.) procyanidins according to degree of polymerization using a diol stationary phase J. Agric. Food Chem. 2006, 54, 1571-1576
39. Douillard, R.; de Mathan, O. Leaf proteins for food use: potential of RUBISCO. In New and Developing Sources of Food Proteins, 1st ed.; Hudson, B. J., Ed.; Chapman and Hall: Boca Raton, FL, USA, 1994; pp 307-342.
40. Grabber, J. H.; Zeller, W. E.; Mueller-Harvey, I. Acetone enhances the direct analysis of procyanidin- and prodelphinidin-based condensed tannins in Lotus species by the butanol-HCl-iron assay J. Agric. Food Chem. 2013, 61, 2669-2678
41. Engström, M. T.; Pälijärvi, M.; Fryganas, C.; Grabber, J. H.; Mueller-Harvey, I.; Salminen, J.-P. Rapid qualitative and quantitative analysis of proanthocyanidin oligomers and polymers by UPLC-MS/MS J. Agric. Food Chem. 2014, 62, 3390-3399
42. Sullivan, M. L.; Zeller, W. E. Efficacy of various naturally occurring caffeic acid derivatives in preventing post-harvest protein losses in forages J. Sci. Food Agric. 2012, 93, 219-226
43. Saxton, A. M. A macro for converting mean separation output to letter groupings in proc mixed. Proceedings, 23rd SAS Users Group International; SAS Institute: Cary, NC, USA, 1998; pp 1243-1246.
44. de Freitas, V.; Carvalho, E.; Mateus, N. Study of carbohydrate influence on protein-tannin aggregation by nephelometry Food Chem. 2003, 81, 503-509
45. Mateus, N.; Carvalho, E.; Luís, C.; de Freitas, V. Influence of the tannin structure on the disruption effect of carbohydrates on protein-tannin aggregates Anal. Chim. Acta 2004, 513, 135-140
46. Delehanty, J. B.; Johnson, B. J.; Hickey, T. E.; Pons, T.; Ligler, F. S. Binding and neutralization of lipopolysaccharides by plant proanthocyanidins J. Nat. Prod. 2007, 70, 1718-1724
47. Barbeau, W. E.; Kinsella, J. E. Ribulose bisphosphate carboxylase/oxygenase (rubisco) from green leaves-potentials as a food protein Food Rev. Int. 1988, 4, 93-127
48. Messman, M. A.; Weiss, W. P.; Albrecht, K. A. In situ disappearance of individual proteins and nitrogen from legume forages containing varying amounts of tannins J. Dairy Sci. 1996, 79, 1430-1436
49. Waghorn, G. C.; Ulyatt, M. J.; John, A.; Fisher, L. J. The effect of condensed tannins on the site of digestion of amino acids and other nutrients in sheep fed on Lotus corniculatus Br. J. Nutr. 1987, 57, 115-126
50. Ge, S.; Kojio, K.; Takahara, A.; Kajiyama, T. Bovine serum albumin adsorption onto immobilized organotrichlorosilane surface: influence of the phase separation on protein adsorption patterns J. Biomater. Sci. Polym. Ed. 1998, 9, 131-150
51. Wetter, L. R.; Deutsch, H. F. Immunological studies on egg white proteins IV. Immunochemical and physical studies of lysozyme J. Biol. Chem. 1951, 192, 237-242
52. Sullivan, M. L.; Hatfield, R. D. Polyphenol oxidase and o-diphenols inhibit postharvest proteolysis in red clover and alfalfa Crop Sci. 2006, 46, 663-670
53. Jöbstl, E.; O'Connell, J.; Fairclough, J. P. A.; Williamson, M. P. Molecular model for astringency produced by polyphenol/protein interactions Biomacromolecules 2004, 5, 942-949
54. Zanchi, D.; Narayanan, T.; Hagenmuller, D.; Baron, A.; Guyot, S.; Cabane, B.; Bouhallab, S. Tannin-assisted aggregation of natively unfolded proteins Europhys. Lett. 2008, 82 58001
55. Andrews, T. J.; Ballment, B. The function of the small subunits of ribulose bisphosphate carboxylase-oxygenase J. Biol. Chem. 1983, 258, 7514-7518
56. 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 Biomacromolecules 2011, 12, 710-715
57. RCSB Protein Data Bank Web site address: http://www.rcsb.org.
58. 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