Procyanidins and inflammation: Molecular targets and health implications

BioFactors

Volumn 38, Issue 4, 2012, Pages 257-265

  Martinez Micaelo, Neus ^a   González Abuín, Noemi ^a   Ardèvol, Anna ^a   Pinent, Montserrat ^a   Blay, Maria Teresa ^a  

^a UNIVERSITAT ROVIRA I VIRGILI   (Spain)

Author keywords

Cyclooxygenase; NF kB; Procyanidin; Prostaglandin

Indexed keywords

ARACHIDONIC ACID; CCAAT ENHANCER BINDING PROTEIN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; CYCLOOXYGENASE 1; CYCLOOXYGENASE 2; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GAMMA INTERFERON; I KAPPA B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 6; INTERLEUKIN 8; LIPOXYGENASE; NEURONAL NITRIC OXIDE SYNTHASE; PHOSPHOLIPASE A2; PROCYANIDIN; PROTEIN P100; PROTEIN P105; PROTEIN P50; PROTEIN P52; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR REL; TRANSCRIPTION FACTOR RELA; TRANSCRIPTION FACTOR RELB; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA;

ADAPTIVE IMMUNITY; BIOAVAILABILITY; CYTOKINE PRODUCTION; DNA SEQUENCE; ENZYME ACTIVATION; ENZYME ACTIVITY; GENE TARGETING; GENETIC TRANSCRIPTION; HEALTH PROMOTION; HUMAN; HYDROGEN BOND; IMMUNOMODULATION; INFLAMMATION; INNATE IMMUNITY; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REVIEW;

ANIMALS; ANTI-INFLAMMATORY AGENTS; BIOLOGICAL AVAILABILITY; HUMANS; INFLAMMATION; INFLAMMATION MEDIATORS; METABOLIC NETWORKS AND PATHWAYS; PROANTHOCYANIDINS; SIGNAL TRANSDUCTION;

EID: 84865121434     PISSN: 09516433     EISSN: 18728081     Source Type: Journal    
DOI: 10.1002/biof.1019     Document Type: Review

References (67)

1. Erdman, J. W., Balentine, D., Arab, L., Beecher, G., Dwyer, J. T., Folts, J., Harnly, J., Hollman, P., Keen, C. L., Mazza, G., Messina, M., Scalbert, A., Vita, J., Williamson, G., and Burrowes, J. ( 2007) Flavonoids and heart health: Proceedings of the ILSI North America Flavonoids Workshop, May 31-June 1, 2005, Washington, DC. J. Nutr. 137, 718S-737S.
2. Landberg, R., Sun, Q., Rimm, E. B., Cassidy, A., Scalbert, A., Mantzoros, C. S., Hu, F. B., and Van Dam, R. M. ( 2011) Selected dietary flavonoids are associated with markers off inflammation and endothelial dysfunction in U.S. Women. J. Nutr. 141, 618-625.
3. Perez-Jimenez, J., Fezeu, L., Touvier, M., Arnault, N., Manach, C., Hercberg, S., Galan, P., and Scalbert, A. ( 2011) Dietary intake of 337 polyphenols in French adults. Am. J. Clin. Nutr. 93, 1220-1228.
4. Scalbert, A., Manach, C., Morand, C., Remesy, C., and Jimenez, L. ( 2005) Dietary polyphenols and the prevention of diseases. Crit. Rev. Food Sci. Nutr. 45, 287-306.
5. De La Iglesia, R., Milagro, F. I., Campion, J., Boque, N., and Martinez, J. A. ( 2010) Healthy properties of proanthocyanidins. Biofactors 36, 159-168.
6. Williamson, G. and Manach, C. ( 2005) Bioavailability and bioefficacy of polyphenols in humans. II. Review of 93 intervention studies. Am. J. Clin. Nutr. 81, 243S-255S.
7. Auger, C., Al-Awwadi, N., Bornet, A., Rouanet, J. M., Gasc, F., Cros, G., and Teissedre, P. L. ( 2004) Catechins and procyanidins in Mediterranean diets. Food Res. Int. 37, 233-245.
8. Yilmaz, Y. and Toledo, R. T. ( 2004) Health aspects of functional grape seed constituents. Trends Food Sci. Technol. 15, 422-433.
9. Kenny, T. P., Keen, C. L., Schmitz, H. H., and Gershwin, M. E. ( 2007) Immune effects of cocoa procyanidin oligomers on peripheral blood mononuclear cells. Exp. Biol. Med. 232, 293-300.
10. Martinez-Micaelo, N., Gonzalez-Abuin, N., Pinent, M., Ardevol, A., Blay, M. ( 2011) Anti-inflammatory effects of procyanidins and docosahexanoic acid in human macrophages THP-1. Inflamm. Res. 60, 258-259.
11. Engler, M. B. and Engler, M. M. ( 2006) The emerging role of flavonoid-rich cocoa and chocolate in cardiovascular health and disease. Nutr. Rev. 64, 109-118.
12. Khan, N., Monagas, M., Llorach, R., Urpi-Sarda, M., Rabassa, M., Estruch, R., and Andres-Lacueva, C. ( 2010) Targeted and metabolomic study of biomarkers of cocoa powder consumption effects on inflammatory biomarkers in patients at high risk of cardiovascular disease. Agro Food Industry Hi-Tech 21, 51-54.
13. Libby, P. ( 2007) Inflammatory mechanisms: the molecular basis of inflammation and disease. Nutr. Rev. 65, S140-S146.
14. Olefsky, J. M. and Glass, C. K. ( 2010) Macrophages, inflammation, and insulin resistance. Annu. Rev. Physiol. 72, 219-246.
15. Selmi, C., Mao, T. K., Keen, C. L., Schmitz, H. H., and Gershwin, M. E. ( 2006) The anti-inflammatory properties of cocoa flavanols. J. Cardiovasc. Pharmacol. 47, S163-S171.
16. Gonzalez, R., Ballester, I., Lopez-Posadas, R., Suarez, M. D., Zarzuelo, A., Martinez-Augustin, O., and Sanchez De Medina, F. ( 2011) Effects of flavonoids and other polyphenols on inflammation. Crit. Rev. Food Sci. Nutr. 51, 331-362.
17. Martinez-Micaelo, N., Gonzalez-Abuin, N., Terra, X., Richart, C., Ardevol, A., Pinent, M., and Blay, M. ( 2012) Omega-3 docosahexaenoic acid and procyanidins inhibit cyclo-oxygenase activity and attenuate NF-kappaB activation through a p105/p50 regulatory mechanism in macrophage inflammation. Biochem. J. 441, 653-663.
18. Scalbert, A. and Williamson, G. ( 2000) Dietary intake and bioavailability of polyphenols. J. Nutr. 130, 2073S-2085S.
19. Baba, S., Osakabe, N., Natsume, M., and Terao, J. ( 2002) Absorption and urinary excretion of procyanidin B2 epicatechin-(4 beta-8)-epicatechin in rats. Free Radic. Biol. Med. 33, 142-148.
20. Holt, R. R., Lazarus, S. A., Sullards, M. C., Zhu, Q. Y., Schramm, D. D., Hammerstone, J. F., Fraga, C. G., Schmitz, H. H., and Keen, C. L. ( 2002) Procyanidin dimer B2 epicatechin-(4 beta-8)-epicatechin in human plasma after the consumption of a flavanol-rich cocoa. Am. J. Clin. Nutr. 76, 798-804.
21. Gonthier, M. P., Donovan, J. L., Texier, O., Felgines, C., Remesy, C., and Scalbert, A. ( 2003) Metabolism of dietary procyanidins in rats. Free Radic. Biol. Med. 35, 837-844.
22. Stoupi, S., Williamson, G., Viton, F., Barron, D., King, L. J., Brown, J. E., and Clifford, M. N. ( 2010) In vivo bioavailability, absorption, excretion, and pharmacokinetics of (14)C procyanidin B2 in male rats. Drug Metab. Dispos. 38, 287-291.
23. Fraga, C. G. and Oteiza, P. I. ( 2011) Dietary flavonoids: role of (-)-epicatechin and related procyanidins in cell signaling. Free Radic. Biol. Med. 51, 813-823.
24. Spencer, J. P., Chaudry, F., Pannala, A. S., Srai, S. K., Debnam, E., and Rice-Evans, C. ( 2000) Decomposition of cocoa procyanidins in the gastric milieu. Biochem. Biophys. Res. Commun. 272, 236-241.
25. Rios, L. Y., Bennett, R. N., Lazarus, S. A., Remesy, C., Scalbert, A., and Williamson, G. ( 2002) Cocoa procyanidins are stable during gastric transit in humans. Am. J. Clin. Nutr. 76, 1106-1110.
26. Tsang, C., Auger, C., Mullen, W., Bornet, A., Rouanet, J. M., Crozier, A., and Teissedre, P. L. ( 2005) The absorption, metabolism and excretion of flavan-3-ols and procyanidins following the ingestion of a grape seed extract by rats. Br. J. Nutr. 94, 170-181.
27. Deprez, S., Mila, I., Huneau, J. F., Tome, D., and Scalbert, A. ( 2001) Transport of proanthocyanidin dimer, trimer, and polymer across monolayers of human intestinal epithelial Caco-2 cells. Antioxid. Redox. Signal. 3, 957-967.
28. Han, X. Z., Shen, T., and Lou, H. X. ( 2007) Dietary polyphenols and their biological significance. Int. J. Mol. Sci. 8, 950-988.
29. Flower, R. J. and Vane, J. R. ( 1972) Inhibition of prostaglandin synthetase in brain explains the anti-pyretic activity of paracetamol (4-acetamidophenol). Nature 240, 410-411.
30. Baumann, J., Von Bruchhausen, F., and Wurm, G. ( 1980) Flavonoids and related compounds as inhibition of arachidonic acid peroxidation. Prostaglandins 20, 627-639.
31. Welton, A. F., Tobias, L. D., Fiedler-Nagy, C., Anderson, W., Hope, W., Meyers, K., and Coffey, J. W. ( 1986) Effect of flavonoids on arachidonic acid metabolism. Prog. Clin. Biol. Res. 213, 231-242.
32. Hong, J., Bose, M., Ju, J., Ryu, J. H., Chen, X., Sang, S., Lee, M. J., and Yang, C. S. ( 2004) Modulation of arachidonic acid metabolism by curcumin and related beta-diketone derivatives: effects on cytosolic phospholipase A(2), cyclooxygenases and 5-lipoxygenase. Carcinogenesis 25, 1671-1679.
33. Kim, H. P., Son, K. H., Chang, H. W., and Kang, S. S. ( 2004) Anti-inflammatory plant flavonoids and cellular action mechanisms. J. Pharmacol. Sci. 96, 229-245.
34. Hamalainen, M., Nieminen, R., Asmawi, M. Z., Vuorela, P., Vapaatalo, H., and Moilanen, E. ( 2011) Effects of flavonoids on prostaglandin E(2) production and on COX-2 and mPGES-1 expressions in activated macrophages. Planta Med. 77, 1504-1511.
35. Kang, Y. J., Wingerd, B. A., Arakawa, T., and Smith, W. L. ( 2006) Cyclooxygenase-2 gene transcription in a macrophage model of inflammation. J. Immunol. 177, 8111-8122.
36. Hou, D. X., Masuzaki, S., Hashimoto, F., Uto, T., Tanigawa, S., Fujii, M., and Sakata, Y. ( 2007) Green tea proanthocyanidins inhibit cyclooxygenase-2 expression in LPS-activated mouse macrophages: molecular mechanisms and structure-activity relationship. Arch. Biochem. Biophys. 460, 67-74.
37. Zhang, W. Y., Liu, H. Q., Xie, K. Q., Yin, L. L., Li, Y., Kwik- Uribe, C. L., and Zhu, X. Z. ( 2006) Procyanidin dimer B2 epicatechin-(4 beta-8)-epicatechin suppresses the expression of cyclooxygenase-2 in endotoxin-treated monocytic cells. Biochem. Biophys. Res. Commun. 345, 508-515.
38. Kundu, J. K., Na, H. K., Chun, K. S., Kim, Y. K., Lee, S. J., Lee, S. S., Lee, O. S., Sim, Y. C., and Surh, Y. J. ( 2003) Inhibition of phorbol ester-induced COX-2 expression by epigallocatechin gallate in mouse skin and cultured human mammary epithelial cells. J. Nutr. 133, 3805S-3810S.
39. Kang, N. J., Lee, K. W., Lee, D. E., Rogozin, E. A., Bode, A. M., Lee, H. J., and Dong, Z. ( 2008) Cocoa procyanidins suppress transformation by inhibiting mitogen-activated protein kinase kinase. J. Biol. Chem. 283, 20664-20673.
40. Meeran, S. M., Vaid, M., Punathil, T., and Katiyar, S. K. ( 2009) Dietary grape seed proanthocyanidins inhibit 12-O-tetradecanoyl phorbol-13-acetate-caused skin tumor promotion in 7, 12-dimethylbenz[a]anthracene-initiated mouse skin, which is associated with the inhibition of inflammatory responses. Carcinogenesis 30, 520-528.
41. Terra, X., Valls, J., Vitrac, X., Merrillon, J. M., Arola, L., Ardevol, A., Blade, C., Fernandez-Larrea, J., Pujadas, G., Salvado, J., and Blay, M. ( 2007) Grape-seed procyanidins act as antiinflammatory agents in endotoxin-stimulated RAW 264.7 macrophages by inhibiting NFkB signaling pathway. J. Agric. Food Chem. 55, 4357-4365.
42. Samuelsson, B., Rouzer, C. A., and Matsumoto, T. ( 1987) Human leukocyte 5-lipoxygenase: an enzyme possessing dual enzymatic activities and a multicomponent regulatory system. Adv. Prostaglandin Thromboxane Leukot. Res. 17A, 1-11.
43. Schramm, D. D., Wang, J. F., Holt, R. R., Ensunsa, J. L., Gonsalves, J. L., Lazarus, S. A., Schmitz, H. H., German, J. B., and Keen, C. L. ( 2001) Chocolate procyanidins decrease the leukotriene-prostacyclin ratio in humans and human aortic endothelial cells. Am. J. Clin. Nutr. 73, 36-40.
44. Sies, H., Schewe, T., Heiss, C., and Kelm, M. ( 2005) Cocoa polyphenols and inflammatory mediators. Am. J. Clin. Nutr. 81, 304S-312S.
45. Seeram, N. P., Zhang, Y., and Nair, M. G. ( 2003) Inhibition of proliferation of human cancer cells and cyclooxygenase enzymes by anthocyanidins and catechins. Nutr. Cancer 46, 101-106.
46. Santangelo, C., Vari, R., Scazzocchio, B., Di Benedetto, R., Filesi, C., and Masella, R. ( 2007) Polyphenols, intracellular signalling and inflammation. Ann. Ist. Super. Sanita 43, 394-405.
47. Mack, C. L. ( 2007) Serum cytokines as biomarkers of disease and clues to pathogenesis. Hepatology 46, 6-8.
48. Mao, T. K., Powell, J., Van De Water, J., Keen, C. L., Schmitz, H. H., Hammerstone, J. F., and Gershwin, M. E. ( 2000) The effect of cocoa procyanidins on the transcription and secretion of interleukin 1 beta in peripheral blood mononuclear cells. Life Sci. 66, 1377-1386.
49. Mao, T. K., Van De Water, J., Keen, C. L., Schmitz, H. H., and Gershwin, M. E. ( 2002) Effect of cocoa flavanols and their related oligomers on the secretion of interleukin-5 in peripheral blood mononuclear cells. J. Med. Food 5, 17-22.
50. Al-Hanbali, M., Ali, D., Bustami, M., Abdel-Malek, S., Al-Hanbali, R., Alhussainy, T., Qadan, F., and Matalka, K. Z. ( 2009) Epicatechin suppresses IL-6, IL-8 and enhances IL-10 production with NF-kappaB nuclear translocation in whole blood stimulated system. Neuroendocrinol. Lett. 30, 131-138.
51. Terra, X., Montagut, G., Bustos, M., Llopiz, N., Ardevol, A., Blade, C., Fernandez-Larrea, J., Pujadas, G., Salvado, J., Arola, L., and Blay, M. ( 2009) Grape-seed procyanidins prevent low-grade inflammation by modulating cytokine expression in rats fed a high-fat diet. J. Nutr. Biochem. 20, 210-218.
52. Terra, X., Palozza, P., Fernandez-Larrea, J., Ardevol, A., Blade, C., Pujadas, G., Salvado, J., Arola, L., and Blay, M. T. ( 2011) Procyanidin dimer B1 and trimer C1 impair inflammatory response signalling in human monocytes. Free Radic. Res. 45, 611-619.
53. Miyake, M., Ide, K., Sasaki, K., Matsukura, Y., Shijima, K., and Fujiwara, D. ( 2008) Oral administration of highly oligomeric procyanidins of Jatoba reduces the severity of collagen-induced arthritis. Biosci. Biotechnol. Biochem. 72, 1781-1788.
54. Yoon, J. H. and Baek, S. J. ( 2005) Molecular targets of dietary polyphenols with anti-inflammatory properties. Yonsei Med. J. 46, 585-596.
55. Ghosh, S., May, M. J., and Kopp, E. B. ( 1998) NF-kappa B and rel proteins: evolutionarily conserved mediators of immune responses. Annu. Rev. Immunol. 16, 225-260.
56. Hayden, M. S., West, A. P., and Ghosh, S. ( 2006) NF-kappa B and the immune response. Oncogene 25, 6758-6780.
57. Li, Q. T. and Verma, I. M. ( 2002) NF-kappa B regulation in the immune system. Nat. Rev. Immunol. 2, 725-734.
58. Hayden, M. S. and Ghosh, S. ( 2004) Signaling to NF-kappa B. Genes Dev. 18, 2195-2224.
59. Oeckinghaus, A. and Ghosh, S. ( 2009) The NF-kappa B family of transcription factors and its regulation. Cold Spring Harb. Perspect. Biol. 1: a000034.
60. Gilmore, T. D. ( 1999) The Rel/NF-kappa B signal transduction pathway: introduction. Oncogene 18, 6842-6844.
61. Pahl, H. L. ( 1999) Activators and target genes of Rel/NF-kappa B transcription factors. Oncogene 18, 6853-6866.
62. Mackenzie, G. G., Carrasquedo, F., Delfino, J. M., Keen, C. L., Fraga, C. G., and Oteiza, P. I. ( 2004) Epicatechin, catechin, and dimeric procyanidins inhibit PMA-induced NF-kappaB activation at multiple steps in Jurkat T cells. FASEB J. 18, 167-169.
63. Chacon, M. R., Ceperuelo-Mallafre, V., Maymo-Masip, E., Mateo-Sanz, J. M., Arola, L., Guitierrez, C., Fernandez-Real, J. M., Ardevol, A., Simon, I., and Vendrell, J. ( 2009) Grape-seed procyanidins modulate inflammation on human differentiated adipocytes in vitro. Cytokine 47, 137-142.
64. Mackenzie, G. G., Delfino, J. M., Keen, C. L., Fraga, C. G., and Oteiza, P. I. ( 2009) Dimeric procyanidins are inhibitors of NF-kappaB-DNA binding. Biochem. Pharmacol. 78, 1252-1262.
65. Terra, X., Pallares, V., Ardevol, A., Blade, C., Fernandez-Larrea, J., Pujadas, G., Salvado, J., Arola, L., and Blay, M. ( 2011) Modulatory effect of grape-seed procyanidins on local and systemic inflammation in diet-induced obesity rats. J. Nutr. Biochem. 22, 380-387.
66. Pallares, V., Calay, D., Cedo, L., Castell-Auvi, A., Raes, M., Pinent, M., Ardevol, A., Arola, L., and Blay, M. ( 2012) Additive, antagonistic, and synergistic effects of procyanidins and polyunsaturated fatty acids over inflammation in RAW 264.7 macrophages activated by lipopolysaccharide. Nutrition 28, 447-457.
67. Pallares, V., Calay, D., Cedo, L., Castell-Auvi, A., Raes, M., Pinent, M., Ardevol, A., Arola, L., and Blay, M. ( 2012) Enhanced anti-inflammatory effect of resveratrol and EPA in treated endotoxin-activated RAW 264.7 macrophages. Br. J. Nutr. 1-12. Available on CJO 2012 doi:10.1017/S0007114511007057.