Monomeric and oligomeric flavanols maintain the endogenous glucocorticoid response in human macrophages in pro-oxidant conditions in vitro

Chemico-Biological Interactions

Volumn 291, Issue , 2018, Pages 237-244

  Veríssimo, Gesiele ^a   Bast, Aalt ^a   Weseler, Antje R ^a  

^a MAASTRICHT UNIVERSITY   (Netherlands)

Author keywords

Antioxidants; Cortisol; Flavonoids; Glucocorticoids; Inflammation

Indexed keywords

11BETA HYDROXYSTEROID DEHYDROGENASE 1; CORTISONE; FLAVANOL DERIVATIVE; GLUCOCORTICOID; HISTONE DEACETYLASE; INTERLEUKIN 8; TERT BUTYL HYDROPEROXIDE; ANTIINFLAMMATORY AGENT; FLAVONOL DERIVATIVE; OXIDIZING AGENT; TUMOR NECROSIS FACTOR;

ARTICLE; CATALYSIS; CELL DIFFERENTIATION; CELL VIABILITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DOWN REGULATION; GENE EXPRESSION; GENETIC TRANSCRIPTION; HORMONE ACTION; HORMONE RESISTANCE; HORMONE RESPONSE; HUMAN; HUMAN CELL; IMMUNOCOMPETENT CELL; IN VITRO STUDY; MACROPHAGE; PHYTOCHEMISTRY; PROTEIN EXPRESSION; THP-1 CELL LINE; CELL LINE; CELL SURVIVAL; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; INFLAMMATION; METABOLISM; PATHOLOGY; TIME FACTOR;

11-BETA-HYDROXYSTEROID DEHYDROGENASE TYPE 1; ANTI-INFLAMMATORY AGENTS; CELL LINE; CELL SURVIVAL; FLAVONOLS; GENE EXPRESSION REGULATION; GLUCOCORTICOIDS; HISTONE DEACETYLASES; HUMANS; INFLAMMATION; INTERLEUKIN-8; MACROPHAGES; OXIDANTS; TERT-BUTYLHYDROPEROXIDE; TIME FACTORS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 85049317816     PISSN: 00092797     EISSN: 18727786     Source Type: Journal    
DOI: 10.1016/j.cbi.2018.06.024     Document Type: Article

References (58)

1. Medzhitov, R., Origin and physiological roles of inflammation. Nature 454:7203 (2008), 428–435.
2. Marshall, S.E., Immunological factors in disease. Walker BRC, N.R., Ralston, S.H., Penman, I.D., (eds.) Davidson's Principles and Practice of Medicine, twenty-second ed., 2014, Elsevier Limited, Amsterdam, 71–96.
3. Medzhitov, R., Inflammation 2010: new adventures of an old flame. Cell 140:6 (2010), 771–776.
4. Chrousos, G.P., Glucocorticoid action: physiology. Jameson JLDG, L.J., De Kretser, D.M., Giudice, L.C., Grossmann, A.B., Mehmed, S., Potts, J.T., Weir, G.C., (eds.) Endocrinology: Adult and Pediatric. 1, seventh ed., 2016, Elsevier Saunders, Philadelphia, USA, 1727–1740.
5. Zhang, G., Ghosh, S., Toll-like receptor-mediated NF-kappaB activation: a phylogenetically conserved paradigm in innate immunity. J. Clin. Invest. 107:1 (2001), 13–19.
6. Gloire, G., Legrand-Poels, S., Piette, J., NF-kappaB activation by reactive oxygen species: fifteen years later. Biochem. Pharmacol. 72:11 (2006), 1493–1505.
7. Flohe, L., Brigelius-Flohe, R., Saliou, C., Traber, M.G., Packer, L., Redox regulation of NF-kappa B activation. Free Radic. Biol. Med. 22:6 (1997), 1115–1126.
8. van den Berg, R., Haenen, G.R., van den Berg, H., Bast, A., Transcription factor NF-kappaB as a potential biomarker for oxidative stress. Br. J. Nutr. 86:Suppl 1 (2001), S121–S127.
9. Adcock, I.M., Barnes, P.J., Molecular mechanisms of corticosteroid resistance. Chest 134:2 (2008), 394–401.
10. Barnes, P.J., Corticosteroid resistance in patients with asthma and chronic obstructive pulmonary disease. J. Allergy Clin. Immunol. 131:3 (2013), 636–645.
11. Bast, A., Haenen, G.R., Ten misconceptions about antioxidants. Trends Pharmacol. Sci. 34:8 (2013), 430–436.
12. de Boer, A., Vos, E., Bast, A., Implementation of the nutrition and health claim regulation - the case of antioxidants. Regul. Toxicol. Pharmacol. 68:3 (2014), 475–487.
13. Milenkovic, D., Vanden Berghe, W., Boby, C., Leroux, C., Declerck, K., Szarc vel Szic, K., et al. Dietary flavanols modulate the transcription of genes associated with cardiovascular pathology without changes in their DNA methylation state. PLoS One, 9(4), 2014, e95527.
14. Ruijters, E.J., Weseler, A.R., Kicken, C., Haenen, G.R., Bast, A., The flavanol (-)-epicatechin and its metabolites protect against oxidative stress in primary endothelial cells via a direct antioxidant effect. Eur. J. Pharmacol. 715:1–3 (2013), 147–153.
15. Weseler, A.R., Ruijters, E.J., Drittij-Reijnders, M.J., Reesink, K.D., Haenen, G.R., Bast, A., Pleiotropic benefit of monomeric and oligomeric flavanols on vascular health–a randomized controlled clinical pilot study. PLoS One, 6(12), 2011, e28460.
16. Laparra, J.M.,J., Masquelier, J., Étude pharmacocinétique des oligomères flavanoliques. Plantes Med. Phytotherap. 9 (1977), 133–142.
17. Laparra, J.M.,J., Lesca, M.F., Blanquet, P., Masquelier, J., Étude pharmacocinetique des oligomeres procyanidoliques totaux du raisin. Acta Ther. 4 (1978), 233–246.
18. Benakis, A., Schopfer, C., Ritschard, J., Disposition of 14C-labelled ENDOTELON in humans. Eur. J. Drug Metab. Pharmacokinet. 33:1 (2008), 37–43.
19. Weseler, A.R., Bast, A., Masquelier's grape seed extract: from basic flavonoid research to a well-characterized food supplement with health benefits. Nutr. J., 16(1), 2017, 5.
20. What is health? The ability to adapt. Lancet, 373(9666), 2009, 781.
21. Rice-Evans, C., Baysal, E., Pashby, D.P., Hochstein, P., t-butyl hydroperoxide-induced perturbations of human erythrocytes as a model for oxidant stress. Biochim. Biophys. Acta 815:3 (1985), 426–432.
22. Altman, S.A., Zastawny, T.H., Randers, L., Lin, Z., Lumpkin, J.A., Remacle, J., et al. tert.-butyl hydroperoxide-mediated DNA base damage in cultured mammalian cells. Mutat. Res. 306:1 (1994), 35–44.
23. Kanupriya, Prasad D., Sai Ram, M., Sawhney, R.C., Ilavazhagan, G., Banerjee, P.K., Mechanism of tert-butylhydroperoxide induced cytotoxicity in U-937 macrophages by alteration of mitochondrial function and generation of ROS. Toxicol. Vitro 21:5 (2007), 846–854.
24. Alia, M., Ramos, S., Mateos, R., Bravo, L., Goya, L., Response of the antioxidant defense system to tert-butyl hydroperoxide and hydrogen peroxide in a human hepatoma cell line (HepG2). J. Biochem. Mol. Toxicol. 19:2 (2005), 119–128.
25. Tomlinson, J.W., Walker, E.A., Bujalska, I.J., Draper, N., Lavery, G.G., Cooper, M.S., et al. 11beta-hydroxysteroid dehydrogenase type 1: a tissue-specific regulator of glucocorticoid response. Endocr. Rev. 25:5 (2004), 831–866.
26. Weseler, A.R., Bast, A., Pleiotropic-acting nutrients require integrative investigational approaches: the example of flavonoids. J. Agric. Food Chem. 60:36 (2012), 8941–8946.
27. Ito, K., Barnes, P.J., Adcock, I.M., Glucocorticoid receptor recruitment of histone deacetylase 2 inhibits interleukin-1beta-induced histone H4 acetylation on lysines 8 and 12. Mol. Cell Biol. 20:18 (2000), 6891–6903.
28. Forman, H.J., Torres, M., Reactive oxygen species and cell signaling: respiratory burst in macrophage signaling. Am. J. Respir. Crit. Care Med. 166:12 Pt 2 (2002), S4–S8.
29. Mosmann, T., Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Meth. 65:1–2 (1983), 55–63.
30. Mizukami, Y., Jo, W.S., Duerr, E.M., Gala, M., Li, J., Zhang, X., et al. Induction of interleukin-8 preserves the angiogenic response in HIF-1alpha-deficient colon cancer cells. Nat. Med. 11:9 (2005), 992–997.
31. Kaur, P., Kaur, G., Bansal, M.P., Tertiary-butyl hydroperoxide induced oxidative stress and male reproductive activity in mice: role of transcription factor NF-kappaB and testicular antioxidant enzymes. Reprod. Toxicol. 22:3 (2006), 479–484.
32. Chung, J., Lee, H.S., Chung, H.Y., Yoon, T.R., Kim, H.K., Salicylideneamino-2-thiophenol inhibits inflammatory mediator genes (RANTES, MCP-1, IL-8 and HIF-1alpha) expression induced by tert-butyl hydroperoxide via MAPK pathways in rat peritoneal macrophages. Biotechnol. Lett. 30:9 (2008), 1553–1558.
33. Brown, D.M., Hutchison, L., Donaldson, K., Stone, V., The effects of PM10 particles and oxidative stress on macrophages and lung epithelial cells: modulating effects of calcium-signaling antagonists. Am. J. Physiol. Lung Cell Mol. Physiol. 292:6 (2007), L1444–L1451.
34. Brown, D.M., Hutchison, L., Donaldson, K., MacKenzie, S.J., Dick, C.A., Stone, V., The effect of oxidative stress on macrophages and lung epithelial cells: the role of phosphodiesterases 1 and 4. Toxicol. Lett. 168:1 (2007), 1–6.
35. Bos, M.A., Vennat, B., Meunier, M.T., Pouget, M.P., Pourrat, A., Fialip, J., Procyanidins from tormentil: antioxidant properties towards lipoperoxidation and anti-elastase activity. Biol. Pharm. Bull. 19:1 (1996), 146–148.
36. de Haan, B.B.S., Post, J.A., Oligomeric proanthocyanidins protect vascular endothelial cells from lipid oxidation. Inflamm. Res., 55, 2006 Supplement 2:S116.
37. Ruijters, E.J., Haenen, G.R., Weseler, A.R., Bast, A., The cocoa flavanol (-)-epicatechin protects the cortisol response. Pharmacol. Res. 79 (2014), 28–33.
38. Barnes, P.J., Adcock, I.M., Glucocorticoid resistance in inflammatory diseases. Lancet 373:9678 (2009), 1905–1917.
39. Farrell, R.J., Kelleher, D., Glucocorticoid resistance in inflammatory bowel disease. J. Endocrinol. 178:3 (2003), 339–346.
40. Adcock, I.M., Lane, S.J., Brown, C.R., Peters, M.J., Lee, T.H., Barnes, P.J., Differences in binding of glucocorticoid receptor to DNA in steroid-resistant asthma. J. Immunol. 154:7 (1995), 3500–3505.
41. Yang-Yen, H.F., Chambard, J.C., Sun, Y.L., Smeal, T., Schmidt, T.J., Drouin, J., et al. Transcriptional interference between c-Jun and the glucocorticoid receptor: mutual inhibition of DNA binding due to direct protein-protein interaction. Cell 62:6 (1990), 1205–1215.
42. Barnes, P.J., Ito, K., Adcock, I.M., Corticosteroid resistance in chronic obstructive pulmonary disease: inactivation of histone deacetylase. Lancet 363:9410 (2004), 731–733.
43. Randall, M.J., Haenen, G.R., Bouwman, F.G., van der Vliet, A., Bast, A., The tobacco smoke component acrolein induces glucocorticoid resistant gene expression via inhibition of histone deacetylase. Toxicol. Lett. 240:1 (2016), 43–49.
44. Ito, K., Hanazawa, T., Tomita, K., Barnes, P.J., Adcock, I.M., Oxidative stress reduces histone deacetylase 2 activity and enhances IL-8 gene expression: role of tyrosine nitration. Biochem. Biophys. Res. Commun. 315:1 (2004), 240–245.
45. Osoata, G.O., Yamamura, S., Ito, M., Vuppusetty, C., Adcock, I.M., Barnes, P.J., et al. Nitration of distinct tyrosine residues causes inactivation of histone deacetylase 2. Biochem. Biophys. Res. Commun. 384:3 (2009), 366–371.
46. To, Y., Ito, K., Kizawa, Y., Failla, M., Ito, M., Kusama, T., et al. Targeting phosphoinositide-3-kinase-delta with theophylline reverses corticosteroid insensitivity in chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med. 182:7 (2010), 897–904.
47. Chapman, K., Holmes, M., Seckl, J., 11beta-hydroxysteroid dehydrogenases: intracellular gate-keepers of tissue glucocorticoid action. Physiol. Rev. 93:3 (2013), 1139–1206.
48. Chapman, K.E., Coutinho, A., Gray, M., Gilmour, J.S., Savill, J.S., Seckl, J.R., Local amplification of glucocorticoids by 11beta-hydroxysteroid dehydrogenase type 1 and its role in the inflammatory response. Ann. N. Y. Acad. Sci. 1088 (2006), 265–273.
49. Gilmour, J.S., Coutinho, A.E., Cailhier, J.F., Man, T.Y., Clay, M., Thomas, G., et al. Local amplification of glucocorticoids by 11 beta-hydroxysteroid dehydrogenase type 1 promotes macrophage phagocytosis of apoptotic leukocytes. J. Immunol. 176:12 (2006), 7605–7611.
50. Zhang, T.Y., Daynes, R.A., Macrophages from 11beta-hydroxysteroid dehydrogenase type 1-deficient mice exhibit an increased sensitivity to lipopolysaccharide stimulation due to TGF-beta-mediated up-regulation of SHIP1 expression. J. Immunol. 179:9 (2007), 6325–6335.
51. Choy, Y.Y., Jaggers, G.K., Oteiza, P.I., Waterhouse, A.L., Bioavailability of intact proanthocyanidins in the rat colon after ingestion of grape seed extract. J. Agric. Food Chem. 61:1 (2013), 121–127.
52. Prasain, J.K., Peng, N., Dai, Y., Moore, R., Arabshahi, A., Wilson, L., et al. Liquid chromatography tandem mass spectrometry identification of proanthocyanidins in rat plasma after oral administration of grape seed extract. Phytomedicine 16:2–3 (2009), 233–243.
53. Serra, A., Macia, A., Romero, M.P., Salvado, M.J., Bustos, M., Fernandez-Larrea, J., et al. Determination of procyanidins and their metabolites in plasma samples by improved liquid chromatography-tandem mass spectrometry. J. Chromatogr. B Analyt. Technol. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 877:11–12 (2009), 1169–1176.
54. Tsang, C., Auger, C., Mullen, W., Bornet, A., Rouanet, J.M., Crozier, A., et al. The absorption, metabolism and excretion of flavan-3-ols and procyanidins following the ingestion of a grape seed extract by rats. Br. J. Nutr. 94:2 (2005), 170–181.
55. Sano, A., Yamakoshi, J., Tokutake, S., Tobe, K., Kubota, Y., Kikuchi, M., Procyanidin B1 is detected in human serum after intake of proanthocyanidin-rich grape seed extract. Biosci. Biotechnol. Biochem. 67:5 (2003), 1140–1143.
56. Actis-Goretta, L., Lévèques, A., Rein, M., Teml, A., Schäfer, C., Hofmann, U., et al. Intestinal absorption, metabolism, and excretion of (–)-epicatechin in healthy humans assessed by using an intestinal perfusion technique. Am. J. Clin. Nutr. 98:4 (2013), 924–933.
57. Shimoi, K., Saka, N., Nozawa, R., Sato, M., Amano, I., Nakayama, T., et al. Deglucuronidation of a flavonoid, luteolin monoglucuronide, during inflammation. Drug Metab. Dispos. 29:12 (2001), 1521–1524.
58. Bartholome, R., Haenen, G., Hollman, C.H., Bast, A., Dagnelie, P.C., Roos, D., et al. Deconjugation kinetics of glucuronidated phase II flavonoid metabolites by beta-glucuronidase from neutrophils. Drug Metabol. Pharmacokinet. 25:4 (2010), 379–387.