Hostname: page-component-cd9895bd7-gxg78 Total loading time: 0 Render date: 2024-12-23T04:54:01.609Z Has data issue: false hasContentIssue false

Green tea catechins suppress NF-κB-mediated inflammatory responses: relevance to nutritional management of inflammation

Published online by Cambridge University Press:  27 January 2011

Naren H. Ravindranath
Affiliation:
Department of Biomedical Sciences, Norris Dental Science Center, Herman Ostrow School of Dentistry, University of Southern California, 925 W 34th Street, Den 4110B, Los Angeles, CA90089, USA email [email protected]
Mepur H. Ravindranath
Affiliation:
Terasaki Foundation Laboratory, 11570 West Olympic Boulevard, Los Angeles, CA90064, USA emails [email protected]; [email protected]
Rights & Permissions [Opens in a new window]

Abstract

Type
Invited Commentary
Copyright
Copyright © The Authors 2011

Blood loss after trauma induces several systemic inflammatory responses culminating in the dysfunction and failure of organs. In this issue of the British Journal of Nutrition, Relja et al. (Reference Relja, Töttel and Breig1) have examined the inflammatory signals at the subcellular, cellular and tissue levels after haemorrhage-induced hepatic injury and resuscitation in rats. Hepatic injury and resuscitation induced the expression of intercellular adhesion molecule-1, neutrophil infiltration and necrosis in the liver, and augmented serum alanine transaminase and IL-6 levels. It also induced IκBα phosphorylation and the activation of NF-κB. Pre-treatment with green tea extract (GTE: catechins >80 %, with >40 % of epigallocatechin gallate (EGCG)) suppressed the inflammatory responses at all levels, including neutrophil infiltration, intercellular adhesion molecule-1 expression and the release of IL-6, and, importantly, suppressed the activation of NF-κB.

The inflammatory responses occurring in the liver after haemorrhage are parallel to the inflammatory events occurring after inducing ischaemia, and EGCG is also active in the latter setting(Reference Giakoustidis, Giakoustidis and Iliadis2Reference Ichikawa, Matsui and Imai5). The anti-inflammatory efficacy of EGCG demonstrated in all these studies generates a unifying hypothesis. Hepatic injury induced by ischaemia(Reference Giakoustidis, Giakoustidis and Iliadis2) caused oxidative stress with enhanced production of reactive oxygen species and TNF-α; both mediated the expression of nuclear factors and kinases, activating the signal transduction pathways to trigger cell death. The liver that stained positive for NF-κB in the ischaemia group remained negative in the EGCG-pre-treated group. Neutrophil infiltration that was enhanced in the ischaemia group was significantly reduced after EGCG. Ischaemia-induced myocardial injury(Reference Aneja, Hake and Burroughs3) also caused significant neutrophil infiltration, an increase in plasma IL-6, and activation of IκB kinase and NF-κB in the tissues. EGCG pre-treatment significantly reduced myocardial damage, neutrophil infiltration and plasma IL-6, and also suppressed the NF-κB pathway. Intestinal injury induced by ischaemia(Reference Giakoustidis, Giakoustidis and Koliakou4) also resulted in an enhanced production of reactive oxygen species, neutrophil infiltration and activation of NF-κB. EGCG pre-treatment significantly deactivated NF-κB, decreased neutrophil infiltration and lowered reactive oxygen species production. All these studies support the conclusion derived by Relja et al. and collectively point out that induced inflammatory responses are mediated through NF-κB-dependent mechanisms, and EGCG per se or in combination with other catechins suppresses NF-κB activation and alleviates inflammation.

There are enumerable reports on the efficacy of EGCG per se or EGCG in combination with other catechins (epigallocatechin or epicatechin gallate or gallocatechin gallate)(Reference Ichikawa, Matsui and Imai5Reference Ludwig, Lorenz and Grimbo9) on inflammatory responses induced by different exogenous and endogenous factors. The inflammatory inducers include polymicrobial sepsis(Reference Wheeler, Lahni and Hake10), lipopolysaccharide(Reference Ichikawa, Matsui and Imai5Reference Yang, Oz and Barve7, Reference Yang, de Villiers and McClain11), Staphylococcus aureus enterotoxin B(Reference Watson, Vicario and Wang12), Helicobacter pylori infection(Reference Lee, Yeo and Choue13), IL-1β alone(Reference Corps, Curry and Buttle8, Reference Singh, Ahmed and Islam14Reference Wheeler, Catravas and Odoms16) or in combination with β-amyloid(Reference Kim, Jeong and Lee17) or oxygen tension(Reference Andriamanalijaona, Kypriotou and Baugé18) or TNF-α(Reference Ludwig, Lorenz and Grimbo9, Reference Heinecke, Grzanna and Au19) or TNF-α alone(Reference Chen, Wheeler and Malhotra20Reference Lee, Jung and Kim22), UV-B(Reference Afaq, Adhami and Ahmad23Reference Song, Bi and Xu25), repetitive oxidative stress(Reference Sen, Chakraborty and Raha26), cigarette smoke condensate(Reference Syed, Afaq and Kweon27), phorbol 12-myristate 13-acetate(Reference Shin, Kim and Jeong28Reference Kundu and Surh30), trinitrobenenesulphonic acid(Reference Abboud, Hake and Burroughs31)- or acetic acid(Reference Ran, Chen and Xiao32)-induced colitis, receptor activator for the NF-κB ligand(Reference Lin, Chen and Wang33, Reference Lee, Jin and Shim34) or high glucose(Reference Wu, Wu and Huang35). Most importantly, all these studies document that consequent to the down-regulation of NF-κB pathways, EGCG or catechin combination suppressed the levels of several pro-inflammatory cytokines (TNF-α(Reference Yang, de Villiers and McClain11, Reference Watson, Vicario and Wang12, Reference Shin, Kim and Jeong28, Reference Ran, Chen and Xiao32, Reference Wu, Wu and Huang35) IL-6(Reference Kim, Jeong and Lee17, Reference Xia, Song and Bi24, Reference Shin, Kim and Jeong28), IL-8(Reference Wheeler, Catravas and Odoms16, Reference Kim, Jeong and Lee17, Reference Chen, Wheeler and Malhotra20, Reference Syed, Afaq and Kweon27, Reference Shin, Kim and Jeong28), interferon-γ(Reference Watson, Vicario and Wang12, Reference Ran, Chen and Xiao32)), chemokine (Fractalkine(Reference Lee, Jung and Kim22)) and enzymes (matrix metaloproteinases-1, -3, -9(Reference Syed, Afaq and Kweon27), -13(Reference Corps, Curry and Buttle8, Reference Ahmed, Wang and Lalonde15, Reference Andriamanalijaona, Kypriotou and Baugé18), NO synthase(Reference Lin and Lin6, Reference Wheeler, Lahni and Hake10, Reference Singh, Ahmed and Islam14, Reference Song, Bi and Xu25, Reference Syed, Afaq and Kweon27, Reference Ran, Chen and Xiao32); cyclo-oxygenase-2(Reference Kim, Jeong and Lee17, Reference Heinecke, Grzanna and Au19, Reference Kundu and Surh30), glucosyl/lactosyl and Gb3 transferases(Reference Moon, Choi and Lee21)), growth factors (vascular endothelial growth factor(Reference Kim, Jeong and Lee17)), cell adhesion molecules (intercellular adhesion molecule-1, vascular cell adhesion molecule-1 and E-selectin(Reference Ludwig, Lorenz and Grimbo9)) and monocyte chemotactic protein-1(Reference Hong, Kim and Chang29). In this regard, the study of Relja et al. is well justified in the use of GTE, since other tea catechins act synergistically with EGCG. It is important to use GTE with a greater percentage of EGCG to counteract inflammation. These preclinical studies on the induced inflammatory responses promote the hypothesis that green tea catechins have the potential to suppress the NF-κB-mediated inflammatory pathway into a salient concept relevant to nutritional management of inflammation. The emerging concept is that EGCG or GTE has the potential to block the NF-κB pathway, which plays a critical role in inflammation induced by various factors and also in malignancy. These aforementioned studies pave the way for phase I and II clinical trials using GTE or EGCG to control trauma, haemorrhage or ischaemia-induced inflammation.

There is no conflict of interest.

References

1Relja, B, Töttel, E, Breig, L, et al. (2011) Effects of green tea catechins on the pro-inflammatory response after haemorrhage/resuscitation in rats. Br J Nutr 105, 17911797.CrossRefGoogle ScholarPubMed
2Giakoustidis, DE, Giakoustidis, AE, Iliadis, S, et al. (2010) Attenuation of liver ischemia/reperfusion induced apoptosis by epigallocatechin-3-gallate via down-regulation of NF-kappaB and c-Jun expression. J Surg Res 159, 720728.CrossRefGoogle ScholarPubMed
3Aneja, R, Hake, PW, Burroughs, TJ, et al. (2004) Epigallocatechin, a green tea polyphenol, attenuates myocardial ischemia reperfusion injury in rats. Mol Med 10, 5562.CrossRefGoogle Scholar
4Giakoustidis, AE, Giakoustidis, DE, Koliakou, K, et al. (2008) Inhibition of intestinal ischemia/reperfusion induced apoptosis and necrosis via down-regulation of the NF-kB, c-Jun and caspace-3 expression by epigallocatechin-3-gallate administration. Free Radic Res 42, 180–148.CrossRefGoogle ScholarPubMed
5Ichikawa, D, Matsui, A, Imai, M, et al. (2004) Effect of various catechins on the IL-12p40 production by murine peritoneal macrophages and a macrophage cell line, J774.1. Biol Pharm Bull 27, 13531358.CrossRefGoogle Scholar
6Lin, YL & Lin, JK (1997) Epigallocatechin-3-gallate blocks the induction of nitric oxide synthase by down-regulating lipopolysaccharide-induced activity of transcription factor nuclear factor-kappaB. Mol Pharmacol 52, 465472.CrossRefGoogle ScholarPubMed
7Yang, F, Oz, HS, Barve, S, et al. (2001) The green tea polyphenol ( − )-epigallocatechin-3-gallate blocks nuclear factor-kappa B activation by inhibiting I kappa B kinase activity in the intestinal epithelial cell line IEC-6. Mol Pharmacol 60, 528533.Google ScholarPubMed
8Corps, AN, Curry, VA, Buttle, DJ, et al. (2004) Inhibition of interleukin-1beta-stimulated collagenase and stromelysin expression in human tendon fibroblasts by epigallocatechin gallate ester. Matrix Biol 23, 163169.CrossRefGoogle ScholarPubMed
9Ludwig, A, Lorenz, M, Grimbo, N, et al. (2004) The tea flavonoid epigallocatechin-3-gallate reduces cytokine-induced VCAM-1 expression and monocyte adhesion to endothelial cells. Biochem Biophys Res Commun 316, 659665.CrossRefGoogle ScholarPubMed
10Wheeler, DS, Lahni, PM, Hake, PW, et al. (2007) The green tea polyphenol epigallocatechin-3-gallate improves systemic hemodynamics and survival in rodent models of polymicrobial sepsis. Shock 28, 353359.CrossRefGoogle ScholarPubMed
11Yang, F, de Villiers, WJ, McClain, CJ, et al. (1998) Green tea polyphenols block endotoxin-induced tumor necrosis factor-production and lethality in a murine model. J Nutr 128, 23342340.CrossRefGoogle ScholarPubMed
12Watson, JL, Vicario, M, Wang, A, et al. (2005) Immune cell activation and subsequent epithelial dysfunction by Staphylococcus enterotoxin B is attenuated by the green tea polyphenol ( − )-epigallocatechin gallate. Cell Immunol 237, 716.CrossRefGoogle ScholarPubMed
13Lee, KM, Yeo, M, Choue, JS, et al. (2004) Protective mechanism of epigallocatechin-3-gallate against Helicobacter pylori-induced gastric epithelial cytotoxicity via the blockage of TLR-4 signaling. Helicobacter 9, 632642.CrossRefGoogle ScholarPubMed
14Singh, R, Ahmed, S, Islam, N, et al. (2002) Epigallocatechin-3-gallate inhibits interleukin-1beta-induced expression of nitric oxide synthase and production of nitric oxide in human chondrocytes: suppression of nuclear factor kappaB activation by degradation of the inhibitor of nuclear factor kappaB. Arthritis Rheum 46, 20792086.CrossRefGoogle ScholarPubMed
15Ahmed, S, Wang, N, Lalonde, M, et al. (2004) Green tea polyphenol epigallocatechin-3-gallate (EGCG) differentially inhibits interleukin-1 beta-induced expression of matrix metalloproteinase-1 and -13 in human chondrocytes. J Pharmacol Exp Ther 308, 767773.CrossRefGoogle ScholarPubMed
16Wheeler, DS, Catravas, JD, Odoms, K, et al. (2004) Epigallocatechin-3-gallate, a green tea-derived polyphenol, inhibits IL-1 beta-dependent proinflammatory signal transduction in cultured respiratory epithelial cells. J Nutr 134, 10391044.CrossRefGoogle Scholar
17Kim, SJ, Jeong, HJ, Lee, KM, et al. (2007) Epigallocatechin-3-gallate suppresses NF-kappaB activation and phosphorylation of p38 MAPK and JNK in human astrocytoma U373MG cells. J Nutr Biochem 18, 587596.CrossRefGoogle ScholarPubMed
18Andriamanalijaona, R, Kypriotou, M, Baugé, C, et al. (2005) Comparative effects of 2 antioxidants, selenomethionine and epigallocatechin-gallate, on catabolic and anabolic gene expression of articular chondrocytes. J Rheumatol 32, 19581967.Google ScholarPubMed
19Heinecke, LF, Grzanna, MW, Au, AY, et al. (2010) Inhibition of cyclooxygenase-2 expression and prostaglandin E2 production in chondrocytes by avocado soybean unsaponifiables and epigallocatechin gallate. Osteoarthr Cartil 18, 220227.CrossRefGoogle ScholarPubMed
20Chen, PC, Wheeler, DS, Malhotra, V, et al. (2002) A green tea-derived polyphenol, epigallocatechin-3-gallate, inhibits IkappaB kinase activation and IL-8 gene expression in respiratory epithelium. Inflammation 26, 233241.CrossRefGoogle Scholar
21Moon, DO, Choi, SR, Lee, CM, et al. (2005) Epigallocatechin-3-gallate suppresses galactose-alpha1,4-galactose-1beta,4-glucose ceramide expression in TNF-alpha stimulated human intestinal epithelial cells through inhibition of MAPKs and NF-kappaB. J Korean Med Sci 20, 548554.CrossRefGoogle ScholarPubMed
22Lee, AS, Jung, YJ, Kim, DH, et al. (2009) Epigallocatechin-3-O-gallate decreases tumor necrosis factor-alpha-induced fractalkine expression in endothelial cells by suppressing NF-kappaB. Cell Physiol Biochem 24, 503510.CrossRefGoogle ScholarPubMed
23Afaq, F, Adhami, VM, Ahmad, N, et al. (2003) Inhibition of ultraviolet B-mediated activation of nuclear factor kappaB in normal human epidermal keratinocytes by green tea constituent ( − )-epigallocatechin-3-gallate. Oncogene 22, 10351044.CrossRefGoogle ScholarPubMed
24Xia, J, Song, X, Bi, Z, et al. (2005) UV-induced NF-kappaB activation and expression of IL-6 is attenuated by ( − )-epigallocatechin-3-gallate in cultured human keratinocytes in vitro. Int J Mol Med 16, 943950.Google ScholarPubMed
25Song, XZ, Bi, ZG & Xu, AE (2006) Green tea polyphenol epigallocatechin-3-gallate inhibits the expression of nitric oxide synthase and generation of nitric oxide induced by ultraviolet B in HaCaT cells. Chin Med J (Engl) 119, 282287.CrossRefGoogle ScholarPubMed
26Sen, P, Chakraborty, PK & Raha, S (2006) Tea polyphenol epigallocatechin 3-gallate impedes the anti-apoptotic effects of low-grade repetitive stress through inhibition of Akt and NFkappaB survival pathways. FEBS Lett 580, 278284.CrossRefGoogle ScholarPubMed
27Syed, DN, Afaq, F, Kweon, MH, et al. (2007) Green tea polyphenol EGCG suppresses cigarette smoke condensate-induced NF-kappaB activation in normal human bronchial epithelial cells. Oncogene 26, 673682.CrossRefGoogle ScholarPubMed
28Shin, HY, Kim, SH, Jeong, HJ, et al. (2007) Epigallocatechin-3-gallate inhibits secretion of TNF-alpha, IL-6 and IL-8 through the attenuation of ERK and NF-kappaB in HMC-1 cells. Int Arch Allergy Immunol 142, 335344.CrossRefGoogle ScholarPubMed
29Hong, MH, Kim, MH, Chang, HJ, et al. (2007) Epigallocatechin-3-gallate inhibits monocyte chemotactic protein-1 expression in endothelial cells via blocking NF-kappaB signaling. Life Sci 80, 19571965.CrossRefGoogle ScholarPubMed
30Kundu, JK & Surh, YJ (2007) Epigallocatechin gallate inhibits phorbol ester-induced activation of NF-kappa B and CREB in mouse skin: role of p38 MAPK. Ann N Y Acad Sci 1095, 504512.CrossRefGoogle ScholarPubMed
31Abboud, PA, Hake, PW, Burroughs, TJ, et al. (2008) Therapeutic effect of epigallocatechin-3-gallate in a mouse model of colitis. Eur J Pharmacol 579, 411417.CrossRefGoogle Scholar
32Ran, ZH, Chen, C & Xiao, SD (2008) Epigallocatechin-3-gallate ameliorates rats colitis induced by acetic acid. Biomed Pharmacother 62, 189196.CrossRefGoogle ScholarPubMed
33Lin, RW, Chen, CH, Wang, YH, et al. (2009) Epigallocatechin gallate inhibition of osteoclastic differentiation via NF-kappaB. Biochem Biophys Res Commun 379, 10331037.CrossRefGoogle ScholarPubMed
34Lee, JH, Jin, H, Shim, HE, et al. (2010) Epigallocatechin-3-gallate inhibits osteoclastogenesis by down-regulating c-Fos expression and suppressing the nuclear factor-kappaB signal. Mol Pharmacol 77, 1725.CrossRefGoogle ScholarPubMed
35Wu, CH, Wu, CF, Huang, HW, et al. (2009) Naturally occurring flavonoids attenuate high glucose-induced expression of proinflammatory cytokines in human monocytic THP-1 cells. Mol Nutr Food Res 53, 984995.CrossRefGoogle ScholarPubMed