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Tea catechins' affinity for human cannabinoid receptors.



Camellia sinensis



Cannabinoid receptor



Among the many known health benefits of tea catechins count anti-inflammatory and neuroprotective activities, as well as effects on the regulation of food intake. Here we address cannabimimetic bioactivity of catechin derivatives occurring in tea leaves as a possible cellular effector of these functionalities. Competitive radioligand binding assays using recombinant human cannabinoid receptors expressed in Chem-1 and CHO cells identified (-)-epigallocatechin-3-O-gallate, EGCG ([K.sup.i]=33.6[micro]M). (-)-epigallocatechin, EGC ([K.sup.i]=35.7[micro]M), and (-)-epicatechin-3-O-gallate, ECG ([K.sup.i]=47.3[micro]M) as ligands with moderate affinity for type 1 cannabinoid receptors, CB1. Binding to CB2 was weaker with inhibition constants exceeding 50[micro]M for EGC and ECG. The epimers (+)-catechin and (-)-epicatechin exhibited negligible affinities for both CB1 and CB2. It can be concluded that central nervous cannabinoid receptors may be targeted by selected tea catechins but signaling via peripheral type receptors is less likely to play a major role in vivo.

[C] 2009 Elsevier GmbH. All rights reserved.


Catechins are the most abundant polyphenols in the leaves of tea (Camellia sinensis (L.) O. KUNZE) but are also found in many fruits and in some legumes, e.g. in cocoa beans (Arts et al. 2000). While the average daily catechin intake in Western diets has been estimated at 50 mg (Arts et al. 2001), "Mediterranean" type diets contain twice as much catechins (Auger et al. 2004) and have become known for their health-promoting effects (Ruidavets et al. 2000). These include a reduced incidence of stroke (Keli et al. 1996; Tanabe et al. 2008), the slowing of age-related cognitive decline (Kuriyama et al. 2006), and protection against obesity (Kao et al. 2000; Murase et al. 2006). Animal studies suggest an additional role of catechins or catechin oligomers in nociception (Rylski et al. 1979; DalBo et al. 2005; Dias et al. 2007; Tang et al. 2007) and in imparting resistance to stress (Abbas and Wink 2009). At the cellular level, catechins induce anti-inflammatory (Tedeschi et al. 2002) and antioxidant activities (Higdon and Frei 2003) but there is some disagreement regarding the signaling pathways that mediate the above functionalities (Cooper et al. 2005). Thus GABAergic, glutamatergic, monoamine and NO systems (Adachi et al. 2006; Chou et al. 2007; Rocha et al. 2007; Kim et al. 2007) have previously been proposed as catechin effectors, among others. Only recently, lipid rafts (Patra et al. 2008) and plasma membrane binding sites (Bastianetto et al. 2009) have been implicated as molecular targets. We therefore hypothesized that catechin pharmacology could involve further sites of action and tested cannabimimetic activities.

Two human cannabinoid receptors (CB) have so far been identified. Of these, CB1 is expressed primarily in the central nervous system (CNS) (Matsuda et al. 1990) where it acts through lipid rafts (Bari et al. 2005). CB1 plays a pivotal role in neuroprotection (Galve-Roperh et al. 2008) and food intake (Richard et al. 2009). CB2, in contrast, is expressed predominantly outside the CNS (Munro et al. 1993) and is most prevalent in cells of the immune system (Lynn and Herkenham 1994). CB ligands comprise natural analgesics (Walker and Hohmann 2005) of which cannabinoids have been extensively investigated (Woelkart et al. 2008). The present study examines in vitro affinities of (-)-epigallocatechin-3-O-gallate (EGCG), (-)-epicatechin-3-O-gallate (ECG), (-)-epigallocatechin EGC, (-)-epicatechin, and (+)-catechin (Fig. 1) for human CB1 and CB2.


Materials and methods

Membrane preparations of recombinant human cannabinoid receptors 1 (Chem-1 cells) and 2 (CHO cells) were purchased from Millipore (Schwalbach, Germany), catechin derivatives were obtained from Extrasynthese (Genay, France), [[.sup.3]]H-CP55940 was purchased from PerkinElmer (Boston, MA, USA) and unlabeled CP55940 was purchased from Sigma-Aldrich (Schnelldorf, Germany). CB1 ([K.sub.d]=29.4nM) and CB2 ([K.sub.d]=12.0nM) saturation characteristics were determined with CP55940 concentrations of 1-12.5nM (six concentration steps), and 1-20nM (five concentration steps), respectively, using 10[micro]g (CB1) or 2.5[micro]g (CB2) of synaptosomes. For radioligand receptor assays, 100[micro]1 of membrane preparations were added to 80[micro]1 of assay buffer (50mM Hepes, 0.5% BSA, pH 7.4), 10[micro]1 of test compounds dissolved in DMSO and l0[micro]1 of [[.sup.3]]H-CP55940, followed by an incubation of 90 min at room temperature in microtiter plates (final concentrations per well: DMSO 5% (v/v), ethanol 0.28% (v/v), radioligand 12.5nM or 15nM, CB1/2 synaptosomes 10[micro]g). Specific binding for each compound at each concentration was defined as total binding minus binding in the presence of unlabeled CP55940 (10[micro]M), and was determined for each concentration of [[.sup.3]]H-CP55940. Reactions were terminated by filtration through a GF/C Filtermat A (PerkinElmer, Boston, MA, USA) using a 96-well Inotech cell harvester (Dietikon, Switzerland) and by subsequent washing of filters with distilled water. Prior to filtration, filter mats were first soaked in buffer containing 0.33% polyethyleneimine for 1 h, and were washed with 50mM Hepes (0.5% BSA, pH 7.4). After filtration, filters were dried at 60 [degrees]C for 60 min and were then transferred to scintillation vials. 4 ml of Rotiszint eco plus scintillation cocktail (Roth, Karlsruhe, Germany) were added to each vial and radioactivity was determined in a WinSpectral 1414 liquid scintillation counter (PerkinElmer Wallac GmbH, Freiburg, Germany). All experiments were performed in triplicate using seven concentration steps per compound investigated. Mean values [+ or -] SD were obtained for each step and served for normalization and curve-fitting. Competitive radioligand displacement was evaluated by nonlinear regression analysis (GraphPad Prism V2.01, GraphPad Software, LaJolla, CA, USA). [K.sub.i] values were derived from the equation by Cheng and Prusoff (1973):

[K.sub.i] = [[E[C.sub.50]]/[1 + [[ligand]/[K.sub.d]]]]

Results and discussion

Dose-dependent binding to CB1 and CB2 was noted for all compounds under study. Overall, [K.sub.i] values differed by several orders of magnitude ranging from 33.6[micro]M for EGCG to over 2.5mM for (+)-catechin and (-)-epicatechin with regard to CB1. Receptor affinities for CB1 were generally stronger than the respective affinities for CB2 (Table 1). While CB1 inhibition constants below 50[micro]M were achieved by EGCG, EGC and ECG, only EGCG exhibited a similar [K.sub.i] for CB2. CB2 half-maximal inhibition could not be determined for (+)-catechin and (-)-epicatechin as values of these flavonoids fell outside the upper detection limit of the displacement assay. The present data suggest that selected tea catechins feature moderate affinity for central type CB whereas binding to peripheral type CB is less prominent (Fig. 2). Thus cannabimimetic activities may contribute to CNS effects of green tea extracts including the mitigation of pain (Singal et al. 2005; Sattayasai et al. 2008), complementing a COX-2 inhibitory role (Kaur et al. 2005) and known opioid receptor functionalities of catechins (Capasso et al. 1998; Katavic et al. 2007). In addition, CB1 ligands EGCG, EGC and ECG in green tea may modulate food intake (Auvichayapat et al 2008; Bose et al. 2008). However, a cautionary note is warranted in that the magnitude of anti-obesity effects is not undisputed (Diepvens et al. 2005) and both anti-nociceptive and anti-obesity activities imply agonistic modulation of CB1 which is unproven by our experiments. Observational studies on neuroprotection by green tea polyphenols (Kakuda 2002; Pan et al. 2003) lend some support to putative CB1 agonistic effects but will require further confirmation, e.g. by monitoring intracellular [Ca.sup.2+] levels or steady state [[.sup.32]]P-GTPase activity. As for anti-allergic properties of catechin-enriched preparations (Maeda-Yamamoto et al. 2007), these are less likely to result from binding to CB in view of mostly poor CB2 [K.sub.i] values.

With respect to both CB1 and CB2, negligible bioactivities were noted for ungallated catechins. In previous reports, the galloyl moiety has been associated with catechins' radical scavenging qualities (Nanjo et al. 1996; Kinjo et al. 2002; Wolfe and Liu 2008), with inhibition of COX-2 (Hou et al. 2007), protein tyrosine phosphatase (Okamoto et al. 2003), pancreatic lipase (Ikeda et al. 2005) and fatty acid synthase (Wang et al. 2003), but not with enhanced GABAergic neurotransmission (Adachi et al. 2007). The 3', 4', 5'-trihydroxyl substitution in the catechin B-ring, in turn, which has been implicated in antioxidant, apoptosis-inducing and beta secretase-inhibiting activity of catechins (Furuno et al. 2002; Saeki et al. 2000; Jeon et al. 2003) did not appear to contribute to CB binding. More detailed structure-activity investigations are invited to address the interplay of galloyl and pyrogallol moieties, as well as further studies on structural and stereochemical prerequisites for cannabinoid signaling.
Table 1

Affinities of catechin derivatives and CP55940 for human
cannabinoid receptors 1 and 2 as determined in competition binding
assays on membrane preparations of recombinant receptors
[[.sup.3]]H-CP55940 was used as radiolabeled ligand. All experiments
were performed in triplicate

Compound                          [K.sub.i](CB1)          95% CI
                                  in [mu]M

(EGCG)                            33.6                    17.2-65.7

(-)-epicatechin-3-O-gallate(ECG)  47.3                    16.7-133.8

(-)-epigallocatechin (EGC)        35.7                    3.5-368.2

(+)-catechin                      [greater than] 2,500.0  n.d.

(-)-epicatechin                   [greater than] 2,500.0  n.d.

CP55940                           0.028                   0.008-.095

Compound                          [K.sub.i] (CB2)  95% CI
                                  in [mu]M
(EGCG)                            42.8             17.9-101.0

(-)-epicatechin-3-O-gallate(ECG)  95.6             23.0-397.4

(-)-epigallocatechin (EGC)        361.3            0.5-24,000

(+)-catechin                      n.d.             n.d.

(-)-epicatechin                   n.d.             n.d.

CP55940                           0.025            0.015-.039

n.d.=not determined.

Recent pharmacokinetic data suggest that green tea polyphenols are readily absorbed in the small intestine and reach peak plasma concentrations at 1.6 to 2.3 hours post ingestion (Stalmach et al. 2009). Apart from indirect evidence using catechin-enriched diets (e.g. Nagao et al. 2009), unfortunately, limited proof is currently available from placebo-controlled trials of catechins to put their putative bioactivities into perspective. Some have concluded to poor effects of catechins on sustained weight loss (Hursel and Westerterp-Plantenga 2009) while others have reported a favourable outcome with regard to plasma glucose, and compliance with diet in overweight subjects (Hill et al. 2007; Rondanelli et al. 2009). None of these early trials have monitored plasma concentrations of ECG and EGCG to assess the uptake of green tea polyphenols (Wang et al. 2008) and results of investigations that have taken such measures into account are still pending (Shen et al. 2009).


In summary, the in vitro targeting of central, and to a lesser degree, of peripheral CB by EGCG, EGC and ECG adds to the complexity of tea catechins' known multilevel functionalities. While bioavailability of gallated forms is generally lower than that of ungallated flavan-3-ols (Warden et al. 2001; Henning et al. 2008), signal strength may be amplified in vivo by non-receptor related mechanisms, e.g. by inhibition of fatty acid amide hydrolase or COX-2 (Jhaveri et al. 2008). Future studies will need to address the impact of these confounders to allow for a balanced view of putative health benefits that may be mediated by CB.


This work was supported by grant #0313848C from the German Federal Ministry of Education, Science, Research and Technology.


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G. Korte, (a), *, A. Dreiseitel (a), P. Schreier (b), A. Oehme (b), S. Locher (b), S. Geiger (c), J. Heilmann (c), P.G. Sand (a)

(a) Department of Psychiatry, University of Regensburg, Franz-Josef-Strauss-Allee 11, H4 R97 93053 Regensburg, Germany

(b) Chair of Food Chemistry, University of Wuerzburg, Am Hubland, 97074 Wuerzburg, Germany

(c) Chair of Pharmaceutical Biology, institute of Pharmacy, University of Regensburg, Universitaetsstrasse 31, 93053 Regensburg, Germany

* Corresponding author. Tel.: +49 941 944 8955; fax: +49 941 944 8956. E-mail address: (G. Korte).

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Author:Korte, G.; Dreiseitel, A.; Schreier, P.; Oehme, A.; Locher, S.; Geiger, S.; Heilmann, J.; Sand, P.G.
Publication:Phytomedicine: International Journal of Phytotherapy & Phytopharmacology
Article Type:Report
Geographic Code:4EUGE
Date:Jan 1, 2010
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