Critique 023: Evidence that PPAR-gamma is a mechanism for the effects of wine polyphenolics on cardiovascular risk. – 27 November 2010

Zoechling A, Liebner F, Jungbauer A.  Red wine: A source of potent ligands for peroxisome proliferator-activated receptor γ.  Food & Function, Journal of the Royal Society of Chemistry, in press.  DOI: 10.1039/c0fo00086h.

Authors’ Abstract

Moderate red wine consumption has been correlated with lower incidences of cardiovascular diseases, inflammation, and metabolic diseases such as type 2 diabetes, obesity, and high blood pressure.  We studied binding of ligands from different wines to the peroxisome proliferator-activated receptor γ (PPARγ), a key factor in glucose and lipid metabolism.  Ellagic acid and epicatechin gallate (ECG) were identified by gas chromatography and mass spectroscopy in the most active wine fractions.  They had an affinity to PPARγ similar to that of the standard pharmaceutical agent rosiglitazone, which is used for the treatment of type 2 diabetes.  The IC50 values of ellagic acid and ECG were 5.7 x 10-7 M and 5.9 x 10-7 M, respectively.  All of the red wines had affinities for PPARγ equivalent to concentrations of rosiglitazone ranging from 52–521 μM.  One hundred milliliters of the tested red wines was equivalent to approximately 1.8–18 mg of rosiglitazone.  This volume contained an activity equivalent of at least a quarter of (and up to four times) the daily dose of this potent anti-diabetes drug.  The ameliorating effects of red wine on metabolic diseases may be partially explained by the presence of PPARγ ligands.

Forum Comments

It is important that biological mechanisms are identified for the observed inverse relation between the moderate consumption of wine and cardiovascular disease shown in most epidemiologic studies.  Experimental studies have shown that alcohol, resveratrol, procyanidins, anthocyanins, quercetin, catechins, isoflavones, myricetin, ellagic acid, and many other of the constituents of wine may play a role, and limited intervention trials in humans have supported such mechanisms by demonstrating biologic changes from the administration of wine.1-3.

The presents study provides a very good description of the multiple polyphenolic substances in red wine that favorably affect the peroxisome proliferator-activated receptor γ (PPARγ), a key factor in glucose and lipid metabolism.  It demonstrates that polyphenols from the skin and seeds of the grape, from the wine, as well as from the oak in barrel fermentation are important. 

Specific comments on analyses:  The paper by Zoechling et al is an elegant example of the needed effort to provide a biochemical mechanism for the biological effects of foods, including wine.  Data on binding of different wine component are carefully produced and this result is interpreted on the light of epidemiological evidence. On the other hand it would have been appropriate providing evidence also for the actual shift of gene expression primed by the same wine component in a cell or animal model.  In this respect, results must be rated appropriate but still as preliminary.  A ligand could have different effects.

Another Forum member stated: This study has investigated binding of wine polyphenols to the binding domain of the human PPAR-gamma receptor.  This does not indicate whether these polyphenols act as PPAR-gamma agonists or antagonists.  There is no biological evidence in this study to support the contention that these polyphenols act through the PPAR-gamma receptor.  The sort of evidence that should have been provided is a comparison with rosiglitazone in a cell population known to respond to PPAR-gamma agonists (e.g. adipocytes).  

Responses that should have been measured to reach the conclusion that wine polyphenols act as PPAR-gamma agonists include the following: (1) comparative changes in PPAR-gamma responsive genes; (2) regulation of PPAR-gamma reporter gene constructs; (3) adipocyte differentiation.  Such responses should all be blocked by a PPAR-gamma antagonist if their mechanism of action is via the PPAR-gamma receptor.  Since PPAR-gamma is an intracellular/nuclear receptor, using a cell system would have given a better indication of the circulating levels of these polyphenols required to produce a PPAR-gamma mediated response, and whether such concentrations could be realistically achieved through wine drinking.

Other Forum members commented:  Bioavailability depends on the physicochemical and biopharmaceutical characteristics of the selected compound and more importantly the route of administration.  Indeed, it is important to stress that upon consumption, bioactive compounds will undergo metabolism by phase 1 and 2 enzymes.  Moreover, binding of the compounds to PPAR gamma needs polyphenols to be present at the site of interaction.  In this study, ellagic acid and epicactechin gallate were found to be the most active wine components with an affinity to PPAR gamma of 570 nM and 590 nM respectively. 

Previous human investigations have demonstrated that upon consumption levels of such compounds in the systemic circulation hardly reach 200 nM.4,5  Moreover, previous studies have also shown that flavanols are metabolized to ring-fission products (valerolactones) and methylated catechins.  These ring-fission products can also be further metabolized in the colon to simple phenolic acids such as 4-hydroxybenzoic acid, 3,4-dihydroxybenzoic acid, 3-methoxy-4-hydroxyhippuric acid, and vanillic acid, which have been detected in human urine after tea consumption.6  However none of the smallest molecules in the wines tested, which for some of them are structurally closely related to the metabolites, were effective in binding PPAR gamma with high affinity.

Using the assay described, the investigators did find that certain substances were particularly active, and those included the gallated catechins as well as ellagic acid.  They then described a number of wines and their “equivalent concentration” by comparison with their standard drug, rosiglitazone.  They also describe the composition of the wines, but the analytical data does not describe the amounts of any of the “active” substances.  So while there is a lot of discussion of the active components, it is not possible to compare any wine’s “activity” with the amount of the key substances.  Lacking such a comparison, it is very hard to conclude that these substances are in fact the responsible factors in the observed activity.

Finally, considering the generally small amounts of these particular substances in wine, their poor absorption, and the liver’s tendency to rapidly conjugate gallate functionality, it would be surprising if this receptor would be exposed to adequate levels of the free substances in vivo.

Forum References

1.  Van Velden DP, Mansvelt EP, Fourie E, Rossouw M, Marais AD.  The Cardioprotective effect of wine on human blood chemistry.  Ann NY Acad Sci 2002;957:337-340.

2.  Leighton F, Urquiaga I.  Changes in cardiovascular risk factors associated with wine consumption in intervention studies in humans.  Ann Epidemiol 2007;17:S32-S36.

3.  Shai I, Wainstein J, Harman-Boehm I, Raz I, Fraser D, Rudich A, Stampfer MJ.  Glycemic effects of moderate alcohol intake among patients with type 2 diabetes: A mulit-center, randomized clinical intervention trial.  Diabetes Care 2007;30:3011-3016.

4.  Henning, S.M., et al.  Bioavailability and antioxidant activity of tea flavanols after consumption of green tea, black tea, or a green tea extract supplement.  The American Journal of Clinical Nutrition 2004;80:1558-1564.

5.  Seeram, N.P., R. Lee, and D. Heber.  Bioavailability of ellagic acid in human plasma after consumption of ellagitannins from pomegranate (Punica granatum L.) juice.  Clinica Chimica Acta 2004;348:63-68.

6.  Pietta PG, et al.  Catechin metabolites after intake of green tea infusions.  BioFactors 1998;8;111-118.

Forum Summary:  It is important that biological mechanisms are identified for the observed inverse relation between the moderate consumption of wine and cardiovascular disease shown in most epidemiologic studies.  This paper is an elegant example of the needed effort to provide a biochemical mechanism for the biological effects of wine.  Data on binding of different wine component are carefully produced and this result is interpreted in light of epidemiological evidence.  On the other hand it would have been appropriate providing evidence also for the actual shift of gene expression primed by the same wine component in a cell or animal model.  In this respect, results must be rated appropriate but still as preliminary.  A ligand could have different effects.  Further, biological evidence is not provided to support the contention that these polyphenols act through the PPAR-gamma receptor.  The sort of evidence that should have been provided is a comparison with rosiglitazone in a cell population known to respond to PPAR-gamma agonists (e.g. adipocytes).

Unfortunately, the analytical data does not describe the amounts of any of the “active” substances.  So while there is a lot of discussion of the active components, it is not possible to compare any wine’s “activity” with the amount of the key substances.  Lacking such a comparison, it is very hard to conclude that these substances are in fact the responsible factors in the observed activity.

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Contributions to this critique by the International Scientific Forum on Alcohol Research were provided by the following members:

Roger Corder, PhD, MRPharmS, William Harvey Research Institute, Queen Mary University of London, UK

R. Curtis Ellison, MD, Section of Preventive Medicine & Epidemiology, Boston University School of Medicine, Boston, MA

Jeremy P. E. Spencer, Reader in Biochemistry, The University of Reading, UK

Creina Stockley, clinical pharmacology, Health and Regulatory Information Manager, Australian Wine Research Institute, Glen Osmond, South Australia, Australia. 

Pierre-Louis Teissedre, PhD, Faculty of Oenology – ISVV, University Victor Segalen Bordeaux 2, Bordeaux, France

Fulvio Ursini, MD, Dept. of Biological Chemistry, University of Padova, Padova, Italy

David Vauzour, PhD, Dept. of Food and Nutritional Sciences, The University of Reading, UK

Andrew L. Waterhouse, PhD, Marvin Sands Professor, Department of Viticulture and Enology, University of California, Davis, USA