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Articles

Butyrate Impairs Energy Metabolism in Isolated Perfused Liver of Fed Rats¹

Marie-Christine Beauvieux^*,2, Pierre Tissier, Henri Gin^*,, Paul Canioni and Jean-Louis Gallis

^* Service de Nutrition et Diabétologie, Hôpital Haut-Lévêque, F-33600 Pessac France and Centre de Résonance Magnétique des Systèmes Biologiques, UMR 5536 CNRS-UB2, F-33076 Bordeaux Cedex France

²To whom correspondence and reprint requests should be addressed. E-mail: mcdb{at}rmsb.u-bordeaux2.fr.

This study was designed to test the effects of short-chain fatty acids (SCFA) with an even number of carbon atoms on hepatic energy metabolism. The effect of the SCFA was evaluated by measuring liver ATP content and oxygen consumption. The ATP content was evaluated using ³¹P nuclear magnetic resonance in isolated liver from fed rats. In addition, respiratory activity (VO₂) was assessed using Clark electrodes. The livers were perfused with acetate, butyrate or a medium chain length fatty acid, octanoate, at a concentration of 0.05–5.0 mmol/L. The addition of each substrate enhanced the rate of the net ATP consumption (V_i), establishing a new ATP steady state that required a perfusion time of 20 min, dependent on the chain length and concentration of the fatty acid (FA). The initial V_i was unchanged for acetate and the ATP level stabilized at 58% of the initial level. Both butyrate and octanoate induced a dose-dependent increase in V_i. This may reflect an ATP-consuming process for the intracellular pH regulation observed during the acidosis associated with the ß-oxidation pathway. At the new steady state, the ATP concentration was 45% of the initial level for both FA. VO₂ was both rapidly and reversibly increased, and the change was a function of butyrate or octanoate concentration and of the chain length. K_m values were similar for butyrate and octanoate. Because all of the effects were similar for butyrate and octanoate, in contrast to acetate, we suggest that the impairment of the energy metabolism by butyrate resulted from an increase in the FADH₂/NADH ratio due to ß-oxidation. In conclusion, the difference in the hepatic oxidation pathways of two products of intestinal fermentation (acetate and butyrate) explains their different actions on energy metabolism.

KEY WORDS: • short-chain fatty acids • butyrate • nuclear magnetic resonance • respiration • rats

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