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Intermittent fasting results in tissue-specific changes in bioenergetics and redox state.

Chausse B, Vieira-Lara MA, Sanchez AB, Medeiros MH, Kowaltowski AJ - PLoS ONE (2015)

Bottom Line: Although the consequences of CR are well studied, the effects of IF on redox status are not.No difference in mitochondrial bioenergetics or redox homeostasis was observed in skeletal muscles of IF animals.Overall, IF affects redox balance in a tissue-specific manner, leading to redox imbalance in the liver and brain and protection against oxidative damage in the heart.

View Article: PubMed Central - PubMed

Affiliation: Departamento de Bioquímica, Instituto de Química, Universidade de São Paulo, São Paulo, Brazil.

ABSTRACT
Intermittent fasting (IF) is a dietary intervention often used as an alternative to caloric restriction (CR) and characterized by 24 hour cycles alternating ad libitum feeding and fasting. Although the consequences of CR are well studied, the effects of IF on redox status are not. Here, we address the effects of IF on redox state markers in different tissues in order to uncover how changes in feeding frequency alter redox balance in rats. IF rats displayed lower body mass due to decreased energy conversion efficiency. Livers in IF rats presented increased mitochondrial respiratory capacity and enhanced levels of protein carbonyls. Surprisingly, IF animals also presented an increase in oxidative damage in the brain that was not related to changes in mitochondrial bioenergetics. Conversely, IF promoted a substantial protection against oxidative damage in the heart. No difference in mitochondrial bioenergetics or redox homeostasis was observed in skeletal muscles of IF animals. Overall, IF affects redox balance in a tissue-specific manner, leading to redox imbalance in the liver and brain and protection against oxidative damage in the heart.

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Reactive oxygen species production is not significantly altered by IF.(A) H2O2 release by isolated mitochondria in the presence of 1 mM ADP (state 3) and 5 mM pyruvate plus 3 mM malate (brain, heart and liver) or 2 mM glutamate plus 2 mM malate (skeletal muscle). (B) Ratio between H2O2 production and O2 consumption by isolated mitochondria under the same conditions as panel A. Data represent averages ± SEM and were compared using t tests (n = 4–6 animals).
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pone.0120413.g004: Reactive oxygen species production is not significantly altered by IF.(A) H2O2 release by isolated mitochondria in the presence of 1 mM ADP (state 3) and 5 mM pyruvate plus 3 mM malate (brain, heart and liver) or 2 mM glutamate plus 2 mM malate (skeletal muscle). (B) Ratio between H2O2 production and O2 consumption by isolated mitochondria under the same conditions as panel A. Data represent averages ± SEM and were compared using t tests (n = 4–6 animals).

Mentions: In addition to determining changes in functional parameters, we measured the release of mitochondrial H2O2, a relatively stable and membrane-permeable ROS often used as a marker for oxidant production (Fig. 4) [28]. Interestingly, we found that IF did not significantly alter absolute H2O2 release in any tissue (Fig. 4A), although liver release was slightly increased (p = 0.07). IF decreased relative H2O2/O2 release (Fig. 4B) in liver due to the enhanced O2 consumption observed in Figs. 2 and 3, and no change in this ratio was observed in other tissues. Since changes in respiratory rates and mitochondrial coupling are often determinant toward mitochondrial oxidant generation, this result is compatible with our finding that IF does not alter mitochondrial bioenergetic parameters in brain, heart and skeletal muscle. Furthermore, the lack of changes in H2O2 in liver are compatible with the prior finding that oxidant release in this tissue is not strongly regulated by respiratory rates and coupling [15].


Intermittent fasting results in tissue-specific changes in bioenergetics and redox state.

Chausse B, Vieira-Lara MA, Sanchez AB, Medeiros MH, Kowaltowski AJ - PLoS ONE (2015)

Reactive oxygen species production is not significantly altered by IF.(A) H2O2 release by isolated mitochondria in the presence of 1 mM ADP (state 3) and 5 mM pyruvate plus 3 mM malate (brain, heart and liver) or 2 mM glutamate plus 2 mM malate (skeletal muscle). (B) Ratio between H2O2 production and O2 consumption by isolated mitochondria under the same conditions as panel A. Data represent averages ± SEM and were compared using t tests (n = 4–6 animals).
© Copyright Policy
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4352038&req=5

pone.0120413.g004: Reactive oxygen species production is not significantly altered by IF.(A) H2O2 release by isolated mitochondria in the presence of 1 mM ADP (state 3) and 5 mM pyruvate plus 3 mM malate (brain, heart and liver) or 2 mM glutamate plus 2 mM malate (skeletal muscle). (B) Ratio between H2O2 production and O2 consumption by isolated mitochondria under the same conditions as panel A. Data represent averages ± SEM and were compared using t tests (n = 4–6 animals).
Mentions: In addition to determining changes in functional parameters, we measured the release of mitochondrial H2O2, a relatively stable and membrane-permeable ROS often used as a marker for oxidant production (Fig. 4) [28]. Interestingly, we found that IF did not significantly alter absolute H2O2 release in any tissue (Fig. 4A), although liver release was slightly increased (p = 0.07). IF decreased relative H2O2/O2 release (Fig. 4B) in liver due to the enhanced O2 consumption observed in Figs. 2 and 3, and no change in this ratio was observed in other tissues. Since changes in respiratory rates and mitochondrial coupling are often determinant toward mitochondrial oxidant generation, this result is compatible with our finding that IF does not alter mitochondrial bioenergetic parameters in brain, heart and skeletal muscle. Furthermore, the lack of changes in H2O2 in liver are compatible with the prior finding that oxidant release in this tissue is not strongly regulated by respiratory rates and coupling [15].

Bottom Line: Although the consequences of CR are well studied, the effects of IF on redox status are not.No difference in mitochondrial bioenergetics or redox homeostasis was observed in skeletal muscles of IF animals.Overall, IF affects redox balance in a tissue-specific manner, leading to redox imbalance in the liver and brain and protection against oxidative damage in the heart.

View Article: PubMed Central - PubMed

Affiliation: Departamento de Bioquímica, Instituto de Química, Universidade de São Paulo, São Paulo, Brazil.

ABSTRACT
Intermittent fasting (IF) is a dietary intervention often used as an alternative to caloric restriction (CR) and characterized by 24 hour cycles alternating ad libitum feeding and fasting. Although the consequences of CR are well studied, the effects of IF on redox status are not. Here, we address the effects of IF on redox state markers in different tissues in order to uncover how changes in feeding frequency alter redox balance in rats. IF rats displayed lower body mass due to decreased energy conversion efficiency. Livers in IF rats presented increased mitochondrial respiratory capacity and enhanced levels of protein carbonyls. Surprisingly, IF animals also presented an increase in oxidative damage in the brain that was not related to changes in mitochondrial bioenergetics. Conversely, IF promoted a substantial protection against oxidative damage in the heart. No difference in mitochondrial bioenergetics or redox homeostasis was observed in skeletal muscles of IF animals. Overall, IF affects redox balance in a tissue-specific manner, leading to redox imbalance in the liver and brain and protection against oxidative damage in the heart.

Show MeSH
Related in: MedlinePlus