Caloric Restriction Influences Hydrogen Peroxide Generation in Mitochondrial Sub-populations from Mouse Liver

Overview

Journal J Bioenerg Biomembr

Publisher Springer

Specialties Biochemistry
Biology
Endocrinology

Date 2011 Apr 21

PMID 21505800

Citations 11

Authors

Kevork Hagopian

Yana Chen

Keira Simmons Domer

Robert Soo Hoo

Trevor Bentley

Roger B McDonald

Jon J Ramsey

Affiliations

Soon will be listed here.

Abstract

Calorie restriction (CR) has been shown to decrease H(2)O(2) production in liver mitochondria, although it is not known if this is due to uniform changes in all mitochondria or changes in particular mitochondrial sub-populations. To address this issue, liver mitochondria from control and CR mice were fractionated using differential centrifugation at 1,000 g, 3,000 g and 10,000 g into distinct populations labeled as M1, M3 and M10, respectively. Mitochondrial protein levels, respiration and H(2)O(2) production were measured in each fraction. CR resulted in a decrease in total protein (mg) in each fraction, although this difference disappeared when adjusted for liver weight (mg protein/g liver weight). No differences in respiration (State 3 or 4) were observed between control and CR mice in any of the mitochondrial fractions. CR decreased H(2)O(2) production in all fractions when mitochondria respired on succinate (Succ), succ+antimycin A (Succ+AA) or pyruvate/malate+rotenone (P/M+ROT). Thus, CR decreased reactive oxygen species (ROS) production under conditions which stimulate mitochondrial complex I ROS production under both forward (P/M+ROT) and backward (Succ & Succ+AA) electron flow. The results indicate that CR decreases H(2)O(2) production in all liver mitochondrial fractions due to a decrease in capacity for ROS production by complex I of the electron transport chain.

Citing Articles

Melatonin Attenuates Calcium Deposition from Vascular Smooth Muscle Cells by Activating Mitochondrial Fusion and Mitophagy via an AMPK/OPA1 Signaling Pathway.

Chen W, Zhou Y, Yang J, Liu F, Wu X, Sha Y Oxid Med Cell Longev. 2020; 2020:5298483.

PMID: 32377301 PMC: 7196154. DOI: 10.1155/2020/5298483.

Use the Protonmotive Force: Mitochondrial Uncoupling and Reactive Oxygen Species.

Berry B, Trewin A, Amitrano A, Kim M, Wojtovich A J Mol Biol. 2018; 430(21):3873-3891.

PMID: 29626541 PMC: 6170739. DOI: 10.1016/j.jmb.2018.03.025.

Production of superoxide and hydrogen peroxide from specific mitochondrial sites under different bioenergetic conditions.

Wong H, Dighe P, Mezera V, Monternier P, Brand M J Biol Chem. 2017; 292(41):16804-16809.

PMID: 28842493 PMC: 5641882. DOI: 10.1074/jbc.R117.789271.

An In Vivo Magnetic Resonance Spectroscopy Study of the Effects of Caloric and Non-Caloric Sweeteners on Liver Lipid Metabolism in Rats.

Janssens S, Ciapaite J, Wolters J, van Riel N, Nicolay K, Prompers J Nutrients. 2017; 9(5).

PMID: 28489050 PMC: 5452206. DOI: 10.3390/nu9050476.

Collaboration between mitochondria and the nucleus is key to long life in Caenorhabditis elegans.

Chang H, Shtessel L, Lee S Free Radic Biol Med. 2014; 78:168-78.

PMID: 25450327 PMC: 4280335. DOI: 10.1016/j.freeradbiomed.2014.10.576.

References

Page M, Robb E, Salway K, Stuart J . Mitochondrial redox metabolism: aging, longevity and dietary effects. Mech Ageing Dev. 2010; 131(4):242-52. DOI: 10.1016/j.mad.2010.02.005. View

Sanz A, Caro P, Ibanez J, Gomez J, Gredilla R, Barja G . Dietary restriction at old age lowers mitochondrial oxygen radical production and leak at complex I and oxidative DNA damage in rat brain. J Bioenerg Biomembr. 2005; 37(2):83-90. DOI: 10.1007/s10863-005-4131-0. View

Lambert A, Wang B, Yardley J, Edwards J, Merry B . The effect of aging and caloric restriction on mitochondrial protein density and oxygen consumption. Exp Gerontol. 2004; 39(3):289-95. DOI: 10.1016/j.exger.2003.12.009. View

Chance B, Sies H, Boveris A . Hydroperoxide metabolism in mammalian organs. Physiol Rev. 1979; 59(3):527-605. DOI: 10.1152/physrev.1979.59.3.527. View

Weindruch R, Cheung M, Verity M, WALFORD R . Modification of mitochondrial respiration by aging and dietary restriction. Mech Ageing Dev. 1980; 12(4):375-92. DOI: 10.1016/0047-6374(80)90070-6. View

Pamplona R, Barja G . Mitochondrial oxidative stress, aging and caloric restriction: the protein and methionine connection. Biochim Biophys Acta. 2006; 1757(5-6):496-508. DOI: 10.1016/j.bbabio.2006.01.009. View

Venditti P, De Rosa R, Caldarone G, Di Meo S . Functional and biochemical characteristics of mitochondrial fractions from rat liver in cold-induced oxidative stress. Cell Mol Life Sci. 2004; 61(24):3104-16. DOI: 10.1007/s00018-004-4308-4. View

Murphy M . How mitochondria produce reactive oxygen species. Biochem J. 2008; 417(1):1-13. PMC: 2605959. DOI: 10.1042/BJ20081386. View

Matamala J, Gianotti M, Pericas J, Quevedo S, Roca P, Palou A . Changes induced by fasting and dietetic obesity in thermogenic parameters of rat brown adipose tissue mitochondrial subpopulations. Biochem J. 1996; 319 ( Pt 2):529-34. PMC: 1217800. DOI: 10.1042/bj3190529. View

10.

Moreno M, Puigserver P, Llull J, Gianotti M, Lanni A, Goglia F . Cold exposure induces different uncoupling-protein thermogenin masking/unmasking processes in brown adipose tissue depending on mitochondrial subtypes. Biochem J. 1994; 300 ( Pt 2):463-8. PMC: 1138185. DOI: 10.1042/bj3000463. View

11.

Venditti P, Costagliola I, Di Meo S . H2O2 production and response to stress conditions by mitochondrial fractions from rat liver. J Bioenerg Biomembr. 2002; 34(2):115-25. DOI: 10.1023/a:1015175925756. View

12.

Sohal R, Weindruch R . Oxidative stress, caloric restriction, and aging. Science. 1996; 273(5271):59-63. PMC: 2987625. DOI: 10.1126/science.273.5271.59. View

13.

Nisoli E, Tonello C, Cardile A, Cozzi V, Bracale R, Tedesco L . Calorie restriction promotes mitochondrial biogenesis by inducing the expression of eNOS. Science. 2005; 310(5746):314-7. DOI: 10.1126/science.1117728. View

14.

Harman D . Aging: a theory based on free radical and radiation chemistry. J Gerontol. 1956; 11(3):298-300. DOI: 10.1093/geronj/11.3.298. View

15.

Hagopian K, Harper M, Ram J, Humble S, Weindruch R, Ramsey J . Long-term calorie restriction reduces proton leak and hydrogen peroxide production in liver mitochondria. Am J Physiol Endocrinol Metab. 2004; 288(4):E674-84. DOI: 10.1152/ajpendo.00382.2004. View

16.

Lopez-Lluch G, Hunt N, Jones B, Zhu M, Jamieson H, Hilmer S . Calorie restriction induces mitochondrial biogenesis and bioenergetic efficiency. Proc Natl Acad Sci U S A. 2006; 103(6):1768-73. PMC: 1413655. DOI: 10.1073/pnas.0510452103. View

17.

Lambert A, Merry B . Effect of caloric restriction on mitochondrial reactive oxygen species production and bioenergetics: reversal by insulin. Am J Physiol Regul Integr Comp Physiol. 2003; 286(1):R71-9. DOI: 10.1152/ajpregu.00341.2003. View

18.

Weindruch R, Sohal R . Seminars in medicine of the Beth Israel Deaconess Medical Center. Caloric intake and aging. N Engl J Med. 1997; 337(14):986-94. PMC: 2851235. DOI: 10.1056/NEJM199710023371407. View

19.

Gredilla R, Sanz A, Lopez-Torres M, Barja G . Caloric restriction decreases mitochondrial free radical generation at complex I and lowers oxidative damage to mitochondrial DNA in the rat heart. FASEB J. 2001; 15(9):1589-91. DOI: 10.1096/fj.00-0764fje. View

20.

Gredilla R, Barja G, Lopez-Torres M . Effect of short-term caloric restriction on H2O2 production and oxidative DNA damage in rat liver mitochondria and location of the free radical source. J Bioenerg Biomembr. 2001; 33(4):279-87. DOI: 10.1023/a:1010603206190. View