Differentiating between apparent and actual rates of H2O2 metabolism by isolated rat muscle mitochondria to test a simple model of mitochondria as regulators of H2O2 concentration

Redox Biology

Volumn 5, Issue , 2015, Pages 216-224

  Treberg, Jason R ^a   Munro, Daniel ^a   Banh, Sheena ^a   Zacharias, Pamela ^a   Sotiri, Emianka ^a  

^a UNIVERSITY OF MANITOBA   (Canada)

Author keywords

Antioxidants; Bioenergetics; Mitochondria; Reactive oxygen species

Indexed keywords

HYDROGEN PEROXIDE; REACTIVE OXYGEN METABOLITE; ANTIRHEUMATIC AGENT; AURANOFIN; SUPEROXIDE;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DIFFUSION; FEMALE; MALE; MATHEMATICAL MODEL; METABOLIC RATE; METABOLIC REGULATION; MITOCHONDRIAL RESPIRATION; MUSCLE MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; RAT; SKELETAL MUSCLE; STEADY STATE; ANIMAL; DRUG EFFECTS; ELECTROCHEMICAL ANALYSIS; FLUOROMETRY; KINETICS; METABOLISM; SPRAGUE DAWLEY RAT;

ANIMALIA; RATTUS;

ANIMALS; ANTIRHEUMATIC AGENTS; AURANOFIN; ELECTROCHEMICAL TECHNIQUES; FEMALE; FLUOROMETRY; HYDROGEN PEROXIDE; KINETICS; MALE; MITOCHONDRIA, MUSCLE; RATS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES; SUPEROXIDES;

EID: 84930945346     PISSN: 22132317     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.redox.2015.05.001     Document Type: Article

References (38)

1. 2 by mouse brain mitochondria. Journal of Bioenergetics and Biomembranes 2014, 46(6):471-477. http://www.ncbi.nlm.nih.gov/pubmed/25248416, 10.1007/s10863-014-9581-9.
2. Jensen P.K. Antimycin-insensitive oxidation of succinate and reduced nicotinamide-adenine dinucleotide in electron-transport particles I. pH dependency and hydrogen peroxide formation. Biochimica et Biophysica Acta 1966, 122(2):157-166.
3. Loschen G., Flohé L., Chance B. Respiratory chain linked H(2)O(2) production in pigeon heart mitochondria. FEBS Letters 1971, 18(2):261-264. http://www.ncbi.nlm.nih.gov/pubmed/11946135, 10.1016/0014-5793(71)80459-3.
4. Boveris A., Oshino N., Chance B. The cellular production of hydrogen peroxide. Biochemical Journal 1972, 128(3):617-630. http://www.ncbi.nlm.nih.gov/pubmed/4404507.
5. Boveris A., Chance B. The mitochondrial generation of hydrogen peroxide. General properties and effect of hyperbaric oxygen. Biochemical Journal 1973, 134(3):707-716. http://www.ncbi.nlm.nih.gov/pubmed/4749271.
6. Brown G.C., Borutaite V. There is no evidence that mitochondria are the main source of reactive oxygen species in mammalian cells. Mitochondrion 2012, 12(1):1-4. http://www.ncbi.nlm.nih.gov/pubmed/21303703, 10.1016/j.mito.2011.02.001.
7. Rolo A.P., Palmeira C.M. Diabetes and mitochondrial function: role of hyperglycemia and oxidative stress. Toxicology and Applied Pharmacology 2006, 212(2):167-178. http://www.ncbi.nlm.nih.gov/pubmed/16490224, 10.1016/j.taap.2006.01.003.
8. Trushina E., McMurray C.T. Oxidative stress and mitochondrial dysfunction in neurodegenerative diseases. Neuroscience 2007, 145(4):1233-1248. http://www.ncbi.nlm.nih.gov/pubmed/17303344, 10.1016/j.neuroscience.2006.10.056.
9. Newsholme P., Gaudel C., Krause M. Mitochondria and diabetes, an intriguing pathogenetic role. Advances in Mitochondrial Medicine 2012, 235-247. Springer. R. Scatena, P. Bottoni, B. Giardina (Eds.).
10. Dugan L.L., You Y.H., Ali S.S., Diamond-Stanic M., Miyamoto S., DeCleves A.E., Andreyev A., Quach T., Ly S., Shekhtman G., Nguyen W., Chepetan A., Le T.P., Wang L., Xu M., Paik K.P., Fogo A., Viollet B., Murphy A., Brosius F., Naviaux R.K., Sharma K. AMPK dysregulation promotes diabetes-related reduction of superoxide and mitochondrial function. Journal of Clinical Investigation 2013, 123(11):4888-4899. http://www.ncbi.nlm.nih.gov/pubmed/24135141, 10.1172/JCI66218.
11. Dai D.F., Chiao Y.A., Marcinek D.J., Szeto H.H., Rabinovitch P.S. Mitochondrial oxidative stress in aging and healthspan. Longevity & Healthspan 2014, 3:6. http://www.ncbi.nlm.nih.gov/pubmed/24860647, 10.1186/2046-2395-3-6.
12. Day B.J. Antioxidant therapeutics: Pandora's box. Free Radical Biology and Medicine 2014, 66:58-64. http://www.ncbi.nlm.nih.gov/pubmed/23856377, 10.1016/j.freeradbiomed.2013.05.047.
13. Mason S., Wadley G.D. Skeletal muscle reactive oxygen species: a target of good cop/bad cop for exercise and disease. Redox Report 2014, 19(3):97-106. http://www.ncbi.nlm.nih.gov/pubmed/24620937, 10.1179/1351000213Y.0000000077.
14. Starkov A.A., Fiskum G., Chinopoulos C., Lorenzo B.J., Browne S.E., Patel M.S., Beal M.F. Mitochondrial α-ketoglutarate dehydrogenase complex generates reactive oxygen species. Journal of Neuroscience 2004, 24(36):7779-7788. http://www.ncbi.nlm.nih.gov/pubmed/15356189, 10.1523/JNEUROSCI.1899-04.2004.
15. Tretter L., Adam-Vizi V. Generation of reactive oxygen species in the reaction catalyzed by α-ketoglutarate dehydrogenase. Journal of Neuroscience 2004, 24(36):7771-7778. http://www.ncbi.nlm.nih.gov/pubmed/15356188, 10.1523/JNEUROSCI.1842-04.2004.
16. Brand M.D., Orr A.L., Perevoshchikova I.V., Quinlan C.L. The role of mitochondrial function and cellular bioenergetics in ageing and disease. British Journal of Dermatology 2013, 169(Suppl. 2):S1-S8. http://www.ncbi.nlm.nih.gov/pubmed/23786614, 10.1111/bjd.12208.
17. Liu S.S. Generating, partitioning, targeting and functioning of superoxide in mitochondria. Bioscience Reports 1997, 17(3):259-272. http://www.ncbi.nlm.nih.gov/pubmed/9337481, 10.1023/A:1027328510931.
18. Liu Y., Fiskum G., Schubert D. Generation of reactive oxygen species by the mitochondrial electron transport chain. Journal of Neurochemistry 2002, 80(5):780-787. http://www.ncbi.nlm.nih.gov/pubmed/11948241, 10.1046/j.0022-3042.2002.00744.x.
19. Adam-Vizi V. Production of reactive oxygen species in brain mitochondria: contribution by electron transport chain and non-electron transport chain sources. Antioxidants & Redox Signaling 2005, 7(9-10):1140-1149. http://www.ncbi.nlm.nih.gov/pubmed/16115017, 10.1089/ars.2005.7.1140.
20. Muller F.L., Liu Y., Abdul-Ghani M.A., Lustgarten M.S., Bhattacharya A., Jang Y.C., Van Remmen H. High rates of superoxide production in skeletal-muscle mitochondria respiring on both complex I- and complex II-linked substrates. Biochemical Journal 2008, 409(2):491-499. http://www.ncbi.nlm.nih.gov/pubmed/17916065, 10.1042/BJ20071162.
21. Quinlan C.L., Treberg J.R., Perevoshchikova I.V., Orr A.L., Brand M.D. Native rates of superoxide production from multiple sites in isolated mitochondria measured using endogenous reporters. Free Radical Biology and Medicine 2012, 53(9):1807-1817. http://www.ncbi.nlm.nih.gov/pubmed/22940066, 10.1016/j.freeradbiomed.2012.08.015.
22. Quinlan C.L., Perevoshchikova I.V., Hey-Mogensen M., Orr A.L., Brand M.D. Sites of reactive oxygen species generation by mitochondria oxidizing different substrates. Redox Biology 2013, 1:304-312. http://www.ncbi.nlm.nih.gov/pubmed/24024165, 10.1016/j.redox.2013.04.005.
23. Goncalves R.L., Quinlan C.L., Perevoshchikova I.V., Hey-Mogensen M., Brand M.D. Sites of superoxide and hydrogen peroxide production by muscle mitochondria assessed ex vivo under conditions mimicking rest and exercise. Journal of Biological Chemistry 2015, 290(1):209-227. http://www.ncbi.nlm.nih.gov/pubmed/25389297, 10.1074/jbc.M114.619072.
24. Treberg J.R., Quinlan C.L., Brand M.D. Hydrogen peroxide efflux from muscle mitochondria underestimates matrix superoxide production - a correction using glutathione depletion. FEBS Journal 2010, 277(13):2766-2778. http://www.ncbi.nlm.nih.gov/pubmed/20491900, 10.1111/j.1742-4658.2010.07693.x.
25. +. Journal of Biological Chemistry 2004, 279(6):4166-4174. http://www.ncbi.nlm.nih.gov/pubmed/14634020, 10.1074/jbc.M308143200.
26. Lambert A.J., Brand M.D. Inhibitors of the quinone-binding site allow rapid superoxide production from mitochondrial NADH:ubiquinone oxidoreductase (complex I). Journal of Biological Chemistry 2004, 279(38):39414-39420. http://www.ncbi.nlm.nih.gov/pubmed/15262965, 10.1074/jbc.M406576200.
27. Rigobello M.P., Folda A., Scutari G., Bindoli A. The modulation of thiol redox state affects the production and metabolism of hydrogen peroxide by heart mitochondria. Archives of Biochemistry and Biophysics 2005, 441(2):112-122. http://www.ncbi.nlm.nih.gov/pubmed/16111648, 10.1016/j.abb.2005.07.007.
28. 2 removal in brain mitochondria via the thioredoxin/Peroxiredoxin System. Journal of Biological Chemistry 2010, 285(36):27850-27858. http://www.ncbi.nlm.nih.gov/pubmed/20558743, 10.1074/jbc.M110.101196.
29. 2 metabolism in skeletal muscle mitochondria. FEBS Letters 2013, 587(12):1799-1804. http://www.ncbi.nlm.nih.gov/pubmed/23669366, 10.1016/j.febslet.2013.04.035.
30. Phung C.D., Ezieme J.A., Turrens J.F. Hydrogen peroxide metabolism in skeletal muscle mitochondria. Archives of Biochemistry and Biophysics 1994, 315(2):479-482. http://www.ncbi.nlm.nih.gov/pubmed/7986095, 10.1006/abbi.1994.1528.
31. Affourtit C., Quinlan C.L., Brand M.D. Measurement of proton leak and electron leak in isolated mitochondria. Mitochondrial Bioenergetics 2012, 165-182. Humana Press, New York. C.M. Palmeira, A.N.J. Moreno (Eds.).
32. Shimomura K., Galvanovskis J., Goldsworthy M., Hugill A., Kaizak S., Lee A., Meadows N., Quwailid M.M., Rydström J., Teboul L., Ashcroft F., Cox R.D. Insulin secretion from β-cells is affected by deletion of nicotinamide nucleotide transhydrogenase. Methods in Enzymology Mitochondrial Function, Part B: Mitochondrial Protein Kinases, Protein Phosphatases and Mitochondrial Diseases 2009, 451-480. Academic Press, Waltman, MA. W.S. Allison, Anne (Eds.).
33. Sheeran F.L., Rydström J., Shakhparonov M.I., Pestov N.B., Pepe S. Diminished NADPH transhydrogenase activity and mitochondrial redox regulation in human failing myocardium. Biochimica et Biophysica Acta 2010, 1797:1138-1148.
34. Sauer L.A. An NAD- and NADP-dependent malic enzyme with regulatory properties in rat liver and adrenal cortex mitochondrial fractions. Biochemical and Biophysical Research Communications 1973, 50(2):524-531. http://www.ncbi.nlm.nih.gov/pubmed/4144006, 10.1016/0006-291X(73)90871-1.
35. +-dependent enzyme. Biochimica et Biophysica Acta 1987, 916(3):446-454. http://www.ncbi.nlm.nih.gov/pubmed/3689803, 10.1016/0167-4838(87)90191-9.
36. Tretter L., Horvath G., Hölgyesi A., Essek F., Adam-Vizi V. Enhanced hydrogen peroxide generation accompanies the beneficial bioenergetic effects of methylene blue in isolated brain mitochondria. Free Radical Biology and Medicine 2014, 77:317-330. http://www.ncbi.nlm.nih.gov/pubmed/25277417, 10.1016/j.freeradbiomed.2014.09.024.
37. Rigobello M.P., Folda A., Baldoin M.C., Scutari G., Bindoli A. Effect of auranofin on the mitochondrial generation of hydrogen peroxide. Role of thioredoxin reductase. Free Radical Research 2005, 39(7):687-695. http://www.ncbi.nlm.nih.gov/pubmed/16036347, 10.1080/10715760500135391.
38. Stanley B.A., Sivakumaran V., Shi S., McDonald I., Lloyd D., Watson W.H., Aon M.A., Paolocci N. Thioredoxin reductase-2 is essential for keeping low levels of H(2)O(2) emission from isolated heart mitochondria. Journal of Biological Chemistry 2011, 286(38):33669-33677. http://www.ncbi.nlm.nih.gov/pubmed/21832082, 10.1074/jbc.M111.284612.