Catalase-dependent H2O2 consumption by cardiac mitochondria and redox-mediated loss in insulin signaling

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 311, Issue 5, 2016, Pages H1091-H1096

  Rindler, Paul M ^a   Cacciola, Angela ^a   Kinter, Michael ^a   Szweda, Luke I ^a  

^a OKLAHOMA MEDICAL RESEARCH FOUNDATION   (United States)

Author keywords

Catalase; H2O2; Heart; Insulin signaling; Mitochondria

Indexed keywords

CATALASE; GLUTATHIONE; GLUTATHIONE DISULFIDE; GLUTATHIONE PEROXIDASE; HYDROGEN PEROXIDE; INSULIN; IODOACETAMIDE; ANTIDIABETIC AGENT; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; PROTEIN KINASE B;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; FAT INTAKE; HEART MITOCHONDRION; LOW FAT DIET; MOUSE; NONHUMAN; OXIDATION REDUCTION REACTION; PEROXISOME; PRIORITY JOURNAL; ANIMAL; DRUG EFFECTS; GENETICS; KNOCKOUT MOUSE; LIPID DIET; METABOLISM; OXIDATIVE STRESS; PHOSPHORYLATION; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CATALASE; DIET, FAT-RESTRICTED; DIET, HIGH-FAT; GLUTATHIONE; GLUTATHIONE DISULFIDE; HYDROGEN PEROXIDE; HYPOGLYCEMIC AGENTS; INSULIN; MICE; MICE, KNOCKOUT; MITOCHONDRIA, HEART; NADP; OXIDATION-REDUCTION; OXIDATIVE STRESS; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION;

EID: 84994578327     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00066.2016     Document Type: Article

References (29)

1. Alfonso-Prieto M, Biarnes X, Vidossich P, Rovira C. The molecular mechanism of the catalase reaction. J Am Chem Soc 131: 11751-11761, 2009.
2. Antunes F, Han D, Cadenas E. Relative contributions of heart mitochondria glutathione peroxidase and catalase to H(2)O(2) detoxification in in vivo conditions. Free Radic Biol Med 33: 1260-1267, 2002.
3. Bulteau AL, Ikeda-Saito M, Szweda LI. Redox-dependent modulation of aconitase activity in intact mitochondria. Biochemistry 42: 14846-14855, 2003.
4. Bulteau AL, O’Neill HA, Kennedy MC, Ikeda-Saito M, Isaya G, Szweda LI. Frataxin acts as an iron chaperone protein to modulate mitochondrial aconitase activity. Science 305: 242-245, 2004.
5. Chance B, Sies H, Boveris A. Hydroperoxide metabolism in mammalian organs. Physiol Rev 59: 527-605, 1979.
6. Crewe C, Kinter M, Szweda LI. Rapid inhibition of pyruvate dehydrogenase: an initiating event in high dietary fat-induced loss of metabolic flexibility in the heart. PLoS One 8: e77280, 2013.
7. Fisher-Wellman KH, Neufer PD. Linking mitochondrial bioenergetics to insulin resistance via redox biology. Trends Endocrinol Metab 23: 142-153, 2012.
8. Gaetani GF, Ferraris AM, Rolfo M, Mangerini R, Arena S, Kirkman HN. Predominant role of catalase in the disposal of hydrogen peroxide within human erythrocytes. Blood 87: 1595-1599, 1996.
9. Ho YS, Xiong Y, Ma W, Spector A, Ho DS. Mice lacking catalase develop normally but show differential sensitivity to oxidant tissue injury. J Biol Chem 279: 32804-32812, 2004.
10. Iwakami S, Misu H, Takeda T, Sugimori M, Matsugo S, Kaneko S, Takamura T. Concentration-dependent dual effects of hydrogen peroxide on insulin signal transduction in H4IIEC hepatocytes. PLoS One 6: e27401, 2011.
11. Manta B, Hugo M, Ortiz C, Ferrer-Sueta G, Trujillo M, Denicola A. The peroxidase and peroxynitrite reductase activity of human erythrocyte peroxiredoxin 2. Arch Biochem Biophys 484: 146-154, 2009.
12. Marinho HS, Real C, Cyrne L, Soares H, Antunes F. Hydrogen peroxide sensing, signaling and regulation of transcription factors. Redox Biol 2: 535-562, 2014.
13. McLain AL, Cormier PJ, Kinter M, Szweda LI. Glutathionylation of alpha-ketoglutarate dehydrogenase: the chemical nature and relative susceptibility of the cofactor lipoic acid to modification. Free Radic Biol Med 61: 161-169, 2013.
14. Nicholls P, Fita I, Loewen PC. Enzymology and structure of catalases. Adv Inorganic Chem 51: 51-106, 2000.
15. Nulton-Persson AC, Szweda LI. Modulation of mitochondrial function by hydrogen peroxide. J Biol Chem 276: 23357-23361, 2001.
16. Paglialunga S, Ludzki A, Root-McCaig J, Holloway GP. In adipose tissue, increased mitochondrial emission of reactive oxygen species is important for short-term high-fat diet-induced insulin resistance in mice. Diabetologia 58: 1071-1080, 2015.
17. Prabhakar R, Vreven T, Morokuma K, Musaev DG. Elucidation of the mechanism of selenoprotein glutathione peroxidase (GPx)-catalyzed hydrogen peroxide reduction by two glutathione molecules: a density functional study. Biochemistry 44: 11864-11871, 2005.
18. Radi R, Turrens JF, Chang LY, Bush KM, Crapo JD, Freeman BA. Detection of catalase in rat heart mitochondria. J Biol Chem 266: 22028-22034, 1991.
19. Reczek CR, Chandel NS. ROS-dependent signal transduction. Curr Opin Cell Biol 33: 8-13, 2015.
20. Rhee SG. Cell signaling. H2O2, a necessary evil for cell signaling. Science 312: 1882-1883, 2006.
21. Rhee SG, Yang KS, Kang SW, Woo HA, Chang TS. Controlled elimination of intracellular H(2)O(2): regulation of peroxiredoxin, catalase, and glutathione peroxidase via post-translational modification. Antioxid Redox Signal 7: 619-626, 2005.
22. Rindler PM, Crewe CL, Fernandes J, Kinter M, Szweda LI. Redox regulation of insulin sensitivity due to enhanced fatty acid utilization in the mitochondria. Am J Physiol Heart Circ Physiol 305: H634-H643, 2013.
23. Rindler PM, Plafker SM, Szweda LI, Kinter M. High dietary fat selectively increases catalase expression within cardiac mitochondria. J Biol Chem 288: 1979-1990, 2013.
24. Sainz N, Rodriguez A, Catalan V, Becerril S, Ramirez B, Gomez-Ambrosi J, Fruhbeck G. Leptin administration downregulates the increased expression levels of genes related to oxidative stress and inflammation in the skeletal muscle of ob/ob mice. Mediators Inflamm 2010: 784343, 2010.
25. Schriner SE, Linford NJ, Martin GM, Treuting P, Ogburn CE, Emond M, Coskun PE, Ladiges W, Wolf N, Van Remmen H, Wallace DC, Rabinovitch PS. Extension of murine life span by overexpression of catalase targeted to mitochondria. Science 308: 1909-1911, 2005.
26. Ussher JR, Koves TR, Jaswal JS, Zhang L, Ilkayeva O, Dyck JR, Muoio DM, Lopaschuk GD. Insulin-stimulated cardiac glucose oxidation is increased in high-fat diet-induced obese mice lacking malonyl CoA decarboxylase. Diabetes 58: 1766-1775, 2009.
27. Veal EA, Day AM, Morgan BA. Hydrogen peroxide sensing and signaling. Mol Cell 26: 1-14, 2007.
28. Vincent HK, Taylor AG. Biomarkers and potential mechanisms of obesity-induced oxidant stress in humans. Int J Obes (Lond) 30: 400-418, 2006.
29. Zhang L, Ussher JR, Oka T, Cadete VJ, Wagg C, Lopaschuk GD. Cardiac diacylglycerol accumulation in high fat-fed mice is associated with impaired insulin-stimulated glucose oxidation. Cardiovasc Res 89: 148-156, 2011.