The Contribution of nicotinamide nucleotide transhydrogenase to peroxide detoxification is dependent on the respiratory state and counterbalanced by other sources of NADPH in liver mitochondria

Journal of Biological Chemistry

Volumn 291, Issue 38, 2016, Pages 20173-20187

  Ronchi, Juliana Aparecida ^a   Francisco, Annelise ^a   Passos, Luiz Augusto Correa ^a   Figueira, Tiago Rezende ^a   Castilho, Roger Frigério ^a  

^a UNIVERSITY OF CAMPINAS   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

AMIDES; BIOCHEMISTRY; CELL MEMBRANES; DETOXIFICATION; ELECTRON TRANSPORT PROPERTIES; MAMMALS; METABOLISM; MITOCHONDRIA; NUCLEOTIDES; PEROXIDES; PHYSIOLOGY;

ELECTROCHEMICAL POTENTIAL; ELECTRON TRANSPORT; GLUTAMATE DEHYDROGENASE; INNER MITOCHONDRIAL MEMBRANES; ISOCITRATE DEHYDROGENASE; LIVER MITOCHONDRIA; RELATIVE CONTRIBUTION; RESPIRATORY SUBSTRATES;

OXIDATION;

GLUTAMATE DEHYDROGENASE; ISOCITRATE DEHYDROGENASE 2; MALATE DEHYDROGENASE (DECARBOXYLATING); NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) TRANSHYDROGENASE; PEROXIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; MITOCHONDRIAL PROTEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; NNT PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL ISOLATION; CONTROLLED STUDY; DETOXIFICATION; ELECTRON TRANSPORT; ENERGY METABOLISM; ENZYME ACTIVITY; LIVER MITOCHONDRION; METABOLISM; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL RESPIRATION; MOUSE; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PEROXIDE METABOLISM; PHOSPHORYLATION; PRIORITY JOURNAL; ANIMAL; ENZYMOLOGY; GENETICS; MUTANT MOUSE STRAIN; OXYGEN CONSUMPTION; PHYSIOLOGY;

ANIMALS; ENERGY METABOLISM; MICE; MICE, MUTANT STRAINS; MITOCHONDRIA, LIVER; MITOCHONDRIAL PROTEINS; NADP; NADP TRANSHYDROGENASE, AB-SPECIFIC; OXYGEN CONSUMPTION; PEROXIDES;

EID: 84987788990     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M116.730473     Document Type: Article

References (51)

1. Agledal, L., Niere, M., and Ziegler, M. (2010) The phosphate makes a difference: cellular functions of NADP. Redox Rep. 15, 2-10
2. Rydström, J. (2006) Mitochondrial NADPH, transhydrogenase and disease. Biochim. Biophys. Acta 1757, 721-726
3. Gameiro, P. A., Laviolette, L. A., Kelleher, J. K., Iliopoulos, O., and Stephanopoulos, G. (2013) Cofactor balance by nicotinamide nucleotide transhydrogenase (NNT) coordinates reductive carboxylation and glucose catabolism in the tricarboxylic acid (TCA) cycle. J. Biol. Chem. 288, 12967-12977
4. Toye, A. A., Lippiat, J. D., Proks, P., Shimomura, K., Bentley, L., Hugill, A., Mijat, V., Goldsworthy, M., Moir, L., Haynes, A., Quarterman, J., Freeman, H. C., Ashcroft, F. M., and Cox, R. D. (2005) A genetic and physiological study of impaired glucose homeostasis control in C57BL/6J mice. Diabetologia 48, 675-686
5. Meimaridou, E., Kowalczyk, J., Guasti, L., Hughes, C. R., Wagner, F., Frommolt, P., Nürnberg, P., Mann, N. P., Banerjee, R., Saka, H. N., Chapple, J. P., King, P. J., Clark, A. J., and Metherell, L. A. (2012) Mutations in NNT encoding nicotinamide nucleotide transhydrogenase cause familial glucocorticoid deficiency. Nat. Genet. 44, 740-742
6. Nicholson, A., Reifsnyder, P. C., Malcolm, R. D., Lucas, C. A., MacGregor, G. R., Zhang, W., and Leiter, E. H. (2010) Diet-induced obesity in two C57BL/6 substrains with intact or mutant nicotinamide nucleotide transhydrogenase (Nnt) gene. Obesity 18, 1902-1905
7. Freeman, H. C., Hugill, A., Dear, N. T., Ashcroft, F. M., and Cox, R. D. (2006) Deletion of nicotinamide nucleotide transhydrogenase: a new quantitative trait locus accounting for glucose intolerance in C57BL/6J mice. Diabetes 55, 2153-2156
8. Fergusson, G., Ethier, M., Guévremont, M., Chrétien, C., Attané, C., Joly, E., Fioramonti, X., Prentki, M., Poitout, V., and Alquier, T. (2014) Defective insulin secretory response to intravenous glucose in C57Bl/6J compared to C57Bl/6N mice. Mol. Metab. 3, 848-854
9. Kraev, A. (2014) Parallel universes of black six biology. Biol. Direct 9, 18
10. Figueira, T. R. (2013) A word of caution concerning the use of Nntmutated C57BL/6 mice substrains as experimental models to study metabolism and mitochondrial pathophysiology. Exp. Physiol. 98, 1643
11. Fontaine, D. A., and Davis, D. B. (2016) Attention to background strain is essential for metabolic research: C57BL/6 and the International Knockout Mouse Consortium. Diabetes 65, 25-33
12. Bourdi, M., Davies, J. S., and Pohl, L. R. (2011) Mispairing C57BL/6 substrains of genetically engineered mice and wild-type controls can lead to confounding results as it did in studies of JNK2 in acetaminophen and concanavalin A liver injury. Chem. Res. Toxicol. 24, 794-796
13. Fujisawa, Y., Napoli, E., Wong, S., Song, G., Yamaguchi, R., Matsui, T., Nagasaki, K., Ogata, T., and Giulivi, C. (2015) Impact of a novel homozygous mutation in nicotinamide nucleotide transhydrogenase on mitochondrial DNA integrity in a case of familial glucocorticoid deficiency. BBA Clin. 3, 70-78
14. Leung, J. H., Schurig-Briccio, L. A., Yamaguchi, M., Moeller, A., Speir, J. A., Gennis, R. B., and Stout, C. D. (2015) Structural biology. Division of labor in transhydrogenase by alternating proton translocation and hydride transfer. Science 347, 178-181
15. Bizouarn, T., Sazanov, L. A., Aubourg, S., and Jackson, J. B. (1996) Estimation of the H+/- ratio of the reaction catalysed by the nicotinamide nucleotide transhydrogenase in chromatophores from overexpressing strains of Rhodospirillum rubrum and in liposomes inlaid with the purified bovine enzyme. Biochim. Biophys. Acta 1273, 4-12
16. Ronchi, J. A., Figueira, T. R., Ravagnani, F. G., Oliveira, H. C., Vercesi, A. E., and Castilho, R. F. (2013) A spontaneous mutation in the nicotinamide nucleotide transhydrogenase gene of C57BL/6J mice results in mitochondrial redox abnormalities. Free Radic. Biol. Med. 63, 446-456
17. Lopert, P., and Patel, M. (2014) Nicotinamide nucleotide transhydrogenase (Nnt) links the substrate requirement in brain mitochondria for hydrogen peroxide removal to the thioredoxin/peroxiredoxin (Trx/Prx) system. J. Biol. Chem. 289, 15611-15620
18. Figueira, T. R., Barros, M. H., Camargo, A. A., Castilho, R. F., Ferreira, J. C., Kowaltowski, A. J., Sluse, F. E., Souza-Pinto, N. C., and Vercesi, A. E. (2013) Mitochondria as a source of reactive oxygen and nitrogen species: from molecular mechanisms to human health. Antioxid. Redox Signal. 18, 2029-2074
19. Vercesi, A. E. (1987) The participation of NADP, the transmembrane potential and the energy-linked NAD(P) transhydrogenase in the process of Ca2+ efflux from rat liver mitochondria. Arch. Biochem. Biophys. 252, 171-178
20. Lehninger, A. L., Vercesi, A., and Bababunmi, E. A. (1978) Regulation of Ca 2+ release from mitochondria by the oxidation-reduction state of pyridine nucleotides. Proc. Natl. Acad. Sci. U.S.A. 75, 1690-1694
21. Estabrook, R. W. (1962) Fluorometric measurement of reduced pyridine nucleotide in cellular and subcellular particles. Anal. Biochem. 4, 231-245
22. Yin, F., Sancheti, H., and Cadenas, E. (2012) Silencing of nicotinamide nucleotide transhydrogenase impairs cellular redox homeostasis and energy metabolism in PC12 cells. Biochim. Biophys. Acta 1817, 401-409
23. Ripoll, V. M., Meadows, N. A., Bangert, M., Lee, A. W., Kadioglu, A., and Cox, R. D. (2012) Nicotinamide nucleotide transhydrogenase (NNT) acts as a novel modulator of macrophage inflammatory responses. FASEB J. 26, 3550-3562
24. Vogel, R., Wiesinger, H., Hamprecht, B., and Dringen, R. (1999) The regeneration of reduced glutathione in rat forebrain mitochondria identifies metabolic pathways providing the NADPH required. Neurosci. Lett. 275, 97-100
25. Davisson, M. T. (2005) Discovery genetics: serendipity in basic research. ILAR J. 46, 338-345
26. Conner, D. A. (2002) Mouse colony management. Curr. Protoc. Mol. Biol. Chapter 23, Unit 23.28
27. Crusio, W. E., Goldowitz, D., Holmes, A., and Wolfer, D. (2009) Standards for the publication of mouse mutant studies. Genes Brain. Behav. 8, 1-4
28. Larsen, S., Nielsen, J., Hansen, C. N., Nielsen, L. B., Wibrand, F., Stride, N., Schroder, H. D., Boushel, R., Helge, J. W., Dela, F., and Hey-Mogensen, M. (2012) Biomarkers of mitochondrial content in skeletal muscle of healthy young human subjects. J. Physiol. 590, 3349-3360
29. Flohé, L., Toppo, S., Cozza, G., and Ursini, F. (2011) A comparison of thiol peroxidase mechanisms. Antioxid. Redox Signal. 15, 763-780
30. Reinhart, P. H., Taylor, W. M., and Bygrave, F. L. (1982) A procedure for the rapid preparation of mitochondria from rat liver. Biochem. J. 204, 731-735
31. Godinot, C., and Gautheron, D. (1971) Regulation of pig heart mitochondrial glutamate dehydrogenase by nucleotides and phosphate: Comparison with pig heart and beef liver purified enzymes. FEBS Lett. 13, 235-240
32. Hsieh, J. Y., Chen, M. C., and Hung, H. C. (2011) Determinants of nucleotide-binding selectivity of malic enzyme. PLoS ONE 6, e25312
33. Lin, R. C., and Davis, E. J. (1974) Malic enzymes of rabbit heart mitochondria. Separation and comparison of some characteristics of a nicotinamide adenine dinucleotide-preferring and a nicotinamide adenine dinucleotide phosphate-specific enzyme. J. Biol. Chem. 249, 3867-3875
34. Chouchani, E. T., Pell, V. R., Gaude, E., Aksentijević, D., Sundier, S. Y., Robb, E. L., Logan, A., Nadtochiy, S. M., Ord, E. N., Smith, A. C., Eyassu, F., Shirley, R., Hu, C. H., Dare, A. J., James, A. M., et al. (2014) Ischaemic accumulation of succinate controls reperfusion injury through mitochondrial ROS. Nature 515, 431-435
35. Arkblad, E. L., Tuck, S., Pestov, N. B., Dmitriev, R. I., Kostina, M. B., Stenvall, J., Tranberg, M., and Rydström, J. (2005) A Caenorhabditis elegans mutant lacking functional nicotinamide nucleotide transhydrogenase displays increased sensitivity to oxidative stress. Free Radic. Biol. Med. 38, 1518-1525
36. Sauer, U., Canonaco, F., Heri, S., Perrenoud, A., and Fischer, E. (2004) The soluble and membrane-bound transhydrogenases UdhA and PntAB have divergent functions in NADPH metabolism of Escherichia coli. J. Biol. Chem. 279, 6613-6619
37. Lenartowicz, E., and Wojtczak, A. B. (1988) Significance of the alanine aminotransferase reaction in the formation of α-ketoglutarate in rat liver mitochondria. Arch. Biochem. Biophys. 260, 309-319
38. Quinlan, C. L., Goncalves, R. L., Hey-Mogensen, M., Yadava, N., Bunik, V. I., and Brand, M. D. (2014) The 2-oxoacid dehydrogenase complexes in mitochondria can produce superoxide/hydrogen peroxide at much higher rates than complex I. J. Biol. Chem. 289, 8312-8325
39. Nicholls, D. G., and Garland, P. B. (1969) The control of isocitrate oxidation by rat liver mitochondria. Biochem. J. 114, 215-225
40. Hoek, J. B., and Rydström, J. (1988) Physiological roles of nicotinamide nucleotide transhydrogenase. Biochem. J. 254, 1-10
41. Chandel, N. S., Budinger, G. R., Choe, S. H., and Schumacker, P. T. (1997) Cellular respiration during hypoxia. Role of cytochrome oxidase as the oxygen sensor in hepatocytes. J. Biol. Chem. 272, 18808-18816
42. Drahota, Z., Kriváková, P., Cervinková, Z., Kmonícková, E., Lotková, H., Kucera, O., and Houstek, J. (2005) tert-Butyl hydroperoxide selectively inhibits mitochondrial respiratory-chain enzymes in isolated rat hepatocytes. Physiol. Res. 54, 67-72
43. Cervinková, Z., Rauchová, H., Kriváková, P., and Drahota, Z. (2008) Inhibition of palmityl carnitine oxidation in rat liver mitochondria by tertbutyl hydroperoxide. Physiol. Res. 57, 133-136
44. Chweih, H., Castilho, R. F., and Figueira, T. R. (2015) Tissue and sex specificities in Ca 2ô handling by isolated mitochondria in conditions avoiding the permeability transition. Exp. Physiol. 100, 1073-1092
45. Liu, H., and Kehrer, J. P. (1996) The reduction of glutathione disulfide produced by t-butyl hydroperoxide in respiring mitochondria. Free Radic. Biol. Med. 20, 433-442
46. Conner, D. A. (2002) Mouse colony management. Curr. Protoc. Mol. Biol. Chapter 23, Unit 23.28
47. Zhang, X., Vincent, A. S., Halliwell, B., and Wong, K. P. (2004) A mechanism of sulfite neurotoxicity: direct inhibition of glutamate dehydrogenase. J. Biol. Chem. 279, 43035-43045
48. Geer, B. W., Krochko, D., Oliver, M. J., Walker, V. K., and Williamson, J. H. (1980) A comparative-study of the NADP-malic enzymes from Drosophila and chick liver. Comp. Biochem. Physiol. B 65, 25-34
49. Figueira, T. R., Castilho, R. F., Saito, A., Oliveira, H. C., and Vercesi, A. E. (2011) The higher susceptibility of congenital analbuminemic rats to Ca2+ -induced mitochondrial permeability transition is associated with the increased expression of cyclophilin D and nitrosothiol depletion. Mol. Genet. Metab. 104, 521-528
50. Chen, Y., Cai, J., and Jones, D. P. (2006) Mitochondrial thioredoxin in regulation of oxidant-induced cell death. FEBS Lett. 580, 6596-6602
51. Figueira, T. R., Melo, D. R., Vercesi, A. E., and Castilho, R. F. (2012) Safranine as a fluorescent probe for the evaluation of mitochondrial membrane potential in isolated organelles and permeabilized cells. Methods Mol. Biol. 810, 103-117