Impaired utilization of membrane potential by complex II-energized mitochondria of obese, diabetic mice assessed using ADP recycling methodology

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 311, Issue 4, 2016, Pages R756-R763

  Fink, Brian D ^a   Bai, Fan ^b   Yu, Liping ^b,c   Sivitz, William I ^a  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b UNIVERSITY OF IOWA   (United States)

^c UNIVERSITY OF IOWA   (United States)

Author keywords

Bioenergetics; Diabetes; Mitochondria; Obesity; Succinate

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; GLUCOSE; OXYGEN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); ROTENONE; STREPTOZOCIN; SUCCINATE DEHYDROGENASE (UBIQUINONE); SUCCINIC ACID; SUPEROXIDE;

ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL FUNCTION; CONTROLLED STUDY; DIABETES MELLITUS; GLUCOSE BLOOD LEVEL; GLUCOSE UTILIZATION; LIPID DIET; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL RESPIRATION; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; SKELETAL MUSCLE; ANIMAL; C57BL MOUSE; CELL CULTURE; CHEMICALLY INDUCED; FEMALE; MALE; METABOLISM; MUSCLE MITOCHONDRION; OXYGEN CONSUMPTION; PATHOPHYSIOLOGY;

ADENOSINE DIPHOSPHATE; ANIMALS; CELLS, CULTURED; DIABETES MELLITUS, TYPE 2; ELECTRON TRANSPORT COMPLEX II; FEMALE; MALE; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MICE, INBRED C57BL; MITOCHONDRIA, MUSCLE; OBESITY; OXYGEN CONSUMPTION; STREPTOZOCIN;

EID: 84990923870     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00232.2016     Document Type: Article

References (37)

1. Bai F, Fink BD, Yu L, Sivitz WI. Voltage-dependent regulation of complex ii energized mitochondrial oxygen flux. PLoS One 11: e0154982, 2016. doi:10.1371/journal.pone.0154982
2. Boudina S, Sena S, Theobald H, Sheng X, Wright JJ, Hu XX, Aziz S, Johnson JI, Bugger H, Zaha VG, Abel ED. Mitochondrial energetics in the heart in obesity-related diabetes: direct evidence for increased uncoupled respiration and activation of uncoupling proteins. Diabetes 56: 2457-2466, 2007. doi:10.2337/db07-0481
3. Boushel R, Gnaiger E, Schjerling P, Skovbro M, Kraunsøe R, Dela F. Patients with type 2 diabetes have normal mitochondrial function in skeletal muscle. Diabetologia 50: 790-796, 2007. doi:10.1007/s00125-007-0594-3
4. Brand MD. The sites and topology of mitochondrial superoxide production. Exp Gerontol 45: 466-472, 2010. doi:10.1016/j.exger.2010.01.003
5. Brand MD, Nicholls DG. Assessing mitochondrial dysfunction in cells. Biochem J 435: 297-312, 2011. doi:10.1042/BJ20110162
6. Brawand F, Folly G, Walter P. Relation between extraand intramitochondrial ATP/ADP ratios in rat liver mitochondria. Biochim Biophys Acta 590: 285-289, 1980. doi:10.1016/0005-2728(80)90199-1
7. Coppey L, Davidson E, Lu B, Gerard C, Yorek M. Vasopeptidase inhibitor ilepatril (AVE7688) prevents obesityand diabetesinduced neuropathy in C57Bl/6J mice. Neuropharmacology 60: 259-266, 2011. doi: 10.1016/j.neuropharm.2010.09.008
8. D’Souza DM, Al-Sajee D, Hawke TJ. Diabetic myopathy: impact of diabetes mellitus on skeletal muscle progenitor cells. Front Physiol 4: 379, 2013. doi:10.3389/fphys.2013.00379
9. Davis EJ, Davis-van Thienen WI. Control of mitochondrial metabolism by the ATP/ADP ratio. Biochem Biophys Res Commun 83: 1260-1266, 1978. doi:10.1016/0006-291X(78)91357-8
10. Davis EJ, Davis-Van Thienen WI. Rate control of phosphorylationcoupled respiration by rat liver mitochondria. Arch Biochem Biophys 233: 573-581, 1984. doi:10.1016/0003-9861(84)90481-8
11. Davis EJ, Lumeng L, Bottoms D. On the relationships between the stoichiometry of oxidative phosphorylation and the phosphorylation potential of rat liver mitochondria as functions of respiratory state. FEBS Lett 39: 9-12, 1974. doi:10.1016/0014-5793(74)80004-9
12. Delaglio F, Grzesiek S, Vuister GW, Zhu G, Pfeifer J, Bax A. NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J Biomol NMR 6: 277-293, 1995. doi:10.1007/BF00197809
13. Fink BD, Herlein JA, Almind K, Cinti S, Kahn CR, Sivitz WI. Mitochondrial proton leak in obesity-resistant and obesity-prone mice. Am J Physiol Regul Integr Comp Physiol 293: R1773-R1780, 2007. doi: 10.1152/ajpregu.00478.2007
14. Fink BD, Hong YS, Mathahs MM, Scholz TD, Dillon JS, Sivitz WI. UCP2-dependent proton leak in isolated mammalian mitochondria. J Biol Chem 277: 3918-3925, 2002. doi:10.1074/jbc.M107955200
15. Gnaiger E. Real-time OXPHOS analysis. In: Mitochondrial Pathways and Respiratory Control: An Introduction ot OXPHOS Analysis. Innsbruck, Austria: Oroboros MiNet Publications, 2014, p. 7-18
16. Heden TD, Neufer PD, Funai K. Looking beyond structure: membrane phospholipids of skeletal muscle mitochondria. Trends Endocrinol Metab 27: 553-562, 2016. doi:10.1016/j.tem.2016.05.007
17. Hernández-Ochoa EO, Vanegas C. Diabetic myopathy and mechanisms of disease. Biochem Pharmacol (Los Angel) 4: e179, 2015
18. Højlund K, Wrzesinski K, Larsen PM, Fey SJ, Roepstorff P, Handberg A, Dela F, Vinten J, McCormack JG, Reynet C, Beck-Nielsen H. Proteome analysis reveals phosphorylation of ATP synthase -subunit in human skeletal muscle and proteins with potential roles in type 2 diabetes. J Biol Chem 278: 10436-10442, 2003. doi:10.1074/jbc.M212881200
19. Johnson BA, Blevins RA. NMR View: A computer program for the visualization and analysis of NMR data. J Biomol NMR 4: 603-614, 1994. doi:10.1007/BF00404272
20. Kelley DE, He J, Menshikova EV, Ritov VB. Dysfunction of mitochondria in human skeletal muscle in type 2 diabetes. Diabetes 51: 2944-2950, 2002. doi:10.2337/diabetes.51.10.2944
21. Klein OL, Krishnan JA, Glick S, Smith LJ. Systematic review of the association between lung function and Type 2 diabetes mellitus. Diabet Med 27: 977-987, 2010. doi:10.1111/j.1464-5491.2010.03073.x
22. Küster U, Bohnensack R, Kunz W. Control of oxidative phosphorylation by the extra-mitochondrial ATP/ADP ratio. Biochim Biophys Acta 440: 391-402, 1976. doi:10.1016/0005-2728(76)90073-6
23. Lambert AJ, Brand MD. Inhibitors of the quinone-binding site allow rapid superoxide production from mitochondrial NADH:ubiquinone oxidoreductase (complex I). J Biol Chem 279: 39414-39420, 2004. doi: 10.1074/jbc.M406576200
24. O’Malley Y, Fink BD, Ross NC, Prisinzano TE, Sivitz WI. Reactive oxygen and targeted antioxidant administration in endothelial cell mitochondria. J Biol Chem 281: 39766-39775, 2006. doi:10.1074/jbc.M608268200
25. Phielix E, Schrauwen-Hinderling VB, Mensink M, Lenaers E, Meex R, Hoeks J, Kooi ME, Moonen-Kornips E, Sels JP, Hesselink MK, Schrauwen P. Lower intrinsic ADP-stimulated mitochondrial respiration underlies in vivo mitochondrial dysfunction in muscle of male type 2 diabetic patients. Diabetes 57: 2943-2949, 2008. doi:10.2337/db08-0391
26. Rhee SG, Chang TS, Jeong W, Kang D. Methods for detection and measurement of hydrogen peroxide inside and outside of cells. Mol Cells 29: 539-549, 2010. doi:10.1007/s10059-010-0082-3
27. Vazquez EJ, Berthiaume JM, Kamath V, Achike O, Buchanan E, Montano MM, Chandler MP, Miyagi M, Rosca MG. Mitochondrial complex I defect and increased fatty acid oxidation enhance protein lysine acetylation in the diabetic heart. Cardiovasc Res 107: 453-465, 2015. doi:10.1093/cvr/cvv183
28. Vojtková J, Ciljaková M, Michnová Z, Tur an T. Chronic complications of diabetes mellitus related to the respiratory system. Pediatr Endocrinol Diabetes Metab 18: 112-115, 2012
29. Walter P, Stucki JW. Regulation of pyruvate carboxylase in rat liver mitochondria by adenine nucleotides and short chain fatty acids. Eur J Biochem 12: 508-519, 1970. doi:10.1111/j.1432-1033.1970.tb00880.x
30. Wanders RJ, Groen AK, Van Roermund CW, Tager JM. Factors determining the relative contribution of the adenine-nucleotide translocator and the ADP-regenerating system to the control of oxidative phosphorylation in isolated ratliver mitochondria. Eur J Biochem 142: 417-424, 1984. doi:10.1111/j.1432-1033.1984.tb08303.x
31. Watson PM, Commins SP, Beiler RJ, Hatcher HC, Gettys TW. Differential regulation of leptin expression and function in A/J vs. C57BL/6J mice during diet-induced obesity. Am J Physiol Endocrinol Metab 279: E356-E365, 2000
32. Wojtczak L, Wojtczak AB, Ernster L. The inhibition of succinate dehydrogenase by oxalacetate. Biochim Biophys Acta 191: 10-21, 1969. doi:10.1016/0005-2744(69)90310-6
33. Wojtczak L, Zaluska H, Wroniszewska A, Wojtczak AB. Assay for the intactness of the outer membrane in isolated mitochondria. Acta Biochim Pol 19: 227-234, 1972
34. Yu L, Fink BD, Herlein JA, Oltman CL, Lamping KG, Sivitz WI. Dietary fat, fatty acid saturation and mitochondrial bioenergetics. J Bioenerg Biomembr46: 33-44, 2014
35. Yu L, Fink BD, Herlein JA, Sivitz WI. Mitochondrial function in diabetes: novel methodology and new insight. Diabetes 62: 1833-1842, 2013. doi:10.2337/db12-1152
36. Yu L, Fink BD, Sivitz WI. Simultaneous quantification of mitochondrial ATP and ROS production. Methods Mol Biol 1264: 149-159, 2015. doi:10.1007/978-1-4939-2257-4_14
37. Zeylemaker WP, Klaasse AD, Slater EC. Studies on succinate dehydrogenase. V. Inhibition by oxaloacetate. Biochim Biophys Acta 191: 229-238, 1969. doi:10.1016/0005-2744(69)90242-3