Mitochondria in the pathogenesis of diabetes: A proteomic view

Protein and Cell

Volumn 3, Issue 9, 2012, Pages 648-660

  Chen, Xiulan ^a   Wei, Shasha ^a,b   Yang, Fuquan ^a  

^a INSTITUTE OF BIOPHYSICS   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

diabetes complication; mitochondria proteomics; T1DM; T2DM

Indexed keywords

MITOCHONDRIAL PROTEIN; ROSIGLITAZONE;

ADIPOSE TISSUE; DIABETES MELLITUS; DIABETIC CARDIOMYOPATHY; DIABETIC NEPHROPATHY; DIABETIC NEUROPATHY; DIABETIC RETINOPATHY; DIABETOGENESIS; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DRUG RECEPTOR BINDING; GEL ELECTROPHORESIS; GLUCOSE HOMEOSTASIS; HUMAN; INSULIN DEPENDENT DIABETES MELLITUS; INSULIN RELEASE; LIVER; MASS SPECTROMETRY; MITOCHONDRION; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PROCESSING; PROTEOMICS; REVIEW; SKELETAL MUSCLE;

EID: 84866165313     PISSN: 1674800X     EISSN: 16748018     Source Type: Journal    
DOI: 10.1007/s13238-012-2043-4     Document Type: Review

References (103)

1. Akude, E., Zherebitskaya, E., Chowdhury, S. K., Smith, D. R., Dobrowsky, R. T., and Fernyhough, P. (2011). Diminished superoxide generation is associated with respiratory chain dysfunction and changes in the mitochondrial proteome of sensory neurons from diabetic rats. Diabetes 60, 288-297.
2. Anello, M., Lupi, R., Spampinato, D., Piro, S., Masini, M., Boggi, U., Del Prato, S., Rabuazzo, A. M., Purrello, F., and Marchetti, P. (2005). Functional and morphological alterations of mitochondria in pancreatic beta cells from type 2 diabetic patients. Diabetologia 48, 282-289.
3. Bantscheff, M., Schirle, M., Sweetman, G., Rick, J., and Kuster, B. (2007). Quantitative mass spectrometry in proteomics: a critical review. Anal Bioanal Chem 389, 1017-1031.
4. Baseler, W. A., Dabkowski, E. R., Williamson, C. L., Croston, T. L., Thapa, D., Powell, M. J., Razunguzwa, T. T., and Hollander, J. M. (2010). Proteomic alterations of distinct mitochondrial subpopulations in the type 1 diabetic heart: contribution of protein import dysfunction. Am J Physiol Regul Integr Comp Physiol 300, R186-200.
5. Befroy, D. E., Petersen, K. F., Dufour, S., Mason, G. F., de Graaf, R. A., Rothman, D. L., and Shulman, G. I. (2007). Impaired mitochondrial substrate oxidation in muscle of insulin-resistant offspring of type 2 diabetic patients. Diabetes 56, 1376-1381.
6. Bindokas, V. P., Kuznetsov, A., Sreenan, S., Polonsky, K. S., Roe, M. W., and Philipson, L. H. (2003). Visualizing superoxide production in normal and diabetic rat islets of Langerhans. J Biol Chem 278, 9796-9801.
7. Boudina, S., Sena, S., Theobald, H., Sheng, X., Wright, J. J., Hu, X. X., Aziz, S., Johnson, J. I., Bugger, H., Zaha, V. G., et al. (2007). Mitochondrial energetics in the heart in obesity-related diabetes: direct evidence for increased uncoupled respiration and activation of uncoupling proteins. Diabetes 56, 2457-2466.
8. Boushel, R., Gnaiger, E., Schjerling, P., Skovbro, M., Kraunsoe, R., and Dela, F. (2007). Patients with type 2 diabetes have normal mitochondrial function in skeletal muscle. Diabetologia 50, 790-796.
9. Brownlee, M. (2005). The pathobiology of diabetic complications: a unifying mechanism. Diabetes 54, 1615-1625.
10. Bugger, H., and Abel, E. D. (2010). Mitochondria in the diabetic heart. Cardiovasc Res 88, 229-240.
11. Bugger, H., Boudina, S., Hu, X. X., Tuinei, J., Zaha, V. G., Theobald, H. A., Yun, U. J., McQueen, A. P., Wayment, B., Litwin, S. E., et al. (2008). Type 1 diabetic akita mouse hearts are insulin sensitive but manifest structurally abnormal mitochondria that remain coupled despite increased uncoupling protein 3. Diabetes 57, 2924-2932.
12. Bugger, H., Chen, D., Riehle, C., Soto, J., Theobald, H. A., Hu, X. X., Ganesan, B., Weimer, B. C., and Abel, E. D. (2009). Tissue-specific remodeling of the mitochondrial proteome in type 1 diabetic akita mice. Diabetes 58, 1986-1997.
13. Chan, D. C. (2006). Mitochondria: dynamic organelles in disease, aging, and development. Cell 125, 1241-1252.
14. Chomentowski, P., Coen, P. M., Radikova, Z., Goodpaster, B. H., and Toledo, F. G. (2011). Skeletal muscle mitochondria in insulin resistance: differences in intermyofibrillar versus subsarcolemmal subpopulations and relationship to metabolic flexibility. J Clin Endocrinol Metab 96, 494-503.
15. Choo, H. J., Kim, J. H., Kwon, O. B., Lee, C. S., Mun, J. Y., Han, S. S., Yoon, Y. S., Yoon, G., Choi, K. M., and Ko, Y. G. (2006). Mitochondria are impaired in the adipocytes of type 2 diabetic mice. Diabetologia 49, 784-791.
16. Chowdhury, S. K., Smith, D. R., and Fernyhough, P. (2012). The role of aberrant mitochondrial bioenergetics in diabetic neuropathy. Neurobiol Dis (In Press).
17. Cui, Z., Hou, J., Chen, X., Li, J., Xie, Z., Xue, P., Cai, T., Wu, P., Xu, T., and Yang, F. (2010). The profile of mitochondrial proteins and their phosphorylation signaling network in INS-1 beta cells. J Proteome Res 9, 2898-2908.
18. D'Hertog, W., Mathieu, C., and Overbergh, L. (2006). Type 1 diabetes: entering the proteomic era. Expert Rev Proteomics 3, 223-236.
19. Dabkowski, E. R., Baseler, W. A., Williamson, C. L., Powell, M., Razunguzwa, T. T., Frisbee, J. C., and Hollander, J. M. (2010). Mitochondrial dysfunction in the type 2 diabetic heart is associated with alterations in spatially distinct mitochondrial proteomes. Am J Physiol Heart Circ Physiol 299, H529-540.
20. Dabkowski, E. R., Williamson, C. L., Bukowski, V. C., Chapman, R. S., Leonard, S. S., Peer, C. J., Callery, P. S., and Hollander, J. M. (2009). Diabetic cardiomyopathy-associated dysfunction in spatially distinct mitochondrial subpopulations. Am J Physiol Heart Circ Physiol 296, H359-369.
21. Deng, W. J., Nie, S., Dai, J., Wu, J. R., and Zeng, R. (2010). Proteome, phosphoproteome and hydroxyproteome of liver mitochondria in diabetic rats at early pathogenic stages. Mol Cell Proteomics 9, 110-116.
22. Duchen, M. R. (2004). Mitochondria in health and disease: perspectives on a new mitochondrial biology. Mol Aspects Med 25, 365-451.
23. Eyrich, B., Sickmann, A., and Zahedi, R. P. (2011). Catch me if you can: mass spectrometry-based phosphoproteomics and quantification strategies. Proteomics 11, 554-570.
24. Fernyhough, P., Roy Chowdhury, S. K., and Schmidt, R. E. (2010). Mitochondrial stress and the pathogenesis of diabetic neuropathy. Expert Rev Endocrinol Metab 5, 39-49.
25. Forbes, J. M., Coughlan, M. T., and Cooper, M. E. (2008). Oxidative stress as a major culprit in kidney disease in diabetes. Diabetes 57, 1446-1454.
26. Graier, W. F., Malli, R., and Kostner, G. M. (2009). Mitochondrial protein phosphorylation: instigator or target of lipotoxicity? Trends Endocrinol Metab 20, 186-193.
27. Greenacre, S. A., and Ischiropoulos, H. (2001). Tyrosine nitration: localisation, quantification, consequences for protein function and signal transduction. Free Radic Res 34, 541-581.
28. Gregersen, N., Hansen, J., and Palmfeldt, J. (2012). Mitochondrial proteomics-a tool for the study of metabolic disorders. J Inherit Metab Dis.
29. Guilherme, A., Virbasius, J. V., Puri, V., and Czech, M. P. (2008). Adipocyte dysfunctions linking obesity to insulin resistance and type 2 diabetes. Nat Rev Mol Cell Biol 9, 367-377.
30. Hojlund, K., Wrzesinski, K., Larsen, P. M., Fey, S. J., Roepstorff, P., Handberg, A., Dela, F., Vinten, J., McCormack, J. G., Reynet, C., et al. (2003). Proteome analysis reveals phosphorylation of ATP synthase beta-subunit in human skeletal muscle and proteins with potential roles in type 2 diabetes. J Biol Chem 278, 10436-10442.
31. Hood, D. A. (2001). Invited Review: contractile activity-induced mitochondrial biogenesis in skeletal muscle. J Appl Physiol 90, 1137-1157.
32. Hu, Y., Suarez, J., Fricovsky, E., Wang, H., Scott, B. T., Trauger, S. A., Han, W., Oyeleye, M. O., and Dillmann, W. H. (2009). Increased enzymatic O-GlcNAcylation of mitochondrial proteins impairs mitochondrial function in cardiac myocytes exposed to high glucose. J Biol Chem 284, 547-555.
33. Kanwar, M., Chan, P. S., Kern, T. S., and Kowluru, R. A. (2007). Oxidative damage in the retinal mitochondria of diabetic mice: possible protection by superoxide dismutase. Invest Ophthalmol Vis Sci 48, 3805-3811.
34. Kartha, G. K., Moshal, K. S., Sen, U., Joshua, I. G., Tyagi, N., Steed, M. M., and Tyagi, S. C. (2008). Renal mitochondrial damage and protein modification in type-2 diabetes. Acta Diabetol 45, 75-81.
35. Kelley, D. E., He, J., Menshikova, E. V., and Ritov, V. B. (2002). Dysfunction of mitochondria in human skeletal muscle in type 2 diabetes. Diabetes 51, 2944-2950.
36. Kim, J. A., Wei, Y., and Sowers, J. R. (2008). Role of mitochondrial dysfunction in insulin resistance. Circ Res 102, 401-414.
37. Kotronen, A., Seppala-Lindroos, A., Bergholm, R., and Yki-Jarvinen, H. (2008). Tissue specificity of insulin resistance in humans: fat in the liver rather than muscle is associated with features of the metabolic syndrome. Diabetologia 51, 130-138.
38. Lamson, D. W., and Plaza, S. M. (2002). Mitochondrial factors in the pathogenesis of diabetes: a hypothesis for treatment. Altern Med Rev 7, 94-111.
39. Leinninger, G. M., Backus, C., Sastry, A. M., Yi, Y. B., Wang, C. W., and Feldman, E. L. (2006a). Mitochondria in DRG neurons undergo hyperglycemic mediated injury through Bim, Bax and the fission protein Drp1. Neurobiol Dis 23, 11-22.
40. Leinninger, G. M., Edwards, J. L., Lipshaw, M. J., and Feldman, E. L. (2006b). Mechanisms of disease: mitochondria as new therapeutic targets in diabetic neuropathy. Nat Clin Pract Neurol 2, 620-628.
41. Lesnefsky, E. J., Slabe, T. J., Stoll, M. S., Minkler, P. E., and Hoppel, C. L. (2001). Myocardial ischemia selectively depletes cardiolipin in rabbit heart subsarcolemmal mitochondria. Am J Physiol Heart Circ Physiol 280, H2770-2778.
42. Lewis, E. J., and Lewis, J. B. (2003). Treatment of diabetic nephropathy with angiotensin II receptor antagonist. Clin Exp Nephrol 7, 1-8.
43. Li, J., Cai, T., Wu, P., Cui, Z., Chen, X., Hou, J., Xie, Z., Xue, P., Shi, L., Liu, P., et al. (2009). Proteomic analysis of mitochondria from Caenorhabditis elegans. Proteomics 9, 4539-4553.
44. Lieber, C. S., Leo, M. A., Mak, K. M., Xu, Y., Cao, Q., Ren, C., Ponomarenko, A., and DeCarli, L. M. (2004). Model of nonalcoholic steatohepatitis. Am J Clin Nutr 79, 502-509.
45. Lopez-Sanchez, L. M., Lopez-Pedrera, C., and Rodriguez-Ariza, A. (2012). Proteomics insights into deregulated protein S-nitrosylation and disease. Expert Rev Proteomics 9, 59-69.
46. Lowell, B. B., and Shulman, G. I. (2005). Mitochondrial dysfunction and type 2 diabetes. Science 307, 384-387.
47. Madsen-Bouterse, S. A., and Kowluru, R. A. (2008). Oxidative stress and diabetic retinopathy: pathophysiological mechanisms and treatment perspectives. Rev Endocr Metab Disord 9, 315-327.
48. Maechler, P., Carobbio, S., and Rubi, B. (2006). In beta-cells, mitochondria integrate and generate metabolic signals controlling insulin secretion. Int J Biochem Cell Biol 38, 696-709.
49. Maechler, P., Li, N., Casimir, M., Vetterli, L., Frigerio, F., and Brun, T. (2010). Role of mitochondria in beta-cell function and dysfunction. Adv Exp Med Biol 654, 193-216.
50. Maechler, P., and Wollheim, C. B. (2001). Mitochondrial function in normal and diabetic beta-cells. Nature 414, 807-812.
51. Mariappan, N., Elks, C. M., Sriramula, S., Guggilam, A., Liu, Z., Borkhsenious, O., and Francis, J. (2009). NF-kappaB-induced oxidative stress contributes to mitochondrial and cardiac dysfunction in type II diabetes. Cardiovasc Res 85, 473-483.
52. Mogensen, M., Sahlin, K., Fernstrom, M., Glintborg, D., Vind, B. F., Beck-Nielsen, H., and Hojlund, K. (2007). Mitochondrial respiration is decreased in skeletal muscle of patients with type 2 diabetes. Diabetes 56, 1592-1599.
53. Mollica, M. P., Lionetti, L., Crescenzo, R., D'Andrea, E., Ferraro, M., Liverini, G., and Iossa, S. (2006). Heterogeneous bioenergetic behaviour of subsarcolemmal and intermyofibrillar mitochondria in fed and fasted rats. Cell Mol Life Sci 63, 358-366.
54. Mootha, V. K., Lindgren, C. M., Eriksson, K. F., Subramanian, A., Sihag, S., Lehar, J., Puigserver, P., Carlsson, E., Ridderstrale, M., Laurila, E., et al. (2003). PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat Genet 34, 267-273.
55. Moreira, P. I., and Oliveira, C. R. (2011). Mitochondria as potential targets in antidiabetic therapy. Handb Exp Pharmacol, 331-356.
56. Moreira, P. I., Santos, M. S., Sena, C., Nunes, E., Seica, R., and Oliveira, C. R. (2005a). CoQ10 therapy attenuates amyloid beta-peptide toxicity in brain mitochondria isolated from aged diabetic rats. Exp Neurol 196, 112-119.
57. Moreira, P. I., Santos, M. S., Sena, C., Seica, R., and Oliveira, C. R. (2005b). Insulin protects against amyloid beta-peptide toxicity in brain mitochondria of diabetic rats. Neurobiol Dis 18, 628-637.
58. Morino, K., Petersen, K. F., Dufour, S., Befroy, D., Frattini, J., Shatzkes, N., Neschen, S., White, M. F., Bilz, S., Sono, S., et al. (2005). Reduced mitochondrial density and increased IRS-1 serine phosphorylation in muscle of insulin-resistant offspring of type 2 diabetic parents. J Clin Invest 115, 3587-3593.
59. Munusamy, S., Saba, H., Mitchell, T., Megyesi, J. K., Brock, R. W., and Macmillan-Crow, L. A. (2009). Alteration of renal respiratory Complex-III during experimental type-1 diabetes. BMC Endocr Disord 9, 2.
60. Nishikawa, T., and Araki, E. (2007). Impact of mitochondrial ROS production in the pathogenesis of diabetes mellitus and its complications. Antioxid Redox Signal 9, 343-353.
61. Nishikawa, T., Edelstein, D., Du, X. L., Yamagishi, S., Matsumura, T., Kaneda, Y., Yorek, M. A., Beebe, D., Oates, P. J., Hammes, H. P., et al. (2000). Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage. Nature 404, 787-790.
62. Ong, S. E., Blagoev, B., Kratchmarova, I., Kristensen, D. B., Steen, H., Pandey, A., and Mann, M. (2002). Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol Cell Proteomics 1, 376-386.
63. Pagliarini, D. J., Calvo, S. E., Chang, B., Sheth, S. A., Vafai, S. B., Ong, S. E., Walford, G. A., Sugiana, C., Boneh, A., Chen, W. K., et al. (2008). A mitochondrial protein compendium elucidates complex I disease biology. Cell 134, 112-123.
64. Pagliarini, D. J., and Dixon, J. E. (2006). Mitochondrial modulation: reversible phosphorylation takes center stage? Trends Biochem Sci 31, 26-34.
65. Pan, S., Chen, R., Aebersold, R., and Brentnall, T. A. (2010). Mass spectrometry based glycoproteomics-from a proteomics perspective. Mol Cell Proteomics 10, R110003251.
66. Patti, M. E., Butte, A. J., Crunkhorn, S., Cusi, K., Berria, R., Kashyap, S., Miyazaki, Y., Kohane, I., Costello, M., Saccone, R., et al. (2003). Coordinated reduction of genes of oxidative metabolism in humans with insulin resistance and diabetes: Potential role of PGC1 and NRF1. Proc Natl Acad Sci U S A 100, 8466-8471.
67. Patti, M. E., and Corvera, S. (2010). The role of mitochondria in the pathogenesis of type 2 diabetes. Endocr Rev 31, 364-395.
68. Patton, W. F. (2000). A thousand points of light: the application of fluorescence detection technologies to two-dimensional gel electrophoresis and proteomics. Electrophoresis 21, 1123-1144.
69. Petersen, K. F., Dufour, S., Befroy, D., Garcia, R., and Shulman, G. I. (2004). Impaired mitochondrial activity in the insulin-resistant offspring of patients with type 2 diabetes. N Engl J Med 350, 664-671.
70. Phillips, C. A., and Molitch, M. E. (2002). The relationship between glucose control and the development and progression of diabetic nephropathy. Curr Diab Rep 2, 523-529.
71. Rabilloud, T., Chevallet, M., Luche, S., and Lelong, C. (2010). Two-dimensional gel electrophoresis in proteomics: Past, present and future. J Proteomics 73, 2064-2077.
72. Rezaul, K., Wu, L., Mayya, V., Hwang, S. I., and Han, D. (2005). A systematic characterization of mitochondrial proteome from human T leukemia cells. Mol Cell Proteomics 4, 169-181.
73. Ritov, V. B., Menshikova, E. V., He, J., Ferrell, R. E., Goodpaster, B. H., and Kelley, D. E. (2005). Deficiency of subsarcolemmal mitochondria in obesity and type 2 diabetes. Diabetes 54, 8-14.
74. Rosen, E. D., and Spiegelman, B. M. (2006). Adipocytes as regulators of energy balance and glucose homeostasis. Nature 444, 847-853.
75. Ross, P. L., Huang, Y. N., Marchese, J. N., Williamson, B., Parker, K., Hattan, S., Khainovski, N., Pillai, S., Dey, S., Daniels, S., et al. (2004). Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents. Mol Cell Proteomics 3, 1154-1169.
76. Ruiz-Romero, C., and Blanco, F. J. (2009). Mitochondrial proteomics and its application in biomedical research. Mol Biosyst 5, 1130-1142.
77. Santos, J. M., Mohammad, G., Zhong, Q., and Kowluru, R. A. (2010). Diabetic retinopathy, superoxide damage and antioxidants. Curr Pharm Biotechnol 12, 352-361.
78. Santos, J. M., Tewari, S., Goldberg, A. F., and Kowluru, R. A. (2011). Mitochondrial biogenesis and the development of diabetic retinopathy. Free Radic Biol Med 51, 1849-1860.
79. Satapati, S., He, T., Inagaki, T., Potthoff, M., Merritt, M. E., Esser, V., Mangelsdorf, D. J., Kliewer, S. A., Browning, J. D., and Burgess, S. C. (2008). Partial resistance to peroxisome proliferator-activated receptor-alpha agonists in ZDF rats is associated with defective hepatic mitochondrial metabolism. Diabetes 57, 2012-2021.
80. Schmeichel, A. M., Schmelzer, J. D., and Low, P. A. (2003). Oxidative injury and apoptosis of dorsal root ganglion neurons in chronic experimental diabetic neuropathy. Diabetes 52, 165-171.
81. Shen, X., Zheng, S., Thongboonkerd, V., Xu, M., Pierce, W. M., Jr., Klein, J. B., and Epstein, P. N. (2004). Cardiac mitochondrial damage and biogenesis in a chronic model of type 1 diabetes. Am J Physiol Endocrinol Metab 287, E896-905.
82. Sivitz, W. I., and Yorek, M. A. (2009). Mitochondrial dysfunction in diabetes: from molecular mechanisms to functional significance and therapeutic opportunities. Antioxid Redox Signal 12, 537-577.
83. Sparre, T., Larsen, M. R., Heding, P. E., Karlsen, A. E., Jensen, O. N., and Pociot, F. (2005). Unraveling the pathogenesis of type 1 diabetes with proteomics: present and future directions. Mol Cell Proteomics 4, 441-457.
84. Suh, J. H., Heath, S. H., and Hagen, T. M. (2003). Two subpopulations of mitochondria in the aging rat heart display heterogenous levels of oxidative stress. Free Radic Biol Med 35, 1064-1072.
85. Suzuki, Y., Atsumi, Y., Matsuoka, K., Nishimaki, K., Ohta, S., Taniyama, M., and Muramatsu, T. (2005). Mitochondrial tRNA(Leu(UUR)) mutation at position 3243 detected in patients with type 1 diabetes. Diabetes Res Clin Pract 67, 92-94.
86. Taylor, S. W., Fahy, E., Zhang, B., Glenn, G. M., Warnock, D. E., Wiley, S., Murphy, A. N., Gaucher, S. P., Capaldi, R. A., Gibson, B. W., et al. (2003). Characterization of the human heart mitochondrial proteome. Nat Biotechnol 21, 281-286.
87. Tewari, S., Santos, J. M., and Kowluru, R. A. (2012). Damaged mitochondrial DNA replication system and the development of diabetic retinopathy. Antioxid Redox Signal 17, 492-504.
88. Thomson, M. (2002). Evidence of undiscovered cell regulatory mechanisms: phosphoproteins and protein kinases in mitochondria. Cell Mol Life Sci 59, 213-219.
89. Trudeau, K., Molina, A. J., Guo, W., and Roy, S. (2010). High glucose disrupts mitochondrial morphology in retinal endothelial cells: implications for diabetic retinopathy. Am J Pathol 177, 447-455.
90. Turko, I. V., Li, L., Aulak, K. S., Stuehr, D. J., Chang, J. Y., and Murad, F. (2003). Protein tyrosine nitration in the mitochondria from diabetic mouse heart. Implications to dysfunctional mitochondria in diabetes. J Biol Chem 278, 33972-33977.
91. Turko, I. V., and Murad, F. (2003). Quantitative protein profiling in heart mitochondria from diabetic rats. J Biol Chem 278, 35844-35849.
92. Turner, N., and Heilbronn, L. K. (2008). Is mitochondrial dysfunction a cause of insulin resistance? Trends Endocrinol Metab 19, 324-330.
93. Verkhratsky, A., and Fernyhough, P. (2008). Mitochondrial malfunction and Ca2+ dyshomeostasis drive neuronal pathology in diabetes. Cell Calcium 44, 112-122.
94. Vial, G., Dubouchaud, H., Couturier, K., Cottet-Rousselle, C., Taleux, N., Athias, A., Galinier, A., Casteilla, L., and Leverve, X. M. (2010). Effects of a high-fat diet on energy metabolism and ROS production in rat liver. J Hepatol 54, 348-356.
95. Wallace, D. C. (1999). Mitochondrial diseases in man and mouse. Science 283, 1482-1488.
96. Wang, Y., Peng, F., Tong, W., Sun, H., Xu, N., and Liu, S. (2010). The nitrated proteome in heart mitochondria of the db/db mouse model: characterization of nitrated tyrosine residues in SCOT. J Proteome Res 9, 4254-4263.
97. Whiting, D. R., Guariguata, L., Weil, C., and Shaw, J. (2011). IDF diabetes atlas: global estimates of the prevalence of diabetes for 2011 and 2030. Diabetes Res Clin Pract 94, 311-321.
98. Wiederkehr, A., and Wollheim, C. B. (2006). Minireview: implication of mitochondria in insulin secretion and action. Endocrinology 147, 2643-2649.
99. Wilson-Fritch, L., Nicoloro, S., Chouinard, M., Lazar, M. A., Chui, P. C., Leszyk, J., Straubhaar, J., Czech, M. P., and Corvera, S. (2004). Mitochondrial remodeling in adipose tissue associated with obesity and treatment with rosiglitazone. J Clin Invest 114, 1281-1289.
100. Yu, T., Sheu, S. S., Robotham, J. L., and Yoon, Y. (2008). Mitochondrial fission mediates high glucose-induced cell death through elevated production of reactive oxygen species. Cardiovasc Res 79, 341-351.
101. Zhu, W., Smith, J. W., and Huang, C. M. (2010). Mass spectrometry-based label-free quantitative proteomics. J Biomed Biotechnol 2010, 840518.
102. Zimmet, P., Alberti, K. G., and Shaw, J. (2001). Global and societal implications of the diabetes epidemic. Nature 414, 782-787.
103. Zischka, H., Weber, G., Weber, P. J., Posch, A., Braun, R. J., Buhringer, D., Schneider, U., Nissum, M., Meitinger, T., Ueffing, M., et al. (2003). Improved proteome analysis of Saccharomyces cerevisiae mitochondria by free-flow electrophoresis. Proteomics 3, 906-916.