Proteomic alterations of distinct mitochondrial subpopulations in the type 1 diabetic heart: Contribution of protein import dysfunction

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 300, Issue 2, 2011, Pages

  Baseler, Walter A ^a,b   Dabkowski, Erinne R ^a,b   Williamson, Courtney L ^a,b   Croston, Tara L ^a,b   Thapa, Dharendra ^a,b   Powell, Matthew J ^c   Razunguzwa, Trust T ^c   Hollander, John M ^a,b  

^a WEST VIRGINIA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Center for Cardiovascular and Respiratory Sciences   (United States)

^c Protea Biosciences   (United States)

Author keywords

Diabetes; Mitochondria

Indexed keywords

ADENINE NUCLEOTIDE TRANSLOCASE; CARRIER PROTEIN; HEAT SHOCK PROTEIN 70; MESSENGER RNA; MITOCHONDRIAL PROTEIN; PHOSPHATE; STRUCTURAL PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CITRIC ACID CYCLE; DEAMINATION; DIABETIC CARDIOMYOPATHY; FATTY ACID OXIDATION; INSULIN DEPENDENT DIABETES MELLITUS; INTERFIBRILLAR MITOCHONDRIA; MALE; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN PROCESSING; PROTEOMICS; RESPIRATORY CHAIN; SUBSARCOLEMMAL MITOCHONDRIA;

3-HYDROXYACYL COA DEHYDROGENASES; ACETYL-COA C-ACYLTRANSFERASE; ANIMALS; BLOOD GLUCOSE; CARBON-CARBON DOUBLE BOND ISOMERASES; CARRIER PROTEINS; CITRIC ACID CYCLE; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 1; DIABETIC CARDIOMYOPATHIES; DOWN-REGULATION; ELECTRON TRANSPORT CHAIN COMPLEX PROTEINS; ENOYL-COA HYDRATASE; GENE EXPRESSION; HEART; HSP70 HEAT-SHOCK PROTEINS; INSULIN; MALE; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MICE, INBRED STRAINS; MITOCHONDRIA, HEART; MITOCHONDRIAL PROTEINS; MUSCLE PROTEINS; MYOCARDIUM; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TRANSPORT; PROTEOME; PROTEOMICS; RACEMASES AND EPIMERASES; RECOMBINANT FUSION PROTEINS; UP-REGULATION;

EID: 79551545013     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00423.2010     Document Type: Article

References (43)

1. Artal-Sanz M, Tavernarakis N. Prohibitin and mitochondrial biology. Trends Endocrinol Metab 20: 394-401, 2009.
2. Baynes JW. Role of oxidative stress in development of complications in diabetes. Diabetes 40: 405-412, 1991.
3. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254, 1976.
4. Bugger H, Boudina S, Hu XX, Tuinei J, Zaha VG, Theobald HA, Yun UJ, McQueen AP, Wayment B, Litwin SE, Abel ED. 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, 2008.
5. Bugger H, Chen D, Riehle C, Soto J, Theobald HA, Hu XX, Ganesan B, Weimer BC, Abel ED. Tissue-specific remodeling of the mitochondrial proteome in type 1 diabetic akita mice. Diabetes 58: 1986-1997, 2009.
6. Calvo S, Jain M, Xie X, Sheth SA, Chang B, Goldberger OA, Spinazzola A, Zeviani M, Carr SA, Mootha VK. Systematic identification of human mitochondrial disease genes through integrative genomics. Nat Genet 38: 576-582, 2006.
7. Chacinska A, Koehler CM, Milenkovic D, Lithgow T, Pfanner N. Importing mitochondrial proteins: machineries and mechanisms. Cell 138: 628-644, 2009.
8. Chacinska A, Rehling P, Guiard B, Frazier AE, Schulze-Specking A, Pfanner N, Voos W, Meisinger C. Mitochondrial translocation contact sites: separation of dynamic and stabilizing elements in formation of a TOM-TIM-preprotein supercomplex. EMBO J 22: 5370-5381, 2003. (Pubitemid 37279947)
9. Craig EE, Hood DA. Influence of aging on protein import into cardiac mitochondria. Am J Physiol Heart Circ Physiol 272: H2983-H2988, 1997.
10. Dabkowski ER, Baseler WA, Williamson CL, Powell M, Razunguzwa TT, Frisbee JC, Hollander JM. 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-H540, 2010.
11. Dabkowski ER, Williamson CL, Bukowski VC, Chapman RS, Leonard SS, Peer CJ, Callery PS, Hollander JM. Diabetic cardiomyopathy-associated dysfunction in spatially distinct mitochondrial subpopulations. Am J Physiol Heart Circ Physiol 296: H359-H369, 2009.
12. Dabkowski ER, Williamson CL, Hollander JM. Mitochondria-specific transgenic overexpression of phospholipid hydroperoxide glutathione peroxidase (GPx4) attenuates ischemia/reperfusion-associated cardiac dysfunction. Free Radic Biol Med 45: 855-865, 2008.
13. Flarsheim CE, Grupp IL, Matlib MA. Mitochondrial dysfunction accompanies diastolic dysfunction in diabetic rat heart. Am J Physiol Heart Circ Physiol 271: H192-H202, 1996.
14. Frazier AE, Chacinska A, Truscott KN, Guiard B, Pfanner N, Rehling P. Mitochondria use different mechanisms for transport of multispanning membrane proteins through the intermembrane space. Mol Cell Biol 23: 7818-7828, 2003. (Pubitemid 37271478)
15. Hamblin M, Friedman DB, Hill S, Caprioli RM, Smith HM, Hill MF. Alterations in the diabetic myocardial proteome coupled with increased myocardial oxidative stress underlies diabetic cardiomyopathy. J Mol Cell Cardiol 42: 884-895, 2007. (Pubitemid 46527591)
16. Huang JH, Joseph AM, Ljubicic V, Iqbal S, Hood DA. Effect of age on the processing and import of matrix-destined mitochondrial proteins in skeletal muscle. J Gerontol A Biol Sci Med Sci 65: 138-146, 2010.
17. Iwai K, Drake SK, Wehr NB, Weissman AM, LaVaute T, Minato N, Klausner RD, Levine RL, Rouault TA. Iron-dependent oxidation, ubiquitination, and degradation of iron regulatory protein 2: implications for degradation of oxidized proteins. Proc Natl Acad Sci USA 95: 4924-4928, 1998. (Pubitemid 28208526)
18. Jiang F, Ryan MT, Schlame M, Zhao M, Gu Z, Klingenberg M, Pfanner N, Greenberg ML. Absence of cardiolipin in the crd1 null mutant results in decreased mitochondrial membrane potential and reduced mitochondrial function. J Biol Chem 275: 22387-22394, 2000.
19. John GB, Shang Y, Li L, Renken C, Mannella CA, Selker JM, Rangell L, Bennett MJ, Zha J. The mitochondrial inner membrane protein mitofilin controls cristae morphology. Mol Biol Cell 16: 1543-1554, 2005.
20. Joshi AS, Zhou J, Gohil VM, Chen S, Greenberg ML. Cellular functions of cardiolipin in yeast. Biochim Biophys Acta 1793: 212-218, 2009.
21. Jüllig M, Hickey AJ, Middleditch MJ, Crossman DJ, Lee SC, Cooper GJS. Characterization of proteomic changes in cardiac mitochondria in streptozotocin-diabetic rats using iTRAQ™ isobaric tags. Proteomics Clin Appl 1: 565-576, 2007.
22. Kane LA, Van Eyk JE. Post-translational modifications of ATP synthase in the heart: biology and function. J Bioenerg Biomembr 41: 145-150, 2009.
23. Kelley DE, He J, Menshikova EV, Ritov VB. Dysfunction of mitochondria in human skeletal muscle in type 2 diabetes. Diabetes 51: 2944-2950, 2002.
24. King KL, Young ME, Kerner J, Huang H, O'Shea KM, Alexson SE, Hoppel CL, Stanley WC. Diabetes or peroxisome proliferator-activated receptor alpha agonist increases mitochondrial thioesterase I activity in heart. J Lipid Res 48: 1511-1517, 2007.
25. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685, 1970.
26. Lesnefsky EJ, Gudz TI, Moghaddas S, Migita CT, Ikeda-Saito M, Turkaly PJ, Hoppel CL. Aging decreases electron transport complex III activity in heart interfibrillar mitochondria by alteration of the cytochrome c binding site. J Mol Cell Cardiol 33: 37-47, 2001. (Pubitemid 32127782)
27. Lesnefsky EJ, Slabe TJ, Stoll MS, Minkler PE, Hoppel CL. Myocardial ischemia selectively depletes cardiolipin in rabbit heart subsarcolemmal mitochondria. Am J Physiol Heart Circ Physiol 280: H2770-H2778, 2001.
28. Lin D. Multidimensional protein identification technology as an effective tool for proteomics. Am Genom Proteom Technol 1: 38-46, 2001.
29. Matsuoka T, Wada J, Hashimoto I, Zhang Y, Eguchi J, Ogawa N, Shikata K, Kanwar YS, Makino H. Gene delivery of Tim44 reduces mitochondrial superoxide production and ameliorates neointimal proliferation of injured carotid artery in diabetic rats. Diabetes 54: 2882-2890, 2005.
30. Nishi H, Ono K, Iwanaga Y, Horie T, Nagao K, Takemura G, Kinoshita M, Kuwabara Y, Mori RT, Hasegawa K, Kita T, Kimura T. MicroRNA-15b modulates cellular ATP levels and degenerates mitochondria via Arl2 in neonatal rat cardiac myocytes. J Biol Chem 285: 4920-4930, 2010.
31. Palmer JW, Tandler B, Hoppel CL. Biochemical properties of subsarcolemmal and interfibrillar mitochondria isolated from rat cardiac muscle. J Biol Chem 252: 8731-8739, 1977. (Pubitemid 8243644)
32. Palmer JW, Tandler B, Hoppel CL. Heterogeneous response of subsarcolemmal heart mitochondria to calcium. Am J Physiol Heart Circ Physiol 250: H741-H748, 1986.
33. 2+ in mitochondrial dysfunction and disease. Cell Calcium 45: 643-650, 2009.
34. Robinson AB, Rudd CJ. Deamidation of glutaminyl and asparaginyl residues in peptides and proteins. Curr Top Cell Regul 8: 247-295, 1974.
35. Rolo AP, Palmeira CM. Diabetes and mitochondrial function: role of hyperglycemia and oxidative stress. Toxicol Appl Pharmacol 212: 167-178, 2006.
36. Rosca MG, Vazquez EJ, Kerner J, Parland W, Chandler MP, Stanley W, Sabbah HN, Hoppel CL. Cardiac mitochondria in heart failure: decrease in respirasomes and oxidative phosphorylation. Cardiovasc Res 80: 30-39, 2008.
37. Scharfe C, Lu HH, Neuenburg JK, Allen EA, Li GC, Klopstock T, Cowan TM, Enns GM, Davis RW. Mapping gene associations in human mitochondria using clinical disease phenotypes. PLoS Comput Biol 5: e1000374, 2009.
38. Shen X, Zheng S, Thongboonkerd V, Xu M, Pierce WM Jr, Klein JB, and Epstein PN. Cardiac mitochondrial damage and biogenesis in a chronic model of type 1 diabetes. Am J Physiol Endocrinol Metab 287: E896-E905, 2004. (Pubitemid 39382925)
39. Stojanovski D, Pfanner N, Wiedemann N. Import of proteins into mitochondria. Methods Cell Biol 80: 783-806, 2007.
40. Turko IV, Murad F. Quantitative protein profiling in heart mitochondria from diabetic rats. J Biol Chem 278: 35844-35849, 2003. (Pubitemid 37102363)
41. Weytjens C, Cosyns B, D'Hooge J, Droogmans S, Lahoutte T, Garbar C, Roossens B, Van Camp G. Evaluation of contractile function and inotropic reserve with tissue velocity, strain and strain rate imaging in streptozotocin-induced diabetes. Eur J Echocardiogr 11: 622-629, 2010.
42. Williamson CL, Dabkowski ER, Baseler WA, Croston TL, Alway SE, Hollander JM. Enhanced apoptotic propensity in diabetic cardiac mitochondria: influence of subcellular spatial location. Am J Physiol Heart Circ Physiol 298: H633-H642, 2010.
43. Zhang Y, Wada J, Hashimoto I, Eguchi J, Yasuhara A, Kanwar YS, Shikata K, Makino H. Therapeutic approach for diabetic nephropathy using gene delivery of translocase of inner mitochondrial membrane 44 by reducing mitochondrial superoxide production. J Am Soc Nephrol 17: 1090-1101, 2006.