Reversal of mitochondrial proteomic loss in type 1 diabetic heart with overexpression of phospholipid hydroperoxide glutathione peroxidase

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 304, Issue 7, 2013, Pages

  Baseler, Walter A ^a   Dabkowski, Erinne R ^a   Jagannathan, Rajaganapathi ^a   Thapa, Dharendra ^a   Nichols, Cody E ^a   Shepherd, Danielle L ^a   Croston, Tara L ^a   Powell, Matthew ^b   Razunguzwa, Trust T ^b   Lewis, Sara E ^a   Schnell, David M ^a   Hollander, John M ^a  

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

^b Protea Biosciences   (United States)

Author keywords

Diabetes mellitus; Heart; Mitochondria; Oxidative stress; Proteomics

Indexed keywords

PHOSPHOLIPID HYDROPEROXIDE GLUTATHIONE PEROXIDASE; REACTIVE OXYGEN METABOLITE; STREPTOZOCIN; GLUTATHIONE PEROXIDASE; PHOSPHOLIPID-HYDROPEROXIDE GLUTATHIONE PEROXIDASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DIABETIC CARDIOMYOPATHY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; HYPERGLYCEMIA; INNER MITOCHONDRIAL MEMBRANE; INSULIN DEPENDENT DIABETES MELLITUS; INTERFIBRILLAR MITOCHONDRIA; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; ANIMAL; ENZYMOLOGY; EXPERIMENTAL DIABETES MELLITUS; FEMALE; GENE EXPRESSION REGULATION; GENETICS; HEART MITOCHONDRION; LIPID PEROXIDATION; MALE; MASS SPECTROMETRY; METABOLISM; PHYSIOLOGY; PROTEOMICS; TRANSGENIC MOUSE; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; BIOLOGICAL TRANSPORT; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 1; DIABETIC CARDIOMYOPATHIES; FEMALE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GLUTATHIONE PEROXIDASE; LIPID PEROXIDATION; MALE; MASS SPECTROMETRY; MICE; MICE, TRANSGENIC; MITOCHONDRIA, HEART; OXIDATIVE STRESS; PROTEOMICS; REACTIVE OXYGEN SPECIES;

MLCS; MLOWN;

EID: 84878217785     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00249.2012     Document Type: Article

References (57)

1. Anderson S, Bankier AT, Barrell BG, de Bruijn MH, Coulson AR, Drouin J, Eperon IC, Nierlich DP, Roe BA, Sanger F, Schreier PH, Smith AJ, Staden R, Young IG. Sequence and organization of the human mitochondrial genome. Nature 290: 457-465, 1981.
2. Baseler WA, Dabkowski ER, Williamson CL, Croston TL, Thapa D, Powell MJ, Razunguzwa TT, Hollander JM. 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-R200, 2011.
3. Becker D, Krayl M, Strub A, Li Y, Mayer MP, Voos W. Impaired interdomain communication in mitochondrial Hsp70 results in the loss of inward-directed translocation force. J Biol Chem 284: 2934-2946, 2009.
4. Bohnert M, Rehling P, Guiard B, Herrmann JM, Pfanner N, van der Laan M. Cooperation of stop-transfer and conservative sorting mechanisms in mitochondrial protein transport. Curr Biol 20: 1227-1232, 2010.
5. 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.
6. 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.
7. 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.
8. Chacinska A, Koehler CM, Milenkovic D, Lithgow T, Pfanner N. Importing mitochondrial proteins: machineries and mechanisms. Cell 138: 628-644, 2009.
9. Chance B, Williams GR. Respiratory enzymes in oxidative phosphorylation. I. Kinetics of oxygen utilization. J Biol Chem 217: 383-393, 1955.
10. Chance B, Williams GR. Respiratory enzymes in oxidative phosphorylation. VI. The effects of adenosine diphosphate on azide-treated mitochondria. J Biol Chem 221: 477-489, 1956.
11. Chen Q, Vazquez EJ, Moghaddas S, Hoppel CL, Lesnefsky EJ. Production of reactive oxygen species by mitochondria: central role of complex III. J Biol Chem 278: 36027-36031, 2003.
12. Dabkowski ER. Quantitative proteomic analysis of distinct mitochondrial subpopulations in diabetic myocardium. FASEB J 22, 2008.
13. 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.
14. Dabkowski ER, Williamson CL, Bukowski VC, Chapman RS, Leonard SS, Peer CJ, Callery PS, Hollander JM. Diabetic cardiomyopathyassociated dysfunction in spatially distinct mitochondrial subpopulations. Am J Physiol Heart Circ Physiol 296: H359-H369, 2009.
15. 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.
16. Feniouk BA, Suzuki T, Yoshida M. Regulatory interplay between proton motive force, ADP, phosphate, and subunit epsilon in bacterial ATP synthase. J Biol Chem 282: 764-772, 2007.
17. Gambill BD, Voos W, Kang PJ, Miao B, Langer T, Craig EA, Pfanner N. A dual role for mitochondrial heat shock protein 70 in membrane translocation of preproteins. J Cell Biol 123: 109-117, 1993.
18. Garcia MJ, McNamara PM, Gordon T, Kannel WB. Morbidity and mortality in diabetics in the Framingham population. Sixteen year follow- up study. Diabetes 23: 105-111, 1974.
19. Gebert N, Joshi AS, Kutik S, Becker T, McKenzie M, Guan XL, Mooga VP, Stroud DA, Kulkarni G, Wenk MR, Rehling P, Meisinger C, Ryan MT, Wiedemann N, Greenberg ML, Pfanner N. Mitochondrial cardiolipin involved in outer-membrane protein biogenesis: implications for Barth syndrome. Curr Biol 19: 2133-2139, 2009.
20. Gevorkyan-Airapetov L, Zohary K, Popov-Celeketic D, Mapa K, Hell K, Neupert W, Azem A, Mokranjac D. Interaction of Tim23 with Tim50 is essential for protein translocation by the mitochondrial TIM23 complex. J Biol Chem 284: 4865-4872, 2009.
21. Godeas C, Sandri G, Panfili E. Distribution of phospholipid hydroperoxide glutathione peroxidase (PHGPx) in rat testis mitochondria. Biochim Biophys Acta 1191: 147-150, 1994.
22. 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.
23. Haraguchi CM, Mabuchi T, Hirata S, Shoda T, Yamada AT, Hoshi K, Yokota S. Spatiotemporal changes of levels of a moonlighting protein, phospholipid hydroperoxide glutathione peroxidase, in subcellular compartments during spermatogenesis in the rat testis. Biol Reprod 69: 885-895, 2003.
24. He H, Giordano FJ, Hilal-Dandan R, Choi DJ, Rockman HA, Mc-Donough PM, Bluhm WF, Meyer M, Sayen MR, Swanson E, Dillmann WH. Overexpression of the rat sarcoplasmic reticulum Ca2 ATPase gene in the heart of transgenic mice accelerates calcium transients and cardiac relaxation. J Clin Invest 100: 380-389, 1997.
25. Hofhaus G, Shakeley RM, Attardi G. Use of polarography to detect respiration defects in cell cultures. Methods Enzymol 264: 476-483, 1996.
26. Hollander JM, Lin KM, Scott BT, Dillmann WH. Overexpression of PHGPx and HSP60/10 protects against ischemia/reoxygenation injury. Free Radic Biol Med 35: 742-751, 2003.
27. Hollander JM, Martin JL, Belke DD, Scott BT, Swanson E, Krishnamoorthy V, Dillmann WH. Overexpression of wild-type heat shock protein 27 and a nonphosphorylatable heat shock protein 27 mutant protects against ischemia/reperfusion injury in a transgenic mouse model. Circulation 110: 3544-3552, 2004.
28. 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.
29. Judge S, Jang YM, Smith A, Hagen T, Leeuwenburgh C. Ageassociated increases in oxidative stress and antioxidant enzyme activities in cardiac interfibrillar mitochondria: implications for the mitochondrial theory of aging. FASEB J 19: 419-421, 2005.
30. Jullig M, Hickey AJ, Middleditch MJ, Crossman DJ, Lee SC, Cooper GJ. Characterization of proteomic changes in cardiac mitochondria in streptozotocin-diabetic rats using iTRAQ isobaric tags. Proteomics Clin Appl 1: 565-576, 2007.
31. Kang PJ, Ostermann J, Shilling J, Neupert W, Craig EA, Pfanner N. Requirement for hsp70 in the mitochondrial matrix for translocation and folding of precursor proteins. Nature 348: 137-143, 1990.
32. Kelley DE, He J, Menshikova EV, Ritov VB. Dysfunction of mitochondria in human skeletal muscle in type 2 diabetes. Diabetes 51: 2944-2950, 2002.
33. 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.
34. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685, 1970.
35. Lesnefsky EJ, Chen Q, Slabe TJ, Stoll MS, Minkler PE, Hassan MO, Tandler B, Hoppel CL. Ischemia, rather than reperfusion, inhibits respiration through cytochrome oxidase in the isolated, perfused rabbit heart: role of cardiolipin. Am J Physiol Heart Circ Physiol 287: H258-H267, 2004.
36. Lin D. Multidimensional protein identification technology as an effective tool for proteomics. Am Genomic/Proteomic Technol 1: 38-46, 2001.
37. Lu J, Holmgren A. Selenoproteins. J Biol Chem 284: 723-727, 2009.
38. Nam S, Nakamuta N, Kurohmaru M, Hayashi Y. Cloning and sequencing of the mouse cDNA encoding a phospholipid hydroperoxide glutathione peroxidase. Gene 198: 245-249, 1997.
39. 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.
40. Perocchi F, Jensen LJ, Gagneur J, Ahting U, von Mering C, Bork P, Prokisch H, Steinmetz LM. Assessing systems properties of yeast mitochondria through an interaction map of the organelle. PLoS Genet 2: e170, 2006.
41. Pfeiffer K, Gohil V, Stuart RA, Hunte C, Brandt U, Greenberg ML, Schagger H. Cardiolipin stabilizes respiratory chain supercomplexes. J Biol Chem 278: 52873-52880, 2003.
42. Pullman ME, Penefsky HS, Datta A, Racker E. Partial resolution of the enzymes catalyzing oxidative phosphorylation. I. Purification and properties of soluble dinitrophenol-stimulated adenosine triphosphatase. J Biol Chem 235: 3322-3329, 1960.
43. Pushpa-Rekha TR, Burdsall AL, Oleksa LM, Chisolm GM, Driscoll DM. Rat phospholipid-hydroperoxide glutathione peroxidase. cDNA cloning and identification of multiple transcription and translation start sites. J Biol Chem 270: 26993-26999, 1995.
44. Ritov VB, Menshikova EV, He J, Ferrell RE, Goodpaster BH, Kelley DE. Deficiency of subsarcolemmal mitochondria in obesity and type 2 diabetes. Diabetes 54: 8-14, 2005.
45. Rosca MG, Okere IA, Sharma N, Stanley WC, Recchia FA, Hoppel CL. Altered expression of the adenine nucleotide translocase isoforms and decreased ATP synthase activity in skeletal muscle mitochondria in heart failure. J Mol Cell Cardiol 46: 927-935, 2009.
46. Schwarz E, Seytter T, Guiard B, Neupert W. Targeting of cytochrome b2 into the mitochondrial intermembrane space: specific recognition of the sorting signal. EMBO J 12: 2295-2302, 1993.
47. Shen X, Zheng S, Thongboonkerd V, Xu M, Pierce WM Jr, Klein JB, Epstein PN. Cardiac mitochondrial damage and biogenesis in a chronic model of type 1 diabetes. Am J Physiol Endocrinol Metab 287: E896- E905, 2004.
48. Singh K, Hood DA. Effect of denervation-induced muscle disuse on mitochondrial protein import. Am J Physiol Cell Physiol 300: C138-C145, 2011.
49. Stojanovski D, Pfanner N, Wiedemann N. Import of proteins into mitochondria. Methods Cell Biol 80: 783-806, 2007.
50. Trounce IA, Kim YL, Jun AS, Wallace DC. Assessment of mitochondrial oxidative phosphorylation in patient muscle biopsies, lymphoblasts, and transmitochondrial cell lines. Methods Enzymol 264: 484-509, 1996.
51. Turko IV, Murad F. Quantitative protein profiling in heart mitochondria from diabetic rats. J Biol Chem 278: 35844-35849, 2003.
52. Ursini F, Maiorino M, Brigelius-Flohe R, Aumann KD, Roveri A, Schomburg D, Flohe L. Diversity of glutathione peroxidases. Methods Enzymol 252: 38-53, 1995.
53. Voos W, Martin H, Krimmer T, Pfanner N. Mechanisms of protein translocation into mitochondria. Biochim Biophys Acta 1422: 235-254, 1999.
54. 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.
55. Williamson CL, Dabkowski ER, Dillmann WH, Hollander JM. Mitochondria protection from hypoxia/reoxygenation injury with mitochondria heat shock protein 70 overexpression. Am J Physiol Heart Circ Physiol 294: H249-H256, 2008.
56. Ye G, Metreveli NS, Donthi RV, Xia S, Xu M, Carlson EC, Epstein PN. Catalase protects cardiomyocyte function in models of type 1 and type 2 diabetes. Diabetes 53: 1336-1343, 2004.
57. Zhou M, Diwu Z, Panchuk-Voloshina N, Haugland RP. A stable nonfluorescent derivative of resorufin for the fluorometric determination of trace hydrogen peroxide: applications in detecting the activity of phagocyte NADPH oxidase and other oxidases. Anal Biochem 253: 162-168, 1997.