Transgenic overexpression of mitofilin attenuates diabetes mellitus-associated cardiac and mitochondria dysfunction

Journal of Molecular and Cellular Cardiology

Volumn 79, Issue , 2015, Pages 212-223

  Thapa, Dharendra ^a   Nichols, Cody E ^a   Lewis, Sara E ^a   Shepherd, Danielle L ^a   Jagannathan, Rajaganapathi ^a   Croston, Tara L ^a   Tveter, Kevin J ^a   Holden, Anthony A ^a   Baseler, Walter A ^a   Hollander, John M ^a  

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

Author keywords

Diabetes mellitus; Electron transport chain; Mitochondria; Mitofilin

Indexed keywords

CYTOCHROME C OXIDASE; MITOFILIN; MUSCLE PROTEIN; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); STREPTOZOCIN; UBIQUINOL CYTOCHROME C REDUCTASE; UNCLASSIFIED DRUG; IMMT PROTEIN, HUMAN; MITOCHONDRIAL PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL FUNCTION; CELL STRUCTURE; CONTROLLED STUDY; DIABETIC CARDIOMYOPATHY; DISEASE MODEL; DISORDERS OF MITOCHONDRIAL FUNCTIONS; FLOW CYTOMETRY; HEART CONTRACTION; HEART EJECTION FRACTION; HEART FUNCTION; HEART MITOCHONDRION; INSULIN DEPENDENT DIABETES MELLITUS; INTERFIBRILLAR MITOCHONDRIA; LIPID PEROXIDATION; MALE; MITOCHONDRIAL MEMBRANE POTENTIAL; MOUSE; NONHUMAN; PROTEIN EXPRESSION; QUALITATIVE ANALYSIS; RESPIRATORY CHAIN; STATE 3 RESPIRATION; TRANSGENIC MOUSE; WILD TYPE; ANIMAL; BODY WEIGHT; ELECTRON TRANSPORT; EXPERIMENTAL DIABETES MELLITUS; HEART; HUMAN; METABOLISM; MITOCHONDRIAL DYNAMICS; NATIVE POLYACRYLAMIDE GEL ELECTROPHORESIS; ORGAN SIZE; OXIDATIVE STRESS; PATHOLOGY; PATHOPHYSIOLOGY; ULTRASTRUCTURE; WESTERN BLOTTING;

MUS; MUS MUSCULUS;

ANIMALS; BLOTTING, WESTERN; BODY WEIGHT; DIABETES MELLITUS, EXPERIMENTAL; ELECTRON TRANSPORT; HEART; HUMANS; LIPID PEROXIDATION; MALE; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE, TRANSGENIC; MITOCHONDRIA, HEART; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL PROTEINS; MUSCLE PROTEINS; MYOCARDIAL CONTRACTION; NATIVE POLYACRYLAMIDE GEL ELECTROPHORESIS; ORGAN SIZE; OXIDATIVE STRESS;

EID: 84916898790     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2014.11.008     Document Type: Article

References (60)

1. Mannella C.A. The relevance of mitochondrial membrane topology to mitochondrial function. Biochim Biophys Acta Feb 2006, 1762(2):140-147.
2. Zick M., Rabl R., Reichert A.S. Cristae formation-linking ultrastructure and function of mitochondria. Biochim Biophys Acta Jan 2009, 1793(1):5-19.
3. Rabl R., Soubannier V., Scholz R., Vogel F., Mendl N., Vasiljev-Neumeyer A., et al. Formation of cristae and crista junctions in mitochondria depends on antagonism between Fcj1 and Su e/g. J Cell Biol Jun 15 2009, 185(6):1047-1063.
4. Davies K.M., Strauss M., Daum B., Kief J.H., Osiewacz H.D., Rycovska A., et al. Macromolecular organization of ATP synthase and complex I in whole mitochondria. Proc Natl Acad Sci U S A Aug 23 2011, 108(34):14121-14126.
5. Gilkerson R.W., Selker J.M., Capaldi R.A. The cristal membrane of mitochondria is the principal site of oxidative phosphorylation. FEBS Lett Jul 10 2003, 546(2-3):355-358.
6. Vogel F., Bornhovd C., Neupert W., Reichert A.S. Dynamic subcompartmentalization of the mitochondrial inner membrane. J Cell Biol Oct 23 2006, 175(2):237-247.
7. Wurm C.A., Jakobs S. Differential protein distributions define two sub-compartments of the mitochondrial inner membrane in yeast. FEBS Lett Oct 16 2006, 580(24):5628-5634.
8. DiMauro S., Bonilla E., Zeviani M., Nakagawa M., DeVivo D.C. Mitochondrial myopathies. Ann Neurol Jun 1985, 17(6):521-538.
9. Wallace D.C. A mitochondrial paradigm of metabolic and degenerative diseases, aging, and cancer: a dawn for evolutionary medicine. Annu Rev Genet 2005, 39:359-407.
10. An J., Shi J., He Q., Lui K., Liu Y., Huang Y., et al. CHCM1/CHCHD6, novel mitochondrial protein linked to regulation of mitofilin and mitochondrial cristae morphology. J Biol Chem Mar 2 2012, 287(10):7411-7426.
11. Darshi M., Mendiola V.L., Mackey M.R., Murphy A.N., Koller A., Perkins G.A., et al. ChChd3, an inner mitochondrial membrane protein, is essential for maintaining crista integrity and mitochondrial function. J Biol Chem Jan 28 2010, 286(4):2918-2932.
12. Frezza C., Cipolat S., Martins de Brito O., Micaroni M., Beznoussenko G.V., Rudka T., et al. OPA1 controls apoptotic cristae remodeling independently from mitochondrial fusion. Cell Jul 14 2006, 126(1):177-189.
13. Paumard P., Vaillier J., Coulary B., Schaeffer J., Soubannier V., Mueller D.M., et al. The ATP synthase is involved in generating mitochondrial cristae morphology. EMBO J Feb 1 2002, 21(3):221-230.
14. Icho T., Ikeda T., Matsumoto Y., Hanaoka F., Kaji K., Tsuchida N. A novel human gene that is preferentially transcribed in heart muscle. Gene Jul 8 1994, 144(2):301-306.
15. Korner C., Barrera M., Dukanovic J., Eydt K., Harner M., Rabl R., et al. The C-terminal domain of Fcj1 is required for formation of crista junctions and interacts with the TOB/SAM complex in mitochondria. Mol Biol Cell Jun 2012, 23(11):2143-2155.
16. John G.B., Shang Y., Li L., Renken C., Mannella C.A., Selker J.M., et al. The mitochondrial inner membrane protein mitofilin controls cristae morphology. Mol Biol Cell Mar 2005, 16(3):1543-1554.
17. Mun J.Y., Lee T.H., Kim J.H., Yoo B.H., Bahk Y.Y., Koo H.S., et al. Caenorhabditis elegans mitofilin homologs control the morphology of mitochondrial cristae and influence reproduction and physiology. J Cell Physiol Sep 2010, 224(3):748-756.
18. Alkhaja A.K., Jans D.C., Nikolov M., Vukotic M., Lytovchenko O., Ludewig F., et al. MINOS1 is a conserved component of mitofilin complexes and required for mitochondrial function and cristae organization. Mol Biol Cell Jan 2012, 23(2):247-257.
19. Harner M., Korner C., Walther D., Mokranjac D., Kaesmacher J., Welsch U., et al. The mitochondrial contact site complex, a determinant of mitochondrial architecture. EMBO J Nov 2 2011, 30(21):4356-4370.
20. Hoppins S., Collins S.R., Cassidy-Stone A., Hummel E., Devay R.M., Lackner L.L., et al. A mitochondrial-focused genetic interaction map reveals a scaffold-like complex required for inner membrane organization in mitochondria. J Cell Biol Oct 17 2011, 195(2):323-340.
21. Pfanner N., van der Laan M., Amati P., Capaldi R.A., Caudy A.A., Chacinska A., et al. Uniform nomenclature for themitochondrial contact site and cristae organizing system. J Cell Biol Mar 31 2014, 204(7):1083-1086.
22. von der Malsburg K., Muller J.M., Bohnert M., Oeljeklaus S., Kwiatkowska P., Becker T., et al. Dual role of mitofilin in mitochondrial membrane organization and protein biogenesis. Dev Cell Oct 18 2011, 21(4):694-707.
23. Zerbes R.M., Bohnert M., Stroud D.A., von der Malsburg K., Kram A., Oeljeklaus S., et al. Role of MINOS in mitochondrial membrane architecture: cristae morphology and outer membrane interactions differentially depend on mitofilin domains. J Mol Biol Sep 14 2012, 422(2):183-191.
24. Bernert G., Fountoulakis M., Lubec G. Manifold decreased protein levels of matrin 3, reduced motor protein HMP and hlark in fetal Down's syndrome brain. Proteomics Dec 2002, 2(12):1752-1757.
25. Myung J., Gulesserian T., Fountoulakis M., Lubec G. Deranged hypothetical proteins Rik protein, Nit protein 2 and mitochondrial inner membrane protein, Mitofilin, in fetal Down syndrome brain. Cell Mol Biol (Noisy-le-Grand) Jul 2003, 49(5):739-746.
26. Van Laar V.S., Dukes A.A., Cascio M., Hastings T.G. Proteomic analysis of rat brain mitochondria following exposure to dopamine quinone: implications for Parkinson disease. Neurobiol Dis Mar 2008, 29(3):477-489.
27. Van Laar V.S., Mishizen A.J., Cascio M., Hastings T.G. Proteomic identification of dopamine-conjugated proteins from isolated rat brain mitochondria and SH-SY5Y cells. Neurobiol Dis Jun 2009, 34(3):487-500.
28. Furukawa A., Kawamoto Y., Chiba Y., Takei S., Hasegawa-Ishii S., Kawamura N., et al. Proteomic identification of hippocampal proteins vulnerable to oxidative stress in excitotoxin-induced acute neuronal injury. Neurobiol Dis Sep 2011, 43(3):706-714.
29. Omori A., Ichinose S., Kitajima S., Shimotohno K.W., Murashima Y.L., Shimotohno K., et al. Gerbils of a seizure-sensitive strain have a mitochondrial inner membrane protein with different isoelectric points from those of a seizure-resistant strain. Electrophoresis Dec 2002, 23(24):4167-4174.
30. Wang Q., Liu Y., Zou X., An M., Guan X., He J., et al. The hippocampal proteomic analysis of senescence-accelerated mouse: implications of Uchl3 and mitofilin in cognitive disorder and mitochondria dysfunction in SAMP8. Neurochem Res Sep 2008, 33(9):1776-1782.
31. Wishart T.M., Paterson J.M., Short D.M., Meredith S., Robertson K.A., Sutherland C., et al. Differential proteomics analysis of synaptic proteins identifies potential cellular targets and protein mediators of synaptic neuroprotection conferred by the slow Wallerian degeneration (Wlds) gene. Mol Cell Proteomics Aug 2007, 6(8):1318-1330.
32. Bugger H., Boudina S., Hu X.X., Tuinei J., Zaha V.G., Theobald H.A., et al. Type 1 diabetic Akita mouse hearts are insulin sensitive but manifest structurally abnormal mitochondria that remain coupled despite increased uncoupling protein 3. Diabetes Nov 2008, 57(11):2924-2932.
33. Baseler W.A., Dabkowski E.R., Williamson C.L., Croston T.L., Thapa D., Powell M.J., et al. Proteomic alterations of distinctmitochondrial subpopulations in the type 1 diabetic heart: contribution of protein import dysfunction. Am J Physiol Regul Integr Comp Physiol Regul Integr Comp Physiol Feb 2011, 300(2):R186-R200.
34. Dabkowski E.R., Williamson C.L., Bukowski V.C., Chapman R.S., Leonard S.S., Peer C.J., et al. Diabetic cardiomyopathy-associated dysfunction in spatially distinct mitochondrial subpopulations. Am J Physiol Heart Circ Physiol Feb 2009, 296(2):H359-H369.
35. He H., Giordano F.J., Hilal-Dandan R., Choi D.J., Rockman H.A., McDonough P.M., et al. Overexpression of the rat sarcoplasmic reticulum Ca2+ ATPase gene in the heart of transgenic mice accelerates calcium transients and cardiac relaxation. J Clin Invest Jul 15 1997, 100(2):380-389.
36. Hollander J.M., Martin J.L., Belke D.D., Scott B.T., Swanson E., Krishnamoorthy V., et al. 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 Dec 7 2004, 110(23):3544-3552.
37. Marber M.S., Mestril R., Chi S.H., Sayen M.R., Yellon D.M., Dillmann W.H. Overexpression of the rat inducible 70-kD heat stress protein in a transgenic mouse increases the resistance of the heart to ischemic injury. J Clin Invest Apr 1995, 95(4):1446-1456.
38. Dabkowski E.R., Williamson C.L., Hollander J.M. Mitochondria-specific transgenic overexpression of phospholipid hydroperoxide glutathione peroxidase (GPx4) attenuates ischemia/reperfusion-associated cardiac dysfunction. Free Radic Biol Med Sep 15 2008, 45(6):855-865.
39. Baseler W.A., Dabkowski E.R., Jagannathan R., Thapa D., Nichols C.E., Shepherd D.L., et al. Reversal of mitochondrial proteomic loss in Type 1 diabetic heart with overexpression of phospholipid hydroperoxide glutathione peroxidase. Am J Physiol Regul Integr Comp Physiol Apr 1 2013, 304(7):R553-R565.
40. Baseler W.A., Thapa D., Jagannathan R., Dabkowski E.R., Croston T.L., Hollander J.M. miR-141 as a regulator of the mitochondrial phosphate carrier (Slc25a3) in the type 1 diabetic heart. Am J Physiol Cell Physiol Dec 15 2012, 303(12):C1244-C1251.
41. Croston T.L., Shepherd D.L., Thapa D., Nichols C.E., Lewis S.E., Dabkowski E.R., et al. Evaluation of the cardiolipin biosynthetic pathway and its interactions in the diabetic heart. Life Sci Sep 3 2013, 93(8):313-322.
42. Williamson C.L., Dabkowski E.R., Baseler W.A., Croston T.L., Alway S.E., Hollander J.M. Enhanced apoptotic propensity in diabetic cardiac mitochondria: influence of subcellular spatial location. Am J Physiol Heart Circ Physiol Feb 2009, 298(2):H633-H642.
43. Bauer M., Cheng S., Jain M., Ngoy S., Theodoropoulos C., Trujillo A., et al. Echocardiographic speckle-tracking based strain imaging for rapid cardiovascular phenotyping in mice. Circ Res Apr 15 2011, 108(8):908-916.
44. Palmer J.W., Tandler B., Hoppel C.L. Biochemical properties of subsarcolemmal and interfibrillar mitochondria isolated from rat cardiac muscle. J Biol Chem Dec 10 1977, 252(23):8731-8739.
45. Croston T.L., Thapa D., Holden A.A., Tveter K.J., Lewis S.E., Shepherd D.L., et al. Functional deficiencies of subsarcolemmal mitochondria in the type 2 diabetic human heart. Am J Physiol Heart Circ Physiol Jul 1 2014, 307(1):H54-H65.
46. Dabkowski E.R., Baseler W.A., Williamson C.L., Powell M., Razunguzwa T.T., Frisbee J.C., et al. Mitochondrial dysfunction in the type 2 diabetic heart is associated with alterations in spatially distinct mitochondrial proteomes. Am J Physiol Heart Circ Physiol Aug 2010, 299(2):H529-H540.
47. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem May 7 1976, 72:248-254.
48. Chance B., Williams G.R. Respiratory enzymes in oxidative phosphorylation. I. Kinetics of oxygen utilization. J Biol Chem Nov 1955, 217(1):383-393.
49. Chance B., Williams G.R. Respiratory enzymes in oxidative phosphorylation. VI. The effects of adenosine diphosphate on azide-treated mitochondria. J Biol Chem Jul 1956, 221(1):477-489.
50. Warshaw J.B. Cellular energy metabolism during fetal development. I. Oxidative phosphorylation in the fetal heart. J Cell Biol May 1969, 41(2):651-657.
51. Trounce I.A., Kim Y.L., Jun A.S., Wallace D.C. Assessment of mitochondrial oxidative phosphorylation in patient muscle biopsies, lymphoblasts, and transmitochondrial cell lines. Methods Enzymol 1996, 264:484-509.
52. Feniouk B.A., Suzuki T., Yoshida M. Regulatory interplay between proton motive force, ADP, phosphate, and subunit epsilon in bacterial ATP synthase. J Biol Chem Jan 5 2007, 282(1):764-772.
53. Pullman M.E., Penefsky H.S., 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 Nov 1960, 235:3322-3329.
54. Rosca M.G., Okere I.A., Sharma N., Stanley W.C., Recchia F.A., Hoppel C.L. Altered expression of the adenine nucleotide translocase isoforms and decreased ATP synthase activity in skeletal muscle mitochondria in heart failure. J Mol Cell Cardiol Jun 2009, 46(6):927-935.
55. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature Aug 15 1970, 227(5259):680-685.
56. Ferreira R.M., Vitorino R., Padrao A.I., Moreira-Goncalves D., Alves R.M., Duarte J.A., et al. Spatially distinct mitochondrial populations exhibit different mitofilin levels. Cell Biochem Funct Jul 2012, 30(5):395-399.
57. Shen X., Zheng S., Thongboonkerd V., Xu M., Pierce W.M., Klein J.B., et al. Cardiac mitochondrial damage and biogenesis in a chronic model of type 1 diabetes. Am J Physiol Endocrinol Metab Nov 2004, 287(5):E896-E905.
58. Song Y., Du Y., Prabhu S.D., Epstein P.N. Diabetic cardiomyopathy in OVE26 mice shows mitochondrial ROS production and divergence between in vivo and in vitro contractility. Rev Diabet Stud Fall 2007, 4(3):159-168.
59. Motyl K., McCabe L.R. Streptozotocin, type I diabetes severity and bone. Biol Proced Online 2009, 11:296-315.
60. Zhang Y., Xu J., Luo Y.X., An X.Z., Zhang R., Liu G., et al. Overexpression of Mitofilin in the Mouse Heart Promotes Cardiac Hypertrophy in Response to Hypertrophic Stimuli. Antioxid Redox Signal Oct 2014, 21(12):1693-1707.