Translocase of inner mitochondrial membrane 44 alters the mitochondrial fusion and fission dynamics and protects from type 2 diabetes

Metabolism: Clinical and Experimental

Volumn 64, Issue 6, 2015, Pages 677-688

  Wang, Yu ^a   Katayama, Akihiro ^a   Terami, Takahiro ^a   Han, Xiaoying ^a,b   Nunoue, Tomokazu ^a   Zhang, Dongxiao ^a   Teshigawara, Sanae ^a   Eguchi, Jun ^a   Nakatsuka, Atsuko ^a   Murakami, Kazutoshi ^a   Ogawa, Daisuke ^a   Furuta, Yasuhide ^c   Makino, Hirofumi ^a   Wada, Jun ^a  

^a OKAYAMA UNIVERSITY   (Japan)

^b MCGILL UNIVERSITY   (Canada)

^c RIKEN Center for Biosystems Dynamics Research   (Japan)

Author keywords

Fission; Fusion; Preprotein import; Reactive oxygen species

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; CARRIER PROTEIN; HEAT SHOCK PROTEIN 70; MEMBRANE PROTEIN; MITOCHONDRIAL PROTEIN; MITOFUSIN 1; MITOFUSIN 2; PROTEIN PRECURSOR; REACTIVE OXYGEN METABOLITE; TRANSLOCASE OF INNER MITOCHONDRIAL MEMBRANE 23; TRANSLOCASE OF INNER MITOCHONDRIAL MEMBRANE 44; UNCLASSIFIED DRUG; TIMM44 PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; BROWN ADIPOCYTE; BROWN ADIPOSE TISSUE; CARBOHYDRATE DIET; CELL FUSION; CELL PROTECTION; CELL SIZE; CONTROLLED STUDY; EMBRYO; FUSION GENE; GENE EXPRESSION; GLUCOSE TOLERANCE TEST; INSULIN SENSITIVITY; INSULIN TOLERANCE TEST; LIPID DIET; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; TRANSGENIC MOUSE; WHITE ADIPOCYTE; WHITE ADIPOSE TISSUE; WILD TYPE; ADIPOCYTE; ANIMAL; C57BL MOUSE; CELL DIFFERENTIATION; DIABETES MELLITUS, EXPERIMENTAL; ENZYMOLOGY; FIBROBLAST; GENETICS; HUMAN; INSULIN RESISTANCE; METABOLISM; MITOCHONDRIAL MEMBRANE POTENTIAL;

ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; ADIPOCYTES; ANIMALS; CARRIER PROTEINS; CELL DIFFERENTIATION; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 2; FIBROBLASTS; HSP70 HEAT-SHOCK PROTEINS; HUMANS; INSULIN RESISTANCE; MEMBRANE POTENTIAL, MITOCHONDRIAL; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MITOCHONDRIAL MEMBRANES; MITOCHONDRIAL PROTEINS;

EID: 84927965410     PISSN: 00260495     EISSN: 15328600     Source Type: Journal    
DOI: 10.1016/j.metabol.2015.02.004     Document Type: Article

References (38)

1. C.M. Kusminski, and P.E. Scherer Mitochondrial dysfunction in white adipose tissue Trends Endocrinol Metab 23 2012 435 443
2. H.J. Choo, J.H. Kim, O.B. Kwon, C.S. Lee, J.Y. Mun, and S.S. Han Mitochondria are impaired in the adipocytes of type 2 diabetic mice Diabetologia 49 2006 784 791
3. K.H. Fisher-Wellman, and P.D. Neufer Linking mitochondrial bioenergetics to insulin resistance via redox biology Trends Endocrinol Metab 23 2012 142 153
4. J.M. Curtis, P.A. Grimsrud, W.S. Wright, X. Xu, R.E. Foncea, and D.W. Graham Downregulation of adipose glutathione S-transferase A4 leads to increased protein carbonylation, oxidative stress, and mitochondrial dysfunction Diabetes 59 2010 1132 1142
5. L. Wilson-Fritch, S. Nicoloro, M. Chouinard, M.A. Lazar, P.C. Chui, and J. Leszyk Mitochondrial remodeling in adipose tissue associated with obesity and treatment with rosiglitazone J Clin Invest 114 2004 1281 1289
6. I. Bogacka, B. Ukropcova, M. McNeil, J.M. Gimble, and S.R. Smith Structural and functional consequences of mitochondrial biogenesis in human adipocytes in vitro J Clin Endocrinol Metab 90 2005 6650 6656
7. L. Wilson-Fritch, A. Burkart, G. Bell, K. Mendelson, J. Leszyk, and S. Nicoloro Mitochondrial biogenesis and remodeling during adipogenesis and in response to the insulin sensitizer rosiglitazone Mol Cell Biol 23 2003 1085 1094
8. C. Vernochet, A. Mourier, O. Bezy, Y. Macotela, J. Boucher, and M.J. Rardin Adipose-specific deletion of TFAM increases mitochondrial oxidation and protects mice against obesity and insulin resistance Cell Metab 16 2012 765 776
9. J. Wada, and Y.S. Kanwar Characterization of mammalian translocase of inner mitochondrial membrane (Tim44) isolated from diabetic newborn mouse kidney Proc Natl Acad Sci U S A 95 1998 144 149
10. Y. Zhang, J. Wada, I. Hashimoto, J. Eguchi, A. Yasuhara, and Y.S. Kanwar 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 2006 1090 1101
11. T. Matsuoka, J. Wada, I. Hashimoto, Y. Zhang, J. Eguchi, and N. Ogawa Gene delivery of Tim44 reduces mitochondrial superoxide production and ameliorates neointimal proliferation of injured carotid artery in diabetic rats Diabetes 54 2005 2882 2890
12. M.O. Dietrich, Z.W. Liu, and T.L. Horvath Mitochondrial dynamics controlled by mitofusins regulate Agrp neuronal activity and diet-induced obesity Cell 155 2013 188 199
13. D.J. Pagliarini, S.E. Calvo, B. Chang, S.A. Sheth, S.B. Vafai, and S.E. Ong A mitochondrial protein compendium elucidates complex I disease biology Cell 134 2008 112 123
14. D. Bar-Yaacov, A. Blumberg, and D. Mishmar Mitochondrial-nuclear co-evolution and its effects on OXPHOS activity and regulation Biochim Biophys Acta 2012 1819 1107 1111
15. A.V. Segre, D. Consortium, investigators M, L. Groop, V.K. Mootha, and M.J. Daly Common inherited variation in mitochondrial genes is not enriched for associations with type 2 diabetes or related glycemic traits PLoS Genet 6 2010 e1001058
16. S.L. Archer Mitochondrial dynamics - mitochondrial fission and fusion in human diseases N Engl J Med 369 2013 2236 2251
17. W.J. Koopman, P.H. Willems, and J.A. Smeitink Monogenic mitochondrial disorders N Engl J Med 366 2012 1132 1141
18. R.J. Youle, and A.M. van der Bliek Mitochondrial fission, fusion, and stress Science 337 2012 1062 1065
19. N. Ishihara, H. Otera, T. Oka, and K. Mihara Regulation and physiologic functions of GTPases in mitochondrial fusion and fission in mammals Antioxid Redox Signal 19 2013 389 399
20. J.T. Cribbs, and S. Strack Functional characterization of phosphorylation sites in dynamin-related protein 1 Methods Enzymol 457 2009 231 253
21. H. Chen, S.A. Detmer, A.J. Ewald, E.E. Griffin, S.E. Fraser, and D.C. Chan Mitofusins Mfn1 and Mfn2 coordinately regulate mitochondrial fusion and are essential for embryonic development J Cell Biol 160 2003 189 200
22. Y.J. Lee, S.Y. Jeong, M. Karbowski, C.L. Smith, and R.J. Youle Roles of the mammalian mitochondrial fission and fusion mediators Fis1, Drp1, and Opa1 in apoptosis Mol Biol Cell 15 2004 5001 5011
23. H. Otera, C. Wang, M.M. Cleland, K. Setoguchi, S. Yokota, and R.J. Youle Mff is an essential factor for mitochondrial recruitment of Drp1 during mitochondrial fission in mammalian cells J Cell Biol 191 2010 1141 1158
24. J. Zhao, T. Liu, S. Jin, X. Wang, M. Qu, and P. Uhlen Human MIEF1 recruits Drp1 to mitochondrial outer membranes and promotes mitochondrial fusion rather than fission EMBO J 30 2011 2762 2778
25. A. Zorzano, M. Liesa, and M. Palacin Role of mitochondrial dynamics proteins in the pathophysiology of obesity and type 2 diabetes Int J Biochem Cell Biol 41 2009 1846 1854
26. D. Sebastian, M.I. Hernandez-Alvarez, J. Segales, E. Sorianello, J.P. Munoz, and D. Sala Mitofusin 2 (Mfn2) links mitochondrial and endoplasmic reticulum function with insulin signaling and is essential for normal glucose homeostasis Proc Natl Acad Sci U S A 109 2012 5523 5528
27. Z. Zhang, N. Wakabayashi, J. Wakabayashi, Y. Tamura, W.J. Song, and S. Sereda The dynamin-related GTPase Opa1 is required for glucose-stimulated ATP production in pancreatic beta cells Mol Biol Cell 22 2011 2235 2245
28. R. Liu, P. Jin, Yu Liqun, Y. Wang, L. Han, and T. Shi Impaired mitochondrial dynamics and bioenergetics in diabetic skeletal muscle PLoS One 9 2014 e92810
29. D. Mokranjac, M. Sichting, D. Popov-Celeketic, K. Mapa, L. Gevorkyan-Airapetov, and K. Zohary Role of Tim50 in the transfer of precursor proteins from the outer to the inner membrane of mitochondria Mol Biol Cell 20 2009 1400 1407
30. Y. Tamura, Y. Harada, T. Shiota, K. Yamano, K. Watanabe, and M. Yokota Tim23-Tim50 pair coordinates functions of translocators and motor proteins in mitochondrial protein import J Cell Biol 184 2009 129 141
31. N.N. Alder, R.E. Jensen, and A.E. Johnson Fluorescence mapping of mitochondrial TIM23 complex reveals a water-facing, substrate-interacting helix surface Cell 134 2008 439 450
32. A. Chacinska, M. Lind, A.E. Frazier, J. Dudek, C. Meisinger, and A. Geissler Mitochondrial presequence translocase: switching between TOM tethering and motor recruitment involves Tim21 and Tim17 Cell 120 2005 817 829
33. S. Martinez-Caballero, S.M. Grigoriev, J.M. Herrmann, M.L. Campo, and K.W. Kinnally Tim17p regulates the twin pore structure and voltage gating of the mitochondrial protein import complex TIM23 J Biol Chem 282 2007 3584 3593
34. M. van der Laan, M. Meinecke, J. Dudek, D.P. Hutu, M. Lind, and I. Perschil Motor-free mitochondrial presequence translocase drives membrane integration of preproteins Nat Cell Biol 9 2007 1152 1159
35. N. Wiedemann, M. van der Laan, D.P. Hutu, P. Rehling, and N. Pfanner Sorting switch of mitochondrial presequence translocase involves coupling of motor module to respiratory chain J Cell Biol 179 2007 1115 1122
36. M.K. Dienhart, and R.A. Stuart The yeast Aac2 protein exists in physical association with the cytochrome bc1-COX supercomplex and the TIM23 machinery Mol Biol Cell 19 2008 3934 3943
37. M. Krayl, J.H. Lim, F. Martin, B. Guiard, and W. Voos A cooperative action of the ATP-dependent import motor complex and the inner membrane potential drives mitochondrial preprotein import Mol Cell Biol 27 2007 411 425
38. O. Slutsky-Leiderman, M. Marom, O. Iosefson, R. Levy, S. Maoz, and A. Azem The interplay between components of the mitochondrial protein translocation motor studied using purified components J Biol Chem 282 2007 33935 33942