Diabetes regulates mitochondrial biogenesis and fission in mouse neurons

Diabetologia

Volumn 53, Issue 1, 2010, Pages 160-169

  Edwards, J L ^a   Quattrini, A ^b   Lentz, S I ^a   Figueroa Romero, C ^a   Cerri, F ^b   Backus, C ^a   Hong, Y ^a   Feldman, E L ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b SAN RAFFAELE HOSPITAL   (Italy)

Author keywords

Diabetic neuropathy; Mitochondrial biogenesis; Mitochondrial fission

Indexed keywords

DYNAMIN I; MITOCHONDRIAL DNA; PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOGENESIS; BRAIN MITOCHONDRION; CELL DIVISION; CELL FUSION; CELL SURVIVAL; CELL ULTRASTRUCTURE; CELL VIABILITY; CONTROLLED STUDY; DIABETIC NEUROPATHY; DISEASE PREDISPOSITION; EMBRYO; GENE; HYPERGLYCEMIA; IN VITRO STUDY; IN VIVO STUDY; KNOCKOUT GENE; METABOLISM; MOUSE; NERVE CELL; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; SPINAL GANGLION;

ANIMALS; APOPTOSIS REGULATORY PROTEINS; BROMODEOXYURIDINE; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASES; CELL CULTURE TECHNIQUES; CELL SURVIVAL; DIABETES MELLITUS, EXPERIMENTAL; DNA, MITOCHONDRIAL; GANGLIA, SPINAL; GENE EXPRESSION REGULATION; GLUTAMINE; GTP PHOSPHOHYDROLASES; HEMOGLOBIN A, GLYCOSYLATED; MICE; MICRORNAS; MITOCHONDRIA; NEURONS; OXIDATIVE STRESS;

EID: 72449133773     PISSN: 0012186X     EISSN: 14320428     Source Type: Journal    
DOI: 10.1007/s00125-009-1553-y     Document Type: Article

References (50)

1. GM Leinninger C Backus AM Sastry YB Yi CW Wang EL Feldman 2006 Mitochondria in DRG neurons undergo hyperglycemic mediated injury through Bim, Bax and the fission protein Drp1 Neurobiol Dis 23 11 22 10.1016/j.nbd.2006.01. 017 1:CAS:528:DC%2BD28XlvFyqsb8%3D 16684605 (Pubitemid 44192383)
2. R Cartoni JC Martinou 2009 Role of mitofusin 2 mutations in the physiopathology of Charcot-Marie-Tooth disease type 2A Exp Neurol 218 268 273 10.1016/j.expneurol.2009.05.003 1:CAS:528:DC%2BD1MXosVWlt70%3D 19427854
3. CL Martin J Albers WH Herman, et al. 2006 Neuropathy among the diabetes control and complications trial cohort 8 years after trial completion Diabetes Care 29 340 344 10.2337/diacare.29.02.06.dc05-1549 16443884
4. AM Vincent LL McLean C Backus EL Feldman 2005 Short-term hyperglycemia produces oxidative damage and apoptosis in neurons FASEB J 19 638 640 1:CAS:528:DC%2BD2MXjtFaksL8%3D 15677696
5. TJ Huang SA Price L Chilton, et al. 2003 Insulin prevents depolarization of the mitochondrial inner membrane in sensory neurons of type 1 diabetic rats in the presence of sustained hyperglycemia Diabetes 52 2129 2136 10.2337/diabetes.52.8.2129 1:CAS:528:DC%2BD3sXlvFCgtb0%3D 12882932 (Pubitemid 36919808)
6. AM Vincent MJ Stevens C Backus LL McLean EL Feldman 2005 Cell culture modeling to test therapies against hyperglycemia-mediated oxidative stress and injury Antioxid Redox Signal 7 1494 1506 10.1089/ars.2005.7.1494 1:CAS:528:DC%2BD2MXhtlWht73K 16356113 (Pubitemid 41767985)
7. JW Russell D Golovoy AM Vincent, et al. 2002 High glucose-induced oxidative stress and mitochondrial dysfunction in neurons FASEB J 16 1738 1748 10.1096/fj.01-1027com 1:CAS:528:DC%2BD38XovVCiur0%3D 12409316 (Pubitemid 35340354)
8. SB Berman FJ Pineda JM Hardwick 2008 Mitochondrial fission and fusion dynamics: the long and short of it Cell Death Differ 15 1147 1152 10.1038/cdd.2008.57 1:CAS:528:DC%2BD1cXntFOlsbY%3D 18437161 (Pubitemid 351850967)
9. T Tatsuta T Langer 2008 Quality control of mitochondria: protection against neurodegeneration and ageing EMBO J 27 306 314 10.1038/sj.emboj.7601972 1:CAS:528:DC%2BD1cXhtVKktLk%3D 18216873 (Pubitemid 351161660)
10. KA Rasbach RG Schnellmann 2007 Signaling of mitochondrial biogenesis following oxidant injury J Biol Chem 282 2355 2362 10.1074/jbc.M608009200 1:CAS:528:DC%2BD2sXmsVeisw%3D%3D 17116659 (Pubitemid 47076768)
11. G Lopez-Lluch N Hunt B Jones, et al. 2006 Calorie restriction induces mitochondrial biogenesis and bioenergetic efficiency Proc Natl Acad Sci USA 103 1768 1773 10.1073/pnas.0510452103 1:CAS:528:DC%2BD28Xhslehtrs%3D 16446459 (Pubitemid 43228768)
12. HY Cohen C Miller KJ Bitterman, et al. 2004 Calorie restriction promotes mammalian cell survival by inducing the SIRT1 deacetylase Science 305 390 392 10.1126/science.1099196 1:CAS:528:DC%2BD2cXls1egtrs%3D 15205477 (Pubitemid 38938153)
13. J St-Pierre S Drori M Uldry, et al. 2006 Suppression of reactive oxygen species and neurodegeneration by the PGC-1 transcriptional coactivators Cell 127 397 408 10.1016/j.cell.2006.09.024 1:CAS:528:DC%2BD28XhtFOkt7rM 17055439 (Pubitemid 44572377)
14. H Li Y Chen AF Jones, et al. 2008 Bcl-xL induces Drp1-dependent synapse formation in cultured hippocampal neurons Proc Natl Acad Sci USA 105 2169 2174 10.1073/pnas.0711647105 1:CAS:528:DC%2BD1cXitl2lsLw%3D 18250306
15. E Smirnova DL Shurland SN Ryazantsev AM van der Bliek 1998 A human dynamin-related protein controls the distribution of mitochondria J Cell Biol 143 351 358 10.1083/jcb.143.2.351 1:CAS:528:DyaK1cXmsl2gtLw%3D 9786947 (Pubitemid 28487855)
16. PP Zhu A Patterson J Stadler DP Seeburg M Sheng C Blackstone 2004 Intra- and intermolecular domain interactions of the C-terminal GTPase effector domain of the multimeric dynamin-like GTPase Drp1 J Biol Chem 279 35967 35974 10.1074/jbc.M404105200 1:CAS:528:DC%2BD2cXmsl2htLo%3D 15208300 (Pubitemid 39100604)
17. DI James PA Parone Y Mattenberger JC Martinou 2003 hFis1, a novel component of the mammalian mitochondrial fission machinery J Biol Chem 278 36373 36379 10.1074/jbc.M303758200 1:CAS:528:DC%2BD3sXnt1ejsL8%3D 12783892 (Pubitemid 37139965)
18. YJ Lee SY Jeong M Karbowski CL Smith RJ Youle 2004 Roles of the mammalian mitochondrial fission and fusion mediators Fis1, Drp1, and Opa1 in apoptosis Mol Biol Cell 15 5001 5011 10.1091/mbc.E04-04-0294 1:CAS:528: DC%2BD2cXpslKns7c%3D 15356267 (Pubitemid 39392214)
19. Y Yoon EW Krueger BJ Oswald MA McNiven 2003 The mitochondrial protein hFis1 regulates mitochondrial fission in mammalian cells through an interaction with the dynamin-like protein DLP1 Mol Cell Biol 23 5409 5420 10.1128/MCB.23.15.5409-5420.2003 1:CAS:528:DC%2BD3sXlslGms70%3D 12861026 (Pubitemid 36950895)
20. KA Sullivan JM Hayes TD Wiggin, et al. 2007 Mouse models of diabetic neuropathy Neurobiol Dis 28 276 285 10.1016/j.nbd.2007.07.022 1:CAS:528:DC%2BD2sXhtlGgsrzL 17804249 (Pubitemid 350116599)
21. J Mayfield 1998 Diagnosis and classification of diabetes mellitus: new criteria Am Fam Physician 58 1355 1370 1:STN:280:DyaK1M%2FitVSnsw%3D%3D 9803200
22. KA Sullivan JH Lillie DA Greene 1996 Digital electron microscopic analysis of regenerating axon clusters in human sural nerve biopsies Soc Neurosci Abstr 24 17 37
23. B Kim PS Leventhal AR Saltiel EL Feldman 1997 Insulin-like growth factor-I-mediated neurite outgrowth in vitro requires MAP kinase activation J Biol Chem 272 21268 21273 10.1074/jbc.272.34.21268 1:CAS:528:DyaK2sXls1OjtLc%3D 9261137 (Pubitemid 27373992)
24. B Kim SS Oh CM van Golen EL Feldman 2004 Differential regulation of insulin receptor substrate-1 degradation during mannitol and okadaic acid induced apoptosis in human neuroblastoma cells Cell Signal 17 769 775 10.1016/j.cellsig.2004.11.001 15722201
25. AM Vincent JW Russell P Low EL Feldman 2004 Oxidative stress in the pathogenesis of diabetic neuropathy Endocr Rev 25 612 628 10.1210/er.2003-0019 1:CAS:528:DC%2BD2cXns1Ght78%3D 15294884 (Pubitemid 39096072)
26. TD Wiggin M Kretzler S Pennathur KA Sullivan FC Brosius EL Feldman 2008 Rosiglitazone treatment reduces diabetic neuropathy in STZ treated DBA/2 J mice Endocrinology 149 4928 4937 10.1210/en.2008-0869 1:CAS:528:DC%2BD1cXhtF2gtbnE 18583417
27. FC Howarth M Jacobson M Shafiullah E Adeghate 2005 Long-term effects of streptozotocin-induced diabetes on the electrocardiogram, physical activity and body temperature in rats Exp Physiol 90 827 835 10.1113/expphysiol.2005.031252 1:STN:280:DC%2BD2Mrps1SksQ%3D%3D 16091403 (Pubitemid 41659553)
28. KA Sullivan SI Lentz JL Roberts Jr EL Feldman 2008 Criteria for creating and assessing mouse models of diabetic neuropathy Curr Drug Targets 9 3 13 10.2174/138945008783431763 1:CAS:528:DC%2BD1cXisFSnsbw%3D 18220709 (Pubitemid 351201677)
29. KA Mattingly MM Ivanova KA Riggs NS Wickramasinghe MJ Barch CM Klinge 2008 Estradiol stimulates transcription of nuclear respiratory factor-1 and increases mitochondrial biogenesis Mol Endocrinol 22 609 622 10.1210/me.2007-0029 1:CAS:528:DC%2BD1cXis12ns78%3D 18048642
30. CJ Lelliott A Ljungberg A Ahnmark, et al. 2007 Hepatic PGC-1beta overexpression induces combined hyperlipidemia and modulates the response to PPARalpha activation Arterioscler Thromb Vasc Biol 27 2707 2713 10.1161/ATVBAHA.107.155739 1:CAS:528:DC%2BD2sXhtlahtLjM 17932310 (Pubitemid 350158926)
31. MG Sun J Williams C Munoz-Pinedo, et al. 2007 Correlated three-dimensional light and electron microscopy reveals transformation of mitochondria during apoptosis Nat Cell Biol 9 1057 1065 10.1038/ncb1630 1:CAS:528:DC%2BD2sXpslGju70%3D 17721514 (Pubitemid 47628238)
32. S Frank B Gaume ES Bergmann-Leitner, et al. 2001 The role of dynamin-related protein 1, a mediator of mitochondrial fission, in apoptosis Dev Cell 1 515 525 10.1016/S1534-5807(01)00055-7 1:CAS:528:DC%2BD3MXotVSntLk%3D 11703942 (Pubitemid 33586103)
33. M Karbowski YJ Lee B Gaume, et al. 2002 Spatial and temporal association of Bax with mitochondrial fission sites, Drp1, and Mfn2 during apoptosis J Cell Biol 159 931 938 10.1083/jcb.200209124 1:CAS:528:DC%2BD3sXjt1ai 12499352 (Pubitemid 36055748)
34. A Cassidy-Stone JE Chipuk E Ingerman, et al. 2008 Chemical inhibition of the mitochondrial division dynamin reveals its role in Bax/Bak-dependent mitochondrial outer membrane permeabilization Dev Cell 14 193 204 10.1016/j.devcel.2007.11.019 1:CAS:528:DC%2BD1cXit1Ojs7w%3D 18267088 (Pubitemid 351189177)
35. AM Powelka A Seth JV Virbasius, et al. 2006 Suppression of oxidative metabolism and mitochondrial biogenesis by the transcriptional corepressor RIP140 in mouse adipocytes J Clin Invest 116 125 136 10.1172/JCI26040 1:CAS:528:DC%2BD28XjslOhsA%3D%3D 16374519 (Pubitemid 43121797)
36. DW Haden HB Suliman MS Carraway, et al. 2007 Mitochondrial biogenesis restores oxidative metabolism during Staphylococcus aureus sepsis Am J Respir Crit Care Med 176 768 777 10.1164/rccm.200701-161OC 1:CAS:528:DC%2BD2sXhtleru77K 17600279 (Pubitemid 47598478)
37. I Bogacka B Ukropcova M McNeil JM Gimble SR Smith 2005 Structural and functional consequences of mitochondrial biogenesis in human adipocytes in vitro J Clin Endocrinol Metab 90 6650 6656 10.1210/jc.2005-1024 1:CAS:528: DC%2BD2MXhtlaltLrL 16204368 (Pubitemid 41759328)
38. S Ghosh N Patel D Rahn, et al. 2007 The thiazolidinedione pioglitazone alters mitochondrial function in human neuron-like cells Mol Pharmacol 71 1695 1702 10.1124/mol.106.033845 1:CAS:528:DC%2BD2sXmt1Wqtbc%3D 17387142 (Pubitemid 47010922)
39. D Kukidome T Nishikawa K Sonoda, et al. 2006 Activation of AMP-activated protein kinase reduces hyperglycemia-induced mitochondrial reactive oxygen species production and promotes mitochondrial biogenesis in human umbilical vein endothelial cells Diabetes 55 120 127 10.2337/diabetes.55.01.06.db05-0943 1:CAS:528:DC%2BD28XlvVSltg%3D%3D 16380484
40. Z Li K Okamoto Y Hayashi M Sheng 2004 The importance of dendritic mitochondria in the morphogenesis and plasticity of spines and synapses Cell 119 873 887 10.1016/j.cell.2004.11.003 1:CAS:528:DC%2BD2MXmsF2n 15607982 (Pubitemid 40017692)
41. A Tinari T Garofalo M Sorice MD Esposti W Malorni 2007 Mitoptosis: different pathways for mitochondrial execution Autophagy 3 282 284 17329965
42. AM James MP Murphy 2002 How mitochondrial damage affects cell function J Biomed Sci 9 475 487 10.1007/BF02254975 1:CAS:528:DC%2BD38XnslWqsbw%3D 12372986
43. M Brownlee 2001 Biochemistry and molecular cell biology of diabetic complications Nature 414 813 820 10.1038/414813a 1:CAS:528: DC%2BD38Xhtlyltg%3D%3D 11742414 (Pubitemid 34000785)
44. HC Lee YH Wei 2005 Mitochondrial biogenesis and mitochondrial DNA maintenance of mammalian cells under oxidative stress Int J Biochem Cell Biol 37 822 834 10.1016/j.biocel.2004.09.010 1:CAS:528:DC%2BD2MXhtVKisbw%3D 15694841 (Pubitemid 40203003)
45. X Wang B Su HG Lee, et al. 2009 Impaired balance of mitochondrial fission and fusion in Alzheimer's disease J Neurosci 29 9090 9103 10.1523/JNEUROSCI. 1357-09.2009 1:CAS:528:DC%2BD1MXovFegu78%3D 19605646
46. C Alexander M Votruba UE Pesch, et al. 2000 OPA1, encoding a dynamin-related GTPase, is mutated in autosomal dominant optic atrophy linked to chromosome 3q28 Nat Genet 26 211 215 10.1038/79944 1:CAS:528: DC%2BD3cXntlGmsL4%3D 11017080 (Pubitemid 30764506)
47. S Bette H Schlaszus B Wissinger R Meyermann M Mittelbronn 2005 OPA1, associated with autosomal dominant optic atrophy, is widely expressed in the human brain Acta Neuropathol 109 393 399 10.1007/s00401-004-0970-8 1:CAS:528:DC%2BD2MXjvF2nt7c%3D 15700187 (Pubitemid 40637312)
48. A Santel S Frank 2008 Shaping mitochondria: the complex posttranslational regulation of the mitochondrial fission protein DRP1 IUBMB Life 60 448 455 10.1002/iub.71 1:CAS:528:DC%2BD1cXhtlKqu7rJ 18465792
49. T Uo J Dworzak C Kinoshita, et al. 2009 Drp1 levels constitutively regulate mitochondrial dynamics and cell survival in cortical neurons Exp Neurol 218 274 285 10.1016/j.expneurol.2009.05.010 1:CAS:528:DC%2BD1MXosVWlt7o%3D 19445933
50. C Figueroa-Romero JA Iniguez-Lluhi J Standler, et al. 2009 SUMOylation of the mitochondrial fission protein Drp1 occurs at multiple nonconsensus sites with the B domain and is linked to its activity cycle FASEB J 10.1096/fj.09-136630 19638400