The Gdap1 knockout mouse mechanistically links redox control to Charcot-Marie-tooth disease

Brain

Volumn 137, Issue 3, 2014, Pages 668-682

  Niemann, Axel ^a   Huber, Nina ^a   Wagner, Konstanze M ^a   Somandin, Christian ^a   Horn, Michael ^a   Lebrun Julien, Frédéric ^a   Angst, Brigitte ^a   Pereira, Jorge A ^a   Halfter, Hartmut ^b   Welzl, Hans ^c   Feltri, M Laura ^d   Wrabetz, Lawrence ^d   Young, Peter ^b   Wessig, Carsten ^e   Toyka, Klaus V ^e   Suter, Ueli ^a  

^a ETH ZURICH   (Switzerland)

^b UNIVERSITY OF MÜNSTER   (Germany)

^c UNIVERSITY OF ZURICH   (Switzerland)

^d UNIVERSITY AT BUFFALO   (United States)

^e UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

animal models; axonal transport; Charcot Marie Tooth disease; demyelinating disease; mitochondria

Indexed keywords

GANGLIOSIDE; GANGLIOSIDE INDUCED DIFFERENTIATION ASSOCIATED PROTEIN 1; GDAP1L1 PROTEIN; GLUTATHIONE DISULFIDE; MEMBRANE PROTEIN; MITOCHONDRIAL DNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOGENESIS; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; CYTOLOGY; EMBRYO; GENE LOSS; GENE MUTATION; HEREDITARY MOTOR SENSORY NEUROPATHY; KNOCKOUT MOUSE; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; MOLECULAR DYNAMICS; MORPHOLOGY; MOUSE; NERVE CELL; NONHUMAN; OUTER MEMBRANE; OXIDATIVE STRESS; PARALOGY; PERIPHERAL NERVOUS SYSTEM; PERIPHERAL NEUROPATHY; PHENOTYPE; PRIORITY JOURNAL; SCHWANN CELL; SPINAL CORD;

ANIMAL MODELS; AXONAL TRANSPORT; CHARCOT-MARIE-TOOTH DISEASE; DEMYELINATING DISEASE; MITOCHONDRIA;

ANIMALS; AXONS; CELLS, CULTURED; CHARCOT-MARIE-TOOTH DISEASE; DISEASE MODELS, ANIMAL; DNA, MITOCHONDRIAL; GLUTATHIONE; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; MITOCHONDRIA; NERVE TISSUE PROTEINS; OXIDATION-REDUCTION; OXIDATIVE STRESS; PHENOTYPE;

EID: 84894572580     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awt371     Document Type: Article

References (58)

1. Arber S, Han B, Mendelsohn M, Smith M, Jessell TM, Sockanathan S. Requirement for the homeobox gene Hb9 in the consolidation of motor neuron identity. Neuron 1999; 23: 659-74.
2. Baloh RH. Mitochondrial dynamics and peripheral neuropathy. Neuroscientist 2008; 14: 12-8.
3. Baloh RH, Schmidt RE, Pestronk A, Milbrandt J. Altered axonal mitochondrial transport in the pathogenesis of Charcot-Marie-Tooth disease from mitofusin 2 mutations. J Neurosci 2007; 27: 422-30.
4. Berger P, Niemann A, Suter U. Schwann cells and the pathogenesis of inherited motor and sensory neuropathies (Charcot-Marie-Tooth disease). Glia 2006; 54: 243-57.
5. Bogdanik LP, Sleigh JN, Tian C, Samuels ME, Bedard K, Seburn KL, et al. Loss of the E3 ubiquitin ligase LRSAM1 sensitizes peripheral axons to degeneration in a mouse model of Charcot-Marie-Tooth disease. Dis Model Mech 2013; 6: 780-92.
6. Bossy-Wetzel E, Barsoum MJ, Godzik A, Schwarzenbacher R, Lipton SA. Mitochondrial fission in apoptosis, neurodegeneration and aging. Curr Opin Cell Biol 2003; 15: 706-16.
7. Boyer O, Nevo F, Plaisier E, Funalot B, Gribouval O, Benoit G, et al. INF2 mutations in Charcot-Marie-Tooth disease with glomerulopathy. N Engl J Med 2011; 365: 2377-88.
8. Cartoni R, Arnaud E, Medard JJ, Poirot O, Courvoisier DS, Chrast R, et al. Expression of mitofusin 2(R94Q) in a transgenic mouse leads to Charcot-Marie-Tooth neuropathy type 2A. Brain 2010; 133 (Pt 5): 1460-9.
9. Cassereau J, Chevrollier A, Bonneau D, Verny C, Procaccio V, Reynier P, et al. A locus-specific database for mutations in GDAP1 allows analysis of genotype-phenotype correlations in Charcot-Marie-Tooth diseases type 4A and 2K. Orphanet J Rare Dis 2011a; 6: 87.
10. Cassereau J, Chevrollier A, Gueguen N, Desquiret V, Verny C, Nicolas G, et al. Mitochondrial dysfunction and pathophysiology of Charcot-Marie-Tooth disease involving GDAP1 mutations. Exp Neurol 2011b; 227: 31-41.
11. Chan DC. Fusion and fission: interlinked processes critical for mitochondrial health. Annu Rev Genet 2012; 46: 265-87.
12. Chen H, Chan DC. Physiological functions of mitochondrial fusion. Ann N Y Acad Sci 2010; 1201: 21-5.
13. Ewaleifoh O, Trinh M, Griffin JW, Nguyen T. A novel system to accelerate the progression of nerve degeneration in transgenic mouse models of neuropathies. Exp Neurol 2012; 237: 153-9.
14. Feltri ML, D'Antonio M, Previtali S, Fasolini M, Messing A, Wrabetz L. P0-Cre transgenic mice for inactivation of adhesion molecules in Schwann cells. Ann N Y Acad Sci 1999; 883: 116-23.
15. Feltri ML, D'Antonio M, Previtali S, Fasolini M, Messing A, Wrabetz L. Conditional disruption of beta 1 integrin in Schwann cells impedes interactions with axons. J Cell Biol 2002; 170: 199-206.
16. Gillespie CS, Sherman DL, Fleetwood-Walker SM, Cottrell DF, Tait S, Garry EM, et al. Peripheral demyelination and neuropathic pain behavior in periaxin-deficient mice. Neuron 2000; 26: 523-31.
17. Horn M, Baumann R, Pereira JA, Sidiropoulos PN, Somandin C, Welzl H, et al. Myelin is dependent on the Charcot-Marie-Tooth Type 4H disease culprit protein FRABIN/FGD4 in Schwann cells. Brain 2012; 135 (Pt 12): 3567-83.
18. Huber N, Guimaraes S, Schrader M, Suter U, Niemann A. Charcot-Marie-Tooth disease-associated mutants of GDAP1 dissociate its roles in peroxisomal and mitochondrial fission. EMBO Rep 2013; 14: 545-52.
19. Ishihara N, Nomura M, Jofuku A, Kato H, Suzuki SO, Masuda K, et al. Mitochondrial fission factor Drp1 is essential for embryonic development and synapse formation in mice. Nat Cell Biol 2009; 11: 958-66.
20. Kabzinska D, Niemann A, Drac H, Huber N, Potulska-Chromik A, Hausmanowa-Petrusewicz I, et al. A new missense GDAP1 mutation disturbing targeting to the mitochondrial membrane causes a severe form of AR-CMT2C disease. Neurogenetics 2011; 12: 145-53.
21. Karbowski M, Norris KL, Cleland MM, Jeong SY, Youle RJ. Role of Bax and Bak in mitochondrial morphogenesis. Nature 2006; 443: 658-62.
22. Korobova F, Ramabhadran V, Higgs HN. An actin-dependent step in mitochondrial fission mediated by the ER-associated formin INF2.Science 2013; 339: 464-7.
23. Lee HC, Wei YH. Mitochondrial biogenesis and mitochondrial DNA maintenance of mammalian cells under oxidative stress. Int J Biochem Cell Biol 2005; 37: 822-34.
24. Li Q, Vande Velde C, Israelson A, Xie J, Bailey AO, Dong MQ, et al. ALS-linked mutant superoxide dismutase 1 (SOD1) alters mitochondrial protein composition and decreases protein import. Proc Natl Acad Sci USA 2010; 107: 21146-51.
25. Malik AN, Czajka A. Is mitochondrial DNA content a potential biomarker of mitochondrial dysfunction? Mitochondrion 2013; 13: 481-92.
26. Marco A, Cuesta A, Pedrola L, Palau F, Marin I. Evolutionary and structural analyses of GDAP1, Involved in Charcot-Marie-Tooth disease, characterize a novel class of glutathione transferase-related genes. Mol Biol Evol 2004; 21: 176-87.
27. Martini R. Animal models for inherited peripheral neuropathies: chances to find treatment strategies? J Neurosci Res 2000; 61: 244-50.
28. Meyer Zu Horste G, Nave KA. Animal models of inherited neuropathies. Curr Opin Neurol 2006; 19: 464-73.
29. Misko A, Jiang S, Wegorzewska I, Milbrandt J, Baloh RH. Mitofusin 2 is necessary for transport of axonal mitochondria and interacts with the Miro/Milton complex. J Neurosci 2010; 30: 4232-40.
30. Moreno-Loshuertos R, Acin-Perez R, Fernandez-Silva P, Movilla N, Perez-Martos A, Rodriguez de Cordoba S, et al. Differences in reactive oxygen species production explain the phenotypes associated with common mouse mitochondrial DNA variants. Nat Genet 2006; 38: 1261-8.
31. Murphy MP. Modulating mitochondrial intracellular location as a redox signal. Sci Signal 2012; 5: pe39.
32. Muyderman H, Hutson PG, Matusica D, Rogers ML, Rush RA. The human G93A-superoxide dismutase-1 mutation, mitochondrial glutathione and apoptotic cell death. Neurochem Res 2009; 34: 1847-56.
33. Niemann A, Berger P, Suter U. Pathomechanisms of mutant proteins in Charcot-Marie-Tooth disease. Neuromolecular Med 2006; 8: 217-42.
34. Niemann A, Ruegg M, La Padula V, Schenone A, Suter U. Gangliosideinduced differentiation associated protein 1 is a regulator of the mitochondrial network: new implications for Charcot-Marie-Tooth disease. J Cell Biol 2005; 170: 1067-78.
35. Niemann A, Wagner KM, Ruegg M, Suter U. GDAP1 mutations differ in their effects on mitochondrial dynamics and apoptosis depending on the mode of inheritance. Neurobiol Dis 2009; 36: 509-20.
36. Noack R, Frede S, Albrecht P, Henke N, Pfeiffer A, Knoll K, et al. Charcot-Marie-Tooth disease CMT4A: GDAP1 increases cellular glutathione and the mitochondrial membrane potential. Hum Mol Genet 2012; 21: 150-62.
37. Parone PA, Da Cruz S, Tondera D, Mattenberger Y, James DI, Maechler P, et al. Preventing mitochondrial fission impairs mitochondrial function and leads to loss of mitochondrial DNA. PLoS One 2008; 3: e3257.
38. Pedrola L, Espert A, Valdes-Sanchez T, Sanchez-Piris M, Sirkowski EE, Scherer SS, et al. Cell expression of GDAP1 in the nervous system and pathogenesis of Charcot-Marie-Tooth type 4A disease. J Cell Mol Med 2008; 12: 679-89.
39. Pedrola L, Espert A, Wu X, Claramunt R, Shy ME, Palau F. GDAP1, the protein causing Charcot-Marie-Tooth disease type 4A, is expressed in neurons and is associated with mitochondria. Hum Mol Genet 2005; 14: 1087-94.
40. Pla-Martin D, Rueda CB, Estela A, Sanchez-Piris M, Gonzalez-Sanchez P, Traba J, et al. Silencing of the Charcot-Marie-Tooth disease-associated gene GDAP1 induces abnormal mitochondrial distribution and affects Ca homeostasis by reducing store-operated Ca entry. Neurobiol Dis 2013; 55: 140-51.
41. Ramabhadran V, Gurel PS, Higgs HN. Mutations to the formin homology 2 domain of INF2 protein have unexpected effects on actin polymerization and severing. J Biol Chem 2012; 287: 34234-45.
42. Robertson J, Kriz J, Nguyen MD, Julien JP. Pathways to motor neuron degeneration in transgenic mouse models. Biochimie 2002; 84: 1151-60.
43. Ryan MT, Stojanovski D. Mitofusins 'bridge' the gap between oxidative stress and mitochondrial hyperfusion. EMBO Rep 2012; 13: 870-1.
44. Scarpulla RC, Vega RB, Kelly DP. Transcriptional integration of mitochondrial biogenesis. Trends Endocrinol Metab 2012; 23: 459-66.
45. Shield AJ, Murray TP, Board PG. Functional characterisation of ganglioside-induced differentiation-associated protein 1 as a glutathione transferase. Biochem Biophys Res Commun 2006; 347: 859-66.
46. Shutt T, Geoffrion M, Milne R, McBride HM. The intracellular redox state is a core determinant of mitochondrial fusion. EMBO Rep 2012; 13: 909-15.
47. Shy ME, Balsamo J, Lilien J, Kamholz J. A molecular basis for hereditary motor and sensory neuropathy disorders. Curr Neurol Neurosci Rep 2001; 1: 77-88.
48. Skre H. Genetic and clinical aspects of Charcot-Marie-Tooth's disease. Clin Genet 1974; 6: 98-118.
49. Somandin C, Gerber D, Pereira JA, Horn M, Suter U. LITAF (SIMPLE) regulates Wallerian degeneration after injury but is not essential for peripheral nerve development and maintenance: implications for Charcot-Marie-Tooth disease. Glia 2012; 60: 1518-28.
50. Suter U, Scherer SS. Disease mechanisms in inherited neuropathies. Nature Rev Neurosci 2003; 4: 714-29.
51. Townsend DM, Tew KD, Tapiero H. The importance of glutathione in human disease. Biomed Pharmacother 2003; 57: 145-55.
52. Vital A, Vital C. Mitochondria and peripheral neuropathies. J Neuropathol Exp Neurol 2012; 71: 1036-46.
53. Wagner KM, Ruegg M, Niemann A, Suter U. Targeting and function of the mitochondrial fission factor GDAP1 are dependent on its tailanchor. PLoS One 2009; 4: e5160.
54. Watanabe N, Dickinson DA, Liu RM, Forman HJ. Quinones and glutathione metabolism. Methods Enzymol 2004; 378: 319-40.
55. Youle RJ, van der Bliek AM. Mitochondrial fission, fusion, and stress. Science 2012; 337: 1062-5.
56. Zimon M, Baets J, Fabrizi GM, Jaakkola E, Kabzinska D, Pilch J, et al. Dominant GDAP1 mutations cause predominantly mild CMT phenotypes. Neurology 2011; 77: 540-8.
57. Zuchner S, Mersiyanova IV, Muglia M, Bissar-Tadmouri N, Rochelle J, Dadali EL, et al. Mutations in the mitochondrial GTPase mitofusin 2 cause Charcot-Marie-Tooth neuropathy type 2A. Nat Genet 2004; 36: 449-51.
58. Zuchner S, Vance JM. Molecular genetics of autosomal-dominant axonal Charcot-Marie-Tooth disease. Neuromolecular Med 2006; 8: 63-74.