Inherited peripheral neuropathies due to mitochondrial disorders

Revue Neurologique

Volumn 170, Issue 5, 2014, Pages 366-374

  Cassereau, J ^a,b,c   Codron, P ^a   Funalot, B ^d,e  

^a ANGERS UNIVERSITY HOSPITAL   (France)

^b CNRS   (France)

^c INSERM   (France)

^d LIMOGES UNIVERSITY HOSPITAL   (France)

^e UNIVERSITY OF LIMOGES   (France)

Author keywords

Bioenergetics; Charcot Marie Tooth disease; Mitochondrial disorders; Mitochondrial DNA; Multisystem disease; Peripheral neuropathies; Polymerase gamma

Indexed keywords

DYNEIN HEAVY CHAIN 1; HEAT SHOCK PROTEIN; KINESIN FAMILY MEMBER 1B; MITOCHONDRIAL DNA; MITOCHONDRIAL PROTEIN; MITOFUSIN 2; PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BIOENERGY; CHRONIC PROGRESSIVE EXTERNAL OPHTHALMOPLEGIA; CLINICAL FEATURE; COWCHOCKS SYNDROME; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DYNC1H1 GENE; GDAP1 GENE; GENE; GENE DELETION; GENE DUPLICATION; GENE MUTATION; HEREDITARY MOTOR SENSORY NEUROPATHY; HUMAN; INFANTILE ONSET SPINOCEREBELLAR ATAXIA; INHERITANCE; KEARNS SAYRE SYNDROME; KIF1B GENE; LEIGH DISEASE; MATERNALLY INHERITED LEIGH SYNDROME; MELAS SYNDROME; MERRF SYNDROME; MFN2 GENE; MITOCHONDRIAL DNA DISORDER; MITOCHONDRIAL DYNAMICS; MNGIE SYNDROME; NARP SYNDROME; NAVAJO NEUROHEPATOPATHY; PERIPHERAL NEUROPATHY; PHENOTYPE; POINT MUTATION; RISK FACTOR; CELL NUCLEUS; COMPLICATION; GENETICS; METABOLISM; MITOCHONDRION; MUTATION; NERVE FIBER TRANSPORT; PATHOPHYSIOLOGY; PERIPHERAL NERVOUS SYSTEM DISEASES; PHYSIOLOGY;

AXONAL TRANSPORT; CELL NUCLEUS; DNA, MITOCHONDRIAL; HUMANS; MITOCHONDRIA; MITOCHONDRIAL DISEASES; MUTATION; PERIPHERAL NERVOUS SYSTEM DISEASES;

EID: 84901197711     PISSN: 00353787     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neurol.2013.11.005     Document Type: Article

References (70)

1. R.A. Capaldi, D.G. Halphen, Y.Z. Zhang, and W. Yanamura Complexity and tissue specificity of the mitochondrial respiratory chain J Bioenerg Biomembr 20 1988 291 311
2. D.C. Chan Mitochondrial fusion and fission in mammals Annu Rev Cell Dev Biol 22 2006 79 99
3. M. Rojo, F. Legros, D. Chateau, and A. Lombes Membrane topology and mitochondrial targeting of mitofusins, ubiquitous mammalian homologs of the transmembrane GTPase Fzo J Cell Sci 115 2002 1663 1674
4. S.A. Detmer, and D.C. Chan Functions and dysfunctions of mitochondrial dynamics Nat Rev Mol Cell Biol 8 2007 870 879
5. G. Benard, N. Bellance, D. James, P. Parrone, H. Fernandez, and T. Letellier et al. Mitochondrial bioenergetics and structural network organization J Cell Sci 120 2007 838 848
6. J.P. Caviston, and E.L. Holzbaur Microtubule motors at the intersection of trafficking and transport Trends Cell Biol 16 2006 530 537
7. N. Hirokawa, and R. Takemura Molecular motors in neuronal development, intracellular transport and diseases Curr Opin Neurobiol 14 2004 564 573
8. S. Cipolat, O. Martins de Brito, B. Dal Zilio, and L. Scorrano OPA1 requires mitofusin 1 to promote mitochondrial fusion Proc Natl Acad Sci U S A 101 2004 15927 15932
9. A. Olichon, L. Baricault, N. Gas, E. Guillou, A. Valette, and P. Belenguer et al. Loss of OPA1 perturbates the mitochondrial inner membrane structure and integrity, leading to cytochrome c release and apoptosis J Biol Chem 278 2003 7743 7746
10. E. Ingerman, E.M. Perkins, M. Marino, J.A. Mears, J.M. McCaffery, and J.E. Hinshaw et al. Dnm1 forms spirals that are structurally tailored to fit mitochondria J Cell Biol 170 2005 1021 1027
11. A. Niemann, M. Ruegg, V. La Padula, A. Schenone, and U. Suter Ganglioside-induced differentiation associated protein 1 is a regulator of the mitochondrial network: new implications for Charcot-Marie-Tooth disease J Cell Biol 170 2005 1067 1078
12. A. Niemann, K.M. Wagner, M. Ruegg, and U. Suter GDAP1 mutations differ in their effects on mitochondrial dynamics and apoptosis depending on the mode of inheritance Neurobiol Dis 36 2009 509 520
13. J.M. Shoffner, M.T. Lott, A.M. Lezza, P. Seibel, S.W. Ballinger, and D.C. Wallace Myoclonic epilepsy and ragged-red fiber disease (MERRF) is associated with a mitochondrial DNA tRNA(Lys) mutation Cell 61 1990 931 937
14. N. Fukuhara, S. Tokiguchi, K. Shirakawa, and T. Tsubaki Myoclonus epilepsy associated with ragged-red fibres (mitochondrial abnormalities): disease entity or a syndrome? Light-and electron-microscopic studies of two cases and review of literature J Neurol Sci 47 1980 117 133
15. Y. Goto, I. Nonaka, and S. Horai A mutation in the tRNA(Leu)(UUR) gene associated with the MELAS subgroup of mitochondrial encephalomyopathies Nature 348 1990 651 653
16. Y. Kobayashi, M.Y. Momoi, K. Tominaga, T. Momoi, K. Nihei, and M. Yanagisawa et al. A point mutation in the mitochondrial tRNA(Leu)(UUR) gene in MELAS (mitochondrial myopathy, encephalopathy, lactic acidosis and stroke-like episodes) Biochem Biophys Res Commun 173 1990 816 822
17. S.G. Pavlakis, P.C. Phillips, S. DiMauro, D.C. De Vivo, and L.P. Rowland Mitochondrial myopathy, encephalopathy, lactic acidosis, and strokelike episodes: a distinctive clinical syndrome Ann Neurol 16 1984 481 488
18. H. Rusanen, K. Majamaa, U. Tolonen, A.M. Remes, R. Myllyla, and I.E. Hassinen Demyelinating polyneuropathy in a patient with the tRNA(Leu)(UUR) mutation at base pair 3243 of the mitochondrial DNA Neurology 45 1995 1188 1192
19. I.J. Holt, A.E. Harding, R.K. Petty, and J.A. Morgan-Hughes A new mitochondrial disease associated with mitochondrial DNA heteroplasmy Am J Hum Genet 46 1990 428 433
20. J.M. Gelfand, J.L. Duncan, C.A. Racine, L.A. Gillum, C.T. Chin, and Y. Zhang et al. Heterogeneous patterns of tissue injury in NARP syndrome J Neurol 258 2011 440 448
21. D.D. de Vries, B.G. van Engelen, F.J. Gabreels, W. Ruitenbeek, and B.A. van Oost A second missense mutation in the mitochondrial ATPase 6 gene in Leigh's syndrome Ann Neurol 34 1993 410 412
22. F.M. Santorelli, S. Shanske, A. Macaya, D.C. DeVivo, and S. DiMauro The mutation at nt 8993 of mitochondrial DNA is a common cause of Leigh's syndrome Ann Neurol 34 1993 827 834
23. D. Leigh Subacute necrotizing encephalomyelopathy in an infant J Neurol Neurosurg Psychiatry 14 1951 216 221
24. R.D. Pitceathly, S.M. Murphy, E. Cottenie, A. Chalasani, M.G. Sweeney, and C. Woodward et al. Genetic dysfunction of MT-ATP6 causes axonal Charcot-Marie-Tooth disease Neurology 79 2012 1145 1154
25. P. Luoma, A. Melberg, J.O. Rinne, J.A. Kaukonen, N.N. Nupponen, and R.M. Chalmers et al. Parkinsonism, premature menopause, and mitochondrial DNA polymerase gamma mutations: clinical and molecular genetic study Lancet 364 2004 875 882
26. A. Melberg, P.O. Lundberg, K.G. Henriksson, Y. Olsson, and E. Stalberg Muscle-nerve involvement in autosomal dominant progressive external ophthalmoplegia with hypogonadism Muscle Nerve 19 1996 751 757
27. T.P. Kearns, and G.P. Sayre Retinitis pigmentosa, external ophthalmophegia, and complete heart block: unusual syndrome with histologic study in one of two cases AMA Arch Ophthalmol 60 1958 280 289
28. L. Santoro, R. Carrozzo, A. Malandrini, F. Piemonte, C. Patrono, and M. Villanova et al. A novel SURF1 mutation results in Leigh syndrome with peripheral neuropathy caused by cytochrome c oxidase deficiency Neuromuscul Disord 10 2000 450 453
29. A. Echaniz-Laguna, D. Ghezzi, M. Chassagne, M. Mayencon, S. Padet, and L. Melchionda et al. SURF1 deficiency causes demyelinating Charcot-Marie-Tooth disease Neurology 81 17 2013 1523 1530
30. M.L. Kennerson, E.M. Yiu, D.T. Chuang, A. Kidambi, S.C. Tso, and C. Ly et al. A new locus for X-linked dominant Charcot-Marie-Tooth disease (CMTX6) is caused by mutations in the pyruvate dehydrogenase kinase isoenzyme 3 (PDK3) gene Hum Mol Genet 22 2013 1404 1416
31. L.L. Williams Pyruvate oxidation in Charcot-Marie-Tooth disease Neurology 29 1979 1492 1498
32. C. Rinaldi, C. Grunseich, I.F. Sevrioukova, A. Schindler, I. Horkayne-Szakaly, and C. Lamperti et al. Cowchock syndrome is associated with a mutation in apoptosis-inducing factor Am J Hum Genet 91 2012 1095 1102
33. G. Van Goethem, B. Dermaut, A. Lofgren, J.J. Martin, and C. Van Broeckhoven Mutation of POLG is associated with progressive external ophthalmoplegia characterized by mtDNA deletions Nat Genet 28 2001 211 212
34. G. Hudson, and P.F. Chinnery Mitochondrial DNA polymerase-gamma and human disease Hum Mol Genet 15 Spec No. 2 2006 R244 R252
35. I. Nishino, A. Spinazzola, and M. Hirano Thymidine phosphorylase gene mutations in MNGIE, a human mitochondrial disorder Science 283 1999 689 692
36. M. Hirano, G. Silvestri, D.M. Blake, A. Lombes, C. Minetti, and E. Bonilla et al. Mitochondrial neurogastrointestinal encephalomyopathy (MNGIE): clinical, biochemical, and genetic features of an autosomal recessive mitochondrial disorder Neurology 44 1994 721 727
37. A.H. Hakonen, S. Goffart, S. Marjavaara, A. Paetau, H. Cooper, and K. Mattila et al. Infantile-onset spinocerebellar ataxia and mitochondrial recessive ataxia syndrome are associated with neuronal complex I defect and mtDNA depletion Hum Mol Genet 17 2008 3822 3835
38. O. Appenzeller, M. Kornfeld, and R. Snyder Acromutilating, paralyzing neuropathy with corneal ulceration in Navajo children Arch Neurol 33 1976 733 738
39. S. Holve, D. Hu, M. Shub, R.W. Tyson, and R.J. Sokol Liver disease in Navajo neuropathy J Pediatr 135 1999 482 493
40. C.L. Karadimas, T.H. Vu, S.A. Holve, P. Chronopoulou, C. Quinzii, and S.D. Johnsen et al. Navajo neurohepatopathy is caused by a mutation in the MPV17 gene Am J Hum Genet 79 2006 544 548
41. A. Spinazzola, C. Viscomi, E. Fernandez-Vizarra, F. Carrara, P. D'Adamo, and S. Calvo et al. MPV17 encodes an inner mitochondrial membrane protein and is mutated in infantile hepatic mitochondrial DNA depletion Nat Genet 38 2006 570 575
42. N. Ishihara, Y. Eura, and K. Mihara Mitofusin 1 and 2 play distinct roles in mitochondrial fusion reactions via GTPase activity J Cell Sci 117 2004 6535 6546
43. A. Misko, S. Jiang, I. Wegorzewska, J. Milbrandt, and R.H. Baloh Mitofusin 2 is necessary for transport of axonal mitochondria and interacts with the Miro/Milton complex J Neurosci 30 2010 4232 4240
44. O.M. de Brito, and L. Scorrano Mitofusin 2 tethers endoplasmic reticulum to mitochondria Nature 456 2008 605 610
45. R. Cartoni, E. Arnaud, J.J. Medard, O. Poirot, D.S. Courvoisier, and R. Chrast et al. Expression of mitofusin 2(R94Q) in a transgenic mouse leads to Charcot-Marie-Tooth neuropathy type 2A Brain 133 2010 1460 1469
46. V. Guillet, N. Gueguen, R. Cartoni, A. Chevrollier, V. Desquiret, and C. Angebault et al. Bioenergetic defect associated with mKATP channel opening in a mouse model carrying a mitofusin 2 mutation FASEB J 25 2011 1618 1627
47. C. Rouzier, S. Bannwarth, A. Chaussenot, A. Chevrollier, A. Verschueren, and N. Bonello-Palot et al. The MFN2 gene is responsible for mitochondrial DNA instability and optic atrophy 'plus' phenotype Brain 135 2012 23 34
48. R.H. Baloh, R.E. Schmidt, A. Pestronk, and J. Milbrandt Altered axonal mitochondrial transport in the pathogenesis of Charcot-Marie-Tooth disease from mitofusin 2 mutations J Neurosci 27 2007 422 430
49. J.M. Vallat, R.A. Ouvrier, J.D. Pollard, C. Magdelaine, D. Zhu, and G.A. Nicholson et al. Histopathological findings in hereditary motor and sensory neuropathy of axonal type with onset in early childhood associated with mitofusin 2 mutations J Neuropathol Exp Neurol 67 2008 1097 1102
50. K. Verhoeven, K.G. Claeys, S. Zuchner, J.M. Schroder, J. Weis, and C. Ceuterick et al. MFN2 mutation distribution and genotype/phenotype correlation in Charcot-Marie-Tooth type 2 Brain 129 2006 2093 2102
51. S. Zuchner, I.V. Mersiyanova, M. Muglia, N. Bissar-Tadmouri, J. Rochelle, and E.L. Dadali et al. Mutations in the mitochondrial GTPase mitofusin 2 cause Charcot-Marie-Tooth neuropathy type 2A Nat Genet 36 2004 449 451
52. J.M. Polke, M. Laura, D. Pareyson, F. Taroni, M. Milani, and G. Bergamin et al. Recessive axonal Charcot-Marie-Tooth disease due to compound heterozygous mitofusin 2 mutations Neurology 77 2011 168 173
53. G.A. Nicholson, C. Magdelaine, D. Zhu, S. Grew, M.M. Ryan, and F. Sturtz et al. Severe early-onset axonal neuropathy with homozygous and compound heterozygous MFN2 mutations Neurology 70 2008 1678 1681
54. K.W. Chung, S.B. Kim, K.D. Park, K.G. Choi, J.H. Lee, and H.W. Eun et al. Early onset severe and late-onset mild Charcot-Marie-Tooth disease with mitofusin 2 (MFN2) mutations Brain 129 2006 2103 2118
55. S. Vucic, M. Kennerson, D. Zhu, E. Miedema, C. Kok, and G.A. Nicholson CMT with pyramidal features. Charcot-Marie-Tooth Neurology 60 2003 696 699
56. S. Zuchner, P. De Jonghe, A. Jordanova, K.G. Claeys, V. Guergueltcheva, and S. Cherninkova et al. Axonal neuropathy with optic atrophy is caused by mutations in mitofusin 2 Ann Neurol 59 2006 276 281
57. A. Estela, D. Pla-Martin, M. Sanchez-Piris, H. Sesaki, and F. Palau Charcot-Marie-Tooth-related gene GDAP1 complements cell cycle delay at G2/M phase in Saccharomyces cerevisiae fis1 gene-defective cells J Biol Chem 286 2011 36777 36786
58. J. Cassereau, A. Chevrollier, N. Gueguen, M.C. Malinge, F. Letournel, and G. Nicolas et al. Mitochondrial complex I deficiency in GDAP1-related autosomal dominant Charcot-Marie-Tooth disease (CMT2K) Neurogenetics 10 2009 145 150
59. R. Noack, S. Frede, P. Albrecht, N. Henke, A. Pfeiffer, and K. Knoll et al. Charcot-Marie-Tooth disease CMT4A: GDAP1 increases cellular glutathione and the mitochondrial membrane potential Hum Mol Genet 21 2012 150 162
60. J. Cassereau, A. Chevrollier, N. Gueguen, V. Desquiret, C. Verny, and G. Nicolas et al. Mitochondrial dysfunction and pathophysiology of Charcot-Marie-Tooth disease involving GDAP1 mutations Exp Neurol 227 2011 31 41
61. S. Ackerley, P.A. James, A. Kalli, S. French, K.E. Davies, and K. Talbot A mutation in the small heat-shock protein HSPB1 leading to distal hereditary motor neuronopathy disrupts neurofilament assembly and the axonal transport of specific cellular cargoes Hum Mol Genet 15 2006 347 354
62. O.V. Evgrafov, I. Mersiyanova, J. Irobi, L. Van Den Bosch, I. Dierick, and C.L. Leung et al. Mutant small heat-shock protein 27 causes axonal Charcot-Marie-Tooth disease and distal hereditary motor neuropathy Nat Genet 36 2004 602 606
63. J. Irobi, K. Van Impe, P. Seeman, A. Jordanova, I. Dierick, and N. Verpoorten et al. Hot-spot residue in small heat-shock protein 22 causes distal motor neuropathy Nat Genet 36 2004 597 601
64. C. d'Ydewalle, J. Krishnan, D.M. Chiheb, P. Van Damme, J. Irobi, and A.P. Kozikowski et al. HDAC6 inhibitors reverse axonal loss in a mouse model of mutant HSPB1-induced Charcot-Marie-Tooth disease Nat Med 17 2011 968 974
65. C. Zhao, J. Takita, Y. Tanaka, M. Setou, T. Nakagawa, and S. Takeda et al. Charcot-Marie-Tooth disease type 2A caused by mutation in a microtubule motor KIF1Bbeta Cell 105 2001 587 597
66. M.N. Weedon, R. Hastings, R. Caswell, W. Xie, K. Paszkiewicz, and T. Antoniadi et al. Exome sequencing identifies a DYNC1H1 mutation in a large pedigree with dominant axonal Charcot-Marie-Tooth disease Am J Hum Genet 89 2011 308 312
67. X.J. Chen, E.N. Levedakou, K.J. Millen, R.L. Wollmann, B. Soliven, and B. Popko Proprioceptive sensory neuropathy in mice with a mutation in the cytoplasmic Dynein heavy chain 1 gene J Neurosci 27 2007 14515 14524
68. S.L. Courchesne, M.F. Pazyra-Murphy, D.J. Lee, and R.A. Segal Neuromuscular junction defects in mice with mutation of dynein heavy chain 1 PloS One 6 2011 e16753
69. T. Hulgan, D.W. Haas, J.L. Haines, M.D. Ritchie, G.K. Robbins, and R.W. Shafer et al. Mitochondrial haplogroups and peripheral neuropathy during antiretroviral therapy: an adult AIDS clinical trials group study AIDS 19 2005 1341 1349
70. P. Fernyhough, T.J. Huang, and A. Verkhratsky Mechanism of mitochondrial dysfunction in diabetic sensory neuropathy J Peripher Nerv Syst 8 2003 227 235