Peripheral neuropathy in mitochondrial disorders

The Lancet Neurology

Volumn 12, Issue 10, 2013, Pages 1011-1024

  Pareyson, Davide ^a   Piscosquito, Giuseppe ^a   Moroni, Isabella ^b   Salsano, Ettore ^a   Zeviani, Massimo ^c,d,e  

^a Department of Clinical Neurosciences   (Italy)

^b Neurology Unit   (Italy)

^c Unit of Molecular Neurogenetics   (Italy)

^d DEPARTMENT OF NEUROSURGERY   (Italy)

^e UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA TOCOPHEROL; ASCORBIC ACID; IDEBENONE; MITOCHONDRIAL DNA; MITOFUSIN 2; RIBOFLAVIN; THIAMINE; UBIDECARENONE;

ALLOGENEIC HEMATOPOIETIC STEM CELL TRANSPLANTATION; BABINSKI REFLEX; CHROMOSOME 1P; DISORDERS OF MITOCHONDRIAL FUNCTIONS; EARLY DIAGNOSIS; ENZYME REPLACEMENT; EXON; GENE THERAPY; GENETIC COUNSELING; HAND TREMOR; HEARING IMPAIRMENT; HETEROZYGOTE; HUMAN; MACROCEPHALY; MITOCHONDRIAL DNA REPLICATION; MNGIE SYNDROME; MUTATION; NERVE CONDUCTION; OPTIC NERVE DISEASE; PERIPHERAL NEUROPATHY; PHENOTYPE; PRIORITY JOURNAL; REVIEW; SPASTIC PARAPLEGIA; TENDON REFLEX; WHITE MATTER;

HEREDITARY SENSORY AND MOTOR NEUROPATHY; HUMANS; MITOCHONDRIAL DISEASES; PERIPHERAL NERVOUS SYSTEM DISEASES;

EID: 84884129498     PISSN: 14744422     EISSN: 14744465     Source Type: Journal    
DOI: 10.1016/S1474-4422(13)70158-3     Document Type: Review

References (105)

1. Finsterer J Mitochondrial neuropathy. Clin Neurol Neurosurg 2005, 107:181-186.
2. McFarland R, Taylor RW, Turnbull DM A neurological perspective on mitochondrial disease. Lancet Neurol 2010, 9:829-840.
3. Rahman S, Hanna MG Diagnosis and therapy in neuromuscular disorders: diagnosis and new treatments in mitochondrial diseases. J Neurol Neurosurg Psychiatry 2009, 80:943-953.
4. Detmer SA, Chan DC Functions and dysfunctions of mitochondrial dynamics. Nat Rev Mol Cell Biol 2007, 8:870-879.
5. Milone M, Benarroch EE Mitochondrial dynamics: general concepts and clinical implications. Neurology 2012, 78:1612-1629.
6. 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, 36:509-520.
7. Züchner S, Mersiyanova IV, Muglia M, et al. Mutations in the mitochondrial GTPase mitofusin 2 cause Charcot-Marie-Tooth neuropathy type 2A. Nat Genet 2004, 36:449-451.
8. Baxter RV, Ben Othmane K, Rochelle JM, et al. Ganglioside-induced differentiation-associated protein-1 is mutant in Charcot-Marie-Tooth disease type 4A/8q21. Nat Genet 2002, 30:21-22.
9. Cuesta A, Pedrola L, Sevilla T, et al. The gene encoding ganglioside-induced differentiation-associated protein 1 is mutated in axonal Charcot-Marie-Tooth type 4A disease. Nat Genet 2002, 30:22-25.
10. Finsterer J Inherited mitochondrial neuropathies. J Neurol Sci 2011, 304:9-16.
11. Milone M, Massie R Polymerase gamma 1 mutations: clinical correlations. Neurologist 2010, 16:84-91.
12. Martin-Negrier ML, Sole G, Jardel C, Vital C, Ferrer X, Vital A TWINKLE gene mutation: report of a French family with an autosomal dominant progressive external ophthalmoplegia and literature review. Eur J Neurol 2011, 18:436-441.
13. Garone C, Tadesse S, Hirano M Clinical and genetic spectrum of mitochondrial neurogastrointestinal encephalomyopathy. Brain 2011, 134:3326-3332.
14. Karadimas CL, Vu TH, Holve SA, et al. Navajo neurohepatopathy is caused by a mutation in the MPV17 gene. Am J Hum Genet 2006, 79:544-548.
15. Hanna MG, Cadia P Pheripheral nerve diseases associated with mitochondrial respiratory chain dysfunction. Peripheral neuropathy 2005, 1937-1949. Elsevier Saunders, Philadelphia. 4th edn. P.J. Dyck, P.K. Thomas (Eds.).
16. Bouillot S, Martin-Négrier ML, Vital A, et al. Peripheral neuropathy associated with mitochondrial disorders: 8 cases and review of the literature. J Peripher Nerv Syst 2002, 7:213-220.
17. Menezes MP, Ouvrier RA Peripheral neuropathy associated with mitochondrial disease in children. Dev Med Child Neurol 2012, 54:407-414.
18. Gilhuis HJ, Schelhaas HJ, Cruysberg JR, Zwarts MJ Demyelinating polyneuropathy in Leber hereditary optic neuropathy. Neuromuscul Disord 2006, 16:394-395.
19. Santoro L, Carrozzo R, Malandrini A, et al. A novel SURF1 mutation results in Leigh syndrome with peripheral neuropathy caused by cytochrome C oxidase deficiency. Neuromuscul Disord 2000, 10:450-453.
20. Rusanen H, Majamaa K, Tolonen U, Remes AM, Myllylä R, Hassinen IE Demyelinating polyneuropathy in a patient with the tRNA (Leu)(UUR) mutation at base pair 3243 of the mitochondrial DNA. Neurology 1995, 45:1188-1192.
21. Pareyson D, Marchesi C Diagnosis, natural history, and management of Charcot-Marie-Tooth disease. Lancet Neurol 2009, 8:654-667.
22. Reilly MM, Murphy SM, Laurá M Charcot-Marie-Tooth disease. J Peripher Nerv Syst 2011, 16:1-14.
23. Yu-Wai-Man P, Griffiths PG, Gorman GS, et al. Multi-system neurological disease is common in patients with OPA1 mutations. Brain 2010, 133:771-786.
24. Amati-Bonneau P, Valentino ML, Reynier P, et al. OPA1 mutations induce mitochondrial DNA instability and optic atrophy 'plus' phenotypes. Brain 2008, 131:338-351.
25. Hudson G, Amati-Bonneau P, Blakely EL, et al. Mutation of OPA1 causes dominant optic atrophy with external ophthalmoplegia, ataxia, deafness and multiple mitochondrial DNA deletions: a novel disorder of mtDNA maintenance. Brain 2008, 131:329-337.
26. Cartoni R, Martinou JC Role of mitofusin 2 mutations in the physiopathology of Charcot-Marie-Tooth disease type 2A. Exp Neurol 2009, 218:268-273.
27. Misko AL, Sasaki Y, Tuck E, Milbrandt J, Baloh RH Mitofusin 2 mutations disrupt axonal mitochondrial positioning and promote axon degeneration. J Neurosci 2012, 32:4145-4155.
28. Züchner S, De Jonghe P, Jordanova A, et al. Axonal neuropathy with optic atrophy is caused by mutations in mitofusin 2. Ann Neurol 2006, 59:276-281.
29. Verhoeven K, Claeys KG, Züchner S, et al. MFN2 mutation distribution and genotype/phenotype correlation in Charcot-Marie-Tooth type 2. Brain 2006, 129:2093-2102.
30. Chung KW, Kim SB, Park KD, et al. Early onset severe and late-onset mild Charcot-Marie-Tooth disease with mitofusin 2 (MFN2) mutations. Brain 2006, 129:2103-2118.
31. Feely SM, Laura M, Siskind CE, et al. MFN2 mutations cause severe phenotypes in most patients with CMT2A. Neurology 2011, 76:1690-1696.
32. Saporta AS, Sottile SL, Miller LJ, Feely SM, Siskind CE, Shy ME Charcot-Marie-Tooth disease subtypes and genetic testing strategies. Ann Neurol 2011, 69:22-33.
33. Murphy SM, Laura M, Fawcett K, et al. Charcot-Marie-Tooth disease: frequency of genetic subtypes and guidelines for genetic testing. J Neurol Neurosurg Psychiatry 2012, 83:706-710.
34. Calvo J, Funalot B, Ouvrier RA, et al. Genotype-phenotype correlations in Charcot-Marie-Tooth disease type 2 caused by mitofusin 2 mutations. Arch Neurol 2009, 66:1511-1516.
35. Vital A, Vital C Mitochondria and peripheral neuropathies. J Neuropathol Exp Neurol 2012, 71:1036-1046.
36. Banchs I, Casasnovas C, Montero J, Martínez-Matos JA, Volpini V Two Spanish families with Charcot-Marie-Tooth type 2A: clinical, electrophysiological and molecular findings. Neuromuscul Disord 2008, 18:974-978.
37. Zhu D, Kennerson ML, Walizada G, Züchner S, Vance JM, Nicholson GA Charcot-Marie-Tooth with pyramidal signs is genetically heterogeneous: families with and without MFN2 mutations. Neurology 2005, 65:496-497.
38. Del Bo R, Moggio M, Rango M, et al. Mutated mitofusin 2 presents with intrafamilial variability and brain mitochondrial dysfunction. Neurology 2008, 71:1959-1966.
39. Chung KW, Suh BC, Cho SY, et al. Early-onset Charcot-Marie-Tooth patients with mitofusin 2 mutations and brain involvement. J Neurol Neurosurg Psychiatry 2010, 81:1203-1206.
40. Brockmann K, Dreha-Kulaczewski S, Dechent P, et al. Cerebral involvement in axonal Charcot-Marie-Tooth neuropathy caused by mitofusin 2 mutations. J Neurol 2008, 255:1049-1058.
41. Nicholson GA, Magdelaine C, Zhu D, et al. Severe early-onset axonal neuropathy with homozygous and compound heterozygous MFN2 mutations. Neurology 2008, 70:1678-1681.
42. Polke JM, Laurá M, Pareyson D, et al. Recessive axonal Charcot-Marie-Tooth disease due to compound heterozygous mitofusin 2 mutations. Neurology 2011, 77:168-173.
43. Boaretto F, Vettori A, Casarin A, et al. Severe CMT type 2 with fatal encephalopathy associated with a novel MFN2 splicing mutation. Neurology 2010, 74:1919-1921.
44. Rouzier C, Bannwarth S, Chaussenot A, et al. The MFN2 gene is responsible for mitochondrial DNA instability and optic atrophy 'plus' phenotype. Brain 2012, 135:23-34.
45. Renaldo F, Amati-Bonneau P, Slama A, et al. MFN2, a new gene responsible for mitochondrial DNA depletion. Brain 2012, 135:e223.
46. Cassereau J, Chevrollier A, Gueguen N, et al. Mitochondrial dysfunction and pathophysiology of Charcot-Marie-Tooth disease involving GDAP1 mutations. Exp Neurol 2011, 227:31-41.
47. Pedrola L, Espert A, Valdés-Sánchez T, et al. Cell expression of GDAP1 in the nervous system and pathogenesis of Charcot-Marie-Tooth type 4A disease. J Cell Mol Med 2008, 12:679-689.
48. Nelis E, Erdem S, Van Den Bergh PY, et al. Mutations in GDAP1: autosomal recessive CMT with demyelination and axonopathy. Neurology 2002, 59:1865-1872.
49. Moroni I, Morbin M, Milani M, et al. Novel mutations in the GDAP1 gene in patients affected with early-onset axonal Charcot-Marie-Tooth type 4A. Neuromuscul Disord 2009, 19:476-480.
50. Sevilla T, Jaijo T, Nauffal D, et al. Vocal cord paresis and diaphragmatic dysfunction are severe and frequent symptoms of GDAP1-associated neuropathy. Brain 2008, 131:3051-3061.
51. Cassereau J, Chevrollier A, Bonneau D, 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 2011, 6:87.
52. Zimoń M, Baets J, Fabrizi GM, et al. Dominant GDAP1 mutations cause predominantly mild CMT phenotypes. Neurology 2011, 77:540-548.
53. Sivera R, Espinós C, Vílchez JJ, et al. Phenotypical features of the p.R120W mutation in the GDAP1 gene causing autosomal dominant Charcot-Marie-Tooth disease. J Peripher Nerv Syst 2010, 15:334-344.
54. Cassereau J, Casasnovas C, Gueguen N, et al. Simultaneous MFN2 and GDAP1 mutations cause major mitochondrial defects in a patient with CMT. Neurology 2011, 76:1524-1526.
55. Vital A, Latour P, Sole G, et al. A French family with Charcot-Marie-Tooth disease related to simultaneous heterozygous MFN2 and GDAP1 mutations. Neuromuscul Disord 2012, 22:735-741.
56. Sciacco M, Prelle A, D'Adda E, et al. Familial mtDNA T8993C transition causing both the NARP and the MILS phenotype in the same generation. A morphological, genetic and spectroscopic study. J Neurol 2003, 250:1498-1500.
57. Uziel G, Moroni I, Lamantea E, et al. Mitochondrial disease associated with the T8993G mutation of the mitochondrial ATPase 6 gene: a clinical, biochemical, and molecular study in six families. J Neurol Neurosurg Psychiatry 1997, 63:16-22.
58. Rojo A, Campos Y, Sánchez JM, et al. NARP-MILS syndrome caused by 8993 T>G mitochondrial DNA mutation: a clinical, genetic and neuropathological study. Acta Neuropathol 2006, 111:610-616.
59. Childs AM, Hutchin T, Pysden K, et al. Variable phenotype including Leigh syndrome with a 9185T>C mutation in the MTATP6 gene. Neuropediatrics 2007, 38:313-316.
60. Castagna AE, Addis J, McInnes RR, et al. Late onset Leigh syndrome and ataxia due to a T to C mutation at bp 9,185 of mitochondrial DNA. Am J Med Genet A 2007, 143:808-816.
61. Craig K, Elliott HR, Keers SM, et al. Episodic ataxia and hemiplegia caused by the 8993T>C mitochondrial DNA mutation. J Med Genet 2007, 44:797-799.
62. Pitceathly RD, Murphy SM, Cottenie E, et al. Genetic dysfunction of MT-ATP6 causes axonal Charcot-Marie-Tooth disease. Neurology 2012, 79:1145-1154.
63. Synofzik M, Schicks J, Wilhelm C, Bornemann A, Schöls L Charcot-Marie-Tooth hereditary neuropathy due to a mitochondrial ATP6 mutation. Eur J Neurol 2012, 19:e114-e116.
64. Xu WY, Gu MM, Sun LH, et al. A nonsense mutation in DHTKD1 causes Charcot-Marie-Tooth disease type 2 in a large Chinese pedigree. Am J Hum Genet 2012, 91:1088-1094.
65. Rinaldi C, Grunseich C, Sevrioukova IF, et al. Cowchock syndrome is associated with a mutation in apoptosis-inducing factor. Am J Hum Genet 2012, 91:1095-1102.
66. Kennerson ML, Yiu EM, Chuang DT, 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 2013, 22:1404-1416.
67. Rantamäki MT, Soini HK, Finnilä SM, Majamaa K, Udd B Adult-onset ataxia and polyneuropathy caused by mitochondrial 8993T→C mutation. Ann Neurol 2005, 58:337-340.
68. Van Goethem G, Mercelis R, Löfgren A, et al. Patient homozygous for a recessive POLG mutation presents with features of MERRF. Neurology 2003, 61:1811-1813.
69. Van Goethem G, Luoma P, Rantamäki M, et al. POLG mutations in neurodegenerative disorders with ataxia but no muscle involvement. Neurology 2004, 63:1251-1257.
70. Hopkins SE, Somoza A, Gilbert DL Rare autosomal dominant POLG1 mutation in a family with metabolic strokes, posterior column spinal degeneration, and multi-endocrine disease. J Child Neurol 2010, 25:752-756.
71. Winterthun S, Ferrari G, He L, et al. Autosomal recessive mitochondrial ataxic syndrome due to mitochondrial polymerase gamma mutations. Neurology 2005, 64:1204-1248.
72. Weiss MD, Saneto RP Sensory ataxic neuropathy with dysarthria and ophthalmoparesis (SANDO) in late life due to compound heterozygous POLG mutations. Muscle Nerve 2010, 41:882-885.
73. Harrower T, Stewart JD, Hudson G, et al. POLG1 mutations manifesting as autosomal recessive axonal Charcot-Marie-Tooth disease. Arch Neurol 2008, 65:133-136.
74. Van Hove JL, Cunningham V, Rice C, et al. Finding twinkle in the eyes of a 71-year-old lady: a case report and review of the genotypic and phenotypic spectrum of TWINKLE-related dominant disease. Am J Med Genet A 2009, 149A:861-867.
75. Hudson G, Deschauer M, Busse K, Zierz S, Chinnery PF Sensory ataxic neuropathy due to a novel C10Orf2 mutation with probable germline mosaicism. Neurology 2005, 64:371-373.
76. Nikali K, Suomalainen A, Saharinen J, et al. Infantile onset spinocerebellar ataxia is caused by recessive mutations in mitochondrial proteins Twinkle and Twinky. Hum Mol Genet 2005, 14:2981-2990.
77. Hakonen AH, Goffart S, Marjavaara S, et al. Infantile-onset spinocerebellar ataxia and mitochondrial recessive ataxia syndrome are associated with neuronal complex I defect and mtDNA depletion. Hum Molec Genet 2008, 17:3822-3835.
78. Nishino I, Spinazzola A, Hirano M Thymidine phosphorylase gene mutations in MNGIE, a human mitochondrial disorder. Science 1999, 283:689-692.
79. Nishino I, Spinazzola A, Papadimitriou A, et al. Mitochondrial neurogastrointestinal encephalomyopathy: an autosomal recessive disorder due to thymidine phosphorylase mutations. Ann Neurol 2000, 47:792-800.
80. Martí R, Verschuuren JJ, Buchman A, et al. Late-onset MNGIE due to partial loss of thymidine phosphorylase activity. Ann Neurol 2005, 58:649-652.
81. Filosto M, Scarpelli M, Tonin P, et al. Pitfalls in diagnosing mitochondrial neurogastrointestinal encephalomyopathy. J Inherit Metab Dis 2011, 34:1199-1203.
82. Bedlack RS, Vu T, Hammans S, et al. MNGIE neuropathy: five cases mimicking chronic inflammatory demyelinating polyneuropathy. Muscle Nerve 2004, 29:364-368.
83. Said G, Lacroix C, Planté-Bordeneuve V, et al. Clinico-pathological aspects of the neuropathy of neurogastrointestinal encephalomyopathy (MNGIE) in four patients including two with a Charcot-Marie-Tooth presentation. J Neurol 2005, 252:655-662.
84. Needham M, Duley J, Hammond S, Herkes GK, Hirano M, Sue CM Mitochondrial disease mimicking Charcot-Marie Tooth disease. J Neurol Neurosurg Psychiatry 2007, 78:99-100.
85. González-Vioque E, Torres-Torronteras J, Andreu AL, et al. Limited dCTP availability accounts for mitochondrial DNA depletion in mitochondrial neurogastrointestinal encephalomyopathy (MNGIE). PLoS Genet 2011, 7:e1002035.
86. Van Goethem G, Schwartz M, Löfgren A, Dermaut B, Van Broeckhoven C, Vissing J Novel POLG mutations in progressive external ophthalmoplegia mimicking mitochondrial neurogastrointestinal encephalomyopathy. Eur J Hum Genet 2003, 11:547-549.
87. Tang S, Dimberg EL, Milone M, Wong LJ Mitochondrial neurogastrointestinal encephalomyopathy (MNGIE)-like phenotype: an expanded clinical spectrum of POLG1 mutations. J Neurol 2012, 259:862-868.
88. Shaibani A, Shchelochkov OA, Zhang S, et al. Mitochondrial neurogastrointestinal encephalopathy due to mutations in RRM2B. Arch Neurol 2009, 66:1028-1032.
89. Spinazzola A, Viscomi C, Fernandez-Vizarra E, et al. MPV17 encodes an inner mitochondrial membrane protein and is mutated in infantile hepatic mitochondrial DNA depletion. Nat Genet 2006, 38:570-575.
90. Spinazzola A, Santer R, Akman OH, et al. Hepatocerebral form of mitochondrial DNA depletion syndrome: novel MPV17 mutations. Arch Neurol 2008, 65:1108-1113.
91. Blakely EL, Butterworth A, Hadden RD, et al. MPV17 mutation causes neuropathy and leukoencephalopathy with multiple mtDNA deletions in muscle. Neuromuscul Disord 2012, 22:587-591.
92. Garone C, Rubio JC, Calvo SE, et al. MPV17 mutations causing adult-onset multisystemic disorder with multiple mitochondrial DNA deletions. Arch Neurol 2012, 69:1648-1651.
93. Emmanuele V, López LC, Berardo A, et al. Heterogeneity of coenzyme Q10 deficiency: patient study and literature review. Arch Neurol 2012, 69:978-983.
94. Spiegel R, Shaag A, Edvardson S, et al. SLC25A19 mutation as a cause of neuropathy and bilateral striatal necrosis. Ann Neurol 2009, 66:419-424.
95. Pfeffer G, Majamaa K, Turnbull DM, Thorburn D, Chinnery PF Treatment for mitochondrial disorders. Cochrane Database Syst Rev 2012, 4. CD004426.
96. Hirano M, Garone C, Quinzii CM CoQ10 deficiencies and MNGIE: two treatable mitochondrial disorders. Biochim Biophys Acta 2012, 1820:625-631.
97. Halter J, Schüpbach WM, Casali C, et al. Allogeneic hematopoietic SCT as treatment option for patients with mitochondrial neurogastrointestinal encephalomyopathy (MNGIE): a consensus conference proposal for a standardized approach. Bone Marrow Transplant 2011, 46:330-337.
98. Moran NF, Bain MD, Muqit MM, Bax BE Carrier erythrocyte entrapped thymidine phosphorylase therapy for MNGIE. Neurology 2008, 71:686-688.
99. Klopstock T, Metz G, Yu-Wai-Man P, et al. Persistence of the treatment effect of idebenone in Leber's hereditary optic neuropathy. Brain 2013, 136:e230.
100. Barboni P, Valentino ML, La Morgia C, et al. Idebenone treatment in patients with OPA1-mutant dominant optic atrophy. Brain 2013, 136:e231.
101. Carelli V, La Morgia C, Sadun AA Mitochondrial dysfunction in optic neuropathies: animal models and therapeutic options. Curr Opin Neurol 2013, 26:52-58.
102. Adhya S, Mahato B, Jash S, Koley S, Dhar G, Chowdhury T Mitochondrial gene therapy: the tortuous path from bench to bedside. Mitochondrion 2011, 11:839-844.
103. Martinelli D, Catteruccia M, Piemonte F, et al. EPI-743 reverses the progression of the pediatric mitochondrial disease-genetically defined Leigh Syndrome. Mol Gen Metab 2012, 107:383-388.
104. Takahashi R, Tokuhei I, Hamaguchi A, Iwasa K, Yamada M Coenzyme Q10 therapy in hereditary motor and sensory neuropathy type VI with novel mitofusin 2 mutation. Intern Med 2012, 51:791-793.
105. Craven L, Elson JL, Irving L, et al. Mitochondrial DNA disease: new options for prevention. Hum Mol Genet 2011, 20:168-174.