ALS5/SPG11/KIAA1840 mutations cause autosomal recessive axonal Charcot-Marie-Tooth disease

Brain

Volumn 139, Issue 1, 2016, Pages 73-85

  Montecchiani, Celeste ^a   Pedace, Lucia ^a   Lo Giudice, Temistocle ^a,b   Casella, Antonella ^a   Mearini, Marzia ^a   Gaudiello, Fabrizio ^a   Pedroso, José L ^c   Terracciano, Chiara ^b   Caltagirone, Carlo ^a,b   Massa, Roberto ^b   St George Hyslop, Peter H St ^d,e,f   Barsottini, Orlando G P ^c   Kawarai, Toshitaka ^g   Orlacchio, Antonio ^a,b  

^a IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^b UNIVERSITY OF ROME TOR VERGATA   (Italy)

^c FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^d UNIVERSITY OF TORONTO   (Canada)

^e UNIVERSITY OF TORONTO   (Canada)

^f UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^g UNIVERSITY OF TOKUSHIMA   (Japan)

Author keywords

ALS5 SPG11 KIAA1840 mutations; Axonal degeneration; Charcot Marie Tooth disease; Spatacsin

Indexed keywords

ADULT; ALS5 GENE; ARTICLE; AUTOSOMAL RECESSIVE DISORDER; CHROMOSOME 8Q; CLINICAL ARTICLE; COMPUTER MODEL; CONTROLLED STUDY; CORPUS CALLOSUM; CORPUS CALLOSUM AGENESIS; DISORDERS OF MITOCHONDRIAL FUNCTIONS; FEMALE; GENE; GENE LOCUS; GENE MUTATION; GENE SEQUENCE; GENETIC ANALYSIS; HEREDITARY MOTOR SENSORY NEUROPATHY; HUMAN; KIAA1840 GENE; MALE; PEDIGREE; PERIPHERAL NEUROPATHY; PRIORITY JOURNAL; SPG11 GENE; CASE CONTROL STUDY; GENETICS; MUTATION; RECESSIVE GENE;

PROTEIN; SPG11 PROTEIN, HUMAN;

CASE-CONTROL STUDIES; CHARCOT-MARIE-TOOTH DISEASE; FEMALE; GENES, RECESSIVE; HUMANS; MALE; MUTATION; PEDIGREE; PERIPHERAL NERVOUS SYSTEM DISEASES; PROTEINS; SPASTIC PARAPLEGIA, HEREDITARY;

EID: 84964665877     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awv320     Document Type: Article

References (78)

1. American Psychiatric Association. Diagnotic and statistical manual of mental disorders. 5th edn. Arlington, VA: American Psychiatric Association; 2013. http://dx.doi.org/10.1176/appi.books.9780890425596
2. Barhoumi C, Amouri R, Ben Hamida C, Ben Hamida M, Machghoul S, Gueddiche M, et al. Linkage of a new locus for autosomal recessive axonal form of Charcot-Marie-Tooth disease to chromosome 8q21. 3. Neuromuscul Disord 2001;11:27-34.
3. Bettencourt C, López-Sendón JL, García-Caldentey J, Rizzu P, Bakker IM, Shomroni O, et al. Exome sequencing is a useful diagnostic tool for complicated forms of hereditary spastic paraplegia. Clin Genet 2014;85:154-8.
4. Bienfait HME. Axonal phenotypes in Charcot-Marie-Tooth disease. Amsterdam, The Netherlands: Faculty of Medicine, University of Amsterdam (AMC-UvA); 2007. http://dare.uva. nl/document/2/47043
5. Bird DT. GeneReviews [Internet] In: Pagon RA, Adam MP, Ardinger HH, Bird DT, Dolan CR, Fong CT, et al. editors. Charcot-Marie-Tooth neuropathy type 2. Seattle, WA: University of Washington, Seattle; 1993-2015. http://www.ncbi. nlm.nih.gov/books/NBK1285
6. Birouk N, Gouider R, Le Guern E, Gugenheim M, Tardieu S, Maisonobe T, et al. Charcot-Marie-Tooth disease type 1A with 17p11. 2 duplication. Clinical and electrophysiological phenotype study and factors influencing disease severity in 119 cases. Brain 1997;120:813-23.
7. Bomont P, Cavalier L, Blondeau F, Ben Hamida C, Belal S, Tazir M, et al. The gene encoding gigaxonin, a new member of the cytoskeletal BTB/kelch repeat family, is mutated in giant axonal neuropathy. Nat Genet 2000;26:370-4.
8. Byrnes LJ, Sondermann H. Structural basis for the nucleotide-dependent dimerization of the large G protein atlastin-1/SPG3A. Proc Natl Acad Sci USA 2011;108:2216-21.
9. Carlesimo GA, Caltagirone C, Gainotti G. The mental deterioration battery: normative data, diagnostic reliability and qualitative analyses of cognitive impairment. The group for the standardization of the mental deterioration battery. Eur Neurol 1996;36:378-84.
10. Carosi L, Lo Giudice T, Di Lullo M, Lombardi F, Babalini C, Gaudiello F, et al. Hereditary spastic paraplegia: a novel mutation and expansion of the phenotype variability in SPG10. J Neurol Neurosurg Psychiatry 2015;86:702-4.
11. Casari G, De Fusco M, Ciarmatori S, Zeviani M, Mora M, Fernandez P, et al. Spastic paraplegia and OXPHOS impairment caused by mutations in paraplegin, a nuclear-encoded mitochondrial metalloprotease. Cell 1998;93:973-83.
12. Cassereau J, Codron P, Funalot B. Inherited peripheral neuropathies due to mitochondrial disorders. Rev Neurol (Paris) 2014;170:366-74.
13. Chiurchiù V, Maccarrone M, Orlacchio A. The role of reticulons in neurodegenerative diseases. Neuromolecular Med [Review] 2014;16:3-15.
14. Claramunt R, Pedrola L, Sevilla T, López de Munain A, Berciano J, Cuesta A, et al. Genetics of Charcot-Marie-Tooth disease type 4A: mutations, inheritance, phenotypic variability, and founder effect. J Med Genet 2005;42:358-65.
15. Cottenie E, Kochanski A, Jordanova A, Bansagi B, Zimon M, Horga A, et al. Truncating and missense mutations in IGHMBP2 cause Charcot-Marie Tooth disease type 2. Am J Hum Genet 2014;95:590-601.
16. Crimella C, Baschirotto C, Arnoldi A, Tonelli A, Tenderini E, Airoldi G, et al. Mutations in the motor and stalk domains of KIF5A in spastic paraplegia type 10 and in axonal Charcot-Marie-Tooth type 2. Clin Genet 2012;82:157-64.
17. Daoud H, Zhou S, Noreau A, Sabbagh M, Belzil V, Dionne-Laporte A, et al. Exome sequencing reveals SPG11 mutations causing juvenile ALS. Neurobiol Aging 2012;33:839. e5-9.
18. De Sandre-Giovannoli A, Chaouch M, Kozlov S, Vallat JM, Tazir M, Kassouri N, et al. Homozygous defects in LMNA, encoding lamin A/C nuclear-envelope proteins, cause autosomal recessive axonal neuropathy in human (Charcot-Marie-Tooth disorder type 2) and mouse. Am J Hum Genet 2002;70:726-36.
19. Del Bo R, Di Fonzo A, Ghezzi S, Locatelli F, Stevanin G, Costa A, et al. SPG11: a consistent clinical phenotype in a family with homozygous spatacsin truncating mutation. Neurogenetics 2007;8:301-5.
20. Denora PS, Schlesinger D, Casali C, Kok F, Tessa A, Boukhris A, et al. Screening of ARHSP-TCC patients expands the spectrum of SPG11 mutations and includes a large scale gene deletion. Hum Mutat 2009;30:500-19.
21. Dyck PJ, Thomas PK, editors. Peripheal neuropathy. 4th edn. Philadelphia, PA: Elsevier Saunders; 2005. http://www.scribd.com/doc/243563627/Peripheral-Neuropathy-2005-Dyck-pdf cribd
22. Dyck PJ, Gutrecht JA, Bastron JA, Karnes WE, Dale AJ. Histologic and teased-fiber measurements of sural nerve in disorders of lower motor and primary sensory neurons. Mayo Clin Proc 1968;43:81-123.
23. Feely S, Laura M, Siskind CE, Sottile S, Davis M, Gibbons VS, et al. MFN2 mutations cause severe phenotypes in most patients with CMT2A. Neurology 2011;76:1690-6.
24. Fridman V, Murphy SM. The spectrum of axonopathies: from CMT2 to HSP. Neurology 2014;83:580-1.
25. Fusco C, Frattini D, Farnetti E, Nicoli D, Casali B, Fiorentino F, et al. Hereditary spastic paraplegia and axonal motor neuropathy caused by a novel SPG3A de novo mutation. Brain Dev 2010;32:592-4.
26. Genari AB, Borghetti VH, Gouvêa SP, Bueno KC, dos Santos PL, dos Santos AC, et al. Characterizing the phenotypic manifestations of MFN2 R104W mutation in Charcot-Marie-Tooth type 2. Neuromuscul Disord 2011;21:428-32.
27. Gess B, Auer-Grumbach M, Schirmacher A, Strom T, Zitzelsberger M, Rudnik-Schö neborn S, et al. HSJ1-related hereditary neuropathies: novel mutations and extended clinical spectrum. Neurology 2014;83:1726-32.
28. Goizet C, Boukhris A, Mundwiller E, Tallaksen C, Forlani S, Toutain A, et al. Complicated forms of autosomal dominant hereditary spastic paraplegia are frequent in SPG10. Hum Mutat 2009;30:376-85.
29. Guelly C, Zhu PP, Leonardis L, Papić L, Zidar J, Schabhü ttl M, et al. Targeted high-throughput sequencing identifies mutations in atlastin-1 as a cause of hereditary sensory neuropathy type I. Am J Hum Genet 2011;88:99-105.
30. Guernsey DL, Jiang H, Bedard K, Evans SC, Ferguson M, Matsuoka M, et al. Mutation in the gene encoding ubiquitin ligase LRSAM1 in patients with Charcot-Marie-Tooth disease. PLoS Genet 2010;6:e1001081.
31. Hammer MB, Eleuch-Fayache G, Schottlaender LV, Nehdi H, Gibbs JR, Arepalli SK, et al. Mutations in GBA2 cause autosomal-recessive cerebellar ataxia with spasticity. Am J Hum Genet 2013;92:245-51.
32. Hanein S, Martin E, Boukhris A, Byrne P, Goizet C, Hamri A, et al. Identification of the SPG15 gene, encoding spastizin, as a frequent cause of complicated autosomal-recessive spastic paraplegia, including Kjellin syndrome. Am J Hum Genet 2008;82:992-1002.
33. Hegele R. LMNA mutation position predicts organ system involvement in laminopathies. Clin Genet 2005;68:31-4.
34. Hehr U, Bauer P, Winner B, Schüle R, Olmez A, Koehler W, et al. Long-term course and mutational spectrum of spatacsin-linked spastic paraplegia. Ann Neurol 2007;62:656-65.
35. Hirst J, Borner GH, Edgar J, Hein MY, Mann M, Buchholz F, et al. Interaction between AP-5 and the hereditary spastic paraplegia proteins SPG11and SPG15. Mol Biol Cell 2013;24:2558-69.
36. Houlden H, Laura M, Wavrant-De Vrièze F, Blake J, Wood N, Reilly MM. Mutations in the HSP27 (HSPB1) gene cause dominant, recessive, and sporadic distal HMN/CMT type 2. Neurology 2008;71:1660-8.
37. Howard HC, Mount DB, Rochefort D, Byun N, Dupré N, Lu J, et al. The K-Cl cotransporter KCC3 is mutant in a severe peripheral neuropathy associated with agenesis of the corpus callosum. Nat Genet 2002;32:384-92.
38. Erratum in Nat Genet 2002;32:681.
39. Ito D, Suzuki N. Seipinopathy: a novel endoplasmic reticulum stressassociated disease [Review]. Brain 2009;132:8-15.
40. Jerath NU, Shy ME. Hereditary motor and sensory neuropathies: Understanding molecular pathogenesis could lead to future treatment strategies. Biochim Biophys Acta 2015;1852:667-78.
41. Landouré G, Zhu PP, Lourenço CM, Johnson JO, Toro C, Bricceno KV, et al. Hereditary spastic paraplegia type 43 (SPG43) is caused by mutation in C19orf12. Hum Mutat 2013;34:1357-60.
42. Leal A, Huehne K, Bauer F, Sticht H, Berger P, Suter U, et al. Identification of the variant Ala335Val of MED25 as responsible for CMT2B2: molecular data, functional studies of the SH3 recognition motif and correlation between wild-type MED25 and PMP22 RNA levels in CMT1A animal models. Neurogenetics 2009;10:275-87.
43. Lee MJ, Cheng TW, Hua MS, Pan MK, Wang J, Stephenson DA, et al. Mutations of the SPG11 gene in patients with autosomal recessive spastic paraparesis and thin corpus callosum. J Neurol Neurosurg Psychiatry 2008;79:607-9.
44. Leonardis L, Auer-Grumbach M, Papić L, Zidar J. The N355K atlastin 1 mutation is associated with hereditary sensory neuropathy and pyramidal tract features. Eur J Neurol 2012;19:992-8.
45. Lo Giudice T, Lombardi F, Santorelli FM, Kawarai T, Orlacchio A. Hereditary spastic paraplegia: clinical-genetic characteristics and evolving molecular mechanisms [Review]. Exp Neurol 2014;261:518-39.
46. Martin E, Schüle R, Smets K, Rastetter A, Boukhris, A, Loureiro JL, et al. Loss of function of glucocerebrosidase GBA2 is responsible for motor neuron defects in hereditary spastic paraplegia. Am J Hum Genet 2013;92:238-44.
47. Martin E, Yanicostas C, Rastetter A, Naini SM, Maouedj A, Kabashi E, et al. Spatacsin and spastizin act in the same pathway required for proper spinal motor neuron axon outgrowth in Zebrafish. Neurobiol Dis 2012;48:299-308.
48. Medical Research Council. Aids to the examination of the peripheral nervous system. Her Majesty's Stationery Office. London, UK; 1981, Memorandum no. 45.
49. Murphy SM, Herrmann DN, McDermott MP, Scherer SS, Shy ME, Reilly MM, et al. Reliability of the CMT neuropathy score (second version) in Charcot-Marie-Tooth disease. J Peripher Nerv Syst 2011;16:191-8.
50. Nicholson GA, Magdelaine C, Zhu D, Grew S, Ryan MM, Sturtz F, et al. Severe early-onset axonal neuropathy with homozygous and compound heterozygous MFN2 mutations. Neurology 2008;70:1678-81.
51. Nishino I, Spinazzola A, Papadimitriou A, Hammans S, Steiner I, Hahn CD, et al. Mitochondrial neurogastrointestinal encephalomyopathy: an autosomal recessive disorder due to thymidine phosphorylase mutations. Ann Neurol 2000;47:792-800.
52. Orlacchio A, Patrono C, Gaudiello F, Rocchi C, Moschella V, Floris R, et al. Silver syndrome variant of hereditary spastic paraplegia: a locus to 4p and allelism with SPG4. Neurology 2008;70:1959-66.
53. Orlacchio A, Babalini C, Borreca A, Patrono C, Massa R, Basaran S, et al. Spatacsin mutations cause autosomal recessive juvenile amyotrophic lateral sclerosis. Brain 2010;133:591-8.
54. Ott J. Linkage analysis and family classification under heterogeneity. Ann Hum Genet 1983;47:311-20.
55. Palumbo C, Massa R, Panico MB, Di Muzio A, Sinibaldi P, Bernardi G, et al. Peripheral nerve extracellular matrix remodelling in Charcot-Marie-Tooth type I disease. Acta Neuropathol 2002;104:287-96.
56. Paisan-Ruiz C, Nath P, Wood NW, Singleton A, Houlden H. Clinical heterogeneity and genotype-phenotype correlations in hereditary spastic paraplegia because of spatacsin mutations (SPG11). Eur J Neurol 2008;15:1065-70.
57. Pehlivan D, Coban Akdemir Z, Karaca E, Bayram Y, Jhangiani S, Yildiz EP, et al. Exome sequencing reveals homozygous TRIM2 mutation in a patient with early onset CMT and bilateral vocal cord paralysis. Hum Genet 2015;134:671-3.
58. Pensato V, Castellotti B, Gellera C, Pareyson D, Ciano C, Nanetti L, et al. Overlapping phenotypes in complex spastic paraplegias SPG11, SPG15, SPG35 and SPG48. Brain 2014;137:1907-20.
59. Pérez-Brangulí F, Mishra HK, Prots I, Havlicek S, Kohl Z, Saul D, et al. Dysfunction of spatacsin leads to axonal pathology in SPG11-linked hereditary spastic paraplegia. Hum Mol Genet 2014;23:4859-74.
60. Pierson TM, Simeonov DR, Sincan M, Adams DA, Markello T, Golas G, et al. Exome sequencing and SNP analysis detect novel compound heterozygosity in fatty acid hydroxylase-associated neurodegeneration. Eur J Hum Genet 2012;20:476-9.
61. Pippucci T, Panza E, Pompilii E, Donadio V, Borreca A, Babalini C, et al. Autosomal recessive hereditary spastic paraplegia with thin corpus callosum: a novel mutation in the SPG11 gene and further evidence for genetic heterogeneity. Eur J Neurol 2009;16:121-6.
62. Querin G, Bertolin C, Martinuzzi A, Bassi MT, Arnoldi A, Polo A, et al. The blurred scenario of motor neuron disorders linked to spatacsin mutations: a case report. Eur J Neurol 2014;21:85-6.
63. Reyes-Marin K, Jimenez-Pancho J, Pozo L, Garcia-Villanueva M, de Blas G, Vazquez JM, Jimenez-Escrig A. A novel myelin protein zero (V136G) homozygous mutation causing late onset demyelinating polyneuropathy with brain white matter lesions. Clin Neurol Neurosurg 2011;113:243-4.
64. Sagnelli A, Piscosquito G, Chiapparini L, Ciano C, Salsano E, Saveri P, et al. X-linked Charcot-Marie-Tooth type 1: strokelike presentation of a novel GJB1 mutation. J Peripher Nerv Syst 2014;19:183-6.
65. Simpson MA, Cross H, Proukakis C, Pryde A, Hershberger R, Chatonnet A, et al. Maspardin is mutated in mast syndrome, a complicated form of Hereditary Spastic Paraplegia associated with dementia. Am J Hum Genet 2003;73:1147-56.
66. Spiegel R, Mandel H, Saada A, Lerer I, Burger A, Shaag A, et al. Delineation of C12orf65-related phenotypes: a genotype-phenotype relationship. Eur J Hum Genet 2014;22:1019-25.
67. Stevanin G, Santorelli FM, Azzedine H, Coutinho P, Chomilier J, Denora PS, et al. Mutations in SPG11, encoding spatacsin, are a major cause of spastic paraplegia with thin corpus callosum. Nat Genet 2007a;39:366-72.
68. Stevanin G, Azzedine H, Denora P, Boukhris A, Tazir M, Lossos A, et al. Mutations in SPG11 are frequent in autosomal recessive spastic paraplegia with thin corpus callosum, cognitive decline and lower motor neuron degeneration. Brain 2007b;131:772-84.
69. Tamiya G, Makino S, Hayashi M, Abe A, Numakura C, Ueki M, et al. A Mutation of COX6A1 causes a recessive axonal or mixed form of Charcot-Marie-Tooth Disease. Am J Hum Genet 2014;95:294-300.
70. Tazir M, Bellatache M, Nouioua S, Vallat JM. Autosomal recessive Charcot-Marie-Tooth disease: from genes to phenotypes. J Peripher Nerv Syst 2013;18:113-29.
71. Tazir M, Hamadouche T, Nouioua S, Mathis S, Vallat JM. Hereditary motor and sensory neuropathies or Charcot-Marie-Tooth diseases: an update. J Neurol Sci 2014;347:14-22.
72. Tessa A, Denora PS, Racis L, Storti E, Orlacchio A, Santorelli FM. Bridging over the troubled heterogeneity of SPG-related pathologies: mechanisms unite what genetics divide [Review]. Curr Mol Med 2014;14:1034-42.
73. Tesson C, Nawara M, Salih MAM, Rossignol R, Zaki MS, Al Balwi M, et al. Alteration of fatty-acid-metabolizing enzymes affects mitochondrial form and function in hereditary spastic paraplegia. Am J Hum Genet 2012;91:1051-64.
74. Timmerman V, Clowes VE, Reid E. Overlapping molecular pathological themes link Charcot-Marie-Tooth neuropathies and hereditary spastic paraplegias [Review]. Exp Neurol 2013;246:14-25.
75. Van Goethem G, Dermaut B, Löfgren A, Martin JJ, Van Broeckhoven C. Mutation of POLG is associated with progressive external ophthalmoplegia characterized by mtDNA deletions. Nat Genet 2001;28:211-2.
76. Yum SW, Zhang J, Mo K, Li J, Scherer SS. A novel recessive NEFL mutation causes a severe, early-onset axonal neuropathy. Ann Neurol 2009;66:759-70.
77. Windpassinger C, Auer-Grumbach M, Irobi J, Patel H, Petek E, Hörl G, et al. Heterozygous missense mutations in BSCL2 are associated with distal hereditary motor neuropathy and Silver syndrome. Nat Genet 2004;36:271-6.
78. Zimoń M1, Baets J, Almeida-Souza L, De Vriendt E, Nikodinovic J, Parman Y, et al. Loss-of-function mutations in HINT1 cause axonal neuropathy with neuromyotonia. Nat Genet 2012:44:1080-3.