Dissection of genetic factors associated with amyotrophic lateral sclerosis

Experimental Neurology

Volumn 262, Issue Part B, 2014, Pages 91-101

  Leblond, Claire S ^a,b   Kaneb, Hannah M ^a,b   Dion, Patrick A ^b,c   Rouleau, Guy A ^a,b  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

Amyotrophic lateral sclerosis; Genetic factors; Heritability; Rare disease; Whole exome sequencing

Indexed keywords

COPPER ZINC SUPEROXIDE DISMUTASE; FUSED IN SARCOMA PROTEIN; TAR DNA BINDING PROTEIN; C9ORF72 PROTEIN, HUMAN; DNA BINDING PROTEIN; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN; PFN1 PROTEIN, HUMAN; PROFILIN; PROTEIN; PROTEIN TDP-43;

AMYOTROPHIC LATERAL SCLEROSIS; AUTOSOMAL DOMINANT INHERITANCE; AUTOSOMAL RECESSIVE INHERITANCE; C9ORF72 GENE; CAG REPEAT; CHROMOSOME 9P; CHROMOSOME 9P21; CHROMOSOME REARRANGEMENT; COPY NUMBER VARIATION; FAMILIAL AMYOTROPHIC LATERAL SCLEROSIS; FAMILY HISTORY; FRONTOTEMPORAL DEMENTIA; FUSED IN SARCOMA GENE; GENE; GENE MUTATION; GENETIC ASSOCIATION; GENETIC RISK; GENETIC SUSCEPTIBILITY; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN A1 GENE; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN A2B1 GENE; HUMAN; INCIDENCE; LINKAGE ANALYSIS; NEXT GENERATION SEQUENCING; NONHUMAN; PENETRANCE; PROFILIN 1 GENE; REVIEW; SEQUENCE ANALYSIS; SINGLE NUCLEOTIDE VARIATION; SPORADIC AMYOTROPHIC LATERAL SCLEROSIS; SUPEROXIDE DISMUTASE 1 GENE; TAR DNA BINDING PROTEIN 43 GENE; WHOLE EXOME SEQUENCING; X CHROMOSOMAL INHERITANCE; GENETIC PREDISPOSITION; GENETICS;

AMYOTROPHIC LATERAL SCLEROSIS; DNA-BINDING PROTEINS; GENETIC ASSOCIATION STUDIES; GENETIC PREDISPOSITION TO DISEASE; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEIN GROUP A-B; HUMANS; PROFILINS; PROTEINS;

EID: 84922481787     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2014.04.013     Document Type: Review

References (160)

1. Abel O., Powell J.F., Andersen P.M., Al-Chalabi A. ALSoD: a user-friendly online bioinformatics tool for amyotrophic lateral sclerosis genetics. Hum. Mutat. 2012, 33:1345-1351.
2. Al-Chalabi A., Andersen P.M., Nilsson P., et al. Deletions of the heavy neurofilament subunit tail in amyotrophic lateral sclerosis. Hum. Mol. Genet. 1999, 8:157-164.
3. Al-Chalabi A., Fang F., Hanby M.F., et al. An estimate of amyotrophic lateral sclerosis heritability using twin data. J. Neurol. Neurosurg. Psychiatry 2010, 81:1324-1326.
4. Alexander M.D., Traynor B.J., Miller N., et al. "True" sporadic ALS associated with a novel SOD-1 mutation. Ann. Neurol. 2002, 52:680-683.
5. Al-Saif A., Al-Mohanna F., Bohlega S. A mutation in sigma-1 receptor causes juvenile amyotrophic lateral sclerosis. Ann. Neurol. 2011, 70:913-919.
6. Andersen P.M., Al-Chalabi A. Clinical genetics of amyotrophic lateral sclerosis: what do we really know?. Nat. Rev. Neurol. 2011, 7:603-615.
7. Arai T., Hasegawa M., Akiyama H., et al. TDP-43 is a component of ubiquitin-positive tau-negative inclusions in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Biochem. Biophys. Res. Commun. 2006, 351:602-611.
8. Awadalla P., Gauthier J., Myers R.A., et al. Direct measure of the de novo mutation rate in autism and schizophrenia cohorts. Am. J. Hum. Genet. 2010, 87:316-324.
9. Beck J., Poulter M., Hensman D., et al. Large C9orf72 hexanucleotide repeat expansions are seen in multiple neurodegenerative syndromes and are more frequent than expected in the UK population. Am. J. Hum. Genet. 2013, 92:345-353.
10. Blauw H.M., Veldink J.H., van Es M.A., et al. Copy-number variation in sporadic amyotrophic lateral sclerosis: a genome-wide screen. Lancet Neurol. 2008, 7:319-326.
11. Blauw H.M., Al-Chalabi A., Andersen P.M., et al. A large genome scan for rare CNVs in amyotrophic lateral sclerosis. Hum. Mol. Genet. 2010, 19:4091-4099.
12. Boxer A.L., Mackenzie I.R., Boeve B.F., et al. Clinical, neuroimaging and neuropathological features of a new chromosome 9p-linked FTD-ALS family. J. Neurol. Neurosurg. Psychiatry 2011, 82:196-203.
13. Brettschneider J., Del Tredici K., Toledo J.B., et al. Stages of pTDP-43 pathology in amyotrophic lateral sclerosis. Ann. Neurol. 2013, 74:20-38.
14. Buratti E., Brindisi A., Giombi M., Tisminetzky S., Ayala Y.M., Baralle F.E. TDP-43 binds heterogeneous nuclear ribonucleoprotein A/B through its C-terminal tail: an important region for the inhibition of cystic fibrosis transmembrane conductance regulator exon 9 splicing. J. Biol. Chem. 2005, 280:37572-37584.
15. Byrne S., Walsh C., Lynch C., et al. Rate of familial amyotrophic lateral sclerosis: a systematic review and meta-analysis. J. Neurol. Neurosurg. Psychiatry 2011, 82:623-627.
16. Chen Y.Z., Bennett C.L., Huynh H.M., et al. DNA/RNA helicase gene mutations in a form of juvenile amyotrophic lateral sclerosis (ALS4). Am. J. Hum. Genet. 2004, 74:1128-1135.
17. Chen Y., Zeng Y., Huang R., et al. No association of five candidate genetic variants with amyotrophic lateral sclerosis in a Chinese population. Neurobiol. Aging 2012, 33. (2721 e3-5).
18. Chesi A., Staahl B.T., Jovicic A., et al. Exome sequencing to identify de novo mutations in sporadic ALS trios. Nat. Neurosci. 2013, 16:851-855.
19. Chio A., Logroscino G., Hardiman O., et al. Prognostic factors in ALS: A critical review. Amyotroph. Lateral Scler. 2009, 10:310-323.
20. Chio A., Schymick J.C., Restagno G., et al. A two-stage genome-wide association study of sporadic amyotrophic lateral sclerosis. Hum. Mol. Genet. 2009, 18:1524-1532.
21. Chio A., Calvo A., Moglia C., et al. A de novo missense mutation of the FUS gene in a "true" sporadic ALS case. Neurobiol. Aging 2011, 32. (553 e23-6).
22. Chio A., Restagno G., Brunetti M., et al. ALS/FTD phenotype in two Sardinian families carrying both C9ORF72 and TARDBP mutations. J. Neurol. Neurosurg. Psychiatry 2012, 83:730-733.
23. Chio A., Logroscino G., Traynor B.J., et al. Global epidemiology of amyotrophic lateral sclerosis: a systematic review of the published literature. Neuroepidemiology 2013, 41:118-130.
24. Chio A., Mora G., Restagno G., et al. UNC13A influences survival in Italian amyotrophic lateral sclerosis patients: a population-based study. Neurobiol. Aging 2013, 34. (357 e1-5).
25. Chow C.Y., Landers J.E., Bergren S.K., et al. Deleterious variants of FIG4, a phosphoinositide phosphatase, in patients with ALS. Am. J. Hum. Genet. 2009, 84:85-88.
26. Ciura S., Lattante S., Le Ber I., et al. Loss of function of C9orf72 causes motor deficits in a zebrafish model of Amyotrophic Lateral Sclerosis. Ann. Neurol 2013, 10.1002/ana.23946.
27. Corcia P., Khoris J., Couratier P., et al. SMN1 gene study in three families in which ALS and spinal muscular atrophy co-exist. Neurology 2002, 59:1464-1466.
28. Corcia P., Mayeux-Portas V., Khoris J., et al. Abnormal SMN1 gene copy number is a susceptibility factor for amyotrophic lateral sclerosis. Ann. Neurol. 2002, 51:243-246.
29. Corcia P., Camu W., Halimi J.M., et al. SMN1 gene, but not SMN2, is a risk factor for sporadic ALS. Neurology 2006, 67:1147-1150.
30. Cronin S., Berger S., Ding J., et al. A genome-wide association study of sporadic ALS in a homogenous Irish population. Hum. Mol. Genet. 2008, 17:768-774.
31. Cronin S., Blauw H.M., Veldink J.H., et al. Analysis of genome-wide copy number variation in Irish and Dutch ALS populations. Hum. Mol. Genet. 2008, 17:3392-3398.
32. Daoud H., Zhou S., Noreau A., et al. Exome sequencing reveals SPG11 mutations causing juvenile ALS. Neurobiol. Aging 2012, 33. (839 e5-9).
33. DeJesus-Hernandez M., Kocerha J., Finch N., et al. De novo truncating FUS gene mutation as a cause of sporadic amyotrophic lateral sclerosis. Hum. Mutat. 2010, 31:E1377-E1389.
34. DeJesus-Hernandez M., Mackenzie I.R., Boeve B.F., et al. Expanded GGGGCC hexanucleotide repeat in noncoding region of C9ORF72 causes chromosome 9p-linked FTD and ALS. Neuron 2011, 72:245-256.
35. Deng H.X., Chen W., Hong S.T., et al. Mutations in UBQLN2 cause dominant X-linked juvenile and adult-onset ALS and ALS/dementia. Nature 2011, 477:211-215.
36. Deng M., Wei L., Zuo X., et al. Genome-wide association analyses in Han Chinese identify two new susceptibility loci for amyotrophic lateral sclerosis. Nat. Genet. 2013, 45:697-700.
37. Dering C., Hemmelmann C., Pugh E., Ziegler A. Statistical analysis of rare sequence variants: an overview of collapsing methods. Genet. Epidemiol. 2011, 35(Suppl. 1):S12-S17.
38. Droppelmann C.A., Wang J., Campos-Melo D., et al. Detection of a novel frameshift mutation and regions with homozygosis within ARHGEF28 gene in familial amyotrophic lateral sclerosis. Amyotroph. Lateral Scler. Frontotemporal Degener. 2013, 14:444-451.
39. Dunckley T., Huentelman M.J., Craig D.W., et al. Whole-genome analysis of sporadic amyotrophic lateral sclerosis. N. Engl. J. Med. 2007, 357:775-788.
40. Ekblom J., Jossan S.S., Oreland L., Walum E., Aquilonius S.M. Reactive gliosis and monoamine oxidase B. J. Neural Transm. Suppl. 1994, 41:253-258.
41. Elden A.C., Kim H.J., Hart M.P., et al. Ataxin-2 intermediate-length polyglutamine expansions are associated with increased risk for ALS. Nature 2010, 466:1069-1075.
42. Fang F., Kamel F., Lichtenstein P., et al. Familial aggregation of amyotrophic lateral sclerosis. Ann. Neurol. 2009, 66:94-99.
43. Farg M.A., Sundaramoorthy V., Sultana J.M., et al. C9ORF72, implicated in amytrophic lateral sclerosis and frontotemporal dementia, regulates endosomal trafficking. Hum. Mol. Genet 2014, 10.1093/hmg/ddu068.
44. Fecto F., Yan J., Vemula S.P., et al. SQSTM1 mutations in familial and sporadic amyotrophic lateral sclerosis. Arch. Neurol. 2011, 68:1440-1446.
45. Fernandez-Santiago R., Sharma M., Berg D., et al. No evidence of association of FLJ10986 and ITPR2 with ALS in a large German cohort. Neurobiol. Aging 2011, 32. (551 e1-4).
46. Figlewicz D.A., Krizus A., Martinoli M.G., et al. Variants of the heavy neurofilament subunit are associated with the development of amyotrophic lateral sclerosis. Hum. Mol. Genet. 1994, 3:1757-1761.
47. Fogh I., D'Alfonso S., Gellera C., et al. No association of DPP6 with amyotrophic lateral sclerosis in an Italian population. Neurobiol. Aging 2011, 32:966-967.
48. Ghatak N.R., Campbell W.W., Lippman R.H., Hadfield M.G. Anterior horn changes of motor neuron disease associated with demyelinating radiculopathy. J. Neuropathol. Exp. Neurol. 1986, 45:385-395.
49. Gijselinck I., Engelborghs S., Maes G., et al. Identification of 2 Loci at chromosomes 9 and 14 in a multiplex family with frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Arch. Neurol. 2010, 67:606-616.
50. Gijselinck I., Van Langenhove T., van der Zee J., et al. A C9orf72 promoter repeat expansion in a Flanders-Belgian cohort with disorders of the frontotemporal lobar degeneration-amyotrophic lateral sclerosis spectrum: a gene identification study. Lancet Neurol. 2012, 11:54-65.
51. Girard S.L., Gauthier J., Noreau A., et al. Increased exonic de novo mutation rate in individuals with schizophrenia. Nat. Genet. 2011, 43:860-863.
52. Greenway M.J., Alexander M.D., Ennis S., et al. A novel candidate region for ALS on chromosome 14q11.2. Neurology 2004, 63:1936-1938.
53. Greenway M.J., Andersen P.M., Russ C., et al. ANG mutations segregate with familial and 'sporadic' amyotrophic lateral sclerosis. Nat. Genet. 2006, 38:411-413.
54. Gros-Louis F., Lariviere R., Gowing G., et al. A frameshift deletion in peripherin gene associated with amyotrophic lateral sclerosis. J. Biol. Chem. 2004, 279:45951-45956.
55. Gros-Louis F., Gaspar C., Rouleau G.A. Genetics of familial and sporadic amyotrophic lateral sclerosis. Biochim. Biophys. Acta 2006, 1762:956-972.
56. Hadano S., Hand C.K., Osuga H., et al. A gene encoding a putative GTPase regulator is mutated in familial amyotrophic lateral sclerosis 2. Nat. Genet. 2001, 29:166-173.
57. Hammer R.P., Tomiyasu U., Scheibel A.B. Degeneration of the human Betz cell due to amyotrophic lateral sclerosis. Exp. Neurol. 1979, 63:336-346.
58. Hanby M.F., Scott K.M., Scotton W., et al. The risk to relatives of patients with sporadic amyotrophic lateral sclerosis. Brain 2011, 134:3454-3457.
59. Hentati A., Bejaoui K., Pericak-Vance M.A., et al. Linkage of recessive familial amyotrophic lateral sclerosis to chromosome 2q33-q35. Nat. Genet. 1994, 7:425-428.
60. Hentati A., Ouahchi K., Pericak-Vance M.A., et al. Linkage of a commoner form of recessive amyotrophic lateral sclerosis to chromosome 15q15-q22 markers. Neurogenetics 1998, 2:55-60.
61. Hosler B.A., Sapp P.C., Berger R., et al. Refined mapping and characterization of the recessive familial amyotrophic lateral sclerosis locus (ALS2) on chromosome 2q33. Neurogenetics 1998, 2:34-42.
62. Hosler B.A., Siddique T., Sapp P.C., et al. Linkage of familial amyotrophic lateral sclerosis with frontotemporal dementia to chromosome 9q21-q22. JAMA 2000, 284:1664-1669.
63. Hughes J.T. Pathology of amyotrophic lateral sclerosis. Adv. Neurol. 1982, 36:61-74.
64. Iossifov I., Ronemus M., Levy D., et al. De novo gene disruptions in children on the autistic spectrum. Neuron 2012, 74:285-299.
65. Iwahashi C.K., Yasui D.H., An H.J., et al. Protein composition of the intranuclear inclusions of FXTAS. Brain 2006, 129:256-271.
66. Jin P., Duan R., Qurashi A., et al. Pur alpha binds to rCGG repeats and modulates repeat-mediated neurodegeneration in a Drosophila model of fragile X tremor/ataxia syndrome. Neuron 2007, 55:556-564.
67. Johnson J.O., Mandrioli J., Benatar M., et al. Exome sequencing reveals VCP mutations as a cause of familial ALS. Neuron 2010, 68:857-864.
68. Kabashi E., Valdmanis P.N., Dion P., et al. TARDBP mutations in individuals with sporadic and familial amyotrophic lateral sclerosis. Nat. Genet. 2008, 40:572-574.
69. Kaivorinne A.L., Moilanen V., Kervinen M., et al. Novel TARDBP sequence variant and C9ORF72 repeat expansion in a family with frontotemporal dementia. Alzheimer Dis. Assoc. Disord 2012, 10.1097/WAD.0b013e318266fae5.
70. Kaneko K., Saito F., Sunohara N., Ikeuchi T. Cytogenetic analysis of 23 Japanese patients with amyotrophic lateral sclerosis. Clin. Genet. 1995, 47:158-160.
71. Kanouchi T., Ohkubo T., Yokota T. Can regional spreading of amyotrophic lateral sclerosis motor symptoms be explained by prion-like propagation?. J. Neurol. Neurosurg. Psychiatry 2012, 83:739-745.
72. Kawamata T., Akiyama H., Yamada T., McGeer P.L. Immunologic reactions in amyotrophic lateral sclerosis brain and spinal cord tissue. Am. J. Pathol. 1992, 140:691-707.
73. Kenna K.P., McLaughlin R.L., Byrne S., et al. Delineating the genetic heterogeneity of ALS using targeted high-throughput sequencing. J. Med. Genet. 2013, 50:776-783.
74. Kim H.J., Kim N.C., Wang Y.D., et al. Mutations in prion-like domains in hnRNPA2B1 and hnRNPA1 cause multisystem proteinopathy and ALS. Nature 2013, 495:467-473.
75. King A., Al-Sarraj S., Troakes C., et al. Mixed tau, TDP-43 and p62 pathology in FTLD associated with a C9ORF72 repeat expansion and p.Ala239Thr MAPT (tau) variant. Acta Neuropathol. 2013, 125:303-310.
76. Klein C.J., Wu Y., Duan X., et al. Novel SOD1 mutation discovered in atypical ALS by whole exome sequencing. J. Neurol. Neurosurg. Psychiatry 2013, 84:943-944.
77. Koppers M., Groen E.J., van Vught P.W., et al. Screening for rare variants in the coding region of ALS-associated genes at 9p21.2 and 19p13.3. Neurobiol. Aging 2013, 34. (1518 e5-7).
78. Kwiatkowski T.J., Bosco D.A., Leclerc A.L., et al. Mutations in the FUS/TLS gene on chromosome 16 cause familial amyotrophic lateral sclerosis. Science 2009, 323:1205-1208.
79. Laaksovirta H., Peuralinna T., Schymick J.C., et al. Chromosome 9p21 in amyotrophic lateral sclerosis in Finland: a genome-wide association study. Lancet Neurol. 2010, 9:978-985.
80. Lambrechts D., Storkebaum E., Morimoto M., et al. VEGF is a modifier of amyotrophic lateral sclerosis in mice and humans and protects motoneurons against ischemic death. Nat. Genet. 2003, 34:383-394.
81. Landers J.E., Melki J., Meininger V., et al. Reduced expression of the Kinesin-Associated Protein 3 (KIFAP3) gene increases survival in sporadic amyotrophic lateral sclerosis. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:9004-9009.
82. Lattante S., Conte A., Zollino M., et al. Contribution of major amyotrophic lateral sclerosis genes to the etiology of sporadic disease. Neurology 2012, 79:66-72.
83. Lesage S., Le Ber I., Condroyer C., et al. C9orf72 repeat expansions are a rare genetic cause of parkinsonism. Brain 2013, 136:385-391.
84. Levine T.P., Daniels R.D., Gatta A.T., Wong L.H., Hayes M.J. The product of C9orf72, a gene strongly implicated in neurodegeneration, is structurally related to DENN Rab-GEFs. Bioinformatics 2013, 29:499-503.
85. Ling S.C., Albuquerque C.P., Han J.S., et al. ALS-associated mutations in TDP-43 increase its stability and promote TDP-43 complexes with FUS/TLS. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:13318-13323.
86. Liscic R.M., Grinberg L.T., Zidar J., Gitcho M.A., Cairns N.J. ALS and FTLD: two faces of TDP-43 proteinopathy. Eur. J. Neurol. 2008, 15:772-780.
87. Logroscino G., Traynor B.J., Hardiman O., et al. Incidence of amyotrophic lateral sclerosis in Europe. J. Neurol. Neurosurg. Psychiatry 2010, 81:385-390.
88. Mackenzie I.R., Rademakers R., Neumann M. TDP-43 and FUS in amyotrophic lateral sclerosis and frontotemporal dementia. Lancet Neurol. 2010, 9:995-1007.
89. Maekawa S., Al-Sarraj S., Kibble M., et al. Cortical selective vulnerability in motor neuron disease: a morphometric study. Brain 2004, 127:1237-1251.
90. Majounie E., Renton A.E., Mok K., et al. Frequency of the C9orf72 hexanucleotide repeat expansion in patients with amyotrophic lateral sclerosis and frontotemporal dementia: a cross-sectional study. Lancet Neurol. 2012, 11:323-330.
91. Maruyama H., Morino H., Ito H., et al. Mutations of optineurin in amyotrophic lateral sclerosis. Nature 2010, 465:223-226.
92. Meyer T., Alber B., Roemer K., et al. High rate of constitutional chromosomal rearrangements in apparently sporadic ALS. Neurology 2003, 60:1348-1350.
93. Millecamps S., Boillee S., Le Ber I., et al. Phenotype difference between ALS patients with expanded repeats in C9ORF72 and patients with mutations in other ALS-related genes. J. Med. Genet. 2012, 49:258-263.
94. Mitchell J., Paul P., Chen H.J., et al. Familial amyotrophic lateral sclerosis is associated with a mutation in D-amino acid oxidase. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:7556-7561.
95. Mockrin S.C., Korn E.D. Acanthamoeba profilin interacts with G-actin to increase the rate of exchange of actin-bound adenosine 5'-triphosphate. Biochemistry 1980, 19:5359-5362.
96. Mok K., Traynor B.J., Schymick J., et al. Chromosome 9 ALS and FTD locus is probably derived from a single founder. Neurobiol. Aging 2012, 33. (209 e3-8).
97. Mori K., Weng S.M., Arzberger T., et al. The C9orf72 GGGGCC repeat is translated into aggregating dipeptide-repeat proteins in FTLD/ALS. Science 2013, 339:1335-1338.
98. Morita M., Al-Chalabi A., Andersen P.M., et al. A locus on chromosome 9p confers susceptibility to ALS and frontotemporal dementia. Neurology 2006, 66:839-844.
99. Munch C., Sedlmeier R., Meyer T., et al. Point mutations of the p150 subunit of dynactin (DCTN1) gene in ALS. Neurology 2004, 63:724-726.
100. Murayama S., Inoue K., Kawakami H., Bouldin T.W., Suzuki K. A unique pattern of astrocytosis in the primary motor area in amyotrophic lateral sclerosis. Acta Neuropathol. 1991, 82:456-461.
101. Neale B.M., Kou Y., Liu L., et al. Patterns and rates of exonic de novo mutations in autism spectrum disorders. Nature 2012, 485:242-245.
102. Neumann M., Sampathu D.M., Kwong L.K., et al. Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science 2006, 314:130-133.
103. Neumann M., Rademakers R., Roeber S., Baker M., Kretzschmar H.A., Mackenzie I.R. A new subtype of frontotemporal lobar degeneration with FUS pathology. Brain 2009, 132:2922-2931.
104. Ng S.B., Turner E.H., Robertson P.D., et al. Targeted capture and massively parallel sequencing of 12 human exomes. Nature 2009, 461:272-276.
105. Nishimura A.L., Mitne-Neto M., Silva H.C., Oliveira J.R., Vainzof M., Zatz M. A novel locus for late onset amyotrophic lateral sclerosis/motor neurone disease variant at 20q13. J. Med. Genet. 2004, 41:315-320.
106. Nishimura A.L., Mitne-Neto M., Silva H.C., et al. A mutation in the vesicle-trafficking protein VAPB causes late-onset spinal muscular atrophy and amyotrophic lateral sclerosis. Am. J. Hum. Genet. 2004, 75:822-831.
107. Orlacchio A., Babalini C., Borreca A., et al. SPATACSIN mutations cause autosomal recessive juvenile amyotrophic lateral sclerosis. Brain 2010, 133:591-598.
108. O'Roak B.J., Vives L., Girirajan S., et al. Sporadic autism exomes reveal a highly interconnected protein network of de novo mutations. Nature 2012, 485:246-250.
109. Parkinson N., Ince P.G., Smith M.O., et al. ALS phenotypes with mutations in CHMP2B (charged multivesicular body protein 2B). Neurology 2006, 67:1074-1077.
110. Rademakers R., van Blitterswijk M. Motor neuron disease in 2012: novel causal genes and disease modifiers. Nat. Rev. Neurol. 2013, 9:63-64.
111. Renton A.E., Majounie E., Waite A., et al. A hexanucleotide repeat expansion in C9ORF72 is the cause of chromosome 9p21-linked ALS-FTD. Neuron 2011, 72:257-268.
112. Ritson G.P., Custer S.K., Freibaum B.D., et al. TDP-43 mediates degeneration in a novel Drosophila model of disease caused by mutations in VCP/p97. J. Neurosci. 2010, 30:7729-7739.
113. Rosen D.R., Siddique T., Patterson D., et al. Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 1993, 362:59-62.
114. Saeed M., Siddique N., Hung W.Y., et al. Paraoxonase cluster polymorphisms are associated with sporadic ALS. Neurology 2006, 67:771-776.
115. Sanders S.J., Murtha M.T., Gupta A.R., et al. De novo mutations revealed by whole-exome sequencing are strongly associated with autism. Nature 2012, 485:237-241.
116. Sapp P.C., Hosler B.A., McKenna-Yasek D., et al. Identification of two novel loci for dominantly inherited familial amyotrophic lateral sclerosis. Am. J. Hum. Genet. 2003, 73:397-403.
117. Sawcer S., Hellenthal G., Pirinen M., et al. Genetic risk and a primary role for cell-mediated immune mechanisms in multiple sclerosis. Nature 2011, 476:214-219.
118. Schiffer D., Cordera S., Cavalla P., Migheli A. Reactive astrogliosis of the spinal cord in amyotrophic lateral sclerosis. J. Neurol. Sci. 1996, 139:27-33. (Suppl.).
119. Schymick J.C., Talbot K., Traynor B.J. Genetics of sporadic amyotrophic lateral sclerosis. Hum. Mol. Genet. 2007, 16(R2):R233-R242.
120. Schymick J.C., Yang Y., Andersen P.M., et al. Progranulin mutations and amyotrophic lateral sclerosis or amyotrophic lateral sclerosis-frontotemporal dementia phenotypes. J. Neurol. Neurosurg. Psychiatry 2007, 78:754-756.
121. Scott L.J., Mohlke K.L., Bonnycastle L.L., et al. A genome-wide association study of type 2 diabetes in Finns detects multiple susceptibility variants. Science 2007, 316:1341-1345.
122. Seelaar H., Klijnsma K.Y., de Koning I., et al. Frequency of ubiquitin and FUS-positive, TDP-43-negative frontotemporal lobar degeneration. J. Neurol. 2010, 257:747-753.
123. Shatunov A., Mok K., Newhouse S., et al. Chromosome 9p21 in sporadic amyotrophic lateral sclerosis in the UK and seven other countries: a genome-wide association study. Lancet Neurol. 2010, 9:986-994.
124. Siddique T., Pericak-Vance M.A., Brooks B.R., et al. Linkage analysis in familial amyotrophic lateral sclerosis. Neurology 1989, 39:919-925.
125. Siddique T., Figlewicz D.A., Pericak-Vance M.A., et al. Linkage of a gene causing familial amyotrophic lateral sclerosis to chromosome 21 and evidence of genetic-locus heterogeneity. N. Engl. J. Med. 1991, 324:1381-1384.
126. Simpson C.L., Lemmens R., Miskiewicz K., et al. Variants of the elongator protein 3 (ELP3) gene are associated with motor neuron degeneration. Hum. Mol. Genet. 2009, 18:472-481.
127. Sofola O.A., Jin P., Qin Y., et al. RNA-binding proteins hnRNP A2/B1 and CUGBP1 suppress fragile X CGG premutation repeat-induced neurodegeneration in a Drosophila model of FXTAS. Neuron 2007, 55:565-571.
128. Sreedharan J., Blair I.P., Tripathi V.B., et al. TDP-43 mutations in familial and sporadic amyotrophic lateral sclerosis. Science 2008, 319:1668-1672.
129. Staats K.A., Van Helleputte L., Jones A.R., et al. Genetic ablation of phospholipase C delta 1 increases survival in SOD1(G93A) mice. Neurobiol. Dis. 2013, 60:11-17.
130. Strong M.J., Hudson A.J., Alvord W.G. Familial amyotrophic lateral sclerosis, 1850-1989: a statistical analysis of the world literature. Can. J. Neurol. Sci. 1991, 18:45-58.
131. Suzuki N., Maroof A.M., Merkle F.T., et al. The mouse C9ORF72 ortholog is enriched in neurons known to degenerate in ALS and FTD. Nat. Neurosci. 2013, 16:1725-1727.
132. Therrien M., Rouleau G.A., Dion P.A., Parker J.A. Deletion of C9ORF72 results in motor neuron degeneration and stress sensitivity in C. elegans. PLoS One 2013, 8:e83450.
133. Ticozzi N., Vance C., Leclerc A.L., et al. Mutational analysis reveals the FUS homolog TAF15 as a candidate gene for familial amyotrophic lateral sclerosis. Am. J. Med. Genet. B Neuropsychiatr. Genet. 2011, 156B:285-290.
134. Turner M.R., Barnwell J., Al-Chalabi A., Eisen A. Young-onset amyotrophic lateral sclerosis: historical and other observations. Brain 2012, 135:2883-2891.
135. Udaka F., Kameyama M., Tomonaga M. Degeneration of Betz cells in motor neuron disease. A Golgi study. Acta Neuropathol. 1986, 70:289-295.
136. Valdmanis P.N., Dupre N., Bouchard J.P., et al. Three families with amyotrophic lateral sclerosis and frontotemporal dementia with evidence of linkage to chromosome 9p. Arch. Neurol. 2007, 64:240-245.
137. van Blitterswijk M., van Es M.A., Hennekam E.A., et al. Evidence for an oligogenic basis of amyotrophic lateral sclerosis. Hum. Mol. Genet. 2012, 21:3776-3784.
138. van Blitterswijk M., van Es M.A., Koppers M., et al. VAPB and C9orf72 mutations in 1 familial amyotrophic lateral sclerosis patient. Neurobiol. Aging 2012, 33. (2950 e1-4).
139. van Blitterswijk M., Baker M.C., DeJesus-Hernandez M., et al. C9ORF72 repeat expansions in cases with previously identified pathogenic mutations. Neurology 2013, 81:1332-1341.
140. van Blitterswijk M., Dejesus-Hernandez M., Niemantsverdriet E., et al. Association between repeat sizes and clinical and pathological characteristics in carriers of C9ORF72 repeat expansions (Xpansize-72): a cross-sectional cohort study. Lancet Neurol. 2013, 12:978-988.
141. Van Deerlin V.M., Sleiman P.M., Martinez-Lage M., et al. Common variants at 7p21 are associated with frontotemporal lobar degeneration with TDP-43 inclusions. Nat. Genet. 2010, 42:234-239.
142. van Es M.A., Van Vught P.W., Blauw H.M., et al. ITPR2 as a susceptibility gene in sporadic amyotrophic lateral sclerosis: a genome-wide association study. Lancet Neurol. 2007, 6:869-877.
143. van Es M.A., van Vught P.W., Blauw H.M., et al. Genetic variation in DPP6 is associated with susceptibility to amyotrophic lateral sclerosis. Nat. Genet. 2008, 40:29-31.
144. van Es M.A., Veldink J.H., Saris C.G., et al. Genome-wide association study identifies 19p13.3 (UNC13A) and 9p21.2 as susceptibility loci for sporadic amyotrophic lateral sclerosis. Nat. Genet. 2009, 41:1083-1087.
145. van Es M.A., Schelhaas H.J., van Vught P.W., et al. Angiogenin variants in Parkinson disease and amyotrophic lateral sclerosis. Ann. Neurol. 2011, 70:964-973.
146. Vance C., Al-Chalabi A., Ruddy D., et al. Familial amyotrophic lateral sclerosis with frontotemporal dementia is linked to a locus on chromosome 9p13.2-21.3. Brain 2006, 129:868-876.
147. Vance C., Rogelj B., Hortobagyi T., et al. Mutations in FUS, an RNA processing protein, cause familial amyotrophic lateral sclerosis type 6. Science 2009, 323:1208-1211.
148. Vissers L.E., de Ligt J., Gilissen C., et al. A de novo paradigm for mental retardation. Nat. Genet. 2010, 42:1109-1112.
149. Wain L.V., Pedroso I., Landers J.E., et al. The role of copy number variation in susceptibility to amyotrophic lateral sclerosis: genome-wide association study and comparison with published loci. PLoS One 2009, 4:e8175.
150. Wijesekera L.C., Leigh P.N. Amyotrophic lateral sclerosis. Orphanet J. Rare Dis. 2009, 4:3.
151. Williams K.L., Warraich S.T., Yang S., et al. UBQLN2/ubiquilin 2 mutation and pathology in familial amyotrophic lateral sclerosis. Neurobiol. Aging 2012, 33. (2527 e3-10).
152. Wills Z., Marr L., Zinn K., Goodman C.S., Van Vactor D. Profilin and the Abl tyrosine kinase are required for motor axon outgrowth in the Drosophila embryo. Neuron 1999, 22:291-299.
153. Wingo T.S., Cutler D.J., Yarab N., Kelly C.M., Glass J.D. The heritability of amyotrophic lateral sclerosis in a clinically ascertained United States research registry. PLoS One 2011, 6:e27985.
154. Winkelmann J., Schormair B., Lichtner P., et al. Genome-wide association study of restless legs syndrome identifies common variants in three genomic regions. Nat. Genet. 2007, 39:1000-1006.
155. Wu M.C., Lee S., Cai T., Li Y., Boehnke M., Lin X. Rare-variant association testing for sequencing data with the sequence kernel association test. Am. J. Hum. Genet. 2011, 89:82-93.
156. Wu C.H., Fallini C., Ticozzi N., et al. Mutations in the profilin 1 gene cause familial amyotrophic lateral sclerosis. Nature 2012, 488:499-503.
157. Xu Z., Poidevin M., Li X., et al. Expanded GGGGCC repeat RNA associated with amyotrophic lateral sclerosis and frontotemporal dementia causes neurodegeneration. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:7778-7783.
158. Yang Y., Hentati A., Deng H.X., et al. The gene encoding alsin, a protein with three guanine-nucleotide exchange factor domains, is mutated in a form of recessive amyotrophic lateral sclerosis. Nat. Genet. 2001, 29:160-165.
159. Yen A.A., Simpson E.P., Henkel J.S., Beers D.R., Appel S.H. HFE mutations are not strongly associated with sporadic ALS. Neurology 2004, 62:1611-1612.
160. Zhang D., Iyer L.M., He F., Aravind L. Discovery of novel DENN proteins: implications for the evolution of eukaryotic intracellular membrane structures and human disease. Front. Genet. 2012, 3:283.