Identification of mutations in Korean patients with amyotrophic lateral sclerosis using multigene panel testing

Neurobiology of Aging

Volumn 37, Issue , 2016, Pages 209.e9-209.e16

  Kim, Hee Jung ^a   Oh, Ki Wook ^b,c   Kwon, Min Jung ^d   Oh, Seong il ^e   Park, Jin seok ^b,c   Kim, Young Eun ^f   Choi, Byung Ok ^f   Lee, Seungbok ^g   Ki, Chang Seok ^f   Kim, Seung Hyun ^b,c  

^a Green Cross Corporation   (South Korea)

^b Hanyang University College of Medicine   (South Korea)

^c Hanyang University College of Medicine   (South Korea)

^d Sungkyunkwan University School of Medicine   (South Korea)

^e Inje University College of Medicine   (South Korea)

^f Sungkyunkwan University School of Medicine   (South Korea)

^g Seoul National University   (South Korea)

Author keywords

ALS; Amyotrophic lateral sclerosis; Multigene panel; Mutation; Next generation sequencing; NGS

Indexed keywords

COPPER ZINC SUPEROXIDE DISMUTASE; SEQUESTOSOME 1; ALS2 PROTEIN, HUMAN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; MAPT PROTEIN, HUMAN; SIGNAL TRANSDUCING ADAPTOR PROTEIN; SQSTM1 PROTEIN, HUMAN; SUPEROXIDE DISMUTASE; TAU PROTEIN;

ADULT; ALS2 GENE; AMYOTROPHIC LATERAL SCLEROSIS; ARTICLE; CONTROLLED STUDY; FEMALE; GENE; GENE FREQUENCY; GENE SEQUENCE; GENETIC ANALYSIS; GENETIC HETEROGENEITY; GENETIC VARIABILITY; HUMAN; KOREAN (PEOPLE); MAJOR CLINICAL STUDY; MALE; MAPT GENE; MISSENSE MUTATION; MULTIGENE PANEL TESTING; PATHOGENESIS; SOD1 GENE; SQSTM1 GENE; AGED; ASIAN CONTINENTAL ANCESTRY GROUP; GENETIC ASSOCIATION STUDY; GENETIC SCREENING; GENETICS; HIGH THROUGHPUT SEQUENCING; MIDDLE AGED; MULTIGENE FAMILY; MUTATION; PROCEDURES;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ADULT; AGED; AMYOTROPHIC LATERAL SCLEROSIS; ASIAN CONTINENTAL ANCESTRY GROUP; FEMALE; GENETIC ASSOCIATION STUDIES; GENETIC TESTING; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; MALE; MIDDLE AGED; MULTIGENE FAMILY; MUTATION; SUPEROXIDE DISMUTASE; TAU PROTEINS;

EID: 84991311810     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2015.09.012     Document Type: Article

References (39)

1. Botstein, D., Risch, N., Discovering genotypes underlying human phenotypes: past successes for mendelian disease, future approaches for complex disease. Nat. Genet. 33:Suppl (2003), 228–237.
2. Brooks, B.R., Miller, R.G., Swash, M., Munsat, T.L., El Escorial revisited: revised criteria for the diagnosis of amyotrophic lateral sclerosis. Amyotroph. Lateral Scler. Other Motor Neuron Disord. 1 (2000), 293–299.
3. Cedarbaum, J.M., Stambler, N., Malta, E., Fuller, C., Hilt, D., Thurmond, B., Nakanishi, A., The ALSFRS-R: a revised ALS functional rating scale that incorporates assessments of respiratory function. BDNF ALS Study Group (Phase III). J. Neurol. Sci. 169 (1999), 13–21.
4. Chio, A., Traynor, B.J., Lombardo, F., Fimognari, M., Calvo, A., Ghiglione, P., Mutani, R., Restagno, G., Prevalence of SOD1 mutations in the Italian ALS population. Neurology 70 (2008), 533–537.
5. Cooper-Knock, J., Hewitt, C., Highley, J.R., Brockington, A., Milano, A., Man, S., Martindale, J., Hartley, J., Walsh, T., Gelsthorpe, C., Baxter, L., Forster, G., Fox, M., Bury, J., Mok, K., McDermott, C.J., Traynor, B.J., Kirby, J., Wharton, S.B., Ince, P.G., Hardy, J., Shaw, P.J., Clinico-pathological features in amyotrophic lateral sclerosis with expansions in C9ORF72. Brain J. Neurol. 135 (2012), 751–764.
6. Couthouis, J., Hart, M.P., Shorter, J., DeJesus-Hernandez, M., Erion, R., Oristano, R., Liu, A.X., Ramos, D., Jethava, N., Hosangadi, D., Epstein, J., Chiang, A., Diaz, Z., Nakaya, T., Ibrahim, F., Kim, H.J., Solski, J.A., Williams, K.L., Mojsilovic-Petrovic, J., Ingre, C., Boylan, K., Graff-Radford, N.R., Dickson, D.W., Clay-Falcone, D., Elman, L., McCluskey, L., Greene, R., Kalb, R.G., Lee, V.M., Trojanowski, J.Q., Ludolph, A., Robberecht, W., Andersen, P.M., Nicholson, G.A., Blair, I.P., King, O.D., Bonini, N.M., Van Deerlin, V., Rademakers, R., Mourelatos, Z., Gitler, A.D., A yeast functional screen predicts new candidate ALS disease genes. Proc. Natl. Acad. Sci. U. S. A. 108 (2011), 20881–20890.
7. Couthouis, J., Raphael, A.R., Daneshjou, R., Gitler, A.D., Targeted exon capture and sequencing in sporadic amyotrophic lateral sclerosis. PLoS Genet., 10, 2014, e1004704.
8. Daoud, H., Valdmanis, P.N., Gros-Louis, F., Belzil, V., Spiegelman, D., Henrion, E., Diallo, O., Desjarlais, A., Gauthier, J., Camu, W., Dion, P.A., Rouleau, G.A., Resequencing of 29 candidate genes in patients with familial and sporadic amyotrophic lateral sclerosis. Arch. Neurol. 68 (2011), 587–593.
9. DeJesus-Hernandez, M., Kocerha, J., Finch, N., Crook, R., Baker, M., Desaro, P., Johnston, A., Rutherford, N., Wojtas, A., Kennelly, K., Wszolek, Z.K., Graff-Radford, N., Boylan, K., Rademakers, R., De novo truncating FUS gene mutation as a cause of sporadic amyotrophic lateral sclerosis. Hum. Mutat. 31 (2010), E1377–E1389.
10. Deng, H.X., Chen, W., Hong, S.T., Boycott, K.M., Gorrie, G.H., Siddique, N., Yang, Y., Fecto, F., Shi, Y., Zhai, H., Jiang, H., Hirano, M., Rampersaud, E., Jansen, G.H., Donkervoort, S., Bigio, E.H., Brooks, B.R., Ajroud, K., Sufit, R.L., Haines, J.L., Mugnaini, E., Pericak-Vance, M.A., Siddique, T., Mutations in UBQLN2 cause dominant X-linked juvenile and adult-onset ALS and ALS/dementia. Nature 477 (2011), 211–215.
11. Dion, P.A., Daoud, H., Rouleau, G.A., Genetics of motor neuron disorders: new insights into pathogenic mechanisms. Nat. Rev. Genet. 10 (2009), 769–782.
12. Eisen, A., Mezei, M.M., Stewart, H.G., Fabros, M., Gibson, G., Andersen, P.M., SOD1 gene mutations in ALS patients from British Columbia, Canada: clinical features, neurophysiology and ethical issues in management. Amyotroph. Lateral Scler. 9 (2008), 108–119.
13. 1000 Genomes Project Consortium et al., 2012 1000 Genomes Project Consortium, Abecasis, G.R., Auton, A., Brooks, L.D., DePristo, M.A., Durbin, R.M., Handsaker, R.E., Kang, H.M., Marth, G.T., McVean, G.A., An integrated map of genetic variation from 1,092 human genomes. Nature 491 (2012), 56–65.
14. Gros-Louis, F., Andersen, P.M., Dupre, N., Urushitani, M., Dion, P., Souchon, F., D'Amour, M., Camu, W., Meininger, V., Bouchard, J.P., Rouleau, G.A., Julien, J.P., Chromogranin B P413L variant as risk factor and modifier of disease onset for amyotrophic lateral sclerosis. Proc. Natl. Acad. Sci. U. S. A. 106 (2009), 21777–21782.
15. Hand, C.K., Mayeux-Portas, V., Khoris, J., Briolotti, V., Clavelou, P., Camu, W., Rouleau, G.A., Compound heterozygous D90A and D96N SOD1 mutations in a recessive amyotrophic lateral sclerosis family. Ann. Neurol. 49 (2001), 267–271.
16. Hayashi, S., Toyoshima, Y., Hasegawa, M., Umeda, Y., Wakabayashi, K., Tokiguchi, S., Iwatsubo, T., Takahashi, H., Late-onset frontotemporal dementia with a novel exon 1 (Arg5His) tau gene mutation. Ann. Neurol. 51 (2002), 525–530.
17. Hayward, C., Brock, D.J., Minns, R.A., Swingler, R.J., Homozygosity for Asn86Ser mutation in the CuZn-superoxide dismutase gene produces a severe clinical phenotype in a juvenile onset case of familial amyotrophic lateral sclerosis. J. Med. Genet., 35, 1998, 174.
18. Hirano, M., Nakamura, Y., Saigoh, K., Sakamoto, H., Ueno, S., Isono, C., Miyamoto, K., Akamatsu, M., Mitsui, Y., Kusunoki, S., Mutations in the gene encoding p62 in Japanese patients with amyotrophic lateral sclerosis. Neurology 80 (2013), 458–463.
19. Jang, J.H., Kwon, M.J., Choi, W.J., Oh, K.W., Koh, S.H., Ki, C.S., Kim, S.H., Analysis of the C9orf72 hexanucleotide repeat expansion in Korean patients with familial and sporadic amyotrophic lateral sclerosis. Neurobiol. Aging 34 (2013), 1311.e7–1311.e9.
20. Jang, M.A., Lee, S.H., Kim, N., Ki, C.S., Frequency and spectrum of actionable pathogenic secondary findings in 196 Korean exomes. Genet. Med., 2015 in press.
21. Johnson, J.O., Mandrioli, J., Benatar, M., Abramzon, Y., Van Deerlin, V.M., Trojanowski, J.Q., Gibbs, J.R., Brunetti, M., Gronka, S., Wuu, J., Ding, J., McCluskey, L., Martinez-Lage, M., Falcone, D., Hernandez, D.G., Arepalli, S., Chong, S., Schymick, J.C., Rothstein, J., Landi, F., Wang, Y.D., Calvo, A., Mora, G., Sabatelli, M., Monsurro, M.R., Battistini, S., Salvi, F., Spataro, R., Sola, P., Borghero, G., ITALSGEN Consortium., Galassi, G., Scholz, S.W., Taylor, J.P., Restagno, G., Chio, A., Traynor, B.J., Exome sequencing reveals VCP mutations as a cause of familial ALS. Neuron 68 (2010), 857–864.
22. Kim, H.J., Kwon, M.J., Choi, W.J., Oh, K.W., Oh, S.I., Ki, C.S., Kim, S.H., Mutations in UBQLN2 and SIGMAR1 genes are rare in Korean patients with amyotrophic lateral sclerosis. Neurobiol. Aging 35 (2014), 1957.e7–1957.e8.
23. Kimura, F., Fujimura, C., Ishida, S., Nakajima, H., Furutama, D., Uehara, H., Shinoda, K., Sugino, M., Hanafusa, T., Progression rate of ALSFRS-R at time of diagnosis predicts survival time in ALS. Neurology 66 (2006), 265–267.
24. Kumar, P., Henikoff, S., Ng, P.C., Predicting the effects of coding non-synonymous variants on protein function using the SIFT algorithm. Nat. Protoc. 4 (2009), 1073–1081.
25. Kwon, M.J., Baek, W., Ki, C.S., Kim, H.Y., Koh, S.H., Kim, J.W., Kim, S.H., Screening of the SOD1, FUS, TARDBP, ANG, and OPTN mutations in Korean patients with familial and sporadic ALS. Neurobiol. Aging 33 (2012), 1017.e17–1017.e23.
26. Lagier-Tourenne, C., Cleveland, D.W., Rethinking ALS: the FUS about TDP-43. Cell 136 (2009), 1001–1004.
27. Millecamps, S., Salachas, F., Cazeneuve, C., Gordon, P., Bricka, B., Camuzat, A., Guillot-Noel, L., Russaouen, O., Bruneteau, G., Pradat, P.F., Le Forestier, N., Vandenberghe, N., Danel-Brunaud, V., Guy, N., Thauvin-Robinet, C., Lacomblez, L., Couratier, P., Hannequin, D., Seilhean, D., Le Ber, I., Corcia, P., Camu, W., Brice, A., Rouleau, G., LeGuern, E., Meininger, V., SOD1, ANG, VAPB, TARDBP, and FUS mutations in familial amyotrophic lateral sclerosis: genotype-phenotype correlations. J. Med. Genet. 47 (2010), 554–560.
28. Mitchell, J.D., Guidelines in motor neurone disease (MND)/amyotrophic lateral sclerosis (ALS) - from diagnosis to patient care. J. Neurol. 247:Suppl 6 (2000), VI/7–VI12.
29. Neumann, M., Sampathu, D.M., Kwong, L.K., Truax, A.C., Micsenyi, M.C., Chou, T.T., Bruce, J., Schuck, T., Grossman, M., Clark, C.M., McCluskey, L.F., Miller, B.L., Masliah, E., Mackenzie, I.R., Feldman, H., Feiden, W., Kretzschmar, H.A., Trojanowski, J.Q., Lee, V.M., Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science 314 (2006), 130–133.
30. Orlacchio, A., Babalini, C., Borreca, A., Patrono, C., Massa, R., Basaran, S., Munhoz, R.P., Rogaeva, E.A., St George-Hyslop, P.H., Bernardi, G., Kawarai, T., SPATACSIN mutations cause autosomal recessive juvenile amyotrophic lateral sclerosis. Brain J. Neurol. 133 (2010), 591–598.
31. Radunovic, A., Leigh, P.N., Cu/Zn superoxide dismutase gene mutations in amyotrophic lateral sclerosis: correlation between genotype and clinical features. J. Neurol. Neurosurg. Psychiatry 61 (1996), 565–572.
32. Renton, A.E., Chio, A., Traynor, B.J., State of play in amyotrophic lateral sclerosis genetics. Nat. Neurosci. 17 (2014), 17–23.
33. Rosen, D.R., Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature, 364, 1993, 362.
34. Rowland, L.P., Shneider, N.A., Amyotrophic lateral sclerosis. N. Engl. J. Med. 344 (2001), 1688–1700.
35. Sunyaev, S., Ramensky, V., Koch, I., Lathe, W. 3rd, Kondrashov, A.S., Bork, P., Prediction of deleterious human alleles. Hum. Mol. Genet. 10 (2001), 591–597.
36. Takahashi, Y., Seki, N., Ishiura, H., Mitsui, J., Matsukawa, T., Kishino, A., Onodera, O., Aoki, M., Shimozawa, N., Murayama, S., Itoyama, Y., Suzuki, Y., Sobue, G., Nishizawa, M., Goto, J., Tsuji, S., Development of a high-throughput microarray-based resequencing system for neurological disorders and its application to molecular genetics of amyotrophic lateral sclerosis. Arch. Neurol. 65 (2008), 1326–1332.
37. Teyssou, E., Takeda, T., Lebon, V., Boillee, S., Doukoure, B., Bataillon, G., Sazdovitch, V., Cazeneuve, C., Meininger, V., LeGuern, E., Salachas, F., Seilhean, D., Millecamps, S., Mutations in SQSTM1 encoding p62 in amyotrophic lateral sclerosis: genetics and neuropathology. Acta Neuropathol. 125 (2013), 511–522.
38. van Blitterswijk, M., van Es, M.A., Hennekam, E.A., Dooijes, D., van Rheenen, W., Medic, J., Bourque, P.R., Schelhaas, H.J., van der Kooi, A.J., de Visser, M., de Bakker, P.I., Veldink, J.H., van den Berg, L.H., Evidence for an oligogenic basis of amyotrophic lateral sclerosis. Hum. Mol. Genet. 21 (2012), 3776–3784.
39. Wu, C.H., Fallini, C., Ticozzi, N., Keagle, P.J., Sapp, P.C., Piotrowska, K., Lowe, P., Koppers, M., McKenna-Yasek, D., Baron, D.M., Kost, J.E., Gonzalez-Perez, P., Fox, A.D., Adams, J., Taroni, F., Tiloca, C., Leclerc, A.L., Chafe, S.C., Mangroo, D., Moore, M.J., Zitzewitz, J.A., Xu, Z.S., van den Berg, L.H., Glass, J.D., Siciliano, G., Cirulli, E.T., Goldstein, D.B., Salachas, F., Meininger, V., Rossoll, W., Ratti, A., Gellera, C., Bosco, D.A., Bassell, G.J., Silani, V., Drory, V.E., Brown, R.H. Jr., Landers, J.E., Mutations in the profilin 1 gene cause familial amyotrophic lateral sclerosis. Nature 488 (2012), 499–503.