Overexpression of KLC2 due to a homozygous deletion in the non-coding region causes SPOAN syndrome

Human Molecular Genetics

Volumn 24, Issue 24, 2015, Pages 6877-6885

  Melo, Uirá S ^a   Macedo Souza, Lucia I ^a   Figueiredo, Thalita ^b,c   Muotri, Alysson R ^d   Gleeson, Joseph G ^e   Coux, Gabriela ^f   Armas, Pablo ^f   Calcaterra, Nora B ^f   Kitajima, João P ^g   Amorim, Simone ^a   Olávio, Thiago R ^a   Griesi Oliveira, Karina ^a   Coatti, Giuliana C ^a   Rocha, Clarissa R R ^a   Martins Pinheiro, Marinalva ^a   Menck, Carlos F M ^a   Zaki, Maha S ^h   Kok, Fernando ^a,g   Zatz, Mayana ^a   Santos, Silvana ^b,c  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b FEDERAL UNIVERSITY OF PARAÍBA   (Brazil)

^c STATE UNIVERSITY OF PARAÍBA   (Brazil)

^d RADY CHILDREN'S HOSPITAL   (United States)

^e ROCKEFELLER UNIVERSITY   (United States)

^f UNIVERSIDAD NACIONAL DE ROSARIO   (Argentina)

^g Mendelics Genomic Analysis   (Brazil)

^h NATIONAL RESEARCH CENTRE   (Egypt)

Author keywords

[No Author keywords available]

Indexed keywords

KINESIN; KINESIN LIGHT CHAIN 2; UNCLASSIFIED DRUG; KINESIN LIGHT-CHAIN PROTEINS; MICROTUBULE ASSOCIATED PROTEIN; ZEBRAFISH PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DEGENERATIVE DISEASE; DISEASE SEVERITY; EXOME; FIBROBLAST; GENE DELETION; GENE MUTATION; GENE OVEREXPRESSION; GENE SEQUENCE; HUMAN; LUCIFERASE ASSAY; MOTONEURON; NEUROPATHY; NEXT GENERATION SEQUENCING; NONHUMAN; OPTIC NERVE ATROPHY; PHENOTYPE; PRIORITY JOURNAL; SPASTIC PARAPLEGIA; SPOAN SYNDROME; ZEBRA FISH; ANIMAL; CHROMOSOME 11; DNA MUTATIONAL ANALYSIS; GENE EXPRESSION; GENETICS; HEREDITARY MOTOR SENSORY NEUROPATHY; HEREDITARY OPTIC ATROPHY; SYNDROME;

ANIMALS; CHROMOSOMES, HUMAN, PAIR 11; DNA MUTATIONAL ANALYSIS; GENE EXPRESSION; HEREDITARY SENSORY AND MOTOR NEUROPATHY; HUMANS; MICROTUBULE-ASSOCIATED PROTEINS; OPTIC ATROPHIES, HEREDITARY; SEQUENCE DELETION; SPASTIC PARAPLEGIA, HEREDITARY; SYNDROME; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84959237166     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddv388     Document Type: Article

References (53)

1. Lo Giudice, T., Lombardi, F., Santorelli, F.M., Kawarai, T. and Orlacchio, A. (2014) Hereditary spastic paraplegia: clinicalgenetic characteristics and evolving molecular mechanisms. Exp. Neurol. Nov., 261, 518-539.
2. Macedo-Souza, L., Kok, F., Santos, S., Amorim, S.C., Starling, A., Nishimura, A., Lezirovitz, K., Lino, A.M. and Zatz, M. (2005) Spastic paraplegia, optic atrophy, and neuropathy is linked to chromosome 11q13. Ann. Neurol., 57, 730-737.
3. Macedo-Souza, L., Kok, F., Santos, S., Licinio, L., Lezirovitz, K., Cavaçana, N., Bueno, C., Amorim, S., Pessoa, A., Graciani, Z. et al. (2009) Spastic paraplegia, optic atrophy, and neuropathy: new observations, locus refinement, and exclusion of candidate genes. Ann. Hum. Genet., 73, 382-387.
4. Windpassinger, C., Auer-Grumbach, M., Irobi, J., Patel, H., Petek, E., Hörl, G., Malli, R., Reed, J.A., Dierick, I., Verpoorten, N. et al. (2004) Heterozygous missense mutations in BSCL2 are associated with distal hereditary motor neuropathy and Silver syndrome. Nat. Genet., 36, 271-276.
5. Novarino, G., Fenstermaker, A.G., Zaki, M.S., Hofree, M., Silhavy, J.L., Heiberg, A.D., Abdellateef, M., Rosti, B., Scott, E., Mansour, L. et al. (2014) Exome sequencing links corticospinal motor neuron disease to common neurodegenerative disorders. Science, 31, 506-511.
6. Vale, R.D. (2003) The molecular motor toolbox for intracellular transport. Cell, 112, 467-480.
7. Hirokawa, N., Noda, Y., Tanaka, Y. and Niwa, S. (2009) Kinesin superfamily motor proteins and intracellular transport. Nat. Rev. Mol. Cell Biol., 10, 682-696.
8. Visscher, K., Schnitzer, M.J. and Block, S.M. (1999) Single kinesin molecules studied with a molecular force clamp. Nature, 400, 184-189.
9. Verhey, K.J. and Hammond, J.W. (2009) Traffic control: regulation of kinesin motors. Nat. Rev. Mol. Cell Biol., 10, 765-777.
10. Hirokawa, N., Niwa, S. and Tanaka, Y. (2010) Molecular motors in neurons: transport mechanisms and roles in brain function, development, and disease. Neuron, 68, 610-638.
11. Pernigo, S., Lamprecht, A., Steiner, R.A. and Dodding, M.P. (2013) Structural basis for kinesin-1: cargo recognition. Science, 340, 356-359.
12. Rahman, A., Friedman, D.S. and Goldstein, L.S.B. (1998) Two kinesin light chain genes in mice: identification and characterization of the encoded proteins. J. Biol. Chem., 273, 15395- 15403.
13. Perlson, E., Maday, S., Fu, M.M., Moughamian, A.J. and Holzbaur, E.L. (2010) Retrograde axonal transport: pathways to cell death? Trends Neurosci., 33, 335.
14. Millecamps, S. and Julien, J.P. (2013) Axonal transport deficits and neurodegenerative diseases. Nat. Rev. Neurosci., 14, 161- 176.
15. Reid, E., Kloos, M., Ashley-Koch, A., Hughes, L., Bevan, S., Svenson, I.K., Graham, F.L., Gaskell, P.C., Dearlove, A., Pericak-Vance, M.A. et al. (2002) A kinesin heavy chain (KIF5A) mutation in hereditary spastic paraplegia (SPG10). Am. J. Hum. Genet., 71, 1189-1194.
16. Ebbing, B., Mann, K., Starosta, A., Jaud, J., Schöls, L., Schüle, R. andWoehlke, G. (2008) Effect of spastic paraplegia mutations in KIF5A kinesin on transport activity. Hum. Mol. Genet., 17, 1245-1252.
17. Caballero Oteyza, A., Battaloğlu, E., Ocek, L., Lindig, T., Reichbauer, J., Rebelo, A.P., Gonzalez, M.A., Zorlu, Y., Ozes, B., Timmann, D. et al. (2014) Motor protein mutations cause a new form of hereditary spastic paraplegia. Neurology, 3, 2007-2016.
18. Lee, J., Srour, M., Kim, D., Hamdan, F.F., Lim, S.H., Brunel- Guitton, C., Décarie, J.C., Rossignol, E., Mitchell, G.A., Schreiber, A. et al. (2015) De novomutations in themotor domain of KIF1A cause cognitive impairment, spastic paraparesis, axonal neuropathy and cerebellar atrophy. Hum. Mutat., 36, 69-78.
19. Munch, C., Rosenbohm, A., Sperfeld, A.D., Uttner, I., Reske, S., Krause, B.J., Sedlmeier, R., Meyer, T., Hanemann, C.O., Stumm, G. et al. (2005) Heterozygous R1101K mutation of the DCTN1 gene in a family with ALS and FTD. Ann. Neurol., 58, 777.
20. Falzone, T.L., Stokin, G.B., Lillo, C., Rodrigues, E.M., Westerman, E.L., Williams, D.S. and Goldstein, L.S. (2009) Axonal stress kinase activation and tau misbehavior induced by kinesin-1 transport defects. J. Neurosci., 29, 5758.
21. Füger, P., Sreekumar, V., Schüle, R., Kern, J.V., Stanchev, D.T., Schneider, C.D., Karle, K.N., Daub, K.J., Siegert, V.K., Flötenmeyer, M. et al. (2012) Spastic paraplegia mutation N256S in the neuronal microtubule motor KIF5A disrupts axonal transport in a Drosophila HSP model. PLoS Genet., 8, e1003066.
22. Valdmanis, P.N., Meijer, I.A., Reynolds, A., Lei, A., MacLeod, P., Schlesinger, D., Zatz, M., Reid, E., Dion, P.A., Drapeau, P. et al. (2007) Mutations in the KIAA0196 gene at the SPG8 locus cause hereditary spastic paraplegia. Am. J. Hum. Genet., 80, 152-161.
23. Lin, P., Li, J., Liu, Q., Mao, F., Li, J., Qiu, R., Hu, H., Song, Y., Yang, Y., Gao, G. et al. (2008) A missense mutation in SLC33A1, which encodes the acetyl-CoA transporter, causes autosomal- dominant spastic paraplegia (SPG42). Am. J. Hum. Genet., 83, 752-759.
24. Clemen, C.S., Tangavelou, K., Strucksberg, K.H., Just, S., Gaertner, L., Regus-Leidig, H., Stumpf, M., Reimann, J., Coras, R., Morgan, R.O. et al. (2010) Strumpellin is a novel valosin-containing protein binding partner linking hereditary spastic paraplegia to protein aggregation diseases. Brain, 133, 2920-2941.
25. Fassier, C., Hutt, J.A., Scholpp, S., Lumsden, A., Giros, B., Nothias, F., Schneider-Maunoury, S., Houart, C. and Hazan, J. (2010) Zebrafish atlastin controls motility and spinal motor axon architecture via inhibition of the BMP pathway. Nat. Neurosci., 13, 1380-1387.
26. Martin, E., Yanicostas, C., Rastetter, A., Naini, S.M., Maouedj, A., Kabashi, E., Rivaud-Péchoux, S., Brice, A., Stevanin, G. and Soussi-Yanicostas, N. (2012) Spatacsin and spastizin act in the same pathway required for proper spinal motor neuron axon outgrowth in zebrafish. Neurobiol. Dis., 48, 299-308.
27. Martin, E., Schüle, R., Smets, K., Rastetter, A., Boukhris, A., Loureiro, J.L., Gonzalez, M.A., Mundwiller, E., Deconinck, T., Wessner, M. et al. (2013) Loss of function of glucocerebrosidase GBA2 is responsible for motor neuron defects in hereditary spastic paraplegia. Am. J. Hum. Genet., 92, 238-244.
28. Song, Y., Wang, M., Mao, F., Shao, M., Zhao, B., Song, Z., Shao, C. and Gong, Y. (2013) Knockdown of Pnpla6 protein results in motor neuron defects in zebrafish. Dis. Model Mech., 6, 404-413.
29. Cremers, F.P.M., Pfeiffer, R.A., van de Pol, T.J., Hofker, M.H., Kruse, T.A., Wieringa, B. and Ropers, H.H. (1987) An interstitial duplication of the X chromosome in a male allows physical fine mapping of probes from the Xq13-q22 region. Hum. Genet., 77, 23-27.
30. Hodes, M.E., Pratt, V.M. and Dlouhy, S.R. (1993) Genetics of Pelizaeus-Merzbacher disease. Dev. Neurosci., 15, 383-394.
31. Inoue, K., Osaka, H., Sugiyama, N., Kawanishi, C., Onishi, H., Nezu, A., Kimura, K., Yamada, Y. and Kosaka, K. (1996) A duplicated PLP gene causing Pelizaeus-Merzbacher disease detected by comparative multiplex PCR. Am. J. Hum. Genet., 59, 32-39.
32. Mimault, C., Giraud, G., Courtois, V., Cailloux, F., Boire, J.Y., Dastugue, B. and Boespflug-Tanguy, O. (1999) Clinical European network on brain dysmyelinating disease. Proteolipoprotein gene analysis in 82 patients with sporadic Pelizaeus- Merzbacher disease: duplications, the major cause of the disease, originate more frequently in male germ cells, but point mutations do not. Am. J. Hum. Genet., 65, 360-369.
33. Carvalho, C.M.B., Ramocki, M.B., Pehlivan, D., Franco, L.M., Gonzaga-Jauregui, C., Fang, P., McCall, A., Pivnick, E.K., Hines-Dowell, S., Seaver, L.H. et al. (2011) Inverted genomic segments and complex triplication rearrangements are mediated by inverted repeats in the human genome. Nat. Genet., 43, 1074-1081.
34. Hertz, J.M., Borglum, A.D., Brandt, C.A., Flint, T. and Bisgaard, C. (1994) Charcot-Marie-Tooth disease type 1A: the parental origin of a de novo 17p11.2-p12 duplication. Clin. Genet., 46, 291-294.
35. Sorour, E., Thompson, P., MacMillan, J. and Upadhyaya, M. (1995) Inheritance of CMT1A duplication from a mosaic father. J. Med. Genet., 32, 483-485.
36. Theuns, J., Brouwers, N., Engelborghs, S., Sleegers, K., Bogaerts, V., Corsmit, E., De Pooter, T., van Duijn, C.M., De Deyn, P.P. and Van Broeckhoven, C. (2006) Promoter mutations that increase amyloid precursor-protein expression are associated with Alzheimer disease. Am. J. Hum. Genet., 78, 936-946.
37. Nagaraj, K., Kristiansen, L.V., Skrzynski, A., Castiella, C., Garcia- Alonso, L. and Hortsch, M. (2009) Pathogenic human L1-CAM mutations reduce the adhesion-dependent activation of EGFR. Hum. Mol. Genet., 18, 3822-3831.
38. Meijer, I.A., Dion, P., Laurent, S., Dupré, N., Brais, B., Levert, A., Puymirat, J., Rioux, M.F., Sylvain, M., Zhu, P.P. et al. (2007) Characterization of a novel SPG3A deletion in a French-Canadian family. Ann. Neurol., 61, 599-603.
39. Havlicek, S., Kohl, Z., Mishra, H.K., Prots, I., Eberhardt, E., Denguir, N., Wend, H., Plötz, S., Boyer, L., Marchetto, M.C. et al. (2014) Gene dosage-dependent rescue of HSP neurite defects in SPG4 patients' neurons. Hum. Mol. Genet., 15, 2527-2541.
40. Bakowska, J.C., Wang, H., Xin, B., Sumner, C.J. and Blackstone, C. (2008) Lack of spartin protein in Troyer syndrome: a loss-offunction disease mechanism? Arch. Neurol., 65, 520-524.
41. Kruer, M.C., Paisán-Ruiz, C., Boddaert, N., Yoon, M.Y., Hama, H., Gregory, A., Malandrini, A., Woltjer, R.L., Munnich, A., Gobin, S. et al. (2010) Defective FA2H leads to a novel form of neurodegeneration with brain iron accumulation (NBIA). Ann. Neurol., 68, 611-618.
42. Li, H. and Durbin, R. (2010) Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics, 26, 589-595.
43. McKenna, A., Hanna, M., Banks, E., Sivachenko, A., Cibulskis, K., Kernytsky, A., Garimella, K., Altshuler, D., Gabriel, S., Daly, M. et al. (2010) The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res., 20, 1297-1303.
44. Wang, K., Li, M. and Hakonarson, H. (2010) ANNOVAR: Functional annotation of genetic variants from next-generation sequencing data. Nucleic Acids Res., 38, e164.
45. Plagnol, V., Curtis, J., Epstein, M., Mok, K.Y., Stebbings, E., Grigoriadou, S., Wood, N.W., Hambleton, S., Burns, S.O., Thrasher, A.J. et al. (2012) A robust model for read count data in exome sequencing experiments and implications for copy number variant calling. Bioinformatics, 28, 2747-2754.
46. Cingolani, P., Platts, A., Wang le, L., Coon, M., Nguyen, T., Wang, L., Land, S.J., Lu, X. and Ruden, D.M. (2012) A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly, 6, 80-92.
47. Marchetto, M.C., Carromeu, C., Acab, A., Yu, D., Yeo, G.W., Mu, Y., Chen, G., Gage, F.H. and Muotri, A.R. (2010) A model for neural development and treatment of Rett syndrome using human induced pluripotent stem cells. Cell, 12, 527-539.
48. Mitne-Neto, M., Machado-Costa, M., Marchetto, M.C., Bengtson, M.H., Joazeiro, C.A., Tsuda, H., Bellen, H.J., Silva, H.C., Oliveira, A.S., Lazar, M. et al. (2011) Downregulation of VAPB expression in motor neurons derived from induced pluripotent stem cells of ALS8 patients. Hum. Mol. Genet., 15, 3642- 3652.
49. Irizarry, R.A., Hobbs, B., Collin, F., Beazer-Barclay, Y.D., Antonellis, K.J., Scherf, U. and Speed, T.P. (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics, 4, 249-264.
50. Schmittgen, T.D. and Livak, K.J. (2008) Analyzing real-time PCR data by the comparative C(T)method. Nat. Protoc., 3, 1101-1108.
51. Soltys, D.T., Rocha, C.R., Lerner, L.K., de Souza, T.A., Munford, V., Cabral, F., Nardo, T., Stefanini, M., Sarasin, A., Cabral-Neto, J.B. et al. (2013) Novel XPG (ERCC5) mutations affect DNA repair and cell survival after ultraviolet but not oxidative stress. Hum. Mutat., 34, 481-489.
52. Favaro, F.P., Alvizi, L., Zechi-Ceide, R.M., Bertola, D., Felix, T.M., de Souza, J., Raskin, S., Twigg, S.R., Weiner, A.M., Armas, P. et al. (2014) A noncoding expansion in EIF4A3 causes Richieri-Costa-Pereira syndrome, a craniofacial disorder associated with limb defects. Am. J. Hum. Genet., 94, 120-128.
53. Niederriter, A., Davis, E.E., Golzio, C., Oh, E.C., Tsai, I.C. and Katsanis, N. (2013) In vivo modeling of the morbid human genome using Danio rerio. J. Vis. Exp., 24, e50338.