Substrate interaction defects in histidylâ tRNA synthetase linked to dominant axonal peripheral neuropathy
dc.contributor.author | Abbott, Jamie A. | |
dc.contributor.author | Meyer‐schuman, Rebecca | |
dc.contributor.author | Lupo, Vincenzo | |
dc.contributor.author | Feely, Shawna | |
dc.contributor.author | Mademan, Inès | |
dc.contributor.author | Oprescu, Stephanie N. | |
dc.contributor.author | Griffin, Laurie B. | |
dc.contributor.author | Alberti, M. Antonia | |
dc.contributor.author | Casasnovas, Carlos | |
dc.contributor.author | Aharoni, Sharon | |
dc.contributor.author | Basel‐vanagaite, Lina | |
dc.contributor.author | Züchner, Stephan | |
dc.contributor.author | Jonghe, Peter | |
dc.contributor.author | Baets, Jonathan | |
dc.contributor.author | Shy, Michael E. | |
dc.contributor.author | Espinós, Carmen | |
dc.contributor.author | Demeler, Borries | |
dc.contributor.author | Antonellis, Anthony | |
dc.contributor.author | Francklyn, Christopher | |
dc.date.accessioned | 2018-03-07T18:23:44Z | |
dc.date.available | 2019-05-13T14:45:23Z | en |
dc.date.issued | 2018-03 | |
dc.identifier.citation | Abbott, Jamie A.; Meyer‐schuman, Rebecca ; Lupo, Vincenzo; Feely, Shawna; Mademan, Inès ; Oprescu, Stephanie N.; Griffin, Laurie B.; Alberti, M. Antonia; Casasnovas, Carlos; Aharoni, Sharon; Basel‐vanagaite, Lina ; Züchner, Stephan ; Jonghe, Peter; Baets, Jonathan; Shy, Michael E.; Espinós, Carmen ; Demeler, Borries; Antonellis, Anthony; Francklyn, Christopher (2018). "Substrate interaction defects in histidylâ tRNA synthetase linked to dominant axonal peripheral neuropathy." Human Mutation 39(3): 415-432. | |
dc.identifier.issn | 1059-7794 | |
dc.identifier.issn | 1098-1004 | |
dc.identifier.uri | https://hdl.handle.net/2027.42/142441 | |
dc.description.abstract | Histidylâ tRNA synthetase (HARS) ligates histidine to cognate tRNA molecules, which is required for protein translation. Mutations in HARS cause the dominant axonal peripheral neuropathy Charcotâ Marieâ Tooth disease type 2W (CMT2W); however, the precise molecular mechanism remains undefined. Here, we investigated three HARS missense mutations associated with CMT2W (p.Tyr330Cys, p.Ser356Asn, and p.Val155Gly). The three mutations localize to the HARS catalytic domain and failed to complement deletion of the yeast ortholog (HTS1). Enzyme kinetics, differential scanning fluorimetry (DSF), and analytical ultracentrifugation (AUC) were employed to assess the effect of these substitutions on primary aminoacylation function and overall dimeric structure. Notably, the p.Tyr330Cys, p.Ser356Asn, and p.Val155Gly HARS substitutions all led to reduced aminoacylation, providing a direct connection between CMT2Wâ linked HARS mutations and loss of canonical ARS function. While DSF assays revealed that only one of the variants (p.Val155Gly) was less thermally stable relative to wildâ type, all three HARS mutants formed stable dimers, as measured by AUC. Our work represents the first biochemical analysis of CMTâ associated HARS mutations and underscores how loss of the primary aminoacylation function can contribute to disease pathology.Diseaseâ causing variants in multiple aminoacylâ tRNA synthetase genes have been linked to the dominant inherited peripheral neuropathy Charcot Marie Tooth (CMT) disease. Here, we employed yeast complementation, enzyme kinetics, differential scanning fluorimetry (DSF), and analytical ultra centrifugation (AUC) to investigate three histidylâ tRNA synthetase (HARS) missense mutations associated with CMT2W (p.Tyr330Cys, p.Ser356Asn, and p.Val155Gly). The mutant substitutions all led to reduced catalytic activity and poorer histidine and ATP binding, illustrating how loss of primary aminoacylation function can contribute to disease pathology. | |
dc.publisher | University of Washington | |
dc.publisher | Wiley Periodicals, Inc. | |
dc.subject.other | Charcotâ Marieâ Tooth disease type 2W | |
dc.subject.other | hereditary motor and sensory neuropathy | |
dc.subject.other | histidylâ tRNA synthetase | |
dc.subject.other | aminoacylâ tRNA synthetase | |
dc.title | Substrate interaction defects in histidylâ tRNA synthetase linked to dominant axonal peripheral neuropathy | |
dc.type | Article | en_US |
dc.rights.robots | IndexNoFollow | |
dc.subject.hlbsecondlevel | Genetics | |
dc.subject.hlbtoplevel | Science | |
dc.subject.hlbtoplevel | Health Sciences | |
dc.description.peerreviewed | Peer Reviewed | |
dc.description.bitstreamurl | https://deepblue.lib.umich.edu/bitstream/2027.42/142441/1/humu23380_am.pdf | |
dc.description.bitstreamurl | https://deepblue.lib.umich.edu/bitstream/2027.42/142441/2/humu23380.pdf | |
dc.identifier.doi | 10.1002/humu.23380 | |
dc.identifier.source | Human Mutation | |
dc.identifier.citedreference | Niesen, F. H., Berglund, H., & Vedadi, M. ( 2007 ). The use of differential scanning fluorimetry to detect ligand interactions that promote protein stability. Nature Protocols, 2 ( 9 ), 2212 â 2221. | |
dc.identifier.citedreference | Hyun, Y. S., Park, H. J., Heo, S. H., Yoon, B. R., Nam, S. H., Kim, S. B., â ¦ Chung, K. W. ( 2014 ). Rare variants in methionylâ and tyrosylâ tRNA synthetase genes in lateâ onset autosomal dominant Charcotâ Marieâ Tooth neuropathy. Clinical Genetics, 86 ( 6 ), 592 â 594. | |
dc.identifier.citedreference | Ibba, M., & Soll, D. ( 2000 ). Aminoacylâ tRNA synthesis. Annual Review of Biochemistry, 69, 617 â 650. | |
dc.identifier.citedreference | Jerath, N. U., & Shy, M. E. ( 2015 ). Hereditary motor and sensory neuropathies: Understanding molecular pathogenesis could lead to future treatment strategies. Biochimica Et Biophysica Acta, 1852 ( 4 ), 667 â 678. | |
dc.identifier.citedreference | Jordanova, A., Irobi, J., Thomas, F. P., Van Dijck, P., Meerschaert, K., Dewil, M., â ¦ Timmerman, V. ( 2006 ). Disrupted function and axonal distribution of mutant tyrosylâ tRNA synthetase in dominant intermediate Charcotâ Marieâ Tooth neuropathy. Nature Genetics, 38 ( 2 ), 197 â 202. | |
dc.identifier.citedreference | Koh, C. Y., Kim, J. E., Wetzel, A. B., de van der Schueren, W. J., Shibata, S., Ranade, R. M., â ¦ Hol, W. G. ( 2014 ). Structures of Trypanosoma brucei methionylâ tRNA synthetase with ureaâ based inhibitors provide guidance for drug design against sleeping sickness. PLoS Neglected Tropical Diseases, 8 ( 4 ), e2775, 1 â 13. | |
dc.identifier.citedreference | Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., â ¦ Higgins, D. G. ( 2007 ). Clustal W and Clustal X version 2.0. Bioinformatics, 3 ( 21 ), 2947 â 2948. | |
dc.identifier.citedreference | Latour, P., Thauvinâ Robinet, C., Baudeletâ Mery, C., Soichot, P., Cusin, V., Faivre, L., â ¦ Rousson, R. ( 2010 ). A major determinant for binding and aminoacylation of tRNA(Ala) in cytoplasmic Alanylâ tRNA synthetase is mutated in dominant axonal Charcotâ Marieâ Tooth disease. American Journal of Human Genetics, 86 ( 1 ), 77 â 82. | |
dc.identifier.citedreference | Laue, T. M., Shah, B. D., Ridgeway, T. M., & Pelletier, S. L. ( 1992 ). In S. Harding, A. Rowe (Eds.), Analytical ultracentrifugation in biochemistry and polymer science (pp. 90 â 125 ). Royal Society of Chemistry, Cambridge, UK. | |
dc.identifier.citedreference | Lee, Y. H., Chang, C. P., Cheng, Y. J., Kuo, Y. Y., Lin, Y. S., & Wang, C. C. ( 2017 ). Evolutionary gain of highly divergent tRNA specificities by two isoforms of human histidylâ tRNA synthetase. Cellular and Molecular Life Sciences, 74 ( 14 ), 2663 â 2677. | |
dc.identifier.citedreference | Lek, M., Karczewski, K. J., Minikel, E. V., Samocha, K. E., Banks, E., Fennell, T., â ¦ Cummings, B. B. and others ( 2016 ). Analysis of proteinâ coding genetic variation in 60,706 humans. Nature, 536 ( 7616 ), 285 â 291. | |
dc.identifier.citedreference | Lupo, V., Garciaâ Garcia, F., Sancho, P., Tello C., Garciaâ Romero, M., Villarreal, L., â ¦ Espinós, C. ( 2016 ). Assessment of targeted nextâ generation sequencing as a tool for the diagnosis of Charcotâ Marieâ Tooth disease and hereditary motor neuropathy. The Journal of Molecular Diagnostics, 18 ( 2 ), 225 â 234. | |
dc.identifier.citedreference | McLaughlin, H. M., Sakaguchi, R., Giblin, W., NISC Comparative Sequencing Program, Wilson, T. E., Biesecker, L., â ¦ Antonellis, A. ( 2012 ). A recurrent lossâ ofâ function alanylâ tRNA synthetase (AARS) mutation in patients with Charcotâ Marieâ Tooth disease type 2N (CMT2N). Human Mutation, 33 ( 1 ), 244 â 253. | |
dc.identifier.citedreference | Meyerâ Schuman, R., & Antonellis, A. ( 2017 ). Emerging mechanisms of aminoacylâ tRNA synthetase mutations in recessive and dominant human disease. Human Molecular Genetics, 26, R114 â R127. | |
dc.identifier.citedreference | Motley, W. W., Talbot, K., & Fischbeck, K. H. ( 2010 ). GARS axonopathy: Not every neuron’s cup of tRNA. Trends in Neuroscience, 33 ( 2 ), 59 â 66. | |
dc.identifier.citedreference | Nam, S. H., Hong, Y. B., Hyun, Y. S., Nam da, E., Kwak, G., Hwang, S. H., â ¦ Chung, K. W. ( 2016 ). Identification of genetic causes of inherited peripheral neuropathies by targeted gene panel sequencing. Molecules and Cells, 39 ( 5 ), 382 â 388. | |
dc.identifier.citedreference | Nangle, L. A., Zhang, W., Xie, W., Yang, X. L., & Schimmel, P. ( 2007 ). Charcotâ Marieâ Tooth diseaseâ associated mutant tRNA synthetases linked to altered dimer interface and neurite distribution defect. Proceedings of the National Academy of Sciences of the United States of America, 104 ( 27 ), 11239 â 11244. | |
dc.identifier.citedreference | Gonzalez, M., Falk, M. J., Gai, X., Postrel, R., Schule, R., & Zuchner, S. ( 2015 ). Innovative genomic collaboration using the GENESIS (GEM.app) platform. Human Mutation, 36 ( 10 ), 950 â 956. | |
dc.identifier.citedreference | Oprescu, S. N., Griffin, L. B., Beg, A. A., & Antonellis, A. ( 2017 ). Predicting the pathogenicity of aminoacylâ tRNA synthetase mutations. Methods, 113, 139 â 151. | |
dc.identifier.citedreference | Pareyson, D., & Marchesi, C. ( 2009 a). Diagnosis, natural history, and management of Charcotâ Marieâ Tooth disease. Lancet Neurology, 8 ( 7 ), 654 â 667. | |
dc.identifier.citedreference | Pareyson, D., & Marchesi, C. ( 2009 b). Natural history and treatment of peripheral inherited neuropathies. Advances in Experimental Medicine and Biology, 652, 207 â 224. | |
dc.identifier.citedreference | Pareyson, D., Marchesi, C., & Salsano, E. ( 2009 ). Hereditary predominantly motor neuropathies. Current Opinion in Neurology, 22 ( 5 ), 451 â 459. | |
dc.identifier.citedreference | Pierce, S. B., Chisholm, K. M., Lynch, E. D., Lee, M. K., Walsh, T., Opitz, J. M., â ¦ King, M. C. ( 2011 ). Mutations in mitochondrial histidyl tRNA synthetase HARS2 cause ovarian dysgenesis and sensorineural hearing loss of Perrault syndrome. Proceedings of the National Academy of Sciences of the United States of America, 108 ( 16 ), 6543 â 6548. | |
dc.identifier.citedreference | Puffenberger, E. G., Jinks, R. N., Sougnez, C., Cibulskis, K., Willert, R. A., Achilly, N. P., â ¦ Strauss, K. A. ( 2012 ). Genetic mapping and exome sequencing identify variants associated with five novel diseases. Plos One, 7 ( 1 ), e28936, 1 â 15. | |
dc.identifier.citedreference | Robert, X., & Gouet, P. ( 2014 ). Deciphering key features in protein structures with the new ENDscript server. Nucleic Acids Research, 42 ( Web Server issue ), W320 â W324. | |
dc.identifier.citedreference | Safka Brozkova, D., Deconinck, T., Griffin, L. B., Ferbert, A., Haberlova, J., Mazanec, R., â ¦ Baets, J. ( 2015 ). Loss of function mutations in HARS cause a spectrum of inherited peripheral neuropathies. Brain, 138 ( Pt 8 ), 2161 â 2172. | |
dc.identifier.citedreference | Schuck, P. ( 1999 ). Sedimentation equilibrium analysis of interference optical data by systematic noise decomposition. Analytical Biochemistry, 272 ( 2 ), 199 â 208. | |
dc.identifier.citedreference | Shy, M. E., Blake, J., Krajewski, K., Fuerst, D. R., Laura, M., Hahn, A. F., â ¦ Reilly, M. ( 2005 ). Reliability and validity of the CMT neuropathy score as a measure of disability. Neurology, 64 ( 7 ), 1209 â 1214. | |
dc.identifier.citedreference | Simons, C., Griffin, L. B., Helman, G., Golas, G., Pizzino, A., Bloom, M., â ¦ Vanderver, A. ( 2015 ). Lossâ ofâ function alanylâ tRNA synthetase mutations cause an autosomalâ recessive earlyâ onset epileptic encephalopathy with persistent myelination defect. American Journal of Human Genetics, 96 ( 4 ), 675 â 681. | |
dc.identifier.citedreference | Sivakumar, K., Kyriakides, T., Puls, I., Nicholson, G. A., Funalot, B., Antonellis, A., â ¦ Goldfarb, L. G. ( 2005 ). Phenotypic spectrum of disorders associated with glycylâ tRNA synthetase mutations. Brain, 128 ( Pt 10 ), 2304 â 2314. | |
dc.identifier.citedreference | Skre, H. ( 1974 ). Genetic and clinical aspects of Charcotâ Marieâ Tooth’s disease. Clinical Genetics, 6 ( 2 ), 98 â 118. | |
dc.identifier.citedreference | Storkebaum, E. ( 2016 ). Peripheral neuropathy via mutant tRNA synthetases: Inhibition of protein translation provides a possible explanation. Bioessays, 38 ( 9 ), 818 â 829. | |
dc.identifier.citedreference | Stum, M., McLaughlin, H. M., Kleinbrink, E. L., Miers, K. E., Ackerman, S. L., Seburn, K. L., â ¦ Burgess, R. W. ( 2011 ). An assessment of mechanisms underlying peripheral axonal degeneration caused by aminoacylâ tRNA synthetase mutations. Molecular and Cellular Neuroscience, 46 ( 2 ), 432 â 443. | |
dc.identifier.citedreference | Timmerman, V., Strickland, A. V., & Zuchner, S. ( 2014 ). Genetics of Charcotâ Marieâ Tooth (CMT) disease within the frame of the human genome project success. Genes, 5 ( 1 ), 13 â 32. | |
dc.identifier.citedreference | Tsai, P. C., Soong, B. W., Mademan, I., Huang, Y. H., Liu, C. R., Hsiao, C. T., â ¦ Lee, Y. C. ( 2017 ). A recurrent WARS mutation is a novel cause of autosomal dominant distal hereditary motor neuropathy. Brain, 140, 1252 â 1266. | |
dc.identifier.citedreference | Vester, A., Velezâ Ruiz, G., McLaughlin, H. M., Lupski, J. R., Talbot, K., Vance, J. M., â ¦ Antonellis, A. ( 2013 ). A lossâ ofâ function variant in the human histidylâ tRNA synthetase (HARS) gene is neurotoxic in vivo. Human Mutation, 34 ( 1 ), 191 â 199. | |
dc.identifier.citedreference | Wolfson, A. D., Pleiss, J. A., & Uhlenbeck, O. C. ( 1998 ). A new assay for tRNA aminoacylation kinetics. RNA, 4 ( 8 ), 1019 â 1023. | |
dc.identifier.citedreference | Xie, W., Nangle, L. A., Zhang, W., Schimmel, P., & Yang, X. L. ( 2007 ). Longâ range structural effects of a Charcotâ Marieâ Tooth diseaseâ causing mutation in human glycylâ tRNA synthetase. Proceedings of the National Academy of Sciences of the United States of America, 104 ( 24 ), 9976 â 9981. | |
dc.identifier.citedreference | Zhang, X., Ling, J., Barcia, G., Jing, L., Wu, J., Barry, B. J., â ¦ Weimer, J. M. ( 2014 ). Stein Q and othersMutations in QARS, encoding glutaminylâ tRNA synthetase, cause progressive microcephaly, cerebralâ cerebellar atrophy, and intractable seizures. American Journal of Human Genetics, 94 ( 4 ), 547 â 558. | |
dc.identifier.citedreference | Niehues, S., Bussmann, J., Steffes, G., Erdmann, I., Kohrer, C., Sun, L., â ¦ Storkebaum, E. ( 2015 ). Impaired protein translation in Drosophila models for Charcotâ Marieâ Tooth neuropathy caused by mutant tRNA synthetases. Nature Communications, 6, 7520, 1 â 12. | |
dc.identifier.citedreference | Abbott, J. A., Francklyn, C. S., & Robeyâ Bond, S. M. ( 2014 ). Transfer RNA and human disease. Frontiers in Genetics, 5, Article 158, 1 â 18. | |
dc.identifier.citedreference | Abbott, J. A., Guth, E., Kim, C., Regan, C., Siu, V. M., Rupar, C. A., â ¦ Robeyâ Bond, S. M. ( 2017 ). The Usher Syndrome type IIIB histidylâ tRNA synthetase mutation confers temperature sensitivity. Biochemistry, 56, 3619 â 3631. | |
dc.identifier.citedreference | Antonellis, A., Ellsworth, R. E., Sambuughin, N., Puls, I., Abel, A., Leeâ Lin, S. Q., â ¦ Middleton, L. T. and others ( 2003 ). Glycyl tRNA synthetase mutations in Charcotâ Marieâ Tooth disease type 2D and distal spinal muscular atrophy type V. American Journal of Human Genetics, 72 ( 5 ), 1293 â 1299. | |
dc.identifier.citedreference | Antonellis, A., & Green, E. D. ( 2008 ). The role of aminoacylâ tRNA synthetases in genetic diseases. Annual Review of Genomics and Human Genetics, 9, 87 â 107. | |
dc.identifier.citedreference | Arnez, J. G., Harris, D. C., Mitschler, A., Rees, B., Francklyn, C. S., & Moras, D. ( 1995 ). Crystal structure of histidylâ tRNA synthetase from Escherichia coli complexed with histidylâ adenylate. EMBO Journal, 14 ( 17 ), 4143 â 4155. | |
dc.identifier.citedreference | Bird, T. D. ( 1993 ). Charcotâ Marieâ Tooth hereditary neuropathy overview. In Adam, M. P., Ardinger, H. H., Pagon, R. A., Wallace, S. E., Bean, L. J. H., Meffird, H. C., â ¦ Ledbetter, N., (editors). GeneReviews(R). Seattle, WA: University of Washington. | |
dc.identifier.citedreference | Boeke, J. D., LaCroute, F., & Fink, G. R. ( 1984 ). A positive selection for mutants lacking orotidineâ 5’â phosphate decarboxylase activity in yeast: 5â fluoroâ orotic acid resistance. Molecular and General Genetics, 197 ( 2 ), 345 â 346. | |
dc.identifier.citedreference | Brookes, E., Cao, W., & Demeler, B. ( 2010 ). A twoâ dimensional spectrum analysis for sedimentation velocity experiments of mixtures with heterogeneity in molecular weight and shape. European Biophysics Journal, 39 ( 3 ), 405 â 414. | |
dc.identifier.citedreference | Brookes, E. D. B. ( 2006 ). Analytical ultracentrifugation data analysis with UltraScanâ III. Analytical ultracentrifugation: Instrumentation, software, and applications. In C.C.H. Wandrey (Ed.), Analytical ultracentrifugation VIII. Progress in colloid and polymer science. Berlin, Heidelberg: Springer. | |
dc.identifier.citedreference | Brookes, E. H., & Demeler, B. ( 2008 ). Parallel computational techniques for the analysis of sedimentation velocity experiments in UltraScan. Colloid and Polymer Science, 286 ( 2 ), 139 â 148. | |
dc.identifier.citedreference | Burns, J., Ouvrier, R., Estilow, T., Shy, R., Laura, M., Pallant, J. F., â ¦ Finkel, R. S. ( 2012 ). Validation of the Charcotâ Marieâ Tooth disease pediatric scale as an outcome measure of disability. Annals of Neurology, 71 ( 5 ), 642 â 652. | |
dc.identifier.citedreference | De Lorenzo, F., Straus, D. S., & Ames, B. N. ( 1972 ). Histidine regulation in Salmonella typhimurium. X. Kinetic studies of mutant histidyl transfer ribonucleic acid synthetases. Journal of Biological Chemistry, 247 ( 8 ), 2302 â 2307. | |
dc.identifier.citedreference | Demeler, B. ( 2010 ). Methods for the design and analysis of sedimentation velocity and sedimentation equilibrium experiments with proteins. Current Protocols in Protein Science, Chapter 7:UNit 7, 13, 7.13.1â 7.13.24. | |
dc.identifier.citedreference | Demeler, B., & Brookes, E. ( 2008 ). Monte Carlo analysis of sedimentation experiments. Colloid and Polymer Science, 286 ( 2 ), 129 â 137. | |
dc.identifier.citedreference | Demeler, B., Gorbet, G., Zollars, D., Dubbs, B., Brookes, E., & Cao, W. ( 2016 ). UltraScanâ III version 3.5: A comprehensive data analysis software package for analytical ultracentrifugation experiments. Retrieved from https://www.ultrascan3.uthscsa.edu/ | |
dc.identifier.citedreference | Dyck, P. J., & Lambert, E. H. ( 1968 ). Lower motor and primary sensory neuron diseases with peroneal muscular atrophy. II. Neurologic, genetic, and electrophysiologic findings in various neuronal degenerations. Archives of Neurology, 18 ( 6 ), 619 â 625. | |
dc.identifier.citedreference | Fahoum, S. K., & Yang, D. C. ( 1987 ). Purification of mammalian histidylâ tRNA synthetase and its interaction with myositisâ specific antiâ Joâ 1 antibodies. Biochemistry, 26 ( 18 ), 5871 â 5877. | |
dc.identifier.citedreference | Froelich, C. A., & First, E. A. ( 2011 ). Dominant Intermediate Charcotâ Marieâ Tooth disorder is not due to a catalytic defect in tyrosylâ tRNA synthetase. Biochemistry, 50 ( 33 ), 7132 â 7145. | |
dc.identifier.citedreference | Frohlich, D., Suchowerska, A. K., Spencer, Z. H., von Jonquieres, G., Klugmann, C. B., Bongers, A., â ¦ Klugmann, M. ( 2017 ). In vivocharacterization of the aspartylâ tRNA synthetase DARS: Homing in on the leukodystrophy HBSL. Neurobiology of Disease, 97 ( Pt A ), 24 â 35. | |
dc.identifier.citedreference | Giuditta, A., Dettbarn, W. D., & Brzin, M. ( 1968 ). Protein synthesis in the isolated giant axon of the squid. Proceedings of the National Academy of Sciences of the United States of America, 59 ( 4 ), 1284 â 1287. | |
dc.identifier.citedreference | Gonzagaâ Jauregui, C., Harel, T., Gambin, T., Kousi, M., Griffin, L. B., Francescatto, L., â ¦ Lupski, J. R. ( 2015 ). Exome sequence analysis suggests that genetic burden contributes to phenotypic variability and complex neuropathy. Cell Reports, 12 ( 7 ), 1169 â 1183. | |
dc.identifier.citedreference | Gonzalez, M., McLaughlin, H., Houlden, H., Guo, M., Yoâ Tsen, L., Hadjivassilious, M., â ¦ Reilly, M. M. and others ( 2013 ). Exome sequencing identifies a significant variant in methionylâ tRNA synthetase (MARS) in a family with lateâ onset CMT2. Journal of Neurology, Neurosurgery, and Psychiatry, 84 ( 11 ), 1247 â 1249. | |
dc.identifier.citedreference | Gorbet, G., Devlin, T., Hernandez Uribe, B. I., Demeler, A. K., Lindsey, Z. L., Ganji, S., â ¦ Demeler, B. ( 2014 ). A parametrically constrained optimization method for fitting sedimentation velocity experiments. Biophysical Journal, 106 ( 8 ), 1741 â 1750. | |
dc.identifier.citedreference | He, W., Bai, G., Zhou, H., Wei, N., White, N. M., Lauer, J., â ¦ Yang, X. L. ( 2015 ). CMT2D neuropathy is linked to the neomorphic binding activity of glycylâ tRNA synthetase. Nature, 526 ( 7575 ), 710 â 714. | |
dc.identifier.citedreference | Hirano, M., Oka, N., Hashiguchi, A., Ueno, S., Sakamoto, H., Takashima, H., â ¦ Nakamura, Y. ( 2016 ). Histopathological features of a patient with Charcotâ Marieâ Tooth disease type 2U/ADâ CMTaxâ MARS. Journal of the Peripheral Nervous System, 21 ( 4 ), 370 â 374. | |
dc.identifier.citedreference | Holt, C. E., & Schuman, E. M. ( 2013 ). The central dogma decentralized: New perspectives on RNA function and local translation in neurons. Neuron, 80 ( 3 ), 648 â 657. | |
dc.owningcollname | Interdisciplinary and Peer-Reviewed |
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