An assessment of mechanisms underlying peripheral axonal degeneration caused by aminoacyl-tRNA synthetase mutations

Molecular and Cellular Neuroscience

Volumn 46, Issue 2, 2011, Pages 432-443

  Stum, Morgane ^a   McLaughlin, Heather M ^b   Kleinbrink, Erica L ^b   Miers, Kathy E ^a   Ackerman, Susan L ^a,c   Seburn, Kevin L ^a   Antonellis, Anthony ^b   Burgess, Robert W ^a  

^a JACKSON LABORATORY   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

Amino acylation; Axonal translation; DI CMTC; Distal spinal muscular atrophy type V; DSMAV; Hereditary motor and sensory neuropathy; HSMN2D

Indexed keywords

ALANINE TRANSFER RNA LIGASE; AMINO ACID TRANSFER RNA LIGASE; GLYCINE TRANSFER RNA LIGASE; TYROSINE TRANSFER RNA LIGASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CEREBELLUM DEGENERATION; CONTROLLED STUDY; EMBRYONIC STEM CELL; GENETIC TRANSFECTION; MOTONEURON; MOUSE; MUTANT; MUTATION; NERVE FIBER DEGENERATION; NONHUMAN; PERIPHERAL NERVE; PERIPHERAL NEUROPATHY; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS; RNA TRANSLATION; SCHWANN CELL;

AMINO ACYL-TRNA SYNTHETASES; ANIMALS; AXONS; CHARCOT-MARIE-TOOTH DISEASE; DISEASE MODELS, ANIMAL; FEMORAL NERVE; IMMUNOHISTOCHEMISTRY; MICE; MICE, INBRED C57BL; MICE, MUTANT STRAINS; MICROSCOPY, CONFOCAL; MUTATION; NERVE DEGENERATION; NEUROMUSCULAR JUNCTION; PERIPHERAL NERVOUS SYSTEM DISEASES; PHENOTYPE; PROTEIN BIOSYNTHESIS; PURKINJE CELLS;

LEPISOSTEIDAE; MUS; WALLERIA;

EID: 78751702871     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mcn.2010.11.006     Document Type: Article

References (45)

1. Achilli, F., Bros-Facer, V., Williams, H.P., Banks, G.T., Alqatari, M., Chia, R., Tucci, V., Groves, M., Nickols, C.D., Seburn, K.L., Kendall, R., Cader, M.Z., Talbot, K., van Minnen, J., Burgess, R.W., Brandner, S., Martin, J.E., Koltzenburg, M., Greensmith, L., Nolan, P.M., Fisher, E.M., 2009. An ENU-induced mutation in mouse glycyl-tRNA synthetase (GARS) causes peripheral sensory and motor phenotypes creating a model of Charcot-Marie-Tooth type 2D peripheral neuropathy. Disease models & mechanisms.
2. Antonellis A., Ellsworth R.E., Sambuughin N., Puls I., Abel A., Lee-Lin S.Q., Jordanova A., Kremensky I., Christodoulou K., Middleton L.T., Sivakumar K., Ionasescu V., Funalot B., Vance J.M., Goldfarb L.G., Fischbeck K.H., Green E.D. Glycyl tRNA synthetase mutations in Charcot-Marie-Tooth disease type 2D and distal spinal muscular atrophy type V. American Journal of Human Genetics 2003, 72:1293-1299.
3. Antonellis A., Green E.D. The role of aminoacyl-tRNA synthetases in genetic diseases. Annual Review of Genomics and Human Genetics 2008, 9:87-107.
4. Antonellis A., Lee-Lin S.Q., Wasterlain A., Leo P., Quezado M., Goldfarb L.G., Myung K., Burgess S., Fischbeck K.H., Green E.D. Functional analyses of glycyl-tRNA synthetase mutations suggest a key role for tRNA-charging enzymes in peripheral axons. The Journal of Neuroscience 2006, 26:10397-10406.
5. Arnez J.G., Dock-Bregeon A.C., Moras D. Glycyl-tRNA synthetase uses a negatively charged pit for specific recognition and activation of glycine. Journal of Molecular Biology 1999, 286:1449-1459.
6. Arroyo E.J., Sirkowski E.E., Chitale R., Scherer S.S. Acute demyelination disrupts the molecular organization of peripheral nervous system nodes. The Journal of Comparative Neurology 2004, 479:424-434.
7. Beebe K., Mock M., Merriman E., Schimmel P. Distinct domains of tRNA synthetase recognize the same base pair. Nature 2008, 451:90-93.
8. Bird T.D., Kraft G.H., Lipe H.P., Kenney K.L., Sumi S.M. Clinical and pathological phenotype of the original family with Charcot-Marie-Tooth type 1B: a 20-year study. Annals of Neurology 1997, 41:463-469.
9. Chihara T., Luginbuhl D., Luo L. Cytoplasmic and mitochondrial protein translation in axonal and dendritic terminal arborization. Nature Neuroscience 2007, 10:828-837.
10. Coleman M.P., Conforti L., Buckmaster E.A., Tarlton A., Ewing R.M., Brown M.C., Lyon M.F., Perry V.H. An 85-kb tandem triplication in the slow Wallerian degeneration (Wlds) mouse. Proceedings of the National Academy of Sciences of the United States of America 1998, 95:9985-9990.
11. Edvardson S., Shaag A., Kolesnikova O., Gomori J.M., Tarassov I., Einbinder T., Saada A., Elpeleg O. Deleterious mutation in the mitochondrial arginyl-transfer RNA synthetase gene is associated with pontocerebellar hypoplasia. American Journal of Human Genetics 2007, 81:857-862.
12. Eichler F.S., Hornemann T., McCampbell A., Kuljis D., Penno A., Vardeh D., Tamrazian E., Garofalo K., Lee H.J., Kini L., Selig M., Frosch M., Gable K., von Eckardstein A., Woolf C.J., Guan G., Harmon J.M., Dunn T.M., Brown R.H. Overexpression of the wild-type SPT1 subunit lowers desoxysphingolipid levels and rescues the phenotype of HSAN1. The Journal of Neuroscience 2009, 29:14646-14651.
13. Ferri A., Sanes J.R., Coleman M.P., Cunningham J.M., Kato A.C. Inhibiting axon degeneration and synapse loss attenuates apoptosis and disease progression in a mouse model of motoneuron disease. Current Biology 2003, 13:669-673.
14. Giuditta A., Chun J.T., Eyman M., Cefaliello C., Bruno A.P., Crispino M. Local gene expression in axons and nerve endings: the glia-neuron unit. Physiological Reviews 2008, 88:515-555.
15. Guo M., Chong Y.E., Beebe K., Shapiro R., Yang X.L., Schimmel P. The C-Ala domain brings together editing and aminoacylation functions on one tRNA. Science (New York, N.Y 2009, 325:744-747.
16. Ibba M., Soll D. Aminoacyl-tRNAs: setting the limits of the genetic code. Genes & Development 2004, 18:731-738.
17. Isohanni P., Linnankivi T., Buzkova J., Lonnqvist T., Pihko H., Valanne L., Tienari P.J., Elovaara I., Pirttila T., Reunanen M., Koivisto K., Marjavaara S., Suomalainen A. DARS2 mutations in mitochondrial leucoencephalopathy and multiple sclerosis. Journal of Medical Genetics 2010, 47:66-70.
18. Jakubowski H., Goldman E. Editing of errors in selection of amino acids for protein synthesis. Microbiological Reviews 1992, 56:412-429.
19. James P.A., Cader M.Z., Muntoni F., Childs A.M., Crow Y.J., Talbot K. Severe childhood SMA and axonal CMT due to anticodon binding domain mutations in the GARS gene. Neurology 2006, 67:1710-1712.
20. Jordanova A., Irobi J., Thomas F.P., Van Dijck P., Meerschaert K., Dewil M., Dierick I., Jacobs A., De Vriendt E., Guergueltcheva V., Rao C.V., Tournev I., Gondim F.A., D'Hooghe M., Van Gerwen V., Callaerts P., Van Den Bosch L., Timmermans J.P., Robberecht W., Gettemans J., Thevelein J.M., De Jonghe P., Kremensky I., Timmerman V. Disrupted function and axonal distribution of mutant tyrosyl-tRNA synthetase in dominant intermediate Charcot-Marie-Tooth neuropathy. Nature Genetics 2006, 38:197-202.
21. Latour P., Thauvin-Robinet C., Baudelet-Mery C., Soichot P., Cusin V., Faivre L., Locatelli M.C., Mayencon M., Sarcey A., Broussolle E., Camu W., David A., Rousson R. A major determinant for binding and aminoacylation of tRNA(Ala) in cytoplasmic alanyl-tRNA synthetase is mutated in dominant axonal Charcot-Marie-Tooth disease. American Journal of Human Genetics 2010, 86:77-82.
22. Lee J.W., Beebe K., Nangle L.A., Jang J., Longo-Guess C.M., Cook S.A., Davisson M.T., Sundberg J.P., Schimmel P., Ackerman S.L. Editing-defective tRNA synthetase causes protein misfolding and neurodegeneration. Nature 2006, 443:50-55.
23. Lee T., Winter C., Marticke S.S., Lee A., Luo L. Essential roles of Drosophila RhoA in the regulation of neuroblast proliferation and dendritic but not axonal morphogenesis. Neuron 2000, 25:307-316.
24. Lin A.C., Holt C.E. Function and regulation of local axonal translation. Current Opinion in Neurobiology 2008, 18:60-68.
25. Loftfield R.B., Vanderjagt D. The frequency of errors in protein biosynthesis. The Biochemical Journal 1972, 128:1353-1356.
26. Logan D.T., Mazauric M.H., Kern D., Moras D. Crystal structure of glycyl-tRNA synthetase from Thermus thermophilus. The EMBO Journal 1995, 14:4156-4167.
27. Mack T.G., Reiner M., Beirowski B., Mi W., Emanuelli M., Wagner D., Thomson D., Gillingwater T., Court F., Conforti L., Fernando F.S., Tarlton A., Andressen C., Addicks K., Magni G., Ribchester R.R., Perry V.H., Coleman M.P. Wallerian degeneration of injured axons and synapses is delayed by a Ube4b/Nmnat chimeric gene. Nature Neuroscience 2001, 4:1199-1206.
28. McLaughlin H.M., Sakaguchi R., Liu C., Igarashi T., Pehlivan D., Chu K., Iyer R., Cruz P., Cherukuri P.F., Hansen N.F., Mullikin J.C., Biesecker L.G., Wilson T.E., Ionasescu V., Nicholson G., Searby C., Talbot K., Vance J.M., Zuchner S., Szigeti K., Lupski J.R., Hou Y.M., Green E.D., Antonellis A. Compound heterozygosity for loss-of-function lysyl-tRNA synthetase mutations in a patient with peripheral neuropathy. American Journal of Human Genetics 2010, 87:560-566.
29. Mi W., Beirowski B., Gillingwater T.H., Adalbert R., Wagner D., Grumme D., Osaka H., Conforti L., Arnhold S., Addicks K., Wada K., Ribchester R.R., Coleman M.P. The slow Wallerian degeneration gene, WldS, inhibits axonal spheroid pathology in gracile axonal dystrophy mice. Brain 2005, 128:405-416.
30. Motley W.W., Talbot K., Fischbeck K.H. GARS axonopathy: not every neuron's cup of tRNA. Trends in Neurosciences 2010, 33:59-66.
31. Nangle L.A., Motta C.M., Schimmel P. Global effects of mistranslation from an editing defect in mammalian cells. Chemistry & Biology 2006, 13:1091-1100.
32. Nangle L.A., Zhang W., Xie W., Yang X.L., Schimmel P. Charcot-Marie-Tooth disease-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 2007, 104:11239-11244.
33. Penno A., Reilly M.M., Houlden H., Laura M., Rentsch K., Niederkofler V., Stoeckli E.T., Nicholson G., Eichler F., Brown R.H., von Eckardstein A., Hornemann T. Hereditary sensory neuropathy type 1 is caused by the accumulation of two neurotoxic sphingolipids. The Journal of Biological Chemistry 2010, 285:11178-11187.
34. Press C., Milbrandt J. Nmnat delays axonal degeneration caused by mitochondrial and oxidative stress. The Journal of Neuroscience 2008, 28:4861-4871.
35. Salazar-Grueso E.F., Kim S., Kim H. Embryonic mouse spinal cord motor neuron hybrid cells. NeuroReport 1991, 2:505-508.
36. Scheper G.C., van der Klok T., van Andel R.J., van Berkel C.G., Sissler M., Smet J., Muravina T.I., Serkov S.V., Uziel G., Bugiani M., Schiffmann R., Krageloh-Mann I., Smeitink J.A., Florentz C., Van Coster R., Pronk J.C., van der Knaap M.S. Mitochondrial aspartyl-tRNA synthetase deficiency causes leukoencephalopathy with brain stem and spinal cord involvement and lactate elevation. Nature Genetics 2007, 39:534-539.
37. Schimmel P. Development of tRNA synthetases and connection to genetic code and disease. Protein Science 2008, 17:1643-1652.
38. Seburn K.L., Nangle L.A., Cox G.A., Schimmel P., Burgess R.W. An active dominant mutation of glycyl-tRNA synthetase causes neuropathy in a Charcot-Marie-Tooth 2D mouse model. Neuron 2006, 51:715-726.
39. Soundararajan P., Miles G.B., Rubin L.L., Brownstone R.M., Rafuse V.F. Motoneurons derived from embryonic stem cells express transcription factors and develop phenotypes characteristic of medial motor column neurons. The Journal of Neuroscience 2006, 26:3256-3268.
40. Storkebaum E., Leitao-Goncalves R., Godenschwege T., Nangle L., Mejia M., Bosmans I., Ooms T., Jacobs A., Van Dijck P., Yang X.L., Schimmel P., Norga K., Timmerman V., Callaerts P., Jordanova A. Dominant mutations in the tyrosyl-tRNA synthetase gene recapitulate in Drosophila features of human Charcot-Marie-Tooth neuropathy. Proceedings of the National Academy of Sciences of the United States of America 2009, 106:11782-11787.
41. Wang W., van Niekerk E., Willis D.E., Twiss J.L. RNA transport and localized protein synthesis in neurological disorders and neural repair. Developmental Neurobiology 2007, 67:1166-1182.
42. Wichterle H., Lieberam I., Porter J.A., Jessell T.M. Directed differentiation of embryonic stem cells into motor neurons. Cell 2002, 110:385-397.
43. Xie W., Nangle L.A., Zhang W., Schimmel P., Yang X.L. Long-range structural effects of a Charcot-Marie-Tooth disease-causing mutation in human glycyl-tRNA synthetase. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:9976-9981.
44. Zhai R.G., Cao Y., Hiesinger P.R., Zhou Y., Mehta S.Q., Schulze K.L., Verstreken P., Bellen H.J. Drosophila NMNAT maintains neural integrity independent of its NAD synthesis activity. PLoS Biology 2006, 4:e416.
45. Zhai R.G., Zhang F., Hiesinger P.R., Cao Y., Haueter C.M., Bellen H.J. NAD synthase NMNAT acts as a chaperone to protect against neurodegeneration. Nature 2008, 452:887-891.