Neurodegenerative disease-associated mutants of a human mitochondrial aminoacyl-tRNA synthetase present individual molecular signatures

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Sauter, Claude ^a   Lorber, Bernard ^a   Gaudry, Agnès ^a   Karim, Loukmane ^a   Schwenzer, Hagen ^a,d   Wien, Frank ^b   Roblin, Pierre ^b,c   Florentz, Catherine ^a   Sissler, Marie ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b SYNCHROTRON SOLEIL   (France)

^c CEMAGREF   (France)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARTATE TRANSFER RNA LIGASE; MITOCHONDRIAL PROTEIN;

ANIMAL; CELL LINE; ENZYME STABILITY; ENZYMOLOGY; GENETICS; HAMSTER; HUMAN; LEUKOENCEPHALOPATHY; METABOLISM; MUTATION; PATHOLOGY;

ANIMALS; ASPARTATE-TRNA LIGASE; CELL LINE; CRICETINAE; ENZYME STABILITY; HUMANS; LEUKOENCEPHALOPATHIES; MITOCHONDRIAL PROTEINS; MUTATION;

EID: 84949239478     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep17332     Document Type: Article

References (48)

1. Schwenzer, H., Zoll, J., Florentz, C., Sissler, M. Pathogenic implications of human mitochondrial aminoacyl-tRNA synthetases. In Topics in Current Chemistry-Aminoacyl-tRNA Synthetases: Applications in Chemistry, Biology and Medicine, Vol. 344 (ed. Kim, S.) 247-292 (Springer, 2014).
2. Wallace, D., Brown, M., Lott, M. Mitochondrial DNA variation in human evolution and disease. Gene 238, 211-230 (1999).
3. Thorburn, D. R. Mitochondrial disorders: prevalence, myths and advances. J. Inherit. Metab. Dis. 27, 349-362 (2004).
4. Rötig, A. Genetic bases of mitochondrial respiratory chain disorders. Diabetes Metab. 36, 97-107 (2010).
5. Boczonadi, V., Horvath, R. Mitochondria: impaired mitochondrial translation in human disease. Int J Biochem Cell Biol. 48, 77-84 (2014).
6. Scheper, G. C. et al. Mitochondrial aspartyl-tRNA synthetase deficiency causes leukoencephalopathy with brain stem and spinal cord involvement and lactate elevation. Nat Genet 39, 534-539 (2007).
7. Suzuki, T., Nagao, A., Suzuki, T. Human mitochondrial tRNAs: biogenesis, function, structural aspects, and diseases. Annu. Rev. Genet. 45, 299-329 (2011).
8. Konovalova, S., Tyynismaa, H. Mitochondrial aminoacyl-tRNA synthetases in human disease. Mol Genet Metab. 108, 206-211 (2013).
9. Diodato, D., Ghezzi, D., Tiranti, V. The Mitochondrial Aminoacyl tRNA Synthetases: Genes and Syndromes. Int J Cell Biol. 2014, 787956 (2014).
10. Schwartzentruber, J. et al. Mutation in the Nuclear Encoded Mitochondrial Isoleucyl tRNA-Synthetase IARS2 in Patients with Cataracts, Growth Hormone Deficiency with Short Stature, Partial Sensorineural Deafness and Peripheral Neuropathy or with Leigh Syndrome. Hum. Mutat. 35, 1285-1289 (2014).
11. Hallmann, K. et al. A homozygous splice-site mutation in CARS2 is associated with progressive myoclonic epilepsy. Neurology 83, 2183-2187 (2014).
12. Sofou, K. et al. Whole exome sequencing reveals mutations in NARS2 and PARS2, encoding the mitochondrial asparaginyl-tRNA synthetase and prolyl-tRNA synthetase, in patients with Alpers syndrome. Mol Genet Genomic Med. 3, 59-68 (2015).
13. Lombès, A., Auré, K., Bellanné-Chantelot, C., Gilleron, M., Jardel, C. Unsolved issues related to human mitochondrial diseases. Biochimie 100, 171-176 (2014).
14. Isohanni, P. et al. DARS2 mutations in mitochondrial leucoencephalopathy and multiple sclerosis. J. Med. Genet. 47, 66-70 (2010).
15. Lin, J. et al. Leukoencephalopathy With Brainstem and Spinal Cord Involvement and Normal Lactate: A New Mutation in the DARS2 Gene. J. Child. Neurol. 25, 1425-1428 (2010).
16. Labauge, P., Dorboz, I., Eymard-Pierre, E., Dereeper, O., Boespflug-Tanguy, O. Clinically asymptomatic adult patient with extensive LBSL MRI pattern and DARS2 mutations. J. Neurol. 258, 335-337 (2011).
17. Miyake, N. et al. A novel homozygous mutation of DARS2 may cause a severe LBSL variant. Clin. Genet. 80, 293-296 (2011).
18. Tzoulis, C. et al. Leukoencephalopathy with brainstem and spinal cord involvement caused by a novel mutation in the DARS2 gene. J. Neurol. 259, 292-296 (2012).
19. van Berge, L. et al. Leukoencephalopathy with brainstem and spinal cord involvement and lactate elevation: clinical and genetic characterization and target for therapy. Brain 137, 1019-1029 (2014).
20. van der Knaap, M. S. et al. A new leukoencephalopathy with brainstem and spinal cord involvement and high lactate. Ann. Neurol. 53, 252-258 (2003).
21. Synofzik, M. et al. Acetazolamide-responsive exercise-induced episodic ataxia associated with a novel homozygous DARS2 mutation. J. Med. Genet. 48, 713-715 (2011).
22. Scheper, G. C., van der Knaap, M. S., Proud, C. G. Translation matters: protein synthesis defects in inherited disease. Nat. Rev. Genet. 8, 711-723 (2007).
23. van Berge, L. et al. Pathogenic mutations causing LBSL affect mitochondrial aspartyl-tRNA synthetase in diverse ways. Biochemical Journal 450, 345-350 (2013).
24. van Berge, L. et al. Leukoencephalopathy with brain stem and spinal cord involvement and lactate elevation is associated with cell-type-dependent splicing of mtAspRS mRNA. Biochem J. 441, 955-962 (2012).
25. Messmer, M. et al. A human pathology-related mutation prevents import of an aminoacyl-tRNA synthetase into mitochondria. Biochem J. 433, 441-446 (2011).
26. Neuenfeldt, A. et al. Thermodynamic properties distinguish human mitochondrial aspartyl-tRNA synthetase from bacterial homolog with same 3D architecture. Nucleic Acids Res. 41, 2698-2708 (2013).
27. Gaudry, A. et al. Redesigned N-terminus enhances expression, solubility, and crystallisability of mitochondrial enzyme. Protein Engineering, Design and Selection 25, 473-481 (2012).
28. Messmer, M. et al. Peculiar inhibition of human mitochondrial aspartyl-tRNA synthetase by adenylate analogs. Biochimie 91, 596-603 (2009).
29. Giegé, R., Touzé, E., Lorber, B., Theóbald-Dietrich, A., Sauter, C. Crystallogenesis trends of free and liganded aminoacyl-tRNA synthetases. Crystal Growth & Design 8, 4297-4306 (2008).
30. Bonnefond, L. et al. Exploiting Protein Engineering and Crystal Polymorphism for Successful X-ray Structure Determination. Crystal Growth & Design 11, 4334-4343 (2011).
31. Cassandrini, D. et al. Pontocerebellar hypoplasia type 6 caused by mutations in RARS2: definition of the clinical spectrum and molecular findings in five patients. J Inherit Metab Dis. 36, 43-53 (2013).
32. Guo, M., Schimmel, P., Yang, X.-L. Functional expansion of human tRNA synthetases achieved by structural inventions. FEBS Lett. 584, 434-442 (2010).
33. Kim, S., You, S., Hwang, D. Aminoacyl-tRNA synthetases and tumorigenesis: more than housekeeping. Nat Rev Cancer. 11, 708-718 (2011).
34. Guo, M., Schimmel, P. Essential nontranslational functions of tRNA synthetases. Nature Chemical Biology 9, 145-153 (2013).
35. Lorber, B., Fischer, F., Bailly, M., Roy, H., Kern, D. Protein analysis by dynamic light scattering: Methods and techniques for students. Biochem. Mol. Biol. Educ. 40, 372-382 (2012).
36. Réfrégiers, M. et al. DISCO synchrotron-radiation circular-dichroism endstation at SOLEIL. J Synchrotron Radiat. 19, 831-835 (2012).
37. Lees, J. G., Smith, B. R., Wien, F., Miles, A. J., Wallace, B. A. CDtool-an integrated software package for circular dichroism spectroscopic data processing, analysis, and archiving. Anal. Biochem. 332, 285-289 (2004).
38. Sreerama, N., Woody, R. W. Estimation of protein secondary structure from circular dichroism spectra: comparison of CONTIN, SELCON, and CDSSTR methods with an expanded reference set. Anal. Biochem 287, 252-260 (2000).
39. Whitmore, L., Wallace, B. A. DICHROWEB, an online server for protein secondary structure analyses from circular dichroism spectroscopic data. Nucleic Acids Research 32, W668-W673 (2004).
40. Lees, J. G., Miles, A. J., Wien, F., Wallace, B. A. A reference database for circular dichroism spectroscopy covering fold and secondary structure space. Bioinformatics 22, 1955-1962 (2006).
41. David, G., Pérez, J. Combined sampler robot and high-performance liquid chromatography: a fully automated system for biological small-angle X-ray scattering experiments at the Synchrotron SOLEIL SWING beamline. J. Appl. Cryst. 42, 892-900 (2009).
42. Konarev, P. V., Petoukhov, M. V., Volkov, V. V., Svergun, D. I. ATSAS 2.1, a program package for small-angle scattering data analysis. J. Appl. Crystallogr. 39, 277-286 (2006).
43. Svergun, D. I. Determination of the regularization parameter in indirect-transform methods using perceptual criteria. J. Appl. Cryst. 25, 495-503 (1992).
44. Evrard, G., Mareuil, F., Bontems, F., Sizun, C., Pérez, J. DADIMODO: a program for refining the structure of multidomain proteins and complexes against small-angle scattering data and NMR-derived restraints. J. Appl. Cryst. 44, 1264-1271 (2011).
45. Svergun, D. I., Barberato, C., Koch, M. H. J. CRYSOL-a Program to Evaluate X-ray Solution Scattering of Biological Macromolecules from Atomic Coordinates. J. Appl. Crystallogr. 28, 768-773 (1995).
46. Jester, B. C., Drillien, R., Ruff, M., Florentz, C. Using Vaccinia's innate ability to introduce DNA into mammalian cells for production of recombinant proteins. J. Biotechnol. 156, 211-213 (2011).
47. Schneider, C. A., Rasband, W. S., Eliceiri, K. NIH Image to ImageJ: 25 years of image analysis. Nat Methods. 9, 671-675 (2012).
48. Cusack, S., Berthet-Colominas, C., Härtlein, M., Nassar, N., Leberman, R. A second class of synthetase structure revealed by X-ray analysis of Escherichia coli seryl-tRNA synthetase at 2.5 A. Nature 347, 249-255 (1990).