Isoleucyl-tRNA synthetase levels modulate the penetrance of a homoplasmic m.4277T>C mitochondrial tRNA Ile mutation causing hypertrophic cardiomyopathy

Human Molecular Genetics

Volumn 21, Issue 1, 2012, Pages 85-100

  Perli, Elena ^a,b   Giordano, Carla ^b   Tuppen, Helen A L ^e   Montopoli, Monica ^f   Montanari, Arianna ^c   Orlandi, Maurizia ^a,b   Pisano, Annalinda ^a,b   Catanzaro, Daniela ^f   Caparrotta, Laura ^f   Musumeci, Beatrice ^a   Autore, Camillo ^a   Morea, Veronica ^g   Di Micco, Patrizio ^a   Campese, Antonio F ^a   Leopizzi, Martina ^a,d   Gallo, Pietro ^b   Francisci, Silvia ^c   Frontali, Laura ^c   Taylor, Robert W ^e   d'Amati, Giulia ^b  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

^c SAPIENZA UNIVERSITY OF ROME   (Italy)

^d SAPIENZA UNIVERSITY OF ROME   (Italy)

^e NEWCASTLE UNIVERSITY   (United Kingdom)

^f UNIVERSITY OF PADOVA   (Italy)

^g CNR   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

AMINOACYL TRANSFER RNA; GALACTOSE; ISOLEUCINE TRANSFER RNA; THYMIDINE; TRANSFER RNA;

ADOLESCENT; ARTICLE; CASE REPORT; CELL VIABILITY; ELECTROPHORESIS; ENZYME ACTIVITY; GENE MUTATION; GENE OVEREXPRESSION; HUMAN; HUMAN TISSUE; HYPERTROPHIC CARDIOMYOPATHY; NUCLEOTIDE SEQUENCE; PATHOGENICITY; PENETRANCE; POINT MUTATION; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN INTERACTION; RESPIRATORY CHAIN; SKELETAL MUSCLE; STEADY STATE;

ADOLESCENT; BASE SEQUENCE; CARDIOMYOPATHY, HYPERTROPHIC; DNA, MITOCHONDRIAL; HUMANS; ISOLEUCINE-TRNA LIGASE; MALE; MITOCHONDRIA; MOLECULAR SEQUENCE DATA; PENETRANCE; POINT MUTATION; RNA, TRANSFER, ILE;

EID: 83455213504     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddr440     Document Type: Article

References (48)

1. McFarland, R., Taylor, R.W. and Turnbull, D.M. (2010) A neurological perspective on mitochondrial disease. Lancet Neurol., 9, 829-840.
2. Wallace, D.C., Singh, G., Lott, M.T., Hodge, J.A., Schurr, T.G., Lezza, A.M., Elsas, L.J. II and Nikoskelainen, E.K. (1988) Mitochondrial DNA mutation associated with Leber's hereditary optic neuropathy. Science, 242, 1427-1430.
3. Prezant, T.R., Agapian, J.V., Bohlman, M.C., Bu, X., Oztas, S., Qiu, W.Q., Arnos, K.S., Cortopassi, G.A., Jaber, L., Rotter, J.I. et al. (1993) Mitochondrial ribosomal RNA mutation associated with both antibiotic-induced and non-syndromic deafness. Nat. Genet., 4, 289-294.
4. Taylor, R.W., Giordano, C., Davidson, M.M., d'Amati, G. and Bain, H. (2003) A homoplasmic mitochondrial transfer ribonucleic acid mutation as a cause of maternally inherited hypertrophic cardiomyopathy. J. Am. Coll. Cardiol., 41, 1786-1796.
5. McFarland, R., Clark, K.M., Morris, A.A., Taylor, R.W., Macphail, S., Lightowlers, R.N. and Turnbull, D.M. (2002) Multiple neonatal deaths due to a homoplasmic mitochondrial DNA mutation. Nat. Genet., 30, 145-146.
6. Limongelli, A., Schaefer, J., Jackson, S., Invernizzi, F., Kirino, Y., Suzuki, T., Reichmann, H. and Zeviani, M. (2004) Variable penetrance of a familial progressive necrotising encephalopathy due to a novel tRNA(Ile) homoplasmic mutation in the mitochondrial genome. J. Med. Genet., 41, 3492-3499.
7. Moreno-Loshuertos, R., Ferrín, G., Acín-Pérez, R., Gallardo, M.E., Viscomi, C., Pérez-Martos, A., Zeviani, M., Fernández-Silva, P. and Enríquez, J.A. (2011) Evolution meets disease: penetrance and functional epistasis of mitochondrial tRNA mutations. PLoS Genet., 7, e1001379.
8. Moreno-Loshuertos, R., Acín-Pérez, R., Fernández-Silva, P., Movilla, N., Pérez-Martos, A., Rodriguez de Cordoba, S., Gallardo, M.E. and Enríquez, J.A. (2006) Differences in reactive oxygen species production explain the phenotypes associated with common mouse mitochondrial DNA variants. Nat. Genet., 38, 1261-1268.
9. Carelli, V., Achilli, A., Valentino, M.L., Rengo, C., Semino, O., Pala, M., Olivieri, A., Mattiazzi, M., Pallotti, F., Carrara, F. et al. (2006) Haplogroup effects and recombination of mitochondrial DNA: novel clues from the analysis of Leber hereditary optic neuropathy pedigrees. Am. J. Hum. Genet., 78, 564-574.
10. Hudson, G., Carelli, V., Spruijt, L., Gerards, M., Mowbray, C., Achilli, A., Pyle, A., Elson, J., Howell, N., La Morgia, C. et al. (2007). Clinical expression of Leber hereditary optic neuropathy is affected by the mitochondrial DNA-haplogroup background. Am. J. Hum. Genet., 81, 228-233.
11. Gil Borlado, M.C., Moreno Lastres, D., Gonzalez Hoyuela, M., Moran, M., Blazquez, A., Pello, R., Marin Buera, L., Gabaldon, T., Garcia Peñas, J.J. et al. (2010) Impact of the mitochondrial genetic background in complex III deficiency. PLoS One, 5, pii: e12801.
12. Estivill, X., Govea, N., Barceló, E., Badenas, C., Romero, E., Moral, L., Scozzri, R., D'Urbano, L., Zeviani, M. and Torroni, A. (1998) Familial progressive sensorineural deafness is mainly due to the mtDNA A1555G mutation and is enhanced by treatment of aminoglycosides. Am. J. Hum. Genet., 62, 27-35.
13. Carelli, V., Giordano, C. and d'Amati, G. (2003) Pathogenic expression of homoplasmic mtDNA mutations needs a complex nuclear-mitochondrial interaction. Trends Genet., 19, 257-262.
14. Davidson, M.M., Walker, W.F., Hernandez-Rosa, E. and Nesti, C. (2009) Evidence for nuclear modifier gene in mitochondrial cardiomyopathy. J. Mol. Cell. Cardiol., 46, 936-942.
15. Kirkman, M.A., Yu-Wai-Man, P., Korsten, A., Leonhardt, M., Dimitriadis, K., De Coo, I.F., Klopstock, T. and Chinnery, P.F. (2009) Gene-environment interactions in Leber hereditary optic neuropathy. Brain, 132, 2317-2326.
16. McFarland, R., Elson, J.L., Taylor, R.W., Howell, N. and Turnbull, D.M. (2004) Assigning pathogenicity to mitochondrial tRNA mutations: when 'definitely maybe' is not good enough. Trends Genet., 20, 591-596.
17. Scaglia, F. and Wong, L.J.C. (2008) Human mitochondrial transfer RNAs: role of pathogenic mutation in disease. Muscle Nerve, 37, 150-171.
18. van Oven, M. and Kayser, M. (2009) Updated comprehensive phylogenetic tree of global human mitochondrial DNA variation. Hum. Mutat., 30, E386-E394.
19. Robinson, B.H., Petrova-Benedict, R., Buncic, J.R. and Wallace, D.C. (1992) Nonviability of cells with oxidative defects in galactose medium: a screening test for affected patient fibroblasts. Biochem. Med. Metab. Biol., 48, 122-126.
20. Zanna, C., Ghelli, A., Porcelli, A.M., Martinuzzi, A., Carelli, V. and Rugolo, M. (2005) Caspase-independent death of Leber's hereditary optic neuropathy cybrids is driven by energetic failure and mediated by AIF and endonuclease G. Apoptosis, 10, 997-1007.
21. Giordano, C., Monopoli, M., Perli, E., Orlandi, M., Fantin, M., Ross-Cisneros, F.N., Caparrotta, L., Martinuzzi, A., Ragazzi, E., Ghelli, A. et al. (2010) Estrogens ameliorate mitochondrial dysfunction in Leber's hereditary optic neuropathy. Brain, 134, 220-234.
22. Stadelmann, C. and Lassmann, H. (2000) Detection of apoptosis in tissue sections. Cell Tissue Res., 301, 19-31.
23. Rorbach, J., Yusoff, A.A., Tuppen, H., Abg-Kamaludin, D.P., Chrzanowska-Lightowlers, Z.M., Taylor, R.W., Turnbull, D.M., McFarland, R. and Lightowlers, R.N. (2008) Overexpression of human mitochondrial valyl tRNA synthetase can partially restore levels of cognate mt-tRNAVal carrying the pathogenic C25U mutation. Nucleic Acids Res., 36, 3065-3074.
24. Francisci, S., De Luca, C., Oliva, R., Morea, V., Tramontano, A. and Frontali, L. (2005) Aminoacylation and conformational properties of yeast mitochondrial tRNA mutants with respiratory deficiency. RNA, 11, 914-927.
25. Berman, H.M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T.N., Weissig, H., Shindyalov, I.N. and Bourne, P.E. (2000) The protein data bank. Nucleic Acids Res., 28, 235-242.
26. Sprinzl, M. and Vassilenko, K.S. (2005) Compilation of tRNA sequences and sequences of tRNA genes. Nucleic Acids Res., 33, 139-140.
27. Pütz, J., Dupuis, B., Sissler, M. and Florentz, C. (2007) Mamit-tRNA, a database of mammalian mitochondrial tRNA primary and secondary structures. RNA, 13, 1184-1190.
28. Park, H., Davison, E. and King, M.P. (2008) Overexpressed mitochondrial leucyl-tRNA synthetase suppresses the A3243G mutation in the mitochondrial tRNALeu(UUR) gene. RNA, 14, 2407-2416.
29. Montanari, A., De Luca, C., Frontali, L. and Francisci, S. (2010) Aminoacyl-tRNA synthetase are multivalent suppressors of defects due to human equivalent mutations in yeast mt tRNA genes. Biochim. Biophys. Acta, 1803, 1050-1057.
30. Li, R. and Guan, M.X. (2010) Human mitochondrial leucyl-tRNA synthetase corrects mitochondrial dysfunctions due to the tRNALeu(UUR) A3243G mutation, associated with mitochondrial encephalomyopathy, lactic acidosis, and stroke-like symptoms and diabetes. Mol. Cell. Biol., 30, 2147-2154.
31. Flicek, P., Amode, M.R., Barrell, D., Beal, K., Brent, S., Chen, Y., Clapham, P., Coates, G., Fairley, S., Fitzgerald, S. et al. (2011) Ensembl 2011. Nucleic Acids Res., 39, D800-D806.
32. Zhu, H.Y., Wang, S.W., Liu, L., Chen, R., Wang, L., Gong, X.L. and Zhang, M.L. (2009) Genetic variants in mitochondrial tRNA genes are associated with essential hypertension in a Chinese Han population. Clin. Chim. Acta, 410, 64-69.
33. Levinger, L., Giege, R. and Florentz, C. (2003) Pathology-related substitutions in human mitochondrial tRNA(Ile) reduce precursor 3' end processing efficiency in vitro. Nucleic Acids Res., 31, 1904-1912.
34. Giegé, R., Sissler, M. and Florentz, C. (1998) Universal rules and idiosyncratic features in tRNA identity. Nucleic Acids Res., 26, 5017-5035.
35. De Luca, C., Besagni, C., Frontali, L., Bolotin-Fukuhara, M. and Francisci, S. (2006) Mutations in yeast mt tRNAs: specific and general suppression by nuclear encoded tRNA interactors. Gene, 377, 169-176.
36. De Luca, C., Zhou, Y., Montanari, A., Morea, V., Oliva, R., Besagni, C., Bolotin-Fukuhara, M., Frontali, L. and Francisci, S. (2009) Can yeast be used to study mitochondrial diseases? Biolistic tRNA mutants for the analysis of mechanisms and suppressors. Mitochondrion, 9, 408-417.
37. Francisci, S., Montanari, A., De Luca, C. and Frontali, L. (2011) Peptides from aminoacyl-tRNA synthetases can cure the defects due to mutations in mt tRNA genes. Mitochondrion, August 31 [Epub ahead of print].
38. Gotz, A., Tyynismaa, H., Euro, L., Ellonen, P., Hyotylainen, T., Ojala, T., Hamalainen, R.H., Tommiska, J., Raivio, T., Oresic, M. et al. (2011) Exome sequencing identifies mitochondrial alanyl-tRNA synthetase mutations in infantile mitochondrial cardiomyopathy. Am. J. Hum. Genet., 88, 635-642.
39. Kirby, D.M., Thorburn, D.R., Turnbull, D.M. and Taylor, R.W. (2007) Biochemical assays of respiratory chain complex activity. Methods Cell. Biol., 80, 93-119.
40. King, M.P. and Attardi, G. (1989)Human cells lackingmtDNA: repopulation with exogenous mitochondria by complementation. Science, 246, 500-503.
41. Pello, R., Marti{dotless}n, M.A., Carelli, V., Nijtmans, L.G., Achilli, A., Pala, M., Torroni, A., Gomez-Duran, A., Ruiz-Pesini, E., Martinuzzi, A. et al. (2008) Mitochondrial DNA background modulates the assembly kinetics of OXPHOS complexes in a cellular model of mitochondrial disease. Hum. Mol. Genet., 17, 4001-4011.
42. Ghelli, A., Porcelli, A.M., Zanna, C., Vidoni, S., Mattioli, S., Barbieri, A., Iommarini, L., Pala, M., Achilli, A., Torroni, A. et al. (2009) The background of mitochondrial DNA haplogroup J increases the sensitivity of Leber's hereditary optic neuropathy cells to 2,5-hexanedione toxicity. PLoS One, 4, e7922.
43. Nishigaki, Y., Marti, R. and Hirano, M. (2004) ND5 is a hot-spot for multiple atypical mitochondrial DNA deletions in mitochondrial neurogastrointestinal encephalomyopathy. Hum. Mol. Genet., 13, 91-101.
44. Cossarizza, A., Riva, A., Pinti, M., Ammannato, S., Fedeli, P., Mussini, C., Esposito, R. and Galli, M. (2003) Increased mitochondrial DNA content in peripheral blood lymphocytes from HIV-infected patients with lipodystrophy. Antivir. Ther., 8, 51-57.
45. Tuppen, H.A., Hogan, V.E., He, L., Blakely, E.L., Worgan, L., Al-Dosary, M., Saretzki, G., Alston, C.L., Morris, A.A., Clarke, M. et al. (2010) The p.M292T NDUFS2 mutation causes complex I-deficient Leigh syndrome in multiple families. Brain, 133, 2952-2963.
46. Saambrook, J., Fritsch, E.F. and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
47. Ling, L.U., Tan, K.B., Lin, H. andChiu, G.N. (2011)The role of reactive oxygen species and autophagy in safingol-induced cell death. Cell Death Dis., 10, e129.
48. Carelli, V., Vergani, L., Bernazzi, B., Zampieron, C., Bucchi, L., Valentino, M., Rengo, C., Torroni, A. and Martinuzzi, A. (2002) Respiratory function in cybrid cell lines carrying European mtDNA haplogroups: implications for Leber's hereditary optic neuropathy. Biochim. Biophys. Acta, 1588, 7-14.