Evolution meets disease: Penetrance and functional epistasis of mitochondrial tRNA mutations

PLoS Genetics

Volumn 7, Issue 4, 2011, Pages

  Moreno Loshuertos, Raquel ^a   Ferrín, Gustavo ^a,e   Acín Pérez, Rebeca ^a,f   Gallardo, M Esther ^b   Viscomi, Carlo ^c   Pérez Martos, Acisclo ^a   Zeviani, Massimo ^c   Fernández Silva, Patricio ^a   Enríquez, José Antonio ^a,d  

^a UNIVERSITY OF ZARAGOZA   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

^c DEPARTMENT OF NEUROSURGERY   (Italy)

^d CENTRO NACIONAL DE INVESTIGACIONES CARDIOVASCULARES CNIC   (Spain)

^e HOSPITAL UNIVERSITARIO REINA SOFÍA   (Spain)

^f WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME C OXIDASE; GALACTOSE; ISOLEUCINE; MITOCHONDRIAL DNA; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); TRANSFER RNA; UBIQUINOL CYTOCHROME C REDUCTASE; ISOLEUCINE TRANSFER RNA; RNA; RNA, MITOCHONDRIAL;

ANIMAL CELL; ARTICLE; BIOGENESIS; CELL RESPIRATION; CONTROLLED STUDY; GENE; GENE MUTATION; GENETIC EPISTASIS; GROWTH INHIBITION; MITOCHONDRIAL TRNA GENE; MOLECULAR EVOLUTION; MOUSE; NONHUMAN; NUCLEIC ACID BASE SUBSTITUTION; OXIDATIVE PHOSPHORYLATION; PENETRANCE; PROTEIN SYNTHESIS; ALLELE; ANIMAL; BAGG ALBINO MOUSE; CELL LINE; GENETICS; HUMAN; METABOLISM; MITOCHONDRION; MOLECULAR CLONING; MUTATION; PROTEIN FOLDING;

ALLELES; ANIMALS; CELL LINE; CLONING, MOLECULAR; EPISTASIS, GENETIC; EVOLUTION, MOLECULAR; HUMANS; MICE; MICE, INBRED BALB C; MITOCHONDRIA; MUTATION; OXIDATIVE PHOSPHORYLATION; PROTEIN FOLDING; REACTIVE OXYGEN SPECIES; RNA; RNA, TRANSFER, ILE;

EID: 79955592354     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1001379     Document Type: Article

References (54)

1. Ruiz-Pesini E, Lott MT, Procaccio V, Poole JC, Brandon MC, et al. (2007) An enhanced MITOMAP with a global mtDNA mutational phylogeny. Nucleic Acids Res 35: D823-828.
2. Jacobs HT, (2003) Disorders of mitochondrial protein synthesis. Hum Mol Genet 12: R293-301.
3. Chomyn A, Enriquez JA, Micol V, Fernandez-Silva P, Attardi G, (2000) The mitochondrial myopathy, encephalopathy, lactic acidosis, and stroke-like episode syndrome-associated human mitochondrial tRNALeu(UUR) mutation causes aminoacylation deficiency and concomitant reduced association of mRNA with ribosomes. J Biol Chem 275: 19198-19209.
4. Enriquez JA, Chomyn A, Attardi G, (1995) MtDNA mutation in MERRF syndrome causes defective aminoacylation of tRNA(Lys) and premature translation termination. Nat Genet 10: 47-55.
5. Hao R, Yao YN, Zheng YG, Xu MG, Wang ED, (2004) Reduction of mitochondrial tRNALeu(UUR) aminoacylation by some MELAS-associated mutations. FEBS Lett 578: 135-139.
6. Yasukawa T, Hino N, Suzuki T, Watanabe K, Ueda T, et al. (2000) A pathogenic point mutation reduces stability of mitochondrial mutant tRNA(Ile). Nucleic Acids Res 28: 3779-3784.
7. Florentz C, (2002) Molecular investigations on tRNAs involved in human mitochondrial disorders. Biosci Rep 22: 81-98.
8. Levinger L, Giege R, 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.
9. Rossmanith W, Karwan RM, (1998) Impairment of tRNA processing by point mutations in mitochondrial tRNA(Leu)(UUR) associated with mitochondrial diseases. FEBS Lett 433: 269-274.
10. Tomari Y, Hino N, Nagaike T, Suzuki T, Ueda T, (2003) Decreased CCA-addition in human mitochondrial tRNAs bearing a pathogenic A4317G or A10044G mutation. J Biol Chem 278: 16828-16833.
11. Guan MX, Enriquez JA, Fischel-Ghodsian N, Puranam RS, Lin CP, et al. (1998) The deafness-associated mitochondrial DNA mutation at position 7445, which affects tRNASer(UCN) precursor processing, has long-range effects on NADH dehydrogenase subunit ND6 gene expression. Mol Cell Biol 18: 5868-5879.
12. Bornstein B, Mas JA, Fernandez-Moreno MA, Campos Y, Martin MA, et al. (2002) The A8296G mtDNA mutation associated with several mitochondrial diseases does not cause mitochondrial dysfunction in cybrid cell lines. Hum Mutat 19: 234-239.
13. Bornstein B, Mas JA, Patrono C, Fernandez-Moreno MA, Gonzalez-Vioque E, et al. (2005) Comparative analysis of the pathogenic mechanisms associated with the G8363A and A8296G mutations in the mitochondrial tRNA(Lys) gene. Biochem J 387: 773-778.
14. Jacobs HT, Holt IJ, (2000) The np 3243 MELAS mutation: damned if you aminoacylate, damned if you don't. Hum Mol Genet 9: 463-465.
15. Janssen GM, Maassen JA, van Den Ouweland JM, (1999) The diabetes-associated 3243 mutation in the mitochondrial tRNA(Leu(UUR)) gene causes severe mitochondrial dysfunction without a strong decrease in protein synthesis rate. J Biol Chem 274: 29744-29748.
16. Limongelli A, Schaefer J, Jackson S, Invernizzi F, Kirino Y, et al. (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: 342-349.
17. McFarland R, Clark KM, Morris AA, Taylor RW, Macphail S, et al. (2002) Multiple neonatal deaths due to a homoplasmic mitochondrial DNA mutation. Nat Genet 30: 145-146.
18. Park H, Davidson E, King MP, (2008) Overexpressed mitochondrial leucyl-tRNA synthetase suppresses the A3243G mutation in the mitochondrial tRNA(Leu(UUR)) gene. Rna 14: 2407-2416.
19. Reid FM, Rovio A, Holt IJ, Jacobs HT, (1997) Molecular phenotype of a human lymphoblastoid cell-line homoplasmic for the np 7445 deafness-associated mitochondrial mutation. Hum Mol Genet 6: 443-449.
20. Rorbach J, Yusoff AA, Tuppen H, Abg-Kamaludin DP, Chrzanowska-Lightowlers ZM, et al. (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.
21. Sasarman F, Antonicka H, Shoubridge EA, (2008) The A3243G tRNALeu(UUR) MELAS mutation causes amino acid misincorporation and a combined respiratory chain assembly defect partially suppressed by overexpression of EFTu and EFG2. Hum Mol Genet 17: 3697-3707.
22. Toompuu M, Tiranti V, Zeviani M, Jacobs HT, (1999) Molecular phenotype of the np 7472 deafness-associated mitochondrial mutation in osteosarcoma cell cybrids. Hum Mol Genet 8: 2275-2283.
23. Tuppen HA, Fattori F, Carrozzo R, Zeviani M, DiMauro S, et al. (2008) Further pitfalls in the diagnosis of mtDNA mutations: homoplasmic mt-tRNA mutations. J Med Genet 45: 55-61.
24. Ozawa M, Nishino I, Horai S, Nonaka I, Goto YI, (1997) Myoclonus epilepsy associated with ragged-red fibers: a G-to-A mutation at nucleotide pair 8363 in mitochondrial tRNA(Lys) in two families. Muscle Nerve 20: 271-278.
25. Silvestri G, Moraes CT, Shanske S, Oh SJ, DiMauro S, (1992) A new mtDNA mutation in the tRNA(Lys) gene associated with myoclonic epilepsy and ragged-red fibers (MERRF). Am J Hum Genet 51: 1213-1217.
26. Tiranti V, Carrara F, Confalonieri P, Mora M, Maffei RM, et al. (1999) A novel mutation (8342G-&A) in the mitochondrial tRNA(Lys) gene associated with progressive external ophthalmoplegia and myoclonus. Neuromuscul Disord 9: 66-71.
27. Borthwick GM, Taylor RW, Walls TJ, Tonska K, Taylor GA, et al. (2006) Motor neuron disease in a patient with a mitochondrial tRNAIle mutation. Ann Neurol 59: 570-574.
28. Taylor RW, Chinnery PF, Bates MJ, Jackson MJ, Johnson MA, et al. (1998) A novel mitochondrial DNA point mutation in the tRNA(Ile) gene: studies in a patient presenting with chronic progressive external ophthalmoplegia and multiple sclerosis. Biochem Biophys Res Commun 243: 47-51.
29. Bayona-Bafaluy MP, Acin-Perez R, Mullikin JC, Park JS, Moreno-Loshuertos R, et al. (2003) Revisiting the mouse mitochondrial DNA sequence. Nucleic Acids Res 31: 5349-5355.
30. Johnson KR, Zheng QY, Bykhovskaya Y, Spirina O, Fischel-Ghodsian N, (2001) A nuclear-mitochondrial DNA interaction affecting hearing impairment in mice. Nat Genet 27: 191-194.
31. Moreno-Loshuertos R, Acin-Perez R, Fernandez-Silva P, Movilla N, Perez-Martos A, et al. (2006) Differences in reactive oxygen species production explain the phenotypes associated with common mouse mitochondrial DNA variants. Nat Genet 38: 1261-1268.
32. Acin-Perez R, Bayona-Bafaluy MP, Fernandez-Silva P, Moreno-Loshuertos R, Perez-Martos A, et al. (2004) Respiratory Complex III Is Required to Maintain Complex I in Mammalian Mitochondria. Molecular Cell 13: 805-815.
33. Bayona-Bafaluy MP, Movilla N, Perez-Martos A, Fernandez-Silva P, Enriquez JA, (2008) Functional genetic analysis of the mammalian mitochondrial DNA encoded peptides: a mutagenesis approach. Methods Mol Biol 457: 379-390.
34. Acin-Perez R, Bayona-Bafaluy MP, Bueno M, Machicado C, Fernandez-Silva P, et al. (2003) An intragenic suppressor in the cytochrome c oxidase I gene of mouse mitochondrial DNA. Hum Mol Genet 12: 329-339.
35. Porcelli AM, Ghelli A, Ceccarelli C, Lang M, Cenacchi G, et al. (2010) The genetic and metabolic signature of oncocytic transformation implicates HIF1alpha destabilization. Hum Mol Genet 19: 1019-1032.
36. Guan MX, Fischel-Ghodsian N, Attardi G, (1996) Biochemical evidence for nuclear gene involvement in phenotype of non-syndromic deafness associated with mitochondrial 12S rRNA mutation. Hum Mol Genet 5: 963-971.
37. Hayashi J, Ohta S, Kikuchi A, Takemitsu M, Goto Y, et al. (1991) Introduction of disease-related mitochondrial DNA deletions into HeLa cells lacking mitochondrial DNA results in mitochondrial dysfunction. Proc Natl Acad Sci U S A 88: 10614-10618.
38. Enriquez JA, Attardi G, (1996) Evidence for aminoacylation-induced conformational changes in human mitochondrial tRNAs. Proc Natl Acad Sci U S A 93: 8300-8305.
39. Enriquez JA, Attardi G, (1996) Analysis of aminoacylation of human mitochondrial tRNAs. Methods Enzymol 264: 183-196.
40. Sun T, Zhang Y, (2008) Pentamidine binds to tRNA through non-specific hydrophobic interactions and inhibits aminoacylation and translation. Nucleic Acids Res 36: 1654-1664.
41. Hayashi J, Ohta S, Kagawa Y, Takai D, Miyabayashi S, et al. (1994) Functional and morphological abnormalities of mitochondria in human cells containing mitochondrial DNA with pathogenic point mutations in tRNA genes. J Biol Chem 269: 19060-19066.
42. Hino N, Suzuki T, Yasukawa T, Seio K, Watanabe K, et al. (2004) The pathogenic A4269G mutation in human mitochondrial tRNA(Ile) alters the T-stem structure and decreases the binding affinity for elongation factor Tu. Genes Cells 9: 243-252.
43. Merante F, Myint T, Tein I, Benson L, Robinson BH, (1996) An additional mitochondrial tRNA(Ile) point mutation (A-to-G at nucleotide 4295) causing hypertrophic cardiomyopathy. Hum Mutat 8: 216-222.
44. Wilson FH, Hariri A, Farhi A, Zhao H, Petersen KF, et al. (2004) A cluster of metabolic defects caused by mutation in a mitochondrial tRNA. Science 306: 1190-1194.
45. Kern AD, Kondrashov FA, (2004) Mechanisms and convergence of compensatory evolution in mammalian mitochondrial tRNAs. Nat Genet 36: 1207-1212.
46. Kondrashov FA, (2005) Prediction of pathogenic mutations in mitochondrially encoded human tRNAs. Hum Mol Genet 14: 2415-2419.
47. Meer MV, Kondrashov AS, Artzy-Randrup Y, Kondrashov FA, (2010) Compensatory evolution in mitochondrial tRNAs navigates valleys of low fitness. Nature 464: 279-282.
48. Chomyn A, Lai ST, Shakeley R, Bresolin N, Scarlato G, et al. (1994) Platelet-mediated transformation of mtDNA-less human cells: analysis of phenotypic variability among clones from normal individuals-and complementation behavior of the tRNALys mutation causing myoclonic epilepsy and ragged red fibers. Am J Hum Genet 54: 966-974.
49. Gallardo ME, Moreno-Loshuertos R, Lopez C, Casqueiro M, Silva J, et al. (2006) m.6267G&A: a recurrent mutation in the human mitochondrial DNA that reduces cytochrome c oxidase activity and is associated with tumors. Hum Mutat 27: 575-582.
50. Hofhaus G, Shakeley RM, Attardi G, (1996) Use of polarography to detect respiration defects in cell cultures. Methods Enzymol 264: 476-483.
51. Fernandez-Vizarra E, Lopez-Perez MJ, Enriquez JA, (2002) Isolation of biogenetically competent mitochondria from mammalian tissues and cultured cells. Methods 26: 292-297.
52. Birch-Machin MA, Turnbull DM, (2001) Assaying mitochondrial respiratory complex activity in mitochondria isolated from human cells and tissues. Methods Cell Biol 65: 97-117.
53. Mosmann T, (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65: 55-63.
54. Chomyn A, (1996) In vivo labeling and analysis of human mitochondrial translation products. Methods Enzymol 264: 197-211.