Molecular dysfunction associated with the human mitochondrial 3302A>G mutation in the MTTL1 (mt-tRNALeu(UUR)) gene

Nucleic Acids Research

Volumn 34, Issue 22, 2006, Pages 6404-6415

  Maniura Weber, Katharina ^a   Helm, Mark ^b   Engemann, Katrin ^a   Eckertz, Sabrina ^a   Möllers, Myriam ^a   Schauen, Matthias ^a   Hayrapetyan, Armine ^b   von Kleist Retzow, Jürgen Christoph ^a   Lightowlers, Robert N ^c   Bindoff, Laurence A ^d   Wiesner, Rudolf J ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c NEWCASTLE UNIVERSITY   (United Kingdom)

^d UNIVERSITY OF BERGEN   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

MITOCHONDRIAL RNA; MITOCHONDRIAL TRANSFER RNA; RNA 16S; TRANSFER RNA; UNCLASSIFIED DRUG;

ARTICLE; GENE MUTATION; HUMAN; MITOCHONDRIAL DNA DISORDER; MOLECULAR STABILITY; NUCLEIC ACID BASE SUBSTITUTION; PRIORITY JOURNAL; PROTEIN STRUCTURE; RNA STRUCTURE;

CELL PROLIFERATION; CLONE CELLS; ELECTRON TRANSPORT; GENES, MITOCHONDRIAL; GENOTYPE; HUMANS; MITOCHONDRIA; MITOCHONDRIAL MYOPATHIES; MUSCLE, SKELETAL; POINT MUTATION; RNA; RNA PRECURSORS; RNA STABILITY; RNA, TRANSFER, LEU; TRANSFER RNA AMINOACYLATION;

EID: 33845908715     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkl727     Document Type: Article

References (39)

1. Taylor,R.W. and Turnbull,D.M. (2005) Mitochondrial DNA mutations in human disease. Nature Rev. Genet., 6, 389-402.
2. Bindoff,L.A., Howell,N., Poulton,J., McCullough,D.A., Morten,K.J., Lightowlers,R.N., Turnbull,D.M. and Weber,K. (1993) Abnormal RNA processing associated with a novel tRNA mutation in mitochondrial DNA. A potential disease mechanism. J. Biol. Chem., 268, 19559-19564.
3. Van Den Bosch,B.J., De Coo,I.F., Hendrickx,A.T., Busch,H.F., De Jong,G., Scholte,H.R. and Smeets,H.J. (2004) Increased risk for cardiorespiratory failure associated with the A3302G mutation in the mitochondrial DNA encoded tRNA(Leu(UUR)) gene. Neuromuscul. Disord., 14, 683-688.
4. Helm,M., Brule,H., Friede,D., Giege,R., Putz,D. and Florentz,C. (2000) Search for characteristic structural features of mammalian mitochondrial tRNAs. RNA, 6, 1356-1379.
5. King,M.P. and Attardi,G. (1989) Human cells lacking mtDNA: Repopulation with exogenous mitochondria by complementation. Science, 246, 500-503.
6. Blau,H.M. and Webster,C. (1981) Isolation and characterization of human muscle cells. Proc. Natl Acad. Sci. USA, 78, 5623-5627.
7. Goto,Y., Nonaka,I. and Horai,S. (1990) A mutation in the tRNA(Leu)(UUR) gene associated with the MELAS subgroup of mitochondrial encephalomyopathies. Nature, 348, 651-653.
8. Rustin,P., Chretien,D., Bourgeron,T., Gerard,B., Rotig,A., Saudubray,J.M. and Munnich,A. (1994) Biochemical and molecular investigations in respiratory chain deficiencies. Clin. Chim. Acta, 228, 35-51.
9. Enriquez,J.A., Chomyn,A. and Attardi,G. (1995) MtDNA mutation in MERRF syndrome causes defective aminoacylation of tRNA(Lys) and premature translation termination. Nature Genet., 10, 47-55.
10. Sohm,B., Frugier,M., Brule,H., Olszak,K., Przykorska,A. and Florentz,C. (2003) Towards understanding human mitochondrial leucine aminoacylation identity. J. Mol. Biol, 328, 995-1010.
11. Fechter,P., Rudinger,J., Giege,R. and Theobald-Dietrich,A. (1998) Ribozyme processed tRNA transcripts with unfriendly internal promoter for T7 RNA polymerase: Production and activity. FEBS Lett., 436, 99-103.
12. Helm,M., Brule,H., Degoul,F., Cepanec,C., Leroux,J.P., Giege,R. and Florentz,C. (1998) The presence of modified nucleotides is required for cloverleaf folding of a human mitochondrial tRNA. Nucleic Acids Res., 26, 1636-1643.
13. Yasukawa,T., Suzuki,T., Ishii,N., Ueda,T., Ohta,S. and Watanabe,K. (2000) Defect in modification at the anticodon wobble nucleotide of mitochondrial tRNA(Lys) with the MERRF encephalomyopathy pathogenic mutation. FEBS Lett., 467, 175-178.
14. Watmough,N.J., Bindoff,L.A., Birch-MacHin,M.A., Jackson,S., Bartlett,K., Ragan,C.I., Poulton,J., Gardiner,R.M., Sherratt,H.S. and Turnbull,D.M. (1990) Impaired mitochondrial beta-oxidation in a patient with an abnormality of the respiratory chain. Studies in skeletal muscle mitochondria. J. Clin. Invest., 85, 177-184.
15. Chomyn,A., Enriquez,J.A., Micol,V., Fernandez-Silva,P. and 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.
16. Yasukawa,T., Suzuki,T., Ueda,T., Ohta,S. and Watanabe,K. (2000) Modification defect at anticodon wobble nucleotide of mitochondrial tRNAs(Leu)(UUR) with pathogenic mutations of mitochondrial myopathy, encephalopathy, lactic acidosis, and stroke-like episodes. J. Biol. Chem., 275, 4251-4257.
17. MacDonald,R.J., Swift,G.H., Przybyla,A.E. and Chirgwin,J.M. (1987) Isolation of RNA using guanidinium salts. Methods Enzymol., 152, 219-227.
18. Schon,E.A., Koga,Y., Davidson,M., Moraes,C.T. and King,M.P. (1992) The mitochondrial tRNA(Leu)(UUR)) mutation in MELAS: A model for pathogenesis. Biochim. Biophys. Acta, 1101, 206-209.
19. Kaufmann,P., Koga,Y., Shanske,S., Hirano,M., DiMauro,S., King,M.P. and Schon,E.A. (1996) Mitochondrial DNA and RNA processing in MELAS. Ann. Neurol., 40, 172-180.
20. Koga,Y., Davidson,M., Schon,E.A. and King,M.P. (1993) Fine mapping of mitochondrial RNAs derived from the mtDNA region containing a point mutation associated with MELAS. Nucleic Acids Res., 21, 657-662.
21. El Meziane,A., Lehtinen,S.K., Holt,I.J. and Jacobs,H.T. (1998) Mitochondrial tRNALeu isoforms in lung carcinoma cybrid cells containing the np 3243 mtDNA mutation. Hum. Mol. Genet., 7, 2141-2147.
22. Jacobs,H.T. and Holt,I.J. (2000) The np 3243 MELAS mutation: Damned if you aminoacylate, damned if you don't. Hum. Mol. Genet., 9, 463-465.
23. Bornstein,B., Mas,J.A., Patrono,C., Fernandez-Moreno,M.A., Gonzalez-Vioque,E., Campos,Y., Carrozzo,R., Martin,M.A., Del Hoyo,P., Santorelli,F.M. 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.
24. Mollers,M., Maniura-Weber,K., Kiseljakovic,E., Bust,M., Hayrapetyan,A., Jaksch,M., Helm,M., Wiesner,R.J. and von Kleist-Retzow,J.C. (2005) A new mechanism for mtDNA pathogenesis: Impairment of post-transcriptional maturation leads to severe depletion of mitochondrial tRNASer(UCN) caused by T7512C and G7497A point mutations. Nucleic Acids Res., 33, 5647-5658.
25. Yasukawa,T., Hino,N., Suzuki,T., Watanabe,K., Ueda,T. and Ohta,S. (2000) A pathogenic point mutation reduces stability of mitochondrial mutant tRNA(Ile). Nucleic Acids Res., 28, 3779-3784.
26. King,M.P., Koga,Y., Davidson,M. and Schon,E.A. (1992) Defects in mitochondrial protein synthesis and respiratory chain activity segregate with the tRNA(Leu(UUR)) mutation associated with mitochondrial myopathy, encephalopathy, lactic acidosis, and strokelike episodes. Mol. Cell. Biol, 12, 480-490.
27. Yan,H., Zareen,N. and Levinger,L. (2006) Naturally occurring mutations in human mitochondrial pre-tRNASer(UCN) can affect the tRNase Z cleavage site, processing kinetics and substrate secondary structure. J. Biol. Chem., 281, 3926-3935.
28. Koga,A., Koga,Y., Akita,Y., Fukiyama,R., Ueki,I., Yatsuga,S. and Matsuishi,T. (2003) Increased mitochondrial processing intermediates associated with three tRNA(Leu(UUR)) gene mutations. Neuromuscul. Disord., 13, 259-262.
29. Levinger,L., Oestreich,I., Florentz,C. and Morl,M. (2004) A Pathogenesis-associated mutation in human mitochondrial tRNA(Leu(UUR)) leads to reduced 3′-end processing and CCA addition. J. Mol. Biol., 337, 535-544.
30. Rossmanith,W. and Karwan,R.M. (1998) Impairment of tRNA processing by point mutations in mitochondrial tRNA(Leu)(UUR) associated with mitochondrial diseases. FEBS Lett., 433, 269-274.
31. Sohm,B., Sissler,M., Park,H., King,M.P. and Florentz,C. (2004) recognition of human mitochondrial tRNA(Leu(UUR)) by its cognate Leucyl-tRNA synthetase. J. Mol. Biol, 339, 17-29.
32. Helm,M., Florentz,C., Chomyn,A. and Attardi,G. (1999) Search for differences in post-transcriptional modification patterns of mitochondrial DNA-encoded wild-type and mutant human tRNA(Lys) and tRNA(Leu(UUR)). Nucleic Acids Res., 27, 756-763.
33. Borner,G.V., Zeviani,M., Tiranti,V., Carrara,F., Hoffmann,S., Gerbitz,K.D., Lochmuller,H., Pongratz,D., Klopstock,T., Melberg,A. et al. (2000) Decreased aminoacylation of mutant tRNAs in MELAS but not in MERRF patients. Hum. Mol. Genet., 9, 467-475.
34. Kirino,Y., Goto,Y.I., Campos,Y., Arenas,J. and Suzuki,T. (2005) Specific correlation between the wobble modification deficiency in mutant tRNAs and the clinical features of a human mitochondrial disease. Proc. Natl Acad. Sci. USA, 102, 7127-7132.
35. Dunbar,D.R., Moonie,P.A., Zeviani,M. and Holt,I.J. (1996) Complex I deficiency is associated with 3243G:C mitochondrial DNA in osteosarcoma cell cybrids. Hum. Mol. Genet., 5, 123-129.
36. Flierl,A., Reichmann,H. and Seibel,P. (1997) Pathophysiology of the MELAS 3243 transition mutation. J. Biol. Chem., 272, 27189-27196.
37. Janssen,G.M., Maassen,J.A. and van Den Ouweland,J.M. (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.
38. Reid,F.M., Vernham,G.A. and Jacobs,H.T. (1994) A novel mitochondrial point mutation in a maternal pedigree with sensorineural deafness. Hum. Mutat., 3, 243-247.
39. Yasukawa,T., Kirino,Y., Ishii,N., Holt,I.J., Jacobs,H.T., Makifuchi,T., Fukuhara,N., Ohta,S., Suzuki,T. and Watanabe,K. (2005) Wobble modification deficiency in mutant tRNAs in patients with mitochondrial diseases. FEBS Lett., 579, 2948-2952.