Induced tRNA Import into Human Mitochondria: Implication of a Host Aminoacyl-tRNA-Synthetase

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Gowher, Ali ^a   Smirnov, Alexandre ^a,b   Tarassov, Ivan ^a   Entelis, Nina ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID TRANSFER RNA LIGASE; ENOLASE; FUNGAL RNA; LYSINE TRANSFER RNA LIGASE; MITOCHONDRIAL RNA; TRANSFER RNA;

ARTICLE; CONTROLLED STUDY; CYTOSOL; DOWN REGULATION; ENZYME REGULATION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IN VIVO STUDY; INTERNALIZATION; MITOCHONDRION; NONHUMAN; PROTEIN EXPRESSION; PROTEIN RNA BINDING; RNA INTERFERENCE; RNA STRUCTURE; RNA TRANSPORT; TARGET CELL;

BASE SEQUENCE; CATION TRANSPORT PROTEINS; ELECTROPHORETIC MOBILITY SHIFT ASSAY; HEP G2 CELLS; HUMANS; INVERTED REPEAT SEQUENCES; LYSINE-TRNA LIGASE; MITOCHONDRIA; PROTEIN BINDING; PROTEIN PRECURSORS; RNA TRANSPORT; RNA, FUNGAL; RNA, TRANSFER; RNA, TRANSFER, LYS; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84879151792     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0066228     Document Type: Article

References (50)

1. Neupert W, (1997) Protein import into mitochondria. Annu Rev Biochem 66: 863-917.
2. Chacinska A, Koehler CM, Milenkovic D, Lithgow T, Pfanner N, (2009) Importing mitochondrial proteins: machineries and mechanisms. Cell 138: 628-644.
3. Tarassov I, Kamenski P, Kolesnikova O, Karicheva O, Martin RP, et al. (2007) Import of nuclear DNA-encoded RNAs into mitochondria and mitochondrial translation. Cell Cycle 6: 2473-2477.
4. Salinas T, Duchene AM, Marechal-Drouard L, (2008) Recent advances in tRNA mitochondrial import. Trends Biochem Sci 33: 320-329.
5. Schneider A, (2011) Mitochondrial tRNA import and its consequences for mitochondrial translation. Annu Rev Biochem 80: 1033-1053.
6. Martin R, Schneller JM, Stahl A, Dirheimer G, (1979) Import of nuclear deoxyribonucleic acid coded lysine-accepting transfer ribonucleic acid (anticodon C-U-U) into yeast mitochondria. Biochemistry 18: 4600-4605.
7. Kamenski P, Kolesnikova O, Jubenot V, Entelis N, Krasheninnikov IA, et al. (2007) Evidence for an Adaptation Mechanism of Mitochondrial Translation via tRNA Import from the Cytosol. Mol Cell 26: 625-637.
8. Tarassov I, Entelis N, Martin R, (1995) Mitochondrial import of a cytoplasmic lysine-tRNA in yeast is mediated by cooperation of cytoplasmic and mitochondrial lysyl-tRNA synthetases. EMBO J 14: 3461-3471.
9. Kamenski P, Smirnova E, Kolesnikova O, Krasheninnikov IA, Martin RP, et al. (2010) tRNA mitochondrial import in yeast: Mapping of the import determinants in the carrier protein, the precursor of mitochondrial lysyl-tRNA synthetase. Mitochondrion 10: 284-293.
10. Entelis N, Brandina I, Kamenski P, Krasheninnikov IA, Martin RP, et al. (2006) A glycolytic enzyme, enolase, is recruited as a cofactor of tRNA targeting toward mitochondria in Saccharomyces cerevisiae. Genes Dev 20: 1609-1620.
11. Brandina I, Graham J, Lemaitre-Guillier C, Entelis N, Krasheninnikov I, et al. (2006) Enolase takes part in a macromolecular complex associated to mitochondria in yeast. Biochim Biophys Acta 1757: 1217-1228.
12. Kolesnikova O, Kazakova H, Comte C, Steinberg S, Kamenski P, et al. (2010) Selection of RNA aptamers imported into yeast and human mitochondria. RNA 16: 926-941.
13. Tarassov I, Entelis N, Martin RP, (1995) An intact protein translocating machinery is required for mitochondrial import of a yeast cytoplasmic tRNA. J Mol Biol 245: 315-323.
14. Kolesnikova OA, Entelis NS, Jacquin-Becker C, Goltzene F, Chrzanowska-Lightowlers ZM, et al. (2004) Nuclear DNA-encoded tRNAs targeted into mitochondria can rescue a mitochondrial DNA mutation associated with the MERRF syndrome in cultured human cells. Hum Mol Genet 13: 2519-2534.
15. Karicheva OZ, Kolesnikova OA, Schirtz T, Vysokikh MY, Mager-Heckel AM, et al. (2011) Correction of the consequences of mitochondrial 3243A>G mutation in the MT-TL1 gene causing the MELAS syndrome by tRNA import into mitochondria. Nucleic Acids Res 39: 8173-8186.
16. Wang G, Shimada E, Zhang J, Hong JS, Smith GM, et al. (2012) Correcting human mitochondrial mutations with targeted RNA import. Proc Natl Acad Sci U S A 109: 4840-4845.
17. Comte C, Tonin Y, Heckel-Mager AM, Boucheham A, Smirnov A, et al. (2012) Mitochondrial targeting of recombinant RNAs modulates the level of a heteroplasmic mutation in human mitochondrial DNA associated with Kearns Sayre Syndrome. Nucleic Acids Res.
18. Kolesnikova OA, Entelis NS, Mireau H, Fox TD, Martin RP, et al. (2000) Suppression of mutations in mitochondrial DNA by tRNAs imported from the cytoplasm. Science 289: 1931-1933.
19. Entelis NS, Kolesnikova OA, Dogan S, Martin RP, Tarassov IA, (2001) 5 S rRNA and tRNA Import into Human Mitochondria. Comparison of in vitro requirements. J Biol Chem 276: 45642-45653.
20. Tolkunova E, Park H, Xia J, King MP, Davidson E, (2000) The human lysyl-tRNA synthetase gene encodes both the cytoplasmic and mitochondrial enzymes by means of an unusual alternative splicing of the primary transcript [In Process Citation]. J Biol Chem 275: 35063-35069.
21. Sepuri NB, Gorla M, King MP, (2012) Mitochondrial Lysyl-tRNA Synthetase Independent Import of tRNA Lysine into Yeast Mitochondria. PLoS One 7: e35321.
22. Entelis N, Kolesnikova O, Kazakova H, Brandina I, Kamenski P, et al. (2002) Import of nuclear encoded RNAs into yeast and human mitochondria: experimental approaches and possible biomedical applications. Genet Eng (NY) 24: 191-213.
23. Entelis NS, Krasheninnikov IA, Martin RP, Tarassov IA, (1996) Mitochondrial import of a yeast cytoplasmic tRNA (Lys): possible roles of aminoacylation and modified nucleosides in subcellular partitioning. FEBS Lett 384: 38-42.
24. Smirnov A, Tarassov I, Mager-Heckel AM, Letzelter M, Martin RP, et al. (2008) Two distinct structural elements of 5S rRNA are needed for its import into human mitochondria. RNA 14: 749-759.
25. Kaminska M, Shalak V, Francin M, Mirande M, (2007) Viral hijacking of mitochondrial lysyl-tRNA synthetase. J Virol 81: 68-73.
26. Mercer TR, Neph S, Dinger ME, Crawford J, Smith MA, et al. (2011) The human mitochondrial transcriptome. Cell 146: 645-658.
27. Rubio MA, Rinehart JJ, Krett B, Duvezin-Caubet S, Reichert AS, et al. (2008) Mammalian mitochondria have the innate ability to import tRNAs by a mechanism distinct from protein import. Proc Natl Acad Sci U S A 105: 9186-9191.
28. Puranam RS, Attardi G, (2001) The RNase P associated with HeLa cell mitochondria contains an essential RNA component identical in sequence to that of the nuclear RNase P. Mol Cell Biol. 21: 548-561.
29. Wang G, Chen HW, Oktay Y, Zhang J, Allen EL, et al. (2010) PNPASE Regulates RNA Import into Mitochondria. Cell 142: 456-467.
30. Smirnov A, Comte C, Mager-Heckel AM, Addis V, Krasheninnikov IA, et al. (2010) Mitochondrial enzyme rhodanese is essential for 5 S ribosomal RNA import into human mitochondria. J Biol Chem 285: 30792-30803.
31. Smirnov A, Entelis N, Martin RP, Tarassov I, (2011) Biological significance of 5S rRNA import into human mitochondria: role of ribosomal protein MRP-L18. Genes Dev 25: 1289-1305.
32. Entelis NS, Kieffer S, Kolesnikova OA, Martin RP, Tarassov IA, (1998) Structural requirements of tRNALys for its import into yeast mitochondria. Proc Natl Acad Sci U S A 95: 2838-2843.
33. Antonellis A, Green ED, (2008) The role of aminoacyl-tRNA synthetases in genetic diseases. Annu Rev Genomics Hum Genet 9: 87-107.
34. Dias J, Octobre G, Kobbi L, Comisso M, Flisiak S, et al. (2012) Activation of human mitochondrial lysyl-tRNA synthetase upon maturation of its premitochondrial precursor. Biochemistry 51: 909-916.
35. Diaz-Lazcoz Y, Aude JC, Nitschke P, Chiapello H, Landes-Devauchelle C, et al. (1998) Evolution of genes, evolution of species: the case of aminoacyl-tRNA synthetases. Mol Biol Evol 15: 1548-1561.
36. Duchene AM, Pujol C, Marechal-Drouard L (2008) Import of tRNAs and aminoacyl-tRNA synthetases into mitochondria. Curr Genet.
37. Negrutskii BS, Deutscher MP, (1991) Channeling of aminoacyl-tRNA for protein synthesis in vivo. Proc Natl Acad Sci U S A 88: 4991-4995.
38. Belostotsky R, Frishberg Y, Entelis N, (2012) Human mitochondrial tRNA quality control in health and disease: a channelling mechanism? RNA Biol 9: 33-39.
39. Salinas T, Duchene AM, Delage L, Nilsson S, Glaser E, et al. (2006) The voltage-dependent anion channel, a major component of the tRNA import machinery in plant mitochondria. Proc Natl Acad Sci U S A 103: 18362-18367.
40. Pancholi V, (2001) Multifunctional alpha-enolase: its role in diseases. Cell Mol Life Sci 58: 902-920.
41. Bouzaidi-Tiali N, Aeby E, Charriere F, Pusnik M, Schneider A, (2007) Elongation factor 1a mediates the specificity of mitochondrial tRNA import in T. brucei. Embo J 26: 4302-4312.
42. Barrey E, Saint-Auret G, Bonnamy B, Damas D, Boyer O, et al. (2011) Pre-microRNA and mature microRNA in human mitochondria. PLoS One 6: e20220.
43. Das S, Ferlito M, Kent OA, Fox-Talbot K, Wang R, et al. (2012) Nuclear miRNA regulates the mitochondrial genome in the heart. Circ Res 110: 1596-1603.
44. Sripada L, Tomar D, Prajapati P, Singh R, Singh AK, et al. (2012) Systematic analysis of small RNAs associated with human mitochondria by deep sequencing: detailed analysis of mitochondrial associated miRNA. PLoS One 7: e44873.
45. Bandiera S, Ruberg S, Girard M, Cagnard N, Hanein S, et al. (2011) Nuclear outsourcing of RNA interference components to human mitochondria. PLoS One 6: e20746.
46. Markham NR, Zuker M, (2005) DINAMelt web server for nucleic acid melting prediction. Nucleic Acids Res 33: W577-581.
47. Markham NR, Zuker M, (2008) UNAFold: software for nucleic acid folding and hybridization. Methods Mol Biol 453: 3-31.
48. Sugimoto N, Nakano S, Katoh M, Matsumura A, Nakamuta H, et al. (1995) Thermodynamic parameters to predict stability of RNA/DNA hybrid duplexes. Biochemistry 34: 11211-11216.
49. Kaminska M, Deniziak M, Kerjan P, Barciszewski J, Mirande M, (2000) A recurrent general RNA binding domain appended to plant methionyl-tRNA synthetase acts as a cis-acting cofactor for aminoacylation. Embo J 19: 6908-6917.
50. Francin M, Kaminska M, Kerjan P, Mirande M, (2002) The N-terminal domain of mammalian Lysyl-tRNA synthetase is a functional tRNA-binding domain. J Biol Chem 277: 1762-1769.