Ribosome Rescue and Translation Termination at Non-Standard Stop Codons by ICT1 in Mammalian Mitochondria

English version České info

Mammalian mitochondrial ICT1, a bacterial ArfB homolog, is interestingly an integral component of the mitoribosome (MRPL58). The mechanism of ribosome rescue by this factor was obscure and is addressed here. Utilizing a homologous mitochondria system of purified components we demonstrate that the integrated ICT1 has no rescue activity, as opposed to a previous model. Rather, purified ICT1 added to mitoribosomes has a general rescue activity; it recycles ribosomes stalled at the end or in the middle of mRNAs and can even hydrolyze peptidyl-tRNA bound to non-programmed ribosomes. These results further imply that ICT1 can function in the translation termination at non-standard stop codons AGA/G in mammalian mitochondria. Our data challenge a previous model claiming that RF1Lmt/mtRF1a is responsible for the translation termination at non-standard stop codons. A mutational study indicates that the unique insertion sequence in ICT1 is essential for peptide release. The function of RF1mt, another member of the class1 RFs in mammalian mitochondria, was also examined and is discussed.

Vyšlo v časopise: Ribosome Rescue and Translation Termination at Non-Standard Stop Codons by ICT1 in Mammalian Mitochondria. PLoS Genet 10(9): e32767. doi:10.1371/journal.pgen.1004616
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004616

Souhrn

Zdroje

1. NeubauerC, GilletR, KelleyAC, RamakrishnanV (2012) Decoding in the absence of a codon by tmRNA and SmpB in the ribosome. Science 335 : 1366–1369.

2. ChadaniY, ItoK, KutsukakeK, AboT (2012) ArfA recruits release factor 2 to rescue stalled ribosomes by peptidyl-tRNA hydrolysis in Escherichia coli. Mol Microbiol 86 : 37–50.

3. ShimizuY (2012) ArfA recruits RF2 into stalled ribosomes. J Mol Biol 423 : 624–631.

4. HandaY, InahoN, NamekiN (2011) YaeJ is a novel ribosome-associated protein in Escherichia coli that can hydrolyze peptidyl-tRNA on stalled ribosomes. Nucleic Acids Res 39 : 1739–1748.

5. GagnonMG, SeetharamanSV, BulkleyD, SteitzTA (2012) Structural Basis for the Rescue of Stalled Ribosomes: Structure of YaeJ Bound to the Ribosome. Science 335 : 1370–1372.

6. DuarteI, NabuursSB, MagnoR, HuynenM (2012) Evolution and diversification of the organellar release factor family. Mol Biol Evol 29 : 3497–3512.

7. RichterR, RorbachJ, PajakA, SmithPM, WesselsHJ, et al. (2010) A functional peptidyl-tRNA hydrolase, ICT1, has been recruited into the human mitochondrial ribosome. EMBO J 29 : 1116–1125.

8. KocEC, CimenH, KumcuogluB, AbuN, AkpinarG, et al. (2013) Identification and characterization of CHCHD1, AURKAIP1, and CRIF1 as new members of the mammalian mitochondrial ribosome. Front Physiol 4 : 183.

9. NozakiY, MatsunagaN, IshizawaT, UedaT, TakeuchiN (2008) HMRF1L is a human mitochondrial translation release factor involved in the decoding of the termination codons UAA and UAG. Genes Cells 13 : 429–438.

10. Soleimanpour-LichaeiHR, KuhlI, GaisneM, PassosJF, WydroM, et al. (2007) mtRF1a is a human mitochondrial translation release factor decoding the major termination codons UAA and UAG. Mol Cell 27 : 745–757.

11. ShimizuY, InoueA, TomariY, SuzukiT, YokogawaT, et al. (2001) Cell-free translation reconstituted with purified components. Nat Biotechnol 19 : 751–755.

12. NissenP, HansenJ, BanN, MoorePB, SteitzTA (2000) The structural basis of ribosome activity in peptide bond synthesis. Science 289 : 920–930.

13. LindC, SundJ, AqvistJ (2013) Codon-reading specificities of mitochondrial release factors and translation termination at non-standard stop codons. Nat Commun 4 : 2940.

14. KorostelevA, AsaharaH, LancasterL, LaurbergM, HirschiA, et al. (2008) Crystal structure of a translation termination complex formed with release factor RF2. Proc Natl Acad Sci USA 105 : 19684–19689.

15. LaurbergM, AsaharaH, KorostelevA, ZhuJ, TrakhanovS, et al. (2008) Structural basis for translation termination on the 70S ribosome. Nature 454 : 852–857.

16. GreberBJ, BoehringerD, LeitnerA, BieriP, Voigts-HoffmannF, et al. (2014) Architecture of the large subunit of the mammalian mitochondrial ribosome. Nature 505 : 515–519.

17. OttM, HerrmannJM (2010) Co-translational membrane insertion of mitochondrially encoded proteins. Biochim Biophys Acta 1803 : 767–775.

18. DujeancourtL, RichterR, Chrzanowska-LightowlersZM, BonnefoyN, HerbertCJ (2013) Interactions between peptidyl tRNA hydrolase homologs and the ribosomal release factor Mrf1 in S. pombe mitochondria. Mitochondrion 13 : 871–880.

19. TemperleyR, RichterR, DennerleinS, LightowlersRN, Chrzanowska-LightowlersZM (2010) Hungry codons promote frameshifting in human mitochondrial ribosomes. Science 327 : 301.

20. KogureH, HandaY, NagataM, KanaiN, GuntertP, et al. (2013) Identification of residues required for stalled-ribosome rescue in the codon-independent release factor YaeJ. Nucleic Acids Res 42 : 3152–63 doi:10.1093/nar/gkt1280

21. HuynenMA, DuarteI, Chrzanowska-LightowlersZM, NabuursSB (2012) Structure based hypothesis of a mitochondrial ribosome rescue mechanism. Biol Direct 7 : 14.

22. SpremulliLL (2007) Large-scale isolation of mitochondrial ribosomes from mammalian tissues. Methods Mol Biol 372 : 265–275.

23. Triana-AlonsoFJ, ChakraburttyK, NierhausKH (1995) The elongation factor 3 unique in higher fungi and essential for protein biosynthesis is an E site factor. J Biol Chem 270 : 20473–20478.

24. TrianaF, NierhausKH, ChakraburttyK (1994) Transfer RNA binding to 80S ribosomes from yeast: evidence for three sites. Biochem. Mol Biol Int 33 : 909–915.

25. TsuboiM, MoritaH, NozakiY, AkamaK, UedaT, et al. (2009) EF-G2mt Is an Exclusive Recycling Factor in Mammalian Mitochondrial Protein Synthesis. Mol Cell 35 : 502–510.

26. HandaY, HikawaY, TochioN, KogureH, InoueM, et al. (2010) Solution structure of the catalytic domain of the mitochondrial protein ICT1 that is essential for cell vitality. J Mol Biol 404 : 260–273.