Structure based hypothesis of a mitochondrial ribosome rescue mechanism

Biology Direct

Volumn 7, Issue , 2012, Pages

  Huynen, Martijn A ^a   Duarte, Isabel ^a   Chrzanowska Lightowlers, Zofia M A ^b   Nabuurs, Sander B ^a,c  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b NEWCASTLE UNIVERSITY   (United Kingdom)

^c Lead Pharma Medicine   (Netherlands)

Author keywords

Class i release factor; Mitochondrial genetic code; MtRF1; MtRF1a; Stalled ribosome; Translation termination

Indexed keywords

VERTEBRATA;

AMINOACYL TRANSFER RIBONUCLEIC ACID HYDROLASE; AMINOACYL TRANSFER RNA; AMINOACYL-TRNA HYDROLASE; BACTERIAL RNA; CARBOXYLESTERASE; MITOCHONDRIAL PROTEIN; MTRF1A PROTEIN, HUMAN; TMRNA; TRANSLATION TERMINATION FACTOR; TRNA, PEPTIDYL; TRNA, PEPTIDYL-;

ANIMAL; ARTICLE; BIOLOGICAL MODEL; GENETICS; HUMAN; METABOLISM; MITOCHONDRION; NUCLEOTIDE SEQUENCE; PHYLOGENY; PROTEIN SYNTHESIS; RIBOSOME; RNA TRANSLATION; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; STOP CODON; THERMUS THERMOPHILUS; VERTEBRATE;

ANIMALS; CARBOXYLIC ESTER HYDROLASES; CODON, TERMINATOR; CONSERVED SEQUENCE; HUMANS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; MODELS, BIOLOGICAL; PEPTIDE CHAIN TERMINATION, TRANSLATIONAL; PEPTIDE TERMINATION FACTORS; PHYLOGENY; PROTEIN BIOSYNTHESIS; RIBOSOMES; RNA, BACTERIAL; RNA, TRANSFER, AMINO ACYL; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, PROTEIN; THERMUS THERMOPHILUS; VERTEBRATES;

EID: 84860607675     PISSN: None     EISSN: 17456150     Source Type: Journal    
DOI: 10.1186/1745-6150-7-14     Document Type: Article

References (38)

1. Brenner S, Stretton AO, Kaplan S. Genetic code: the 'nonsense' triplets for chain termination and their suppression. Nature 1965, 206:994-998. 10.1038/206994a0, 5320272.
2. Brenner S, Barnett L, Katz ER, Crick FH. UGA: a third nonsense triplet in the genetic code. Nature 1967, 213:449-450. 10.1038/213449a0, 6032223.
3. Scolnick E, Tompkins R, Caskey T, Nirenberg M. Release factors differing in specificity for terminator codons. Proc Natl Acad Sci U S A 1968, 61:768-774. 10.1073/pnas.61.2.768, 225226, 4879404.
4. Frolova L, Le Goff X, Rasmussen HH, Cheperegin S, Drugeon G, Kress M, Arman I, Haenni AL, Celis JE, Philippe M, et al. A highly conserved eukaryotic protein family possessing properties of polypeptide chain release factor. Nature 1994, 372:701-703. 10.1038/372701a0, 7990965.
5. Korostelev AA. Structural aspects of translation termination on the ribosome. RNA 2011, 17:1409-1421. 10.1261/rna.2733411, 3153966, 21700725.
6. Weixlbaumer A, Jin H, Neubauer C, Voorhees RM, Petry S, Kelley AC, Ramakrishnan V. Insights into translational termination from the structure of RF2 bound to the ribosome. Science 2008, 322:953-956. 10.1126/science.1164840, 2642913, 18988853.
7. Laurberg M, Asahara H, Korostelev A, Zhu J, Trakhanov S, Noller HF. Structural basis for translation termination on the 70 S ribosome. Nature 2008, 454:852-857. 10.1038/nature07115, 18596689.
8. Korostelev A, Zhu J, Asahara H, Noller HF. Recognition of the amber UAG stop codon by release factor RF1. EMBO J 2010, 29:2577-2585. 10.1038/emboj.2010.139, 2928684, 20588254.
9. Korostelev A, Asahara H, Lancaster L, Laurberg M, Hirschi A, Zhu J, Trakhanov S, Scott WG, Noller HF. Crystal structure of a translation termination complex formed with release factor RF2. Proc Natl Acad Sci U S A 2008, 105:19684-19689. 10.1073/pnas.0810953105, 2604991, 19064930.
10. Zoldak G, Redecke L, Svergun DI, Konarev PV, Voertler CS, Dobbek H, Sedlak E, Sprinzl M. Release factors 2 from Escherichia coli and Thermus thermophilus: structural, spectroscopic and microcalorimetric studies. Nucleic Acids Res 2007, 35:1343-1353. 10.1093/nar/gkl696, 1849895, 17272297.
11. Wimberly BT, Brodersen DE, Clemons WM, Morgan-Warren RJ, Carter AP, Vonrhein C, Hartsch T, Ramakrishnan V. Structure of the 30S ribosomal subunit. Nature 2000, 407:327-339. 10.1038/35030006, 11014182.
12. Ogle JM, Brodersen DE, Clemons WM, Tarry MJ, Carter AP, Ramakrishnan V. Recognition of cognate transfer RNA by the 30S ribosomal subunit. Science 2001, 292:897-902. 10.1126/science.1060612, 11340196.
13. Temperley R, Richter R, Dennerlein S, Lightowlers RN, Chrzanowska-Lightowlers ZM. Hungry codons promote frameshifting in human mitochondrial ribosomes. Science 2010, 327:301. 10.1126/science.1180674, 20075246.
14. Lightowlers RN, Chrzanowska-Lightowlers ZM. Terminating human mitochondrial protein synthesis: a shift in our thinking. RNA Biol 2010, 7:282-286. 10.4161/rna.7.3.12023, 20458175.
15. Soleimanpour-Lichaei HR, Kuhl I, Gaisne M, Passos JF, Wydro M, Rorbach J, Temperley R, Bonnefoy N, Tate W, Lightowlers R, et al. mtRF1a is a human mitochondrial translation release factor decoding the major termination codons UAA and UAG. Mol Cell 2007, 27:745-757. 10.1016/j.molcel.2007.06.031, 1976341, 17803939.
16. Nozaki Y, Matsunaga N, Ishizawa T, Ueda T, Takeuchi N. HMRF1L is a human mitochondrial translation release factor involved in the decoding of the termination codons UAA and UAG. Genes Cells 2008, 13:429-438. 10.1111/j.1365-2443.2008.01181.x, 18429816.
17. Richter R, Rorbach J, Pajak A, Smith PM, Wessels HJ, Huynen MA, Smeitink JA, Lightowlers RN, Chrzanowska-Lightowlers ZM. A functional peptidyl-tRNA hydrolase, ICT1, has been recruited into the human mitochondrial ribosome. EMBO J 2010, 29:1116-1125. 10.1038/emboj.2010.14, 2845271, 20186120.
18. Antonicka H, Ostergaard E, Sasarman F, Weraarpachai W, Wibrand F, Pedersen AM, Rodenburg RJ, van der Knaap MS, Smeitink JA, Chrzanowska-Lightowlers ZM, et al. Mutations in C12orf65 in patients with encephalomyopathy and a mitochondrial translation defect. Am J Hum Genet 2010, 87:115-122. 10.1016/j.ajhg.2010.06.004, 2896764, 20598281.
19. Young DJ, Edgar CD, Murphy J, Fredebohm J, Poole ES, Tate WP. Bioinformatic, structural, and functional analyses support release factor-like MTRF1 as a protein able to decode nonstandard stop codons beginning with adenine in vertebrate mitochondria. RNA 2010, 16:1146-1155. 10.1261/rna.1970310, 2874167, 20421313.
20. Zhang Y, Spremulli LL. Identification and cloning of human mitochondrial translational release factor 1 and the ribosome recycling factor. Biochim Biophys Acta 1998, 1443:245-250. 10.1016/S0167-4781(98)00223-1, 9838146.
21. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997, 25:3389-3402. 10.1093/nar/25.17.3389, 146917, 9254694.
22. Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 1994, 22:4673-4680. 10.1093/nar/22.22.4673, 308517, 7984417.
23. Guindon S, Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 2003, 52:696-704. 10.1080/10635150390235520, 14530136.
24. Abascal F, Zardoya R, Posada D. ProtTest: selection of best-fit models of protein evolution. Bioinformatics 2005, 21:2104-2105. 10.1093/bioinformatics/bti263, 15647292.
25. Feenstra KA, Pirovano W, Krab K, Heringa J. Sequence harmony: detecting functional specificity from alignments. Nucleic Acids Res 2007, 35:W495-W498. 10.1093/nar/gkm406, 1933219, 17584793.
26. Krieger E, Koraimann G, Vriend G. Increasing the precision of comparative models with YASARA NOVA-a self-parameterizing force field. Proteins 2002, 47:393-402. 10.1002/prot.10104, 11948792.
27. Canutescu AA, Shelenkov AA, Dunbrack RL. A graph-theory algorithm for rapid protein side-chain prediction. Protein Sci 2003, 12:2001-2014. 10.1110/ps.03154503, 2323997, 12930999.
28. Krieger E, Joo K, Lee J, Raman S, Thompson J, Tyka M, Baker D, Karplus K. Improving physical realism, stereochemistry, and side-chain accuracy in homology modeling: Four approaches that performed well in CASP8. Proteins 2009, 77(Suppl 9):114-122. 2922016, 19768677.
29. Hooft RW, Vriend G, Sander C, Abola EE. Errors in protein structures. Nature 1996, 381:272.
30. Nakamura Y, Ito K. A tripeptide discriminator for stop codon recognition. FEBS Lett 2002, 514:30-33. 10.1016/S0014-5793(02)02330-X, 11904176.
31. Ito K, Uno M, Nakamura Y. A tripeptide 'anticodon' deciphers stop codons in messenger RNA. Nature 2000, 403:680-684. 10.1038/35001115, 10688208.
32. Wohlgemuth I, Pohl C, Rodnina MV. Optimization of speed and accuracy of decoding in translation. EMBO J 2010, 29:3701-3709. 10.1038/emboj.2010.229, 2982755, 20842102.
33. Jorgensen F, Adamski FM, Tate WP, Kurland CG. Release factor-dependent false stops are infrequent in Escherichia coli. J Mol Biol 1993, 230:41-50. 10.1006/jmbi.1993.1124, 8450549.
34. Freistroffer DV, Kwiatkowski M, Buckingham RH, Ehrenberg M. The accuracy of codon recognition by polypeptide release factors. Proc Natl Acad Sci U S A 2000, 97:2046-2051. 10.1073/pnas.030541097, 15751, 10681447.
35. Temperley RJ, Wydro M, Lightowlers RN, Chrzanowska-Lightowlers ZM. Human mitochondrial mRNAs-like members of all families, similar but different. Biochim Biophys Acta 2010, 1797:1081-1085. 10.1016/j.bbabio.2010.02.036, 3003153, 20211597.
36. Szczesny RJ, Borowski LS, Brzezniak LK, Dmochowska A, Gewartowski K, Bartnik E, Stepien PP. Human mitochondrial RNA turnover caught in flagranti: involvement of hSuv3p helicase in RNA surveillance. Nucleic Acids Res 2010, 38:279-298. 10.1093/nar/gkp903, 2800237, 19864255.
37. Hayes CS, Keiler KC. Beyond ribosome rescue: tmRNA and co-translational processes. FEBS Lett 2009, 584:413-419.
38. Handa Y, Inaho N, Nameki N. YaeJ is a novel ribosome-associated protein in Escherichia coli that can hydrolyze peptidyl-tRNA on stalled ribosomes. Nucleic Acids Res 2010, 39:1739-1748. 3061065, 21051357.