Archaeal aminoacyl-tRNA synthetases interact with the ribosome to recycle tRNAs

Nucleic Acids Research

Volumn 42, Issue 8, 2014, Pages 5191-5201

  Godinic Mikulcic, Vlatka ^a   Jaric, Jelena ^a   Greber, Basil J ^b   Franke, Vedran ^a   Hodnik, Vesna ^c   Anderluh, Gregor ^c,d   Ban, Nenad ^b   Weygand Durasevic, Ivana ^a  

^a UNIVERSITY OF ZAGREB   (Croatia)

^b ETH ZURICH   (Switzerland)

^c UNIVERSITY OF LJUBLJANA   (Slovenia)

^d NATIONAL INSTITUTE OF CHEMISTRY   (Slovenia)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID TRANSFER RNA LIGASE; ARGININE; CYANAMIDE; RIBOSOME PROTEIN; SERINE;

ARTICLE; BACTERIAL GENOME; BINDING AFFINITY; BINDING SITE; BIOINFORMATICS; CODON; CONTROLLED STUDY; ENZYME ANALYSIS; METHANOTHERMOBACTER THERMAUTOTROPHICUS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN CROSS LINKING; PROTEIN DETERMINATION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RNA SEQUENCE; SURFACE PLASMON RESONANCE;

AMINO ACYL-TRNA SYNTHETASES; ARCHAEA; ARGININE-TRNA LIGASE; GENOME, ARCHAEAL; METHANOBACTERIACEAE; PROTEIN BIOSYNTHESIS; RIBOSOMAL PROTEINS; RIBOSOMES; RNA, TRANSFER; SERINE-TRNA LIGASE;

EID: 84899817129     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku164     Document Type: Article

References (51)

1. Ling, J., Reynolds, N. and Ibba, M. (2009) Aminoacyl-tRNA synthesis and translational quality control. Annu. Rev. Microbiol., 63, 61-78.
2. Schmeing, T.M. and Ramakrishnan, V. (2009) What recent ribosome structures have revealed about the mechanism of translation. Nature, 461, 1234-1242.
3. Klinge, S., Voigts-Hoffmann, F., Leibundgut, M. and Ban, N. (2012) Atomic structures of the eukaryotic ribosome. Trends Biochem. Sci., 37, 189-198.
4. Melnikov, S., Ben-Shem, A., Garreau de Loubresse, N., Jenner, L., Yusupova, G. and Yusupov, M. (2012) One core, two shells: bacterial and eukaryotic ribosomes. Nat. Struct. Mol. Biol., 19, 560-567.
5. Wilson, D.N. and Doudna Cate, J.H. (2012) The structure and function of the eukaryotic ribosome. Cold Spring Harb. Perspect. Biol., 4, a011536.
6. Negrutskii, B.S. and Deutscher, M.P. (1991) Channeling of aminoacyl-tRNA for protein synthesis in vivo. Proc. Natl Acad. Sci. USA, 88, 4991-4995.
7. Kaminska, M., Havrylenko, S., Decottignies, P., Le Marechal, P., Negrutskii, B. and Mirande, M. (2009) Dynamic organization of aminoacyl-tRNA synthetase complexes in the cytoplasm of human cells. J. Biol. Chem., 284, 13746-13754.
8. Mirande, M. (2010) Processivity of translation in the eukaryote cell: role of aminoacyl-tRNA synthetases. FEBS Lett., 584, 443-447.
9. David, A., Netzer, N., Strader, M.B., Das, S.R., Chen, C.Y., Gibbs, J., Pierre, P., Bennink, J.R. and Yewdell, J.W. (2011) RNA binding targets aminoacyl-tRNA synthetases to translating ribosomes. J. Biol. Chem., 286, 20688-20700.
10. Cannarozzi, G., Schraudolph, N.N., Faty, M., von Rohr, P., Friberg, M.T., Roth, A.C., Gonnet, P., Gonnet, G. and Barral, Y. (2010) A role for codon order in translation dynamics. Cell, 141, 355-367.
11. Shao, Z.Q., Zhang, Y.M., Feng, X.Y., Wang, B. and Chen, J.Q. (2012) Synonymous codon ordering: a subtle but prevalent strategy of bacteria to improve translational efficiency. PLoS One, 7, e33547.
12. Novoa, E.M. and Ribas de Pouplana, L. (2012) Speeding with control: codon usage, tRNAs, and ribosomes. Trends Genet., 28, 574-581.
13. Harris, C.L. (1987) An aminoacyl-tRNA synthetase complex in Escherichia coli. J. Bacteriol., 169, 2718-2723.
14. Kuhner, S., van Noort, V., Betts, M.J., Leo-Macias, A., Batisse, C., Rode, M., Yamada, T., Maier, T., Bader, S., Beltran-Alvarez, P. et al. (2009) Proteome organization in a genome-reduced bacterium. Science, 326, 1235-1240.
15. Goldgur, Y. and Safro, M. (1994) Aminoacyl-tRNA synthetases from Haloarcula marismortui: an evidence for a multienzyme complex in a procaryotic system. Biochem. Mol. Biol. Int., 32, 1075-1083.
16. Hausmann, C.D., Praetorius-Ibba, M. and Ibba, M. (2007) An aminoacyl-tRNA synthetase:elongation factor complex for substrate channeling in archaeal translation. Nucleic Acids Res., 35, 6094-6102.
17. Quevillon, S., Agou, F., Robinson, J.C. and Mirande, M. (1997) The p43 component of the mammalian multi-synthetase complex is likely to be the precursor of the endothelial monocyte-activating polypeptide II cytokine. J. Biol. Chem., 272, 32573-32579.
18. Kyriacou, S.V. and Deutscher, M.P. (2008) An important role for the multienzyme aminoacyl-tRNA synthetase complex in mammalian translation and cell growth. Mol. Cell, 29, 419-427.
19. Havrylenko, S., Legouis, R., Negrutskii, B. and Mirande, M. (2011) Caenorhabditis elegans evolves a new architecture for the multi-aminoacyl-tRNA synthetase complex. J. Biol. Chem., 286, 28476-28487.
20. Hausmann, C.D. and Ibba, M. (2008) Aminoacyl-tRNA synthetase complexes: molecular multitasking revealed. FEMS Microbiol. Rev., 32, 705-721.
21. Raina, M., Elgamal, S., Santangelo, T.J. and Ibba, M. (2012) Association of a multi-synthetase complex with translating ribosomes in the archaeon Thermococcus kodakarensis. FEBS Lett., 586, 2232-2238.
22. Praetorius-Ibba, M., Rogers, T.E., Samson, R., Kelman, Z. and Ibba, M. (2005) Association between Archaeal prolyl-and leucyl-tRNA synthetases enhances tRNA(Pro) aminoacylation. J. Biol. Chem., 280, 26099-26104.
23. Praetorius-Ibba, M., Hausmann, C.D., Paras, M., Rogers, T.E. and Ibba, M. (2007) Functional association between three archaeal aminoacyl-tRNA synthetases. J. Biol. Chem., 282, 3680-3687.
24. Hausmann, C.D. and Ibba, M. (2008) Structural and functional mapping of the archaeal multi-aminoacyl-tRNA synthetase complex. FEBS Lett., 582, 2178-2182.
25. Bec, G., Kerjan, P. and Waller, J.P. (1994) Reconstitution in vitro of the valyl-tRNA synthetase-elongation factor (EF) 1 beta gamma delta complex. Essential roles of the NH2-terminal extension of valyl-tRNA synthetase and of the EF-1 delta subunit in complex formation. J. Biol. Chem., 269, 2086-2092.
26. Bilokapic, S., Maier, T., Ahel, D., Gruic-Sovulj, I., Soll, D., Weygand-Durasevic, I. and Ban, N. (2006) Structure of the unusual seryl-tRNA synthetase reveals a distinct zinc-dependent mode of substrate recognition. EMBO J., 25, 2498-2509.
27. Bilokapic, S., Ivic, N., Godinic-Mikulcic, V., Piantanida, I., Ban, N. and Weygand-Durasevic, I. (2009) Idiosyncratic helix-turn-helix motif in Methanosarcina barkeri seryl-tRNA synthetase has a critical architectural role. J. Biol. Chem., 284, 10706-10713.
28. Godinic-Mikulcic, V., Jaric, J., Hausmann, C.D., Ibba, M. and Weygand-Durasevic, I. (2011) An archaeal tRNA-synthetase complex that enhances aminoacylation under extreme conditions. J. Biol. Chem., 286, 3396-3404.
29. Keller, A., Nesvizhskii, A.I., Kolker, E. and Aebersold, R. (2002) Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal. Chem., 74, 5383-5392.
30. Kohler, R., Boehringer, D., Greber, B., Bingel-Erlenmeyer, R., Collinson, I., Schaffitzel, C. and Ban, N. (2009) YidC and Oxa1 form dimeric insertion pores on the translating ribosome. Mol. Cell, 34, 344-353.
31. Wienken, C.J., Baaske, P., Rothbauer, U., Braun, D. and Duhr, S. (2010) Protein-binding assays in biological liquids using microscale thermophoresis. Nat. Commun., 1, 100.
32. Jerabek-Willemsen, M., Wienken, C.J., Braun, D., Baaske, P. and Duhr, S. (2011) Molecular interaction studies using microscale thermophoresis. Assay Drug Dev. Technol., 9, 342-353.
33. Francklyn, C.S., First, E.A., Perona, J.J. and Hou, Y.M. (2008) Methods for kinetic and thermodynamic analysis of aminoacyl-tRNA synthetases. Methods, 44, 100-118.
34. Targanski, I. and Cherkasova, V. (2008) Analysis of genomic tRNA sets from Bacteria, Archaea, and Eukarya points to anticodon-codon hydrogen bonds as a major determinant of tRNA compositional variations. RNA, 14, 1095-1109.
35. Diaconu, M., Kothe, U., Schlunzen, F., Fischer, N., Harms, J.M., Tonevitsky, A.G., Stark, H., Rodnina, M.V. and Wahl, M.C. (2005) Structural basis for the function of the ribosomal L7/12 stalk in factor binding and GTPase activation. Cell, 121, 991-1004.
36. Ballesta, J.P. and Remacha, M. (1996) The large ribosomal subunit stalk as a regulatory element of the eukaryotic translational machinery. Prog. Nucleic Acid Res. Mol. Biol., 55, 157-193.
37. Grela, P., Bernado, P., Svergun, D., Kwiatowski, J., Abramczyk, D., Grankowski, N. and Tchorzewski, M. (2008) Structural relationships among the ribosomal stalk proteins from the three domains of life. J. Mol. Evol., 67, 154-167.
38. Shimizu, T., Nakagaki, M., Nishi, Y., Kobayashi, Y., Hachimori, A. and Uchiumi, T. (2002) Interaction among silkworm ribosomal proteins P1, P2 and P0 required for functional protein binding to the GTPase-associated domain of 28S rRNA. Nucleic Acids Res., 30, 2620-2627.
39. Greber, B.J., Boehringer, D., Godinic-Mikulcic, V., Crnkovic, A., Ibba, M., Weygand-Durasevic, I. and Ban, N. (2012) Cryo-EM structure of the archaeal 50S ribosomal subunit in complex with initiation factor 6 and implications for ribosome evolution. J. Mol. Biol., 418, 145-160.
40. Blaha, G., Gurel, G., Schroeder, S.J., Moore, P.B. and Steitz, T.A. (2008) Mutations outside the anisomycin-binding site can make ribosomes drug-resistant. J. Mol. Biol., 379, 505-519.
41. Naganuma, T., Nomura, N., Yao, M., Mochizuki, M., Uchiumi, T. and Tanaka, I. (2010) Structural basis for translation factor recruitment to the eukaryotic/archaeal ribosomes. J. Biol. Chem., 285, 4747-4756.
42. Stapulionis, R. and Deutscher, M.P. (1995) A channeled tRNA cycle during mammalian protein synthesis. Proc. Natl Acad. Sci. USA, 92, 7158-7161.
43. Petrushenko, Z.M., Budkevich, T.V., Shalak, V.F., Negrutskii, B.S. and El'skaya, A.V. (2002) Novel complexes of mammalian translation elongation factor eEF1A.GDP with uncharged tRNA and aminoacyl-tRNA synthetase. Implications for tRNA channeling. Eur. J. Biochem., 269, 4811-4818.
44. Brandt, F., Etchells, S.A., Ortiz, J.O., Elcock, A.H., Hartl, F.U. and Baumeister, W. (2009) The native 3D organization of bacterial polysomes. Cell, 136, 261-271.
45. Brandt, F., Carlson, L.A., Hartl, F.U., Baumeister, W. and Grunewald, K. (2010) The three-dimensional organization of polyribosomes in intact human cells. Mol. Cell, 39, 560-569.
46. Yokobori, S., Kitamura, A., Grosjean, H. and Bessho, Y. (2013) Life without tRNAArg-adenosine deaminase TadA: evolutionary consequences of decoding the four CGN codons as arginine in Mycoplasmas and other Mollicutes. Nucleic Acids Res., 41, 6531-6543.
47. Teichmann, T., Urban, C. and Beier, H. (1994) The tRNA(Ser)-isoacceptors and their genes in Nicotiana rustica: genome organization, expression in vitro and sequence analyses. Plant Mol. Biol., 24, 889-901.
48. Sakamoto, K., Ishimaru, S., Kobayashi, T., Walker, J.R. and Yokoyama, S. (2004) The Escherichia coli argU10(Ts) phenotype is caused by a reduction in the cellular level of the argU tRNA for the rare codons AGA and AGG. J. Bacteriol., 186, 5899-5905.
49. Sprinzl, M. and Vassilenko, K.S. (2005) Compilation of tRNA sequences and sequences of tRNA genes. Nucleic Acids Res., 33, D139-D140.
50. Yamada, Y., Matsugi, J. and Ishikura, H. (2003) tRNA1Ser(G34) with the anticodon GGA can recognize not only UCC and UCU codons but also UCA and UCG codons. Biochim. Biophys. Acta, 1626, 75-82.
51. Gustilo, E.M., Vendeix, F.A. and Agris, P.F. (2008) tRNA's modifications bring order to gene expression. Curr. Opin. Microbiol., 11, 134-140.