A SelB/EF-Tu/aIF2γ-like protein from Methanosarcina mazei in the GTP-bound form binds cysteinyl-tRNACys

Journal of Structural and Functional Genomics - Tập 16 - Trang 25-41 - 2015
Tatsuo Yanagisawa1,2, Ryohei Ishii1,3, Yasushi Hikida1,2,3, Ryuya Fukunaga1,3,4, Toru Sengoku1,2,3, Shun-ichi Sekine1,5,3, Shigeyuki Yokoyama1,2,3
1RIKEN Systems and Structural Biology Center, Yokohama, Japan
2RIKEN Structural Biology Laboratory, Yokohama, Japan
3Department of Biophysics and Biochemistry, Graduate School of Science, The University of Tokyo, Tokyo, Japan
4Department of Biochemistry, School of Medicine, Johns Hopkins University, Baltimore, USA
5RIKEN Center for Life Science Technologies, Yokohama, Japan

Tóm tắt

The putative translation elongation factor Mbar_A0971 from the methanogenic archaeon Methanosarcina barkeri was proposed to be the pyrrolysine-specific paralogue of EF-Tu (“EF-Pyl”). In the present study, the crystal structures of its homologue from Methanosarcina mazei (MM1309) were determined in the GMPPNP-bound, GDP-bound, and apo forms, by the single-wavelength anomalous dispersion phasing method. The three MM1309 structures are quite similar (r.m.s.d. < 0.1 Å). The three domains, corresponding to domains 1, 2, and 3 of EF-Tu/SelB/aIF2γ, are packed against one another to form a closed architecture. The MM1309 structures resemble those of bacterial/archaeal SelB, bacterial EF-Tu in the GTP-bound form, and archaeal initiation factor aIF2γ, in this order. The GMPPNP and GDP molecules are visible in their co-crystal structures. Isothermal titration calorimetry measurements of MM1309·GTP·Mg2+, MM1309·GDP·Mg2+, and MM1309·GMPPNP·Mg2+ provided dissociation constants of 0.43, 26.2, and 222.2 μM, respectively. Therefore, the affinities of MM1309 for GTP and GDP are similar to those of SelB rather than those of EF-Tu. Furthermore, the switch I and II regions of MM1309 are involved in domain–domain interactions, rather than nucleotide binding. The putative binding pocket for the aminoacyl moiety on MM1309 is too small to accommodate the pyrrolysyl moiety, based on a comparison of the present MM1309 structures with that of the EF-Tu·GMPPNP·aminoacyl-tRNA ternary complex. A hydrolysis protection assay revealed that MM1309 binds cysteinyl (Cys)-tRNACys and protects the aminoacyl bond from non-enzymatic hydrolysis. Therefore, we propose that MM1309 functions as either a guardian protein that protects the Cys moiety from oxidation or an alternative translation factor for Cys-tRNACys.

Tài liệu tham khảo

Kaziro Y, Itoh H, Kozasa T, Nakafuku M, Satoh T (1991) Structure and function of signal-transducing GTP-binding proteins. Annu Rev Biochem 60:349–400 Weijland A, Harmark K, Cool RH, Anborgh PH, Parmeggiani A (1992) Elongation factor Tu: a molecular switch in protein biosynthesis. Mol Microbiol 6:683–688 Sprinzl M (1994) Elongation factor Tu: a regulatory GTPase with an integrated effector. Trends Biochem Sci 19:245–250 Clark BF, Nyborg J (1997) The ternary complex of EF-Tu and its role in protein biosynthesis. Curr Opin Struct Biol 7:110–116 Rodnina MV, Wintermeyer W (2001) Fidelity of aminoacyl-tRNA selection on the ribosome: kinetic and structural mechanisms. Annu Rev Biochem 70:415–435 Nilsson J, Nissen P (2005) Elongation factors on the ribosome. Curr Opin Struct Biol 15:349–354 Asahara H, Uhlenbeck OC (2005) Predicting the binding affinities of misacylated tRNAs for Thermus thermophilus EF-Tu-GTP. Biochemistry 44:11254–11261 Rodnina MV, Fricke R, Wintermeyer W (1994) Transient conformational states of aminoacyl-tRNA during ribosome binding catalyzed by elongation factor Tu. Biochemistry 33:12267–12275 Ohta S, Nakanishi M, Tsuboi M, Arai K, Kaziro Y (1977) Structural fluctuation of the polypeptide-chain elongation factor Tu. A comparison of factors from Escherichia coli and Thermus thermophilus HB8. Eur J Biochem 78:599–608 Kjeldgaard M, Nissen P, Thirup S, Nyborg J (1993) The crystal structure of elongation factor EF-Tu from Thermus aquaticus in the GTP conformation. Structure 1:35–50 Berchtold H, Reshetnikova L, Reiser CO, Schirmer NK, Sprinzl M, Hilgenfeld R (1993) Crystal structure of active elongation factor Tu reveals major domain rearrangements. Nature 365:126–132 Yatime L, Mechulam Y, Blanquet S, Schmitt E (2006) Structural switch of the gamma subunit in an archaeal aIF2 alpha gamma heterodimer. Structure 14:119–128 Schmitt E, Panvert M, Lazennec-Schurdevin C, Coureux PD, Perez J, Thompson A, Mechulam Y (2012) Structure of the ternary initiation complex aIF2-GDPNP-methionylated initiator tRNA. Nat Struct Mol Biol 19:450–454 Stolboushkina E, Nikonov S, Zelinskaya N, Arkhipova V, Nikulin A, Garber M, Nikonov O (2013) Crystal structure of the archaeal translation initiation factor 2 in complex with a GTP analogue and Met-tRNAf(Met). J Mol Biol 425:989–998 Commans S, Böck A (1999) Selenocysteine inserting tRNAs: an overview. FEMS Microbiol Rev 23:335–351 Thanbichler M, Böck A (2001) Functional analysis of prokaryotic SELB proteins. BioFactors 14:53–59 Leibundgut M, Flick C, Thanbichler M, Böck A, Ban N (2005) Selenocysteine tRNA-specific elongation factor SelB is a structural chimaera of elongation and initiation factors. EMBO J 24:11–22 Berry MJ, Banu L, Harney JW, Larsen PR (1993) Functional characterization of the eukaryotic SECIS elements which direct selenocysteine insertion at UGA codons. EMBO J 12:3315–3322 Suppmann S, Persson BC, Böck A (1999) Dynamics and efficiency in vivo of UGA-directed selenocysteine insertion at the ribosome. EMBO J 18:2284–2293 Copeland PR, Driscoll DM (1999) Purification, redox sensitivity, and RNA binding properties of SECIS-binding protein 2, a protein involved in selenoprotein biosynthesis. J Biol Chem 274:25447–25454 Copeland PR, Fletcher JE, Carlson BA, Hatfield DL, Driscoll DM (2000) A novel RNA binding protein, SBP2, is required for the translation of mammalian selenoprotein mRNAs. EMBO J 19:306–314 Srinivasan G, James CM, Krzycki JA (2002) Pyrrolysine encoded by UAG in Archaea: charging of a UAG-decoding specialized tRNA. Science 296:1459–1462 Hao B, Gong W, Ferguson TK, James CM, Krzycki JA, Chan MK (2002) A new UAG-encoded residue in the structure of a methanogen methyltransferase. Science 296:1462–1466 Krzycki JA (2005) The direct genetic encoding of pyrrolysine. Curr Opin Microbiol 8:706–712 Blight SK, Larue RC, Mahapatra A, Longstaff DG, Chang E, Zhao G, Kang PT, Green-Church KB, Chan MK, Krzycki JA (2004) Direct charging of tRNA(CUA) with pyrrolysine in vitro and in vivo. Nature 431:333–335 Polycarpo C, Ambrogelly A, Berube A, Winbush SM, McCloskey JA, Crain PF, Wood JL, Söll D (2004) An aminoacyl-tRNA synthetase that specifically activates pyrrolysine. Proc Nat Acad Sci USA 101:12450–12454 Namy O, Rousset JP, Napthine S, Brierley I (2004) Reprogrammed genetic decoding in cellular gene expression. Mol Cell 13:157–168 Ibba M, Söll D (2004) Aminoacyl-tRNAs: setting the limits of the genetic code. Genes Dev 18:731–738 Zhang Y, Baranov PV, Atkins JF, Gladyshev VN (2005) Pyrrolysine and selenocysteine use dissimilar decoding strategies. J Biol Chem 280:20740–20751 Longstaff DG, Blight SK, Zhang L, Green-Church KB, Krzycki JA (2007) In vivo contextual requirements for UAG translation as pyrrolysine. Mol Microbiol 63:229–241 Nissen P, Kjeldgaard M, Thirup S, Polekhina G, Reshetnikova L, Clark BF, Nyborg J (1995) Crystal structure of the ternary complex of Phe-tRNAPhe, EF-Tu, and a GTP analog. Science 270:1464–1472 Abel K, Yoder MD, Hilgenfeld R, Jurnak F (1996) An alpha to beta conformational switch in EF-Tu. Structure 4:1153–1159 Nissen P, Kjeldgaard M, Thirup S, Nyborg J (1999) The crystal structure of Cys-tRNACys-EF-Tu-GDPNP reveals general and specific features in the ternary complex and in tRNA. Structure 7:143–156 Morikawa K, la Cour TF, Nyborg J, Rasmussen KM, Miller DL, Clark BF (1978) High resolution X-ray crystallographic analysis of a modified form of the elongation factor Tu: guanosine diphosphate complex. J Mol Biol 125:325–338 Polekhina G, Thirup S, Kjeldgaard M, Nissen P, Lippmann C, Nyborg J (1996) Helix unwinding in the effector region of elongation factor EF-Tu-GDP. Structure 4:1141–1151 Song H, Parsons MR, Rowsell S, Leonard G, Phillips SE (1999) Crystal structure of intact elongation factor EF-Tu from Escherichia coli in GDP conformation at 2.05-Å resolution. J Mol Biol 285:1245–1256 Schmitt E, Blanquet S, Mechulam Y (2002) The large subunit of initiation factor aIF2 is a close structural homologue of elongation factors. EMBO J 21:1821–1832 Roll-Mecak A, Alone P, Cao C, Dever TE, Burley SK (2004) X-ray structure of translation initiation factor eIF2gamma: implications for tRNA and eIF2alpha binding. J Biol Chem 279:10634–10642 Sokabe M, Yao M, Sakai N, Toya S, Tanaka I (2006) Structure of archaeal translational initiation factor 2 betagamma-GDP reveals significant conformational change of the beta-subunit and switch 1 region. Proc Natl Acad Sci USA 103:13016–13021 Yatime L, Mechulam Y, Blanquet S, Schmitt E (2007) Structure of an archaeal heterotrimeric initiation factor 2 reveals a nucleotide state between the GTP and the GDP states. Proc Natl Acad Sci USA 104:18445–18450 Nikonov O, Stolboushkina E, Nikulin A, Hasenöhrl D, Bläsi U, Manstein DJ, Fedorov R, Garber M, Nikonov S (2007) New insights into the interactions of the translation initiation factor 2 from archaea with guanine nucleotides and initiator tRNA. J Mol Biol 373:328–336 Milburn MV, Tong L, deVos AM, Brünger A, Yamaizumi Z, Nishimura S, Kim SH (1990) Molecular switch for signal transduction: structural differences between active and inactive forms of protooncogenic ras proteins. Science 247:939–945 Sprang SR (1997) G protein mechanisms: insights from structural analysis. Annu Rev Biochem 66:639–678 Deppenmeier U, Johann A, Hartsch T, Merkl R, Schmitz RA, Martinez-Arias R, Henne A, Wiezer A, Baeumer S, Jacobi C, Brueggemann H, Lienard T, Christmann A, Boemecke M, Steckel S, Bhattacharyya A, Lykidis A, Overbeek R, Gottschalk G (2002) The genome of Methanosarcina mazei: evidence for lateral gene transfer between bacteria and archaea. J Mol Microbiol Biotechnol 4:453–461 Atkinson GC, Hauryliuk V, Tenson T (2011) An ancient family of SelB elongation factor-like proteins with a broad but disjunct distribution across archaea. BMC Evol Biol 11:22 Collaborative Computational Project (1994) Number 4. Acta Crystallogr. D50:760–763 Davis IW, Murray LW, Richardson JS, Richardson DC (2004) MOLPROBITY: structure validation and all-atom contact analysis for nucleic acids and their complexes. Nucleic Acids Res 32:W615–W619 Holm L, Kaariainen S, Rosenstrom P, Schenkel A (2008) Searching protein structure databases with DaliLite v. 3. Bioinformatics 24:2780–2781 Kobayashi K, Kikuno I, Kuroha K, Saito K, Ito K, Ishitani R, Inada T, Nureki O (2010) Structural basis for mRNA surveillance by archaeal Pelota and GTP-bound EF1α complex. Proc Natl Acad Sci USA 107:17575–17579 Kobayashi K, Saito K, Ishitani R, Ito K, Nureki O (2012) Structural basis for translation termination by archaeal RF1 and GTP-bound EF1α complex. Nucleic Acids Res 40:9319–9328 Grøftehauge MK, Therkelsen MØ, Taaning R, Skrydstrup T, Morth JP, Nissen P (2013) Identifying ligand-binding hot spots in proteins using brominated fragments. Acta Crystallogr F69:1060–1065 Parmeggiani A, Krab IM, Watanabe T, Nielsen RC, Dahlberg C, Nyborg J, Nissen P (2006) Enacyloxin IIa pinpoints a binding pocket of elongation factor Tu for development of novel antibiotics. J Biol Chem 281:2893–2900 Holbrook SR, Kim SH (1989) Molecular model of the G protein alpha subunit based on the crystal structure of the HRAS protein. Proc Natl Acad Sci USA 86:1751–1755 Saraste M, Sibbald PR, Wittinghofer A (1990) The P-loop-a common motif in ATP- and GTP-binding proteins. Trends Biochem Sci 15:430–434 Leipe DD, Wolf YI, Koonin EV, Aravind L (2002) Classification and evolution of P-loop GTPases and related ATPases. J Mol Biol 317:41–72 Daviter T, Wieden HJ, Rodnina MV (2003) Essential role of histidine 84 in elongation factor Tu for the chemical step of GTP hydrolysis on the ribosome. J Mol Biol 332:689–699 Laalami S, Grentzmann G, Bremaud L, Cenatiempo Y (1996) Messenger RNA translation in prokaryotes: GTPase centers associated with translational factors. Biochimie 78:577–589 Mansilla F, Knudsen CR, Laurberg M, Clark BF (1997) Mutational analysis of Escherichia coli elongation factor Tu in search of a role for the N-terminal region. Protein Eng 10:927–934 Thanbichler M, Böck A, Goody RS (2000) Kinetics of the interaction of translation factor SelB from Escherichia coli with guanosine nucleotides and selenocysteine insertion sequence RNA. J Biol Chem 275:20458–20466 Arai N, Kaziro Y (1975) Mechanism of the ribosome-dependent uncoupled GTPase reaction catalyzed by polypeptide chain elongation factor G. J Biochem 77:439–447 Agrawal RK, Penczek P, Grassucci RA, Frank J (1998) Visualization of elongation factor G on the Escherichia coli 70S ribosome: the mechanism of translocation. Proc Natl Acad Sci USA 95:6134–6138 Agrawal RK, Heagle AB, Penczek P, Grassucci RA, Frank J (1999) EF-G-dependent GTP hydrolysis induces translocation accompanied by large conformational changes in the 70S ribosome. Nat Struct Biol 6:643–647 Stark H, Rodnina MV, Wieden HJ, van Heel M, Wintermeyer W (2000) Large-scale movement of elongation factor G and extensive conformational change of the ribosome during translocation. Cell 100:301–309 Valle M, Zavialov A, Sengupta J, Rawat U, Ehrenberg M, Frank J (2003) Locking and unlocking of ribosomal motions. Cell 114:123–134 Hansson S, Singh R, Gudkov AT, Liljas A, Logan DT (2005) Crystal structure of a mutant elongation factor G trapped with a GTP analogue. FEBS Lett 579:4492–4497 Wilden B, Savelsbergh A, Rodnina MV, Wintermeyer W (2006) Role and timing of GTP binding and hydrolysis during EF-G-dependent tRNA translocation on the ribosome. Proc Natl Acad Sci USA 103:13670–13675 Connell SR, Takemoto C, Wilson DN, Wang H, Murayama K, Terada T, Shirouzu M, Rost M, Schüler M, Giesebrecht J, Dabrowski M, Mielke T, Fucini P, Yokoyama S, Spahn CM (2007) Structural basis for interaction of the ribosome with the switch regions of GTP-bound elongation factors. Mol Cell 25:751–764 Hauryliuk V, Hansson S, Ehrenberg M (2008) Cofactor dependent conformational switching of GTPases. Biophys J 95:1704–1715 Noble CG, Song H (2008) Structural studies of elongation and release factors. Cell Mol Life Sci 65:1335–1346 Frolova L, Le Goff X, Zhouravleva G, Davydova E, Philippe M, Kisselev L (1996) Eukaryotic polypeptide chain release factor eRF3 is an eRF1- and ribosome-dependent guanosine triphosphatase. RNA 2:334–341 Kong C, Ito K, Walsh MA, Wada M, Liu Y, Kumar S, Barford D, Nakamura Y, Song H (2004) Crystal structure and functional analysis of the eukaryotic class II release factor eRF3 from S. pombe. Mol Cell 14:233–245 Hauryliuk V, Zavialov A, Kisselev L, Ehrenberg M (2006) Class-1 release factor eRF1 promotes GTP binding by class-2 release factor eRF3. Biochimie 88:747–757 des Georges A, Hashem Y, Unbehaun A, Grassucci RA, Taylor D, Hellen CU, Pestova TV, Frank J (2014) Structure of the mammalian ribosomal pre-termination complex associated with eRF1-eRF3-GDPNP. Nucleic Acids Res 42:3409–3418 Zavialov AV, Buckingham RH, Ehrenberg M (2001) A posttermination ribosomal complex is the guanine nucleotide exchange factor for peptide release factor RF3. Cell 107:115–124 Gao H, Zhou Z, Rawat U, Huang C, Bouakaz L, Wang C, Cheng Z, Liu Y, Zavialov A, Gursky R, Sanyal S, Ehrenberg M, Frank J, Song H (2007) RF3 induces ribosomal conformational changes responsible for dissociation of class I release factors. Cell 129:929–941 Zhou J, Lancaster L, Trakhanov S, Noller HF (2012) Crystal structure of release factor RF3 trapped in the GTP state on a rotated conformation of the ribosome. RNA 18:230–240 Roll-Mecak A, Cao C, Dever TE, Burley SK (2000) X-ray structures of the universal translation initiation factor IF2/eIF5B: conformational changes on GDP and GTP binding. Cell 103:781–792 Roll-Mecak A, Alone P, Cao C, Dever TE, Burley SK (2003) X-ray structure of translation initiation factor eIF2 gamma: implications for tRNA and eIF2alpha binding. J Biol Chem 279:10634–10642 Kuhle B, Ficner R (2014) eIF5B employs a novel domain release mechanism to catalyze ribosomal subunit joining. EMBO J 33:1177–1191 Paleskava A, Konevega AL, Rodnina MV (2012) Thermodynamics of the GTP-GDP-operated conformational switch of selenocysteine-specific translation factor SelB. J Biol Chem 287:27906–27912 Hauenstein SI, Perona JJ (2008) Redundant synthesis of cysteinyl-tRNACys in Methanosarcina mazei. J Biol Chem 283:22007–22017 Pingoud A, Urbanke C, Krauss G, Peters F, Maass G (1977) Ternary complex formation between elongation factor Tu, GTP and aminoacyl-tRNA: an equilibrium study. Eur J Biochem 78:403–409 Otwinowski Z, Minor W (1997) Processing of X-ray Diffraction Data Collected in Oscillation Mode. Methods Enzymol 276:307–326 Weeks CM, Miller R (1999) Optimizing Shake-and-Bake for proteins. Acta Crystallogr. D55:492–500 Terwilliger TC (2003) SOLVE and RESOLVE: automated structure solution and density modification. Methods Enzymol 374:22–37 Cohen SX, Ben Jelloul M, Long F, Vagin A, Knipscheer P, Lebbink J, Sixma TK, Lamzin VS, Murshudov GN, Perrakis A (2008) ARP/wARP and molecular replacement: the next generation. Acta Crystallogr D64:49–60 Jones TA, Zou JY, Cowan SW, Kjeldgaard M (1991) Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr A47:110–119 Emsley P, Cowtan K (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D60:2126–2132 Brünger AT, Adams PD, Clore GM, DeLano WL, Gros P, Grosse-Kunstleve RW, Jiang JS, Kuszewski J, Nilges M, Pannu NS, Read RJ, Rice LM, Simonson T, Warren GL (1998) Simulated-annealing real-space refinement as a tool in model building. Acta Crystallogr D54:905–921 Murshudov GN, Skubák P, Lebedev AA, Pannu NS, Steiner RA, Nicholls RA, Winn MD, Long F, Vagin AA (2011) REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallogr D67:355–367 Adams PD, Afonine PV, Bunkóczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung L-W, Kapral GJ, Grosse-Kunstleve RW, McCoy AJ, Moriarty NW, Oeffner R, Read RJ, Richardson DC, Richardson JS, Terwilliger TC, Zwart PH (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D66:213–221 Krissinel E, Henrick K (2004) Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr D60:2256–2268 Yanagisawa T, Ishii R, Fukunaga R, Kobayashi T, Sakamoto K, Yokoyama S (2008) Crystallographic studies on multiple conformational states of active-site loops in pyrrolysyl-tRNA synthetase. J Mol Biol 378:634–652 Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680 Gouet P, Courcelle E, Stuart DI, Metoz F (1999) ESPript: analysis of multiple sequence alignments in PostScript. Bioinformatics 15:305–308