Selenocysteine tRNA-specific elongation factor SelB is a structural chimaera of elongation and initiation factors

EMBO Journal

Volumn 24, Issue 1, 2005, Pages 11-22

  Leibundgut, Marc ^a   Frick, Christian ^a   Thanbichler, Martin ^b   Böck, August ^b   Ban, Nenad ^a  

^a ETH ZURICH   (Switzerland)

^b UNIVERSITY OF MUNICH   (Germany)

Author keywords

Initiation; Protein synthesis; Pyrrolysine; SECIS; Selenocysteine

Indexed keywords

AMINO ACID; APOPROTEIN; ELONGATION FACTOR; ELONGATION FACTOR SELB; GUANOSINE DIPHOSPHATE; GUANOSINE TRIPHOSPHATASE; GUANOSINE TRIPHOSPHATE DERIVATIVE; INITIATION FACTOR; INITIATION FACTOR 2; INITIATION FACTOR 5B; LYSINE DERIVATIVE; MESSENGER RNA; PHOSPHATE; PYRROLYSINE; SELENOCYSTEINE; TRANSFER RNA; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ARTICLE; BINDING SITE; CHIMERA; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; METHANOCOCCUS MARIPALUDIS; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN RNA BINDING; PROTEIN SYNTHESIS; RIBOSOME; RNA STRUCTURE; RNA TRANSLATION; SELENOCYSTEINE INSERTING SEQUENCE; STOP CODON; X RAY ANALYSIS;

AMINO ACID SEQUENCE; ARCHAEAL PROTEINS; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; DNA MUTATIONAL ANALYSIS; EUKARYOTIC INITIATION FACTORS; GUANOSINE DIPHOSPHATE; GUANOSINE TRIPHOSPHATE; METHANOCOCCUS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; PEPTIDE ELONGATION FACTORS; PROKARYOTIC INITIATION FACTORS; PROTEIN BINDING; PROTEIN CONFORMATION; RNA, TRANSFER; SEQUENCE ALIGNMENT;

EID: 13244277554     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.emboj.7600505     Document Type: Article

References (56)

1. Abel K, Yoder MD, Hilgenfeld R, Jurnak F (1996) An α to β conformational switch in EF-Tu. Structure 4: 1153-1159
2. Ævarsson A, Brazhnikov E, Garber M, Zheltonosova J, Chirgadze Y, al-Karadaghi S, Svensson LA, Liljas A (1994) Three-dimensional structure of the ribosomal translocase: elongation factor G from Thermus thermophilus. EMBO J 13: 3669-3677
3. Allmang C, Carbon P, Krol A (2002) The SBP2 and 15.5 kD/Snu13p proteins share the same RNA binding domain: identification of SBP2 amino acids important to SECIS RNA binding. RNA 8: 1308-1318
4. Andersen GR, Pedersen L, Valente L, Chatterjee I, Kinzy TG, Kjeldgaard M, Nyborg J (2000) Structural basis for nucleotide exchange and competition with tRNA in the yeast elongation factor complex eEF1A:eEF1Bα. Mol Cell 6: 1261-1266
5. Atkins JF, Gesteland RF (2000) The twenty-first amino acid. Nature 407, 463, 465
6. Sec of Escherichia coli is the determinant for binding to elongation factors SELB or Tu. J Biol Chem 266: 20375-20379
7. Baron C, Böck A (1995) The selenocysteine-inserting tRNA species: structure and function. In tRNA: Structure, Biosynthesis, and Function, Söll D, RajBhandary UL (eds) pp 529-544. Washington, DC: ASM Press
8. Baron C, Sturchler C, Wu XQ, Gross HJ, Krol A, Böck A (1994) Eukaryotic selenocysteine inserting tRNA species support selenoprotein synthesis in Escherichia coli. Nucleic Acids Res 22: 2228-2233
9. Ser. J Mol Biol 231: 274-292
10. 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
11. Berry MJ, Banu L, Chen YY, Mandel SJ, Kieffer JD, Harney JW, Larsen PR (1991) Recognition of UGA as a selenocysteine codon in type I deiodinase requires sequences in the 3′ untranslated region. Nature 353: 273-276
12. 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) Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr D 54: 905-921
13. Commans S, Böck A (1999) Selenocysteine inserting tRNAs: an overview. FEMS Microbiol Rev 23: 335-351
14. 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
15. Czworkowski J, Wang J, Steitz TA, Moore PB (1994) The crystal structure of elongation factor G complexed with GDP, at 2.7 Å resolution. EMBO J 13: 3661-3668
16. Dell VA, Miller DL, Johnson AE (1990) Effects of nucleotide- and aurodox-induced changes in elongation factor Tu conformation upon its interactions with aminoacyl transfer RNA. A fluorescence study. Biochemistry 29: 1757-1763
17. Fagegaltier D, Hubert N, Yamada K, Mizutani T, Carbon P, Krol A (2000) Characterization of mSelB, a novel mammalian elongation factor for selenoprotein translation. EMBO J 19: 4796-4805
18. Forchhammer K, Leinfelder W, Böck A (1989) Identification of a novel translation factor necessary for the incorporation of selenocysteine into protein. Nature 342: 453-456
19. Förster C, Ott G, Forchhammer K, Sprinzl M (1990) Interaction of a selenocysteine-incorporating tRNA with elongation factor Tu from E. coli. Nucleic Acids Res 18: 487-491
20. Fourmy D, Guittet E, Yoshizawa S (2002) Structure of prokaryotic SECIS mRNA hairpin and its interaction with elongation factor SelB. J Mol Biol 324: 137-150
21. fMet binding site of initiation factor IF2. EMBO J 19: 5233-5240
22. Hatfield DL (2001) Selenium: Its Molecular Biology and Role in Human Health. Boston/Dordrecht/London: Kluwer Academic Publishers
23. Hilgenfeld R, Böck A, Wilting R (1996) Structural model for the selenocysteine-specific elongation factor SelB. Biochimie 78: 971-978
24. Hill KE, Lloyd RS, Burk RF (1993) Conserved nucleotide sequences in the open reading frame and 3′ untranslated region of selenoprotein P mRNA. Proc Natl Acad Sci USA 90: 537-541
25. Hubert N, Sturchler C, Westhof E, Carbon P, Krol A (1998) The 9/4 secondary structure of eukaryotic selenocysteine tRNA: more pieces of evidence. RNA 4: 1029-1033
26. Ibba M, Söll D (2002) Genetic code: introducing pyrrolysine. Curr Biol 12: R464-R466
27. 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 A 47: 110-119
28. Kapp LD, Lorsch JR (2004) GTP-dependent recognition of the methionine moiety on initiator tRNA by translation factor eIF2. J Mol Biol 335: 923-936
29. Keeling PJ, Fast NM, McFadden GI (1998) Evolutionary relationship between translation initiation factor eIF-2γ and selenocysteine-specific elongation factor SELB: change of function in translation factors. J Mol Evol 47: 649-655
30. 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
31. Klein DJ, Moore PB, Steitz TA (2004) The roles of ribosomal proteins in the structure assembly, and evolution of the large ribosomal subunit. J Mol Biol 340: 141-177
32. Kozak M (1990) Downstream secondary structure facilitates recognition of initiator codons by eukaryotic ribosomes. Proc Natl Acad Sci USA 87: 8301-8305
33. Kromayer M, Wilting R, Tormay P, Böck A (1996) Domain structure of the prokaryotic selenocysteine-specific elongation factor SelB. J Mol Biol 262: 413-420
34. Kyriakopoulos A, Behne D (2002) Selenium-containing proteins in mammals and other forms of life. Rev Physiol Biochem Pharmacol 145: 1-46
35. Marintchev A, Kolupaeva VG, Pestova TV, Wagner G (2003) Mapping the binding interface between human eukaryotic initiation factors 1A and 5B: a new interaction between old partners. Proc Natl Acad Sci USA 100: 1535-1540
36. fMet-binding domain of B. stearothermophilus initiation factor IF2. EMBO J 19: 1918-1926
37. Phe, EF-Tu, and a GTP analog. Science 270: 1464-1472
38. Cys-EF-Tu-GDPNP reveals general and specific features in the ternary complex and in tRNA. Struct Fold Des 7: 143-156
39. Olsen DS, Savner EM, Mathew A, Zhang F, Krishnamoorthy T, Phan L, Hinnebusch AG (2003) Domains of eIF1A that mediate binding to eIF2, eIF3 and eIF5B and promote ternary complex recruitment in vivo. EMBO J 22: 193-204
40. Otwinowski Z, Minor W (1997) Processing X-ray diffraction data collected in oscillation mode. Methods Enzymol 276: 307-326
41. Pestova TV, Lomakin IB, Lee JH, Choi SK, Dever TE, Hellen CU (2000) The joining of ribosomal subunits in eukaryotes requires eIF5B. Nature 403: 332-335
42. 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
43. Roll-Mecak A, Alone P, Cao C, Dever TE, Burley SK (2004) X-ray structure of translation initiation factor eIF2γ: implications for tRNA and eIF2γ binding. J Biol Chem 279: 10634-10642
44. 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
45. Rother M, Mathes I, Lottspeich F, Böck A (2003) Inactivation of the selB gene in Methanococcus maripaludis: effect on synthesis of selenoproteins and their sulfur-containing homologs. J Bacteriol 185: 107-114
46. Rother M, Resch A, Gardner WL, Whitman WB, Böck A (2001) Heterologous expression of archaeal selenoprotein genes directed by the SECIS element located in the 3′ non-translated region. Mol Microbiol 40: 900-908
47. Rother M, Wilting R, Commans S, Böck A (2000) Identification and characterisation of the selenocysteine-specific translation factor SelB from the archaeon Methanococcus jannaschii. J Mol Biol 299: 351-358
48. 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
49. Selmer M, Su XD (2002) Crystal structure of an mRNA-binding fragment of Moorella thermoacetica elongation factor SelB. EMBO J 21: 4145-4153
50. Shin BS, Maag D, Roll-Mecak A, Arefin MS, Burley SK, Lorsch JR, Dever TE (2002) Uncoupling of initiation factor eIF5B/IF2 GTPase and translational activities by mutations that lower ribosome affinity. Cell 111: 1015-1025
51. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25: 4876-4882
52. Tujebajeva RM, Copeland PR, Xu XM, Carlson BA, Harney JW, Driscoll DM, Hatfield DL, Berry MJ (2000) Decoding apparatus for eukaryotic selenocysteine insertion. EMBO Rep 1: 158-163
53. Valle M, Zavialov A, Li W, Stagg SM, Sengupta J, Nielsen RC, Nissen P, Harvey SC, Ehrenberg M, Frank J (2003) Incorporation of aminoacyl-tRNA into the ribosome as seen by cryo-electron microscopy. Nat Struct Biol 10: 899-906
54. Vitagliano L, Masullo M, Sica F, Zagari A, Bocchini V (2001) The crystal structure of Sulfolobus solfataricus elongation factor 1α in complex with GDP reveals novel features in nucleotide binding and exchange. EMBO J 20: 5305-5311
55. Sec-dependent assembly of the selenocysteine decoding apparatus. Mol Cell 11: 773-781
56. Zinoni F, Heider J, Böck A (1990) Features of the formate dehydrogenase mRNA necessary for decoding of the UGA codon as selenocysteine. Proc Natl Acad Sci USA 87: 4660-4664