Biopolym. Cell. 2013; 29(4):311-323.
http://dx.doi.org/10.7124/bc.000825
Reviews
Recognition of tRNAs with a long variable arm by aminoacyl-tRNA synthetases
1Tukalo M. A., 1Yaremchuk G. D., 1Kovalenko O. P., 1Kriklivyi I. A., 1Gudzera O. I.
  1. Institute of Molecular Biology and Genetics, NAS of Ukraine
    150, Akademika Zabolotnoho Str., Kyiv, Ukraine, 03680

Abstract

In prokaryotic cells three tRNA species, tRNASer, tRNALeu and tRNATyr, possess a long variable arm of 11–20 nucleotides (type 2 tRNA) rather than usual 4 or 5 nucleotides (type 1 tRNA). In this review we have summarized the results of our research on the structural basis for recognition and discrimination of type 2 tRNAs by Thermus thermophilus seryl-, tyrosyl- and leucyl-tRNA synthetases (SerRS, TyrRS and LeuRS) obtained by X-ray crystallography and chemical probing tRNA in solution. Crystal structures are now known of all three aminoacyl-tRNA synthetases complexed with type 2 tRNAs and the different modes of tRNA recognition represented by these structures will be discussed. In particular, emphasis will be given to the results on recognition of characteristic shape of type 2 tRNAs by cognate synthetases. In tRNASer, tRNATyr and tRNALeu the orientation of the long variable arm with respect to the body of the tRNA is different and is controlled by different packing of the core. In the case of SerRS the N-terminal domain and in the case of TyrRS, the C-terminal domain, bind to the characteristic long variable arm of the cognate RNA, thus recognizing the unique shape of the tRNA. The core of T. thermophilus tRNALeu has several layers of unusual base-pairs, which are revealed by the crystal structure of tRNALeu complexed with T. thermophilus LeuRS and by probing a ligand-free tRNA by specific chemical reagents in solution. In the crystal structure of the LeuRS-tRNALeu complex the unique D-stem structure is recognized by the C-terminal domain of LeuRS and these data are in good agreement with those obtained in solution. LeuRS has canonical class I mode of tRNA recognition, approaching the tRNA acceptor stem from the D-stem and minor groove of the acceptor stem side. SerRS also has canonical class II mode of tRNA recognition and approaches tRNASer from opposite, variable stem and major groove of acceptor stem site. And finally, TyrRS in strong contrast to canonical class I system has class II mode of tRNA recognition.
Keywords: type 2 tRNA, long variable arm, aminoacyl-tRNA synthetase, tRNA recognition, aminoacyl-tRNA synthetase complexes
Full text: (PDF, in English)

References

[1] Giege R., Sissler M. Florentz C. Universal rules and idiosyncratic features in tRNA identity Nucleic Acids Res 1998 26, N 22:5017–5035.
[2] Eriani G., Delarue M., Poch O., Gangloff J., Moras D. Partition of tRNA synthetases into two classes based on mutually exclusive sets of sequence motifs Nature 1990 347, N 6289 P. 203–206.
[3] Cusack S., Berthet-Colominas C., Hartlein M., Nassar N., Leberman R. A second class of synthetase structure revealed by X-ray analysis of Escherichia coli seryl-tRNA synthetase at 2.5 A Nature 1990 347, N 6290:249–255.
[4] Ibba M., Soll D. Aminoacyl-tRNA synthesis Annu. Rev. Biochem 2000 69:617–650.
[5] Fraser T. H., Rich A. Amino acids are not all initially attached to the same position on transfer RNA molecules Proc. Natl Acad. Sci. USA 1975 72, N 8:3044–3048.
[6] Sprinzl M., Cramer F. Site of aminoacylation of tRNAs from Escherichia coli with respect to the 2'or 3'-hydroxyl group of the terminal adenosine Proc. Natl Acad. Sci. USA 1975 72, N 8:3049–3053.
[7] Kavran J. M., Gundllapalli S., O'Donoghue P., Englert M., Soll D., Steitz T. A. Structure of pyrrolysyl-tRNA synthetase, an archaeal enzyme for genetic code innovation Proc. Natl Acad. Sci. USA 2007 104, N 27:11268–11273.
[8] Kamtekar S., Hohn M. J., Park H. S. et al. Toward understanding phosphoseryl-tRNACys formation: the crystal structure of Methanococcus maripaludis phosphoseryl-tRNA synthetase Proc. Natl Acad. Sci. USA 2007 104, N 8:2620–2625.
[9] Cusack S., Hartlein M., Leberman R. Sequence, structural and evolutionary relationships between class 2 aminoacyl-tRNA synthetases Nucleic Acids Res 1991 19, N 13:3489– 3498.
[10] Delarue M., Moras D. The aminoacyl-tRNA synthetase family: modules at work Bioessays 1993 15, N 10:675–687.
[11] Cusack S., Yaremchuk A., Tukalo M. tRNA recognition by aminoacyl-tRNA synthetases The many faces of tRNA / Eds D. S. Eggleston, C. D. Prescott, N. D. Pearson London: Acad. Press, 1997:55–65.
[12] Sprinzl M., Vassilenko K. S. Compilation of tRNA sequences and sequences of tRNA genes Nucleic Acids Res 2005 33 (Database issue) D139–140.
[13] Yaremchuk A. D., Tukalo M. A., Konovalenko A. V., Egorova S. P., Matsuka G. Kh. Isolation of seryl-tRNA synthetase from Thermus thermophilus HB-27 Biopolym. Cell 1989 5, N 5 P. 83–86.
[14] Garber M. B., Agalarov S. Ch., Eliseikina I. A. et al. Purification and crystallization of components of the protein-synthesizing system from Thermus thermophilus J. Crystal Growth 1991 110, N 1–2:228–236.
[15] Garber M. B., Yaremchuk A. D., Tukalo M. A., Egorova S. P., Berthet-Colominas C., Leberman R. Crystals of seryl-tRNA synthetase from Thermus thermophilus. Preliminary crystallographic data J. Mol. Biol 1990 213, N 4:631–632.
[16] Fujinaga M., Berthet-Colominas C., Yaremchuk A. D., Tukalo M. A., Cusack S. Refined crystal structure of seryl-tRNA synthetase from Thermus thermophilus at 2.5 C resolution J. Mol. Biol 1993 234, N 1:222–233.
[17] Cusack S., Berthet-Colominas C., Biou V., Borel F., Fujinaga M., Hartlein M., Krikliviy I., Nassar N., Price S., Tukalo M. A., Yaremchuk A., Leberman R. The crystal structure of seryl-tRNA synthetase and its complexes with ATP and tRNASer The translation apparatus: structure, function, regulation, evolution New-York; London: Plenum Press, 1993:1–12.
[18] Biou V., Yaremchuk A., Tukalo M., Cusack S. The 2.9 C crystal structure of T. thermophilus seryl-tRNA synthetase complexed with tRNA(Ser) Science 1994 263, N 5152:1404– 1410.
[19] Belrhali H., Yaremchuk A., Tukalo M. et al. Crystal structures at 2.5 angstrom resolution of seryl-tRNA synthetase complexed with two analogs of seryl adenylate Science 1994 263, N 5152 P. 1432–1436.
[20] Belrhali H., Yaremchuk A., Tukalo M., et al. The structural basis for seryl-adenylate and Ap4A synthesis by seryl-tRNA synthetase Structure 1995 3, N 4:341–352.
[21] Cavarelli J., Eriani G., Rees B. et al. The active site of yeast aspartyl-tRNA synthetase: structural and functional aspects of the aminoacylation reaction EMBO J 1994 13, N 2 P. 327–337.
[22] Yaremchuk A., Tukalo M., Grotli M., Cusack S. A succession of substrate induced conformational changes ensures the amino acid specificity of Thermus thermophilus prolyl-tRNA synthetase: comparison with histidyl-tRNA synthetase J. Mol. Biol 2001 309, N 4:989–1002.
[23] Arnez J. G., Moras D. Structural and functional consideration of the aminoacylation reaction Trends Biochem. Sci 1998 22, N 6 P. 211–216.
[24] Krikliviy I. A., Kovalenko O. P., Gudzera O. Y., Yaremchuk A. D., Tukalo M. A. Isolation and purification isoaccepting tRNA1Ser and tRNA2Ser from Thermus thermophilus Biopolym. Cell 2006 22, N 6:425–432.
[25] Petrushenko Z. M., Kovalenko O. P., Mal'chenko N. N., Krikliviy I. A., Yaremchuk A. D., Tukalo M. A. The primary structure of tRNASer from Thermus thermophilus Biopolym. cell 1997 13, N 3:202–208.
[26] Himeno H., Hasegawa T., Ueda T., Watanabe K., Shimizu M. Conversion of aminoacylation specificity from tRNATyr to tRNASer in vitro Nucleic Acids Res 1990 18, N 23:6815– 6819.
[27] Asahara H., Himeno H., Tamura K. et al. Escherichia coli seryltRNA synthetase recognizes tRNASer by its characteristic tertiary structure J. Mol. Biol 1994 236, N 3:738–748.
[28] Yaremchuk A. D., Tukalo M. A., Krikliviy I. A. et al. Crystallization of the seryl-tRNA synthetase-tRNASer complex from Thermus thermophilus J. Mol. Biol 1992 224, N 2 519–522.
[29] Yaremchuk A. D., Tukalo M. A., Krikliviy I. et al. A new crystal form of the complex between seryl-tRNA synthetase and tRNA (Ser) from Thermus thermophilus that diffracts to 2.8 C resolution FEBS Lett 1992 310, N 2:157–161.
[30] Kovalenko O. P., Petrushenko Z. M., Mal'chenko N. N., Krikliviy I. A., Yaremchuk A. D., Tukalo M. A. Studies of interaction sites between tRNA2Ser from Thermus thermophilus and seryltRNA synlhetase by chemical modification Biopolym. Cell 1997 13, N 4:298–302.
[31] Kovalenko O. P., Kriklivyi I. A., Tukalo M. A. Study of tertiary structure elements of tRNASer from Thermus thermophilus in solution Biopolym. Cell 2000 16, N 2:115–123.
[32] Vlassov VV, Giegé R, Ebel JP. Tertiary structure of tRNAs in solution monitored by phosphodiester modification with ethylnitrosourea. Eur J Biochem. 1981;119(1):51-9.
[33] Peattie D. A., Gilbert W. Chemical probes for higher-order structure in RNA Proc. Natl Acad. Sci. USA 1980 77, N 8 P. 4679–4682.
[34] Cusack S., Yaremchuk A., Tukalo M. The crystal structure of the ternary complex of T. thermophilus seryl-tRNA synthetase with tRNASer and seryl-adenylate analogue reveals a conformational switch in the active site EMBO J 1996 15, N 11:2834– 2842.
[35] Starzyk R. M., Webster T. A., Schimmel P. Evidence for dispensable sequences inserted into a nucleotide fold Science 1987 237, N 4822:1614–1618.
[36] Nureki O., Vassylyev D. G., Tateno M. et al. Enzyme structure with two catalytic sites for double-sieve selection of substrate Science 1998 280, N 5363:578–582.
[37] Silvian L., Wang J., Steitz T. A. Insights into editing from an IletRNA synthetase structure with tRNAIle and mupirocin Science 1999 285, N 5430:1074–1077.
[38] Schmidt E., Schimmel P. Mutational isolation of a sieve for editing in a transfer RNA synthetase Science 1994 264, N 5156:265–267.
[39] Lincecum T. L. Jr., Tukalo M., Yaremchuk A. et al. Structural and mechanistic basis of preand posttransfer editing by leucyltRNA synthetase Mol. Cell 2003 11, 4:951–963.
[40] Asahara H., Himeno H., Tamura K., Hasegawa T., Watanabe K., Shimizu M. Recognition nucleotides of Escherichia coli tRNALeu and its elements facilitating discrimination from tRNASer and tRNATyr J. Mol. Biol 1993 231, N 2 P. 219– 229.
[41] Yaremchuk A. D., Kovalenko O. P., Gudzera O. I., Tukalo M. A. Molecular cloning, sequencing and expression in Escherichia coli cells Thermus thermophilus leucyl-tRNA synthetase Biopolym. Cell 2011 27, N 6:436–441.
[42] Yaremchuk A., Cusack S., Gudzera O., Grotli M., Tukalo M. Crystallization and preliminary crystallographic analysis of Thermus thermophilus leucyl-tRNA synthetase and its complexes with leucine and a non-hydrolysable leucyl-adenylate analogue Acta Crystallogr. D Biol. Crystallogr–2000 56, Pt 5 P. 667–669.
[43] Cusack S., Yaremchuk A., Tukalo M. The 2 C crystal structure of leucyl-tRNA synthetase and its complex with a leucyl-adenylate analogue EMBO J 2000 19, N 10:2351–2361.
[44] Yaremchuk A. D., Gudzera O. I., Egorova S. P., Rozhko D. I., Krikliviy I. A., Tukalo M. A. Leucyl-tRNA synthetase from Thermus thermophilus. Purification and some properties of the crystallizing enzyme Biopolym. Cell 2001 17, N 3 P. 216–220.
[45] Tukalo M., Yaremchuk A., Fukunaga R., Yokoyama S., Cusack S. The crystal structure of leucyl-tRNA synthetase complexed with tRNALeu in the post-transfer-editing conformation Nat. Struct. Mol. Biol 2005 12, N 10:923–930.
[46] Gudzera O. I., Yaremchuk A. D., Tukalo M. A. Functional role of C-terminal domain of Thermus thermophilus leucyl-tRNA synthetase Biopolym. Cell 2010 26, N 6:478–485.
[47] Hsu J. L., Rho S. B., Vannella K. M., Martinis S. A. Functional divergence of a unique C-terminal domain of leucyl-tRNA synthetase to accommodate its splicing and aminoacylation roles J. Biol. Chem 2006 281, N 32:23075–23082.
[48] Fukunaga R., Yokoyama S. The C-terminal domain of the archaeal leucyl-tRNA synthetase prevents misediting of isoleucyl-tRNAIle Biochemistry 2007 46, N 17:4985–4996.
[49] Kovalenko O., Kriklivyi I., Yaremchuk A., Tukalo M. Comparative studies the tertiary structure of T. thermophilus tRNASer and tRNALeu and the sites of interaction with cognate aminoacyltRNA synthetases by chemical modification methods 18th tRNA Workshop «tRNA 2000» (8th–12th April 2000, Cambridge) Cambridge: BioDesign Publications, 2001:20.
[50] Palencia A., Crepin T., Vu M. T., Lincecum T. L. Jr., Martinis S. A., Cusack S. Structural dynamics of the aminoacylation and proofeading functional cycle of bacterial leucyl-tRNA synthetase Nat. Struct. Mol. Biol 2012 19, N 7:677–684.
[51] Kovalenko O. P., Kriklivyi I. A., Tukalo M. A. Participation of nitrogen bases in the tertiary folding of tRNALeu from Thermus thermophilus Biopolym. Cell 2003 19, N 2:151–156.
[52] Fukunaga R., Ishitani R., Nureki O., Yokoyama S. Crystallization of leucyl-tRNA synthetase complexed with tRNALeu from the archaeon Pyrococcus horikoshii Acta Crystallogr. Sect. F. Struct. Biol. Cryst. Commun 2005 61, Pt 1:30–32.
[53] Rock F. L., Mao W., Yaremchuk A. et al. An antifungal agent inhibits an aminoacyl-tRNA synthetase by trapping tRNA in the editing site Science 2007 316, N 5832:1759–1761.
[54] Asahara H., Nameki N., Hasegawa T. In vitro selection of RNAs aminoacylated by Escherichia coli leucyl-tRNA synthetase J. Mol. Biol 1998 283, N 3:605–618.
[55] Tocchini-Valentini G., Saks M. E., Abelson J. tRNA leucine identity and recognition sets J. Mol. Biol 2000 298, N 5:779–793.
[56] Larkin D. C., Williams A. M., Martinis S. A., Fox G. E. Identification of essential domains for Escherichia coli tRNALeu aminoacylation and amino acid editing using minimalist RNA molecules Nucleic Acids Res 2002 30, N 10:2103–2113.
[57] Cusack S. Eleven down and nine to go Nat. Struct. Biol 1995 2, N 10:824–831.
[58] Brick P., Blow D. M. Crystal structure of a deletion mutant of a tyrosyl-tRNA synthetase complexed with tyrosine J. Mol. Biol 1987 194, N 2:287–294.
[59] Yaremchuk A. D., Kovalenko O. P., Gudzera O. I., Tukalo M. A. Molecular cloning, sequencing and sequence analysis of Thermus thermophilus tyrosyl-tRNA synthetase Biopolym. Cell 2004 20, N 1–2:144–149.
[60] Yaremchuk A., Kriklivyi I., Tukalo M., Cusack S. Class I tyrosyltRNA synthetase has a class II mode of cognate tRNA recognition EMBO J 2002 21, N 14:3829–3240.
[61] Bedouelle H., Guez-Ivanier V., Nageotte R. Discrimination between transfer-RNAs by tyrosyl-tRNA synthetase Biochimie 1993 75, N 12:1099–1108.
[62] Egorova S. P., Yaremchuk A. D., Krikliviy I. A., Tukalo M. A. Comparative analysis of interaction sites of tRNA from Thermus thermophilus and Escherichia coli with cognate aminoacyl tRNA synthetases by the chemical modification and nuclease hydrolysis methods Bioor. Khimiya 1998 24, N 8:593–600.
[63] Ruff M., Krishnaswamy S., Boeglin M. et al. Class II aminoacyl transfer RNA synthetases: crystal structure of yeast aspartyltRNA synthetase complexed with tRNAAsp Science 1991 252, N 5013:1682–1689.
[64] Rould M. A., Perona J. J., Soll D., Steitz T. A. Structure of E. coli glutaminyl-tRNA synthetase complexed with tRNAGln and ATP t 2.8 C resolution Science 1989 246, N 4934:1135–1142.
[65] Cramer F., Faulhammer H., von der Haar F., Sprinzl M., Sternbach H. Aminoacyl-tRNA synthetases from baker's yeast: reacting site of aminoacylation is not uniform for all tRNAs FEBS Lett 1975 56, N 2:212–214.
[66] Kobayashi T., Nureki O., Ishitani R. et al. Structural basis for orthogonal tRNA specificities of tyrosyl-tRNA synthetases for genetic code expansion Nat. Struct. Biol 2003 10, N 6:425–432.
[67] Yang X. L., Otero F. J., Ewalt K. L. et al. Two conformations of a crystalline human tRNA synthetase-tRNA complex: implications for protein synthesis EMBO J 2006 25, N 12:2919–2929.
[68] Hou Y. M., Schimmel P. Modeling with in vitro kinetic parameters for the elaboration of transfer RNA identity in vivo Biochemistry 1989 28, N 12:4942–4947.
[69] Himeno H., Hasegawa T., Ueda T., Watanabe K., Shimizu M. Conversion of aminoacylation specificity from tRNATyr to tRNASer in vitro Nucleic Acids Res 1990 18, N 23:6815–6819.
[70] Fechter P., Rudinger-Thirion J., Tukalo M., Giege R. Major tyrosine identity determinants in Methanococcus jannaschii and Saccharomyces cerevisiae tRNATyr are conserved but expressed differently Eur. J. Biochem 2001 268, N 3:761–767.
[71] Hauenstein S., Zhang C. M., Hou Y. M., Perona J. J. Shape-selective RNA recognition by cysteinyl-tRNA synthetase Nat. Struct. Mol. Biol 2004 11, N 11:1134–1141.
[72] Soma A., Himeno H. Cross-species aminoacylation of tRNA with a long variable arm between Escherichia coli and Saccharomyces cerevisiae Nucleic Acids Res 1998 26, N 19:4374–4381.
[73] Lenhard B., Orellana O., Ibba M., Weygand-Durasevic I. tRNA recognition and evolution of determinants in seryl-tRNA synthesis Nucleic Acids Res 1999 27, N 3:721–729.
[74] Sidorik L. L., Gudzera O. I., Dragovoz V. A., Tukalo M. A., Beresten S. F. Immuno-chemical non-cross-reactivity between eukaryotic and prokaryotic seryl-tRNA synthetase FEBS Let 1991 292, N 1, 2:76–78.
[75] Xu X., Shi Y., Zhang H. M. et al. Unique domain appended to vertebrate tRNA synthetase is essential for vascular development Nat. Commun 2012 3, N 2:1–9.
[76] Petrushenko Z. M., Tukalo M. A., Gudzera O. I et al. Identification of interaction sites of tRNALeu from cow mammary gland with the cognate aminoacyl-tRNA synthetase by the chemical modification method Rus. J. Bioorg. Chem 1990 16, N 12:1647–1652.
[77] Dock-Bregeon A. C., Garsia A., Giege R., Moras D. The contacts of yeast tRNASer with seryl-tRNA synthetase studied by footprinting experiments Eur. J. Biochem 1990 188, N 2 P. 283–290.
[78] Kalachnyuk L. G., Tukalo M. A., Matsuka G. Kh. Identification of interaction sites of tRNAGCUSer from the bovine liver with cognate aminoacyl-tRNA synthetase by the chemical modification method Ukr. Biokhim. Zh 1992 64, N 6:38–42.
[79] Wu X. Q., Gross H. J. The long extra arms of human tRNA (Ser(Sec)) and tRNASer function as major identity elements for serylation in an orientation-dependent, but not sequence-specific manner Nucl. Acids Res 1993 21, N 24 P.5589–5594.
[80] Bonfils G., Jaquenoud M., Bontron S. et al. Leucyl-tRNA synthetase controls TORC1 via the EGO complex Mol. Cell 2012 46, N 1:105–110.
[81] Han J. M., Jeong S. J., Park M. C.et al. Leucyl-tRNA synthetase is an intracellular leucine sensor for the mTORC1-signaling pathway Cell 2012 149, N 2:410–424.