The catalytic domain of topological knot tRNA methyltransferase (TrmH) discriminates between substrate tRNA and nonsubstrate tRNA via an induced-fit process

Journal of Biological Chemistry

Volumn 288, Issue 35, 2013, Pages 25562-25574

  Ochi, Anna ^a,e   Makabe, Koki ^b,f   Yamagami, Ryota ^a   Hirata, Akira ^a   Sakaguchi, Reiko ^c   Hou, Ya Ming ^c   Watanabe, Kazunori ^a,g   Nureki, Osamu ^d   Kuwajima, Kunihiro ^b,h   Hori, Hiroyuki ^a  

^a EHIME UNIVERSITY   (Japan)

^b OKAZAKI INSTITUTE FOR INTEGRATIVE BIOSCIENCE   (Japan)

^c THOMAS JEFFERSON UNIVERSITY   (United States)

^d UNIVERSITY OF TOKYO   (Japan)

^e HOKKAIDO UNIVERSITY   (Japan)

^f YAMAGATA UNIVERSITY   (Japan)

^g OKAYAMA UNIVERSITY   (Japan)

^h GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROCESS; C-TERMINAL REGIONS; CATALYTIC DOMAINS; CHIMERIC PROTEINS; METHYLTRANSFERASES; PRE-STEADY STATE; RECOGNITION SITE; SITE DIRECTED MUTAGENESIS;

PROTEINS; RNA;

TOPOLOGY;

TRANSFER RNA METHYLTRANSFERASE;

AMINO ACID SUBSTITUTION; ARTICLE; BACTERIAL CELL; BINDING AFFINITY; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME MECHANISM; ESCHERICHIA COLI; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN STABILITY; SITE DIRECTED MUTAGENESIS; THERMUS THERMOPHILUS;

PRE-STEADY STATE KINETICS; PROTEIN STRUCTURE; RNA METHYLATION; RNA METHYLTRANSFERASE; RNA MODIFICATION; RNA-BINDING PROTEINS; RNA-PROTEIN INTERACTION; SPOU FAMILY; SPOUT SUPERFAMILY; TRANSFER RNA (TRNA);

AMINO ACID MOTIFS; BACTERIAL PROTEINS; ESCHERICHIA COLI; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; RNA, BACTERIAL; RNA, TRANSFER; SUBSTRATE SPECIFICITY; THERMUS THERMOPHILUS; TRNA METHYLTRANSFERASES;

EID: 84883372113     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.485128     Document Type: Article

References (67)

1. Dunin-Horkawicz, S., Czerwoniec, A., Gajda, M. J., Feder, M., Grosjean, H., and Bujnicki, J. M. (2006) MODOMICS: a database of RNA modification pathways. Nucleic Acids Res. 34, D145-D149
2. Rozenski, J., Crain, P. F., and McCloskey, J. A. (1999) The RNA modification database: 1999 update. Nucleic Acids Res. 27, 196-197
3. Jühling, F., Mörl, M., Hartmann, R. K., Sprinzl, M., Stadler, P. F., and Pütz, J. (2009) tRNAdb 2009: compilation of tRNA sequences and tRNA genes. Nucleic Acids Res. 37, D159-D162
4. Robertus, J. D., Ladner, J. E., Finch, J. T., Rhodes, D., Brown, R. S., Clark, B. F., and Klug, A. (1974) Structure of yeast phenylalanine tRNA at 3 Å resolution. Nature 250, 546-551
5. Kim, S. H., Sussman, J. L., Suddath, F. L., Quigley, G. J., McPherson, A., Wang, A. H., Seeman, N. C., and Rich, A. (1974) The general structure of transfer RNA molecules. Proc. Natl. Acad. Sci. U.S.A. 71, 4970-4974
6. Jöckel, S., Nees, G., Sommer, R., Zhao, Y., Cherkasov, D., Hori, H., Ehm, G., Schnare, M., Nain, M., Kaufmann, A., and Bauer, S. (2012) The 2'-Omethylation status of a single guanosine controls transfer RNA mediated Toll-like receptor 7 activation or inhibition. J. Exp. Med. 209, 235-241
7. Gehrig, S., Eberle, M.-E., Botschen, F., Rimbach, K., Eberle, F., Eigenbrod, T., Kaiser, S., Holmes, W. M., Erdmann, V. A., Sprinzl, M., Bec, G., Keith, G., Dalpke, A. H., and Helm, M. (2012) Identification of modifications in microbial, native tRNA that suppress immunostimulatory activity. J. Exp. Med. 209, 225-233
8. Gustafsson, C., Reid, R., Greene, P. J., and Santi, D. V. (1996) Identification of new RNA modifying enzymes by iterative genome search using known modifying enzymes as probes. Nucleic Acids Res. 24, 3756-3762
9. Persson, B. C., Jäger, G., and Gustafsson, C. (1997) The spoU gene of Escherichia coli, the fourth gene of the spot operon, is essential for tRNA (Gm18) 2'-O-methyltransferase activity. Nucleic Acids Res. 25, 3969-3973
10. Hori, H., Yamazaki, N., Matsumoto, T., Watanabe, Y., Ueda, T., Nishikawa, K., Kumagai, I., and Watanabe, K. (1998) Substrate recognition of tRNA (guanosine-2')-methyltransferase from Thermus thermophilus HB27. J. Biol. Chem., 273, 25721-25727
11. Hori, H., Suzuki, T., Sugawara, K., Inoue, Y., Shibata, T., Kuramitsu S., Yokoyama, S., Oshima, T., and Watanabe, K. (2002) Identification and characterization of tRNA (Gm18) methyltransferase from Thermus thermophilus HB8: domain structure and conserved amino acid sequence motifs. Genes Cells 7, 259-272
12. Hori, H., Kubota, S., Watanabe, K., Kim, J. M., Ogasawara, T., Sawasaki, T., and Endo, Y. (2003) Aquifex aeolicus tRNA (Gm18) methyltransferase has unique substrate specificity. J. Biol. Chem. 278, 25081-25090
13. Cavaillé, J., Chetouani, F., and Bachellerie, J.-P. (1999) The yeast Saccharomyces cerevisiae YDL112w ORF encodes the putative 2'-O-ribose methyltransferase catalyzing the formation of Gm18 in tRNAs. RNA 5, 66-81
14. Nureki, O., Watanabe, K., Fukai, S., Ishii, R., Endo, Y., Hori, H., and Yokoyama, S. (2004) Deep knot structure for construction of active site and cofactor binding site of tRNA modification enzyme. Structure 12, 593-602
15. Schubert, H. L., Blumenthal, R. M., and Cheng, X. (2003) Many paths to methyltransfer: a chronicle of convergence. Trends Biochem. Sci. 28, 329-335
16. Nureki, O., Shirouzu, M., Hashimoto, K., Ishitani, R., Terada, T., Tamakoshi, M., Oshima, T., Chijimatsu, M., Takio, K., Vassylyev, D. G., Shibata, T., Inoue, Y., Kuramitsu, S., and Yokoyama, S. (2002) An enzyme with a deep trefoil knot for the active-site architecture. Acta Crystallogr. D Biol. Crystallogr. 58, 1129-1137
17. Watanabe, K., Nureki, O., Fukai, S., Ishii, R., Okamoto, H., Yokoyama, S., Endo, Y., and Hori, H. (2005) Roles of conserved amino acid sequence motifs in the SpoU (TrmH) RNA methyltransferase family. J. Biol. Chem. 280, 10368-10377
18. Watanabe, K., Nureki, O., Fukai, S., Endo, Y., and Hori, H. (2006) Functional categorization of the conserved basic amino acid residues in TrmH (tRNA(Gm18)methyltransferase) enzymes. J. Biol. Chem. 281, 34630-34639
19. Ochi, A., Makabe, K., Kuwajima, K., and Hori, H. (2010) Flexible recognition of the tRNA G18 methylation target site by TrmH methyltransferase through first binding and induced fit processes. J. Biol. Chem. 285, 9018-9029
20. Awai, T., Ochi, A., Ihsanawati, Sengoku, T., Hirata, A., Bessho, Y., Yokoyama, S., and Hori, H. (2011) Substrate tRNA recognition mechanism of a multisite-specific tRNA methyltransferase, Aquifex aeolicus Trm1, based on the X-ray crystal structure. J. Biol. Chem. 286, 35236-35246
21. Ny, T., and Björk, G. R. (1980) Cloning and restriction mapping of the trmA gene coding for transfer ribonucleic acid (5-methyluridine)- methyltransferase in Escherichia coli K-12. J. Bacteriol. 142, 371-379
22. Ishida, K., Kunibayashi, T., Tomikawa, C., Ochi, A., Kanai, T., Hirata, A., Iwashita, C., and Hori, H. (2011) Pseudouridine at position 55 in tRNA controls the contents of other modified nucleotides for low-temperature adaptation in the extreme-thermophilic eubacterium Thermus thermophilus. Nucleic Acids Res. 39, 2304-2318
23. Brissette, P., Ballou, D. P., and Massey, V. (1989) Determination of the dead time of a stopped-flow fluorometer. Anal. Biochem. 181, 234-238
24. Byström, A. S., and Björk, G. R. (1982) Chromosomal location and cloning of the gene (trmD) responsible for the synthesis of tRNA (m1G) methyltransferase in Escherichia coli K-12. Mol. Gen. Genet. 188, 440-446
25. Ahn, H. J., Kim, H. W., Yoon, H. J., Lee, B. I., Suh, S. W., and Yang, J. K. (2003) Crystal structure of tRNA (m1G37) methyltransferase: insights into tRNA recognition. EMBO J. 22, 2593-2603
26. Elkins, P. A., Watts, J. M., Zalacain, M., van Thiel, A., Vitazka, P. R., Redlak, M., Andraos-Selim, C., Rastinejad, F., and Holmes, W. M. (2003) Insights into catalysis by a knotted TrmD tRNA methyltransferase. J. Mol. Biol. 333, 931-949
27. Liu, J., Wang, W., Shin, D. H., Yokota, H., Kim, R., and Kim, S.-H. (2003) Crystal structure of tRNA (m1G37) methyltransferase from Aquifex aeolicus at 2.6 Å resolution: a novel methyltransferase fold. Proteins 53, 326-328
28. Anantharaman, V., Koonin, E. V., and Aravind, L. (2002) SPOUT: a class of methyltransferases that includes spoU and trmD RNA methylase superfamilies, and novel superfamilies of predicted prokaryotic RNA methylases. J. Mol. Microbiol. Biotechnol. 4, 71-75
29. Kuratani, M., Bessho, Y., Nishimoto, M., Grosjean, H., and Yokoyama, S. (2008) Crystal structure and mutational study of a unique SpoU family archaeal methylase that forms 2'-O-methylcytidine at position 56 of tRNA. J. Mol. Biol. 375, 1064-1075
30. Pleshe, E., Truesdell, J., and Batey, R. T. (2005) Structure of a class II TrmH tRNA-modifying enzyme from Aquifex aeolicus. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 61, 722-728
31. Lim, K., Zhang, H., Tempczyk, A., Krajewski, W., Bonander, N., Toedt, J., Howard, A., Eisenstein, E., and Herzberg, O. (2003) Structure of the YibK methyltransferase from Haemophilus influenzae (HI0766): a cofactor bound at a site formed by a knot. Proteins 51, 56-67
32. Liu, R. J., Zhou, M., Fang, Z. P., Wang, M., Zhou, X. L., and Wang, E. D. (2013) The tRNA recognition mechanism of the minimalist SPOUT methyltransferase, TrmL. Nucleic Acids Res., in press
33. Tkaczuk, K. L., Dunin-Horkawicz, S., Purta, E., and Bujnicki, J. M. (2007) Structural and evolutionary bioinformatics of the SPOUT superfamily of methyltransferases. BMC Bioinformatics 8, 73
34. Purta, E., van Vliet, F., Tkaczuk, K. L., Dunin-Horkawicz, S., Mori, H., Droogmans, L., and Bujnicki, J. M. (2006) The yfhQ gene of Escherichia coli encodes a tRNA:Cm32/Um32 methyltransferase. BMC Mol. Biol. 7, 23
35. Benítez-Páez, A., Villarroya, M., Douthwaite, S., Gabaldón, T., and Armengod, M. E. (2010) YibK is the 2'-O- methyltransferase TrmL that modifies the wobble nucleotide in Escherichia coli tRNA (Leu) isoacceptors. RNA 16, 2131-2143
36. Renalier, M. H., Joseph, N., Gaspin, C., Thebault, P., and Mougin, A. (2005) The Cm56 tRNA modification in archaea is catalyzed either by a specific 2'-O-methylase or a C/D sRNP. RNA 11, 1051-1063
37. Lövgren, J. M., and Wikström, P. M. (2001) The rlmB gene is essential for formation of Gm2251 in 23S rRNA but not for ribosome maturation in Escherichia coli. J. Bacteriol. 183, 6957-6960
38. Michel, G., Sauvé, V., Larocque, R., Li, Y., Matte, A., and Cygler, M. (2002) The structure of the RlmB 23S rRNA methyltransferase reveals a new methyltransferase fold with a unique knot. Structure 10, 1303-1315
39. Treede, I., Jakobsen, L., Kirpekar, F., Vester, B., Weitnauer, G., Bechthold, A., and Douthwaite, S. (2003) The avilamycin resistance determinants AviRa and AviRb methylate 23S rRNA at the guanosine 2535 base and the uridine 2479 ribose. Mol. Microbiol. 49, 309-318
40. Mosbacher, T. G., Bechthold, A., and Schulz, G. E. (2005) Structure and function of the antibiotic resistance-mediating methyltransferase AviRb from Streptomyces viridochromogenes. J. Mol. Biol. 345, 535-545
41. Kempenaers, M., Roovers, M., Oudjama, Y., Tkaczuk, K. L., Bujnicki, J. M., and Droogmans, L. (2010) New archaeal methyltransferases forming 1-methyladenosine or 1-methyladenosine and 1-methylguanosine at position 9 of tRNA. Nucleic Acids Res. 38, 6533-6543
42. Chen, H. Y., and Yuan, Y. A. (2010) Crystal structure of Mj1640/DUF358 protein reveals a putative SPOUT-class RNA methyltransferase. J. Mol. Cell Biol. 2, 366-374
43. Chatterjee, K., Blaby, I. K., Thiaville, P. C., Majumder, M., Grosjean, H., Yuan, Y. A., Gupta, R., and de Crécy-Lagard, V. (2012) The archaeal COG1901/DUF358 SPOUT-methyltransferase members, together with pseudouridine synthase Pus10, catalyze the formation of 1-methylpseudouridine at position 54 of tRNA. RNA 18, 421-433
44. Wurm, J. P., Griese, M., Bahr, U., Held, M., Heckel, A., Karas, M., Soppa, J., and Wöhnert, J. (2012) Identification of the enzyme responsible for N1- methylation of pseudouridine 54 in archaeal tRNAs. RNA 18, 412-420
45. Vallat, B. K., Pillardy, J.,Májek, P., Meller, J., Blom, T., Cao, B., and Elber, R. (2009) Building and assessing atomic models of proteins from structural templates: learning and benchmarks. Proteins 76, 930-945
46. Seno, T., Kobayashi, M., and Nishimura, S. (1968) Purification of Escherichia coli methionine tRNAF and methionine tRNAM and studies on their biophysical and biochemical properties. Biochim. Biophys. Acta 169, 80-94
47. Taniguchi, H., and Hayashi, N. (1998) A liquid chromatography/ electrospray mass spectrometric study on the post-transcriptional modification of tRNA. Nucleic Acids Res. 26, 1481-1486
48. Koren, R., and Hammes, G. G. (1976) A kinetic study of protein-protein interactions. Biochemistry 15, 1165-1171
49. Alsallaq, R., and Zhou, H. X. (2008) Electrostatic rate enhancement and transient complex of protein-protein association. Proteins 71, 320-335
50. Hori, H., Saneyoshi, M., Kumagai, I., Miura, K., and Watanabe, K. (1989) Effects of modification of 4-thiouridine in E coli tRNA(fMet) on its methyl acceptance activity by thermostable Gm-methylases. J. Biochem. 106, 798-802
51. Matsumoto, T., Nishikawa, K., Hori, H., Ohta, T., Miura, K., and Watanabe, K. (1990) Recognition sites of tRNA by a thermostable tRNA (guanosine-2'-)-methyltransferase from Thermus thermophilus HB27. J. Biochem. 107, 331-338
52. Wurm, J. P., Meyer, B., Bahr, U., Held, M., Frolow, O., Kötter, P., Engels, J. W., Heckel, A., Karas, M., Entian, K. D., and Wöhnert, J. (2010) The ribosome assembly factor Nep1 responsible for Bowen-Conradi syndrome is a pseudouridine-N1-specific methyltransferase. Nucleic Acids Res. 38, 2387-2398
53. Meyer, B., Wurm, J. P., Kötter, P., Leisegang, M. S., Schilling, V., Buchhaupt, M., Held, M., Bahr, U., Karas, M., Heckel, A., Bohnsack, M. T., Wöhnert, J., and Entian, K. D. (2011) The Bowen-Conradi syndrome protein Nep1 (Emg1) has a dual role in eukaryotic ribosome biogenesis, as an essential assembly factor and in the methylation of Ψ1191 in yeast 18S rRNA. Nucleic Acids Res. 39, 1526-1537
54. de Crécy-Lagard, V., Brochier-Armanet, C., Urbonavicius, J., Fernandez, B., Phillips, G., Lyons, B., Noma, A., Alvarez, S., Droogmans, L., Armengaud, J., and Grosjean, H. (2010) Biosynthesis of wyosine derivatives in tRNA: an ancient and highly diverse pathway in Archaea. Mol. Biol. Evol. 27, 2062-2077
55. Goto-Ito, S., Ito, T., Ishii, R., Muto, Y., Bessho, Y., and Yokoyama, S. (2008) Crystal structure of archaeal tRNA(m(1)G37)methyltransferase aTrm5. Proteins 72, 1274-1289
56. Goto-Ito, S., Ito, T., Kuratani, M., Bessho, Y., and Yokoyama, S. (2009) Tertiary structure checkpoint at anticodon loop modification in tRNA functional maturation. Nat. Struct. Mol. Biol. 16, 1109-1115
57. Björk, G. R., Jacobsson, K., Nilsson, K., Johansson, M. J., Byström, A. S., and Persson, O. P. (2001) A primordial tRNA modification required for the evolution of life EMBO J. 20, 231-239
58. Brulé, H., Elliott, M., Redlak, M., Zehner, Z. E., and Holmes, W. M. (2004) Isolation and characterization of the human tRNA-(N1G37) methyltransferase (TRM5) and comparison to the Escherichia coli TrmD protein. Biochemistry 43, 9243-9255
59. Lee, C., Kramer, G., Graham, D. E., and Appling, D. R. (2007) Yeast mitochondrial initiator tRNA is methylated at guanosine 37 by the Trm5- encoded tRNA (guanine-N1-)-methyltransferase. J. Biol. Chem. 282, 27744-27753
60. Paris, Z., Horáková, E., Rubio, M. A., Sample, P., Fleming, I. M., Armocida, S., Lukes, J., and Alfonzo, J. D. (2013) The T. brucei TRM5 methyltransferase plays an essential role in mitochondrial protein synthesis and function. RNA 19, 649-658
61. Christian, T., and Hou, Y. M. (2007) Distinct determinants of tRNA recognition by the TrmD and Trm5 methyl transferases. J. Mol. Biol. 373, 623-632
62. Christian, T., Lahoud, G., Liu, C., and Hou, Y. M. (2010) Control of catalytic cycle by a pair of analogous tRNA modification enzymes. J. Mol. Biol. 400, 204-217
63. Lahoud, G., Goto-Ito, S., Yoshida, K., Ito, T., Yokoyama, S., and Hou, Y. M. (2011) Differentiating analogous tRNA methyltransferases by fragments of the methyl donor. RNA 17, 1236-1246
64. Sakaguchi, R., Giessing, A., Dai, Q., Lahoud, G., Liutkeviciute, Z., Klimasauskas, S., Piccirilli, J., Kirpekar, F., and Hou, Y. M. (2012) Recognition of guanosine by dissimilar tRNA methyltransferases. RNA 18, 1687-1701
65. Sabina, J., and Söll, D. (2006) The RNA-binding PUA domain of archaeal tRNA-guanine transglycosylase is not required for archaeosine formation. J. Biol. Chem. 281, 6993-7001
66. Ishitani, R., Nureki, O., Nameki, N., Okada, N., Nishimura, S., and Yokoyama, S. (2003) Alternative tertiary structure of tRNA for recognition by a posttranscriptional modification enzyme. Cell 113, 383-394
67. Tomikawa, C., Yokogawa, T., Kanai, T., and Hori, H. (2010) N7-Methylguanine at position 46 (m7G46) in tRNA from Thermus thermophilus is required for cell viability through a tRNA modification network. Nucleic Acids Res. 38, 942-957