Stabilization of tRNA (m1G37) methyltransferase [TrmD]from Aquifex aeolicus by an intersubunit disulfide bond formation

Genes to Cells

Volumn 13, Issue 8, 2008, Pages 807-816

  Toyooka, Takashi ^a   Awai, Takako ^a   Kanai, Tamotsu ^a   Imanaka, Tadayuki ^a   Hori, Hiroyuki ^a,b  

^a EHIME UNIVERSITY   (Japan)

^b KYOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOSINE; DISULFIDE; DITHIOTHREITOL; MUTANT PROTEIN; PROTEIN SUBUNIT; RECOMBINANT PROTEIN; SERINE; TRANSFER RNA METHYLTRANSFERASE; BACTERIAL PROTEIN; CYSTEINE;

ALPHA HELIX; AQUIFEX AEOLICUS; ARTICLE; BACTERIAL CELL; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME ASSAY; ENZYME STABILITY; GEL FILTRATION CHROMATOGRAPHY; INCUBATION TEMPERATURE; INCUBATION TIME; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRECIPITATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DETERMINATION; PROTEIN STRUCTURE; STRUCTURE ANALYSIS; WILD TYPE; AMINO ACID SEQUENCE; BACTERIUM; CHEMICAL STRUCTURE; CHEMISTRY; CIRCULAR DICHROISM; ENZYMOLOGY; METABOLISM; MOLECULAR GENETICS; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE; SEQUENCE ALIGNMENT;

AQUIFEX AEOLICUS;

AMINO ACID SEQUENCE; BACTERIA; BACTERIAL PROTEINS; CIRCULAR DICHROISM; CYSTEINE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; RECOMBINANT PROTEINS; SEQUENCE ALIGNMENT; TRNA METHYLTRANSFERASES;

EID: 48649085955     PISSN: 13569597     EISSN: 13652443     Source Type: Journal    
DOI: 10.1111/j.1365-2443.2008.01207.x     Document Type: Article

References (48)

1. Ahn, H.J., Kim, H.W., Yoon, H.J., Lee, B., Suh, S.S. & Yang, J.K. (2003) Crystal structure of tRNA (m1G37) methyltransferase: Insights into tRNA recognition. EMBO J. 22, 2593-2603.
2. Anantharaman, V., Koonin, E.V. & 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.
3. Baba, T., Ara, T., Hasegawa, M., Takai, Y., Okumura, Y., Baba, M., Datsenko, K.A., Tomita, M., Wanner, B.L. & Mori, H. (2006) Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: The Keio collection. Mol. Syst. Biol. 2, 2006-2008.
4. Beeby, M., O'Connor, B.D., Ryttersgaard, C., Boutz, D.R., Perry, L.J. & Yeates, T.O. (2005) The genomics of disulfide bonding and protein stabilization in thermophiles. PLoS Biol. 3, e309.
5. Björk, G.R. (1995) Biosynthesis and function of modified nucleosides. In: TRNA: Structure, Biosynthesis and Function (eds D. Söll & U.L. RajBhandary), pp. 165-205. Washington DC: ASM Press.
6. Björk, G.R., Kerstin, J., Nilsson, K., Johansson, M.J.O., Byström, A.S. & Persson, O.P. (2001) A primordial tRNA modification required for the evolution of life? EMBO J. 20, 231-239.
7. Björk, G.R., Wikstrom, P.M. & Byström, A.S. (1989) Prevention of translational frameshifting by the modified nucleoside 1-methylguanosine. Science 244, 986-989.
8. Burggraf, S., Olsen, G.J., Stetter, K.O. & Woese, C.R. (1992) A phylogenetic analysis of Aquifex pyrophilus. Syst. Appl. Microbiol. 15, 353-356.
9. Byström, A.S. & 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.
10. Christian, T. & Hou, Y.M. (2007) Distinct determinants of tRNA recognition by the TrmD and Trm5 methyl transferases. J. Mol. Biol. 373, 623-632.
11. Christian, T., Evilia C., Williams S. & Hou Y.M. (2004) Distinct origins of tRNA (m1G37) methyltransferase. J. Mol. Biol. 339, 707-719.
12. Clark, D.J., Hill, C., Martin, S.R. & Thomas, J.O. (1988) α-helix in the carboxy-terminal domains of histones H1 and H5. EMBO J. 7, 69-75.
13. Deckert, G., Warren, P.V., Gaasterland, T., Young, W.G., Lenox, A.L., Graham, D.E., Overbeek, R., Snead, M.A., Keller, M., Aujay, M., Huber, R., Feldman, R.A., Short, J.M., Olsen, G.J. & Swanson, R.V. (1998) The complete genome of the hyperthermophilic bacterium Aquifex aeolicus. Nature 392, 353-358.
14. Droogmans, L. & Grosjean, H. (1987) Enzymatic conversion of guanosine 3′ adjacent to the anticodon of yeast tRNAPhe to N1-methylguanosine and the Wye nucleoside: Dependence on the anticodon sequence. EMBO J. 6, 477-483.
15. Dunin-Horkawicsz, S., Czerwoniec, A., Gajda, M.J., Feder, M., Grosjean, H. & Bujnicki, J.M. (2006) MODOMICS: A database of RNA modification pathways. Nucleic Acids Res. 34, D145-D149.
16. Elkins, P.A., Watts, J.M., Zalacain, M., van, Thiel, A., Vitazka, P.R., Redlak, M., Andraos-Selim, C., Rastinejad, F. & Holmes, W.M. (2003) Insights into catalysis by a knotted TrmD tRNA methyltransferase. J. Mol. Biol. 333, 931-949.
17. Farabaugh, P.J. & Björk, G.R. (1999) How translational accuracy influences reading frame maintenance. EMBO J. 18, 1427-1434.
18. Garcia, G.R. & Goodenough-Lashhua, D.M. (1998) Appendix 3: General properties of RNA-modifying and -editing enzymes. In: Modification and Editing of RNA (eds H. Grosjean & R. Benne), pp. 555-560. Washington DC: ASM Press.
19. Gouet, P., Courcelle, E., Stuart, D.I. & Métoz, F. (1999) ESPript: Analysis of multiple sequence alignments in PostScript. Bioinformatics 15, 305-308.
20. Greenfield, N.J. (1996) Methods to estimate the conformation of proteins and polypeptides from circular dichroism data. Analytical Biochem. 235, 1-10.
21. Grosjean, H. (2005) Modification and editing of RNA: Historical overview and important facts to remember. In: Fine-Tuning of RNA Functions by Modification and Editing (ed. H. Grosjean), pp. 1-22. Berlin: Springer-Verlag.
22. Grosjean, H., Droogmans, L., Roovers, M. & Keith, G. (2007) Detection of enzymatic activity of transfer RNA modification enzymes using radiolabeled tRNA substrates. In: Methods in Enzymology vol. 425 RNA modification (ed. J.M. Gott), pp. 57-102. Amsterdam: Elsevier.
23. Hagervall, T.G., Tuohy, T.M.F., Atkins, J.F. & Björk, G.R. (1993) Deficiency of 1-methylguanosine in tRNA from Salmonella typhimurium induces frameshifting by quadruplet translocation. J. Mol. Biol. 232, 756-765.
24. Henne, A., Brüggemann, H., Raasch, C. et al. (2004) The genome sequence of the extreme thermophile Thermus thermophilus. Nat. Biotechnol. 22, 547-553.
25. Hori, H., Kubota, S., Watanabe, K., Kim, J.M., Ogasawara, T., Sawasaki, T. & Endo, Y. (2003) Aquifex aeolicus tRNA (Gm18) methyltransferase has unique substrate specificity. tRNA recognition mechanism of the enzyme. J. Biol. Chem. 278, 25081-25090.
26. Hori, H., Suzuki, T., Sugawara, K., Inoue, Y., Shibata, T., Kuramitsu, S., Yokoyama, S., Oshima, T. & 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.
27. Kimball, M.E., Szeto, K.S. & Söll, D. (1974) The nucleotide sequence of phenylalanine tRNA from Mycoplasma sp. (Kid). Nucleic Acids Res. 1, 1721-1732.
28. Lee, C., Kramer, G., Graham, D.E. & 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.
29. Liu, J., Wang, W., Shin, D.H., Yokota, H., Kim, R. & Kim, S.H. (2003) Crystal structure of tRNA (m1G37) methyltransferase from Aquifex aeolicus at 2.6.Åresolution: A novel methyltransferase fold. Proteins 53, 326-328.
30. Noma, A., Kirino, Y., Ikeuchi, Y. & Suzuki, T. (2006) Biosynthesis of wybutosine, a hyper-modified nucleoside in eukaryotic phenylalanine tRNA. EMBO J. 25, 2142-2154.
31. 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. & Yokoyama, S. (2002) An enzyme with a deep trefoil knot for the active-site architecture. Acta Crystallogr. D Biol. Crystallogr. 58, 1129-1137.
32. Nureki, O., Watanabe, K., Fukai, S., Ishii, R., Endo, Y., Hori, H. & Yokoyama, S. (2004) Deep knot structure for construction of active site and cofactor binding site of tRNA modification enzyme. Structure 12, 593-602.
33. O'Dwyer, K., Watts, J.M., Biswas, S., Ambrad, J., Barber, M., Brulé, H., Petit, C., Holmes, D.J., Zalacain, M. & Holmes, W.M. (2004) Characterization of Streptococcus pneumoniae TrmD, a tRNA methyltransferase essential for growth. J. Bacteriol. 186, 2346-2354.
34. Okamoto, H., Watanabe, K., Ikeuchi, Y., Suzuki, T., Endo, Y. & Hori, H. (2004) Substrate tRNA recognition mechanism of tRNA (m7G46) methyltransferase from Aquifex aeolicus. J. Biol. Chem. 279, 49151-49159.
35. Osorio-Almeida, M.L., Guillemaut, P., Keith, G., Canaday, J. & Weil, J.H. (1980) Primary structure of three leucine transfer RNAs from bean chloroplast. Biochem. Biophys. Res. Commun. 92, 102-108.
36. Pedone, E., D'Ambrosio, K., De Simone, G., Rossi, M., Pedone, C. & Bartolucci, S. (2006) Insights on a new PDI-like family: Structural and functional analysis of a protein disulfide oxidoreductase from the bacterium Aquifex aeolicus. J. Mol. Biol. 356, 155-164.
37. Persson, B.C., Jager, G. & 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, 4093-4097.
38. Roovers, M., Wouters, J., Bujnicki, J.M., Tricot, C., Stalon, V., Grosjean, H. & Droogmans, L. (2004) A primordial RNA modification enzyme: The case of tRNA (m1A) methyltransferase. Nucleic Acids Res. 32, 465-476.
39. Rozenski, J., Crain, P.F. & McCloskey, J.A. (1999) The RNA Modification Database: 1999 update. Nucleic Acids Res. 27, 196-197.
40. Schubert, H.G., Blumenthal, R.M. & Cheng, X. (2003) Many paths to methyltransfer: A chronicle of convergence. Trends Biochem Sci. 28, 329-335.
41. Sprinzl, M., Horn, C., Brown, M., Ioudovitch, A. & Steinberg, S. (1998) Compilation of tRNA sequences and sequences of tRNA genes. Nucleic Acids Res. 26, 148-153.
42. Suzuki, Y., Noma, A., Suzuki, T., Senda, M., Senda, T., Ishitani, R. & Nureki, O. (2007) Crystal structure of the radical SAM enzyme catalyzing tricyclic modified base formation in tRNA. J. Mol. Biol. 372, 1204-1214.
43. Takeda, H., Toyooka, T., Ikeuchi, Y., Yokobori, S., Okadome, K., Takano, F., Oshima, T., Suzuki, T., Endo, Y. & Hori, H. (2006) The substrate specificity of tRNA (m1G37) methyltransferase (TrmD) from Aquifex aeolicus. Genes Cells 11, 1353-1365.
44. Thompson, J.D., Higgins, D.G. & Gibson, T.J. (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.
45. Tkaczuk, K.L., Dunin-Horkawicz, S., Purta, E. & Bujnicki, J.M. (2007) Structural and evolutionary bioinformatics of the SPOUT superfamily of methyltransferases. BMC Bioinformatics 8, 73.
46. Tomikawa, C., Ochi, A. & Hori, H. (2008) The C-terminal region of thermophilic tRNA (m7G46) methyltransferase (TrmB) stabilizes the dimer structure and enhances fidelity of methylation. Proteins 71, 1400-1408.
47. Watanabe, K., Nureki, O., Fukai, S., Endo, Y. & Hori, H. (2006) Functional categorization of the conserved basic amino acid residues in TrmH (tRNA (Gm18) methyltransferase) enzymes. J. Biol. Chem. 281, 34630-34639.
48. Watanabe, K., Nureki, O., Fukai, S., Ishii, R., Okamoto, H., Yokoyama, S., Endo, Y. & Hori, H. (2005) Roles of conserved amino acid sequence motifs in the SpoU (TrmH) RNA methyltransferase family. J. Biol. Chem. 280, 10368-10377.