Ligand-mediated anticodon conformational changes occur during tRNA methylation by a TrmD methyltransferase

Biochemistry

Volumn 44, Issue 17, 2005, Pages 6629-6639

  Watts, Joseph M ^a   Gabruzsk, J ^b   Holmes, Walter M ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^b MERCK RESEARCH LABORATORIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATALYSIS; CONFORMATIONS; ENERGY TRANSFER; ESCHERICHIA COLI; FLUORESCENCE; RNA;

ANTICODON CONFORMATION; FLUORESCENCE ENERGY TRANSFER; PHOSPHODIESTERS;

BIOCHEMISTRY;

METHYLTRANSFERASE; RNA;

ANTICODON; ARTICLE; CATALYSIS; CONTROLLED STUDY; ENERGY TRANSFER; ESCHERICHIA COLI; FLUORESCENCE; LIGAND BINDING; METHYLATION; NONHUMAN; PRIORITY JOURNAL; RNA BINDING; RNA METHYLATION; RNA SYNTHESIS; STREPTOCOCCUS PNEUMONIAE; SUBSTITUTION REACTION;

ADENOSINE; AMINO ACID SEQUENCE; ANTICODON; BASE SEQUENCE; ESCHERICHIA COLI PROTEINS; FLUORESCENCE RESONANCE ENERGY TRANSFER; LIGANDS; METHYLATION; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; PROTEIN CONFORMATION; PROTEIN FOOTPRINTING; RNA, TRANSFER, LEU; RNA-BINDING PROTEINS; S-ADENOSYLMETHIONINE; SEQUENCE ALIGNMENT; THERMOTOGA MARITIMA; TRNA METHYLTRANSFERASES;

ESCHERICHIA COLI; STREPTOCOCCUS PNEUMONIAE;

EID: 17844369412     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi0481038     Document Type: Article

References (48)

1. Bystrom, A. S., and Bjork, 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, 440-6.
2. Holmes, W. M., Andraos-Selim, C., Roberts, I., and Wahab, S. Z. (1992) Structural requirements for tRNA methylation. Action of Escherichia coli tRNA(guanosine-1)methyltransferase on tRNA-(1leu) structural variants, J. Biol. Chem. 267, 13440-5.
3. Brule, 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, 9243-55.
4. 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, 931-49.
5. Bjork, G. R., Wikstrom, P. M., and Bystrom, A. S. (1989) Prevention of translational frameshifting by the modified nucleoside 1-methylguanosine, Science 244, 986-9.
6. O'Dwyer, K., Watts, J. M., Biswas, S., Ambrad, J., Barber, M., Brule, H., Petit, C., Holmes, D. J., Zalacain, M., and Holmes, W. M. (2004) Characterization of Streptococcus pneumoniae trmd, a tRNA methyltransferase essential for growth, J. Bacteriol. 186, 2346-54.
7. Bjork, G. R., Jacobsson, K., Nilsson, K., Johansson, M. J., Bystrom, A. S., and Persson, O. P. (2001) A primordial tRNA modification required for the evolution of life? EMBO J. 20, 231-9.
8. Persson, B. C., Bylund, G. O., Berg, D. E., and Wikstrom, P. M. (1995) Functional analysis of the ffh-trmd region of the Escherichia coli chromosome by using reverse genetics, J. Bacteriol. 177, 5554-60.
9. Kobayashi, K., Ehrlich, S. D., Albertini, A., Amati, G., Andersen, K. K., Arnaud, M., Asai, K., Ashikaga, S., Aymerich, S., Bessieres, P., Boland, F., Brignell, S. C., Bron, S., Bunai, K., Chapuis, J., Christiansen, L. C., Danchin, A., Debarbouille, M., Dervyn, E., Deuerling, E., Devine, K., Devine, S. K., Dreesen, O., Errington, J., Fillinger, S., Foster, S. J., Fujita, Y., Galizzi, A., Gardan, R., Eschevins, C., Fukushima, T., Haga, K., Harwood, C. R., Hecker, M., Hosoya, D., Hullo, M. F., Kakeshita, H., Karamata, D., Kasahara, Y., Kawamura, F., Koga, K., Koski, P., Kuwana, R., Imamura, D., Ishimaru, M., Ishikawa, S., Ishio, I., Le Coq, D., Masson, A., Mauel, C., Meima, R., Mellado, R. P., Moir, A., Moriya, S., Nagakawa, E., Nanamiya, H., Nakai, S., Nygaard, P., Ogura, M., Ohanan, T., O'Reilly, M., O'Rourke, M., Pragai, Z., Pooley, H. M., Rapoport, G., Rawlins, J. P., Rivas, L. A., Rivolta, C., Sadaie, A., Sadaie, Y., Sarvas, M., Sato, T., Saxild, H. H., Scanlan, E., Schumann, W., Seegers, J. F., Sekiguchi, J., Sekowska, A., Seror, S. J., Simon, M., Stragier, P., Studer, R., Takamatsu, H., Tanaka, T., Takeuchi, M., Thomaides, H. B., Vagner, V., van Dijl, J. M., Watabe, K., Wipat, A., Yamamoto, H., Yamamoto, M., Yamamoto, Y., Yamane, K., Yata, K., Yoshida, K., Yoshikawa, H., Zuber, U., and Ogasawara, N. (2003) Essential Bacillus subtilis genes, Proc. Natl. Acad. Sci. U.S.A. 100, 4678-83.
10. Gabryszuk, J., and Holmes, W. M. (1997) TRNA recognition for modification: solution probing of tRNA complexed with Escherichia coli tRNA (guanosine-1) methyltransferase, Rna 3, 1327-36.
11. Robertus, J. D., Ladner, J. E., Finch, J. T., Rhodes, D., Brown, R. S., Clark, B. P., and Klug, A. (1974) Structure of yeast phenylalanine tRNA at 3 Å resolution, Nature 250, 546-51.
12. Jack, A., Ladner, J. E., and Klug, A. (1976) Crystallographic refinement of yeast phenylalanine transfer RNA at 2-5 Å resolution, J. Mol. Biol. 108, 619-49.
13. Hingerty, B., Brown, R. S., and Jack, A. (1978) Further refinement of the structure of yeast tRNAphe, J. Mol. Biol. 124, 523-34.
14. Klimasauskas, S., Kumar, S., Roberts, R. J., and Cheng, X. (1994) Hhai methyltransferase flips its target base out of the DNA helix, Cell 76, 357-69.
15. Shi, H., and Moore, P. B. (2000) The crystal structure of yeast phenylalanine tRNA at 1.93 Å resolution: a classic structure revisited, RNA 6, 1091-105.
16. Stuart, J. W., Gdaniec, Z., Guenther, R., Marszalek, M., Sochacka, E., Malkiewicz, A., and Agris, P. F. (2000) Functional anticodon architecture of human tRNAlys3 includes disruption of intraloop hydrogen bonding by the naturally occurring amino acid modification, t6a, Biochemistry 39, 13396-404.
17. Cabello-Villegas, J., Winkler, M. E., and Nikonowicz, E. P. (2002) Solution conformations of unmodified and a(37)n(6)-dimethylallyl modified anticodon stem-loops of Escherichia coli tRNA(phe), J. Mol. Biol. 319, 1015-34.
18. Yarian, C. S., Basti, M. M., Cain, R. J., Ansari, G., Guenther, R. H., Sochacka, E., Czerwinska, G., Malkiewicz, A., and Agris, P. F. (1999) Structural and functional roles of the n1- and n3-protons of psi at tRNA's position 39, Nucleic Acids Res. 27, 3543-9.
19. Adamiak, D. A., Rypniewski, W. R., Milecki, J., and Adamiak, R. W. (2001) The 1.19 Å X-ray structure of 2′-o-me(cgcgcg)(2) duplex shows dehydrated RNA with 2-methyl-2,4-pentanediol in the minor groove, Nucleic Acids Res. 29, 4144-53.
20. Yap, L. P., and Musier-Forsyth, K. (1995) Transfer RNA aminoacylation: identification of a critical ribose 2′-hydroxyl-base interaction, RNA 1, 418-24.
21. Micura, R., Pils, W., Hobartner, C., Grubmayr, K., Ebert, M. O., and Jaun, B. (2001) Methylation of the nucleobases in RNA oligonucleotides mediates duplex-hairpin conversion, Nucleic Acids Res. 29, 3997-4005.
22. Stuart, J. W., Koshlap, K. M., Guenther, R., and Agris, P. F. (2003) Naturally-occurring modification restricts the anticodon domain conformational space of tRNA(phe), J. Mol. Biol. 334, 901-18.
23. Bjork, G. R., Ericson, J. U., Gustafsson, C. E., Hagervall, T. G., Jonsson, Y. H., and Wikstrom, P. M. (1987) Transfer RNA modification, Annu. Rev. Biochem. 56, 263-87.
24. Nissen, P., Kjeldgaard, M., Thirup, S., Polekhina, G., Reshetnikova, L., Clark, B. P., and Nyborg, J. (1995) Crystal structure of the ternary complex of phe-tRNAphe, ef-tu, and a gtp analog. Science 270, 1464-72.
25. Cabello-Villegas, J., Tworowska, I., and Nikonowicz, E. P. (2004) Metal ion stabilization of the u-turn of the a37 n6-dimethylallyl-modified anticodon stem-loop of Escherichia coli tRNAphe, Biochemistry 43, 55-66.
26. Hoang, C., and Ferre-D'Amare, A. R. (2001) Cocrystal structure of a tRNA psi55 pseudouridine synthase: nucleotide flipping by an RNA-modifying enzym, Cell 107, 929-39.
27. 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, 383-94.
28. Ward, D. C., Reich, E., and Stryer, L. (1969) Fluorescence studies of nucleotides and polynucleotides. I. Formycin, 2-aminopurine riboside, 2,6-diaminopurine riboside, and their derivatives, J. Biol. Chem. 244, 1228-37.
29. Holz, B., Klimasauskas, S., Serva, S., and Weinhold, E. (1998) 2-Aminopurine as a fluorescent probe for DNA base flipping by methyltransferases, Nucleic Acids Res. 26, 1076-83.
30. Cheng, X., and Blumenthal, R. M., Eds. (1999) S-Adenosylmethionine- Dependent Methyltrasferases: Structures and Functions, World Scientific Pub Co., River, Edge, NJ.
31. Cheng, X., and Roberts, R. J. (2001) Adomet-dependent methylation, DNA methyltransferases and base flipping, Nucleic Acids Res. 29, 3784-95.
32. Guest, C. R., Hochstrasser, R. A., Sowers, L. C., and Millar, D. P. (1991) Dynamics of mismatched base pairs in DNA, Biochemistry 30, 3271-9.
33. Xu, D., Evans, K. O., and Nordlund, T. M. (1994) Melting and premelting transitions of an oligomer measured by DNA base fluorescence and absorption, Biochemistry 33, 9592-9.
34. Christine, K. S., MacFarlane, A. W. T., Yang, K., and Stanley, R. J. (2002) Cyclobutylpyrimidine dimer base flipping by DNA photolyase, J. Biol. Chem. 277, 38339-44.
35. Selvin, P. R. (2000) The renaissance of fluorescence resonance energy transfer, Nat. Struct. Biol. 7, 730-4.
36. Redlak, M., Andraos-Selim, C., Giege, R., Florentz, C., and Holmes, W. M. (1997) Interaction of tRNA with tRNA (guanosine-1)methyltransferase: binding specificity determinants involve the dinucleotide g36pg37 and tertiary structure, Biochemistry 36, 8699-709.
37. Altschul, S. F., Gish, W., Miller, W., Myers, E. W., and Lipman, D. J. (1990) Basic local alignment search too, J. Mol. Biol. 215, 403-10.
38. Clarke, P. (1999) Labeling and purification of RNA synthesized by in vitro transcription, in Rna-Protein Interaction Protocols (Haynes, S., Ed.) pp 1 -10, Humana Press, Inc., Totowa, NJ.
39. Silberklang, M., Prochiantz, A., Haenni, A. L., and Rajbhandary, U. L. (1977) Studies on the sequence of the 3′-terminal region of turnip-yellow-mosaic-virus RNA, Eur. J. Biochem. 72, 465-78.
40. Setzer, D. R. (1999) Measuring equilibrium and kinetic constants using gel retardation assays, Methods Mol. Biol. 118, 115-28.
41. Sybyl, version 6.8, Tripos Inc., St. Louis, MO, .
42. Brickmann, J. G. T., Heiden, W., and Waldherr-Techner, M. (1992) Examining and manipulating molecular surfaces: generation and manipulation of solid models with the MOLCAD molecular graphics system, J. Mol. Graph. 10, 35.
43. Thompson, J. D., Higgins, D. G., and 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, 4673-80.
44. Valeur, B. (2002) Molecular Fluorescence: Principles and Applications, Wiley-VCH, Weinheim and New York.
45. 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, 2593-603.
46. Schweisguth, D. C., and Moore, P. B. (1997) On the conformation of the anticodon loops of initiator and elongator methionine tRNAs, J. Mol. Biol. 267, 505-19.
47. dos Remedios, C. G., and Moens, P. D. (1995) Fluorescence resonance energy transfer spectroscopy is a reliable "ruler" for measuring structural changes in proteins. Dispelling the problem of the unknown orientation factor, J. Struct. Biol. 115, 175-85.
48. Lakowicz, J. R. (1999) Principles of Fluorescence Spectroscopy, 2nd ed., Kluwer Academic/Plenum, New York.