Crystal Structure of Thermus thermophilus tRNA m1A58 Methyltransferase and Biophysical Characterization of Its Interaction with tRNA

Journal of Molecular Biology

Volumn 377, Issue 2, 2008, Pages 535-550

  Barraud, Pierre ^a   Golinelli Pimpaneau, Béatrice ^b   Atmanene, Cédric ^c   Sanglier, Sarah ^c   Van Dorsselaer, Alain ^c   Droogmans, Louis ^d   Dardel, Frédéric ^a   Tisné, Carine ^a  

^a UNIVERSITÉ PARIS DESCARTES   (France)

^b LABORATOIRE D ENZYMOLOGIE ET BIOCHIMIE STRUCTURALES   (France)

^c INSTITUT DE RECHERCHES SUBATOMIQUES   (France)

^d UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

Author keywords

m1A58 methyltransferase; noncovalent mass spectrometry; protein RNA interactions; TrmI; X ray structure

Indexed keywords

METHYLTRANSFERASE; TETRAMER; TRANSFER RNA;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; CATALYSIS; CONTROLLED STUDY; CRYSTAL STRUCTURE; ELECTROSPRAY MASS SPECTROMETRY; METHYLATION; MUTAGENESIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN RNA BINDING; THERMUS THERMOPHILUS;

MYCOBACTERIUM TUBERCULOSIS; THERMUS THERMOPHILUS;

EID: 40049103631     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2008.01.041     Document Type: Article

References (63)

1. J. Rozenski P.F. Crain J.A. McCloskey The RNA Modification Database: 1999 update Nucleic Acids Res. 27 1999 196 197
2. J. Anderson L. Phan A.G. Hinnebusch The Gcd10p/Gcd14p complex is the essential two-subunit tRNA(1-methyladenosine) methyltransferase of Saccharomyces cerevisiae Proc. Natl Acad. Sci. USA 97 2000 5173 5178
3. L. Droogmans M. Roovers J.M. Bujnicki C. Tricot T. Hartsch V. Stalon H. Grosjean Cloning and characterization of tRNA (m1A58) methyltransferase (TrmI) from Thermus thermophilus HB27, a protein required for cell growth at extreme temperatures Nucleic Acids Res. 31 2003 2148 2156
4. J. Anderson L. Phan R. Cuesta B.A. Carlson M. Pak K. Asano The essential Gcd10p–Gcd14p nuclear complex is required for 1-methyladenosine modification and maturation of initiator methionyl-tRNA Genes Dev. 12 1998 3650 3662
5. S.G. Ozanick J.M. Bujnicki D.S. Sem J.T. Anderson Conserved amino acids in each subunit of the heteroligomeric tRNA m1A58 MTase from Saccharomyces cerevisiae contribute to tRNA binding Nucleic Acids Res. 35 2007 6808 6819
6. J.M. Bujnicki In silico analysis of the tRNA:m1A58 methyltransferase family: homology-based fold prediction and identification of new members from Eubacteria and Archaea FEBS Lett. 507 2001 123 127
7. A. Gupta P.H. Kumar T.K. Dineshkumar U. Varshney H.S. Subramanya Crystal structure of Rv2118c: an AdoMet-dependent methyltransferase from Mycobacterium tuberculosis H37Rv J. Mol. Biol. 312 2001 381 391
8. M. Roovers J. Wouters J.M. Bujnicki C. Tricot V. Stalon H. Grosjean L. Droogmans A primordial RNA modification enzyme: the case of tRNA (m1A) methyltransferase Nucleic Acids Res. 32 2004 465 476
9. 58 tRNA methyltransferase Nucleic Acids Res. 32 2004 1018 1027
10. H.L. Schubert R.M. Blumenthal X. Cheng Many paths to methyltransfer: a chronicle of convergence Trends Biochem. Sci. 28 2003 329 335
11. J.A. Loo Studying noncovalent protein complexes by electrospray ionization mass spectrometry Mass Spectrom. Rev. 16 1997 1 23
12. J.A. Loo Electrospray ionization mass spectrometry: a technology for studying noncovalent macromolecular complexes Int. J. Mass Spectrom. 200 2000 175 186
13. A.J. Heck R.H. Van Den Heuvel Investigation of intact protein complexes by mass spectrometry Mass Spectrom. Rev. 23 2004 368 389
14. T.D. Veenstra Electrospray ionization mass spectrometry: a promising new technique in the study of protein/DNA noncovalent complexes Biochem. Biophys. Res. Commun. 257 1999 1 5
15. J.L. Beck M.L. Colgrave S.F. Ralph M.M. Sheil Electrospray ionization mass spectrometry of oligonucleotide complexes with drugs, metals, and proteins Mass Spectrom. Rev. 20 2001 61 87
16. S.A. Hofstadler R.H. Griffey Analysis of noncovalent complexes of DNA and RNA by mass spectrometry Chem. Rev. 101 2001 377 390
17. F. Rusconi F. Guillonneau D. Praseuth Contributions of mass spectrometry in the study of nucleic acid-binding proteins and of nucleic acid–protein interactions Mass Spectrom. Rev. 21 2002 305 348
18. C.V. Robinson E.W. Chung B.B. Kragelund J. Knudsen R.T. Aplin F.M. Poulsen C.M. Dobson Probing the nature of noncovalent interactions by mass spectrometry. A study of protein–CoA ligand binding and assembly J. Am. Chem. Soc. 118 1996 8646 8653
19. H. Rogniaux A. Van Dorsselaer P. Barth J.F. Biellmann J. Barbanton M. van Zandt Binding of aldose reductase inhibitors: correlation of crystallographic and mass spectrometric studies J. Am. Soc. Mass Spectrom. 10 1999 635 647
20. H.Y. Mei D.P. Mack A.A. Galan N.S. Halim A. Heldsinger J.A. Loo Discovery of selective, small-molecule inhibitors of RNA complexes: I. The Tat protein/TAR RNA complexes required for HIV-1 transcription Bioorg. Med. Chem. 5 1997 1173 1184
21. C. Liu L.P. Tolic S.A. Hofstadler A.C. Harms R.D. Smith C. Kang N. Sinha Probing RegA/RNA interactions using electrospray ionization-Fourier transform ion cyclotron resonance-mass spectrometry Anal. Biochem. 262 1998 67 76
22. N. Potier L.J. Donald I. Chernushevich A. Ayed W. Ens C.H. Arrowsmith Study of a noncovalent trp repressor: DNA operator complex by electrospray ionization time-of-flight mass spectrometry Protein Sci. 7 1998 1388 1395
23. N. Hagan D. Fabris Direct mass spectrometric determination of the stoichiometry and binding affinity of the complexes between nucleocapsid protein and RNA stem–loop hairpins of the HIV-1 Psi-recognition element Biochemistry 42 2003 10736 10745
24. T. Kilic S. Sanglier A. Van Dorsselaer D. Suck Oligomerization behavior of the archaeal Sm2-type protein from Archaeoglobus fulgidus Protein Sci. 15 2006 2310 2317
25. S. Hamilton J. Odili M.D. Pacifico G.D. Wilson J.M. Kupsch Effect of imidazole on the solubility of a His-tagged antibody fragment Hybrid. Hybridomics 22 2003 347 355
26. A.J. McCoy R.W. Grosse-Kunstleve L.C. Storoni R.J. Read Likelihood-enhanced fast translation functions Acta Crystallogr. Sect. D 61 2005 458 464
27. G. Schluckebier M. O'Gara W. Saenger X. Cheng Universal catalytic domain structure of AdoMet-dependent methyltransferases J. Mol. Biol. 247 1995 16 20
28. E.B. Fauman R.M. Blumenthal X. Cheng Structure and evolution of AdoMet-dependent methyltransferases X. Cheng R.M. Blumenthal S -Adenosylmethionine-Dependent Methyltransferases: Structures and Functions 1999 World Scientific Publishing Singapore 1 38
29. N.A. Baker D. Sept S. Joseph M.J. Holst J.A. McCammon Electrostatics of nanosystems: application to microtubules and the ribosome Proc. Natl Acad. Sci. USA 98 2001 10037 10041
30. A.A. Rostom C.V. Robinson Detection of the intact GroEL chaperonin assembly by mass spectrometry J. Am. Chem. Soc. 121 1999 4718 4719
31. W.J. van Berkel R.H. van den Heuvel C. Versluis A.J. Heck Detection of intact megadalton protein assemblies of vanillyl-alcohol oxidase by mass spectrometry Protein Sci. 9 2000 435 439
32. S. Sanglier H. Ramstrom J. Haiech E. Leize A. Van Dorsselaer Electrospray ionization mass spectrometry analysis revealed a similar to 310 kDa noncovalent hexamer of HPr kinase/phosphatase from Bacillus subtilis Int. J. Mass Spectrom. 219 2002 681 696
33. S. Sanglier E. Leize A. Van Dorsselaer F. Zal Comparative ESI-MS study of approximately 2.2 MDa native hemocyanins from deep-sea and shore crabs: from protein oligomeric state to biotope J. Am. Soc. Mass Spectrom. 14 2003 419 429
34. H. Rogniaux S. Sanglier K. Strupat S. Azza O. Roitel V. Ball Mass spectrometry as a novel approach to probe cooperativity in multimeric enzymatic systems Anal. Biochem. 291 2001 48 61
35. R.D. Smith K.J. Light-Wahl The observation of non-covalent interactions in solution by electrospray ionization mass spectrometry: promise, pitfalls and prognosis Biol. Mass Spectrom. 22 1993 493 501
36. A. Kapur J.L. Beck S.E. Brown N.E. Dixon M.M. Sheil Use of electrospray ionization mass spectrometry to study binding interactions between a replication terminator protein and DNA Protein Sci. 11 2002 147 157
37. R. Gupta S.M. Hamdan N.E. Dixon M.M. Sheil J.L. Beck Application of electrospray ionization mass spectrometry to study the hydrophobic interaction between the epsilon and theta subunits of DNA polymerase III Protein Sci. 13 2004 2878 2887
38. L.A. Cassiday L.L. Lebruska L.M. Benson S. Naylor W.G. Owen L.J. Maher III Binding stoichiometry of an RNA aptamer and its transcription factor target Anal. Biochem. 306 2002 290 297
39. C. Dominguez R. Boelens A.M. Bonvin HADDOCK: a protein–protein docking approach based on biochemical or biophysical information J. Am. Chem. Soc. 125 2003 1731 1737
40. A.A. McCarthy J.G. McCarthy The structure of two N -methyltransferases from the caffeine biosynthetic pathway Plant Physiol. 144 2007 879 889
41. A. Kettani M. Gueron J.L. Leroy Amino proton exchange processes in mononucleosides J. Am. Chem. Soc. 119 1997 1108 1115
42. R. Stewart M.G. Harris Amino group acidity in nucleotide bases Can. J. Chem. 55 1977 3807 3814
43. P.A. Elkins J.M. Watts M. Zalacain A. van Thiel P.R. Vitazka M. Redlak Insights into catalysis by a knotted TrmD tRNA methyltransferase J. Mol. Biol. 333 2003 931 949
44. J. Labahn J. Granzin G. Schluckebier D.P. Robinson W.E. Jack I. Schildkraut W. Saenger Three-dimensional structure of the adenine-specific DNA methyltransferase M• Taq I in complex with the cofactor S -adenosylmethionine Proc. Natl Acad. Sci. USA 91 1994 10957 10961
45. P.H. Tran Z.R. Korszun S. Cerritelli S.S. Springhorn S.A. Lacks Crystal structure of the DpnM DNA adenine methyltransferase from the DpnII restriction system of Streptococcus pneumoniae bound to S -adenosylmethionine Structure 6 1998 1563 1575
46. 6-adenine DNA methyltransferase M• Taq I in complex with DNA and a cofactor analog Nat. Struct. Biol. 8 2001 121 125
47. G. Schluckebier P. Zhong K.D. Stewart T.J. Kavanaugh C. Abad-Zapatero The 2.2 A structure of the rRNA methyltransferase ErmC′ and its complexes with cofactor and cofactor analogs: implications for the reaction mechanism J. Mol. Biol. 289 1999 277 291
48. G. Maravic M. Feder S. Pongor M. Flogel J.M. Bujnicki Mutational analysis defines the roles of conserved amino acid residues in the predicted catalytic pocket of the rRNA:m6A methyltransferase ErmC′ J. Mol. Biol. 332 2003 99 109
49. S. Bheemanaik Y.V. Reddy D.N. Rao Structure, function and mechanism of exocyclic DNA methyltransferases Biochem. J. 399 2006 177 190
50. A. Jeltsch Beyond Watson and Crick: DNA methylation and molecular enzymology of DNA methyltransferases ChemBioChem 3 2002 274 293
51. 6-adenine DNA methyltransferase from Thermus aquaticus Biochemistry 38 1999 1426 1434
52. 6-methyltransferase J. Biol. Chem. 273 1998 17333 17342
53. Collaborative Computational Project Number 4 The CCP4 suite: programs for protein crystallography Acta Crystallogr. Sect. D 50 1994 760 763
54. E. Potterton P. Briggs M. Turkenburg E. Dodson A graphical user interface to the CCP4 program suite Acta Crystallogr. Sect. D 59 2003 1131 1137
55. + ESF–EAMCB Newsletter on Protein Crystallography 1992 Daresbury Laboratory Warrington, UK
56. P.R. Evans Proceedings of the CCP4 Study Weekend: Data Collection and Processing 1993 Science and Engineering Research Council, Daresbury Laboratory Warrington, UK
57. A. Perrakis R. Morris V.S. Lamzin Automated protein model building combined with iterative structure refinement Nat. Struct. Biol. 6 1999 458 463
58. G.N. Murshudov A.A. Vagin E.J. Dodson Refinement of macromolecular structures by the maximum-likelihood method Acta Crystallogr. Sect. D 53 1997 240 255
59. P. Emsley K. Cowtan Coot: model-building tools for molecular graphics Acta Crystallogr. Sect. D 60 2004 2126 2132
60. M.D. Winn M.N. Isupov G.N. Murshudov Use of TLS parameters to model anisotropic displacements in macromolecular refinement Acta Crystallogr. Sect. D 57 2001 122 133
61. T. Meinnel S. Blanquet Maturation of pre-tRNA(fMet) by Escherichia coli RNase P is specified by a guanosine of the 5′-flanking sequence J. Biol. Chem. 270 1995 15908 15914
62. F. Dardel MC-Fit: using Monte-Carlo methods to get accurate confidence limits on enzyme parameters Comput. Appl. Biosci. 10 1994 273 275
63. A.T. Brunger P.D. Adams G.M. Clore W.L. DeLano P. Gros R.W. Grosse-Kunstleve Crystallography and NMR system: a new software suite for macromolecular structure determination Acta Crystallogr. Sect. D 54 1998 905 921