A catalytic intermediate and several flavin redox states stabilized by folate-dependent tRNA methyltransferase from bacillus subtilis

Biochemistry

Volumn 50, Issue 23, 2011, Pages 5208-5219

  Hamdane, Djemel ^a   Guérineau, Vincent ^b   Un, Sun ^c   Golinelli Pimpaneau, Béatrice ^a  

^a LABORATOIRE D ENZYMOLOGIE ET BIOCHIMIE STRUCTURALES   (France)

^b CNRS   (France)

^c DIF   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ACID TREATMENTS; AIR-STABLE; ANAEROBIC CONDITIONS; ANAEROBIC TITRATION; BACILLUS SUBTILIS; BOUND MOLECULES; CATALYTIC INTERMEDIATES; DOUBLE-RESONANCE SPECTROSCOPY; HIGH-FIELD; KINETIC TRAPPING; MASS SPECTROMETRY ANALYSIS; METHYLENE DONOR; METHYLTRANSFERASES; PURIFIED ENZYME; REDOX STATE; SPECTROSCOPIC STUDIES; THERMODYNAMIC STABILIZATION;

ALKYLATION; BACILLI; BACTERIOLOGY; ENZYME ACTIVITY; KETONES; MASS SPECTROMETRY; METHYLATION; PARAMAGNETIC RESONANCE; PARAMAGNETISM; PHENOLS; PURIFICATION; RESONANCE; SPECTROSCOPIC ANALYSIS;

REACTION INTERMEDIATES;

FOLIC ACID; FORMALDEHYDE; OXYGEN; QUERCETIN; TRANSFER RNA METHYLTRANSFERASE;

ARTICLE; BACILLUS SUBTILIS; CATALYSIS; MASS SPECTROMETRY; OXIDATION REDUCTION STATE; PRIORITY JOURNAL; RNA METHYLATION; STOICHIOMETRY;

BACILLUS SUBTILIS; BINDING SITES; CATALYSIS; ELECTRON SPIN RESONANCE SPECTROSCOPY; FLAVIN-ADENINE DINUCLEOTIDE; FOLIC ACID; KINETICS; OXIDATION-REDUCTION; RNA, TRANSFER; SPECTROMETRY, FLUORESCENCE; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; THERMODYNAMICS; TRNA METHYLTRANSFERASES;

BACILLUS SUBTILIS;

EID: 79958787896     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi1019463     Document Type: Article

References (44)

1. Motorin, Y. and Helm, M. (2010) tRNA stabilization by modified nucleotides Biochemistry 49, 4934-4944
2. Delk, A. S., Nagle, D. P., Jr., Rabinowitz, J. C., and Straub, K. M. (1979) The methylenetetrahydrofolate-mediated biosynthesis of ribothymidine in the transfer-RNA of Streptococcus faecalis: Incorporation of hydrogen from solvent into the methyl moiety Biochem. Biophys. Res. Commun. 86, 244-251 (Pubitemid 9099094)
3. Delk, A. S., Nagle, D. P., Jr., and Rabinowitz, J. C. (1980) Methylenetetrahydrofolate-dependent biosynthesis of ribothymidine in transfer RNA of Streptococcus faecalis. Evidence for reduction of the 1-carbon unit by FADH2 J. Biol. Chem. 255, 4387-4390 (Pubitemid 10060717)
4. 5U methyltransferase in bacteria: Evolutionary implications Nucleic Acids Res. 33, 3955-3964 (Pubitemid 41487256)
5. Nishimasu, H., Ishitani, R., Yamashita, K., Iwashita, C., Hirata, A., Hori, H., and Nureki, O. (2009) Atomic structure of a folate/FAD-dependent tRNA T54 methyltransferase Proc. Natl. Acad. Sci. U.S.A. 106, 8180-8185
6. Payne, G., Heelis, P. F., Rohrs, B. R., and Sancar, A. (1987) The active form of Escherichia coli DNA photolyase contains a fully reduced flavin and not a flavin radical, both in vivo and in vitro Biochemistry 26, 7121-7127
7. Gutierrez, A., Lian, L. Y., Wolf, C. R., Scrutton, N. S., and Roberts, G. C. (2001) Stopped-flow kinetic studies of flavin reduction in human cytochrome P450 reductase and its component domains Biochemistry 40, 1964-1975 (Pubitemid 32165665)
8. Hanley, S. C., Ost, T. W., and Daff, S. (2004) The unusual redox properties of flavocytochrome P450 BM3 flavodoxin domain Biochem. Biophys. Res. Commun. 325, 1418-1423 (Pubitemid 39535919)
9. Mattevi, A. (2006) To be or not to be an oxidase: Challenging the oxygen reactivity of flavoenzymes Trends Biochem. Sci. 31, 276-283 (Pubitemid 43674353)
10. Hamdane, D., Skouloubris, S., Myllykallio, H., and Golinelli-Pimpaneau, B. (2010) Expression and purification of untagged and histidine-tagged folate-dependent tRNA:m(5)U54 methyltransferase from Bacillus subtilis Protein Expression Purif. 73, 83-89
11. Un, S., Dorlet, P., and Rutherford, A. W. (2001) A high-field EPR tour of radicals in photosystems I and II Appl. Magn. Reson. 21, 341-361 (Pubitemid 33571730)
12. Grosjean, H., Droogmans, L., Roovers, M., and Keith, G. (2007) Detection of enzymatic activity of transfer RNA modification enzymes using radiolabeled tRNA substrates Methods Enzymol. 425, 55-101
13. Massey, V. and Palmer, G. (1966) On the existence of spectrally distinct classes of flavoprotein semiquinones. A new method for the quantitative production of flavoprotein semiquinones Biochemistry 5, 3181-3189
14. Okafuji, A., Schnegg, A., Schleicher, E., Mobius, K., and Weber, S. (2008) g-Tensors of the flavin adenine dinucleotide radicals in glucose oxidase: A comparative multifrequency electron paramagnetic resonance and electron-nuclear double resonance study J. Phys. Chem. B 112, 3568-3574
15. +-translocating NADH:quinone oxidoreductase from Vibrio cholerae J. Am. Chem. Soc. 125, 265-275 (Pubitemid 36068663)
16. Schleicher, E., Wenzel, R., Ahmad, M., Batschauer, A., Essen, L. O., Hitomi, K., Getzoff, E. D., Bittl, R., Weber, S., and Okafuji, A. (2010) The Electronic State of Flavoproteins: Investigations with Proton Electron-Nuclear Double Resonance Appl. Magn. Reson. 37, 339-352
17. Kay, C. W., Bittl, R., Bacher, A., Richter, G., and Weber, S. (2005) Unambiguous determination of the g-matrix orientation in a neutral flavin radical by pulsed electron-nuclear double resonance at 94 GHz J. Am. Chem. Soc. 127, 10780-10781 (Pubitemid 41129824)
18. Schleicher, E., Hitomi, K., Kay, C. W., Getzoff, E. D., Todo, T., and Weber, S. (2007) Electron nuclear double resonance differentiates complementary roles for active site histidines in (6-4) photolyase J. Biol. Chem. 282, 4738-4747 (Pubitemid 47100916)
19. Hitomi, K., Kim, S. T., Iwai, S., Harima, N., Otoshi, E., Ikenaga, M., and Todo, T. (1997) Binding and catalytic properties of Xenopus (6-4) photolyase J. Biol. Chem. 272, 32591-32598 (Pubitemid 28011948)
20. Usman, A., Brazard, J., Martin, M. M., Plaza, P., Heijde, M., Zabulon, G., and Bowler, C. (2009) Spectroscopic characterization of a (6-4) photolyase from the green alga Ostreococcus tauri J. Photochem. Photobiol., B 96, 38-48
21. Li, J., Uchida, T., Ohta, T., Todo, T., and Kitagawa, T. (2006) Characteristic structure and environment in FAD cofactor of (6-4) photolyase along function revealed by resonance Raman spectroscopy J. Phys. Chem. B 110, 16724-16732 (Pubitemid 44373402)
22. Bradley, L. H. and Swenson, R. P. (1999) Role of glutamate-59 hydrogen bonded to N(3)H of the flavin mononucleotide cofactor in the modulation of the redox potentials of the Clostridium beijerinckii flavodoxin. Glutamate-59 is not responsible for the pH dependency but contributes to the stabilization of the flavin semiquinone Biochemistry 38, 12377-12386
23. Biskup, T., Schleicher, E., Okafuji, A., Link, G., Hitomi, K., Getzoff, E. D., and Weber, S. (2009) Direct observation of a photoinduced radical pair in a cryptochrome blue-light photoreceptor Angew. Chem., Int. Ed. 48, 404-407
24. Schleicher, E., Bittl, R., and Weber, S. (2009) New roles of flavoproteins in molecular cell biology: Blue-light active flavoproteins studied by electron paramagnetic resonance FEBS J. 276, 4290-4303
25. 2+ Ions in Frozen Aqueous Solutions Appl. Magn. Reson. 37, 247-256
26. Johnson, J. L., Hamm-Alvarez, S., Payne, G., Sancar, G. B., Rajagopalan, K. V., and Sancar, A. (1988) Identification of the second chromophore of Escherichia coli and yeast DNA photolyases as 5,10-methenyltetrahydrofolate Proc. Natl. Acad. Sci. U.S.A. 85, 2046-2050 (Pubitemid 24315825)
27. Scrima, A., Vetter, I. R., Armengod, M. E., and Wittinghofer, A. (2005) The structure of the TrmE GTP-binding protein and its implications for tRNA modification EMBO J. 24, 23-33 (Pubitemid 40188460)
28. Cook, R. J. and Wagner, C. (1986) Purification of rat liver folate-binding protein: Cytosol I Methods Enzymol. 122, 251-255 (Pubitemid 16017514)
29. Schirch, V. and Strong, W. B. (1989) Interaction of folylpolyglutamates with enzymes in one-carbon metabolism Arch. Biochem. Biophys. 269, 371-380 (Pubitemid 19075749)
30. Kim, D. W., Huang, T., Schirch, D., and Schirch, V. (1996) Properties of tetrahydropteroylpentaglutamate bound to 10-formyltetrahydrofolate dehydrogenase Biochemistry 35, 15772-15783 (Pubitemid 26422314)
31. Knighton, D. R., Kan, C. C., Howland, E., Janson, C. A., Hostomska, Z., Welsh, K. M., and Matthews, D. A. (1994) Structure of and kinetic channelling in bifunctional dihydrofolate reductase-thymidylate synthase Nat. Struct. Biol. 1, 186-194 (Pubitemid 24974835)
32. Trujillo, M., Donald, R. G., Roos, D. S., Greene, P. J., and Santi, D. V. (1996) Heterologous expression and characterization of the bifunctional dihydrofolate reductase-thymidylate synthase enzyme of Toxoplasma gondii Biochemistry 35, 6366-6374 (Pubitemid 26164070)
33. Pawelek, P. D., Allaire, M., Cygler, M., and MacKenzie, R. E. (2000) Channeling efficiency in the bifunctional methylenetetrahydrofolate dehydrogenase/cyclohydrolase domain: The effects of site-directed mutagenesis of NADP binding residues Biochim. Biophys. Acta 1479, 59-68 (Pubitemid 30345624)
34. 4folate complexes of Escherichia coli methylenetetrahydrofolate reductase reveal a spartan strategy for a ping-pong reaction Biochemistry 44, 11447-11457 (Pubitemid 41209080)
35. Miller, S. M., Massey, V., Ballou, D., Williams, C. H., Jr., Distefano, M. D., Moore, M. J., and Walsh, C. T. (1990) Use of a site-directed triple mutant to trap intermediates: Demonstration that the flavin C(4a)-thiol adduct and reduced flavin are kinetically competent intermediates in mercuric ion reductase Biochemistry 29, 2831-2841 (Pubitemid 20122619)
36. Salomon, M., Christie, J. M., Knieb, E., Lempert, U., and Briggs, W. R. (2000) Photochemical and mutational analysis of the FMN-binding domains of the plant blue light receptor, phototropin Biochemistry 39, 9401-9410 (Pubitemid 30626330)
37. Zoltowski, B. D., Schwerdtfeger, C., Widom, J., Loros, J. J., Bilwes, A. M., Dunlap, J. C., and Crane, B. R. (2007) Conformational switching in the fungal light sensor Vivid Science 316, 1054-1057 (Pubitemid 46799496)
38. Sumner, J. S. and Matthews, R. G. (1992) Stereochemistry and mechanism of hydrogen transfer between NADPH and methylenetetrahydrofolate in the reaction catalyzed by methylenetetrahydrofolate reductase from pig liver J. Am. Chem. Soc. 114, 6949-6956
39. Carreras, C. W. and Santi, D. V. (1995) The catalytic mechanism and structure of thymidylate synthase Annu. Rev. Biochem. 64, 721-762
40. Perry, K. M., Carreras, C. W., Chang, L. C., Santi, D. V., and Stroud, R. M. (1993) Structures of thymidylate synthase with a C-terminal deletion: Role of the C-terminus in alignment of 2-deoxyuridine 5-monophosphate and 5,10-methylenetetrahydrofolate Biochemistry 32, 7116-7125 (Pubitemid 23223114)
41. Trimmer, E. E., Ballou, D. P., Galloway, L. J., Scannell, S. A., Brinker, D. R., and Casas, K. R. (2005) Aspartate 120 of Escherichia coli methylenetetrahydrofolate reductase: Evidence for major roles in folate binding and catalysis and a minor role in flavin reactivity Biochemistry 44, 6809-6822 (Pubitemid 40632399)
42. Massey, V. (1994) Activation of molecular oxygen by flavins and flavoproteins J. Biol. Chem. 269, 22459-22462 (Pubitemid 24273342)
43. Palfey, B. A., Bjornberg, O., and Jensen, K. F. (2001) Insight into the chemistry of flavin reduction and oxidation in Escherichia coli dihydroorotate dehydrogenase obtained by rapid reaction studies Biochemistry 40, 4381-4390 (Pubitemid 32319583)
44. Wang, R. and Thorpe, C. (1991) Reactivity of medium-chain acyl-CoA dehydrogenase toward molecular oxygen Biochemistry 30, 7895-7901