Two Fe-S clusters catalyze sulfur insertion by radical-SAM methylthiotransferases (original) (raw)

• Fontecave, M., Ollagnier-de-Choudens, S. & Mulliez, E. Biological radical sulfur insertion reactions. Chem. Rev. 103, 2149–2166 (2003).
  Article CAS Google Scholar
• Jenner, L., Demeshkina, N., Yusupova, G. & Yusupov, M. Structural rearrangements of the ribosome at the tRNA proofreading step. Nat. Struct. Mol. Biol. 17, 1072–1078 (2010).
  Article CAS Google Scholar
• Wei, F.Y. et al. Deficit of tRNA(Lys) modification by Cdkal1 causes the development of type 2 diabetes in mice. J. Clin. Invest. 121, 3598–3608 (2011).
  Article CAS Google Scholar
• Atta, M. et al. _S_-Adenosylmethionine–dependent radical-based modification of biological macromolecules. Curr. Opin. Struct. Biol. 20, 684–692 (2010).
  Article CAS Google Scholar
• Kowalak, J.A. & Walsh, K.A. β-methylthio-aspartic acid: identification of a novel posttranslational modification in ribosomal protein S12 from Escherichia coli. Protein Sci. 5, 1625–1632 (1996).
  Article CAS Google Scholar
• Sofia, H.J., Chen, G., Hetzler, B.G., Reyes-Spindola, J.F. & Miller, N.E. Radical SAM, a novel protein superfamily linking unresolved steps in familiar biosynthetic pathways with radical mechanisms: functional characterization using new analysis and information visualization methods. Nucleic Acids Res. 29, 1097–1106 (2001).
  Article CAS Google Scholar
• Lee, K.H. et al. Characterization of RimO, a new member of the methylthiotransferase subclass of the radical SAM superfamily. Biochemistry 48, 10162–10174 (2009).
  Article CAS Google Scholar
• Hernández, H.L. et al. MiaB, a bifunctional radical-_S_-adenosylmethionine enzyme involved in the thiolation and methylation of tRNA, contains two essential [4Fe-4S] clusters. Biochemistry 46, 5140–5147 (2007).
  Article Google Scholar
• Arragain, S. et al. Identification of eukaryotic and prokaryotic methylthiotransferase for biosynthesis of 2-methylthio-_N_-6-threonylcarbamoyladenosine in tRNA. J. Biol. Chem. 285, 28425–28433 (2010).
  Article CAS Google Scholar
• Arragain, S. et al. Post-translational modification of ribosomal proteins. structural and functional characterization of RimO from Thermotoga maritima, a radical _S_-adenosylmethionine methylthiotransferase. J. Biol. Chem. 285, 5792–5801 (2010).
  Article CAS Google Scholar
• Anantharaman, V., Koonin, E.V. & Aravind, L. TRAM, a predicted RNA-binding domain, common to tRNA uracil methylation and adenine thiolation enzymes. FEMS Microbiol. Lett. 197, 215–221 (2001).
  Article CAS Google Scholar
• Booker, S.J., Cicchillo, R.M. & Grove, T.L. Self-sacrifice in radical _S_-adenosylmethionine proteins. Curr. Opin. Chem. Biol. 11, 543–552 (2007).
  Article CAS Google Scholar
• Ugulava, N.B., Sacanell, C.J. & Jarrett, J.T. Spectroscopic changes during a single turnover of biotin synthase: destruction of a [2Fe-2S] cluster accompanies sulfur insertion. Biochemistry 40, 8352–8358 (2001).
  Article CAS Google Scholar
• Frey, P.A., Hegeman, A.D. & Ruzicka, F.J. The radical SAM superfamily. Crit. Rev. Biochem. Mol. Biol. 43, 63–88 (2008).
  Article CAS Google Scholar
• Pierrel, F., Douki, T., Fontecave, M. & Atta, M. MiaB protein is a bifunctional radical-_S_-adenosylmethionine enzyme involved in thiolation and methylation of tRNA. J. Biol. Chem. 279, 47555–47563 (2004).
  Article CAS Google Scholar
• Vey, J.L. & Drennan, C.L. Structural insights into radical generation by the radical SAM superfamily. Chem. Rev. 111, 2487–2506 (2011).
  Article CAS Google Scholar
• Duschene, K.S., Veneziano, S.E., Silver, S.C. & Broderick, J.B. Control of radical chemistry in the AdoMet radical enzymes. Curr. Opin. Chem. Biol. 13, 74–83 (2009).
  Article CAS Google Scholar
• Zhang, Q. & Liu, W. Complex biotransformations catalyzed by radical _S_-adenosylmethionine enzymes. J. Biol. Chem. 286, 30245–30252 (2011).
  Article CAS Google Scholar
• Branden, C. & Tooze, J. Introduction to Protein Structure Vol. 2, 59–60 (Garland Publishing, New York, 1999).
• Holm, L. & Rosenstrom, P. Dali server: conservation mapping in 3D. Nucleic Acids Res. 38, W545–W549 (2010).
  Article CAS Google Scholar
• Andreeva, A. et al. Data growth and its impact on the SCOP database: new developments. Nucleic Acids Res. 36, D419–D425 (2008).
  Article CAS Google Scholar
• Baikalov, I. et al. Structure of the Escherichia coli response regulator NarL. Biochemistry 35, 11053–11061 (1996).
  Article CAS Google Scholar
• Schnell, R., Agren, D. & Schneider, G. 1.9-Å structure of the signal receiver domain of the putative response regulator NarL from Mycobacterium tuberculosis. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 64, 1096–1100 (2008).
  Article CAS Google Scholar
• Maris, A.E. et al. Dimerization allows DNA target site recognition by the NarL response regulator. Nat. Struct. Biol. 9, 771–778 (2002).
  Article CAS Google Scholar
• Porter, S.L., Wadhams, G.H. & Armitage, J.P. Signal processing in complex chemotaxis pathways. Nat. Rev. Microbiol. 9, 153–165 (2011).
  Article CAS Google Scholar
• Berkovitch, F., Nicolet, Y., Wan, J.T., Jarrett, J.T. & Drennan, C.L. Crystal structure of biotin synthase, an _S_-adenosylmethionine–dependent radical enzyme. Science 303, 76–79 (2004).
  Article CAS Google Scholar
• Hänzelmann, P. & Schindelin, H. Crystal structure of the _S_-adenosylmethionine-dependent enzyme MoaA and its implications for molybdenum cofactor deficiency in humans. Proc. Natl. Acad. Sci. USA 101, 12870–12875 (2004).
  Article Google Scholar
• Lees, N.S. et al. ENDOR spectroscopy shows that guanine N1 binds to [4Fe-4S] cluster II of the _S_-adenosylmethionine-dependent enzyme MoaA: mechanistic implications. J. Am. Chem. Soc. 131, 9184–9185 (2009).
  Article CAS Google Scholar
• Zheng, B., Chen, X.D., Zheng, S.L. & Holm, R.H. Selenium as a structural surrogate of sulfur: template-assisted assembly of five types of tungsten-iron-sulfur/selenium clusters and the structural fate of chalcogenide reactants. J. Am. Chem. Soc. 134, 6479–6490 (2012).
  Article CAS Google Scholar
• Wilker, J.J. & Lippard, S.J. Methylation of iron-sulfur complexes by trimethyl phosphate. Inorg. Chem. 38, 3569–3574 (1999).
  Article CAS Google Scholar
• Petrey, D. & Honig, B. GRASP2: visualization, surface properties, and electrostatics of macromolecular structures and sequences. Methods Enzymol. 374, 492–509 (2003).
  Article CAS Google Scholar
• Iwig, D.F. & Booker, S.J. Insight into the polar reactivity of the onium chalcogen analogues of _S_-adenosyl-L-methionine. Biochemistry 43, 13496–13509 (2004).
  Article CAS Google Scholar
• Tse Sum Bui, B., Mattioli, T.A., Florentin, D., Bolbach, G. & Marquet, A. Escherichia coli biotin synthase produces selenobiotin. Further evidence of the involvement of the [2Fe-2S]2+ cluster in the sulfur insertion step. Biochemistry 45, 3824–3834 (2006).
  Article Google Scholar
• Syper, L. & Mlochowski, J. The convenient syntheses of organoselenium reagents. Synthesis, 439–442 (1984).
• Fish, W.W. Rapid colorimetric micromethod for the quantitation of complexed iron in biological samples. Methods Enzymol. 158, 357–364 (1988).
  Article CAS Google Scholar
• Beinert, H. Semi-micro methods for analysis of labile sulfide and of labile sulfide plus sulfane sulfur in unusually stable iron sulfur proteins. Anal. Biochem. 131, 373–378 (1983).
  Article CAS Google Scholar
• Then, J. & Truper, H.G. Sulfide oxidation in _Ectothiorhodospira abdelmalekii_—evidence for the catalytic role of cytochrome c-551. Arch. Microbiol. 135, 254–258 (1983).
  Article CAS Google Scholar
• Pierrel, F., Hernandez, H.L., Johnson, M.K., Fontecave, M. & Atta, M. MiaB protein from _Thermotoga maritima_—characterization of an extremely thermophilic tRNA-methylthiotransferase. J. Biol. Chem. 278, 29515–29524 (2003).
  Article CAS Google Scholar
• Gehrke, C.W. & Kuo, K.C. Ribonucleoside analysis by reversed-phase high-performance liquid-chromatography. J. Chromatogr. 471, 3–36 (1989).
  Article CAS Google Scholar
• te Velde, G. & Baerends, E.J. Numerical integration for polyatomic systems. J. Comput. Phys. 99, 84–98 (1992).
  Article CAS Google Scholar
• Vosko, S.H., Wilk, L. & Nusair, M. Accurate spin-dependent electron liquid correlation energies for local spin-density calculations—a critical analysis. Can. J. Phys. 58, 1200–1211 (1980).
  Article CAS Google Scholar
• Becke, A.D. Density-functional exchange-energy approximation with correct asymptotic-behavior. Phys. Rev. A 38, 3098–3100 (1988).
  Article CAS Google Scholar
• Perdew, J.P. Density-functional approximation for the correlation energy of the inhomogeneous electron gas. Phys. Rev. B Condens. Matter 33, 8822–8824 (1986).
  Article CAS Google Scholar
• Szilagyi, R.K. & Winslow, M.A. On the accuracy of density functional theory for iron-sulfur clusters. J. Comput. Chem. 27, 1385–1397 (2006).
  Article CAS Google Scholar
• Noodleman, L., Peng, C.Y., Case, D.A. & Mouesca, J.M. Orbital interactions, electron delocalization and spin coupling in iron-sulfur clusters. Coord. Chem. Rev. 144, 199–244 (1995).
  Article CAS Google Scholar
• Acton, T.B. et al. Robotic cloning and protein production platform of the Northeast Structural Genomics Consortium. Methods Enzymol. 394, 210–243 (2005).
  Article CAS Google Scholar
• Jansson, M. et al. High-level production of uniformly 15N- and 13C-enriched fusion proteins in Escherichia coli. J. Biomol. NMR 7, 131–141 (1996).
  Article CAS Google Scholar
• Doublié, S. et al. Crystallization and preliminary X-ray analysis of the 9 kDa protein of the mouse signal recognition particle and the selenomethionyl-SRP9. FEBS Lett. 384, 219–221 (1996).
  Article Google Scholar
• Otwinowski, Z. & Minor, W. Processing of X-ray diffraction data collected in oscillation mode. Macromol. Crystallogr. A. 276, 307–326 (1997).
  Article CAS Google Scholar
• McCoy, A.J. et al. Phaser crystallographic software. J. Appl. Crystallogr. 40, 658–674 (2007).
  Article CAS Google Scholar
• McRee, D.E. XtalView Xfit—a versatile program for manipulating atomic coordinates and electron density. J. Struct. Biol. 125, 156–165 (1999).
  Article CAS Google Scholar
• Brünger, A.T. et al. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54, 905–921 (1998).
  Article Google Scholar