Skip to main content
SpringerLink
Log in

Iron–Sulfur Clusters in “Radical SAM” Enzymes: Spectroscopy and Coordination

  • Chapter
  • First Online:
Metals in Biology

Part of the book series: Biological Magnetic Resonance ((BIMR,volume 29))

Abstract

There is increasing evidence for the versatility of the coordination of iron–sulfur clusters in biology. In addition to cysteine residues as the most favored ligand and providing sulfur coordination, oxygenbased (aspartate, tyrosinate …) and nitrogen-based (histidine, arginine …) residues have also been observed as ligands to the clusters. Furthermore, low-molecular-weight substrates (citrate in the case of aconitase) and cofactors (S-adenosylmethionine, SAM, in the case of “Radical SAM” enzymes) have been shown to bind to one of the iron atoms of the [4Fe–4S] clusters where they are then activated. In this chapter we discuss the potential as well as the limitations of ENDOR and HYSCORE spectroscopy for characterizing metalloprotein coordination and, more specifically, the cluster–SAM complexes that are essential intermediates in pyruvate formate lyase-activating enzyme, lysine 2,3 aminomutase, and ribonucleotide reductase activating enzyme. These three systems are prototypes for the “Radical SAM” enzyme superfamily, whose chemistry seems to be extensively utilized in the metabolism of all living organisms.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 189.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Beinert H. 2000. Iron-sulfur proteins: ancient structures, still full of surprises. J Biol Inorg Chem 5:2–15.

    PubMed  CAS  Google Scholar 

  2. Green J, Paget MS. 2004. Bacterial redox sensors. Nature Rev Microbiol 2:954–966.

    CAS  Google Scholar 

  3. Flint DH, Allen RM. 1996. Iron-sulfur proteins with nonredox functions. Chem Rev 96:2315–2334.

    PubMed  CAS  Google Scholar 

  4. Fontecave M, Mulliez E, Ollagnier-de Choudens S. 2001. Adenosylmethionine as a source of 5′-deoxyadenosyl radicals. Curr Opin Chem Biol 5:506–511.

    PubMed  CAS  Google Scholar 

  5. Cheek J, Broderick JB. 2001. Adenosylmethionine-dependent iron-sulfur enzymes: versatile clusters in a radical new role. J Biol Inorg Chem 6:209–226.

    PubMed  CAS  Google Scholar 

  6. Frey PA, Magnusson OT. 2003. S-adenosylmethionine: a wolf in sheep's clothing, or a rich man's adenosylcobalamin? Chem Rev 103:2129–2148.

    PubMed  CAS  Google Scholar 

  7. Volbeda A, Charon MH, Piras C, Hatchikian EC, Frey M, Fontecilla-Camps JC. 1995. Crystal structure of the nickel-iron hydrogenase from Desulfovibrio gigas. Nature 373:580–587.

    CAS  Google Scholar 

  8. Nicolet Y, Piras C, Legrand P, Hatchikian CE, Fontecilla-Camps JC. 1999. Desulfovibrio desulfuricans iron hydrogenase: the structure shows unusual coordination to an active site Fe binuclear center. Structure 7:13–23.

    PubMed  CAS  Google Scholar 

  9. Peters JW, Lanzilotta WN, Lemon BJ, Seefeldt LC. 1998. X-ray crystal structure of the Fe-only hydrogenase (CpI) from Clostridium pasteurianum to 1.8 angstrom resolution. Science 282:1853–1858.

    PubMed  CAS  Google Scholar 

  10. Berkovitch F, Nicolet Y, Wan JT, Jarrett JT, Drennan CL. 2004. Crystal structure of biotin synthase, an S-adenosylmethionine-dependent radical enzyme. Science 303:76–79.

    PubMed  CAS  Google Scholar 

  11. Calzolai L, Gorst CM, Zhao ZH, Teng Q, Adams MW, La Mar GN. 1995. 1H NMR investigation of the electronic and molecular structure of the four-iron cluster ferredoxin from the hyperthermophile Pyrococcus furiosus: identification of Asp 14 as a cluster ligand in each of the four redox states. Biochemistry 34:11373–11384.

    PubMed  CAS  Google Scholar 

  12. Dobritzsch D, Schneider G, Schnackerz, KD, Lindqvist Y. 2001. Crystal structure of dihydropyrimidine dehydrogenase, a major determinant of the pharmacokinetics of the anti-cancer drug 5-fluorouracil. EMBO J 20:650–660.

    PubMed  CAS  Google Scholar 

  13. 13. Bückel W. Personal communication.

    Google Scholar 

  14. Layer G, Moser J, Heinz DW, Jahn D, Schubert W-D. 2003. Crystal structure of coproporphyrinogen III oxidase reveals cofactor geometry of Radical SAM enzymes. EMBO J 22:6214–6224.

    PubMed  CAS  Google Scholar 

  15. Walsby CJ, Ortillo D, Broderick WE, Broderick JB, Hoffman BM. 2002. An anchoring role for FeS clusters: chelation of the amino acid moiety of S-adenosylmethionine to the unique iron site of the [4Fe–4S] cluster of pyruvate formate-lyase activating enzyme. J Am Chem Soc 124:11270–11271.

    PubMed  CAS  Google Scholar 

  16. Hänzelmann P, Schindelin H. 2004. Crystal structure of the S-adenosylmethionine-dependent enzyme MoaA and its implications for molybdenum cofactor deficiency in humans. Proc Natl Acad Sci USA 10:12870–12875.

    Google Scholar 

  17. Lepore BW, Ruzicka FJ, Frey PA Ringe D. 2005. The X-ray crystal structure of lysine-2,3-aminomutase from Clostridium subterminale. Proc Natl Acad Sci USA 102:13819–13824.

    CAS  Google Scholar 

  18. Gambarelli S, Luttringer F, Padovani D, Mulliez E Fontecave M. 2005. Activation of the anaerobic ribonucleotide reductase by S-adenosylmethionine. ChemBioChem 6:1–3.

    Google Scholar 

  19. Beinert H, Kennedy MC, Stout CD. 1996. Aconitase as iron-sulfur protein, enzyme, and iron-regulatory protein. Chem Rev 96:2335–2374.

    PubMed  CAS  Google Scholar 

  20. Werst MM, Kennedy MC, Beinert H, Hoffman BM. 1990. 17O, 1H, and 2H electron nuclear double resonance characterization of solvent, substrate, and inhibitor binding to the [4Fe–4S]+ cluster of aconitase. Biochemistry 29:10526–10532.

    PubMed  CAS  Google Scholar 

  21. Telser J, Emptage MH, Merkle H, Kennedy MC, Beinert H, Hoffman BM. 1986. 17O electron nuclear double resonance characterization of substrate binding to the [4Fe– 4S]+ cluster of reduced active aconitase. J Biol Chem 261:4840–4846.

    PubMed  CAS  Google Scholar 

  22. Kennedy MC, Werst M, Telser J, Emptage MH, Beinert H, Hoffman BM. 1987. Mode of substrate carboxyl binding to the [4Fe–4S]+ cluster of reduced aconitase as studied by 17O and 13C electron-nuclear double resonance spectroscopy. Proc Natl Acad Sci USA 84:8854–8858.

    PubMed  CAS  Google Scholar 

  23. Sofia HJ, Chen G, Hetzler BG, Reyes-Spindola JF, Miller NE. 2001. 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.

    PubMed  CAS  Google Scholar 

  24. Frey PA, Booker S. 1999. Radical intermediates in the reaction of lysine 2,3-aminomutase. In Advances in Free Radical Chemistry, 2:1–43. Ed Z Zard. Greenwich: JAI Press.

    Google Scholar 

  25. Buis JM, Broderick JB. 2005. Pyruvate formate-lyase activating enzyme: elucidation of a novel mechanism for glycyl radical formation. Arch Biochem Biophys 433:288–296.

    PubMed  CAS  Google Scholar 

  26. Fontecave M, Mulliez E, Logan DT. 2002. Deoxyribonucleotide synthesis in anaerobic microorganisms: the class III ribonucleotide reductase. In Progress in Nucleic Acid Research and Molecular Biology, 72:95–127. Ed K Moldave. San Diego: Elsevier Science.

    Google Scholar 

  27. Magnusson OT, Reed G Frey PA. 1999. Spectroscopic evidence for the participation of an allylic analogue of the 5′-deoxyadenosyl radical in the reaction of lysine 2,3-aminomutase. J Am Chem Soc 121:9764–9765.

    CAS  Google Scholar 

  28. Frey M, Rothe M, Wagner AF, Knappe J. 1994. Adenosylmethionine-dependent synthesis of the glycyl radical in pyruvate formate-lyase by abstraction of the glycine C-2 pro-S hydrogen atom: studies of [2H]-glycine-substituted enzyme and peptides homologous to the glycine 734 site. J Biol Chem 269:12432–12437.

    PubMed  CAS  Google Scholar 

  29. Kilgore JL, Aberhart DJ. 1991. Lysine 2,3-aminomutase: role of S-adenosyl-l-methionine in the mechanism: demonstration of tritium transfer from (2RS,3RS)-[3-3H]lysine to S-adenosyl-L-methionine. J Chem Soc Perkin Trans 1:79–84.

    Google Scholar 

  30. Cheek J, Broderick JB. 2002. Direct H atom abstraction from spore photoproduct C-6 initiates DNA repair in the reaction catalyzed by spore photoproduct lyase: evidence for a reversibly generated adenosyl radical intermediate. J Am Chem Soc 124:2860–2861.

    PubMed  CAS  Google Scholar 

  31. Wagber AF, Frey M, Neugebauer FA, Schafer W, Knappe J. 1992. The free radical in pyruvate formate-lyase is located on glycine-734. Proc Natl Acad Sci USA 89:996–1000.

    Google Scholar 

  32. Kulzer R, Pils T, Kappl R, Huttermann J, Knappe J. 1998. Reconstitution and characterization of the polynuclear iron–sulfur cluster in pyruvate formate-lyase-activating enzyme: molecular properties of the holoenzyme form. J Biol Chem 273:4897–4903.

    PubMed  CAS  Google Scholar 

  33. Henshaw TF, Cheek J, Broderick JB. 2000. The [4Fe–4S]1+ cluster of pyruvate formate-lyase activating enzyme generates the glycyl radical on pyruvate formate-lyase: EPR-detected single turnover. J Am Chem Soc 122:8331–8332.

    CAS  Google Scholar 

  34. Broderick JB, Duderstadt RE, Fernandez DC, Wojtuszewski K, Henshaw TF, Johnson, MK. 1997. Pyruvate formate-lyase activating enzyme is an iron–sulfur protein. J Am Chem Soc 119:7396–7397.

    CAS  Google Scholar 

  35. Walsby CJ, Hong W, Broderick WE, Cheek J, Ortillo D, Broderick JB, Hoffman BM. 2002. Electron-nuclear double resonance spectroscopic evidence that S-adenosylmethionine binds in contact with the catalytically active [4Fe–4S]+ cluster of pyruvate formate-lyase activating enzyme. J Am Chem Soc 124:3143–3151.

    PubMed  CAS  Google Scholar 

  36. Lieder KW, Booker S, Ruzicka FJ, Beinert H, Reed GH, Frey PA. 1998. S-Adenosylmethionine-dependent reduction of lysine 2,3-aminomutase and observation of the catalytically functional iron–sulfur centers by electron paramagnetic resonance. Biochemistry 37:2578–2585.

    PubMed  CAS  Google Scholar 

  37. Jordan A, Reichard P. 1998. Ribonucleotide reductases. Annu Rev Biochem 67:71–98.

    PubMed  CAS  Google Scholar 

  38. Logan DT, Mulliez E, Larsson KM, Bodevin S, Atta M, Garnaud PE, Sjöberg B-M, Fontecave M. 2003. A metal binding site in the catalytic subunit of anaerobic ribonucleotide reductase. Proc Natl Acad Sci USA 100:3826–3831.

    PubMed  CAS  Google Scholar 

  39. Tamarit J, Mulliez E, Meier C, Trautwein A, Fontecave M. 1999. The anaerobic ribonucleotide reductase from E. coli: the small protein is an activating enzyme containing a [4Fe–4S]2+ center. J Biol Chem 274:31291–31296.

    PubMed  CAS  Google Scholar 

  40. Padovani D, Thomas F, Trautwein AX, Mulliez E, Fontecave M. 2001, Activation of class III ribonucleotide reductase from E. coli: the electron transfer from the iron sulfur center to S-adenosyl methionine. Biochemistry 40:6713–6719.

    PubMed  CAS  Google Scholar 

  41. Ollagnier S, Mulliez E, Schmidt PP, Eliasson R, Gaillard J, Deronzier C, Bergman T, Graslund A, Reichard P, Fontecave M. 1997. Activation of the anaerobic ribonucleotide reductase from Escherichia coli: the essential role of the iron-sulfur center for S-adenosylmethionine reduction. J Biol Chem 272:24216–24223.

    PubMed  CAS  Google Scholar 

  42. Mulliez E, Padovani D, Atta M, Alcouffe C, Fontecave M. 2001. Activation of class III ribonucleotide reductase by flavodoxin: a protein radical-driven electron transfer to the iron–sulfur center. Biochemistry 40:3730–3736.

    PubMed  CAS  Google Scholar 

  43. Fontecave M, Ollagnier-de-Choudens S, Mulliez E. 2003. Biological radical sulfur insertion reactions. Chem Rev 103:2149–2166.

    PubMed  CAS  Google Scholar 

  44. Jarrett JT. 2005. The novel structure and chemistry of iron–sulfur clusters in the adenosylmethionine-dependent radical enzyme biotin synthase. Arch Biochem Biophys 433:312–321.

    PubMed  CAS  Google Scholar 

  45. Pierrel F, Douki T, Fontecave M, Atta M. 2004. MiaB protein is a bifunctional radical-S-adenosylmethionine enzyme involved in thiolation and methylation of tRNA. J Biol Chem 279:47555–17563.

    PubMed  CAS  Google Scholar 

  46. Layer G, Grage K, Teschner T, Schunemann V, Breckau D, Masoumi A, Jahn M, Heathcote P, Trautwein AX, Jahn D. 2005. Radical S-adenosylmethionine enzyme coproporphyrinogen III oxidase HemN: functional features of the [4Fe–4S] cluster and the two bound S-adenosyl-L-methionine. J Biol Chem 280:29038–29046.

    PubMed  CAS  Google Scholar 

  47. Leuthner B, Leutwein C, Schulz H, Horth P, Haehnel W, Schiltz E, Schagger H, Heider J. 1998. Biochemical and genetic characterization of benzylsuccinate synthase from Thauera aromatica: a new glycyl radical enzyme catalysing the first step in anaerobic toluene metabolism. Mol Microbiol 28:615–628.

    PubMed  CAS  Google Scholar 

  48. O'Brien JR, Raynaud C, Croux C, Girbal L, Soucaille P, Lanzilotta WN. 2004. Insight into the mechanism of the B12-independent glycerol dehydratase from Clostridium butyricum: preliminary biochemical and structural characterization. Biochemistry 43:4635–4645.

    PubMed  Google Scholar 

  49. Andrei PI, Pierik AJ, Zauner S, Andrei-Selmer LC, Selmer T. 2004. Subunit composition of the glycyl radical enzyme p-hydroxyphenylacetate decarboxylase: a small subunit, HpdC, is essential for catalytic activity. Eur J Biochem 271:2225–2230.

    PubMed  CAS  Google Scholar 

  50. Rebeil R, Sun Y, Chooback L, Pedraza-Reyes M, Kinsland C, Begley TP, Nicholson WL. 1998. Spore photoproduct lyase from Bacillus subtilis spores is a novel iron–sulfur DNA repair enzyme which shares features with proteins such as class III anaerobic ribonucleotide reductases and pyruvate–formate lyases. J Bacteriol 180:4879–4885.

    PubMed  CAS  Google Scholar 

  51. Fang Q, Peng J, Dierks T. 2004. Post-translational formylglycine modification of bacterial sulfatases by the radical S-adenosylmethionine protein AtsB. J Biol Chem 279:14570–14578.

    PubMed  CAS  Google Scholar 

  52. Rubach JK, Brazzolotto X, Gaillard J, Fontecave M. 2005. Biochemical characterization of the HydE and HydG iron-only hydrogenase maturation enzymes from Thermatoga maritima. FEBS Lett 579:5055–5060.

    CAS  Google Scholar 

  53. van Lenthe E, van der Avoird A, Hagen WR, Reijerse EJ. 2000. Density functional calculations of g-tensors of low-spin iron(I) and iron(III) porphyrins. J Phys Chem A 104:2070–2077.

    CAS  Google Scholar 

  54. Malkina OL, Vaara J, Schimmelpfenning B, Munzarova M, Malkin VG, Kaupp M. 2000. Density functional calculations of electronic g-tensors using spin-orbit pseudopotentials and mean-field all-electron spin-orbits operators. J Am Chem Soc 122:9206– 9218.

    CAS  Google Scholar 

  55. Vrajmasu VV, Bominaar EL, Meyer J, Münck E. 2002. Mössbauer study of reduced rubredoxin as purified and in whole cells: structural correlation analysis of spin hamiltonian parameters. Inorg Chem 41:6358–6371.

    PubMed  CAS  Google Scholar 

  56. Gambarelli S, Mouesca J-M. 2004. Correlation between the magnetic g tensors and the local cysteine geometries for a series of reduced [2Fe–2S*] protein clusters: a quantum chemical density functional theory and structural analysis. Inorg Chem 43:1441–1451.

    PubMed  CAS  Google Scholar 

  57. Solomon EI, Szilagyi RK, DeBeer George S, Basumallick L. 2004. Electronic structure of metal sites in proteins and models: contributions to function in blue copper proteins. Chem Rev 104:419–458.

    PubMed  CAS  Google Scholar 

  58. Hwang HJ, Nagraj N, Lu Y. 2006. Spectroscopic characterizations of bridging cysteine ligand variants of an engineered Cu2(Scys)2 CuA azurin. Inorg Chem 45:102–107.

    PubMed  CAS  Google Scholar 

  59. Schansker G, Goussias C, Petrouleas V, Rutherford AW. 2002. Reduction of the Mn cluster of the water-oxidizing enzyme by nitric oxide: formation of an S-2 state. Biochemistry 41:3057–3064.

    PubMed  CAS  Google Scholar 

  60. Wu AJ, Penner-Hahn JE, Pecoraro VL. 2004. Structural, spectroscopic, and reactivity models for the manganese catalases. Chem Rev 104:903–938.

    PubMed  CAS  Google Scholar 

  61. Hagen WR. 1989. g-strain: inhomogeneous broadening in metalloprotein EPR. In Advanced EPR Applications in Biology and Biochemistry, pp. 785–811. Ed AJ Hoff. Amsterdam: Elsevier.

    Google Scholar 

  62. Hoffman BM. 2003. ENDOR of metalloenzymes. Acc Chem Res 36:522–529.

    PubMed  CAS  Google Scholar 

  63. Hoffman BM. 2003. Electron-nuclear double resonance spectroscopy (and electron spin-echo envelope modulation spectroscopy) in bioinorganic chemistry. Proc Natl Acad Sci USA 100:3575–3578.

    PubMed  CAS  Google Scholar 

  64. Brecht M, Van Gastel M, Buhrke T, Friedrich B, Lubitz W. 2003. Direct detection of a hydrogen ligand in the [NiFe] center of the regulatory H2-sensing hydrogenase from Ralstonia eutropha in its reduced state by HYSCORE and ENDOR spectroscopy. J Am Chem Soc 125:13075–13083.

    PubMed  CAS  Google Scholar 

  65. Walsby CJ, Krepkiy D, Petering DH, Hoffman BM. 2003. Cobalt-substituted zinc finger 3 of transcription factor IIIA: interactions with cognate DNA detected by 31P ENDOR spectroscopy. J Am Chem Soc 125:7502–7503.

    PubMed  CAS  Google Scholar 

  66. Lendzian F. 2005. Structure and interactions of amino acid radicals in class I ribonucleotide reductase studied by ENDOR and high-field EPR spectroscopy. Biochim Biophys Acta 1707:67–90.

    PubMed  CAS  Google Scholar 

  67. Gemperle C, Schweiger A. 1991. Pulsed electron-nuclear double resonance methodology. Chem Rev 91:1481–1505.

    CAS  Google Scholar 

  68. Schweiger A, Jeschke G. 2001. Principles of pulsed electron paramagnetic resonance. Oxford: Oxford UP.

    Google Scholar 

  69. Telser J, Huang H, Lee H-I, Adams MW, Hoffman BM. 1998. Site Valencies and Spin Coupling in the 3Fe and 4Fe (S = 1/2) clusters of Pyrococcus furiosus ferredoxin by 57Fe ENDOR. J Am Chem Soc 120:861–870.

    CAS  Google Scholar 

  70. Bennati M, Weiden N, Dinse KP, Hedderich R. 2004. 57Fe ENDOR spectroscopy on the iron–sulfur cluster involved in substrate reduction of heterodisulfide reductase. J Am Chem Soc 126:8378–8379.

    PubMed  CAS  Google Scholar 

  71. Walsby CJ, Hong W, Broderick WE, Cheek J, Ortillo D, Broderick JB, Hoffman BM. 2002. Electron-nuclear double resonance spectroscopic evidence that S-adenosylmethionine binds in contact with the catalytically active [4Fe–4S]+ cluster of pyruvate formate-lyase activating enzyme. J Am Chem Soc 124:3143–3151.

    PubMed  CAS  Google Scholar 

  72. Walsby C, Ortillo D, Broderick WE, Broderick JB, Hoffman BM. 2002. An anchoring role for FeS clusters: chelation of the amino acid moiety of S-adenosylmethionine to the unique iron site of the [4Fe–4S] cluster of pyruvate formate–lyase activating enzyme. J Am Chem Soc 124:11270–11271.

    PubMed  CAS  Google Scholar 

  73. Hole EO, Nelson WH, Sagstuen E, Close DM. 1998. Electron paramagnetic resonance and electron nuclear double resonance studies of x-irradiated crystals of cytosine hydrochloride, Part I: free radical formation at 10 K after high radiation doses. Radiat Res 149:109–119.

    PubMed  CAS  Google Scholar 

  74. Hole EO, Sagstuen E, Nelson WH, Close DM. 2000. Free radical formation in x-irradiated crystals of 2′-deoxycytidine hydrochloride: electron magnetic resonance studies at 10 K. Radiat Res 153:823–834.

    PubMed  CAS  Google Scholar 

  75. Moriaud F, Gambarelli S, Lamotte B, Mouesca J-M. 2001. Detailed proton Q-band ENDOR study of the electron spin population distribution in the reduced [4Fe–4S]1+ state. J Phys Chem B 105:9631–9642.

    CAS  Google Scholar 

  76. Hoffman BM, Martinsen J, Venters RA. 1984. General theory of polycrystalline ENDOR patterns: g and hyperfine tensors of arbitrary symmetry and relative orientation. J Magn Reson 59:110–123.

    CAS  Google Scholar 

  77. Bender CJ, Rosenzweig AC, Lippard SJ, Peisach J. 1994. Nuclear hyperfine coupling of nitrogen in the coordination sphere of the diiron center of methane monooxygenase hydroxylase. J Biol Chem 269:15993–15998.

    PubMed  CAS  Google Scholar 

  78. Riedel A, Fetzner S, Rampp M, Lingens F, Liebl U, Zimmermann J-L, Nitschke W. 1995. EPR, electron spin echo modulation, and electron nuclear double resonance studies of the 2Fe–2S centers of the 2-halobenzoate 1,2-dioxygenase from Burkholderia (Pseudomonas) cepacia 2CBS. J Biol Chem 270:30869–30873.

    PubMed  CAS  Google Scholar 

  79. Lee HC, Scheuring E, Peisach J, Chance MR. 1997. Electron spin echo enveloppe modulation and extended x-ray absorption fine structure studies of active site models of oxygenated cobalt-substituted hemoproteins: correlating electron-nuclear couplings and metal–ligand bond lengths. J Am Chem Soc 119:12201–12209.

    CAS  Google Scholar 

  80. Ke S-C, Warncke K. 1999. Interactions of substrate and product radicals with CoII in cobalamin and with the active site in ethanolamine deaminase, characterized by ESE- EPR and 14N ESEEM spectroscopies. J Am Chem Soc 121:9922–9927.

    CAS  Google Scholar 

  81. Kofman V, Farver O, Pecht I, Goldfarb D. 1996. Two-dimensional pulsed EPR spectroscopy of the copper protein azurin. J Am Chem Soc 118:1201–1206.

    CAS  Google Scholar 

  82. Dikanov SA, Davydov RM, Gräslund A, Bowman MK. 1998. Two-dimensional ESEEM spectroscopy of nitrogen hyperfine couplings in methemerythrin and azidomethemerythrin. J Am Chem Soc 120:6797–6805.

    CAS  Google Scholar 

  83. Tyryshkin AM, Dikanov SA, Reijerse EJ, Burgard C, Hüttermann J. 1999. Characterization of bimodal coordination structure in nitrosyl heme complexes through hyperfine couplings with pyrrole and protein nitrogens. J Am Chem Soc 121:3396–3406.

    CAS  Google Scholar 

  84. Van Doorslaer S, Jeschke G, Epel B, Goldfarb D, Eichel R-A, Kräuther B, Schweiger A. 2003. Axial solvent coordination in “base-off” Cob(II)alamin and related Co(II)- corrinates revealed by 2D-EPR. J Am Chem Soc 125:5915–5927.

    PubMed  CAS  Google Scholar 

  85. Foerster S, van Gastel M, Brecht M, Lubitz W. 2005. An orientation-selected ENDOR and HYSCORE study of the Ni–C active state of Desulfovibrio vulgaris Miyazaki F hydrogenase. J Biol Inorg Chem 10:51–62.

    PubMed  CAS  Google Scholar 

  86. Dikanov SA, Xun L, Karpiel AB, Tyryshkin AM, Bowman MK. 1996. Orientationally-selected two-dimensional ESEEM spectroscopy of the Rieske-type iron–sulfur cluster in 2,4,5-trichlorophenoxyacetate monooxygenase from Burkholderia cepacia AC1100. J Am Chem Soc 118:8408–8416.

    CAS  Google Scholar 

  87. Maryasov AG, Bowman MK. 2004. Hyperfine sublevel correlation (HYSCORE) spectra for paramagnetic centers with nuclear spin I = 1 having isotropic hyperfine interactions. J Phys Chem B 108:9412–9420.

    CAS  Google Scholar 

  88. Middleton P, Dickson DPE, Johnson CE, Rush JD. 1978. Interpretation of the Mössbauer spectra of the four-iron ferredoxin from Bacillus stearothermophilus. Eur J Biochem 88:135–141.

    CAS  Google Scholar 

  89. Bertrand P, More C, Guigliarelli B, Fournel A, Bennett B, Howes B. 1994. Biological polynuclear clusters coupled by magnetic interactions: from the point dipole approximation to a local spin model. J Am Chem Soc 116:3078–3086.

    CAS  Google Scholar 

  90. Bertrand P, More C, Cammensuli P. 1995. Evidence for a magic magnetic configuration between FMN and the [2Fe–2S]+ center of phthalate dioxygenase reductase of Pseudomonas cepacia. J Am Chem Soc 117:1807–1809.

    CAS  Google Scholar 

  91. Moriaud F, Gambarelli S, Lamotte B, Mouesca J-M. 2001. Single-crystal 57Fe Q-band ENDOR study of the 4 Iron–4 sulfur cluster in its reduced [4Fe–4S]1+ state. J Magn Reson 153:238–245.

    PubMed  CAS  Google Scholar 

  92. Barone V, Bencini A, Cossi M, Di Matteo A, Mattesini M, Totti F. 1998. Assessment of a combined QM/MM approach for the study of large nitroxyde systems in vacuo and in condensed phases. J Am Chem Soc 120:7069–7078.

    CAS  Google Scholar 

  93. Improta R, Barone V. 2004. Interplay of electronic, environnemental, and vibrational effects in determining the hyperfine coupling constants of organic free radicals. Chem Rev 104:1231–1253.

    PubMed  CAS  Google Scholar 

  94. Mouesca J-M, Rius G, Lamotte B. 1993. Single-crystal proton ENDOR studies of the [Fe4S4]3+ cluster: determination of the spin population distribution and proposal of a model to interpret the 1H NMR paramagnetic shifts in high-potential ferredoxins. J Am Chem Soc 115:4714–4731.

    CAS  Google Scholar 

  95. Werst M, Kennedy MC, Houseman ALP, Beinert H, Hoffman BM. 1990. Characterization of the [4Fe–4S]+ cluster at the active site of aconitase by 57Fe, 33S, and 14N electron nuclear double resonance spectroscopy. Biochemistry 29:10533–10540.

    PubMed  CAS  Google Scholar 

  96. Walsby CJ, Ortillo D, Yang J, Mnyepi MR, Broderick WE, Hoffman BM, Broderick JB. 2005. Spectroscopic approaches to elucidating novel iron–sulfur chemistry in the “radical SAM” protein superfamily. Inorg Chem 44:727–741.

    PubMed  CAS  Google Scholar 

  97. Gurbiel RJ, Doan PE, Gassner GT, Macke TJ, Case DA, Ohnishi T, Fee JA, Ballou DP, Hoffman BM. 1996. Active site structure of Rieske-type proteins: electron nuclear double resonance studies of isotopically labeled phthalate dioxygenase from Pseudomonas cepacia and Rieske protein from Rhodobacter capsulatus and molecular modeling studies of a Rieske center. Biochemistry 35:7834–7845.

    PubMed  CAS  Google Scholar 

  98. Rocklin AM, Tierney DL, Kofman V, Brunhuber NMW, Hoffman BM, Christoffersen RE, Reich NO, Lipscomb JD, Que LJr. 1999. Role of the nonheme Fe(II) center in the biosynthesis of the plant hormone ethylene. Proc Natl Acad Sci USA 96:7905–7909.

    PubMed  CAS  Google Scholar 

  99. Chen D, Walsby C, Hoffman BM, Frey PA. 2003. Coordination and mechanism of reversible cleavage of S-adenosylmethionine by the [4Fe–4S] center in lysine 2,3- aminomutase. J Am Chem Soc 125:11788–11789.

    PubMed  CAS  Google Scholar 

  100. Shergill J, Joannou CL, Mason JR, Cammack R. 1995. Coordination of the Rieske-type [2Fe–2S] cluster of the terminal iron–sulfur protein of Pseudomonas putida benzene 1,2-dioxygenase, studied by one- and two-dimensional electron spin-echo envelope modulation spectroscopy. Biochemistry 34:6533–16542.

    Google Scholar 

  101. Samoilova RI, Kolling D, Uzawa T, Iwasaki T, Crofts A, Dikanov SA. 2002. The interaction of the Rieske iron–sulfur protein with occupants of the Q0-site of the bc1 complex, probed by electron spin echo envelope modulation. J Biol Chem 277:4605–4608.

    PubMed  CAS  Google Scholar 

  102. Iwasaki T, Kounosu A, Uzawa T, Samoilova RI, Dikanov SA. 2004. Orientation-selected 15N-HYSCORE detection of weakly coupled nitrogens around the archaeal rieske [2Fe–2S] center. J Am Chem Soc 126:13902–13903.

    PubMed  CAS  Google Scholar 

  103. 103. Gambarelli S, Mulliez E, Fontecave M. Unpublished results.

    Google Scholar 

  104. Vey JL, Yang J, Li M, Broderick WE, Broderick JB, Drennan CL. 2008. Structural basis for glycyl radical formation by pyruvate formate-lyase activating enzyme. Proc Natl Acad Sci USA 105:16137–16141.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Service de Chimie Inorganique et Biologique, INAC/SCIB, CEA-Grenoble, 17 rue des Martyrs, 38054, Grenoble cedex 9, France

    Serge Gambarelli

  2. Laboratoire de Chimie et Biochimie des Métaux, CNRSCEA-Université Joseph Fourier n° 5249, iRTSV/LCBM, CEA-Grenoble, Grenoble, France

    Etienne Mulliez & Marc Fontecave

Authors
  1. Serge Gambarelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Etienne Mulliez
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Marc Fontecave
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Serge Gambarelli .

Editor information

Editors and Affiliations

  1. Center for Magnetic Resonance, University of Queensland, St. Lucia, 4072, Australia

    Graeme Hanson

  2. University of Denver, 2190 E. Iliff Avenue,F.W. Olin Hall,Room 202, Denver, 80208-0001, USA

    Lawrence Berliner

Rights and permissions

Reprints and permissions

Copyright information

© 2010 Springer Science+Business Media, LLC

About this chapter

Cite this chapter

Gambarelli, S., Mulliez, E., Fontecave, M. (2010). Iron–Sulfur Clusters in “Radical SAM” Enzymes: Spectroscopy and Coordination. In: Hanson, G., Berliner, L. (eds) Metals in Biology. Biological Magnetic Resonance, vol 29. Springer, New York, NY. https://doi.org/10.1007/978-1-4419-1139-1_4

Download citation

Publish with us

Policies and ethics

Search

Navigation