Cofactors of sulfite reductase

Based on the findings of the preliminary crystallographic analysis, the biochemical data (Dahl et al., 1993) and the sequence data (Klenk et al., 1997), the following model of sulfite reductase was constructed.

Figure 4.7: Model of sulfite reductase deduced from crystallographic analysis. The α-subunit contains the siroheme right next to a [4Fe-4S] cluster a second [4Fe-4S] cluster was 15 Å away. The β-subunit contains another iron-sulfur cluster that was at least 38 Å away from the others. The distance to the clusters (1B, 2B 3B) of the other αβ-unit (α’,β’) is at least 31 Å.

The siroheme was located in exchange coupling distance from the [4Fe-4S] cluster 1. Another cluster was located most probably also in the α-subunit within a distance that was compatible with fast and efficient electron transfer between the centers. The third cluster however was located at the other side of the αβ-arrangement. The function of this third cluster (3A) being electron transfer to the active site was almost inconceivable. The shortest distance to the next

cluster was 31 Å to the equivalent cluster (3B) of the other β-subunit so electron transfer across αβ-units was not a possibility. On the other hand it was strange that an enzyme that catalyzes a six-electron reduction contained an iron-sulfur cluster that was not involved in electron transfer.

5 References

Abrahams, J. P. & Leslie, A. G. W. (1996) Methods used in the structure determination of bovine mitochondrial F1 ATPase, Acta Cryst D52, 30-42

Achenbach-Richter, L., Gupta, R., Stetter, K. O., and Woese C. R. (1987) Were the original eubacteria thermophiles?, Syst Appl Microbiol 9, 34-39.

Achim C., Golinelli M.-P., Bominaar E. L., Meyer, J., Münck, E. (1996) Mossbauer study of Cys56Ser mutant 2Fe ferredoxin from Clostridium pasteurianum: evidence for double exchange in an [2Fe-2S]⁺ cluster. J Am Chem Soc 118, 8168-8169.

Adams, M. W. W. (1993) Enzymes and proteins from organisms that grow near and obove 100°C, Annual Rev Microbiol 47, 627-658.

Angove, H. C. Yoo, J. S., Burgess, B. K. & Münck, E. (1997) Mössbauer and EPR Evidence for an All-Ferrous Fe4S4 Cluster with S = 4 in the Fe Protein of Nitrogenase, J Am Chem Soc 119, 8730-8731.

Bamford, V., Dobbin, P. S., Richardson, D. J., and Hemmings, A. M. (1999) Open conformation of a flavocytochrome c3 fumarate reductase, Nature Struct Biol 6, 1104-1107 Beinert, H., Orme-Johnson, W. H., and Palmer, G. (1978) Special techniques for the preparation of samples for low-temperature EPR spectroscopy, Methods Enzymol 54, 111-132.

Belinsky, M. I. (1995) Exchange model of the {[Fe4S4]-Fe} active site of sulfite reductase, Chem Phys 201, 343-356

Bensadoun, A., & Weinstein, D. (1976) Assay of proteins in the presence of interfering materials, Anal Biochem 70, 241-50.

Bick, J. A., & Leustek, T. (1998) Plant sulfur metabolism - the reduction of sulfate to sulfite, Curr Opin Plant Biol 1, 240-244.

Binda, C., Newton-Vinson, P., Hubálek, F., Edmondson, D. E. and Mattevi, A. (2002) Structure of human monoamine oxidase B, a drug target for the treatment of neurological disorders, Nature Struct Biol 1, 22-26

Blundell, T. L. & Johnson, L. N. (1994) Crystallization of proteins, in Protein Crystallography 4. Auflage edit. (Blundell, T. L. & Johnson, L. N., eds.), pp. 59-82. Academic Press Inc., San Diego.

Brüggemann, H., Falinski, F., and Deppenmeier, U. (2000) Structure of the F420H2:quinone oxidoreductase of Archaeoglobus fulgidus, Eur J Biochem 267, 5810-5814.

Brünger, A. T. (1992) Free R value: a novel statistical quantity for assessing the accuracy of crystal structures, Nature 355, 472-475.

Brünger, A. T. (1993) Assessment of phase accuracy by cross validation: the free R value.

Methods und applications, Acta Cryst D 49, 24-36.

Brünger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse-Kunstleve, R.

W., Jiang, J. S., Kuszewski, J., Nilges, M., Pannu, N. S., Read, R. J., Rice, L. M., Simonson, T., Warren, G. L. (1998) Crystallography and NMR system: A new software suite for macromolecular structure determination, Acta Cryst D 54, 905-921.

Brunold, C., Rennenberg, H., De Kok, L. J., Stulen, I., Davidian, J.-C. (2000) Sulfur Nutrition and Sulfur Assimilation in Higher Plants: molecular, biochemical and physiological aspects, Haupt, Berne.

Büchert, T. (2001) Structure and function of adenosine 5'-phosphosulfate reductase, Ph. D.

Thesis, Universität Konstanz, Konstanz.

Burdinski, D., Bill, E., Birkelbach, F., Wieghardt, K. & Chaudhuri, P. (2001) Long-Range Exchange Interactions and Integer-Spin St = 2 EPR Spectra of a Cr^IIIZn^IICr^III Species with Multiplet Mixing, Inorg Chem 40, 1160-1166.

Burgess, B. K., Stiefel, E. I. & Newton, W. E. (1980) Oxidation-reduction properties and complexation reactions of the iron-molybdenum cofactor of nitrogenase, J Biol Chem 255, 353-356.

Cameron, E. M. (1982) Sulfate and sulfate reduction in the early Precambrian oceans, Nature 296, 145-148.

Carter Jr., C. W. & Carter, C. W. (1979) Protein crystallization using incomplete factorial experiments, J Biol Chem 254, 12219-12223.

Castro, H. F., Williams, N. H., and Ogram, A. (2000) Phylogeny of sulfate-reducing bacteria, FEMS Microbiol Ecol 31, 1-9.

Chan, J. M., Christiansen, J., Dean, D. R., Seefeldt, L. C. (1999) Spectroscopic evidence for changes in the redox state of the nitrogenase P-cluster during turnover, Biochemistry 38, 5779-85.

Chapman, M. S. &Blanc, E. (1997) Potential use of real-space refinement in protein structure determination, Acta Cryst D 53, 203-206.

Chen, K., Tilley, G. J., Sridhar, V., Prasad, G. S., Stout, C. D., Armstrong, F. A., and Burgess, B. K. (1999) Alteration of the reduction potential of the [4Fe-4S](2+/+) cluster of Azotobacter vinelandii ferredoxin I, J Biol Chem 274, 36479-36487

Christner, J. A., Münck, E., Janick, P. A. & Siegel, L. M. (1981) Mössbauer spectroscopic studies of E. coli sulfite reductase, J Biol Chem 256, 2096-2101

Christner, J. A., Münck, E., Kent, T. A., Janick, P. A., Salerno, J. C., & Siegel, L. M. (1984) Exchange coupling between siroheme and [4Fe-4S] cluster in E. coli sulfite reductase.

Mössbauer studies and coupling models for a 2-electron reduced enzyme state and complexes with sulfide, J Am Chem Soc 106, 6786-6794.

Cole, J. A. & Ferguson, S. J. (1988) Forty-Second Symposium of the Society for Gerneral Microbiology: The Nitrogen and Sulphur Cycles, Cambridge Univ. Press, Cambridge.

Collaborative Computational Project No. 4. (1994) The CCP4 Suite: Programs for protein crystallography, Acta Cryst D 50, 760-763.

Cooper, S. J., Garner, C. D., Hagen, W. R., Lindley, P. F. and Bailey, S. (2000) Hybrid-Cluster Protein (HCP) from Desulfovibrio Vulgaris (Hildenborough) at 1.6 Å Resolution, Biochemistry 39, 15044-15054.

Cort, J. R., Santhana Mariappan, S. V. Kim, C.-Y., Park, M. S., Peat, T. S., Waldo, G. S., Terwilliger, T. C. & Kennedy, M. A. (2001) Solution structure of Pyrobaculum aerophilium DsrC, an archaeal homologue of the gamma subunit of dissimilatory sulfite reductase, Eur J Biochem 268, 5842-5850.

Cowtan, K. (1994), Joint CCP4 and ESF-EACBM Newsletter on Protein Crystallography, 31, p34-38.

Cowtan, K. D. & Main, P. (1996) Phase combination and cross validation in iterated density-modification calculations, Acta Cryst D 52, 43-48.

Crane, B. R., Siegel, L. M., and Getzoff, E. D. (1995) Sulfite reductase structure at 1.6 Å:

evolution and catalysis for reduction of inorganic anions, Science 270, 59-67.

Crane, B. R., Siegel, L. M., and Getzoff, E. D. (1997a) Structures of the siroheme- and Fe4S4-containing active center of sulfite reductase in different states of oxidation: heme activation via reduction-gated exogenous ligand exchange, Biochemistry 36, 12101-12119.

Crane, B. R., Siegel, L. M., and Getzoff, E. D. (1997b) Probing the catalytic mechanism of sulfite reductase by X-ray crystallography: structures of the Escherichia coli hemoprotein in complex with substrates, inhibitors, intermediates, and products, Biochemistry 36, 12120-12137.

Cromer, D. T. & Liberman, D. (1970) Relativistic calculation of anomalous scattering factors for X-rays, J Chem Phys 53, 1891-1898.

Cypionka, H., and Pfennig, N. (1986) Growth yields of Desulfotomaculatum orientis with hydrogen in chemostat culture, Arch Microbiol 143, 396-399.

Dahl, C., and Trüper, H. G., (2001) Sulfite Reductase and APS Reductase from Archaeoglobus fulgidus, Methods Enzymol 331, 472-441.

Dahl, C., Koch, H.-G., Keuken, O., and Trüper, H. G. (1990) Purification and characterization of ATP sulfurylase from the exremely thermophilic archaebacterial sulfate-reducer, Archaeoglobus fulgidus, FEMS Microbiol Lett 67, 27-32.

Dahl, C., Speich, N. and Trüper, H. G., (1994) Enymology and Molecular Biology of Sulfate reduction in Extremely Thermophilic Archaeon Archaeoglobus fulgidus, Methods Enzymol 243, 331-352.

Dauter, Z., Wilson, K. S., Sieker, L. C., Meyer, J., and Moulis, J.-M. (1997) Atomic resolution (0.94 A) structure of Clostridium acidurici ferredoxin. Detailed geometry of [4Fe-4S] clusters in a protein, Biochemistry 36, 16065-16073

Denke, E., Merbitz-Zahradnik, T., Hatzfeld, O. M., Snyder, C. H., Link, T. A., and Trumpower, B.L. (1998) Alteration of the midpoint potential and catalytic activity of the rieske sulfur protein by changes of amino acids forming hydrogen bonds to the iron-sulfur cluster, J Biol Chem 273, 9085-9093

Deppenmeier, U., Blaut, M., and Gottschalk, G. (1991) H2:heterodisulfide oxidoreductase, a second energy-conserving system in the methanogenic strain Gö 1, Arch Microbiol 155, 272-277.

Deppenmeier, U., Blaut, M., Mahlmann, A., and Gottschalk, G. (1990) Reduced F420:heterodisulfide oxidoreductase, a proton-translocating redox system in methanogenic bacteria, Proc Natl Acad Sci USA 87, 9449-9453.

Deppenmeier, U., Müller, V., and Gottschalk, G. (1996) Pathways of energy conservation in methanogenic Archaea, Arch Microbiol 165, 149-163.

Deuereux, R., Delaney, M., Widdel, F. & Stahl, H. D. (1989) Natural relationship among sulfate-reducing eubacteria, J Bacteriol 171, 6689-6695.

Diederichs, K. (2003) personal communication.

Dixon, D. A., Lindner, D. L., Branchaud, B. & Libscomb, W. N. (1979) Conformations and electronic structures of oxidized and reduced isoalloxazine, Biochemistry 18, 5770-5775.

Drenth, J. (1994) Principles of Protein X-ray Crystallography, Springer Verlag, Heidelberg.

Einsle, O., Akif Tezcan, E., Andrade, S. L. A., Schmid, B., Yoshida, M., Howard, J. B., Rees, D. C. (2002) Nitrogenase MoFe-Protein at 1.16 Å Resolution: A Central Ligand in the FeMo-Cofactor, Science 297, 1696-1700.

Esnouf, R. M. (1997) An extensively modified version of MolScript that includes greatly enhanced coloring capabilities, J Mol Graph 15, 132-134.

Feng, D. F., and Doolittle, R. F. (1997) Converting amino acid alignment scores into measures of evolutionary time: a simulation study of various relationships, J Mol Evol 44, 361-370.

Feng, D. F., Cho, G., and Doolittle, R. F. (1997) Determining divergence times with a protein clock: update and reevaluation, Proc Natl Acad Sci USA 94, 13028-13033.

Fitz, R. M., and Cypionka, H. (1989) A study on electron transport-driven proton translocation in Desulfovibrio desulfuricans, Arch Microbiol 152, 369-376.

Fitz, R. M., and Cypionka, H. (1991) Generation of a proton gradient in Desulfovibrio vulgaris, Arch Microbiol 155, 444-448.

Fritz, G. (1999) Structure and function of redox proteins involved in dissimilatory sulfate reduction: Adenosine 5'-phosphosulfate reductase and multiheme cytochromes, Ph. D. Thesis, Universität Konstanz, Konstanz.

Fritz, G., Büchert, T., and Kroneck, P. M. H. (1999) in Flavins and Flavoproteins (Ghisla, S., Kroneck, P. M. H., Macheroux, P., and Sund, H., eds), pp. 767-774, R. Weber Agency for Scientific Publications, Berlin

Fritz, G., Büchert, T., and Kroneck, P. M. H. (2002a) The function of the [4Fe-4S] clusters and FAD in bacterial and archaeal adenylylsulfate reductases. Evidence for flavin-catalyzed reduction of adenosine 5'-phosphosulfate,J Biol Chem 277, 26066-26073

Fritz, G., Büchert, T., Huber, H., Stetter, K. O., and Kroneck, P. M. H. (2000) Adenylylsulfate reductases from archaea and bacteria are 1:1 alphabeta-heterodimeric iron-sulfur flavoenzymes high similarity of molecular properties emphasizes their central role in sulfur metabolism, FEBS Lett 473, 63-66

Fritz, G., Roth, A., Schiffer, A., Büchert, T., Bourenkov, K., Bartunik, H. D., Huber, H., Stetter, K. O., Kroneck, P. M. H., and Ermler, U. (2002b) Crystal structure of the adenylylsulfate reductase from the hyperthermophilic Archaeon Archaeoglobus fulgidus at 1.6Ǻ resolution, Proc Natl Acad Sci USA 99, 1836-1841.

Fu, J., Gnatt, A. L., Bushnell, D. A., Jensen, G. J., Thompson, N. E., Burgess, R. R., David, P. R. and Kornberg, R. D. (1999) Yeast RNA Polymerase II at 5 Å Resolution, Cell 98, 799–

810.

Fujii, T., Hata, Y., Wakaki, T., Tanaka, N., and Oshima, T. (1996) Novel zinc-binding centre in thermoacidophilic archaeal ferredoxins, Nature Struct Biol 3, 834-837

Ghisla, S. & Massey, V. (1986) New flavins for old: artificial flavins as active site probes of flavoproteins Biochem J 239, 1–12.

Ghosh, P., Bill, E., Weyhermuller, T., Neese, F., Wieghardt, K. (2003) Noninnocence of the ligand glyoxal-bis(2-mercaptoanil). The electronic structures of [Fe(gma)]2, [Fe(gma)(py)] x py, [Fe(gma)(CN)]1-/0, [Fe(gma)I], and [Fe(gma)(PR3)(n)] (n = 1, 2). Experimental and theoretical evidence for "excited state" coordination, J Am Chem Soc 125, 1293-1308.

Goa, J. (1953) A micro-biuret method for protein determination: determination of total protein in cerebrospinal fluid, Scand J Clin Lab Invest 5, 219-222.

Green, D. W., Ingram, V. M. & Perutz, M. F. (1954) The structure of hemoglobin. IV. Sign determination by the isomorphous replacement method, Proc Roy Soc A 225, 287-307.

Grouse, B. R. Meyer, J., Johnson, M. K. (1995) Spectroscopic Evidence for a Reduced Fe2S2

Cluster with a S = 9/2 Ground State in Mutant Forms of Clostridium pasteurianum 2Fe Ferredoxin, J Am Chem Soc 117, 9612-9613.

Guex, N. & Peitsch, M. C. (1996) Swiss-PdbViewer: A fast and easy-to-use PDB viewer for Macintosh and PC, PDB Quart Newslett 77, 7-10.

Hagen, W. R., Wassink, H., Eady, R. R., Smith, B. E. & Haaker, H. (1987) Quantitative EPR of an S=7/2 system in thione-oxidized MoFe proteins of nitrogenase, Eur J Biochem 169, 457-465.

Hall, L. H., Bowers, M. L., and Durfor, C. N. (1987) Further consideration of flavin coenzyme biochemistry afforded by geometry-optimized molecular orbitas calculations, Biochemistry 26, 7401-7409.

Hall, M. H., Prince, R. H. & Cammack, R. (1979) EPR spectroscopy of the iron-sulphur cluster and sirohaem in the dissimilatory sulphite reductase from Desulfovibrio Gigas, Biochim Biophys Res Commun 581, 27-33.

Hansen, T. A. (1994) Metabolism of sulfate-reducing prokaryotes, Antonie Van Leeuwenhoek 66, 165-185.

Hendrickson, W. A., Smith, J. L., Phizackerley, R. P. & Merrit, E. A. (1988) Crystallographic structure analysis of lamprey hemoglobin from anomalous dispersion of synchrotron radiation, Proteins 4, 77-88.

Hipp, W. M., Pott, A. S., Thum-Schmitz, N., Faath, I., Dahl, C., and Trüper, H. G. (1997) Towards the phylogeny of APS reductases and sirohaem sulfite reductases in sulfate-reducing and sulfur-oxidizing prokaryotes, Microbiology 143, 2891-2902.

Hittel, D. S. & Voordouw, G. (2000) Overexpression, purification and immunodetection of DsrD from Desulfovibrio vugaris (Hildenborough), Antonie Van Leeuwenhoek 77, 13–22.

Hollemann, A. F. & Wiberg, E. (1985) Lehrbuch der anorganischen Chemie, 91.-100. Aufl., Walter de Gruyter, Berlin.

Holm, L., and Sander, C. (1993) Protein structure comparison by alignment of distance matrices, J Mol Biol 233, 123-138

Holm, L., and Sander, C. (1993) Protein structure comparison by alignment of distance matrices, J Mol Biol 233, 123-138

Hoppe, W. (1957) Die Faltmolekülmethode: eine neue Methode zur Bestimmung der Kristallstruktur bei ganz oder teilweise bekannten Molekülstrukturen, Acta Cryst 10, 750-751.

Huber, R. (1965) Die automatisierte Faltmolekülmethode, Acta Cryst 19, 353-356.

Iverson, T. M., Luna-Chavez, C., Cecchini, G., and Rees, D. C. (1999) Structure of the Escherichia coli fumarate reductase respiratory complex, Science 284, 1961-1966

Jancarik, J. & Kim, S.-H. (1991) Sparse matrix sampling: a screening method for crystallization of proteins, J Appl Cryst 24, 409-411.

Janick P. & Siegel L. M. (1983) Electron paramagnetic resonance and optical evidence for interaction between siroheme and Fe4S4 prosthetic groups in complexes of Escherichia coli sulfite reductase hemoprotein with added ligands, Biochemistry 22, 504-15.

Janick, P. & Siegel, L. M. (1982) Electron Paramagnetic Resonance and optical Spectroscopic evidence for interaction between siroheme and Fe4S4 prostetic groups in Escherichia coli sulfite reductase hemoprotein subunit, Biochemistry 21, 3538-3547.

Janick, P., Rueger, D. C., Krueger, R. J., Barber, M. J., Siegel, L. M. (1983) Characterization of complexes between Escherichia coli sulfite reductase hemoprotein subunit and its substrates sulfite and nitrite, Biochemistry 22, 396.

Jones, T., Zou, J., Cowan, S., Kjeldgaard, M. (1998) Improved methods for building protein models in electron-density maps and the location of errors in these models, Acta Cryst A47, 110-119.

Kabsch, W. (1993) Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants, J Appl Cryst 26, 795-800.

Karkhoff-Schweizer, R. R., Huber, D. P., and Voordouw, G. (1995) Conservation of the genes for dissimilatory sulfite reductase from Desulfovibrio vulgaris and Archaeoglobus fulgidus allows their detection by PCR, Appl Environ Microbiol 61, 290–296.

Karplus, P. A. and Schulz, G. E. (1987) Refined structure of glutathione reductase at 1.54 Å resolution, J Mol Biol 195, 701–729.

Kendrew, J. C., Dickerson, R. E., Strandberg, B. E., Hart, R. G., Davies, D. R., Phillips, D. C.

& Shore, V. C. (1960) Structure of myoglobin; a three-dimensional Fourier synthesis at 2 Å resolution, Nature 185, 422-427.

Klenk, H. P., Clayton, R. A., Tomb, J. F., White, O., Nelson, K. E., Ketchum, K. A., Dodson, R. J., Gwinn, M., Hickey, E. K., Peterson, J. D., Richardson, D. L., Kerlavage, A. R., Graham, D. E., Kyrpides, N. C., Fleischmann, R. D., Quackenbush, J., Lee, N. H., Sutton, G.

G., Gill, S., Kirkness, E. F., Dougherty, B. A., McKenney, K., Adams, M. D., Loftus, B., and Venter, J. C. (1997) The complete genome sequence of the hyperthermophilic, sulphate-reducing archaeon Archaeoglobus fulgidus [published erratum appears in Nature 1998 Jul 2;394(6688):101], Nature 390, 364-370.

Kleywegt, G .J. & Jones, T. A. (1994) in From First Map to Final Model (Bailey, S., Hubbard, R. and Waller, D. eds) pp. 59-66 SERC Daresbury Laboratory, Warrington.

Kleywegt, G. J. & Jones, T. A. (1999) Software for handling macromolecular envelopes, Acta Cryst D55, 941-944.

Kleywegt, G. J. (1996) Use of Non-crystallographic Symmetry in Protein Structure Refinement, Acta Cryst D52, 842-857.

Kraulis, P. (1991) MOLSCRIPT: a program to produce both detailed and schematic plots of proteins, J Appl Cryst 24, 946-950.

Kroder, M.-J. (1997) Biochemie und Mikrobiologie der Reduktion von Trithionat und Thiosulfat in dem sulfatreduzierenden Bakterium Desulfovibrio desulfuricans, Ph. D. Thesis, Universität Konstanz, Konstanz.

La Fortelle, E. & Bricogne, G. (1997) Maximum- Likelihood Heavy- Atom Parameter Refinement for Multiple Isomorphous Replacement and Multiwavelength Anomalous Diffraction Methods, Methods Enzymol 276, 472-494.

Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4, Nature 227, 680-685.

Lampreia, J., Pereira, A. S., and Moura, J. J. G. (1994) Adenylylsulfate reductase from sulfate-reducing bacteria, Methods Enzymol 243, 241-260.

Lancaster, C. R. D., Kröger, A., Auer, M., and Michel, H. (1999) Structure of fumarate reductase from Wolinella succinogenes at 2.2 Å resolution, Nature 402, 377-385.

Lawson Daku, L. M., Pecaut, J., Lenormand-Foucaut, A., Vieux-Melchior, B., Iveson, P. and Jordanov, J. (2003) Investigation of the Reduced High-Potential Iron-Sulfur Protein from Chromatium vinosum and Relevant Model Compounds: A Unified Picture of the Electronic Structure of [Fe4S4]²⁺ Systems through Magnetic and Optical Studies, Inorg Chem 42, 6824-6850.

Lee, J.-P. & Peck, H. D. (1971) Purification of the enzyme reducing trithionate from Desulfovibrio Gigas and its identification as desulfoviridin, Biochem Biophys Res Commun 45, 583-589.

Lee, J.-P., LeGall, J. & Peck, H. D. (1973) Isolation of Assimilatory- and Dissimilatory-Type Sulfite Reductases from Desulfovibrio vulgaris, J Bacteriol 115, 529-542.

LeGall, J., and Fauque, G. (1988) Dissimilatory reduction of sulfur compounds, in biology of anaerobic microorganisms. (Zehnder, A. J. B., Ed.), pp. 587-639, John Wiley and Sons, New York.

Lennon, B. W., Williams, C. H. & Ludwig, M. (1999) Crystal structure of reduced thioredoxin reductase from Escherichia coli: Structural flexibility in the isoalloxazine ring of the flavin adenine dinucleotide cofactor, Protein Science 8, 2366-2379.

Leys, D., Tsapin, A. S., Nealson, K. H., Meyer, T. E., Cusanovich, M. A. & Van Beeumen, J.

J. (1999) Structure and mechanism of the flavocytochrome c fumarate reductase of Shewanella putrefaciens MR-1, Nat Struct Biol 6, 1113-1117.

Li, J., Nelson, M. R., Peng, C. Y., Bashford, D., and Noodleman, L. (1998) Incorporating Protein Environments in Density Functional Theory: A Self-Consistent Reaction Field

Calculation of Redox Potentials of [2Fe2S] Clusters in Ferredoxin and Phthalate Dioxygenase Reductase, J Phys Chem A 102, 6311-6324.

Lui, S. M., Soriano, A. & Cowan, J. A. (1994) Electronic properties of the dissimilatory sulfite reductase from Desulfovibrio vulgaris (Hildenborough): comparitative studies of optical spectra and relative reduction potentials for the [Fe4S4]-sirohaem prostetic centers, Biochem J 304, 441-447.

Macedo, S., Mitchell, E. P., Romao, C. V., Cooper, S. J., Coelho, R., Liu, M. Y., Xavier, A.

V., LeGall, J., Bailey, S. Garner, C. D. Hagen, W. R., Teixeira, M., Carrondo, M. A. and Lindley, P. (2002) Hybrid cluster proteins (HCPs) from Desulfovibrio desulfuricans ATCC 27774 and Desulfovibrio vulgaris (Hildenborough): X-ray structures at 1.25 Å resolution using synchrotron radiation, J Biol Inorg Chem 7, 514-525.

Marritt, S. J. & Hagen, W. R. (1996) Dissimilatory sulfite reductase revisited, Eur J Biochem 238, 724-727.

Massa, W. (1994) Kristallstrukturbestimmung, Teubner Studienbücher: Chemie, Stuttgart.

Massey, V., Müller, F., Feldberg, R., Schuman, M., Sullivan, P. A., Howell, L. G., Mayhew, S. G., Matthews, R. G., and Foust, G. P. (1969) The reactivity of flavoproteins with sulfite.

Possible relevance to the problem of oxygen reactivity, J Biol Chem 244, 3999-4006.

Maté, M. J., Ortiz-Lombardía, M., Boitel, B., Haouz, A., Tello, D., Susin, S. A., Penninger, J., Kroemer, G. and Alzari, P. M. (2002) The crystal structure of the mouse apoptosis-inducing factor AIF, Nature Struct Biol 6, 442-446.

Mattevi, A., Tedeschi, G., Bacchella, L., Coda, A., Negri, A., and Ronchi, S. (1999) Structure of L-aspartate oxidase: implications for the succinate dehydrogenase/fumarate reductase oxidoreductase family, Structure 7, 745-756

Matthews, B. W. (1968) Solvent content of protein crystals, J Mol Biol 33, 491-497.

McPherson, A. (1982) Preparation and analysis of protein crystals, Wiley & Sons, New York.

McRee, D. E. (1993) Practical Protein Crystallography, Academic Press Inc., San Diego.

Merritt, E. A. & Bacon, D. J. (1997) Raster3D: Photorealistic molecular graphics, Meth Enzymol 277, 505-524.

Michaels, G. B., Davidson, J. T., and Peck, H. D., Jr. (1970) A flavin-sulfite adduct as an intermediate in the reaction catalyzed by adenylyl sulfate reductase from Desulfovibrio vulgaris, Biochem Biophys Res Commun 39, 321-328.

Mizuno, N., Voordouw, G., Miki, K., Sarai, A. & Higuchi, Y. (2003) Crystal Structure of Dissimilatory Sulfite Reductase D (DsrD) Protein—Possible Interaction with B- and Z-DNA by Its Winged-Helix Motif, Structure 11, 1133–1140.

Moura, I., LeGall, J., Lino, A. R., Peck, H. D., Fauque, G., Xavier, A. V., DerVartanian, D.

V., Moura, J. J. G., & Huynh, B. H. (1988) Characterisation of Two Dissimilatory Sulfite Reductases from the Sulfate-Reducing Bacteria. Mössbauer and EPR Studies, J Am Chem Soc 110, 1075-1082.

Müller, F., and Massey, V. (1969) Flavin-sulfite complexes and their structures, J Biol Chem 244, 4007-4016.

Murphy, M. J. & Siegel, L. M. (1973) Siroheme and sirohydrochlorin. The basis for a new type of porphyrin-related prosthetic group common to both assimilatory and dissimilatory sulfite reductases, J Biol Chem 248, 6911

Neese, F. (1995) The program EPR, Quantum Chemistry Program Exchange. Bulletin 15:5.

Odom, J. M., and Peck, H. D., Jr. (1981) Localization of dehydrogenases, reductases, and electron transfer components in the sulfate-reducing bacterium Desulfovibrio gigas, J Bacteriol 147, 161-169.

Ostrowski, J., Barber, M. J., Rueger, D. C., Miller B. E., Siegel, L. M. & Kredich, N. M.

(1989) Characterization of the flavoprotein moieties of NADPH-sulfite reductase from Salmonella typhimurium and Escherichia coli. Physicochemical and catalytic properties, amino acid sequence deduced from DNA sequence of cysJ, and comparison with NADPH-cytochrome P-450 reductase, J Biol Chem 264, 15726-15808.

Otwinowski, Z. & Minor, W. (1996) Processing of X-ray diffraction data collected in oscillation mode, Meth Enzymol 276, 307-326.

Peck, H. D., Jr. & Bramlett, R. N. (1982) Flavoproteins in sulfur metabolism, in Flavins and Flavoproteins (Massey, V. & Williams, C. H., ed.), Elsevier Science Publishers, Amsterdam

Peck, H. D., Jr. (1959) The ATP-dependent reduction of sulfate with hydrogen in extracts of Desulfovibrio desulfuricans, Proc Natl Acad Sci USA 45, 701-708.

Peck, H. D., Jr., and LeGall, J. (1994) Inorganic Microbial Sulfur Metabolism, Methods Enzymol 243.

Peinemann, S., Hedderich, R., Blaut, M., Thauer, R. K., and Gottschalk, G. (1990) ATP Synthesis coupled to electron transfer from H2 to the heterodisulfide of 2-mercaptoethanesulfonate and 7-mercaptoheptanoylthreonine phosphate in vesicle preparations of the methanogenic bacterium strain Gö 1, FEBS Lett 263, 57-60.

Perutz, M. F., Rossmann, M. G., Cullis, A. F., Muirhead, H., Will, G. & North, A. C. T.

(1960) Structure of haemoglobin; a three-dimensional Fourier synthesis at 5.5 Å resolution, obtained by X-ray analysis, Nature 185, 416-422.

Pflugrath, J. W. (1999) The finer things in X-ray diffraction data collection, Acta Cryst D 55, 1718-1725.

Philippsen, A. (2002) DINO: Visualizing Structural Biology http://www.dino3d.org

Pierik, A. J., and Hagen, W. R. (1991) S = 9/2 EPR signals are evidence against coupling between the siroheme and the Fe/S cluster prosthetic groups in Desulfovibrio vulgaris (Hildenborough) dissimilatory sulfite reductase, Eur J Biochem 195, 505-516.

Postgate, J. R. (1984) The sulphate reducing bacteria, 2nd ed., Cambridge University Press, Cambridge.

Rabilloud, T. (1990) Mechanism of protein silver staining in polyacrylamide gels: a ten year synthesis, Electrophoresis 11, 785-794.

Rawlings, J., Shah, V. K., Chisnell, J. R., Brill, W. J., Zimmermann, R., Münck, E., Orme-Johnson, W. H. (1978) Novel metal cluster in the iron-molybdenum cofactor of nitrogenase.

Spectroscopic evidence, J Biol Chem 253, 1001-4.

Roberts, D. L., Freeman, F. E., and Kim, J.-J. P. (1996) Three-dimensional structure of human electron transfer flavoprotein to 2.1-A resolution, Proc Natl Acad Sci USA 93, 14355-14360 Rossmann, M. G. & Blow, D. M. (1962) The detection of subunits within the crystallographic asymmetric unit, Acta Cryst 15, 24-31.

Roth, A., Fritz, G., Büchert, T., Huber, H., Stetter, K. O., Ermler, U., and Kroneck, P. M. H.

(2000) Crystallization and preliminary X-ray analysis of adenylylsulfate reductase from Archaeoglobus fulgidus, Acta Cryst D56, 1673-1675.

Schägger, H. & von Jagow, G. (1987) Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa, Anal Microbiol 158, 418-421.

Schidlowski, M. (1986) Evolution of the early sulfur cycle, in Geochemistry of the Earth surface and process of Mineral Formation, pp. 29-49, Granada.

Schidlowski, M., Hayes, J. M., and Kaplan, I. R. (1983) Isotopic inferences of ancient biochemistries: carbon, sulfur, hydrogen, and nitrogen, in Earth's earliest biosphere, its origin and evolution. (Schopf, J. W., Ed.), pp. 149-186, Princeton University Press, Princeton, N.J.

Schiffer, A (2000) Structural and functional investigations on the iron-sulfur flavoenzyme adenosine 5'-phosphosulfate reductase (APSR) from the sulfate-reducing archaeon Archaeoglobus fulgidus, Diploma Thesis, Universität Konstanz, Konstanz.

Schneider, T. R., Sheldrick, G. M. (2002) Substructure solution with SHELXD, Acta Cryst D 58, 1772-1779.

Schreuder, H. A., Prick, P. A. J., Wierenga, R. K., Vriend, G., Wilson, K. S., Hol, W. G. J.

and Drenth, J. (1989) Crystal structure of the p-hydroxybenzoate hydroxylase-substrate complex refined at 1.9 Å resolution. Analysis of the enzyme-substrate and enzyme-product complexes, J Mol Biol 208, 679–696.

Siegel, L. M. & Davis, P. S. (1974) Reduced nicotinamide adenine dinucleotide phosphate-sulfite reductase of enterobacteria. IV. The Escherichia coli hemoflavoprotein: subunit

Siegel, L. M. & Davis, P. S. (1974) Reduced nicotinamide adenine dinucleotide phosphate-sulfite reductase of enterobacteria. IV. The Escherichia coli hemoflavoprotein: subunit

Im Dokument Structural and functional investigations on multi-site metallo enzymes of the biological sulfur cycle (Seite 112-134)