Journal of Bioenergetics and Biomembranes

, Volume 26, Issue 1, pp 67–88 | Cite as

Structure-function studies of [2Fe-2S] ferredoxins

  • Hazel M. Holden
  • Bruce L. Jacobson
  • John K. Hurley
  • Gordon Tollin
  • Byung-Ha Oh
  • Lars Skjeldal
  • Young Kee Chae
  • Hong Cheng
  • Bin Xia
  • John L. Markley
Article

Abstract

The ability to overexpress [2Fe-2S] ferredoxins inEscherichia coli has opened up exciting research opportunities. High-resolution x-ray structures have been determined for the wild-type ferredoxins produced by the vegetative and heterocyst forms ofAnabaena strain 7120 (in their oxidized states), and these have been compared to structural information derived from multidimensional, multinuclear NMR spectroscopy. The electron delocalization in these proteins in their oxidized and reduced states has been studied by1H,2H,13C, and15N NMR spectroscopy. Site-directed mutagenesis has been used to prepare variants of these ferredoxins. Mutants (over 50) of the vegetative ferredoxin have been designed to explore questions about cluster assembly and stabilization and to determine which residues are important for recognition and electron transfer to the redox partnerAnabaena ferredoxin reductase. The results have shown that serine can replace cysteine at each of the four cluster attachment sites and still support cluster assembly. Electron transfer has been demonstrated with three of the four mutants. Although these mutants are less stable than the wild-type ferredoxin, it has been possible to determine the x-ray structure of one (C49S) and to characterize all four by EPR and NMR. Mutagenesis has identified residues 65 and 94 of the vegetative ferredoxin as crucial to interaction with the reductase. Three-dimensional models have been obtained by x-ray diffraction analysis for several additional mutants: T48S, A50V, E94K (four orders of magnitude less active than wild type in functional assays), and A43S/A45S/T48S/A50N (quadruple mutant).

Key words

[2Fe-2S] ferredoxins electron transport x-ray crystallography nuclear magnetic resonance spectroscopy fast reaction kinetics mutagenesis iron-sulfur cluster assembly heterologous expression stable-isotope labeling Anabaena 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Alam, J., Whitaker, R. A., Krogmann, D. W., and Curtis, S. E. (1986). Isolation and sequence of the gene for ferredoxin I from the cyanobacteriumAnabaena sp. strain PCC 7120,J. Bacteriol. 168, 1265–1271.Google Scholar
  2. Ausubel, F. M., Brent, R., Kingston, R. E., Moore, D. D., Seidman, J. G., Smith, J. A., and Struhl, K. (eds.) (1989).Current Protocols in Molecular Biology, Wiley, New York.Google Scholar
  3. Backes, G., Mino, Y., Loehr, T. M., Meyer, T. E., Cusanovich, M. A., Sweeney, W. V., Adman, E. T., and Sanders-Loehr, J. (1991). The environment of Fe4S4 clusters in ferredoxins and high-potential iron proteins. New information from x-ray crystallography and resonance Raman spectroscopy,J. Am. Chem. Soc. 113, 2055–2064.Google Scholar
  4. Barker, W. C., George, D. G., Srinivasarao, G. Y., and Yeh, L. S. (1992). Database of protein sequence alignments,Biophys. J. 61, A348 (Abstract #2000).Google Scholar
  5. Bernstein, F. C., Koetzle, T. F., Williams, G. J. B., Meyer, E. F., Jr., Brice, M. D., Rogers, J. R., Kennard, O., Shimanouchi, T., and Tasumi, M. (1977). The protein data bank: a computer-based archival file for macromolecular structures,J. Mol. Biol. 112, 535–542.Google Scholar
  6. Bhattacharyya, A. K., Tollin, G., Davis, M., and Edmondson, D. E. (1983). Laser flash photolysis studies of intramolecular electron transfer in milk xanthine oxidase,Biochemistry 22, 5270–5279.Google Scholar
  7. Böhme, H., and Haselkorn, R. (1988). Molecular cloning and nucleotide sequence analysis of the gene coding for heterocyst ferredoxin from the cyanobacteriumAnabaena sp. strain PCC 7120,Mol. Gen. Genet. 214, 278–285.Google Scholar
  8. Böhme, H., and Haselkorn, R. (1989). Expression ofAnabaena ferredoxin genes inEscherichia coli, Plant Mol. Biol. 12, 667–672.Google Scholar
  9. Böhme, H., and Schrautemeier, B. (1987). Comparative characterization of ferredoxins from heterocysts and vegetative cells ofAnabaena variabilis, Biochim. Biophys. Acta 891, 1–7.Google Scholar
  10. Breiter, D. R., Meyer, T. E., Rayment, I., and Holden, H. M. (1991). The molecular structure of the high-potential iron-sulfur protein isolated fromEctothiorhodospira halophila determined at 2.5 Å resolution,J. Biol. Chem. 266, 18660–18867.Google Scholar
  11. Chae, Y. K., Abildgaard, F., Mooberry, E. S., and Markley, J. L. (1993). Multinuclear, multidimensional NMR studies ofAnabaena 7120 heterocyst ferredoxin. Sequence-specific resonance assignments and secondary structure in solution of the oxidized form,Biochemistry, submitted.Google Scholar
  12. Chan, T.-M., and Markley, J. L. (1982). Heteronuclear (1H,13C) two-dimensional chemical shift correlation NMR spectroscopy of a protein. Ferredoxin fromAnabaena variabilis, J. Am. Chem. Soc. 104, 4010–4011.Google Scholar
  13. Chan, T.-M., and Markley, J. L. (1983). Nuclear magnetic resonance studies of two-iron-two-sulfur ferredoxins. 5. Hyperfine-shifted peaks in1H and13C spectra,Biochemistry 22, 6008–6010.Google Scholar
  14. Chan, T.-M., Hermodson, M. A., Ulrich, E. L., and Markley, J. L. (1983a). Nuclear magnetic resonance studies of two-iron-two-sulfur ferredoxins. 2. Determination of the sequence ofAnabaena variabilis ferredoxin II, assignment of aromatic resonances in proton spectra, and effects of chemical modifications,Biochemistry 22, 5988–5995.Google Scholar
  15. Chan, T.-M., Ulrich, E. L., and Markley, J. L. (1983b). Nuclear magnetic resonance studies of two-iron-two-sulfur ferredoxins. 4. Interactions with redox partners.Biochemistry 22, 6002–6007.Google Scholar
  16. Cheng, H., Westler, W. M., Xia, B., Oh, B.-H., and Markley, J. L. (1993a). Protein expression, selective isotopic labeling, and analysis of hyperfine-shifted NMR signals ofAnabaena 7120 vegetative [2Fe-2S] ferredoxin, in preparation.Google Scholar
  17. Cheng, H., Xia, B., Reed, G. H., and Markley, J. L. (1993b). Optical, EPR and1H NMR spectroscopy of serine-ligated [2Fe-2S] ferredoxins produced by site-directed mutagenesis of cysteine residues in recombinantAnabaena 7120 vegetative ferredoxin,Biochemistry, submitted.Google Scholar
  18. Coghlan, V. M., and Vickery, L. E. (1989). Expression of human ferredoxin and assembly of the iron-sulfur center inEscherichia coli.Proc. Natl. Acad. Sci. USA 86, 835–839.Google Scholar
  19. Coghlan, V. M., and Vickery, L. E. (1991). Site-specific mutations in human ferredoxin that affect binding to ferredoxin reductase and cytochrome P450scc, J. Biol. Chem. 266, 18606–18612.Google Scholar
  20. Coghlan, V. M., and Vickery, L. E. (1992). Electrostatic interactions stabilizing ferredoxin electron transfer complexes. Distribution by “conservative” mutations,J. Biol. Chem. 267, 8932–8935.Google Scholar
  21. Cupp, J. R., and Vickery, L. E. (1988). Identification of free and [Fe2S2]-bound cysteine residues of adrenodoxin,J. Biol. Chem. 263, 17418–17421.Google Scholar
  22. Cusanovich, M. A. (1991). Photochemical initiation of electron transfer reactions.Photochem. Photobiol. 53, 845–857.Google Scholar
  23. Cushman, D. W., Tsai, R., and Gunsales, I. C. (1967). The ferroprotein component of a methylene hydroxylase,Biochem. Biophys. Res. Commun. 26, 577–583.Google Scholar
  24. Deng, W. P., and Nickoloff, J. A. (1992). Site-directed mutagenesis of virtually any plasmid by eliminating a unique site,Anal. Biochem. 200, 81–88.Google Scholar
  25. Dugad, L. B., Le Mar, G. N., Banci, L., and Bertini, I. (1990). Identification of localized redox states in plant-type two-iron ferredoxins using the nuclear Overhauser effect,Biochemistry 29, 2263–2271.Google Scholar
  26. Dunham, W. R., Palmer, G., Sands, R. H., and Bearden, A. J. (1971). On the structure of the iron-sulfur complex in the two-iron ferredoxins,Biochim. Biophys. Acta 253, 373–384.Google Scholar
  27. Evans, D. J., and Leigh, G. J. (1991). The coordination of esters of amino acids to {Fe4S4}2+ clusters,J. Inorg. Biochem. 42, 25–35.Google Scholar
  28. Fukuyama, K., Hase, T., Matsumoto, S., Tsukihara, T., Katsube, Y., Tanaka, N., Kakudo, M., Wada, K., and Matsubara, H., (1980). Structure ofS. platensis [2Fe-2S] ferredoxin and evolution of chloroplast-type ferredoxins,Nature (London)286, 522–524.Google Scholar
  29. Gerber, N. C., Horiuchi, T., Koga, H., and Sligar, S. G. (1990). Identification of 2Fe-2S cysteine ligands in putidaredoxin,Biochem. Biophys. Res. Commun. 169, 1016–1020.Google Scholar
  30. Gomez-Moreno, C., Sancho, J., Fillat, M. F., Pueyo, J. J., and Edmondson, D. E. (1987). Complex formation between ferredoxin-NADP+-oxidoreductase and flavodoxin, inFlavins and Flavoproteins 1987 (Edmondson, D. E., and McCormick, D. B., eds.), deGruyter, Berlin, pp. 335–339.Google Scholar
  31. Greenfield, N. J., Wu, X., and Jordan, F. (1989). Proton magnetic resonance spectra of adrenodoxin: features of the aromatic region,Biochim. Biophys. Acta 995, 246–254.Google Scholar
  32. Gurbiel, R. J., Batie, C. J., Sivaraja, M., True, A. E., Fee, J. A., Hoffman, B. M., and Ballou, D. P. (1989). Electron-nuclear double resonance spectroscopy of15N-enriched phthalate dioxygenase fromPseudomonas cepacia proves that two histidines are coordinated to the [2Fe-2S] Rieske-type clusters,Biochemistry 28, 4861–4871.Google Scholar
  33. Gurbiel, R. J., Ohnishi, T., Robertson, D. E., Daldal, F., and Hoffman, B. M. (1991). Q-Band ENDOR spectra of the Rieske protein fromRhodobactor capsulatus ubiquinol-cytochromec oxidoreductase show two histidines coordinated to the [2Fe-2S] cluster.Biochemistry 30, 11579–11584.Google Scholar
  34. Hazzard, J. T., McLendon, G., Cusanovich, M. A., Das, G., Sherman, F., and Tollin, G. (1988). Effects of amino acid replacements in yeast iso-1 cytochromec on heme accessibility and intracomplex electron transfer in complexes with cytochromec peroxidase.Biochemistry 27, 4445–4451.Google Scholar
  35. Hazzard, J. T., Rong, S. Y. and Tollin, G. (1991). Ionic strength dependence of electron transfer from bovine mitochondrial cytochromec to bovine cytochromec oxidase,Biochemistry 30, 213–222.Google Scholar
  36. Hervas, M., Navarro, J. A. and Tollin, G. (1992). A laser flash spectroscopy study of the kinetics of electron transfer from spinach Photosystem I to spinach and algal ferredoxins.Photochem. Photobiol. 56, 319–324.Google Scholar
  37. Houseman, A. L. P., Oh, B.-H., Kennedy, M C., Fan, C., Werst, M. M., Beinert, H., Markley, J. L., and Hoffman, B. M. (1992).14,15N,13C,57Fe,1,2H Q-band ENDOR study of Fe-S proteins with clusters that have endogenous sulfur ligands,Biochemistry 31, 2073–2080.Google Scholar
  38. Hurley, J. K., Salamon, Z., Meyer, T. E., Fitch, J. C., Cusanovich, M. A., Markley, J. L., Cheng, H., Xia, B., Chae, Y. K., Medina, M., Gomez-Moreno, C., and Tollin, G. (1993a). Amino acid residues inAnabaena ferredoxin crucial to interaction with ferredoxin-NADP+ reductase: site-directed mutagenesis and laser flash photolysis,Biochemistry,32, 9346–9354.Google Scholar
  39. Hurley, J. K., Cheng, H., Xia, B., Markley, J. L., Medina, M., Gomez-Moreno C., and Tollin, G., (1993b). An aromatic amino acid residue is required at position 65 inAnabaena ferredoxin for rapid electron transfer to ferredoxin : NADP+ reductase,J. Am. Chem. Soc., in press.Google Scholar
  40. Jacobson, B. L., Chae, Y. K., Böhme, H., Markley, J. L., and Holden, H. M. (1992). Crystallization and preliminary analysis of oxidized recombinant heterocyst [2Fe-2S] ferredoxin fromAnabaena 7120,Arch. Biochem. Biophys. 294, 279–281.Google Scholar
  41. Jacobson, B. L., Chae, Y. K., Markley, J. L., Rayment, I., and Holden, H. M. (1993a). Molecular structure of the oxidized, recombinant, heterocyst [2Fe-2S] ferredoxin fromAnabaena 7120 determined to 1.7Å resolution,Biochemistry 32, 6788–6793.Google Scholar
  42. Jacobson, B. L., Cheng, H., Markley, J. L., and Holden, H. M. (1993b), in preparation.Google Scholar
  43. Karplus, P. A., Daniels, M. J., and Herriott, J. R. (1991). Atomic structure of ferredoxin-NADP+ reductase: prototype for a structurally novel flavoenzyme family,Science 251, 60–66.Google Scholar
  44. Kassner, R. J., and Yang, W. (1977). A theoretical model for the effects of solvent and protein dielectric on the redox potentials of iron-sulfur clusters,J. Am. Chem. Soc. 99, 4351–4355.Google Scholar
  45. Kraulis, P. J. (1991).Molscript: a program to produce both detailed and schematic plots of protein structures,J. Appl. Crystallogr. 24, 946–950.Google Scholar
  46. Kunkel, T. A., Roberts, J. D., and Zakour, R. A. (1987). Rapid and efficient site-specific mutagenesis without phenotypic selection,Methods Enzymol. 154, 367–382.Google Scholar
  47. Masaki, R., Yoshikawa, S., and Matsubara, H. (1982). Steady-state kinetics of oxidation of reduced ferredoxin with ferredoxin-NADP+ reductase,Biochim. Biophys. Acta 700, 101–109.Google Scholar
  48. Mason, J. I., and Boyd, G. S. (1971). The cholesterol side-chain cleavage enzyme system in mitochondria of human term placenta,Eur. J. Biochem. 21, 308–321.Google Scholar
  49. Matsubara, H., and Hase, T. (1983). Phylogenetic consideration of ferredoxin sequences in plants, particularly algae, inProteins and Nucleic Acids in Plant Systematics (Jensen, U., and Fairbrothers, D. E., eds.), Springer-Verlag, Berlin, Heidelberg.Google Scholar
  50. Matsubara, H., Hase, T., Wakabayashi, S., and Wada K. (1980). Structure and evolution of chloroplast- and bacterial-type ferredoxin, inThe Evolution of Protein Structure and Function (Sigman, D. S., and Brazier, H. A. B., eds.), Academic Press, New York, pp. 245–266.Google Scholar
  51. Mauro, J. M., Fishel, L. A., Hazzard, J. T., Meyer, T. E., Tollin, G., Cusanovich, M. A., and Kraut, J. (1988). Tryptophan-191 → phenylalanine, a proximal-side mutation in yeast cytochromec peroxidase that strongly affects the kinetics of ferrocytochromec oxidation,Biochemistry 27, 6243–6256.Google Scholar
  52. Meyer, T. E., Rivera, M., Walker, F. A., Mauk, M. R., Mauk, A. G., Cusanovich, M. A., and Tollin, G. (1993). Laser flash photolysis studies of electron transfer to the cytochromeb 5-cytochromec complex,Biochemistry 32, 622–627.Google Scholar
  53. Mittal, S., Zhu, Y.-Z., and Vickery, L. E. (1988). Molecular cloning and sequence analysis of human placental ferredoxin,Arch. Biochem. Biophys. 264, 383–391.Google Scholar
  54. Miura, S., and Ichikawa, Y. (1991a). Proton nuclear magnetic resonance investigation of adrenodoxin. Assignment of aromatic resonances and evidence for a conformational similarity with ferredoxin fromSpirulina platensis, Eur. J. Biochem. 197, 747–757.Google Scholar
  55. Miura, S., and Ichikawa, Y. (1991b). Conformational change of adrenodoxin induced by reduction of iron-sulfur cluster,J. Biol. Chem. 266, 6252–6258.Google Scholar
  56. Mooberry, E. S., Oh, B.-H., and Markley, J. L. (1989). Improvement of13C-15N chemical shift correlation spectroscopy by implementing time proportional phase incrementation,J. Magn. Reson. 85, 147–149 (1989).Google Scholar
  57. Oh, B.-H., and Markley, J. L. (1990a). Multinuclear magnetic resonance studies of the 2Fe-2S* ferredoxin fromAnabaena sp. strain PCC 7120: 1. Hydrogen-1 resonance assignments and secondary structure in solution of the oxidized form,Biochemistry 29, 3993–4004.Google Scholar
  58. Oh, B.-H., and Markley, J. L. (1990b). Multinuclear magnetic resonance studies of the 2Fe-2S* ferredoxin fromAnabaena sp. strain PCC 7120: 3. Detection and characterization of hyperfine-shifted nitrogen-15 and hydrogen-1 resonances of the oxidized form,Biochemistry 29, 4012–4017.Google Scholar
  59. Oh, B.-H., Westler, W. M., Darba, P., and Markley, J. L. (1988). Protein carbon-13 spin systems by a single two-dimensional nuclear magnetic resonance experiment,Science 240, 908–911.Google Scholar
  60. Oh, B.-H., Westler, W. M., and Markley, J. L. (1989). Carbon-13 spin system directed strategy for assigning cross peaks in the COSY fingerprint region of a protein,J. Am. Chem. Soc. 111, 3083–3085.Google Scholar
  61. Oh, B.-H., Mooberry, E. S., and Markley, J. L. (1990). Multinuclear magnetic resonance studies of the 2Fe-2S* ferredoxin fromAnabaena sp. strain PCC 7120: 2. Sequence-specific carbon-13 and nitrogen-15 resonance assignments of the oxidized form,Biochemistry 29, 4004–4011.Google Scholar
  62. Okamura, T., John, M. E., Zuber, M. X., Simpson, E. R., and Waterman, M. R. (1985). Molecular cloning and amino acid sequence of the precursor form of bovine adrenodoxin: Evidence for a previously unidentified COOH-terminal peptide,Proc. Natl. Acad. Sci. USA 82, 5705–5709.Google Scholar
  63. Peterson, J. A., Lorence, M. C., and Amarneh, B. (1990). Putidaredoxin reductase and putidaredoxin. Cloning, sequence determination, and heterologous expression of the proteins,J. Biol. Chem. 265, 6066–6073.Google Scholar
  64. Pochapsky, T. C., and Ye, X. M. (1991).1H NMR identification of a β-sheet structure and description of folding topology in putidaredoxin,Biochemistry 30, 3850–3856.Google Scholar
  65. Poe, M., Phillips, W. D., Glickson, J. D., and San Pietro, A. (1971). Proton magnetic resonance studies of the ferredoxins from spinach and parsley.Proc. Natl. Acad. Sci. USA 68, 68–71.Google Scholar
  66. Przysiecki, C. T., Bhattacharyya, A. K., Tollin, G., and Cusanovich, M. A. (1985). Kinetics of reduction ofClostridium pasteurianum rubredoxin by laser photoreduced spinach ferredoxin: NADP+ reductase and free flavins,J. Biol. Chem. 260, 1452–1458.Google Scholar
  67. Rayment, I., Wesenberg, G., Meyer, T. E., Cusanovich, M. A., and Holden, H. M. (1992). Three-dimensional structure of the high-potential iron-sulfur protein isolated from the purple phototrophic bacteriumRhodocyclus tenuis determined and refined at 1.5 Å resolution,J. Mol. Biol. 228, 672–686.Google Scholar
  68. Robbins, A. H., and Stout, C. D. (1989). Structure of activated aconitase: formation of the [4Fe-4S] cluster in the crystal,Proc. Natl. Acad. Sci. USA 86, 3639–3643.Google Scholar
  69. Rothery, R. A., and Weiner, J. H. (1991). Alteration of the ironsulfur composition ofEscherichia coli dimethyl sulfoxide reductase by site-directed mutagenesis,Biochemistry 30, 8296–8305.Google Scholar
  70. Rypniewski, W. R., Breiter, D. R., Benning, M. M., Wesenberg, G., Oh, B.-H., Markley, J. L., Rayment, I., and Holden, H. M. (1991). Crystallization and structure determination to 2.5 Å resolution of the oxidized [2Fe-2S] ferredoxin isolated fromAnabaena 7120,Biochemistry 30, 4126–4131.Google Scholar
  71. Salamon, Z., and Tollin, G. (1992). Cyclic voltammetric behavior of [2Fe-2S] ferredoxins at a lipid bilayer modified electrode,Bioelectrochem. Bioenerg. 27, 381–391.Google Scholar
  72. Sambrook, J., Fritsch, E. F., and Maniatis, T. (1989).Molecular Cloning, A Laboratory Manual, Cold Spring Harbor Laboratory Press, Plainview, New York.Google Scholar
  73. Sanger, F., Niklen, S., and Coulson, A. R. (1977). DNA sequencing with chain-terminating inhibitors,Proc. Natl. Acad. Sci. USA 74, 5463–5467.Google Scholar
  74. Schrautemeier, B., and Böhme, H. (1985). A distinct ferredoxin for nitrogen fixation isolated from heterocysts of the cyanobacteriumAnabaena variabilis, FEBS Lett. 184, 304–308.Google Scholar
  75. Skjeldal, L., Westler, W. M., and Markley, J. L. (1990). Detection and characterization of hyperfine shifted resonances in the proton NMR spectrum ofAnabaena 710 ferredoxin at high magnetic fields,Arch. Biochem. Biophys. 278, 482–485.Google Scholar
  76. Skjeldal, L., Markley, J. L., Coghlan, V. M., and Vickery, L. (1991a). Hydrogen-1 NMR spectra of vertebrate [2Fe-2S] ferredoxins. Hyperfine resonances suggest different electron delocalization patterns from plant ferredoxins,Biochemistry 30, 9078–9083.Google Scholar
  77. Skjeldal, L., Westler, W. M., Oh, B.-H., Krezel, A. M., Holden, H. M., Jacobson, B. L., Rayment, I., and Markley, J. L. (1991b). Two-dimensional magnetization exchange spectroscopy ofAnabaena 7120 ferredoxin. Nuclear Overhauser effect and electron self-exchange cross peaks from amino acid residues surrounding the 2Fe-2S* cluster,Biochemistry 30, 7363–7368.Google Scholar
  78. Springer, B. A., and Sligar, S. G. (1987). High-level expression of sperm whale myoglobin inEscherichia coli, Proc. Nat. Acad. Sci., USA 84, 8961–8965.Google Scholar
  79. Stockman, B. J., and Markley, J. L. (1990). Stable-isotope assisted protein NMR spectroscopy in solution, inAdvances in Biophysical Chemistry, Vol. 1 (Bush, C. A., ed.), JAI Press, Greenwich, Connecticut, pp. 1–46.Google Scholar
  80. Sussman, J. L., Shoham, M., and Harel, M. (1989). Protein adaptation to extreme salinity: the crystal structure of 2Fe2S ferredoxin fromHalobacterium Marismortui, inComputer-Assisted Modeling of Receptor-Ligand Interactions: Theoretical Aspects and Applications to Drug Design, Alan R. Liss, New York, pp. 171–187.Google Scholar
  81. Ta, D. T., and Vickery, L. E. (1992). Cloning, sequencing, and overexpression of a [2Fe-2S] ferredoxin gene fromEscherichia coli, J. Biol. Chem. 267, 11120–11125.Google Scholar
  82. Tanaka, M., Haniu, M., Yasunobu, K. T., Roa, K. K., and Hall, D. O. (1976). The complete amino acid sequence ofSpirulina platensis ferredoxin,Biochem. Biophys. Res. Commun. 69, 759–765.Google Scholar
  83. Tollin, G., and Hazzard, J. T. (1991). Intra- and intermolecular electron transfer processes in redox proteins,Arch. Biochem. Biophys. 287, 1–7.Google Scholar
  84. Tollin, G., Hurley, J. K., Hazzard, J. T., and Meyer, T. E. (1993). Use of laser flash photolysis time-resolved spectrophotometry to investigate interprotein and intraprotein electron transfer mechanisms,Biophys. Chem., in press.Google Scholar
  85. Tsukihara, T., Fukuyama, K., Nakamura, M., Katsube, Y., Tanaka, N., Kakudo, M., Wada, K., Hase, T., and Matsubara, H. (1981). X-ray analysis of a [2Fe-2S] ferredoxin fromSpirulina platensis. Main chain fold and location of side chains at 2.5 Å resolution,J. Biochem. 90, 1763–1773.Google Scholar
  86. Tsukihara, T., Fukuyama, K., and Katsube, Y. (1986). Structurefunction relationship of [2Fe-2S] ferredoxins, inIron-Sulfur Protein Research (Matsubara, H., Katsube, Y., and Wada, K., eds.), Japan Sci. Soc. Press, Tokyo, pp. 59–68.Google Scholar
  87. Tsukihara, T., Fukuyama, K., Mizushima, M., Harioka, T., Kusunoki, M., Katsube, Y., Hase, T., and Matsubara, H. (1990). Structure of the [2Fe-2S] ferredoxin I from the blue-green algaAphanothece sacrum at 2.2 Å resolution,J. Mol. Biol. 216, 399–410.Google Scholar
  88. Walker, M. C., Pueyo, J. J., Gomez-Moreno, C., and G. Tollin (1990). Comparison of the kinetics of reduction and intramolecular electron transfer in electrostatic and covalent complexes of ferredoxin-NADP+ reductase and flavodoxin fromAnabaena PCC 7119,Arch. Biochem. Biophys. 281, 76–83.Google Scholar
  89. Walker, M. C., Pueyo, J. J., Navarro, J. A., Gomez-Moreno, C., and Tollin, G. (1991). Comparison of the kinetics of reduction and intramolecular electron transfer in electrostatic and covalent complexes of ferredoxin-NADP+ reductase and flavodoxin fromAnabaena PCC 7119,Arch. Biochem. Biophys. 287, 351–358.Google Scholar
  90. Werth, M. T., Cecchini, G., Manodori, A., Acdrell, B. A. C., Schröder, I., Gunsalus, R. T., and Johnson, M. K. (1990). Sitedirected mutagenesis of conserved cysteine residues inEscherichia coli fumarate reductase: modification of the spectroscopic and electrochemical properties of the [2Fe-2S] cluster,Proc. Natl. Acad. Sci. USA 87, 8965–8969.Google Scholar
  91. Wishart, D. S., Sykes, B. D., and Richards, F. M. (1992). The chemical shift index: a fast and simple method for the assignment of protein secondary structure through NMR spectroscopy,Biochemistry 31, 1647–1651.Google Scholar
  92. Xia, B., Cheng, H., Skjeldal, L., Coghlan, V. M., Vickery, L. E., and Markley, J. L. (1993). Multinuclear magnetic resonance and mutagenesis studies of the histidine residues of human placental ferredoxin, in preparation.Google Scholar
  93. Ye, X. M., Pochapsky, T. C., and Pochapsky, S. S. (1992).1H NMR sequential assignments and identification of secondary structural elements in oxidized putidaredoxin, and electron-transfer protein fromPseudomonas, Biochemistry 31, 1961–1968.Google Scholar
  94. Zanetti, G. and Merati, G. (1987). Interaction between photosystem I and ferredoxin. Identification by chemical cross-linking of the polypeptide which binds ferredoxin,Eur. J. Biochem. 169, 143–146.Google Scholar
  95. Zanetti, G., Morelli, D., Ronchi, S., Negri, A., Aliverti, A., and Curti, B. (1988). Structural studies on the interaction between ferredoxin and ferredoxin-NADP+ reductase,Biochemistry 27, 3753–3759.Google Scholar

Copyright information

© Plenum Publishing Corporation 1994

Authors and Affiliations

  • Hazel M. Holden
    • 1
    • 4
  • Bruce L. Jacobson
    • 1
  • John K. Hurley
    • 2
  • Gordon Tollin
    • 2
  • Byung-Ha Oh
    • 3
  • Lars Skjeldal
    • 3
  • Young Kee Chae
    • 3
    • 4
  • Hong Cheng
    • 3
  • Bin Xia
    • 3
    • 4
  • John L. Markley
    • 3
    • 4
  1. 1.Institute for Enzyme ResearchUniversity of Wisconsin-MadisonMadison
  2. 2.Department of BiochemistryUniversity of ArizonaTucson
  3. 3.Department of BiochemistryUniversity of Wisconsin-MadisonMadison
  4. 4.Graduate Program in BiophysicsUniversity of Wisconsin-MadisonMadison

Personalised recommendations