Cloning, sequencing and expression of the gene for flavodoxin from Megasphaera elsdenii and the effects of removing the protein negative charge that is closest to N(1) of the bound FMN

European Journal of Biochemistry

Volumn 267, Issue 14, 2000, Pages 4434-4444

  Geoghegan, Susan M ^a   Mayhew, Stephen G ^a   Yalloway, Gary N ^a   Butler, Geraldine ^a  

^a UNIVERSITY COLLEGE DUBLIN   (Ireland)

Author keywords

Cloning; Flavodoxin; FMN; Megasphaera elsdenii; Mutagenesis

Indexed keywords

FLAVINE MONONUCLEOTIDE; FLAVODOXIN; HYDROQUINONE;

ARTICLE; ESCHERICHIA COLI; MOLECULAR CLONING; NONHUMAN; OXIDATION REDUCTION REACTION; PKA; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN ANALYSIS; RUMEN MICROORGANISM; SITE DIRECTED MUTAGENESIS;

AMINO ACID SEQUENCE; BACILLACEAE; BASE SEQUENCE; CLONING, MOLECULAR; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ESCHERICHIA COLI; FLAVODOXIN; GLUTAMIC ACID; HYDROGEN-ION CONCENTRATION; HYDROQUINONES; KINETICS; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; OXIDATION-REDUCTION; PROTEIN BINDING; RECOMBINANT PROTEINS; SEQUENCE ANALYSIS, DNA; TEMPERATURE; THERMODYNAMICS;

ESCHERICHIA COLI; MEGASPHAERA ELSDENII;

EID: 0033927369     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1432-1327.2000.01490.x     Document Type: Article

References (59)

1. 1. Mayhew, S.G. & Ludwig, M.L. (1975) Flavodoxins and electron-transferring flavoproteins. In Enzymes Vol. 12, 3rd edn (Boyer, P.D., ed.), pp. 57-118. Academic Press, New York, USA.
2. 2. Mayhew, S.G. & Tollin, G. (1992) General properties of Flavodoxins. In Chemistry and Biochemistry of Flavoenzymes, Vol. 3 (Müller, F., ed.), pp. 389-426. CRC Press, Boca Raton, FL, USA.
3. 3. Ludwig, M.L. & Luschinsky, C.L. (1992) Structure and redox properties of clostridial flavodoxin. In Chemistry and Biochemistry of Flavoenzymes, Vol. 3 (Müller, F., ed.), pp. 427-466. CRC Press, Boca Raton, FL, USA.
4. 4. Anderson, R.F. (1983) Energetics of the one-electron reduction steps of riboflavin, FMN and FAD to their fully reduced forms. Biochim. Biophys. Acta 722, 158-162.
5. 5. Mayhew. S.G. (1999) The effects of pH and semiquinone formation on the oxidation-reduction potentials of flavin mononucleotide. A reappraisal. Eur. J. Biochem. 265, 698-702.
6. 6. Carr, M.C., Curley, G.P., Mayhew, S.G. & Voordouw, G. (1990) Effects of substituting asparagine for glycine-61 in flavodoxin from Desulfovibrio vulgaris (Hildenborough). Biochem. Int. 20, 1025-1032.
7. 7. Swenson, R.P. & Krey, G.D. (1994) Site-directed mutagenesis of tyrosine-98 in the flavodoxin from Desulfovibrio vulgaris (Hildenborough): regulation of oxidation-reduction properties of the bound FMN cofactor by aromatic, solvent, and electrostatic interactions. Biochemistry 33, 8505-8514.
8. 8. Zhou, Z.M. & Swenson, R.P. (1995) Electrostatic effects of surface acidic amino acid residues on the oxidation-reduction potentials of the flavodoxin from Desulfovibrio vulgaris (Hildenborough). Biochemistry 34, 3183-3192.
9. 9. Zhou, Z.M. & Swenson, R.P. (1996) Evaluation of the electrostatic effect of the 5′-phosphate of the flavin mononucleotide cofactor on the oxidation-reduction potentials of the flavodoxin from Desulfovibrio vulgaris (Hildenborough). Biochemistry 35, 12443-12454.
10. 10. Zhou, Z.M. & Swenson, R.P. (1996) The cumulative electrostatic effect of aromatic stacking interactions and the negative electrostatic environment of the flavin mononucleotide binding site is a major determinant of the reduction potential for the flavodoxin from Desulfavibrio vulgaris (Hildenborough). Biochemistry 35, 15980-15988.
11. 11. Chang, F.C. & Swenson, R.P. (1997) Regulation of oxidation-reduction potentials through redox-linked ionization in the Y98H mutant of the Desulfovibrio vulgaris (Hildenborough) flavodoxin: direct proton nuclear magnetic resonance spectroscopic evidence for the redox-dependent shift in the pKa of histidine-98. Biochemistry 36, 9013-9021.
12. 12. Curley, G.P., Carr, M.C., Mayhew, S.G. & Voordouw, G. (1991) Redox and flavin-binding properties of recombinant flavodoxin from Desulfovibrio vulgaris (Hildenborough). Eur. J. Biochem. 202, 1091-1100.
13. 13. O'Farrell, P.A., Walsh, M.A., McCarthy, A.A., Higgins, T.M., Voordouw, G. & Mayhew, S.G. (1998) Modulation of the redox potentials of FMN in Desulfovibrio vulgaris flavodoxin; thermodynamic properties and crystal structures of glycine-61 mutants. Biochemistry 37, 8405-8416.
14. 14. Ludwig, M.L., Pattridge, K.A., Metzger, A.L., Dixon, M.M., Eren, M., Feng, Y.C. & Swenson, R.P. (1997) Control of oxidation-reduction potentials in flavodoxin from Clostridium beijerinckii: the role of conformation changes. Biochemistry 36, 1259-1280.
15. 15. Chang, F.-C. & Swenson, R.P. (1999) The midpoint potentials for the oxidized-semiquinone couple for Gly57 mutants of the Clostridium beijerinckii flavodoxin correlate with changes in the hydrogen-bonding interaction with the proton on N(5) of the reduced flavin mononucleotide cofactor as measured by NMR chemical shift temperature dependencies. Biochemistry 38, 7168-7176.
16. 16. Bradley, L.H. & Swenson, R.P. (1999) Role of glutamate-59 hydrogen bonded to N (3) H of the flavin mononucleotide cofactor in the modulation of the redox potentials of the Clostridium heijerinckii flavodoxin. Glutamate-59 is not responsible for the pH dependency but contributes to the stabilization of the flavin semiquinone. Biochemistry 38, 12377-12386.
17. 17. Lostao, A.G., Gómez-Moreno, C, Mayhew, S.G. & Sancho, J. (1997) Differential stabilization of the three FMN redox forms by tyrosine 94 and tryptophan 57 in flavodoxin from Anabaena and its influence on the redox potentials. Biochemistry 36, 14334-14344.
18. 18. Mayhew, S.G. & Massey, V. (1969) Purification and properties of flavodoxin from Peptostreptococcus elsdenii. J. Biol. Chem. 244, 794-802.
19. 19. van Mierlo, C.P.M., Müller, F. & Vervoort, J. (1990) Secondary and tertiary structure characteristics of Megasphaera elsdenii flavodoxin in the reduced state as determined by 2-dimensional H-1 NMR. Eur. J. Biochem. 189, 589-600.
20. 20. van Mierlo, C.P.M., Vervoort, J., Müller, F. & Bacher, A. (1990) A 2-dimensional H-1 NMR study on Megasphaera elsdenii flavodoxin in the reduced state - sequential assignments. Eur. J. Biochem. 187, 521-541.
21. 21. van Mierlo, C.P.M., van der Sanden, B.P.J., van Woensel, P., Müller, F. & Vervoort, J. (1990) A two-dimensional H-1-NMR study on Megasphaera elsdenii flavodoxin in the oxidized state and some comparisons with the two-electron reduced state. Eur. J. Biochem. 194, 199-216.
22. 22. van Mierlo, C.P.M., Lijnzaad, P., Vervoort, J.M., Iler, F., Berendsen, H.J.C. & Devlieg, J. (1990) Tertiary structure of two-electron reduced Megasphaera elsdenii flavodoxin and some implications, as determined by two-dimensional H-1-NMR and restrained molecular dynamics. Eur. J. Biochem. 194, 185-198.
23. 23. Wijmenga, S.S. & van Mierlo, C.P.M. (1991) Three-dimensional correlated NMR study of Megasphaera elsdenii flavodoxin in the oxidized state. Eur. J. Biochem. 195, 807-822.
24. 24. Sharkey, C.T., Mayhew, S.G., Higgins, T.M. & Walsh, M.A. (1997) Crystallographic studies on flavodoxin from Megasphaera elsdenii. In Flavins and Flavoproteins 1996 (Stevenson, K., Massey, V. & Williams, C.H. Jr, eds.), pp. 445-448. University of Calgary Press, Calgary, Canada.
25. 25. Ludwig, M.L., Schopfer, L.M., Metzger, A.L., Pattridge, K.A. & Massey, V. (1990) Structure and oxidation-reduction behavior of 1-deaza-FMN flavodoxins: modulation of redox potentials in flavodoxins. Biochemistry 29, 10364-10375.
26. 26. Vervoort, J., Müller, F., Mayhew, S.G., van den Berg, W.A.M., Moonen, C.T.W. & Bacher, A. (1986) A comparative carbon-13, nitrogen-15, and phosphorus-31 nuclear magnetic resonance study on the flavodoxins from Clostridium MP, Megasphaera elsdenii and Azotobacter vinelandii. Biochemistry 25, 6789-6799.
27. 15N-labelIed flavins, free and bound to Megasphaera elsdenii apoflavodoxin. Eur. J. Biochem. 138, 481-489.
28. 28. Moonen, C.T.W., Vervoort, J. & Müller, F. (1984) Some new ideas about the possible regulation of redox potentials in flavoprotein, with special reference to flavodoxins. In Flavins and Flavoproteins (Bray, R.C., Engel, P.C. & Mayhew, S.G., eds.), pp. 493-496. de Gruyter, Berlin, Germany.
29. 29. Vervoort, J., van Berkel, W.J.H., Mayhew, S.G., Müller, F., Bacher, A., Nielsen, P. & Le Gall, J. (1986) Properties of the complexes of riboflavin 3′5′ bisphosphate and the apoflavodoxins from Megasphaera elsdenii and Desulfovibrio vulgaris. Eur. J. Biochem. 161, 749-756.
30. 30. Walsh, M.A., McCarthy, A., O'farrell, P.A., McCardle, P., Cunningham, P.D., Mayhew, S.G. & Higgins, T.M. (19981) X-ray crystal structure of the Desulfovibrio vulgaris apoflavodoxinriboflavin complex. Eur. J. Biochem. 258, 362-371.
31. 31. Swenson, R.P. & Zhou, Z. (1997) Role of electrostatic interactions in the regulation of the one-electron reduction potentials in the Desulfovibrio flavodoxin. In Flavins and Flavoproteins (Stevenson, K.J., Massey, V. & Williams, C.H. Jr, eds.). pp. 427-436. University of Calgary Press, Calgary, Canada.
32. 32. Geoghegan, S.M., Butler, G. & Mayhew, S.G. (1995) Cloning of the gene for flavodoxin from the anaerobic bacterium Megasphaera elsdenii. Biochem. Soc. Trans. 23, 384S.
33. 33. Mayhew, S.G., Foust, G.P. & Massey, V. (1969) Oxidation-reduction properties of flavodoxin from Peptostreptococcus elsdenii. J. Biol. Chem. 244, 803-810.
34. 34. Sambrook, J., Fritsch, E.F. & Maniatis, T. (1989) Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, USA.]
35. 35. Ausubel, F.M., Brent, R., Kingston, R.E., Moore, D.D., Seidman, J.G., Smith, J.A. & Struhl, K. (1996). Current Protocols in Molecular Biology, Vols 1-3. John Wiley, New York, USA.
36. 36. Murray, M.G. & Thompson, W.F. (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res. 8, 4321-4325.
37. 37. Tanaka, M., Haniu, M., Yasunobu. K.T., Mayhew, S.G. & Massey, V. (1973) The primary structure of Peptostreptococcus elsdenii flavodoxin. J. Biol. Chem. 248, 4354-4366.
38. 38. Tanaka, M., Haniu, M., Yasunohu, K.T., Mayhew, S.G. & Massey, V. (1974) Correction of the amino acid sequence of Peptostreptococcus elsdenii flavodoxin. J. Biol. Chem. 249, 4397.
39. 39. Geoghegan, S.M. & Mayhew, S.G. (1997) Effects of changing the surface glutamate-14 to lysine on the properties of flavodoxin from Megasphaera elsdenii. In Flavins and Flavoproteins (Stevenson, K.J., Massey, V. & Williams, C.H. Jr, eds), pp. 437-440. University of Calgary Press, Calgary, Canada.
40. 40. Goodin, M., Mauk, A.C. & Smith, M. (1987) The peroxide complex of yeast cytochrome c peroxidase contains two distinct radical species, neither of which resides at methionine 172 or tryptophan 51. J. Biol. Chem. 262, 7719-7724.
41. 41. Kunkel, TA., Roberts, J.D. & Zakour, R.A. (1987) Rapid and efficient site-specific mutagenesis without phenotypic selection. Methods Enzymol. 154, 367-382.
42. 42. Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein using the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
43. 43. Wassink, J.M. & Mayhew, S.G. (1975) Fluorescence titration with apoflavodoxin: a sensitive assay for riboflavin 5′-phosphate and flavin adenine dinucleotide in mixtures. Anal. Biochem. 68, 609-616.
44. 44. Mayhew, S.G. (1971) Studies on flavin binding in flavodoxins. Biochim. Biophys. Acta 235, 289-302.
45. 45. Massey, V. & Hemmerich, P. (1978) Photo-reduction of flavoproteins and other biological compounds catalyzed by deazaflavins. Biochemistry 17, 9-16.
46. 46. Mayhew, S.G. (1999) Potentiometric measurement of redox potentials. In Methods in Molecular Biology, Vol. 131, Flavoprotein Protocols (Chapman, S.K. & Reid, G.A., eds.), pp. 49-59. Humana Press Inc, Totowa, NJ, USA.
47. 47. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
48. 48. Becker, D.F., Fuchs, J.A., Banfield, D.K., Funk, W.D., MacGillivray, T.A. & Stankovitch, M.T. (1993) Characterization of wild-type and active-site mutant in Escherichia coli of short-chain acyl-CoA dehydrogenase from Megasphaera elsdenii. Biochemistry 32, 10736-10742.
49. 49. O'Neill, H., Mayhew, S.G. & Butler, G. (1998) Cloning and analysis of the genes for a novel electron-transferring flavoprotein from Megasphaera elsdenii. Expression and characterization of the recombinant protein. J. Biol. Chem. 273, 21015-21024.
50. 50. O'Farrell, P.A. (1993) An anvestigation of the flavin-binding site of flavodoxin from Desulfovibrio vulgaris by site-directed mutagenesis. PhD Thesis, National University of Ireland.
51. 51. Yalloway, G.N., Mayhew, S.G., Malthouse, J.P.G., Gallagher, M.E. & Curley, G.P. (1999) pH-dependent spectroscopic changes associated with the hydroquinone of FMN in flavodoxins. Biochemistry 38, 3753-3762.
52. 52. Gast, R., Valk, B.E., Müller, F., Mayhew, S.G. & Veeger, C. (1976) Studies on the binding of FMN by apoflavodoxin from Peptostreptococcus elsdenii. Biochem. Biophys. Acta 446, 463-471.
53. 53. Müller, F. (1992) Free flavins; syntheses, chemical and physical properties. In Chemistry and Biochemistry of Flavoenzymes, Vol. 1 (Müller, F., ed.), pp. 1-71. CRC Press, Boca Raton, FL, USA.
54. 54. Stankovich, M. (1980) An anaerobic spectroelectrochemical cell for studying spectral and redox properties of flavoproteins. Anal. Biochem. 109, 295-308.
55. 55. van Dijk, C., van Leeuwen, J.W. & Veeger, C. (1982) Electrochemical behaviour of low-potential electron-transferring proteins at the mercury electrode. Bioelectrochem. Bioeng. 9, 7143-7159.
56. 56. van Leeuwen, J.W., van Dijk, C. & Veeger, C. (1983) A pulse-radiolysis study of the reduction of flavodoxin from Megasphaera elsdenii by viologen radicals. A conformational change as a possible regulating mechanism. Eur. J. Biochem. 135, 601-607.
57. 57. Baker, E.N. & Hubbard, R.E. (1984) Hydrogen bonding in globular proteins. Prog. Biophys. Mol. Biol. 44, 97-179.
58. 58. O'Farrell, P.A., Walsh, M.A., McCarthy, A.A., Higgins, T.M., Voordouw, G. & Mayhew, S.G. (1998) Modulation of the redox potentials of FMN in Desulfovibrio vulgaris flavodoxin: thermodynamic properties and crystal structures of glycine-61 mutants. Biochemistry 37, 8405-8416.
59. 15N NMR spectra of the hydroquinone of Desulfovibrio vulgaris flavodoxin and its G61A mutant. In Flavins and Flavoproteins (Ghisla, S., Kroneck, P., Macheroux, P. & Sund, H., eds.), pp. 187-190. Rudolf Weber, Berlin, Germany.