Dual role of FMN in flavodoxin function: Electron transfer cofactor and modulation of the protein-protein interaction surface

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1797, Issue 2, 2010, Pages 262-271

  Frago, Susana ^a   Lans, Isaias ^a   Navarro, José A ^b   Hervás, Manuel ^b   Edmondson, Dale E ^c   De la Rosa, Miguel A ^b   Gómez Moreno, Carlos ^a   Mayhew, Stephen G ^d   Medina, Milagros ^a  

^a UNIVERSITY OF ZARAGOZA   (Spain)

^b UNIVERSITY OF SEVILLE   (Spain)

^c EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY COLLEGE DUBLIN   (Ireland)

Author keywords

Electron transfer; Ferredoxin NADP+ reductase; Flavodoxin; FMN analogues; Photosystem I; Protein protein interaction; Reduction potential

Indexed keywords

FLAVINE MONONUCLEOTIDE; FLAVODOXIN;

ARTICLE; DIPOLE; ELECTRON TRANSPORT; NUCLEIC ACID STRUCTURE; OXIDATION REDUCTION REACTION; PHOTOSYSTEM I; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN PROTEIN INTERACTION; SURFACE PROPERTY;

ANABAENA; ELECTRON TRANSPORT; FLAVIN MONONUCLEOTIDE; FLAVODOXIN; KINETICS; MODELS, MOLECULAR; OXIDATION-REDUCTION; PHOTOSYSTEM I PROTEIN COMPLEX; PROTEIN CONFORMATION; STATIC ELECTRICITY;

ANABAENA;

EID: 73249122894     PISSN: 00052728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbabio.2009.10.012     Document Type: Article

References (50)

1. +. FEBS J. 276 (2009) 3942-3958
2. + reductase with its substrates: Optimal interaction for efficient electron transfer. Photosynth. Res. 79 (2004) 113-131
3. + and to ferredoxin. Eur. J. Biochem. 187 (1990) 39-48
4. + reductase. Biochim. Biophys. Acta 1787 (2009) 144-154
5. + reductase in Anabaena: role of flavodoxin hydrophobic residues in protein-protein interactions. Biochemistry 47 (2008) 1207-1217
6. + reductase. Role of flavodoxin residues in protein-protein interaction and electron transfer. Biochemistry 44 (2005) 97-104
7. + reductase in Anabaena PCC 7119. Biochemistry 42 (2003) 2036-2045
8. Worrall J.A., Reinle W., Bernhardt R., and Ubbink M. Transient protein interactions studied by NMR spectroscopy: the case of cytochrome c and adrenodoxin. Biochemistry 42 (2003) 7068-7076
9. Crowley P.B., and Carrondo M.A. The architecture of the binding site in redox protein complexes: implications for fast dissociation. Proteins 55 (2004) 603-612
10. Sétif P. In: Golbeck J.H. (Ed). Electron transfer from the bound iron-sulfur clusters to ferredoxin/flavodoxin: kinetic and structural properties of ferredoxin/flavodoxin reduction by photosystem I (2006), Book Springer, Dordrecht, The Netherlands 439-454
11. Sétif P., Fischer N., Lagoutte B., Bottin H., and Rochaix J.D. The ferredoxin docking site of photosystem I. Biochim. Biophys. Acta 1555 (2002) 204-209
12. + reductase with ferredoxin and flavodoxin. Proteins 72 (2008) 848-862
13. Rao S.T., Shaffie F., Yu C., Satyshur K.A., Stockman B.J., Markley J.L., and Sundarlingam M. Structure of the oxidized long-chain flavodoxin from Anabaena 7120 at 2 A resolution. Protein Sci. 1 (1992) 1413-1427
14. Nogues I., Campos L.A., Sancho J., Gomez-Moreno C., Mayhew S.G., and Medina M. Role of neighboring FMN side chains in the modulation of flavin reduction potentials and in the energetics of the FMN:apoprotein interaction in Anabaena flavodoxin. Biochemistry 43 (2004) 15111-15121
15. Lostao A., Gomez-Moreno C., Mayhew S.G., and Sancho J. 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 (1997) 14334-14344
16. Frago S., Goñi G., Herguedas B., Peregrina J.R., Serrano A., Perez-Dorado I., Molina R., Gomez-Moreno C., Hermoso J.A., Martinez-Julvez M., Mayhew S.G., and Medina M. Tuning of the FMN binding and oxido-reduction properties by neighboring side chains in Anabaena flavodoxin. Arch. Biochem. Biophys. 467 (2007) 206-217
17. + reductase. Role of Trp(57) and Tyr(94). J. Biol. Chem. 277 (2002) 22338-22344
18. Walsh C., Fisher J., Spencer R., Graham D.W., Ashton W.T., Brown J.E., Brown R.D., and Rogers E.F. Chemical and enzymatic properties of riboflavin analogues. Biochemistry 17 (1978) 1942-1951
19. Walsh J.D., and Miller A.-F. Flavin reduction potential tuning by substitution and bending. J. Mol. Struct. (Teochem) 623 (2003) 185-195
20. Light D.R., and Walsh C. Flavin analogs as mechanistic probes of adrenodoxin reductase-dependent electron transfer to the cholesterol side chain cleavage cytochrome P-450 of the adrenal cortex. J. Biol. Chem. 255 (1980) 4264-4277
21. Nishino T., Nishino T., Schopfer L.M., and Massey V. Reactivity of chicken liver xanthine dehydrogenase containing modified flavins. J. Biol. Chem. 264 (1989) 6075-6085
22. Schopfer L.M., Wessiak A., and Massey V. Interpretation of the spectra observed during oxidation of p-hydroxybenzoate hydroxylase reconstituted with modified flavins. J. Biol. Chem. 266 (1991) 13080-13085
23. Ghisla S., and Massey V. New flavins for old: artificial flavins as active site probes of flavoproteins. Biochem. J. 239 (1986) 1-12
24. Yorita K., Misaki H., Palfey B.A., and Massey V. On the interpretation of quantitative structure-function activity relationship data for lactate oxidase. Proc. Natl. Acad. Sci. U.S.A. 97 (2000) 2480-2485
25. Genzor C.G., Perales-Alcon A., Sancho J., and Romero A. Closure of a tyrosine/tryptophan aromatic gate leads to a compact fold in apo flavodoxin. Nat. Struct. Biol. 3 (1996) 329-332
26. Edmondson D.E., and Tollin G. Chemical and physical characterization of the Shethna flavoprotein and apoprotein and kinetics and thermodynamics of flavin analog binding to the apoprotein. Biochemistry 10 (1971) 124-132
27. Rogner M., Nixon P.J., and Diner B.A. Purification and characterization of photosystem I and photosystem II core complexes from wild-type and phycocyanin-deficient strains of the cyanobacterium Synechocystis PCC 6803. J. Biol. Chem. 265 (1990) 6189-6196
28. 6 and plastocyanin oxidation by Photosystem I. Biochim. Biophys. Acta 1184 (1994) 235-241
29. Mathis P., and Sétif P. Near infra-red absorption spectra of the chlorophyll a cations and triplet state in vivo. Isr. J. Chem. 21 (1981) 316-320
30. Shin K., Tagawa K., and Arnon D.I. Crystallization of ferredoxin-TPN reductase and its role in the fhotosynthetic apparatus of chloroplasts. Biochem. Z. (1963) 338
31. Frago S., Martinez-Julvez M., Serrano A., and Medina M. Structural analysis of FAD synthetase from Corynebacterium ammoniagenes. BMC Microbiol. 8 (2008) 160
32. Medina M., Martinez-Julvez M., Hurley J.K., Tollin G., and Gomez-Moreno C. Involvement of glutamic acid 301 in the catalytic mechanism of ferredoxin-NADP+ reductase from Anabaena PCC 7119. Biochemistry 37 (1998) 2715-2728
33. Mayhew S.G. Potentiometric measurement of oxidation-reduction potentials. Methods Mol. Biol. 131 (1999) 49-59
34. Medina M., Hervas M., Navarro J.A., De la Rosa M.A., Gomez-Moreno C., and Tollin G. A laser flash absorption spectroscopy study of Anabaena sp. PCC 7119 flavodoxin photoreduction by photosystem I particles from spinach. FEBS Lett. 313 (1992) 239-242
35. Muhlenhoff U., and Setif P. Laser flash absorption spectroscopy study of flavodoxin reduction by photosystem I in Synechococcus sp. PCC 7002. Biochemistry 35 (1996) 1367-1374
36. 6 to photosystem I. Experimental evidence on the evolution of the reaction mechanism. Biochemistry 34 (1995) 11321-11326
37. Meyer T.E., Zhao Z.G., Cusanovich M.A., and Tollin G. Transient kinetics of electron transfer from a variety of c-type cytochromes to plastocyanin. Biochemistry 32 (1993) 4552-4559
38. Sigfridsson K., Hansson Ö., Karlsson G.B., Baltzer L., Nordling M., and Lundberg L.G. Spectroscopic and kinetic characterization of the spinach plastocyanin mutant Tyr83-His: a histidine residue with a high pK value. Biochim. Biophys. Acta 1228 (1995) 28-36
39. M.J. Frisch, G.W. Trucks, H.B. Schlegel, G.E. Scuseria, M.A. Robb, J.R. Cheeseman, V.G. Zakrzewski, J.A. Montgomery, R.E. Stratmann and J.C. Burant. Gaussian, Inc., Pittsburgh PA 2003.
40. Bayly C.L., Cieplak P., Cornell W.D., and Kollman P.A. A well-behaved electrostatic potential based method sing charge restraints for deriving atomic charges: the RESP model. J. Phys. Chem. 97 (1993) 10269-10280
41. Case D.A., Cheatham III T.E., Darden T., Gohlke H., Luo R., Merz Jr. K.M., Onufriev A., Simmerling C., Wang B., and Woods R.J. The AMBER biomolecular simulation programs. J. Comput. Chem. 26 (2005) 1668-1688
42. Wang J., Wolf R.M., Caldwell J.W., Kollman P.A., and Case D.A. Development and testing of a general amber force field. J. Comput. Chem. 25 (2004) 1157-1174
43. W.L. Delano, They PyMOL molecular graphics system, DeLano Scientific, San Carlos, CA, USA (2002) http://www.pymol.org.
44. Humphrey W., Dalke A., and Schulten K. VMD-visual molecular dynamics. J. Mol. Graph. 14 (1996) 33-38
45. Anderson R.F. Energetics of the one-electron reduction steps of riboflavin, FMN and FAD to their fully reduced forms. Biochim. Biophys. Acta 722 (1983) 158-162
46. Mayhew S.G. The effects of pH and semiquinone formation on the oxidation-reduction potentials of flavin mononucleotide. A reappraisal. Eur. J. Biochem. 265 (1999) 698-702
47. Muller F., and Massey V. Flavin-sulfite complexes and their structures. J. Biol. Chem. 244 (1969) 4007-4016
48. Stankovich M.T. In: Müller F. (Ed). Redox properties of flavins and flavoproteins (1991), Book CRC Press, Inc., Boca Raton, Fl. 401-425
49. Meimberg K., Lagoutte B., Bottin H., and Muhlenhoff U. The PsaE subunit is required for complex formation between photosystem I and flavodoxin from the cyanobacterium Synechocystis sp. PCC 6803. Biochemistry 37 (1998) 9759-9767
50. + reductase in a cyanobacterium. Biochemistry 38 (1999) 12735-12746