Gating mechanisms for biological electron transfer: Integrating structure with biophysics reveals the nature of redox control in cytochrome P450 reductase and copper-dependent nitrite reductase

FEBS Letters

Volumn 586, Issue 5, 2012, Pages 578-584

  Leferink, Nicole G H ^a   Pudney, Christopher R ^a   Brenner, Sibylle ^a,c   Heyes, Derren J ^a   Eady, Robert R ^b   Samar Hasnain, S ^b   Hay, Sam ^a   Rigby, Stephen E J ^a   Scrutton, Nigel S ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UNIVERSITY OF LIVERPOOL   (United Kingdom)

^c ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

Conformationally controlled electron transfer; Electron transfer; Gating; Proton coupled electron transfer

Indexed keywords

CYTOCHROME P450 REDUCTASE; METHIONINE SYNTHASE REDUCTASE; NITRITE REDUCTASE;

ACHROMOBACTER XYLOSOXIDANS; CATALYSIS; CHANNEL GATING; CONFORMATIONAL TRANSITION; ELECTRON TRANSPORT; ENZYME CONFORMATION; ENZYME KINETICS; ENZYME STRUCTURE; HUMAN; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OXIDATION REDUCTION REACTION; PHOTOLYSIS; PRIORITY JOURNAL; PROTON TRANSPORT; REVIEW; X RAY CRYSTALLOGRAPHY;

ACHROMOBACTER DENITRIFICANS; ANIMALS; BACTERIAL PROTEINS; CRYSTALLOGRAPHY, X-RAY; ELECTRON TRANSPORT; HUMANS; MODELS, MOLECULAR; NADPH-FERRIHEMOPROTEIN REDUCTASE; NITRITE REDUCTASES; OXIDATION-REDUCTION; PROTEIN CONFORMATION;

EID: 84857917046     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2011.07.003     Document Type: Review

References (47)

1. R.A. Marcus, and N. Sutin Electron transfers in chemistry and biology Biochim. Biophys. Acta 811 1985 265 322 (Pubitemid 15246565)
2. V.L. Davidson Protein control of true, gated, and coupled electron transfer reactions Acc. Chem. Res. 41 2008 730 738
3. M. Wang, D.L. Roberts, R. Paschke, T.M. Shea, B.S.S. Masters, and J.J.P. Kim Three-dimensional structure of NADPH-cytochrome P450 reductase: Prototype for FMN- and FAD-containing enzymes Proc. Natl. Acad. Sci. USA 94 1997 8411 8416 (Pubitemid 27335052)
4. S. Brenner, S. Hay, A.W. Munro, and N.S. Scrutton Inter-flavin electron transfer in cytochrome P450 reductase - effects of solvent and pH identify hidden complexity in mechanism FEBS J. 275 2008 4540 4557
5. M.B. Murataliev, R. Feyereisen, and A. Walker Electron transfer by diflavin reductases Biochim. Biophys. Acta 1698 2004 1 26 (Pubitemid 38446896)
6. C.C. Page, C.C. Moser, X.X. Chen, and P.L. Dutton Natural engineering principles of electron tunnelling in biological oxidation-reduction Nature 402 1999 47 52
7. A. Gutierrez, M. Paine, C.R. Wolf, N.S. Scrutton, and G.C.K. Roberts Relaxation kinetics of cytochrome P450 reductase: Internal electron transfer is limited by conformational change and regulated by coenzyme binding Biochemistry 41 2002 4626 4637 (Pubitemid 34275664)
8. A. Gutierrez, A.W. Munro, A. Grunau, C.R. Wolf, N.S. Scrutton, and G.C.K. Roberts Interflavin electron transfer in human cytochrome P450 reductase is enhanced by coenzyme binding - Relaxation kinetic studies with coenzyme analogues Eur. J. Biochem. 270 2003 2612 2621 (Pubitemid 36723991)
9. W.L. Backes, and R.W. Kelley Organization of multiple cytochrome P450s with NADPH-cytochrome P450 reductase in membranes Pharmacol. Ther. 98 2003 221 233 (Pubitemid 36513776)
10. V.L. Davidson Unraveling the kinetic complexity of interprotein electron transfer reactions Biochemistry 35 1996 14035 14039 (Pubitemid 26384397)
11. L. Aigrain, D. Pompon, S. Morera, and G. Truan Structure of the open conformation of a functional chimeric NADPH cytochrome P450 reductase EMBO Rep. 10 2009 742 747
12. D. Hamdane, C.W. Xia, S.C. Im, H.M. Zhang, J.J.P. Kim, and L. Waskell Structure and Function of an NADPH-Cytochrome P450 Oxidoreductase in an Open Conformation Capable of Reducing Cytochrome P450 J. Biol. Chem. 284 2009 11374 11384
13. E.D. Garcin, C.M. Bruns, S.J. Lloyd, D.J. Hosfield, M. Tiso, R. Gachhui, D.J. Stuehr, J.A. Tainer, and E.D. Getzoff Structural basis for isozyme-specific regulation of electron transfer in nitric-oxide synthase J. Biol. Chem. 279 2004 37918 37927 (Pubitemid 39195507)
14. A.L. Shen, and C.B. Kasper Role of acidic residues in the interaction of NADPH-cytochrome-P450 oxidoreductase with cytochrome-P450 and cytochrome-c J. Biol. Chem. 270 1995 27475 27480
15. A. Grunau, K. Geraki, J.G. Grossmann, and A. Gutierrez Conformational dynamics and the energetics of protein-ligand interactions: Role of interdomain loop in human cytochrome p450 reductase Biochemistry 46 2007 8244 8255 (Pubitemid 47075964)
16. C. Xia, D. Hamdane, A.L. Shen, V. Choi, C.B. Kasper, M. Pearl, H. Zhang, S.-C. Im, L. Waskell, and J.-J.P. Kim Conformational changes of NADPH-cytochrome P450 oxidoreductase are essential for catalysis and cofactor binding J. Biol. Chem. 286 2011 16246 16260
17. J. Ellis, A. Gutierrez, I.L. Barsukov, W.C. Huang, J.G. Grossmann, and G.C.K. Roberts Domain motion in cytochrome P450 reductase: conformational equilibria revealed by NMR and small-angle X-ray scattering J. Biol. Chem. 284 2009 36628 36637
18. S. Hay, S. Brenner, B. Khara, A.M. Quinn, S.E. Rigby, and N.S. Scrutton Nature of the energy landscape for gated electron transfer in a dynamic redox protein J. Am. Chem. Soc. 132 2010 9738 9745
19. S.E.J. Rigby, X. Lou, H.S. Toogood, K.R. Wolthers, and N.S. Scrutton ELDOR spectroscopy reveals that energy landscapes in human methionine synthase reductase are extensively remodeled following ligand and partner protein binding Chem. Bio. Chem. 12 2011 863 867
20. K.R. Wolthers, X.D. Lou, H.S. Toogood, D. Leys, and N.S. Scrutton Mechanism of coenzyme binding to human methionine synthase reductase revealed through the crystal structure of the FNR-like module and isothermal titration calorimetry Biochemistry 46 2007 11833 11844 (Pubitemid 47623751)
21. C.R. Pudney, T. McGrory, P. Lafite, J.Y. Pang, S. Hay, D. Leys, M.J. Sutcliffe, and N.S. Scrutton Parallel pathways and free-energy landscapes for enzymatic hydride transfer probed by hydrostatic pressure Chem. Bio. Chem. 10 2009 1379 1384
22. H.B. Gray, B.G. Malmstrom, and R.J.P. Williams Copper coordination in blue proteins J. Biol. Inorg. Chem. 5 2000 551 559
23. S. Hammes-Schiffer Theory of proton-coupled electron transfer in energy conversion processes Acc. Chem. Res. 42 2009 1881 1889
24. S. Hammes-Schiffer, and A.V. Soudackov Proton-coupled electron transfer in solution, proteins, and electrochemistry J. Phys. Chem. B 112 2008 14108 14123
25. A. Sirjoosingh, and S. Hammes-Schiffer Proton-coupled electron transfer versus hydrogen atom transfer: generation of charge-localized diabatic states J. Phys. Chem. A 115 2011 2367 2377
26. J.L. Dempsey, J.R. Winkler, and H.B. Gray Proton-coupled electron flow in protein redox machines Chem. Rev. 110 2010 7024 7039
27. M.H. Huynh, and T.J. Meyer Proton-coupled electron transfer Chem. Rev. 107 2007 5004 5064 (Pubitemid 350225868)
28. A to heme a and altered EPR spectra in mutants close to heme a of cytochrome oxidase Biochemistry 47 2008 11499 114509
29. D.L. Jenson, and B.A. Barry Proton-coupled electron transfer in photosystem II: proton inventory of a redox active tyrosine J. Am. Chem. Soc. 131 2009 10567 10573
30. S. Brenner, D.J. Heyes, S. Hay, M.A. Hough, R.R. Eady, S.S. Hasnain, and N.S. Scrutton Demonstration of proton-coupled electron transfer in the copper-containing nitrite reductases J. Biol. Chem. 284 2009 25973 25983
31. D.J. Heyes, M. Sakuma, and N.S. Scrutton Solvent-slaved protein motions accompany proton but not hydride tunneling in light-activated protochlorophyllide oxidoreductase Angew Chem. Int. Ed. Engl. 48 2009 3850 3853
32. D.J. Heyes, A.M. Quinn, P.M. Cullis, M. Lee, A.W. Munro, and N.S. Scrutton Internal electron transfer in multi-site redox enzymes is accessed by laser excitation of thiouredopyrene-3,6,8-trisulfonate (TUPS) Chem. Commun. (Camb) 2009 1124 1126
33. L. Geren, B. Durham, and F. Millett Use of ruthenium photoreduction techniques to study electron transfer in cytochrome oxidase Methods Enzymol. 456 2009 507 520
34. H.M. Girvan, D.J. Heyes, N.S. Scrutton, and A.W. Munro Laser photoexcitation of NAD(P)H induces reduction of P450 BM3 heme domain on the microsecond time scale J. Am. Chem. Soc. 129 2007 6647 6653 (Pubitemid 46799364)
35. A.J. Dunford, K.J. McLean, M. Sabri, H.E. Seward, D.J. Heyes, N.S. Scrutton, and A.W. Munro Rapid P450 heme iron reduction by laser photoexcitation of Mycobacterium tuberculosis CYP121 and CYP51B1. Analysis of CO complexation reactions and reversibility of the P450/P420 equilibrium J. Biol. Chem. 282 2007 24816 24824 (Pubitemid 47347520)
36. W.G. Zumft Cell biology and molecular basis of denitrification Microbiol. Mol. Biol. Rev. 61 1997 533 616 (Pubitemid 28006959)
37. M.J. Ellis, F.E. Dodd, G. Sawers, R.R. Eady, and S.S. Hasnain Atomic resolution structures of native copper nitrite reductase from Alcaligenes xylosoxidans and the active site mutant Asp92Glu J. Mol. Biol. 328 2003 429 438 (Pubitemid 36407585)
38. O. Farver, R.R. Eady, Z.H. Abraham, and I. Pecht The intramolecular electron transfer between copper sites of nitrite reductase: a comparison with ascorbate oxidase FEBS Lett. 436 1998 239 242 (Pubitemid 28468563)
39. K. Kobayashi, S. Tagawa, Deligeer, and S. Suzuki The pH-dependent changes of intramolecular electron transfer on copper-containing nitrite reductase J. Biochem. 126 1999 408 412 (Pubitemid 29408212)
40. S. Suzuki, Deligeer, K. Yamaguchi, K. Kataoka, K. Kobayashi, S. Tagawa, T. Kohzuma, S. Shidara, H. Iwasaki, and Deligeer. Deligeer Spectroscopic characterization and intramolecular electron transfer processes of native and type 2 Cu-depleted nitrite reductases J. Biol. Inorg. Chem. 2 1997 265 274 (Pubitemid 27187586)
41. N.G.H. Leferink, C. Han, S.V. Antonyuk, D.J. Heyes, S.E.J. Rigby, M.A. Hough, R.R. Eady, N.S. Scrutton, and S.S. Hasnain Proton coupled electron transfer in the catalytic cycle of Alcaligenes xylosoxidans copper-dependent nitrite reductase Biochemistry 50 2011 4121 4131
42. S. Suzuki, K. Kataoka, and K. Yamaguchi Metal coordination and mechanism of multicopper nitrite reductase Acc. Chem. Res. 33 2000 728 735
43. R.W. Strange, L.M. Murphy, F.E. Dodd, Z.H. Abraham, R.R. Eady, B.E. Smith, and S.S. Hasnain Structural and kinetic evidence for an ordered mechanism of copper nitrite reductase J. Mol. Biol. 287 1999 1001 1009 (Pubitemid 29188883)
44. K. Kataoka, H. Furusawa, K. Takagi, K. Yamaguchi, and S. Suzuki Functional analysis of conserved aspartate and histidine residues located around the type 2 copper site of copper-containing nitrite reductase J. Biochem. 127 2000 345 350 (Pubitemid 30136919)
45. S.V. Antonyuk, R.W. Strange, G. Sawers, R.R. Eady, and S.S. Hasnain Atomic resolution structures of resting-state, substrate- and product-complexed Cu-nitrite reductase provide insight into catalytic mechanism Proc. Natl. Acad. Sci. USA 102 2005 12041 12046 (Pubitemid 41291125)
46. M.A. Hough, S.V. Antonyuk, R.W. Strange, R.R. Eady, and S.S. Hasnain Crystallography with online optical and X-ray absorption spectroscopies demonstrates an ordered mechanism in copper nitrite reductase J. Mol. Biol. 378 2008 353 361
47. M.A. Hough, R.R. Eady, and S.S. Hasnain Identification of the proton channel to the active site type 2 Cu center of nitrite reductase: structural and enzymatic properties of the His254Phe and Asn90Ser mutants Biochemistry 47 2008 13547 13553