Designed azurins show lower reorganization free energies for intraprotein electron transfer

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 26, 2013, Pages 10536-10540

  Farver, Ole ^a   Marshall, Nicholas M ^b   Wherland, Scot ^c   Lu, Yi ^b   Pecht, Israel ^d  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^c WASHINGTON STATE UNIVERSITY   (United States)

^d WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

Blue copper; Cupredoxin; Marcus inverted region; Reorganization energy; Type 1 copper

Indexed keywords

AZURIN; MUTANT PROTEIN;

ABSORPTION; ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; ELECTRON SPIN RESONANCE; ELECTRON TRANSPORT; ENERGY CONVERSION; HYDROGEN BOND; METAL BINDING; PH; PH ELECTRODE; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA;

BLUE COPPER; CUPREDOXIN; MARCUS INVERTED REGION; REORGANIZATION ENERGY; TYPE 1 COPPER;

AZURIN; COPPER; DISULFIDES; ELECTRON SPIN RESONANCE SPECTROSCOPY; ELECTRON TRANSPORT; KINETICS; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; PROTEIN ENGINEERING; PSEUDOMONAS AERUGINOSA; PULSE RADIOLYSIS; RECOMBINANT PROTEINS; THERMODYNAMICS;

EID: 84879521462     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1215081110     Document Type: Article

References (39)

1. Messerschmidt A, Huber R, Wieghardt K, Poulos T, eds (2001) Handbook of Metalloproteins (Wiley, New York), Vol 2.
2. Kobayashi C, Baldridge K, Onuchic JN (2003) Multiple versus single pathways in electron transfer in proteins: Influence of protein dynamics and hydrogen bonds. J Chem Phys 119(6):3550-3558.
3. Skourtis SS, Balabin IA, Kawatsu T, Beratan DN (2005) Protein dynamics and electron transfer: Electronic decoherence and non-Condon effects. Proc Natl Acad Sci USA 102(10):3552-3557.
4. Farver O, Pecht I (2007) Elucidation of electron-transfer pathways in copper and iron proteins by pulse radiolysis experiments. Prog Inorg Chem 55:1-78.
5. Davidson VL (2008) Protein control of true, gated, and coupled electron transfer reactions. Acc Chem Res 41(6):730-738.
6. Gray HB, Winkler JR (2003) Electron tunneling through proteins. Q Rev Biophys 36(3): 341-372.
7. Solomon EI, Szilagyi RK, DeBeer George S, Basumallick L (2004) Electronic structures of metal sites in proteins and models: contributions to function in blue copper proteins. Chem Rev 104(2):419-458.
8. Khoshtariya DE, et al. (2010) Fundamental signatures of short- and long-range electron transfer for the blue copper protein azurin at Au/SAM junctions. Proc Natl Acad Sci USA 107(7):2757-2762.
9. Canters GW, Gilardi G (1993) Engineering type 1 copper sites in proteins. FEBS Lett 325(1-2):39-48.
10. Pascher T, Karlsson BG, Nordling M, Malmström BG, Vänngård T (1993) Reduction potentials and their pH dependence in site-directed-mutant forms of azurin from Pseudomonas aeruginosa. Eur J Biochem 212(2):289-296.
11. Langen R, et al. (1995) Electron tunneling in proteins: Coupling through a beta strand. Science 268(5218):1733-1735.
12. Farver O, et al. (1996) Structure-function correlation of intramolecular electron transfer in wild type and single-site mutated azurins. Chem Phys 204(2-3):271-277.
13. Skov LK, Pascher T, Winkler JR, Gray HB (1998) Rates of intramolecular electron transfer in Ru(bpy)2(im)(His83)-modified azurin increase below 220 K. J Am Chem Soc 120(5):1102-1103.
14. Gray HB, Malmström BG, Williams RJP (2000) Copper coordination in blue proteins. J Biol Inorg Chem 5(5):551-559.
15. Vila AJ, Fernández CO (2001) Copper in electron transfer proteins. Handbook of Metalloproteins, eds Messerschmidt A, Huber R, Wieghardt K, Poulos T (Wiley, New York), Vol 1, pp 813-856.
16. Dennison C (2005) Investigating the structure and function of cupredoxins. Coord Chem Rev 249(24):3025-3054.
17. Garner DK, et al. (2006) Reduction potential tuning of the blue copper center in Pseudomonas aeruginosa azurin by the axial methionine as probed by unnatural amino acids. J Am Chem Soc 128(49):15608-15617.
18. Farver O, Pecht I (2011) Electron transfer in blue copper proteins. Coord Chem Rev 255(7-8):757-773.
19. Wilson TD, Yu Y, Lu Y (2013) Understanding copper-thiolate containing electron transfer centers by incorporation of unnatural amino acids and the CuA center into the type 1 copper protein azurin. Coord Chem Rev 257(1):260-276.
20. Bixon M, Jortner J (1999) Electron transfer - From isolated molecules to biomolecules. Adv Chem Phys 106:35-202.
21. Kuznetsov AM, Ulstrup JA (1999) Theory of electron transfer in bridged and supramolecular systems. J Incl Phenom Macro 35(1-2):45-54.
22. Beratan DN, Onuchic JN, Winkler JR, Gray HB (1992) Electron-tunneling pathways in proteins. Science 258(5089):1740-1741.
23. Marcus RA, Sutin N (1985) Electron transfers in chemistry and biology. Biochim Biophys Acta 811(3):265-322.
24. Marcus RA (1993) Electron-transfer reactions in chemistry: Theory and experiment (Nobel lecture). Angew Chem 32(8):1111-1121.
25. Marshall NM, et al. (2009) Rationally tuning the reduction potential of a single cupredoxin beyond the natural range. Nature 462(7269):113-116.
26. Crane BR, Di Bilio AJ, Winkler JR, Gray HB (2001) Electron tunneling in single crystals of Pseudomonas aeruginosa azurins. J Am Chem Soc 123(47):11623-11631.
27. Klapper MH, Faraggi M (1979) Applications of pulse radiolysis to protein chemistry. Q Rev Biophys 12(4):465-519.
28. Gray HB, Winkler JR (1996) Electron transfer in proteins. Annu Rev Biochem 65: 537-561.
29. Duggleby RG (1980) Estimation of the reliability of parameters obtained by nonlinear regression. Eur J Biochem 109(1):93-96.
30. Farver O, Lu Y, Ang MC, Pecht I (1999) Enhanced rate of intramolecular electron transfer in an engineered purple CuA azurin. Proc Natl Acad Sci USA 96(3):899-902.
31. Di Bilio AJ, et al. (1997) Reorganization energy of blue copper: Effects of temperature and driving force on the rates of electron transfer in ruthenium- and osmium-modified azurins. J Am Chem Soc 119(41):9921-9922.
32. Marcus RA (2007) H and other transfers in enzymes and in solution: Theory and computations, a unified view. 2. Applications to experiment and computations. J Phys Chem B 111(24):6643-6654.
33. Kornyshev AA, Kuznetsov AM, Ulstrup J, Stimming U (1997) Medium effects on elementary charge transfer processes in liquid and solid environments. J Phys Chem B 101(31):5917-5935.
34. Lancaster KM, et al. (2011) Electron transfer reactivity of type zero Pseudomonas aeruginosa azurin. J Am Chem Soc 133(13):4865-4873.
35. Augustin MA, Yandell JK (1979) Rates of electron-transfer reactions of some copper (II)-phenanthroline complexes with cytochrome-C(II) and tris(phenanthroline)cobalt (II)ion. Inorg Chem 18(3):577-583.
36. Winkler JR, Wittung-Stafshede P, Leckner J, Malmström BG, Gray HB (1997) Effects of folding on metalloprotein active sites. Proc Natl Acad Sci USA 94(9):4246-4249.
37. Farver O, Zhang J, Chi Q, Pecht I, Ulstrup J (2001) Deuterium isotope effect on the intramolecular electron transfer in Pseudomonas aeruginosa azurin. Proc Natl Acad Sci USA 98(8):4426-4430.
38. New SY, Marshall NM, Hor TSA, Xue F, Lu Y (2012) Redox tuning of two biological copper centers through non-covalent interactions: same trend but different magnitude. Chem Commun (Camb) 48(35):4217-4219.
39. Yanagisawa S, Banfield MJ, Dennison C (2006) The role of hydrogen bonding at the active site of a cupredoxin: The Phe114Pro azurin variant. Biochemistry 45(29): 8812-8822.