Could tyrosine and tryptophan serve multiple roles in biological redox processes?

Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences

Volumn 373, Issue 2037, 2015, Pages

  Jay, R Winkler ^a   Gray, Harry B ^a  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Azurin; Cytochrome p450; Electron transfer; Hopping; Protein radical

Indexed keywords

ENZYMES; FREE RADICAL REACTIONS; PROTEINS;

AZURIN; BLUE-COPPER PROTEINS; CYTOCHROME P450; ELECTRON TRANSFER; HOPPING; REACTIVE INTERMEDIATE; TRANSPORT CHARGES; TRYPTOPHAN RESIDUES;

AMINO ACIDS;

AZURIN; COPPER; HYDROGEN PEROXIDE; OXYGEN; TRYPTOPHAN; TYROSINE;

CHEMISTRY; CONFORMATION; ELECTRON; OXIDATION REDUCTION REACTION; PSEUDOMONAS AERUGINOSA;

AZURIN; COPPER; ELECTRONS; HYDROGEN PEROXIDE; MOLECULAR CONFORMATION; OXIDATION-REDUCTION; OXYGEN; PSEUDOMONAS AERUGINOSA; TRYPTOPHAN; TYROSINE;

EID: 84922572228     PISSN: 1364503X     EISSN: None     Source Type: Journal    
DOI: 10.1098/rsta.2014.0178     Document Type: Article

References (56)

1. Sjöberg BM. 1997 Ribonucleotide reductases-a group of enzymes with different metallosites and a similar mechanism. Struct. Bonding 88, 139-173. (doi:10.1007/3-540-62870-3-5)
2. Stubbe J, Nocera DG, Yee CS, Chang MCY. 2003 Radical initiation in the class I ribonucleotide reductase: long-range proton-coupled electron transfer? Chem. Rev. 103, 2167-2201. (doi:10.1021/cr020421u)
3. Stubbe J, van der DonkWA. 1998 Protein radicals in enzyme catalysis. Chem. Rev. 98, 705-762. (doi:10.1021/cr9400875)
4. Argirevic T, Riplinger C, Stubbe J, Neese F, Bennati M. 2012 ENDOR spectroscopy and DFT calculations: evidence for the hydrogen-bond network within α2 in the PCET of E. coli ribonucleotide reductase. J. Am. Chem. Soc. 134, 17 661-17 670. (doi:10.1021/ja3071682)
5. Holder PG, Pizano AA, Anderson BL, Stubbe J, Nocera DG. 2012 Deciphering radical transport in the large subunit of class I ribonucleotide reductase. J. Am. Chem. Soc. 134, 1172-1180. (doi:10.1021/ja209016j)
6. Offenbacher AR, Minnihan EC, Stubbe J, Barry BA. 2013 Redox-linked changes to the hydrogen-bonding network of ribonucleotide reductase β2. J. Am. Chem. Soc. 135, 6380-6383. (doi:10.1021/ja3032949)
7. Worsdorfer B et al. 2013 Function of the diiron cluster of Escherichia coli class Ia ribonucleotide reductase in proton-coupled electron transfer. J. Am. Chem. Soc. 135, 8585-8593. (doi:10.1021/ja401342s)
8. 730 •) in the radical propagation pathway of the Escherichia coli class Ia ribonucleotide reductase. J. Am. Chem. Soc. 133, 18 420-18 432. (doi:10.1021/ja207455k)
9. Offenbacher AR, Burns LA, Sherrill CD, Barry BA. 2013 Redox-linked conformational control of proton-coupled electron transfer: Y122 in the ribonucleotide reductase β2 subunit. J. Phys. Chem. B 117, 8457-8468. (doi:10.1021/jp404757r)
10. A radical pairs in D1 protein variants of photosystem II: long range electron transfer in the Marcus inverted region. J. Phys. Chem. B 117, 3308-3314. (doi:10.1021/jp400337j)
11. Keough JM, Zuniga AN, Jenson DL, Barry BA. 2013 Redox control and hydrogen bonding networks: proton-coupled electron transfer reactions and tyrosine Z in the photosynthetic oxygen-evolving complex. J. Phys. Chem. B 117, 1296-1307. (doi:10.1021/jp3118314)
12. 2 state reveals the importance of charges in the oxygen-evolving center during catalysis: a unifying model. Biochemistry 51, 2054-2064. (doi:10.1021/bi2015794)
13. Sancar A. 2003 Structure and function of DNA photolyase and cryptochrome blue-light photoreceptors. Chem. Rev. 103, 2203-2238. (doi:10.1021/cr0204348)
14. Taylor JS. 1994 Unraveling the molecular pathway from sunlight to skin cancer. Acc. Chem. Res. 27, 76-82. (doi:10.1021/ar00039a003)
15. Li YF, Heelis PF, Sancar A. 1991 Active site of DNA photolyase: tryptophan-306 is the intrinsic hydrogen atom donor essential for flavin radical photoreduction and DNA repair in vitro. Biochemistry 30, 6322-6329. (doi:10.1021/bi00239a034)
16. Aubert C, Mathis P, Eker APM, Brettel K. 1999 Intraprotein electron transfer between tyrosine and tryptophan in DNA photolysase from Anacystis nidulans. Proc. Natl Acad. Sci. USA 96, 5423-5427. (doi:10.1073/pnas.96.10.5423)
17. Byrdin M, Eker APM, Vos MH, Brettel K. 2003 Dissection of the triple tryptophan electron transfer chain in Escherichia coli DNA photolyase: Trp382 is the primary donor in photoactivation. Proc. Natl Acad. Sci. USA 100, 8676-8681. (doi:10.1073/pnas.1531645100)
18. Kodali G, Siddiqui SU, Stanley RJ. 2009 Charge redistribution in oxidized and semiquinone E. coli DNA photolyase upon photoexcitation: Stark spectroscopy reveals a rationale for the position of Trp382. J. Am. Chem. Soc. 131, 4795-4807. (doi:10.1021/ja809214r)
19. Lukacs A, Eker APM, Byrdin M, Villette S, Pan J, Brettel K, Vos MH. 2006 Role of the middle residue in the triple tryptophan electron transfer chain of DNA photolyase: ultrafast spectroscopy of a Trp→Phe mutant. J. Phys. Chem. B 110, 15 654-15 658. (doi:10.1021/jp063686b)
20. Woiczikowski PB, Steinbrecher T, Kubař T, Elstner M. 2011 Nonadiabatic QM/MM simulations of fast charge transfer in Escherichia coli DNA photolyase. J. Phys. Chem. B 115, 9846-9863. (doi:10.1021/jp204696t)
21. Aubert C, Vos MH, Mathis P, Eker APM, Brettel K. 2000 Intraprotein radical transfer during photoactivation of DNA photolyase. Nature 405, 586-590. (doi:10.1038/35014644)
22. Davidson VL, Liu AM. 2012 Tryptophan tryptophylquinone biosynthesis: a radical approach to posttranslational modification. Biochim. Biophys. Acta 1824, 1299-1305. (doi:10.1016/j. bbapap.2012.01.008)
23. Geng JF, Dornevil K, Davidson VL, Liu AM. 2013 Tryptophan-mediated charge-resonance stabilization in the bis-Fe(IV) redox state of MauG. Proc. Natl Acad. Sci. USA 110, 9639-9644. (doi:10.1073/pnas.1301544110)
24. Yukl ET, Liu FG, Krzystek J, Shin S, Jensen LMR, Davidson VL, Wilmot CM, Liu A. 2013 Diradical intermediate within the context of tryptophan tryptophylquinone biosynthesis. Proc. Natl Acad. Sci. USA 110, 4569-4573. (doi:10.1073/pnas.1215011110)
25. Davidson VL,Wilmot CM. 2013 Posttranslational biosynthesis of the protein-derived cofactor tryptophan tryptophylquinone. Annu. Rev. Biochem. 82, 531-550. (doi:10.1146/annurev-biochem-051110-133601)
26. JiangN, Kuznetsov A, Nocek JM, Hoffman BM, Crane BR, Hu XQ, Beratan DN. 2013 Distanceindependent charge recombination kinetics in cytochrome c-cytochrome c peroxidase complexes: compensating changes in the electronic coupling and reorganization energies. J. Phys. Chem. B 117, 9129-9141. (doi:10.1021/jp401551t)
27. Wallrapp FH, Voityuk AA, Guallar V. 2013 In-silico assessment of protein-protein electron transfer. A case study: cytochrome c peroxidase-cytochrome c. PLoS Comput. Biol. 9, e1002990. (doi:10.1371/journal.pcbi.1002990)
28. Butchosa C, Simon S, Voityuk AA. 2010 Electron transfer from aromatic amino acids to guanine and adenine radical cations in π stacked and T-shaped complexes. Org. Biomol. Chem. 8, 1870-1875. (doi:10.1039/b927134a)
29. Shih C et al. 2008 Tryptophan-accelerated electron flow through proteins. Science 320, 1760-1762. (doi:10.1126/science.1158241)
30. I-modified Pseudomonas aeruginosa azurins. Chem. Eur. J. 17, 5350-5361. (doi:10.1002/chem.201002162)
31. Warren JJ, Ener ME, Vlèek A, Winkler JR, Gray HB. 2012 Electron hopping through proteins. Coord. Chem. Rev. 256, 2478-2487. (doi:10.1016/j.ccr.2012.03.032)
32. Takematsu K et al. 2013 Tryptophan-accelerated electron flow across a protein-protein interface. J. Am. Chem. Soc. 134, 15 515-15 525. (doi:10.1021/ja406830d)
33. Warren JJ, Herrera N, Hill MG, Winkler JR, Gray HB. 2013 Electron flow through nitrotyrosinate in Pseudomonas aeruginosa azurin. J. Am. Chem. Soc. 135, 11 151-11 158. (doi:10.1021/ja403734n)
34. Renaud N, Berlin YA, Lewis FD, Ratner MA. 2013 Between superexchange and hopping: an intermediate charge-transfer mechanism in poly(A)-poly(T) DNA hairpins. J. Am. Chem. Soc. 135, 3953-3963. (doi:10.1021/ja3113998)
35. Zhang Y, Liu C, Balaeff A, Skourtis SS, Beratan DN. 2014 Biological charge transfer via flickering resonance. Proc. Natl Acad. Sci. USA 111, 10 049-10 054. (doi:10.1073/pnas.1316519111)
36. Marcus RA, Sutin N. 1985 Electron transfers in chemistry and biology. Biochim. Biophys. Acta 811, 265-322. (doi:10.1016/0304-4173(85)90014-X)
37. Hammes-Schiffer S, Stuchebrukhov AA. 2010 Theory of coupled electron and proton transfer reactions. Chem. Rev. 110, 6939-6960. (doi:10.1021/cr1001436)
38. Migliore A, Polizzi NF, Therien MJ, Beratan DN. 2014 Biochemistry and theory of protoncoupled electron transfer. Chem. Rev. 114, 3381-3465. (doi:10.1021/cr4006654)
39. Weinberg DR et al. 2012 Proton-coupled electron transfer. Chem. Rev. 112, 4016-4093. (doi:10.1021/cr200177j)
40. Gray HB,Winkler JR. 2010 Electron flow through metalloproteins. Biochim. Biophys. Acta 1797, 1563-1572. (doi:10.1016/j.bbabio.2010.05.001)
41. Winkler JR, Gray HB. 2014 Electron flow through metalloproteins. Chem. Rev. 114, 3369-3380. (doi:10.1021/cr4004715)
42. Winkler JR, Gray HB. 2014 Long-range electron tunneling. J. Am. Chem. Soc. 136, 2930-2939. (doi:10.1021/ja500215j)
43. Denisov IG, Makris TM, Sligar SG, Schlichting I. 2005 Structure and chemistry of cytochrome P450. Chem. Rev. 105, 2253-2277. (doi:10.1021/cr0307143)
44. BM3 (CYP102A1): connecting the dots. Chem. Soc. Rev. 41, 1218-1260. (doi:10.1039/c1cs15192d)
45. Johnson EF, Stout CD. 2013 Structural diversity of eukaryotic membrane cytochrome P450s. J. Biol. Chem. 288, 17 082-17 090. (doi:10.1074/jbc.R113.452805)
46. Amdursky N, Molotskii M, Gazit E, Rosenman G. 2010 Elementary building blocks of selfassembled peptide nanotubes. J. Am. Chem. Soc. 132, 15 632-15 636. (doi:10.1021/ja104373e)
47. Hauser CAE, Zhang SG. 2010 Nanotechnology: peptides as biological semiconductors. Nature 468, 516-517. (doi:10.1038/468516a)
48. Vargas M, Malvankar NS, Tremblay PL, Leang C, Smith JA, Patel P, Snoeyenbos-West O, Nevin KP, Lovley DR. 2013 Aromatic amino acids required for pili conductivity and long-range extracellular electron transport in Geobacter sulfurreducens. mBio 4, e00270-13. (doi:10.1128/mBio.00210-13)
49. Girvan HM, Seward HE, Toogood HS, Cheesman MR, Leys D, Munro AW. 2007 Structural and spectroscopic characterization of P450 BM3 mutants with unprecedented P450 heme iron ligand sets-new heme ligation states influence conformational equilibria in P450 BM3. J. Biol. Chem. 282, 564-572. (doi:10.1074/jbc.M607949200)
50. Munro AW, Malarkey K, McKnight J, Thomson AJ, Kelly SM, Price NC, Lindsay JC, Coggins JR,Miles JS. 1994 The role of tryptophan-97 of cytochrome P450 BM3 from Bacillus megaterium in catalytic function-evidence against the "covalent switching" hypothesis of P450 electrontransfer. Biochem. J. 303, 423-428.
51. Denisov IG, Baas BJ, Grinkova YV, Sligar SG. 2007 Cooperativity in cytochrome P450 3A4: linkages in substrate binding, spin state, uncoupling, and product formation. J. Biol. Chem. 282, 7066-7076. (doi:10.1074/jbc.M609589200)
52. Grinkova YV, Denisov IG, McLean MA, Sligar SG. 2013 Oxidase uncoupling in heme monooxygenases: human cytochrome P450 CYP3A4 in nanodiscs. Biochem. Biophys. Res. Commun. 430, 1223-1227. (doi:10.1016/j.bbrc.2012.12.072)
53. Staudt H, Lichtenb F, Ullrich V. 1974 Role of NADH in uncoupled microsomal monoxygenations. Eur. J. Biochem. 46, 99-106. (doi:10.1111/j.1432-1033.1974.tb03601.x)
54. Puntarulo S, Cederbaum AI. 1998 Production of reactive oxygen species by microsomes enriched in specific human cytochrome P450 enzymes. Free Rad. Biol. Med. 24, 1324-1330. (doi:10.1016/S0891-5849(97)00463-2)
55. De Matteis F, Dawson SJ, Pons N, Pipino S. 2002 Bilirubin and uroporphyrinogen oxidation by induced cytochrome P4501A and cytochrome P4502B-role of polyhalogenated biphenyls of different configuration. Biochem. Pharmacol. 63, 615-624. (doi:10.1016/S0006-2952(01)00851-6)
56. De Matteis F, Ballou DP, Coon MJ, Estabrook RW, Haines DC. 2012 Peroxidase-like activity of uncoupled cytochrome P450: studies with bilirubin and toxicological implications of uncoupling. Biochem. Pharmacol. 84, 374-382. (doi:10.1016/j.bcp.2012.04.016)