The nature of tryptophan radicals involved in the long-range electron transfer of lignin peroxidase and lignin peroxidase-like systems: Insights from quantum mechanical/molecular mechanics simulations

Proteins: Structure, Function and Bioinformatics

Volumn 80, Issue 5, 2012, Pages 1476-1483

  Bernini, Caterina ^a   Pogni, Rebecca ^a   Basosi, Riccardo ^a   Sinicropi, Adalgisa ^a  

^a UNIVERSITY OF SIENA   (Italy)

Author keywords

DFT; Enzyme; EPR; G tensors; Hyperfine coupling constants

Indexed keywords

LIGNIN PEROXIDASE; TRYPTOPHAN;

ARTICLE; COPRINUS; COPRINUS CINEREUS; ELECTRON SPIN RESONANCE; ELECTRON TRANSPORT; MOLECULAR DYNAMICS; OXIDATION REDUCTION REACTION; PHANEROCHAETE; PRIORITY JOURNAL; QUANTUM MECHANICS;

ELECTRON TRANSPORT; IONS; MOLECULAR DYNAMICS SIMULATION; OXIDATION-REDUCTION; PEROXIDASES; PHANEROCHAETE; TRYPTOPHAN;

COPRINOPSIS CINEREA; PHANEROCHAETE CHRYSOSPORIUM;

EID: 84859440124     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.24046     Document Type: Article

References (63)

1. Wong DWS. Structure and action mechanism of ligninolytic enzymes. Appl Biochem Biotechnol 2009; 157: 174-209.
2. Higuchi T. Look back over the studies of lignin biochemistry. J Wood Sci 2006; 52: 2-8.
3. Goodwin DG, Aust SD, Grover TA. Evidence for veratryl alcohol as a redox mediator in lignin peroxidase catalyzed oxidation. Biochemistry 1995; 34: 5060-5065.
4. Miki K, Kondo R, Renganathan V, Mayfield MB, Gold MH. Mechanism of aromatic ring cleavage of a 8-biphenylyl ether dimer catalyzed by lignin peroxidase of Phanerochaete chrysosporium. Biochemistry 1988; 27: 4787-4794.
5. Tien M, Kirk TK. Lignin-degrading enzyme from the hymenomycete Phanerochaete chrysosporium birds. Science 1983; 221: 661-663.
6. Doyle WA, Blodig W, Veitch NC, Piontek K, Smith AT. Two substrate interaction sites in lignin peroxidase revealed by site-directed mutagenesis. Biochemistry 1998; 37: 15097-15105.
7. Blodig W, Smith AT, Winterhalter HK, Piontek K. Evidence from spin-trapping for a transient radical on tryptophan residue 171 of lignin peroxidase. Arch Biochem Biophys 1999; 370: 86-92.
8. Timofeevski SL, Nie G, Reading NS, Aust SD. Addition of veratryl alcohol oxidase activity to manganese peroxidase by site-directed mutagenesis. Biochem Biophys Res Commun 1999; 256: 500-504.
9. Blodig W, Smith AT, Doyle WA, Piontek K. Crystal structures of pristine and oxidatively processed lignin peroxidase expressed in Escherichia coli and W171F variant that eliminates the redox active tryptophan 171. J Mol Biol 2001; 305: 851-861.
10. Choinowski T, Blodig W, Winterhalter HK, Piontek K. The crystal structure of lignin peroxidase at 1.70 Å resolution reveals a hydroxy group on the Cβ of tryptophan 171: a novel radical site formed during the redox cycle. J Mol Biol 1999; 286: 809-827.
11. Blodig W, Doyle WA, Smith AT, Winterhalter HK, Choinowski T, Piontek K. Autocatalytic formation of a hydroxy group at Cβ of Trp171 in lignin peroxidase. Biochemistry 1998; 37: 8832-8838.
12. Smith AT, Doyle WA, Dorlet P, Ivancich A. Spectroscopic evidence for an engineered, catalytically active Trp radical that creates the unique reactivity of lignin peroxidase. Proc Natl Acad Sci USA 2009; 106: 16084-16089.
13. Senn HM, Thiel W. QM/MM Methods for Biomolecular Systems. Angew Chem Int Ed 2009; 48: 1198-1229.
14. Shaik S, Cohen S, Wang Y, Chen H, Kumar D, Thiel W. P450 enzymes: their structure, reactivity, and selectivities modeled by QM/MM calculations. Chem Rev 2010; 110: 949-1017.
15. Lin H, Truhlar DG. QM/MM: what have we learned, where are we, and where do we go from here? Theor Chem Acc 2007; 117: 185-199.
16. Schöneboom JC, Neese F, Thiel W. Toward identification of the compound I reactive intermediate in cytochrome P450 chemistry: a QM/MM study of its EPR and Mo1ssbauer parameters. J Am Chem Soc 2005; 127: 5840-5853.
17. Chen H, Lai W, Shaik S. Multireference and multiconfiguration ab initio methods in heme-related systems: what have we learned so far? J Phys Chem B 2011; 115: 1727-1742.
18. Altun A, Yokoyama S, Morokuma K. Color tuning in short wavelength-sensitive human and mouse visual pigments: ab initio quantum mechanics/molecular mechanics studies. J Phys Chem A 2009; 113: 11685-11692.
19. Pistolesi S, Sinicropi A, Pogni R, Basosi R, Ferré N, Olivucci M. Modeling the fluorescence of protein-embedded tryptophans with ab initio multiconfigurational quantum chemistry: the limiting cases of parvalbumin and monellin. J Phys Chem B 2009; 113: 16082-16090.
20. Sundararajan M, Riplinger C, Orio M, Wennmohs F, Neese F. Spectroscopic Properties of Protein-Bound Cofactors: Calculation by Combined Quantum Mechanical/Molecular Mechanical (QM/MM) Approaches. Encyclopedia of Inorganic and Bioinorganic Chemistry, 2011.
21. Sinicropi A, Andruniow T, Ferrè N, Basosi R, Olivucci M. Properties of the emitting state of the green fluorescent protein resolved at the CASPT2//CASSCF/CHARMM Level. J Am Chem Soc 2005; 127: 11534-11535.
22. Cimino P, Pedone A, Stendardo E, Barone V. Interplay of stereo-electronic, environmental, and dynamical effects in determining the EPR parameters of aromatic spin-probes: INDCO as a test case. Phys Chem Chem Phys 2010; 12: 3741-3746.
23. Olsson MHM, Hong G, Warshel A. Frozen density functional free energy simulations of redox proteins:computational studies of the reduction potential of plastocyanin and rusticyanin. J Am Chem Soc 2003; 125: 5025-5039.
24. Kamerlin SCL, Haranczyk M, Warshel A. Progress in ab initio QM/MM free-energy simulations of electrostatic energies in proteins: accelerated QM/MM Studies of pKa, redox reactions and solvation free energies. J Phys Chem B 2009; 113: 1253-1272.
25. Warshel A, Sharma PK, Kato M, Parson WW. Modeling electrostatic effects in proteins. Biochim Biophys Acta 2006; 1764: 1647-1676.
26. Sinnecker S, Flores M, Lubitz W. Protein-cofactor interactions in bacterial reaction centers from Rhodobacter sphaeroides R-26: effect of hydrogen bonding on the electronic and geometric structure of the primary quinone. A density functional theory study. Phys Chem Chem Phys 2006; 8: 5659-5670.
27. Barone V, Cimino P. Validation of the B3LYP/N07D and PBE0/N07D Computational models for the calculation of electronic g-tensors. J Chem Theor Comput 2009; 5: 192-199.
28. Brogioni B, Biglino D, Sinicropi A, Reijerse E, Giardina P, Sannia G, Lubitz W, Basosi R. Characterization of radical intermediates in the laccase-mediator systems. A multifrequency EPR, ENDOR and DFT/PCM investigation. Phys Chem Chem Phys 2008; 10: 7284-7292.
29. Pavone M, Cimino P, Crescenzi O, Sillanpää A, Barone V. Interplay of intrinsic, environmental, and dynamic effects in tuning the EPR parameters of nitroxides: further insights from an integrated computational approach. J Phys Chem B 2007; 111: 8928-8939.
30. van Gastel M, Lubitz W, Lassmann G, Neese F. Electronic structure of the cysteine thiyl radical: A DFT and correlated ab initio study. J Am Chem Soc 2004; 126: 2237-2246.
31. Baute D, Arieli D, Neese F, Zimmermann H, Weckhuysen BM, Goldfarb D. Carboxylate binding in copper histidine complexes in solution and in Zeolite Y X- and W-band pulsed EPR ENDOR combined with DFT calculations. J Am Chem Soc 2004; 126: 11733-11745.
32. Svistunenko DA, Jones GA. Tyrosyl radicals in proteins: a comparison of empirical and density functional calculated EPR parameters. Phys Chem Chem Phys 2009; 11: 6600.
33. Martin E, Samoilova RI, Narasimhulu KV, Lin T-J, O'Malley PJ, Wraight CA, Dikanov SA. Hydrogen bonding and spin density distribution in the QB semiquinone of bacterial reaction centers and comparison with the QA Site. J Am Chem Soc 2011; 133: 5525-5537.
34. Bernini C, Pogni R, Ruiz-Dueñas FJ, Martínez AT, Basosi R, Sinicropi A. EPR Parameters of amino acid radicals in P. eryngii versatile peroxidase and its W164Y variant computed at the QM/MM level. Phys Chem Chem Phys 2011; 13: 5078-5098.
35. Pauwels E, Declerck R, Verstraelen T, De Sterck B, Kay CWM, Van Speybroeck V, Waroquier M. Influence of protein environment on the electron paramagnetic resonance properties of flavoprotein radicals: a QM/MM study. J Phys Chem B 2010; 114: 16655-16665.
36. Hart R, O'Malley PJ. A quantum mechanics/molecular mechanics study of the tyrosine residue, TyrD, of Photosystem II. Biochim Biophys Acta 2010; 1797: 250-254.
37. Porro CS, Kumar D, de Visser SP. Electronic properties of pentacoordinated heme complexes in cytochrome P450 enzymes: search for an Fe(I) oxidation state. Phys Chem Chem Phys 2009; 11: 10219-10226.
38. Lin T-J, O'Malley PJ. An ONIOM study of the QA site semiquinone in the Rhodobacter sphaeroides photosynthetic reaction centre. J Mol Struct Theochem 2008; 870: 31-35.
39. Colombo MC, VandeVondele JV, Van Doorslaer S, Laio A, Guidoni L, Rothlisberger U. Copper binding sites in the C-terminal domain of mouse prion protein: a hybrid (QM/MM) molecular dynamics study. Proteins 2008; 70: 1084-1098.
40. Sinnecker S, Neese F. QM/MM calculations with DFT for taking into account protein effects on the EPR and optical spectra of metalloproteins. Plastocyanin as a case study. J Comput Chem 2006; 27: 1463-1475.
41. Moon S, Patchkovskii S, Salahub DR. QM/MM calculations of EPR hyperfine coupling constants in blue copper proteins. J Mol Struct Theochem 2003; 632: 287-295.
42. MacKerell Jr.AD, Bashford D, Bellott M, Dunbrack RL, Jr., Evanseck JD, Field MJ, Fischer S, Gao J, Guo H, Ha S, Joseph-McCarthy D, Kuchnir L, Kuczera K, Lau FTK, Mattos C, Michnick S, Ngo T, Nguyen DT, Prodhom B, Reiher WE, III, Roux B, Schlenkrich M, Smith JC, Stote R, Straub J, Watanabe M, Wiórkiewicz-Kuczera J, Yin D, Karplus M. All-atom empirical potential for molecular modeling and dynamics Studies of proteins. J Phys Chem B 1998; 102: 3586-3616.
43. Phillips JC, Braun R, Wang W, Gumbart J, Tajkhorshid E, Villa E, Chipot C, Skeel RD, Kale L, Schulten, K. Scalable molecular dynamics with NAMD. J Comput Chem 2005; 26: 1781-1802.
44. Aquiliante F, De Vico L, Ferré N, Ghigo G, Malmqvist P-Å, Neogrady P, Pedersen TB, Pitonak M, Reiher M, Roos BO, Serrano-Andrés L, Urban M, Veryazov V, Lindh R. MOLCAS 7: the next generation. J Comput Chem 2009; 31: 224-247.
45. Ponder JW. Tinker4.2-software tools for molecular design, Available at: ; 2004.
46. Neese F. ORCA. An ab initio, density functional and semiempirical program package, Version 28; Bonn University: Germany; 2010.
47. Becke AD. Density functional thermochemistry. III. The role of exact exchange. J Chem Phys 1993; 98: 5648-5652.
48. Lee C, Yang W, Parr RG. Development of the Colle-Salvetti correlation-energy formula into a functional of the electron density. Phys Rev B 1988; 37: 785-789.
49. Stephens PJ, Devlin FJ, Chabalowski CF, Frisch MJ. Ab initio calculation of vibrational absorption and circular dichroism spectra using density functional force fields. J Phys Chem 1994; 98: 11623-11627.
50. Barone V. Recent advances in density functional methods (Part I). World Scientific Publishing Co.; Singapore, 1995. pp 287-334.
51. Barone V, Polimeno A. Toward an integrated computational approach to CW-ESR spectra of free radicals. Phys Chem Chem Phys 2006; 8: 4609-4629.
52. Godbout N, Salahub DR, Andzelm J, Wimmer E. Optimization of Gaussian-type basis sets for local spin density functional calculations. Part I. Boron through neon, optimization technique and validation. Can J Chem 1992; 70: 560-571.
53. Un S. The g-values and hyperfine coupling of amino acid radicals in proteins: comparison of experimental measurements with ab initio calculations. Magn Res Chem 2005; 43: S229-S236.
54. Miller JE, Gradinaru C, Crane BR, Di Bilio AJ, Wehbi WA, Un S, Winkler JR, Gray HB. Spectroscopy and reactivity of a photogenerated tryptophan radical in a structurally defined protein environment. J Am Chem Soc 2003; 125: 14220-14221.
55. Pogni R, Baratto MC, Teutloff C, Giansanti S, Ruiz-Duenas FJ, Choinowski T, Piontek K, Martinez AT, Lendzian F, Basosi R. A tryptophan neutral radical in the oxidized state of versatile peroxidase from Pleurotus eryngii. J Biol Chem 2006; 28: 9517-9526.
56. Ruiz-Dueñas FJ, Pogni R, Morales M, Giansanti S, Mate MJ, Romero A, Martínez MJ, Basosi R, Martínez AT. Protein radicals in fungal versatile peroxidase: catalytic tryptophan radical in both compound I and compound II and studies on W164Y, W164H, and W164S variants. J Biol Chem 2009; 284: 7986-7994.
57. Neese F. Density functional theory and epr spectroscopy: a guided tour. EPR Newsletter 2009; 18: 4.
58. Further validation would require reliable calculations of the relevant redox potential by proper QM/MM approaches (Refs. 23-25).
59. Sivaraja M, Goodin DB, Smith M, Hoffman BM. Identification by ENDOR of Trp191 as the free-radical site in cytochrome c peroxidase compound ES. Science 1989; 245: 738-740.
60. Huyett JE, Doan PE, Gurbiel R, Houseman ALP, Sivaraja M, Goodin DB, Hoffman BM. Compound ES of cytochrome c peroxidase contains a Trp n-cation radical: characterization by CW and pulsed Q-band ENDOR spectroscopy. J Am Chem Soc 1995; 117: 9033-9041.
61. Himo F, Eriksson LA. Theoretical study of model tryptophan radicals and radical cations: comparison with experimental data of DNA photolyase, cytochrome c peroxidase, and ribonucleotide reductase. J Phys Chem B 1997; 101: 9811-9819.
62. Miller MA, Han GW, Kraut J. A cation binding motif stabilizes the compound I radical of cytochrome c peroxidase. Proc Natl Acad Sci USA 1994; 91: 11118-11122.
63. Menyhárd DK, Náray-Szabó Electrostatic effect on electron transfer at the active site of heme peroxidases: a comparative molecular orbital study on cytochrome c peroxidase and ascorbate peroxidase. J Phys Chem B 1999; 103: 227-233.