Abstract
The mechanism for the oxidation of catechol by catechol oxidase has been studied using B3LYP hybrid density functional theory. On the basis of the X-ray structure of the enzyme, the molecular system investigated includes the first-shell protein ligands of the two metal centers as well as the second-shell ligand Cys92. The cycle starts out with the oxidized, open-shell singlet complex with oxidation states Cu2(II,II) with a μ-η2:η2 bridging peroxide, as suggested experimentally, which is obtained from the oxidation of Cu2(I,I) by dioxygen. The substrate of each half-reaction is a catechol molecule approaching the dicopper complex: the first half-reaction involves Cu(I) oxidation by peroxide and the second one Cu(II) reduction. The quantitative potential energy profile of the reaction is discussed in connection with experimental data. Since no protons leave or enter the active site during the catalytic cycle, no external base is required. Unlike the previous density functional theory study, the dicopper complex has a charge of +2.
Similar content being viewed by others
References
Solomon EI, Baldwin MJ, Lowery MD (1992) Chem Rev 92:521–542
Solomon EI, Sundaram UM, Machonkin TE (1996) Chem Rev 96:2563–2605
Cuff ME, Miller KI, van Holde KE, Hendrickson WA (1998) J Mol Biol 278:855–870
Gaykema WPJ, Hol WGJ, Vereijken JM, Soeter NM, Bak HJ, Beintema JJ (1984) Nature 309:23–29
Magnus KA, Tonthat H, Carpenter JE (1994) Chem Rev 94:727–735
Cary JW, Lax AR, Flurkey WH (1992) Plant Mol Biol 20:245–253
Deverall BJ (1961) Nature 189:311–315
Baruah P, Swain T (1959) J Sci Food Agric 10:125–129
Mayer AM, Harel E (1979) Phytochemistry 18:193–215
Walker JRL, Ferrar PH (1998) Biotechnol Genet Eng Rev 15:457–498
Klabunde T, Eicken C, Sacchettini JC, Krebs B (1998) Nat Struct Biol 5:1084–1090
Eicken C, Zippel F, Buldt-Karentzopoulos K, Krebs B (1998) FEBS Lett 436:293–299
Wilcox DE, Porras AG, Hwang YT, Lerch K, Winkler ME, Solomon EI (1985) J Am Chem Soc 107:4015–4027
Eicken C, Krebs B, Sacchettini JC (1999) Curr Opin Struct Biol 9:677–683
Granata A, Monzani E, Bubacco L, Casella L (2006) Chem Eur J 12:2504–2514
Ros JR, Rodriguezlopez JN, Garciacanovas F (1994) Biochim Biophys Acta Protein Struct Mol Enzymol 1204:33–42
Granata A, Monzani E, Casella L (2004) J Biol Inorg Chem 9:903–913
Siegbahn PEM (2004) J Biol Inorg Chem 9:577–590
Siegbahn PEM (2003) J Biol Inorg Chem 8:567–576
Battaini G, Granata A, Monzani E, Gullotti M, Casella L (2006) Adv Inorg Chem Bioinorg Stud 58:185–233
Siegbahn PEM (2003) Q Rev Biophys 36:91–145
Lee SY, Lipscomb JD (1999) Biochemistry 38:4423–4432
Orville AM, Lipscomb JD (1997) Biochemistry 36:14044–14055
Bassan A, Borowski T, Siegbahn PEM (2004) Dalton Trans 20:3153–3162
Koval IA, Gamez P, Belle C, Selmeczi K, Reedijk J (2006) Chem Soc Rev 35:814–840
Ackermann J, Meyer F, Kaifer E, Pritzkow H (2002) Chem Eur J 8:247–258
Berreau LM, Mahapatra S, Halfen JA, Houser RP, Young VG, Tolman WB (1999) Angew Chem Int Ed Engl 38:207–210
Wegner R, Gottschaldt M, Gorls H, Jager EG, Klemm D (2001) Chem Eur J 7:2143–2157
Torelli S, Belle C, Hamman S, Pierre JL, Saint-Aman E (2002) Inorg Chem 41:3983–3989
Koval IA, Belle C, Selmeczi K, Philouze C, Saint-Aman E, Schuitema AM, Gamez P, Pierre JL, Reedijk J (2005) J Biol Inorg Chem 10:739–750
Than R, Feldmann AA, Krebs B (1999) Coord Chem Rev 182:211–241
Kao CH, Wei HH, Liu YH, Lee GH, Wang Y, Lee CJ (2001) J Inorg Biochem 84:171–178
Torelli S, Belle C, Gautier-Luneau I, Pierre JL, Saint-Aman E, Latour JM, Le Pape L, Luneau D (2000) Inorg Chem 39:3526–3536
Belle C, Beguin C, Gautier-Luneau I, Hamman S, Philouze C, Pierre JL, Thomas F, Torelli S (2002) Inorg Chem 41:479–491
Merkel M, Moller N, Piacenza M, Grimme S, Rompel A, Krebs B (2005) Chem Eur J 11:1201–1209
Koval IA, Sehmeczi K, Belle C, Philouze C, Saint-Aman E, Gautier-Luneau I, Schuitema AM, van Vliet M, Gamez P, Roubeau O, Luken M, Krebs B, Lutz M, Spek AL, Pierre JL, Reedijk J (2006) Chem Eur J 12:6138–6150
Monzani E, Battaini G, Perotti A, Casella L, Gullotti M, Santagostini L, Nardin G, Randaccio L, Geremia S, Zanello P, Opromolla G (1999) Inorg Chem 38:5359–5369
Selmeczi K, Reglier M, Giorgi M, Speier G (2003) Coord Chem Rev 245:191–201
Born K, Comba P, Daubinet A, Fuchs A, Wadepohl H (2007) J Biol Inorg Chem 12:36–48
Santagostini L, Gullotti M, Monzani E, Casella L, Dillinger R, Tuczek F (2000) Chem Eur J 6:519–522
Mahadevan V, DuBois JL, Hedman B, Hodgson KO, Stack TDP (1999) J Am Chem Soc 121:5583–5584
Becke AD (1988) Phys Rev A 38:3098–3100
Becke AD (1993) J Chem Phys 98:5648–5652
Becke AD (1993) J Chem Phys 98:1372–1377
Lee CT, Yang WT, Parr RG (1988) Phys Rev B 37:785–789
Schrödinger LLC (2003) MacroModel 8.5. Portland, OR
Hay PJ, Wadt WR (1985) J Chem Phys 82:299–310
Frisch MJ, Trucks GW, Schlegel HB, Scuseria GE, Robb MA, Cheeseman JR, Montgomery JA Jr, Vreven T, Kudin KN, Burant JC, Millam JM, Iyengar SS, Tomasi J, Barone V, Mennucci B, Cossi M, Scalmani G, Rega N, Petersson GA, Nakatsuji H, Hada M, Ehara M, Toyota K, Fukuda R, Hasegawa J, Ishida M, Nakajima T, Honda Y, Kitao O, Nakai H, Klene M, Li X, Knox JE, Hratchian HP, Cross JB, Bakken V, Adamo C, Jaramillo J, Gomperts R, Stratmann RE, Yazyev O, Austin AJ, Cammi R, Pomelli C, Ochterski JW, Ayala PY, Morokuma K, Voth GA, Salvador P, Dannenberg JJ, Zakrzewski G, Dapprich S, Daniels AD, Strain MC, Farkas O, Malick DK, Rabuck AD, Raghavachari K, Foresman JB, Ortiz JV, Cui Q, Baboul AG, Clifford S, Cioslowski J, Stefanov BB, Liu G, Liashenko A, Piskorz P, Komaromi I, Martin RL, Fox DJ, Keith T, Al-Laham MA, Peng CY, Nanayakkara A, Challacombe M, Gill PMW, Johnson B, Chen W, Wong MW, Gonzalez C, Pople JA (2003) Gaussian 03, revision B.05. Gaussian, Pittsburgh
Tannor DJ, Marten B, Murphy R, Friesner RA, Sitkoff D, Nicholls A, Ringnalda M, Goddard WA, Honig B (1994) J Am Chem Soc 116:11875–11882
Marten B, Kim K, Cortis C, Friesner RA, Murphy RB, Ringnalda MN, Sitkoff D, Honig B (1996) J Phys Chem 100:11775–11788
Blomberg MRA, Siegbahn PEM, Babcock GT (1998) J Am Chem Soc 120:8812–8824
Curtiss LA, Raghavachari K, Redfern PC, Pople JA (2000) J Chem Phys 112:7374–7383
Siegbahn PEM, Blomberg MRA (1999) Annu Rev Phys Chem 50:221–249
Siegbahn PEM, Blomberg MRA (2000) Chem Rev 100:421–437
Blomberg MRA, Siegbahn PEM (2001) J Phys Chem B 105:9375–9386
Pelmenschikov V, Cho KB, Siegbahn PEM (2004) J Comput Chem 25:311–321
Pelmenschikov V, Siegbahn PEM (2003) J Biol Inorg Chem 8:653–662
Rompel A, Fischer H, Meiwes D, Buldt-Karentzopoulos K, Dillinger R, Tuczek F, Witzel H, Krebs B (1999) J Biol Inorg Chem 4:56–63
Fontecave M, Ollagnier-de-Choudens S, Mulliez E (2003) Chem Rev 103:2149–2166
Whittaker MM, Whittaker JW (1988) J Biol Chem 263:6074–6080
Proshlyakov DA, Pressler MA, Babcock GT (1998) Proc Natl Acad Sci USA 95:8020–8025
Decker H, Dillinger R, Tuczek F (2000) Angew Chem Int Ed Engl 39:1591–1595
Matoba Y, Kumagai T, Yamamoto A, Yoshitsu H, Sugiyama M (2006) J Biol Chem 281:8981–8990
Acknowledgment
M.G. thanks the MEC for research grants and J.M. Luis for valuable discussions. We thank the reviewers for helpful comments.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Güell, M., Siegbahn, P.E.M. Theoretical study of the catalytic mechanism of catechol oxidase. J Biol Inorg Chem 12, 1251–1264 (2007). https://doi.org/10.1007/s00775-007-0293-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00775-007-0293-z