Skip to main content
Log in

Theoretical study of the catalytic mechanism of catechol oxidase

  • Original Paper
  • Published:
JBIC Journal of Biological Inorganic Chemistry Aims and scope Submit manuscript

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-η22 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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12
Fig. 13
Fig. 14
Fig. 15
Fig. 16
Fig. 17
Fig. 18
Fig. 19

Similar content being viewed by others

References

  1. Solomon EI, Baldwin MJ, Lowery MD (1992) Chem Rev 92:521–542

    Article  CAS  Google Scholar 

  2. Solomon EI, Sundaram UM, Machonkin TE (1996) Chem Rev 96:2563–2605

    Article  PubMed  CAS  Google Scholar 

  3. Cuff ME, Miller KI, van Holde KE, Hendrickson WA (1998) J Mol Biol 278:855–870

    Article  PubMed  CAS  Google Scholar 

  4. Gaykema WPJ, Hol WGJ, Vereijken JM, Soeter NM, Bak HJ, Beintema JJ (1984) Nature 309:23–29

    Article  CAS  Google Scholar 

  5. Magnus KA, Tonthat H, Carpenter JE (1994) Chem Rev 94:727–735

    Article  CAS  Google Scholar 

  6. Cary JW, Lax AR, Flurkey WH (1992) Plant Mol Biol 20:245–253

    Article  PubMed  CAS  Google Scholar 

  7. Deverall BJ (1961) Nature 189:311–315

    Article  CAS  Google Scholar 

  8. Baruah P, Swain T (1959) J Sci Food Agric 10:125–129

    Article  CAS  Google Scholar 

  9. Mayer AM, Harel E (1979) Phytochemistry 18:193–215

    Article  CAS  Google Scholar 

  10. Walker JRL, Ferrar PH (1998) Biotechnol Genet Eng Rev 15:457–498

    PubMed  CAS  Google Scholar 

  11. Klabunde T, Eicken C, Sacchettini JC, Krebs B (1998) Nat Struct Biol 5:1084–1090

    Article  PubMed  CAS  Google Scholar 

  12. Eicken C, Zippel F, Buldt-Karentzopoulos K, Krebs B (1998) FEBS Lett 436:293–299

    Article  PubMed  CAS  Google Scholar 

  13. Wilcox DE, Porras AG, Hwang YT, Lerch K, Winkler ME, Solomon EI (1985) J Am Chem Soc 107:4015–4027

    Article  CAS  Google Scholar 

  14. Eicken C, Krebs B, Sacchettini JC (1999) Curr Opin Struct Biol 9:677–683

    Article  PubMed  CAS  Google Scholar 

  15. Granata A, Monzani E, Bubacco L, Casella L (2006) Chem Eur J 12:2504–2514

    Article  CAS  Google Scholar 

  16. Ros JR, Rodriguezlopez JN, Garciacanovas F (1994) Biochim Biophys Acta Protein Struct Mol Enzymol 1204:33–42

    CAS  Google Scholar 

  17. Granata A, Monzani E, Casella L (2004) J Biol Inorg Chem 9:903–913

    Article  PubMed  CAS  Google Scholar 

  18. Siegbahn PEM (2004) J Biol Inorg Chem 9:577–590

    Article  PubMed  CAS  Google Scholar 

  19. Siegbahn PEM (2003) J Biol Inorg Chem 8:567–576

    PubMed  CAS  Google Scholar 

  20. Battaini G, Granata A, Monzani E, Gullotti M, Casella L (2006) Adv Inorg Chem Bioinorg Stud 58:185–233

    Google Scholar 

  21. Siegbahn PEM (2003) Q Rev Biophys 36:91–145

    Article  PubMed  CAS  Google Scholar 

  22. Lee SY, Lipscomb JD (1999) Biochemistry 38:4423–4432

    Article  PubMed  CAS  Google Scholar 

  23. Orville AM, Lipscomb JD (1997) Biochemistry 36:14044–14055

    Article  PubMed  CAS  Google Scholar 

  24. Bassan A, Borowski T, Siegbahn PEM (2004) Dalton Trans 20:3153–3162

    Article  PubMed  Google Scholar 

  25. Koval IA, Gamez P, Belle C, Selmeczi K, Reedijk J (2006) Chem Soc Rev 35:814–840

    Article  PubMed  CAS  Google Scholar 

  26. Ackermann J, Meyer F, Kaifer E, Pritzkow H (2002) Chem Eur J 8:247–258

    Article  CAS  Google Scholar 

  27. Berreau LM, Mahapatra S, Halfen JA, Houser RP, Young VG, Tolman WB (1999) Angew Chem Int Ed Engl 38:207–210

    Article  CAS  Google Scholar 

  28. Wegner R, Gottschaldt M, Gorls H, Jager EG, Klemm D (2001) Chem Eur J 7:2143–2157

    Article  CAS  Google Scholar 

  29. Torelli S, Belle C, Hamman S, Pierre JL, Saint-Aman E (2002) Inorg Chem 41:3983–3989

    Article  PubMed  CAS  Google Scholar 

  30. 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

    Article  PubMed  CAS  Google Scholar 

  31. Than R, Feldmann AA, Krebs B (1999) Coord Chem Rev 182:211–241

    Article  Google Scholar 

  32. Kao CH, Wei HH, Liu YH, Lee GH, Wang Y, Lee CJ (2001) J Inorg Biochem 84:171–178

    Article  PubMed  CAS  Google Scholar 

  33. 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

    Article  PubMed  CAS  Google Scholar 

  34. Belle C, Beguin C, Gautier-Luneau I, Hamman S, Philouze C, Pierre JL, Thomas F, Torelli S (2002) Inorg Chem 41:479–491

    Article  PubMed  CAS  Google Scholar 

  35. Merkel M, Moller N, Piacenza M, Grimme S, Rompel A, Krebs B (2005) Chem Eur J 11:1201–1209

    Article  CAS  Google Scholar 

  36. 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

    Article  CAS  Google Scholar 

  37. 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

    Article  CAS  Google Scholar 

  38. Selmeczi K, Reglier M, Giorgi M, Speier G (2003) Coord Chem Rev 245:191–201

    Article  CAS  Google Scholar 

  39. Born K, Comba P, Daubinet A, Fuchs A, Wadepohl H (2007) J Biol Inorg Chem 12:36–48

    Article  PubMed  CAS  Google Scholar 

  40. Santagostini L, Gullotti M, Monzani E, Casella L, Dillinger R, Tuczek F (2000) Chem Eur J 6:519–522

    Article  CAS  Google Scholar 

  41. Mahadevan V, DuBois JL, Hedman B, Hodgson KO, Stack TDP (1999) J Am Chem Soc 121:5583–5584

    Article  CAS  Google Scholar 

  42. Becke AD (1988) Phys Rev A 38:3098–3100

    Article  PubMed  CAS  Google Scholar 

  43. Becke AD (1993) J Chem Phys 98:5648–5652

    Article  CAS  Google Scholar 

  44. Becke AD (1993) J Chem Phys 98:1372–1377

    Article  CAS  Google Scholar 

  45. Lee CT, Yang WT, Parr RG (1988) Phys Rev B 37:785–789

    Article  CAS  Google Scholar 

  46. Schrödinger LLC (2003) MacroModel 8.5. Portland, OR

  47. Hay PJ, Wadt WR (1985) J Chem Phys 82:299–310

    Article  CAS  Google Scholar 

  48. 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

  49. 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

    Article  CAS  Google Scholar 

  50. Marten B, Kim K, Cortis C, Friesner RA, Murphy RB, Ringnalda MN, Sitkoff D, Honig B (1996) J Phys Chem 100:11775–11788

    Article  CAS  Google Scholar 

  51. Blomberg MRA, Siegbahn PEM, Babcock GT (1998) J Am Chem Soc 120:8812–8824

    Article  CAS  Google Scholar 

  52. Curtiss LA, Raghavachari K, Redfern PC, Pople JA (2000) J Chem Phys 112:7374–7383

    Article  CAS  Google Scholar 

  53. Siegbahn PEM, Blomberg MRA (1999) Annu Rev Phys Chem 50:221–249

    Article  PubMed  CAS  Google Scholar 

  54. Siegbahn PEM, Blomberg MRA (2000) Chem Rev 100:421–437

    Article  PubMed  CAS  Google Scholar 

  55. Blomberg MRA, Siegbahn PEM (2001) J Phys Chem B 105:9375–9386

    Article  CAS  Google Scholar 

  56. Pelmenschikov V, Cho KB, Siegbahn PEM (2004) J Comput Chem 25:311–321

    Article  PubMed  CAS  Google Scholar 

  57. Pelmenschikov V, Siegbahn PEM (2003) J Biol Inorg Chem 8:653–662

    Article  PubMed  CAS  Google Scholar 

  58. 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

    Article  PubMed  CAS  Google Scholar 

  59. Fontecave M, Ollagnier-de-Choudens S, Mulliez E (2003) Chem Rev 103:2149–2166

    Article  PubMed  CAS  Google Scholar 

  60. Whittaker MM, Whittaker JW (1988) J Biol Chem 263:6074–6080

    PubMed  CAS  Google Scholar 

  61. Proshlyakov DA, Pressler MA, Babcock GT (1998) Proc Natl Acad Sci USA 95:8020–8025

    Article  PubMed  CAS  Google Scholar 

  62. Decker H, Dillinger R, Tuczek F (2000) Angew Chem Int Ed Engl 39:1591–1595

    Article  PubMed  CAS  Google Scholar 

  63. Matoba Y, Kumagai T, Yamamoto A, Yoshitsu H, Sugiyama M (2006) J Biol Chem 281:8981–8990

    Article  PubMed  CAS  Google Scholar 

Download references

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

Authors

Corresponding author

Correspondence to Mireia Güell.

Rights and permissions

Reprints 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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00775-007-0293-z

Keywords

Navigation