Advances in studying bioinorganic reaction mechanisms: isotopic probes of activated oxygen intermediates in metalloenzymes

Current Opinion in Chemical Biology

Volumn 11, Issue 2, 2007, Pages 142-150

  Roth, Justine P ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COPPER AMINE OXIDASE; CUPRIC ION; ENZYME; GLUCOSE OXIDASE; ISOTOPE; METALLOENZYME; OXIDOREDUCTASE; OXYGEN; SUPEROXIDE DISMUTASE; UNCLASSIFIED DRUG; UNSPECIFIC MONOOXYGENASE;

ENZYME MECHANISM; FRACTIONATION; HYDROGEN BOND; INORGANIC CHEMISTRY; ISOTOPE ANALYSIS; MOLECULAR PROBE; OXYGEN AFFINITY; REVIEW; STRUCTURE ANALYSIS;

AMINE OXIDASE (COPPER-CONTAINING); CHEMISTRY, BIOINORGANIC; DOPAMINE BETA-HYDROXYLASE; ENZYMES; GLUCOSE OXIDASE; KINETICS; METALS; OXYGEN; OXYGEN ISOTOPES;

EID: 34047136256     PISSN: 13675931     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cbpa.2007.01.683     Document Type: Review

References (37)

1. Biological Inorganic Chemistry. In: Bertini I., Gray H.B., Stiefel E.I., and Valentine J.S. (Eds). Structure and Reactivity (2006), University Science Books, Sausalito, California
2. Decker A., and Solomon E.I. Dioxygen activation by copper, heme and non-heme iron enzymes: comparison of electronic structures and reactivities. Curr Opin Chem Biol 9 (2005) 152-163
3. Prigge S.T., Eipper B.A., Mains R.E., and Amzel L.M. Dioxygen binds end-on to mononuclear copper in a precatalytic enzyme complex. Science 304 (2004) 864-867. This paper presents the crystal structure of an oxygenated intermediate in peptidylglycine α-hydroxylating monooxygenase and assigns it as a copper(II) superoxide species.
4. Wilmot C.M., and Pearson A.R. Cryocrystallography of metalloprotein reaction intermediates. Curr Opin Chem Biol 6 (2002) 202-207
5. Roth J.P., and Klinman J.P. Oxygen-18 isotope effects as a probe of enzymatic activation of molecular oxygen. In: Kohen A., and Limbach H.-H. (Eds). Isotope Effects in Chemistry and Biology (2006), CRC Press, Boca Raton 645-666. Studies of oxygen isotope effects published between 1993 and 2004 are reviewed and discussed in the context of supporting mechanistic data. Descriptions of cytochrome P450, lipoxygenase, tyrosine hydroxylase and soluble methane monooxygenase are included in addition to some of the enzymes described in this review.
6. 2 activation in chemical and biological systems. J Mol Cat A 251 (2006) 100-107
7. Huskey W.P. Origins and interpretations of heavy atom isotope effects. In: Cook P.F. (Ed). Enzyme Mechanism from Isotope Effects (1991), CRC Press, Boca Raton 37-73
8. 18O in oxygen binding to the reversible oxygen carriers hemoglobin, myoglobin, hemerythrin, and hemocyanin: a new probe for oxygen binding and reductive activation by proteins. J Am Chem Soc 115 (1993) 8891-8897
9. 2.
10. 2 complexes, and critically evaluates the ability of the computational approach to reproduce experimental isotopic shifts for ground state structures.
11. 2 binding. The trend is most easily attributed to a dominant contribution to the KIE from the O-O stretching mode, supporting a commonly made assumption that the isotope effect upon the reaction coordinate frequency is negligible.
12. 2. Some discussion is provided as to the physical origin of the oxygen isotope effects and the contributions from both the O-O and metal-O stretching modes.
13. Macdonald I.D.G., Sligar S.G., Christian J.F., Unno M., and Champion P. Identification of the Fe-O-O bending mode in oxycytochrome P450cam by resonance Raman spectroscopy. J Am Chem Soc 121 (1999) 376-380
14. Hirota S., Ogura T., Appelman E.H., Shinzawa-Itoh K., Yoshikawa S., and Kitagawa T. Observation of a new oxygen-isotope-sensitive Raman band for oxyhemoproteins and its implications in heme pocket structures. J Am Chem Soc 116 (1994) 10564-10570
15. 2 stretching modes in oxyhemoglobins. Proc Natl Acad Sci USA 98 (2001) 479-484
16. Brunold T.C., and Solomon E.I. Reversible dioxygen binding to hemerythrin. 1. Electronic structures of deoxy- and oxyhemerythrin. J Am Chem Soc 121 (1999) 8277-8287
17. Ling J., Nestor L.P., Czernuszewicz R.S., Spiro T.G., Fraczkiewicz R., Sharma K.D., Loehr T.M., and Sanders-Loehr J. Common oxygen binding site in hemocyanins from arthropods and mollusks. Evidence from Raman spectroscopy and normal coordinate analysis. J Am Chem Soc 116 (1994) 7682-7691
18. Baldwin M.J., Root D.E., Pate J.E., Fujisawa K., Kitajima N., and Soloman E.I. Spectroscopic studies of side-on peroxide-bridged binuclear copper(II) model complexes of relevance to oxyhemocyanin and oxytyrosinase. J Am Chem Soc 114 (1992) 10421-10431
19. 2 activation by the flavoprotein glucose oxidase. Proc Natl Acad Sci USA 100 (2003) 62-67
20. Valentine J.S., Doucette P.A., and Potter S.Z. Copper-zinc superoxide dismutase and amyotrophic lateral sclerosis. Annu Rev Biochem 74 (2005) 563-593
21. - radicals catalyzed by superoxide dismutase. A pulse radiolytic investigation. Isr J Chem 10 (1972) 1095-1106
22. 2 intermediates with superoxide and peroxide structures are predicted.
23. 18O KIEs using quantum mechanical ET theory are described.
24. 2. J Biol Chem 269 (1994) 2405-2410
25. Dooley D.M., McGuirl M.A., Brown D.E., Turowski P.N., McIntire W.S., and Knowles P.F. A Cu(I)-semiquinone state in substrate-reduced amine oxidase. Nature 349 (1991) 262-264
26. Turowski P.N., McGuirl M.A., and Dooley D.M. Intramolecular electron transfer rate between active-site copper and topaquinone in pea seedling amine oxidase. J Biol Chem 268 (1993) 17680-17682
27. 2 binds to Cu(I).
28. Klinman J.P. The multi-functional topa-quinone copper amine oxidases. Biochim Biophys Acta 1647 (2003) 131-137
29. Mills S.A., Goto Y., Su Q., Plastino J., and Klinman J.P. Mechanistic comparison of the cobalt-substituted and wild-type copper amine oxidase from Hansenula polymorpha. Biochemistry 41 (2002) 10577-10584
30. Takahashi K., and Klinman J.P. Relationship of stopped flow to steady state parameters in the dimeric copper amine oxidase from Hansenula polymorpha and the role of zinc in inhibiting activity at alternate copper-containing subunits. Biochemistry 45 (2006) 4683-4694
31. Su Q., and Klinman J.P. Probing the mechanism of proton coupled electron transfer to dioxygen: the oxidation half-reaction of bovine serum amine oxidase. Biochemistry 37 (1998) 12513-12525
32. Francisco W.A., Wille G., Smith A.J., Merkler D.J., and Klinman J.P. Investigation of the pathway for inter-copper electron transfer in peptidylglycine α-amidating monooxygenase. J Am Chem Soc 126 (2004) 13168-13169
33. Klinman J.P. The copper-enzyme family of dopamine β-monooxygenase and peptidylglycine α-hydroxylating monooxygenase: resolving the chemical pathway for substrate hydroxylation. J Biol Chem 281 (2006) 3013-3016. This is a recent review of mechanistic studies conducted over the course of several years including those described in [36] and [37]. The results are analyzed in the context of the proposed reactive oxidants and found to be most consistent with a copper(II) superoxide species effecting C-H oxidation.
34. Crespo A., Marti M.A., Roitberg A.E., Amzel L.M., and Estrin D.A. The catalytic mechanism of peptidylglycine α -hydroxylating monooxygenase investigated by computer simulation. J Am Chem Soc 128 (2006) 12817-12828. This paper presents computational results indicating that copper(II) superoxide and copper(II) peroxide intermediates are unlikely to abstract an H{radical dot} from an unactivated C-H bond. A copper(III)oxide/copper(II)oxyl radical is suggested as an alternative. This species is proposed to form following net hydrogen atom transfer to a copper(II) hydroperoxide intermediate.
35. Chen P., and Solomon E.I. Oxygen activation by the noncoupled binuclear copper site in peptidylglycine α-hydroxylating monooxygenase. Reaction mechanism and role of the noncoupled nature of the active site. J Am Chem Soc 126 (2004) 4991-5000. This paper presents computational studies which generally support the mechanism proposed by Klinman and coworkers ([36] and [37]), although the reactive intermediate is specifically formulated as having a side-on copper(II) superoxide structure. An alternative view of the steps subsequent to irreversible C-H oxidation step is proposed.
36. Francisco W.A., Blackburn N.J., and Klinman J.P. Oxygen and hydrogen isotope effects in an active site tyrosine to phenylalanine mutant of peptidylglycine α-hydroxylating monooxygenase: mechanistic implications. Biochemistry 42 (2003) 1813-1819
37. Evans J.P., Ahn K., and Klinman J.P. Evidence that dioxygen and substrate activation are tightly coupled in dopamine β-monooxygenase. J Biol Chem 278 (2003) 49691-49698