Interdomain long-range electron transfer becomes rate-limiting in the Y216A variant of tyramine β-monooxygenase

Biochemistry

Volumn 52, Issue 7, 2013, Pages 1179-1191

  Osborne, Robert L ^a,d   Zhu, Hui ^a,b   Iavarone, Anthony T ^a,b   Blackburn, Ninian J ^c   Klinman, Judith P ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^d NONE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

C-H BOND CLEAVAGE; DICOPPER; ELECTRON PARAMAGNETIC RESONANCE SPECTRUM; ELECTRON STORAGE; ELECTRON TRANSFER; INTER-DOMAIN; ISOTOPE EFFECT; ISOTOPIC PARAMETERS; LONG-RANGE ELECTRON TRANSFER; MONONUCLEAR COPPER; MONOOXYGENASES; PARADIGM SHIFTS; RATE LIMITING; STEADY-STATE KINETICS;

AMINO ACIDS; COPPER; ELECTRON TRANSITIONS; ENZYMES; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; ISOTOPES; LIGANDS; MAGNETIC RESONANCE; PARAMAGNETISM; RATE CONSTANTS; X RAY ABSORPTION SPECTROSCOPY;

AMINES;

CUPROUS ION; ENZYME; ISOTOPE; LIGAND; PROTEIN VARIANT; TYRAMINE BETA MONOOXYGENASE; UNCLASSIFIED DRUG;

ARTICLE; COPPER METABOLISM; ELECTRON SPIN RESONANCE; ELECTRON TRANSPORT; ENZYME SUBSTRATE COMPLEX; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; PRIORITY JOURNAL; STEADY STATE; X RAY ABSORPTION SPECTROSCOPY;

ALANINE; ANIMALS; CATALYTIC DOMAIN; COPPER; DROSOPHILA PROTEINS; ELECTRON SPIN RESONANCE SPECTROSCOPY; ELECTRON TRANSPORT; ENZYME ACTIVATION; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; KINETICS; MIXED FUNCTION OXYGENASES; MUTATION; OCTOPAMINE; OXIDATION-REDUCTION; TYRAMINE; X-RAY ABSORPTION SPECTROSCOPY;

EID: 84874073581     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi3013609     Document Type: Article

References (42)

1. Evans, P. D. (1985) Octopamine. In Comprehensive Insect Physiology, Biochemistry and Pharmacology (Kerknt, G. A. and Gilbert, L. I., Eds.) pp 499-530, Pergamon, Oxford, U.K.
2. Klinman, J. P. (2006) The copper-enzyme family of dopamine β-monooxygenase and peptidylglycine α-hydroxylating monooxygenase: Resolving the chemical pathway for substrate hydroxylation J. Biol. Chem. 281, 3013-3016
3. Eipper, B. A., Quon, A. S. W., Mains, R. E., Boswell, J. S., and Blackburn, N. J. (1995) The catalytic core of peptidylglycine α-hydroxylating monooxygenase: Investigation by site-directed mutagenesis, Cu X-ray absorption spectroscopy, and electron paramagnetic resonance Biochemistry 34, 2857-2865
4. Gray, E. E., Small, S. N., and McGuirl, M. A. (2006) Expression and characterization of recombinant tyramine β-monooxygenase from Drosophila: A monomeric copper-containing hydroxylase Protein Expression Purif. 47, 162-170
5. Prigge, S. T., Eipper, B. A., Mains, R. E., and Amzel, L. M. (1997) Amidation of bioactive peptides: The structure of peptidylglycine α-hydroxylating monooxygenase Science 278, 1300-1305
6. Prigge, S. T., Kolhekar, A. S., Eipper, B. A., Mains, R. E., and Amzel, L. M. (1999) Substrate-mediated electron transfer in peptidylglycine α-hydroxylating monooxygenase Nature 6, 976-983
7. Prigge, S. T., Eipper, B. A., Mains, R. E., and Amzel, L. M. (2004) Dioxygen binds end-on to mononuclear copper in a precatalytic complex Science 304, 864-867
8. Siebert, X., Eipper, B. A., Mains, R. E., Prigge, S. T., Blackburn, N. J., and Amzel, L. M. (2005) The catalytic copper of peptidylglycine α-hydroxylating monooxygenase also plays a critical structural role Biophys. J. 89, 3312-3319
9. Blackburn, N. J., Pettingill, T. M., Seagraves, K. S., and Shigeta, R. T. (1990) Characterization of a carbon monoxide complex of reduced dopamine β-hydroxylase. Evidence for inequivalence of the Cu(I) centers J. Biol. Chem. 265, 15383-15386
10. Klinman, J. P. (1996) Mechanisms whereby mononuclear copper proteins functionalize organic substrates Chem. Rev. 96, 2541-2561
11. Boswell, J. S., Reedy, B. J., Kulathila, R., Merkler, D., and Blackburn, N. J. (1996) Structural investigations on the coordination environment of the active site copper centers of recombinant bifunctional peptidylglycine α-amidating enzyme Biochemistry 35, 12241-12250
12. Reedy, B. J. and Blackburn, N. J. (1994) Preparation and characterization of half-apo dopamine-β-hydroxylase by selective removal of CuA. Identification of a sulfur ligand at the dioxygen binding site by EXAFS and FTIR spectroscopy J. Am. Chem. Soc. 116, 1924-1931
13. Scott, R. A., Sullivan, R. J., DeWolf, W. E., Dolle, R. E., and Kruse, L. I. (1988) The copper sites of dopamine β-hydroxylase: An X-ray absorption spectroscopic study Biochemistry 27, 5411-5417
14. Hess, C. R., Klinman, J. P., and Blackburn, N. J. (2010) The copper centers of tyramine β-monooxygenase and its catalytic-site methionine variants. An X-ray absorption study J. Biol. Inorg. Chem. 15, 1195-1207
15. Goldstein, M., Joh, T. H., and Garvey, T. Q., III (1968) Kinetic studies of the enzymic dopamine β-hydroxylation reaction Biochemistry 7, 2724-2730
16. Klinman, J. P., Humphries, H., and Voet, J. G. (1980) Deduction of kinetic mechanism in multisubstrate enzyme reactions from tritium isotope effects J. Biol. Chem. 255, 11648-11651
17. Brenner, M. C. and Klinman, J. P. (1989) Correlation of copper valency with product formation in single turnovers of dopamine β-monooxygenase Biochemistry 28, 4664-4670
18. Francisco, W. A., Merkler, D. J., Blackburn, N. J., and Klinman, J. P. (1998) Kinetic mechanism and intrinsic isotope effects for the peptidylglycine α-amidating enzyme reaction Biochemistry 37, 8244-8252
19. Tian, G., Berry, J. A., and Klinman, J. P. (1994) Oxygen-18 kinetic isotope effects in the dopamine β-monooxygenase reaction: Evidence for a new chemical mechanism in non-heme metallomonooxygenases Biochemistry 33, 226-234
20. Crespo, A., Martí, M. A., Roitberg, A. E., Amzel, L. M., and Estrin, D. A. (2006) The catalytic mechanism of peptidylglycine α-hydroxylating monooxygenase investigated by computer simulation J. Am. Chem. Soc. 128, 12817-12828
21. Francisco, W. A., Blackburn, N. J., and Klinman, J. P. (2003) Oxygen and hydrogen isotope effects in an active site tyrosine to phenylalanine mutant of peptidylglycine α-hydroxylating monooxygenase: Mechanistic implications Biochemistry 42, 1813-1819
22. Evans, J. P., Ahn, K., and Klinman, J. P. (2003) Evidence that dioxygen and substrate activation are tightly coupled in dopamine β-monooxygenase. Implications for the reactive oxygen species J. Biol. Chem. 278, 49691-49698
23. Evans, J. P., Blackburn, N. J., and Klinman, J. P. (2006) The catalytic role of the copper ligand H172 of peptidylglycine α-hydroxylating monooxygenase: A kinetic study of the H172A mutant Biochemistry 45, 15419-15429
24. Chen, P. and Solomon, E. I. (2004) 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, 4991-5000
25. Kunishita, A., Kubo, M., Sugimoto, H., Ogura, T., Sato, K., Takui, T., and Itoh, S. (2009) Mononuclear copper(II)-superoxo complexes that mimic the structure and reactivity of the active centers of PHM and DβM J. Am. Chem. Soc. 131, 2788-2789
26. A site of peptidylglycine α-hydroxylating monooxygenase and dopamine β-monooxygenase Inorg. Chem. 51, 9465-9480
27. Francisco, W. A., Wille, G., Smith, A. J., Merkler, D. J., and Klinman, J. P. (2004) Investigation of the pathway for inter-copper electron transfer in peptidylglycine α-amidating monooxygenase J. Am. Chem. Soc. 126, 13168-13169
28. Bell, J., El Meskini, R., D'Amato, D., Mains, R. E., and Eipper, B. A. (2003) Mechanistic investigation of peptidylglycine α-hydroxylating monooxygenase via intrinsic tryptophan fluorescence and mutagenesis Biochemistry 42, 7133-7142
29. Hess, C. R., Wu, Z., Ng, A., Gray, E. E., McGuirl, M. M., and Klinman, J. P. (2008) Hydroxylase activity of Met471Cys tyramine β-monooxygenase J. Am. Chem. Soc. 130, 11939-11944
30. Hess, C. R., McGuirl, M. M., and Klinman, J. P. (2008) Mechanism of the insect enzyme, tyramine β-monooxygenase, reveals differences from the mammalian enzyme, dopamine β-monooxygenase J. Biol. Chem. 283, 3042-3049
31. George, G. N. (1990) Exafspak, Stanford Synchrotron Radiation Laboratory, Stanford, CA.
32. Binsted, N., Gurman, S. J., and Campbell, J. W. (1998) Excurve, version 9.2, Daresbury Laboratory, Warrington, U.K.
33. Gurman, S. J., Binsted, N., and Ross, I. (1984) A rapid, exact curved-wave theory for EXAFS calculations J. Phys. C: Solid State Phys. 17, 143-151
34. Gurman, S. J., Binsted, N., and Ross, I. (1986) A rapid, exact curved-wave theory for EXAFS calculations. II. The multiple-scattering contributions J. Phys. C: Solid State Phys. 19, 1845-1861
35. Binsted, N. and Hasnain, S. S. (1996) State-of-the-art analysis of whole X-ray absorption spectra J. Synchrotron Radiat. 3, 185-196
36. Blackburn, N. J., Rhames, F. C., Ralle, M., and Jaron, S. (2000) Major changes in copper coordination accompany reduction of peptidylglycine monooxygenase: Implications for electron transfer and the catalytic mechanism J. Biol. Inorg. Chem. 5, 341-353
37. Osborne, R. L., Zhu, H., Iavarone, A. T., Hess, C. R., and Klinman, J. P. (2012) Inactivation of Met471Cys tyramine β-monooxygenase results from site-specific cysteic acid formation Biochemistry 51, 7488-7495
38. Miller, S. M. and Klinman, J. P. (1985) Secondary isotope effects and structure-reactivity correlations in the dopamine β-monooxygenase reaction: Evidence for a chemical mechanism Biochemistry 24, 2114-2127
39. Miller, S. M. and Klinman, J. P. (1983) Magnitude of the intrinsic isotope effects in the dopamine β-monooxygenase reaction Biochemistry 22, 3091-3096
40. Nagel, Z. D., Dong, M., Bahnson, B. J., and Klinman, J. P. (2011) Impaired conformational landscapes as revealed in anomalous Arrhenius prefactors Proc. Natl. Acad. Sci. U.S.A. 108, 10520-10525
41. Sharma, S. and Klinman, J. P. (2013) Kinetic detection of impaired protein conformational landscapes: double mutants of soybean lipoxygenase. In preparation.
42. Osborne, R. L. and Klinman, J. P. (2011) Insights into the proposed copper oxygen intermediates that regulate the mechanism of reactions catalyzed by dopamine β-monooxygenase, peptidylglycine α-hydroxylating monooxygenase, and tyramine β-monooxygenase. In Copper Oxygen Chemistry (Karlin, K. D., and Itoh, S., Eds.) Vol. 4, pp 1-22, Wiley Series on Reactive Intermediates in Chemistry and Biology, Wiley & Sons, Ltd., New York.