A copper-methionine interaction controls the pH-dependent activation of peptidylglycine monooxygenase

Biochemistry

Volumn 50, Issue 50, 2011, Pages 10819-10828

  Bauman, Andrew T ^a,b   Broers, Brenda A ^a   Kline, Chelsey D ^a   Blackburn, Ninian J ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b VLST Corporation   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CONFORMATIONAL CHANGE; CYS RESIDUES; EXAFS; EXTENDED X-RAY ABSORPTION FINE STRUCTURE DATUM; INTERACTION CONTROLS; LIMITED DATA; MODEL-BASED OPC; MONOOXYGENASES; NEW STUDY; PH DEPENDENCE; PH RANGE; PH-DEPENDENT; PROTEIN CONFORMATION; PROTON TUNNELING; PROTONATED; RIGID CONFORMERS; SEQUENCE COMPARISONS; SIDE-CHAINS; VIBRATIONAL MODES; WILD TYPES;

AMINO ACIDS; CATALYST ACTIVITY; COPPER; EXTENDED X RAY ABSORPTION FINE STRUCTURE SPECTROSCOPY; LIGANDS;

PH EFFECTS;

COPPER; CYSTEINE; IMIDAZOLE; METHIONINE; PEPTIDYLGLYCINE MONOOXYGENASE; UNCLASSIFIED DRUG; UNSPECIFIC MONOOXYGENASE;

ACIDITY; ALKALINITY; ARTICLE; CATALYSIS; CONTROLLED STUDY; ENZYME ACTIVATION; PH; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN INTERACTION; X RAY ABSORPTION SPECTROSCOPY;

AMINO ACID SUBSTITUTION; BIOCATALYSIS; CATALYTIC DOMAIN; COPPER; ENZYME ACTIVATION; FOURIER ANALYSIS; HUMANS; HYDROGEN-ION CONCENTRATION; KINETICS; METHIONINE; MIXED FUNCTION OXYGENASES; MODELS, MOLECULAR; MULTIENZYME COMPLEXES; MUTANT PROTEINS; OXIDATION-REDUCTION; PROTEIN BINDING; PROTEIN CONFORMATION; RECOMBINANT PROTEINS; X-RAY ABSORPTION SPECTROSCOPY;

EID: 83455169461     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi201193j     Document Type: Article

References (45)

1. Prigge, S. T., Mains, R. E., Eipper, B. A., and Amzel, L. M. (2000) New insights into copper monooxygenases and peptide amidation: Structure, mechanism and function Cell. Mol. Life Sci. 57, 1236-1259 (Pubitemid 30663481)
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 (Pubitemid 43845909)
3. 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
4. Hess, C. R., Wu, Z., Ng, A., Gray, E. E., McGuirl, M. A., and Klinman, J. P. (2008) Hydroxylase activity of Met471Cys tyramine β-monooxygenase J. Am. Chem. Soc. 130, 11939-11944
5. Blackburn, N. J., Hasnain, S. S., Pettingill, T. M., and Strange, R. W. (1991) Copper K-EXAFS studies of oxidized and reduced dopamine-β- hydroxylase: Confirmation of a sulfur ligand to Cu(I) in the reduced enzyme J. Biol. Chem. 266, 23120-23127 (Pubitemid 21908768)
6. Pettingill, T. M., Strange, R. W., and Blackburn, N. J. (1991) Carbonmonoxy dopamine-β-hydroxylase: Structural characterization by FTIR, fluorescence and XAS spectroscopy J. Biol. Chem. 266, 16996-17003 (Pubitemid 21907897)
7. Boswell, J. S., Reedy, B. J., Kulathila, R., Merkler, D. J., 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 (Pubitemid 26331245)
8. M-OOH intermediate Biochemistry 43, 5735-5747 (Pubitemid 38623608)
9. Prigge, S. T., Kolhekar, A. S., 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 (Pubitemid 27495743)
10. 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 Nat. Struct. Biol. 6, 976-983 (Pubitemid 29463313)
11. 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 (Pubitemid 41636086)
12. Chufan, E. E., Prigge, S. T., Siebert, X., Eipper, B. A., Mains, R. E., and Amzel, L. M. (2010) Differential reactivity between two copper sites in peptidylglycine α-hydroxylating monooxygenase J. Am. Chem. Soc. 132, 15565-15572
13. Magnus, K. A., Hazes, B., Ton-That, H., Bonaventura, C., Bonaventura, J., and Hol, W. G. J. (1994) Crystallographic analysis of oxygenated and deoxygenated states of arthropod hemocyanin shows unusual differences Proteins: Struct., Funct., Genet. 19, 302-309 (Pubitemid 24254061)
14. Gerdemann, C., Eicken, C., and Krebs, B. (2002) The crystal structure of catechol oxidase: New insight into the function of type-3 copper proteins Acc. Chem. Res. 35, 183-191
15. 2 activation by binuclear Cu sites: Noncoupled versus exchange coupled reaction mechanisms Proc. Natl. Acad. Sci. U.S.A. 101, 13105-13110 (Pubitemid 39213988)
16. Matoba, Y., Kumagai, T., Yamamoto, A., Yoshitsu, H., and Sugiyama, M. (2006) Crystallographic evidence that the dinuclear copper center of tyrosinase is flexible during catalysis J. Biol. Chem. 281, 8981-8990 (Pubitemid 43848005)
17. Lewis, E. A. and Tolman, W. B. (2004) Reactivity of dioxygen-copper systems Chem. Rev. 104, 1047-1076
18. 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 oxygen activation J. Biol. Chem. 278, 49691-49698 (Pubitemid 37548801)
19. Bauman, A. T., Yukl, E. T., Alkevich, K., McCormack, A. L., and Blackburn, N. J. (2006) The hydrogen peroxide reactivity of peptidylglycine monooxygenase supports a Cu(II)-superoxo catalytic intermediate J. Biol. Chem. 281, 4190-4198 (Pubitemid 43847847)
20. 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 (Pubitemid 38495790)
21. 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
22. Kolhekar, A. S., Keutman, H. T., Mains, R. E., Quon, A. S. W., and Eipper, B. A. (1997) Peptidylglycine α-hydroxylating monooxygenase: Active site residues, disulfide linkages, and a two-domain model of the catalytuc core Biochemistry 36, 10901-10909 (Pubitemid 27396245)
23. Blackburn, N. J., Rhames, F. C., Ralle, M., and Jaron, S. (2000) Major changes in copper coordination accompany reduction of peptidylglycine monooxygenase J. Biol. Inorg. Chem. 5, 341-353
24. Bauman, A. T., Jaron, S., Yukl, E. T., Burchfiel, J. R., and Blackburn, N. (2006) pH dependence of peptidylglycine monooxygenase. Mechanistic implications for Cu-methionine binding dynamics Biochemistry 45, 11140-11150 (Pubitemid 44413661)
25. Jaron, S. and Blackburn, N. J. (1999) Does superoxide channel between the copper centers in peptidylglycine monooxygenase? A new mechanism based on carbon monoxide reactivity Biochemistry 38, 15086-15096 (Pubitemid 129520339)
26. Bauman, A. T., Ralle, M., and Blackburn, N. (2007) Large scale production of the copper enzyme peptidylglycine monooxygenase using an automated bioreactor Protein Expression Purif. 51, 34-38 (Pubitemid 44821861)
27. George, G. N. (1990) EXAFSPAK; Stanford Synchrotron Radiation Laboratory, Menlo Park, CA.
28. Binsted, N., Gurman, S. J., and Campbell, J. W. (1998) EXCURV9.2; Daresbury Laboratory, Warrington, England.
29. 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
30. 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
31. Binsted, N. and Hasnain, S. S. (1996) State of the art analysis of whole X-ray absorption spectra J. Synchrotron Radiat. 3, 185-196
32. Loftin, I. R., Franke, S., Blackburn, N. J., and McEvoy, M. M. (2007) Unusual Cu(I)/Ag(I) coordination of Escherichia coli CusF as revealed by atomic resolution crystallography and X-ray absorption spectroscopy Protein Sci. 16, 2287-2293 (Pubitemid 47481664)
33. Loftin, I. R., Blackburn, N. J., and McEvoy, M. M. (2009) Tryptophan Cu(I)-π interaction fine-tunes the metal binding properties of the bacterial metallochaperone CusF J. Biol. Inorg. Chem. 14, 905-912
34. Bagai, I., Liu, W., Rensing, C., Blackburn, N. J., and McEvoy, M. M. (2007) Substrate-linked conformational change in the periplasmic component of a Cu(I)/Ag(I) efflux system J. Biol. Chem. 282, 35695-35702 (Pubitemid 350277135)
35. Sarret, G., Favier, A., Coves, J., Hazemann, J. L., Mergeay, M., and Bersch, B. (2010) CopK from Cupriavidus metallidurans CH34 binds Cu(I) in a tetrathioether site: Characterization by X-ray absorption and NMR spectroscopy J. Am. Chem. Soc. 132, 3770-3777
36. Rubino, J. T., Riggs-Gelasco, P., and Franz, K. J. (2010) Methionine motifs of copper transport proteins provide general and flexible thioether-only binding sites for Cu(I) and Ag(I) J. Biol. Inorg. Chem. 15, 1033-1049
37. Wu, M. M., Grabe, M., Adams, S., Tsien, R. Y., Moore, H. P., and Machen, T. E. (2001) Mechanisms of pH regulation in the regulated secretory pathway J. Biol. Chem. 276, 33027-33035
38. Diliberto, E. J., Jr. and Allen, P. L. (1981) Mechanism of dopamine β-hydroxylation. Semidehydroascorbate as the enzyme oxidation product of ascorbate J. Biol. Chem. 256, 3385-3393 (Pubitemid 11076999)
39. Xin, X., Mains, R. E., and Eipper, B. A. (2004) Monooxygenase X, a member of the copper-dependent monooxygenase family localized to the endoplasmic reticulum J. Biol. Chem. 279, 48159-48167 (Pubitemid 39540971)
40. Guss, J. M., Harrowell, P. R., Murata, M., Norris, V. A., and Freeman, H. C. (1986) Crystal structure analyses of reduced (CuI) poplar plastocyanin at six pH values J. Mol. Biol. 192, 361-387
41. Li, C., Sato, K., Monari, S., Salard, I., Sola, M., Banfield, M. J., and Dennison, C. (2011) Metal-binding loop length is a determinant of the pKa of a histidine ligand at a type 1 copper site Inorg. Chem. 50, 482-488
42. Bertini, I., Luchinat, C., and Monnanni, R. (1985) Evidence of the breaking of the copper-imidazolate bridge in copper/cobalt-substituted superoxide dismutase upon reduction of the Cu(II) centers J. Am. Chem. Soc. 107, 2178-2179
43. Blackburn, N. J., Hasnain, S. S., Binsted, N., Diakun, G. P., Garner, C. D., and Knowles, P. F. (1984) An extended-X-ray-absorption-fine-structure study of bovine erythrocyte superoxide dismutase in aqueous solution. Direct evidence for three-coordinate Cu(I) in the reduced enzyme Biochem. J. 219, 985-990
44. Banci, L., Bertini, I., Cramaro, F., Del Conte, R., and Viezzoli, M. S. (2002) The solution structure of reduced dimeric copper zinc superoxide dismutase. The structural effects of dimerization Eur. J. Biochem. 269, 1905-1915 (Pubitemid 34429672)
45. Li, C., Banfield, M. J., and Dennison, C. (2007) Engineering copper sites in proteins: Loops confer native structures and properties to chimeric cupredoxins J. Am. Chem. Soc. 129, 709-718 (Pubitemid 46147772)