Methane monooxygenase hydroxylase and B component interactions

Biochemistry

Volumn 45, Issue 9, 2006, Pages 2913-2926

  Zhang, Jingyan ^a   Wallar, Bradley J ^a,b   Popescu, Codrina V ^a,c   Renner, Daniel B ^a   Thomas, David D ^a   Lipscomb, John D ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

^b GRAND VALLEY STATE UNIVERSITY   (United States)

^c URSINUS COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMICAL REACTIONS; CONFORMATIONS; MUTAGENESIS; ORGANIC COMPOUNDS; PROBES; SUBSTRATES;

AFFINITY MEASUREMENTS; BINDING SURFACE; CYSTEINE RESIDUES; ELECTROSTATIC INTERACTIONS; FLUORESCENT PROBES; METHANE MONOOXYGENASE HYDROXYLASE; MMOB-MMOH BINDING; SITE-BEARING HYDROXYLASE COMPONENT; SPIN LABELS;

SOLUTIONS;

4 MALEIMIDO 2,2,6,6 TETRAMETHYL 1 PIPERIDINYLOXY; 5 [[[(2 IODOACETYL)AMINO]ETHYL]AMINO]NAPHTHALENE 1 SULFONIC ACID; 6 BROMOACETYL 2 DIMETHYLAMINONAPHTHALENE; CYSTEINE; FLUORESCENT DYE; METHANE MONOOXYGENASE; METHANE MONOOXYGENASE HYDROXYLASE; METHANE MONOOXYGENASE REGULATORY COMPONENT; NAPHTHALENE DERIVATIVE; PIPERIDINE DERIVATIVE; SULFONIC ACID DERIVATIVE; UNCLASSIFIED DRUG;

ANISOTROPY; ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CATALYSIS; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ELECTRON SPIN RESONANCE; ENZYME SUBSTRATE; HYDROPHILICITY; IONIC STRENGTH; KINETICS; METHYLOSINUS TRICHOSPORIUM; MOLECULAR STABILITY; NONHUMAN; PH MEASUREMENT; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN METABOLISM; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REACTION ANALYSIS; REDUCTION; SITE DIRECTED MUTAGENESIS; SPIN LABELING; STRUCTURE ANALYSIS; TECHNIQUE; THERMODYNAMICS;

2-NAPHTHYLAMINE; BINDING SITES; CATALYSIS; CIRCULAR DICHROISM; CYSTEINE; FLUORESCENCE POLARIZATION; KINETICS; MAGNETIC RESONANCE SPECTROSCOPY; METHYLOSINUS TRICHOSPORIUM; MULTIENZYME COMPLEXES; MUTAGENESIS, SITE-DIRECTED; OXYGENASES; PROTEIN ISOFORMS; PROTEIN STRUCTURE, TERTIARY; SUBSTRATE SPECIFICITY; TIME FACTORS;

METHYLOSINUS TRICHOSPORIUM;

EID: 33644690580     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi052256t     Document Type: Article

References (53)

1. Dalton, H. (1980) Oxidation of hydrocarbons by methane monooxygenase from a variety of microbes, Adv. Appl. Microbiol. 26, 71-87.
2. Woodland, M. P., and Dalton, H. (1984) Purification and characterization of component A of the methane monooxygenase from Methylococcus capsulatus (Bath), J. Biol. Chem. 259, 53-59.
3. Green, J., and Dalton, H. (1985) Protein B of soluble methane monooxygenase from Methylococcus capsulatus (Bath). A novel regulatory protein of enzyme activity, J, Biol, Chem. 260, 15795-15801.
4. Fox, B. G., Froland, W. A., Dege, J. E., and Lipscomb, J. D. (1989) Methane monooxygenase from Methylosinus trichosporium OB3b. Purification and properties of a three-component system with high specific activity from a type II methanotroph, J. Biol. Chem. 264, 10023-10033.
5. Wallar, B. J., and Lipscomb, J. D. (1996) Dioxygen activation by enzymes containing binuclear non-heme iron clusters, Chem. Rev. 96, 2625-2657.
6. Feig, A. L., and Lippard, S. J. (1994) Reactions of non-heme iron-(II) centers with dioxygen in biology and chemistry, Chem. Rev. 94, 759-805.
7. Merkx, M., Kopp, D. A., Sazinsky, M. H., Blazyk, J. L., Muller, J., and Lippard, S. J. (2001) Dioxygen activation and methane hydroxylation by soluble methane monooxygenase: a tale of two irons and three proteins, Angew. Chem., Int. Ed. 40, 2782-2807.
8. Brazeau, B. J., and Lipscomb, J. D. (2000) Electron transfer and radical forming reactions of methane monooxygenase, Subcell. Biochem. 35, 233-277.
9. Lee, S.-K., Nesheim, J. C., and Lipscomb, J. D. (1993) Transient intermediates of the methane monooxygenase catalytic cycle, J. Biol. Chem. 268, 21569-21577.
10. Rosenzweig, A. C., Frederick, C. A., Lippard, S. J., and Nordlund, P. (1993) Crystal structure of a bacterial non-haem iron hydroxylase that catalyses the biological oxidation of methane, Nature 366, 537-543.
11. Elango, N., Radhakrishnan, R., Froland, W. A., Wallar, B. I, Earhart, C. A;., Lipscomb, J. D., and Ohlendorf, D. H. (1997) Crystal structure of the hydroxylase component of methane monooxygenase from Methylosinus trichosporium OB3b, Protein Sci. 6, 556-568.
12. Lindqvist, Y., Huang, W. J., Schneider, G., and Shanklin, J. (1996) Crystal structure of delta(9) stearoyl-acyl carrier protein desaturase from castor seed and its relationship to other diiron proteins, EMBO J. 15, 4081-4092.
13. Sazinsky, M. H., Bard, J., Di Donate, A., and Lippard, S. J. (2004) Crystal structure of the toluene/o-xylene monooxygenase hydroxylase from Pseudomonas stutzen OX1. Insight into the substrate specificity, substrate channeling, and active site tuning of multicomponent monooxygenases, J. Biol. Chem. 279, 30600-30610.
14. Dyer, D. H., Lyle, K. S., Rayment, I., and Fox, B. G. (2005) X-ray structure of putative acyl-ACP desaturase DesA2 from Mycobacterium tuberculosis H37Rv, Protein Sci. 14, 1508-1517.
15. Froland, W. A., Andersson, K. K., Lee, S.-K., Liu, Y., and Lipscomb, J. D. (1992) Methane monooxygenase component B and reductase alter the regioselectivity of the hydroxylase component-catalyzed reactions. A novel role for protein-protein interactions in an oxygenase mechanism, J. Biol. Chem. 267, 17588-17597.
16. Fox, B. G., Liu, Y., Dege, J. E., and Lipscomb, J. D. (1991) Complex formation between the protein components of methane monooxygenase from Methylosinus trichosporium OB3b. Identification of sites of component interaction, J. Biol. Chem. 266, 540-550.
17. Davydov, A., Davydov, R., Gräslund, A., Lipscomb, J. D., and Andersson, K. K. (1997) Radiolytic reduction of methane monooxygenase dinuclear iron cluster at 77 K-EPR evidence for conformational change upon reduction or binding of component B to the diferric state, J. Biol. Chem. 272, 7022-7026.
18. Pulver, S. C., Froland, W. A., Lipscomb, J. D., and Solomon, E. I. (1997) Ligand field circular dichroism and magnetic circular dichroism studies of component B and substrate binding to the hydroxylase component of methane monooxygenase, J. Am. Chem. Soc. 119, 387-395.
19. IV cluster, J. Am. Chem. Soc. 115, 6450-6451.
20. Liu, K. E., Valentine, A. M., Wang, D. L., Huynh, B. H., Edmondson, D. E., Salifoglou, A., and Lippard, S. J. (1995) Kinetic and spectroscopic characterization of intermediates and component interactions in reactions of methane monooxygenase from Methylococcus capsulatus (Bath), J. Am. Chem. Soc. 117, 10174-10185.
21. Brazeau, B. J., and Lipscomb, J. D. (2000) Kinetics and activation thermodynamics of methane monooxygenase compound Q formation and reaction with substrates, Biochemistry 39, 13503-13515.
22. Chang, S. L., Wallar, B. J., Lipscomb, J. D., and Mayo, K. H. (1999) Solution structure of component B from methane monooxygenase derived through heteronuclear NMR and molecular modeling, Biochemistry 38, 5799-5812.
23. Chang, S. L., Wallar, B. J., Lipscomb, J. D., and Mayo, K. H. (2001) Residues in Methylosinus trichosporium OB3b methane monooxygenase component B involved in molecular interactions with reduced- and oxidized-hydroxylase component: a role for the N-terminus, Biochemistry 40, 9539-9551.
24. Walters, K. J., Gassner, G. T., Lippard, S. J., and Wagner, G. (1999) Structure of the soluble methane monooxygenase regulatory protein B, Proc. Natl. Acad. Sci. U.S.A. 96, 7877-7882.
25. Wallar, B. J., and Lipscomb, J. D. (2001) Methane monooxygenase component B mutants alter the kinetics of steps throughout the catalytic cycle, Biochemistry 40, 2220-2233.
26. Nesheim, J. C., and Lipscomb, J. D. (1996) Large isotope effects in methane oxidation catalyzed by methane monooxygenase: evidence for C-H bond cleavage in a reaction cycle intermediate, Biochemistry 35, 10240-10247.
27. Brazeau, B. J., Wallar, B. J., and Lipscomb, J. D. (2001) Unmasking of deuterium kinetic isotope effects on the methane monooxygenase compound Q reaction by site-directed mutagenesis of component B, J. Am. Chem. Soc. 123, 10421-10422.
28. MacArthur, R., Sazinsky, M. H., Kuehne, H., Whittington, D. A., Lippard, S. J., and Brudvig, G. W. (2002) Component B binding to the soluble methane monooxygenase hydroxylase by saturation-recovery EPR spectroscopy of spin-labeled MMOB, J. Am. Chem. Soc. 124, 13392-13393.
29. cam and methane monooxygenase: lessons in tuning nature's powerful reagents, Biochem. Biophys. Res. Commun. 312, 143-148.
30. Hubbell, W. L., Cafiso, D. S., and Altenbach, C. (2000) Identifying conformational changes with site-directed spin labeling, Nat. Struct. Biol. 7, 735-739.
31. Altenbach, C., Froncisz, W., Hemker, R., Hassane, M., and Hubbell, W. L. (2005) Accessibility of nitroxide side chains: Absolute Heisenberg exchange rates from power saturation EPR, Biophys. J. 89, 2103-2112.
32. Fox, B. G., Froland, W. A., Jollie, D. R., and Lipscomb, J. D. (1990) Methane monooxygenase from Methylosinus trichosporium OB3b, Methods Enzymol. 188, 191-202.
33. Oh, K. J., Altenbach, C., Collier, R. J., and Hubbell, W. L. (2000) Site directed spin labeling of proteins. Applications to diphtheria toxin, Methods Mol Biol. 145, 147-169.
34. Altenbach, C., Greenhalgh, D. A., Khorana, H. G., and Hubbell, W. L. (1994) A collision gradient method to determine the immersion depth of nitroxides in lipid bilayers: application to spin-labeled mutants of bacteriorhodopsin, Proc. Natl. Acad. Sci. U.S.A. 91, 1667-1671.
35. Kirby, T. L., Karim, C. B., and Thomas, D. D. (2004) Electron paramagnetic resonance reveals a large-scale conformational change in the cytoplasmic domain of phospholamban upon binding to the sarcoplasmic reticulum Ca-ATPase, Biochemistry 43, 5842-5852.
36. Nelson, W. D., Blakely, S. E., Nesmelov, Y. E., and Thomas, D. D. (2005) Site-directed spin labeling reveals a conformational switch in the phosphorylation domain of smooth muscle myosin, Proc. Natl. Acad. Sci. U.S.A. 102, 4000-4005.
37. Columbus, L., and Hubbell, W. L. (2004) Mapping backbone dynamics in solution with site-directed spin labeling: GCN4-58 bZip free and bound to DNA, Biochemistry 43, 7273-7287.
38. Lakowicz, J. R. (1999) Fluorescence anisotropy, in Principles of Fluorescence Spectroscopy (Lakowicz, J. R., Ed.) pp 291-320, Kluwer Academic/Plenum Publishers, New York.
39. Brazeau, B. J., and Lipscomb, J. D. (2003) Key amino acid residues in the regulation of soluble methane monooxygenase catalysis by component B, Biochemistry 42, 5618-5631.
40. Liu, Y., Nesheim, J. C., Lee, S.-K., and Lipscomb, J. D. (1995) Gating effects of component B on oxygen activation by the methane monooxygenase hydroxylase component, J. Biol. Chem. 270, 24662-24665.
41. Hiratsuka, T. (1999) ATP-induced opposite changes in the local environments around Cys697 (SH2) and Cys707 (SH1) of the myosin motor domain revealed by the PRODAN fluorescence, J. Biol. Chem. 274, 29156-29163.
42. Owenius, R., Österlund, M., Lindgren, M., Svensson, M., Olsen, O., Persson, E., Freskgard, P.-O., and Carllson, U. (2000) Properties of spin and fluorescent labels at a receptor-ligand interface, Biophys. J. 77, 2237-2250.
43. Mendelson, R. A., Morales, M. F., and Bolts, J. (1973) Segmental flexibility of the S-I moiety of myosin, Biochemistry 12, 2250-2255.
44. Osada, H., Nakanishi, M., Tsuboi, M., Kinosita, K., Jr., and Ikegami, A. (1984) Rotational dynamics of immunoglobulins with fluorescent haptens on a membrane surface, Biochim. Biophys. Acta 773, 321-324.
45. Callaghan, A. J., Smith, T. J., Slade, S. E., and Dalton, H. (2002) Residues near the N-terminus of protein B control autocatalytic proteolysis and the activity of soluble methane monooxygenase, Eur. J. Biochem. 269, 1835-1843.
46. Zhang, J., and Lipscomb, J., D. (2006) Role of the C-terminal region of the B component of Methylosinus trichosporium OB3b methane monooxygenase in the regulation of oxygen activation, Biochemistry (in press).
47. Gassner, G. T., and Lippard, S. J. (1999) Component interactions in the soluble methane monooxygenase system from Methylococcus capsulatus (Bath), Biochemistry 38, 12768-12785.
48. Paulsen, K. E., Liu, Y., Fox, B. G., Lipscomb, J. D., Münck, E., and Stankovich, M. T. (1994) Oxidation-reduction potentials of the methane monooxygenase hydroxylase component from Methylosinus trichosporium OB3b, Biochemistry 33, 713-722.
49. Brandstetter, H., Whittington, D. A., Lippard, S. J., and Frederick, C. A. (1999) Mutational and structural analyses of the regulatory protein B of soluble methane monooxygenase from Methylococcus capsulatus (Bath), Chem. Biol. 6, 441-449.
50. Balendra, S., Lesieur, C., Smith, T. J., and Dalton, H. (2002) Positively charged amino acids are essential for electron transfer and protein-protein interactions in the soluble methane monooxygenase complex from Methylococcus capsulatus (Bath), Biochemistry 47, 2571-2579.
51. cam electron-transfer complex, Biochemistry 28, 8201-8205.
52. cam binding surface as defined by site-directed mutagenesis and electrostatic modeling, Biochemistry 29, 7381-7386.
53. Hendrich, M. P., Münck, E., Fox, B. G., and Lipscomb, J. D. (1990) Integer-spin EPR studies of the fully reduced methane monooxygenase hydroxylase component, J. Am. Chem. Soc. 112, 5861-5865.