The binding and release of oxygen and hydrogen peroxide are directed by a hydrophobic tunnel in cholesterol oxidase

Biochemistry

Volumn 47, Issue 19, 2008, Pages 5368-5377

  Chen, Lin ^a   Lyubimov, Artem Y ^b   Brammer, Leighanne ^b   Vrielink, Alice ^b,c   Sampson, Nicole S ^a  

^a STONY BROOK UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CATALYST ACTIVITY; CHOLESTEROL; CRYSTAL STRUCTURE; HYDROGEN PEROXIDE; MOLECULAR OXYGEN;

CATALYTIC EFFICIENCY; GASEOUS SUBSTRATES; PUTATIVE GATES; REDOX ENZYME CHOLESTEROL OXIDASE;

ENZYMES;

CHOLESTEROL OXIDASE; HYDROGEN PEROXIDE; INDOLE; OXYGEN; QUERCETIN; STEROID; STEROL; TRYPTOPHAN;

ARTICLE; CATALYSIS; CHANNEL GATING; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; GENE CONSTRUCT; GENE MUTATION; HYDROPHOBICITY; OXIDATION; OXYGEN SATURATION; PRIORITY JOURNAL; STEADY STATE; WILD TYPE;

BINDING SITES; CHOLESTEROL OXIDASE; CRYSTALLOGRAPHY, X-RAY; HYDROGEN PEROXIDE; HYDROPHOBICITY; ISOENZYMES; KINETICS; MODELS, MOLECULAR; MUTATION; OXYGEN; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY;

EID: 43249129470     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi800228w     Document Type: Article

References (50)

1. Tilton, R. F., Jr., Kuntz, 1. D., Jr., and Petsko, G. A. (1984) Cavities in proteins: Structure of a metmyoglobin-xenon complex solved to 1.9 Å. Biochemistry 23, 2849-2857.
2. Whittington, D. A., Rosenzweig, A. C., Frederick, C. A., and Lippard, S. J. (2001) Xenon and halogenated alkanes track putative substrate binding cavities in the soluble methane monooxygenase hydroxylase. Biochemistry 40, 3476-3482.
3. Duff, A. P., Trambaiolo, D. M., Cohen, A. E., Ellis, P. J., Juda, G. A., Shepard, E. M., Langley, D. B., Dooley, D. M., Freeman, H. C., and Guss, J. M. (2004) Using xenon as a probe for dioxygen-binding sites in copper amine oxidases. J. Mol. Biol. 344, 599-607.
4. de Sanctis, D., Dewilde, S., Pesce, A., Moens, L., Ascenzi, P., Hankeln, T., Burmester, T., and Bolognesi, M. (2004) Mapping protein matrix cavities in human cytoglobin through Xe atom binding. Biochem. Biophys. Res. Commun. 316, 1217-1221.
5. Raushel, F. M., Thoden, J. B., and Holden, H. M. (2003) Enzymes with molecular tunnels. Acc. Chem. Res. 36, 539-548.
6. Hyde, C. C., Ahmed, S. A., Padlan, E. A., Miles, E. W., and Davies, D. R. (1988) Three-dimensional structure of the tryptophan synthase α2β2 multienzyme complex from Salmonella typhimurium. J. Biol. Chem. 263, 17857-17871.
7. Huang, X., and Raushel, F. M. (2000) Restricted passage of reaction intermediates through the ammonia tunnel of carbamoyl phosphate synthetase. J. Biol. Chem. 275, 26233-26240.
8. Raushel, F. M., Thoden, J. B., and Holden, H. M. (1999) The amidotransferase family of enzymes: Molecular machines for the production and delivery of ammonia. Biochemistry 38, 7891-7899.
9. Fan, Y., Lund, L., Yang, L., Raushel, F. M., and Gao, Y.-Q. (2008) Mechanism for the transport of ammonia within carbamoyl phosphate synthetase determined by molecular dynamics simulations. Biochemistry 47, 2935-2944.
10. Manjasetty, B. A., Powlowski, J., and Vrielink, A. (2003) Crystal structure of a bifunctional aldolase-dehydrogenase: Sequestering a reactive and volatile intermediate. Proc. Natl. Acad. Sci. U.S.A. 100, 6992-6997.
11. 2 tunnel gating mechanism in the bifunctional carbon monoxide dehydrogenase/acetyl coenzyme A synthase from Moorella thermoacetica. J. Biol. Inorg. Chem. 9, 525-532.
12. Tan, X., Volbeda, A., Fontecilla-Camps, J. C., and Lindahl, P. A. (2006) Function of the tunnel in acetylcoenzyme A synthase/carbon monoxide dehydrogenase. J. Biol. Inorg. Chem. 11, 371-378.
13. Knapp, M. J., and Klinman, J. P. (2003) Kinetic studies of oxygen reactivity in soybean lipoxygenase-1. Biochemistry 42, 11466-11475.
14. Knapp, M. J., Seebeck, F. P., and Klinman, J. P. (2001) Steric control of oxygenation regiochemistry in soybean lipoxygenase-1. J. Am. Chem. Soc. 123, 2931-2932.
15. Saam, J., Ivanov, I., Walther, M., Holzhutter, H. G., and Kuhn, H. (2007) Molecular dioxygen enters the active site of 12/15-lipoxygenase via dynamic oxygen access channels. Proc. Natl. Acad. Sci. U.S.A. 104, 13319-13324.
16. Furse, K. E., Pratt, D. A., Schneider, C., Brash, A. R., Porter, N. A., and Lybrand, T. P. (2006) Molecular dynamics simulations of arachidonic acid-derived pentadienyl radical intermediate complexes with COX-I and COX-2: Insights into oxygenation regio-and stereoselectivity. Biochemistry 45, 3206-3218.
17. Mukherjee, A., Brinkley, D. W., Chang, K. M., and Roth, J. P. (2007) Molecular oxygen dependent steps in fatty acid oxidation by cyclooxygenase-1. Biochemistry 46, 3975-3989.
18. Johnson, B. J., Cohen, J., Welford, R. W., Pearson, A. R., Schulten, K., Klinman, J. P., and Wilmot, C. M. (2007) Exploring molecular oxygen pathways in Hansenula polymorpha copper-containing amine oxidase. J. Biol. Chem. 282, 17767-17776.
19. Wilce, M. C. J., Dooley, D. M., Freeman, H. C., Guss, J. M., Matsunami, H., McIntire, W. S., Ruggiero, C. E., Tanizawa, K., and Yamaguchi, H. (1997) Crystal structures of the copper-containing amine oxidase from Arthrobacter globiformis in the nolo and apo forms: Implications for the biogenesis of topaquinone. Biochemistry 36, 16116-16133.
20. Mims, M. P., Porras, A. G., Olson, J. S., Noble, R. W., and Peterson, J. A. (1983) Ligand binding to heme proteins. An evaluation of distal effects. J. Biol. Chem. 258, 14219-14232.
21. Ostermann, A., Waschipky, R., Parak, F. G., and Nienhaus, G. U. (2000) Ligand binding and conformational motions in myoglobin. Nature 404, 205-208.
22. Schmidt, M., Nienhaus, K., Pahl, R., Krasselt, A., Anderson, S., Parak, F., Nienhaus, G. U., and Srajer, V. (2005) Ligand migration pathway and protein dynamics in myoglobin: A time-resolved crystallographic study on L29W MbCO. Proc. Natl. Acad. Sci. U.S.A. 102, 11704-11709.
23. Scott, E. E., and Gibson, Q. H. (1997) Ligand migration in sperm whale myoglobin. Biochemistry 36, 11909-11917.
24. Hiromoto, T., Fujiwara, S., Hosokawa, K., and Yamaguchi, H. (2006) Crystal structure of 3-hydroxybenzoate hydroxylase from Comamonas testosteroni has a large tunnel for substrate and oxygen access to the active site. J. Mol. Biol. 364, 878-896.
25. Moustafa, I. M., Foster, S., Lyubimov, A. Y., and Vrielink, A. (2006) Crystal structure of LAAO from Calloselasma rhodostoma with an L-phenylalanine substrate: Insights into structure and mechanism. J. Mol. Biol. 364, 991-1002.
26. Coulombe, R., Yue, K. Q., Ghisla, S., and Vrielink, A. (2001) Oxygen access to the active site of cholesterol oxidase through a narrow channel is gated by an Arg-Glu pair. J. Biol. Chem. 276, 30435-30441.
27. Montet, Y., Amara, P., Volbeda, A., Vernede, X., Hatchikian, E. C., Field, M. J., Frey, M., and Fontecilla-Camps, J. C (1997) Gas access to the active site of Ni-Fe hydrogenases probed by X-ray crystal-lography and molecular dynamics. Nat. Struct. Biol. 4, 523-526.
28. Lario, P., Sampson, N. S., and Vrielink, A. (2003) Sub-atomic resolution crystal structure of cholesterol oxidase: What atomic resolution crystallography reveals about enzyme mechanism and the role of the FAD cofactor in redox activity. J. Mol. Biol. 326, 1635-1650.
29. Sampson, N. S., and Kass, I. J. (1997) Isomerization, but not oxidation, is suppressed by a single point mutation, E361Q, in the reaction catalyzed by cholesterol oxidase. J. Am. Chem. Soc. 119, 855-862.
30. Ye, Y., Lario, P., Vrielink, A., and Sampson, N. S. (2001) The presence of a hydrogen bond betwen asparagine 485 and the π system of FAD modulates the redox potential in the reaction catalyzed by cholesterol oxidase. Biochemistry 40, 13779-13787.
31. Kass, I. J., and Sampson, N. S. (1998) The importance of Glu 361 position in the reaction catalyzed by cholesterol oxidase. Bioorg. Med. Chem. Lett. 8, 2663-2668.
32. Stankovich, M. T. (1980) An anaerobic spectroelectrochemical cell for studying the spectral and redox properties of flavoproteins. Anal. Biochem. 109, 295-308.
33. Stankovich, M. (2002) Potentiometrie Measurements of Proteins, Bioelectrochemistry (Wilson, G. S., Ed.) pp 487-509, Wiley-VCH, Weinheim, Germany.
34. Lyubimov, A. Y., Lario, P. I., Moustafa, I., and Vrielink, A. (2006) Atomic resolution crystallography reveals how changes in pH shape the protein microenvironment. Nat. Chem. Biol. 2, 259-264.
35. Pflugrath, J. W. (1999) The finer things in X-ray diffraction data collectionnera Crystallogr. D55, 1718-1725.
36. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D53, 240-255.
37. Emsley, P., and Cowtan, K. (2004) Coot: Model-building tools for molecular graphics. Acta Crystallogr. D60, 2126-2132.
38. Sheldrick, G. M., and Schneider, T. R. (1997) SHELXL: High-resolution refinement, Methods in Enzymology (Carter, C. W. J., and Sweet, R. M., Eds.) pp 319-343, Academic Press, Boston.
39. Vaguine, A. A., Richelle, J., and Wodak, S. J. (1999) SFCHECK: A unified set of procedures for evaluating the quality of macro-molecular structure-factor data and their agreement with the atomic model. Acta Crystallogr. D55, 191-205.
40. Project, C. C. (1994) The CCP4 suite: Programs for protein crystallography. Acta Crystallogr. D50, 760-763.
41. DeLano, W. L. (2006) The PyMOL Molecular Graphics System, DeLano Scientific, San Carlos, CA.
42. Chen, L. (2007) The binding and release of oxygen and hydrogen peroxide are directed through a hydrophobic tunnel in cholesterol oxidase. Ph.D. Thesis, Department of Chemistry, Stony Brook University, Stony Brook, NY.
43. Lyubimov, A. (2006) A structural study of cholesterol oxidase at atomic and subatomic resoultion. Ph.D. Thesis, Department of Chemistry, University of California, Santa Cruz, CA.
44. Cornish-Bowden, A., and Cardenas, M. L. (1987) Co-operativity in monomelic enzymes. J. Theor. Biol. 124, 1-23.
45. Ricard, J., and Cornish-Bowden, A. (1987) Co-operative and allosteric enzymes: 20 years on. Eur. J. Biochem. 166, 255-272.
46. Pettersson, G. (1986) Mechanistic origin of the sigmoidal rate behaviour of glucokinase. Biochem. J. 233, 347-350.
47. Pettersson, G. (1986) Mechanistic origin of the kinetic cooperativity of hexokinase type Ll from wheat germ. Eur. J. Biochem. 154, 167-170.
48. Umhau, S., Pollegioni, L., Molla, G., Diederichs, K., Weite, W., Pilone, M. S., and Ghisla, S. (2000) The X-ray structure of D-amino acid oxidase at very high resolution identifies the chemical mechanism of flavin-dependent substrate dehydrogenation. Proc. Natl. Acad. Sci. U.S.A. 97, 12463-12468.
49. Weeks, A., Lund, L., and Raushel, F. M. (2006) Tunneling of intermediates in enzyme-catalyzed reactions. Curr. Opin. Chem. Biol. 10, 465-472.
50. Quaye, O., Lountos, G. T., Fan, F., Orville, A. M., and Gadda, G. (2008) Role of Glu312 in binding and positioning of the substrate for the hydride transfer reaction in choline oxidase. Biochemistry 47, 243-256.