The cluster of hydrophobic residues controls the entrance to the active site of choline oxidase

Biochemistry

Volumn 48, Issue 40, 2009, Pages 9599-9605

  Xin, Yao ^a   Gadda, Giovanni ^a   Hamelberg, Donald ^a  

^a GEORGIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE; BROWNIAN DYNAMICS SIMULATIONS; CATALYTIC PROCESS; CHOLINE OXIDASE; ELECTROSTATIC POTENTIALS; GATING MECHANISMS; HYDROPHOBIC RESIDUES; RATE OF COLLISION; RATE-LIMITING STEPS; SOLVENT-ACCESSIBLE SURFACES; X RAY CRYSTAL STRUCTURES;

BROWNIAN MOVEMENT; HYDROPHOBICITY; MOLECULAR DYNAMICS; VEHICULAR TUNNELS;

ENZYMES;

CHOLINE OXIDASE;

ARTICLE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME MECHANISM; HYDROPHOBICITY; MOLECULAR DYNAMICS; PRIORITY JOURNAL; STRUCTURE ANALYSIS;

ALCOHOL OXIDOREDUCTASES; AMINO ACIDS; CATALYSIS; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; ION CHANNEL GATING; STATIC ELECTRICITY;

EID: 70350050563     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi901295a     Document Type: Article

References (55)

1. Allison, S. A., Northrup, S. H., and McCammon, J. A. (1986) Simulation of biomolecular diffusion and complex formation. Biophys. J. 49, 167-175.
2. McCammon, J. A., and Northrup, S. H. (1981) Gated binding of ligands to proteins. Nature 293, 316-317.
3. Carlson, H. A., Smith, R. D., Khazanov, N. A., Kirchhoff, P. D., Dunbar, J. B., Jr., and Benson, M. L. (2008) Differences between high- and low-affinity complexes of enzymes and nonenzymes. J. Med. Chem. 51, 6432-6441.
4. Murray, L. J., Garcia-Serres, R., McCormick, M. S., Davydov, R., Naik, S. G., Kim, S. H., Hoffman, B. M., Huynh, B. H., and Lippard, S. J. (2007) Dioxygen activation at non-heme diiron centers: Oxidation of a proximal residue in the I100W variant of toluene/o-xylene monooxygenase hydroxylase. Biochemistry 46, 14795-14809. (Pubitemid 350308871)
5. Zhou, H. X., Wlodek, S. T., and McCammon, J. A. (1998) Conformation gating as a mechanism for enzyme specificity. Proc. Natl. Acad. Sci. U.S.A. 95, 9280-9283.
6. Chang, C. E., Shen, T., Trylska, J., Tozzini, V., and Mccammon, J. A. (2006) Gated binding of ligands to HIV-1 protease: Brownian dynamics simulations in a coarse-grained model. Biophys. J. 90, 3880-3885. (Pubitemid 43846106)
7. Hritz, J., Zoldak, G., and Sedlak, E. (2006) Cofactor assisted gating mechanism in the active site of NADH oxidase from Thermus thermophilus. Proteins 64, 465-476. (Pubitemid 43993654)
8. Kato, M., Wynn, R. M., Chuang, J. L., Brautigam, C. A., Custorio, M., and Chuang, D. T. (2006) A synchronized substrate-gating mechanism revealed by cubic-core structure of the bovine branched-chain α-ketoacid dehydrogenase complex. EMBO J. 25, 5983-5994. (Pubitemid 44967779)
9. Murray, L. J., and Lippard, S. J. (2007) Substrate trafficking and dioxygen activation in bacterial multicomponent monooxygenases. Acc. Chem. Res. 40, 466-474.
10. Shen, T. Y., Tai, K., and McCammon, J. A. (2001) Statistical analysis of the fractal gating motions of the enzyme acetylcholinesterase. Phys. Rev. E 63, 041902.
11. Xu, Y., Shen, J., Luo, X., Silman, I., Sussman, J., Chen, K., and Jiang, H. (2003) How does Huperzine A Enter and Leave the Binding Gorge of Acetylcholinesterase? Steered Molecular Dynamics Simulations. J. Am. Chem. Soc. 125, 11340-11349.
12. Niu, C., Xu, Y., Xu, Y., Luo, X., Duan, W., Silman, I., Sussman, J., Zhu, W., Chen, K., Shen, J., and Jiang, H. (2005) Dynamic Mechanism of E2020 Binding to Acetylcholinesterase: A Steered Molecular Dynamics Simulation. J. Phys. Chem. B 109, 23730-23738.
13. Hornak, V., Okur, A., Rizzo, R. C., and Simmerling, C. (2006) HIV-1 protease flaps spontaneously close to the correct structure in simulations following manual placement of an inhibitor into the open state. J. Am. Chem. Soc. 128, 2812-2813.
14. Galiano, L., Ding, F., Veloro, A. M., Blackburn, M. E., Simmerling, C., and Fanucci, G. E. (2009) Drug pressure selected mutations in HIV-1 protease alter flap conformations. J. Am. Chem. Soc. 131, 430-431.
15. Liu, F., Kovalevsky, A. Y., Louis, J. M., Boross, P. I., Wang, Y. F., Harrison, R. W., and Weber, I. T. (2006) Mechanism of drug resistance revealed by the crystal structure of the unliganded HIV-1 protease with F53L mutation. J. Mol. Biol. 358, 1191-1199.
16. Hamelberg, D., and McCammon, J. A. (2005) Fast peptidyl cis-trans isomerization within the flexible Gly-rich flaps of HIV-1 protease. J. Am. Chem. Soc. 127, 13778-13779.
17. Ishima, R., Wingfield, P. T., Stahl, S. J., Kaufman, J. D., and Torchia, D. A. (1998) Using amide H-1 and N-15 transverse relaxation to detect millisecond time-scale motions in perdeuterated proteins: Application to HIV-1 protease. J. Am. Chem. Soc. 120, 10534-10542.
18. Torbeev, V. Y., Raghuraman, H., Mandal, K., Senapati, S., Perozo, E., and Kent, S. B. (2009) Dynamics of "flap" structures in three HIV-1 protease/inhibitor complexes probed by total chemical synthesis and pulse-EPR spectroscopy. J. Am. Chem. Soc. 131, 884-885.
19. Hornak, V., Okur, A., Rizzo, R. C., and Simmerling, C. (2005) HIV-1 protease flaps spontaneously open and reclose in molecular dynamics simulations. Proc. Natl. Acad. Sci. U.S.A. 103, 915-920.
20. Ikuta, S., Imamura, S., Misaki, H., and Horiuti, Y. (1977) Purification and characterization of choline oxidase from Arthrobacter globiformis. J. Biochem. 82, 1741-1749. (Pubitemid 8240336)
21. Fan, F., and Gadda, G. (2005) On the catalytic mechanism of choline oxidase. J. Am. Chem. Soc. 127, 2067-2074.
22. O'Callaghan, J., and Condon, S. (2000) Growth of Lactococcus lactis strains at low water activity: Correlation with the ability to accumulate glycine betaine. Int. J. Food Microbiol. 55, 127-131.
23. 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.
24. Orville, A. M., Lountos, G. T., Finnegan, S., Gadda, G., and Prabhakar, R. (2009) Crystallographic, spectroscopic, and computational analysis of a flavin C4a-oxygen adduct in choline oxidase. Biochemistry 48, 720-728.
25. Gadda, G., Fan, F., and Hoang, J. V. (2006) On the contribution of the positively charged headgroup of choline to substrate binding and catalysis in the reaction catalyzed by choline oxidase. Arch. Biochem. Biophys. 451, 182-187.
26. Ghanem, M., and Gadda, G. (2006) Effects of reversing the protein positive charge in the proximity of the flavin N(1) locus of choline oxidase. Biochemistry 45, 3437-3447. (Pubitemid 43376363)
27. Hecht, H. J., Kalisz, H. M., Hendle, J., Schmid, R. D., and Schomburg, D. (1993) Crystal Structure of Glucose Oxidase from Aspergillus niger Refined at 2.3 Angstrom Resolution. J. Mol. Biol. 229, 153-172.
28. Hallberg, B. M., Leitner, C., Haltrich, D., and Divne, C. (2004) Crystal structure of the 270 kDa homotetrameric lignin-degrading enzyme pyranose 2-oxidase. J. Mol. Biol. 341, 781-796.
29. Bannwarth, M., Bastian, S., Heckmann-Pohl, D., Giffhorn, F., and Schulz, G. E. (2004) Crystal structure of pyranose 2-oxidase from the white-rot fungus Peniophora sp. Biochemistry 43, 11683-11690. (Pubitemid 39277613)
30. Hallberg, B. M., Henriksson, G., Pettersson, G., and Divne, C. (2002) Crystal structure of the flavoprotein domain of the extracellular flavocytochrome cellobiose dehydrogenase. J. Mol. Biol. 315, 421-434.
31. Schwab, F., van Gunsteren, W. F., and Zagrovic, B. (2008) Computational study of the mechanism and the relative free energies of binding of anticholesteremic inhibitors to squalene-hopene cyclase. Biochemistry 47, 2945-2951. (Pubitemid 351328847)
32. Morris, G. M., Goodsell, D. S., Halliday, R. S., Huey, R., Hart, W. E., Belew, R. K., and Olson, A. J. (1998) Automated docking using a Lamarckian genetic algorithm and an empirical binding free energy function. J. Comput. Chem. 19, 1639-1662.
33. Bayly, C. I., Cieplak, P., Cornell, W. D., and Kollman, P. A. (1993) A Well-Behaved Electrostatic Potential Based Method Using Charge Restraints for Deriving Atomic Charges: The Resp Model. J. Phys. Chem. 97, 10269-10280.
34. Cornell, W. D., Cieplak, P., Bayly, C. I., and Kollman, P. A. (1993) Application of Resp Charges to Calculate Conformational Energies, Hydrogen-Bond Energies, and Free-Energies of Solvation. J. Am. Chem. Soc. 115, 9620-9631.
35. Frisch, M. J., Trucks, G. W., Schlegel, H. B., Scuseria, G. E., Robb, M. A., Cheeseman, J. R., Montgomery, J., Jr., Vreven, T., Kudin, K. N., Burant, J. C., Millam, J. M., Iyengar, S. S., Tomasi, J., Barone, V., Mennucci, B., Cossi, M., Scalmani, G., Rega, N., Petersson, G. A., Nakatsuji, H., Hada, M., Ehara, M., Toyota, K., Fukuda, R., Hasegawa, J., Ishida, M., Nakajima, T., Honda, Y., Kitao, O., Nakai, H., Klene, M., Li, X., Knox, J. E., Hratchian, H. P., Cross, J. B., Bakken, V., Adamo, C., Jaramillo, J., Gomperts, R., Stratmann, R. E., Yazyev, O., Austin, A. J., Cammi, R., Pomelli, C., Ochterski, J. W., Ayala, P. Y., Morokuma, K., Voth, G. A., Salvador, P., Dannenberg, J. J., Zakrzewski, V. G., Dapprich, S., Daniels, A. D., Strain, M. C., Farkas, O., Malick, D. K., Rabuck, A. D., Raghavachari, K., Foresman, J. B., Ortiz, J. V., Cui, Q., Baboul, A. G., Clifford, S., Cioslowski, J., Stefanov, B. B., Liu, G., Liashenko, A., Piskorz, P., Komaromi, I., Martin, R. L., Fox, D. J., Keith, T., Al-Laham, M. A., Peng, C. Y., Nanayakkara, A., Challacombe, M., Gill, P. M. W., Johnson, B., Chen, W., Wong, M. W., Gonzalez, C., and Pople, J. A. (2004) Gaussian 03 , revision E.01, Gaussian, Inc., Wallingford, CT.
36. Case, D. A., Cheatham, T. E. III, Darden, T., Gohlke, H., Luo, R., Merz, K. M., Jr., Onufriev, A., Simmerling, C., Wang, B., and Woods, R. J. (2005) The Amber biomolecular simulation programs. J. Comput. Chem. 26, 1668-1688.
37. Case, D. A., Darden, T. A., Cheatham, T. E., III, Simmerling, C. L., Wang, J., Duke, R. E., Luo, R., Crowly, M., Walker, R. C., Zhang, W., Merz, K. M., Wang, B., Hayik, S., Roitberg, A., Seabra, G., Kolossváry, I., Wong, K. F., Pasani, F., Vanicek, J., Wu, X., Brozell, S. R., Steinbrecher, T., Gohlke, H., Yang, L., Tan, C., Mongan, J., Hornak, V., Cui, G., Mathews, D. H., Seetin, M. G., Sagui, C., Babin, V., and Kollman, P. A. (2008) AMBER 10 , University of California, San Fransisco.
38. Hornak, V., Abel, R., Okur, A., Strockbine, B., Roitberg, A., and Simmerling, C. (2006) Comparison of multiple Amber force fields and development of improved protein backbone parameters. Proteins 65, 712-725. (Pubitemid 44583220)
39. Wang, J., Wolf, R. M., Caldwell, J. W., Kollman, P. A., and Case, D. A. (2004) Development and testing of a general amber force field. J. Comput. Chem. 25, 1157-1174.
40. Cerutti, D. S., Duke, R., Freddolino, P. L., Fan, H., and Lybrand, T. P. (2008) Vulnerability in Popular Molecular Dynamics Packages Concerning Langevin and Andersen Dynamics. J. Chem. Theory Comput. 4, 1669-1680.
41. Smart, O. S., Goodfellow, J. M., and Wallace, B. A. (1993) The pore dimensions of gramicidin A. Biophys. J. 65, 2455-2460.
42. Baker, N. A., Sept, D., Joseph, S., Holst, M. J., and McCammon, J. A. (2001) Electrostatics of nanosystems: Application to microtubules and the ribosome. Proc. Natl. Acad. Sci. U.S.A. 98, 10037-10041.
43. Warren, L. (2007) The PyMOL Molecular Graphics System , DeLano Scientific LLC, San Carlos, CA.
44. Humphrey, W., Dalke, A., and Schulten, K. (1996) VMD: Visual molecular dynamics. J. Mol. Graphics 14, 27-38.
45. Gabdoulline, R. R., and Wade, R. C. (1997) Simulation of the diffusional association of barnase and barstar. Biophys. J. 72, 1917-1929.
46. Gabdoulline, R. R., and Wade, R. C. (1998) Brownian dynamics simulation of protein-protein diffusional encounter. Methods 14, 329-341. (Pubitemid 28404535)
47. Gabdoulline, R. R., and Wade, R. C. (1999) On the protein-protein diffusional encounter complex. J. Mol. Recognit. 12, 226-234.
48. Elcock, A. H., Gabdoulline, R. R., Wade, R. C., and McCammon, J. A. (1999) Computer simulation of protein-protein association kinetics: Acetylcholinesterase-fasciculin. J. Mol. Biol. 291, 149-162.
49. Gabdoulline, R. R., and Wade, R. C. (1996) Effective charges for macromolecules in solvent. J. Phys. Chem. 100, 3868-3878.
50. Ghanem, M., and Gadda, G. (2005) On the catalytic role of the conserved active site residue His466 of choline oxidase. Biochemistry 44, 893-904. (Pubitemid 40129649)
51. Rungsrisuriyachai, K., and Gadda, G. (2008) On the role of histidine 351 in the reaction of alcohol oxidation catalyzed by choline oxidase. Biochemistry 47, 6762-6769. (Pubitemid 351898931)
52. Hamelberg, D., Shen, T., and McCammon, J. A. (2005) Relating kinetic rates and local energetic roughness by accelerated molecular-dynamics simulations. J. Chem. Phys. 122, 241103.
53. McCammon, J. A., and Harvey, S. C. (1987) Dynamics of proeins and nucleic acids , University of Cambridge Press, Cambridge, U.K.
54. Zhou, H. X. (1998) Theory of the diffusion-influenced substrate binding rate to a buried and gated active site. J. Chem. Phys. 108, 8146-8154.
55. Gorfe, A. A., Lu, B., Yu, Z., and McCammon, J. A. (2009) Enzymatic Activity versus Structural Dynamics: The Case of Acetylcholinesterase Tetramer. Biophys. J. 97, 897-905.