Discrimination between CO and O2 in heme oxygenase: Comparison of static structures and dynamic conformation changes following CO photolysis

Biochemistry

Volumn 51, Issue 43, 2012, Pages 8554-8562

  Sugishima, Masakazu ^a,b   Moffat, Keith ^b,c   Noguchi, Masato ^a  

^a KURUME UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b UNIVERSITY OF CHICAGO   (United States)

^c UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CONFORMATION CHANGE; CONFORMATIONAL CHANGE; CRYOGENIC TEMPERATURES; DIFFERENCE-FOURIER MAP; HEME DEGRADATION; HEME IRON; HEME OXYGENASES; LIGAND BINDING; LIGAND-FREE; PRODUCT INHIBITION; PROTEIN MOTION; STATIC STRUCTURES; STERIC HINDRANCES; STRUCTURAL CHANGE;

CARBON MONOXIDE; CHEMICAL REACTIONS; IRON COMPOUNDS; PHOTOLYSIS;

PORPHYRINS;

CARBON MONOXIDE; HEME; HEME OXYGENASE; OXYGEN;

ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DEGRADATION KINETICS; ENZYME CONFORMATION; ENZYME STRUCTURE; HYDROGEN BOND; LIGAND BINDING; PHOTOLYSIS; PRIORITY JOURNAL;

ANIMALS; CARBON MONOXIDE; CRYSTALLOGRAPHY, X-RAY; HEME OXYGENASE (DECYCLIZING); MOLECULAR DYNAMICS SIMULATION; OXYGEN; PHOTOLYSIS; PROTEIN BINDING; PROTEIN CONFORMATION; RATS;

EID: 84868138296     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi301175x     Document Type: Article

References (41)

1. Tenhunen, R., Marver, H. S., and Schmid, R. (1968) The enzymatic conversion of heme to bilirubin by microsomal heme oxygenase Proc. Natl. Acad. Sci. U.S.A. 61, 748-755
2. Ortiz de Montellano, P. R. (2000) The mechanism of heme oxygenase Curr. Opin. Chem. Biol. 4, 221-227
3. Kikuchi, G., Yoshida, T., and Noguchi, M. (2005) Heme oxygenase and heme degradation Biochem. Biophys. Res. Commun. 338, 558-567
4. Ryter, S. W., Alam, J., and Choi, A. M. (2006) Heme oxygenase-1/carbon monoxide: From basic science to therapeutic applications Physiol. Rev. 86, 583-650
5. 2-dependent verdoheme degradation by heme oxygenase: Reaction mechanisms and potential physiological roles of the dual pathway degradation J. Biol. Chem. 280, 36833-36840
6. Yoshida, T., Noguchi, M., and Kikuchi, G. (1980) A new intermediate of heme degradation catalyzed by the heme oxygenase system J. Biochem. 88, 557-563
7. Sakamoto, H., Omata, Y., Adachi, Y., Palmer, G., and Noguchi, M. (2000) Separation and identification of the regioisomers of verdoheme by reversed-phase ion-pair high-performance liquid chromatography, and characterization of their complexes with heme oxygenase J. Inorg. Biochem. 82, 113-121
8. Migita, C. T., Mansfield Matera, K., Ikeda-Saito, M., Olson, J. S., Fujii, H., Yoshimura, T., Zhou, H., and Yoshida, T. (1998) The oxygen and carbon monoxide reactions of heme oxygenase J. Biol. Chem. 273, 945-949
9. Springer, B. A., Sligar, S. G., Olson, J. S., and Phillips, G. N., Jr. (1994) Mechanisms of ligand recognition in myoglobin Chem. Rev. 94, 699-714
10. Hargrove, M. S., Barry, J. K., Brucker, E. A., Berry, M. B., Phillips, G. N., Jr., Olson, J. S., Arredondo-Peter, R., Dean, J. M., Klucas, R. V., and Sarath, G. (1997) Characterization of recombinant soybean leghemoglobin a and apolar distal histidine mutants J. Mol. Biol. 266, 1032-1042
11. Kuriyan, J., Wilz, S., Karplus, M., and Petsko, G. A. (1986) X-ray structure and refinement of carbon-monoxy (Fe II)-myoglobin at 1.5 Å resolution J. Mol. Biol. 192, 133-154
12. Vojtěchovský, J., Chu, K., Berendzen, J., Sweet, R. M., and Schlichting, I. (1999) Crystal structures of myoglobin-ligand complexes at near-atomic resolution Biophys. J. 77, 2153-2174
13. Lim, M., Jackson, T. A., and Anfinrud, P. A. (1995) Binding of CO to myoglobin from a heme pocket docking site to form nearly linear Fe-C-O Science 269, 962-966
14. Antonyuk, S. V., Rustage, N., Petersen, C. A., Arnst, J. L., Heyes, D. J., Sharma, R., Berry, N. G., Scrutton, N. S., Eady, R. R., Andrew, C. R., and Hasnain, S. S. (2011) Carbon monoxide poisoning is prevented by the energy costs of conformational changes in gas-binding haemproteins Proc. Natl. Acad. Sci. U.S.A. 108, 15780-15785
15. Nuernberger, P., Lee, K. F., Bonvalet, A., Bouzhir-Sima, L., Lambry, J. C., Liebl, U., Joffre, M., and Vos, M. H. (2011) Strong ligand-protein interactions revealed by ultrafast infrared spectroscopy of CO in the heme pocket of the oxygen sensor FixL J. Am. Chem. Soc. 133, 17110-17113
16. 2 in HO-1 Biochemistry 42, 9898-9905
17. Unno, M., Matsui, T., and Ikeda-Saito, M. (2007) Structure and catalytic mechanism of heme oxygenase Nat. Prod. Rep. 24, 553-570
18. Friedman, J., Meharenna, Y. T., Wilks, A., and Poulos, T. L. (2007) Diatomic ligand discrimination by the heme oxygenases from Neisseria meningitidis and Pseudomonas aeruginosa J. Biol. Chem. 282, 1066-1071
19. Sugishima, M., Sakamoto, H., Noguchi, M., and Fukuyama, K. (2004) CO-trapping site in heme oxygenase revealed by photolysis of its CO-bound heme complex: Mechanism of escaping from product inhibition J. Mol. Biol. 341, 7-13
20. Schlichting, I., Berendzen, J., Phillips, G. N., Jr., and Sweet, R. M. (1994) Crystal structure of photolysed carbonmonoxy-myoglobin Nature 371, 808-812
21. Teng, T. Y., Šrajer, V., and Moffat, K. (1994) Photolysis-induced structural changes in single crystals of carbonmonoxy myoglobin at 40 K Nat. Struct. Biol. 1, 701-705
22. Hartmann, H., Zinser, S., Komninos, P., Schneider, R. T., Nienhaus, G. U., and Parak, F. (1996) X-ray structure determination of a metastable state of carbonmonoxy myoglobin after photodissociation Proc. Natl. Acad. Sci. U.S.A. 93, 7013-7016
23. Chu, K., Vojtchovsky, J., McMahon, B. H., Sweet, R. M., Berendzen, J., and Schlichting, I. (2000) Structure of a ligand-binding intermediate in wild-type carbonmonoxy myoglobin Nature 403, 921-923
24. Adachi, S., Park, S. Y., Tame, J. R., Shiro, Y., and Shibayama, N. (2003) Direct observation of photolysis-induced tertiary structural changes in hemoglobin Proc. Natl. Acad. Sci. U.S.A. 100, 7039-7044
25. Yamaoka, M., Sugishima, M., Noguchi, M., Fukuyama, K., and Mizutani, Y. (2011) Protein dynamics of heme-heme oxygenase-1 complex following carbon monoxide dissociation J. Raman Spectrosc. 42, 910-916
26. Otwinowski, Z. and Minor, W. (1997) Processing of X-ray Diffraction Data Collected in Oscillation Mode Methods Enzymol. 276, 307-326
27. 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
28. Emsley, P. and Cowtan, K. (2004) Coot: Model-building tools for molecular graphics Acta Crystallogr. D60, 2126-2132
29. Chen, V. B., Arendall, W. B., III, Headd, J. J., Keedy, D. A., Immormino, R. M., Kapral, G. J., Murray, L. W., Richardson, J. S., and Richardson, D. C. (2010) MolProbity: All-atom structure validation for macromolecular crystallography Acta Crystallogr. D66, 12-21
30. Ursby, T. and Bourgeois, D. (1997) Improved estimation of structure-factor difference amplitudes from poorly accurate data Acta Crystallogr. A53, 564-575
31. Paithankar, K. S., Owen, R. L., and Garman, E. F. (2009) Absorbed dose calculations for macromolecular crystals: Improvements to RADDOS J. Synchrotron Radiat. 16, 152-162
32. Unno, M., Matsui, T., Chu, G. C., Couture, M., Yoshida, T., Rousseau, D. L., Olson, J. S., and Ikeda-Saito, M. (2004) Crystal structure of the dioxygen-bound heme oxygenase from Corynebacterium diphtheriae: Implications for heme oxygenase function J. Biol. Chem. 279, 21055-21061
33. Takahashi, S., Ishikawa, K., Takeuchi, N., Ikeda-Saito, M., Yoshida, T., and Rousseau, D. L. (1995) Oxygen-Bound Heme-Heme Oxygenase Complex: Evidence for a Highly Bent Structure of the Cooridnated Oxygen J. Am. Chem. Soc. 117, 6002-6006
34. Ostermann, A., Waschipky, R., Parak, F. G., and Nienhaus, G. U. (2000) Ligand binding and conformational motions in myoglobin Nature 404, 205-208
35. Migita, C. T., Togashi, S., Minakawa, M., Zhang, X., and Yoshida, T. (2005) Evidence for the hydrophobic cavity of heme oxygenase-1 to be a CO-trapping site Biochem. Biophys. Res. Commun. 338, 584-589
36. Sato, H., Sugishima, M., Sakamoto, H., Higashimoto, Y., Shimokawa, C., Fukuyama, K., Palmer, G., and Noguchi, M. (2009) Crystal structure of rat haem oxygenase-1 in complex with ferrous verdohaem: Presence of a hydrogen-bond network on the distal side Biochem. J. 419, 339-345
37. Petřek, M., Otyepka, M., Banáš, P., Košinová, P., Koča, J., and Damborský, J. (2006) CAVER: A New Tool to Explore Routes from Protein Clefts, Pockets and Cavities BMC Bioinf. 7, 316
38. Mizutani, Y. and Kitagawa, T. (2001) Ultrafast dynamics of myoglobin probed by time-resolved resonance Raman spectroscopy Chem. Rec. 1, 258-275
39. Šrajer, V., Teng, T., Ursby, T., Pradervand, C., Ren, Z., Adachi, S., Schildkamp, W., Bourgeois, D., Wulff, M., and Moffat, K. (1996) Photolysis of the carbon monoxide complex of myoglobin: Nanosecond time-resolved crystallography Science 274, 1726-1729
40. Tomita, A., Sato, T., Ichiyanagi, K., Nozawa, S., Ichikawa, H., Chollet, M., Kawai, F., Park, S. Y., Tsuduki, T., Yamato, T., Koshihara, S. Y., and Adachi, S. (2009) Visualizing breathing motion of internal cavities in concert with ligand migration in myoglobin Proc. Natl. Acad. Sci. U.S.A. 106, 2612-2616
41. The PyMOL Molecular Graphics System, version 1.3r1 (2010) Schrödinger, LLC, New York.