1H NMR characterization of the solution active site structure of substrate-bound, cyanide-inhibited heme oxygenase from Neisseria meningitidis: Comparison to crystal structures

Biochemistry

Volumn 43, Issue 31, 2004, Pages 10112-10126

  Liu, Yangzhong ^a   Zhang, Xuhong ^b   Yoshida, Tadashi ^b   La Mar, Gerd N ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b YAMAGATA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CYANIDES; ELECTRONIC STRUCTURE; ENZYMES; HYDROGEN BONDS; MOLECULAR STRUCTURE; NUCLEAR MAGNETIC RESONANCE; PROTONS; SUBSTRATES;

DIPOLAR SHIFTS; HOMOLOGY; OXYGENASE; PROXIMAL HELICES;

CRYSTAL STRUCTURE;

ARGININE; CARBOXYLIC ACID; CYANIDE; HEME; HEME OXYGENASE; HEMIN; HISTIDINE; IRON; NITRIC OXIDE; PROPIONIC ACID DERIVATIVE; PYRROLE; SOLVENT; WATER; BACTERIAL PROTEIN; ENZYME INHIBITOR; HEMO PROTEIN, NEISSERIA MENINGITIDIS; PEPTIDE FRAGMENT; PROTON;

ARTICLE; CHEMICAL STRUCTURE; CORYNEBACTERIUM DIPHTHERIAE; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; HYDROGEN BOND; NEISSERIA MENINGITIDIS; NONHUMAN; NUCLEAR OVERHAUSER EFFECT; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTON NUCLEAR MAGNETIC RESONANCE; SEQUENCE HOMOLOGY; STEREOCHEMISTRY; AMINO ACID SEQUENCE; ANIMAL; BINDING SITE; CHEMISTRY; COMPARATIVE STUDY; CRYSTALLIZATION; DRUG ANTAGONISM; ENZYME SPECIFICITY; ENZYMOLOGY; HUMAN; METABOLISM; METHODOLOGY; MOLECULAR GENETICS; NUCLEAR MAGNETIC RESONANCE; PROTEIN BINDING; PROTEIN SECONDARY STRUCTURE; SOLUTION AND SOLUBILITY; THERMODYNAMICS;

BACTERIA (MICROORGANISMS); CORYNEBACTERIUM; CORYNEBACTERIUM DIPHTHERIAE; INSERTION SEQUENCES; MAMMALIA; NEISSERIA; NEISSERIA MENINGITIDIS;

AMINO ACID SEQUENCE; ANIMALS; BACTERIAL PROTEINS; BINDING SITES; CRYSTALLIZATION; CYANIDES; ENZYME INHIBITORS; HEME; HEME OXYGENASE (DECYCLIZING); HEMIN; HUMANS; HYDROGEN BONDING; MOLECULAR SEQUENCE DATA; NEISSERIA MENINGITIDIS; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PEPTIDE FRAGMENTS; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTONS; SOLUTIONS; SUBSTRATE SPECIFICITY; THERMODYNAMICS; WATER;

EID: 3543123507     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi049438s     Document Type: Article

References (68)

1. Tenhunen, R., Marver, H. S., and Schmid, R. (1969) Microsomal heme oxygenase. Characterization of the enzyme, J. Biol. Chem. 244, 6388-6394.
2. Maines, M. D. (1988) Heme oxygenase: function, multiplicity, regulatory mechanisms, and clinical applications, FASEB J. 2, 2557-2568.
3. Yoshida, T., and Migita, C. T. (2000) Mechanism of heme degradation by heme oxygenase, J. Inorg. Biochem. 82, 33-41.
4. Wilks, A. (2002) Heme Oxygenase: Evolution, Structure, and Mechanism, Antioxid. Redox Signal. 4, 603-614.
5. Ortiz de Montellano, P. R., and Auclair, K. (2003) in The Porphryin Handbook (Kadish, K. M., Smith, K. M., and Guilard, R., Eds.) pp 175-202, Elsevier Science, San Diego, CA.
6. Schmitt, M. P. (1997) Utilization of host iron sources by Corynebacterium dihtheriae: identification of a gene whose product is homologous to eukaryotic heme oxygenases and is required for acquisition of iron from heme and hemoglobin J. Bacteriol. 179, 838-845.
7. Zhu, W., Willks, A., and Stojiljkovic, I. (2000) Degradation of heme in gram-negative bacteria: the product of the hemO gene of Neisseriae is a heme oxygenase J. Bacteriol. 182, 6783-6790.
8. Bullen, J. J., and Griffiths, E. (1999) in Iron and Infection: Molecular, Physiological, and Clinical Aspects, pp 87-213, John Wiley and Sons, New York.
9. Ratliff, M., Zhu, M., Deshmukh, R., Wilks, A., and Stojiljkovic, I. (2001) Homologues of Neisserial Heme Oxygenase in Gram-Negative Bacteria: Degradation of Heme by the Product of the pigA Gene of Pseudomonas aeruginosa, J. Bacteriol. 183, 6394-6403.
10. Wilks, A., and Schmitt, M. P. (1998) Expression and characterization of a heme oxygenase (HmuO) from Corynebacterium diphtheriae J. Biol. Chem. 273, 837-841.
11. Beale, S. I. (1994) Biosynthesis of open-chain tetrapyrroles in plants, algae, and cyanobacteria, Ciba Foundation Symposium 180, 156-168.
12. Ortiz de Montellano, P. R. (1998) Heme Oxygenase Mechanism: Evidence for an Electrophilic, Ferric Peroxide Species, Acc. Chem. Res. 31, 543-549.
13. Schuller, D. J. (2001) in Handbook of Metalloproteins (Messerschmidt, A., Huber, R., Poulos, T. L., and Wieghardt, K., Eds.) pp 317-327, John Wiley & Sons, Inc., New York.
14. Davydov, R. M., Yoshida, T., Ikeda-Saito, M., and Hoffman, B. M. (1999) Hydroperoxy-Heme Oxygenase Generated by Cryoreduction Catalyzes the Formation of α-meso-Hydroxyheme as Detected by EPR and ENDOR, J. Am. Chem. Soc. 121, 10656-10657.
15. Davydov, R., Kofman, V., Fujii, H., Yoshida, T., Ikeda-Saito, M., and Hoffman, B. M. (2002) Catalytic mechanism of heme oxygenase through EPR and ENDOR of cryoreduced oxy-heme oxygenase and its Asp 140 mutants J. Am. Chem. Soc. 124, 1798-1808.
16. Ortiz de Montellano, P. R. (1995) in Cytochrome P450: Structure, Mechanism, and Biochemistry (Ortiz de Montellano, P. R., Ed.) pp 245-304, Plenum Press, New York.
17. Schuller, D. J., Wilks, A., Ortiz de Montellano, P. R., and Poulos, T. L. (1999) Crystal structure of human heme oxygenase-1 Nat. Struct. Biol. 6, 860-867.
18. Lad, L., Wang, J., Li, H., Friedman, J., Bhaskar, B., Ortiz de Montellano, P. R., and Poulos, T. L. (2003) Crystal Structures of the Ferric, Ferrous, and Ferrous-NO Forms of the Asp140A1a Mutant of Human Heme Oxygenase-1: Catalytic Implications, J. Mol. Biol. 330, 527-538.
19. Sugishima, M., Omata, Y., Kakuta, Y., Sakamoto, H., Noguchi, M., and Fukuyama, K. (2000) Crystal structure of rat heme oxygenase-1 in complex with heme, FEBS Lett. 471, 61-66.
20. Sugishima, M., Sakamoto, H., Higashimoto, Y., Omata, Y., Hayashi, S., Noguchi, M., and Fukuyama, K. (2002) Crystal structure of rat heme oxygenase-1 in complex with heme bound to azide: Implication for regiospecific hydroxylation of heme at the α-meso carbon, J. Biol. Chem., 45086-45090.
21. Sugishima, M., Sakamoto, H., Noguchi, M., and Fukuyama, K. (2003) Crystal Structures of CO-, CN-, and NO-Bound Forms of Rat Heme Oxygenase-1 (HO-1) in Complex with Heme: Structural Implications for Discrimination between CO and O2 in HO-1, Biochemistry 42, 9898-9905.
22. Lad, L., Schuller, D. J., Shimizu, H., Friedman, J., Li, H., Ortiz de Montellano, P. R., and Poulos, T. L. (2003) Comparison of the Heme-free and -bound Crystal Structures of Human Heme Oxygenase-1, J. Biol. Chem. 278, 7834-7843.
23. Sugishima, M., Sakamoto, H., Kakuta, Y., Omata, Y., Hayashi, S., Noguchi, M., and Fukuyama, K. (2002) Crystal Structue of Rat Apo-Heme Oxygenase-1 (HO-1): Mechanism of Heme Binding in HO-1 Inferred from Structural Comparison of the Apo and Heme Complex Forms, Biochemistry 41, 7293-7300.
24. Schuller, D. J., Zhu, W., Stojiljkovic, I., Wilks, A., and Poulos, T. L. (2001) Crystal structure of heme oxygenase from the Gram-negative pathogen Neisseria meningitidis and a comparison with mammalian heme oxygeanse-1, Biochemistry 40, 11552-11558.
25. Friedman, J. M., Lad, L., Deshmukh, R., Li, H. Y., Wilks, A., and Poulos, T. L. (2003) Crystal structures of the NO- and CO-bound heme oxygenase from Neisseriae meningitidis-Implications for O2 activation, J. Biol. Chem. 278, 34654-34659.
26. Hirotsu, S., Chu, G. C., Unno, M., Lee, D.-S., Yoshida, T., Park, S.-Y., Shiro, Y., and Ikeda-Saito, M. (2004) The Crystal Structures of the Ferric and Ferrous Forms of the Heme Complex of HmuO, a Heme Oxygenase of Corynebacterium diphtheriae, J. Biol. Chem. 279, 11937-11947.
27. 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 coordinated oxygen, J. Am. Chem. Soc. 117, 6002-6006.
28. 1H NMR investigation of the molecular and electronic structure of the active site of substrate-bound human heme oxygenase: the nature of the distal hydrogen bond donor to bound ligands, J. Am. Chem. Soc. 120, 8875-8884.
29. 1H NMR of the active site of substrate-bound, cyanide-ligated, human heme oxygenase. Comparison to the crystal structure of the water-ligated form, J. Biol. Chem. 276, 15676-15687,
30. Li, Y., Syvitski, R. T., Auclair, K., Wilks, A., Ortiz de Montellano, P. R., and La Mar, G. N. (2002) Solution NMR characterization of an unusual distal H-bond network in the active site of the cyanide-inhibited, human heme oxygenase complex of the symmetric substrate, 2,4-dimethyldeuteriohemin, J. Biol. Chem. 277, 33018-33031.
31. 1H NMR investigation of the active site molecular and electronic structures of the substrate-bound, cyanide-inhibited bacterial heme oxygenase from C. diphtheriae, J. Biol. Chem. 279, 6651-6663.
32. 1H NMR detection of immobilized water molecules within a strong hydrogen-bonding network in the distal side of substrate-bound human heme oxygenase, J. Am. Chem. Soc. 124, 14296-14297.
33. 15N NMR spectroscopic characterization of substrate-bound cyanide-inhibited, human heme oxygenase: water occupation of the distal cavity, J. Am. Chem. Soc. 125, 13392-13403.
34. 1H NMR Investigation of the Solution Structure of Substrate-free Human Heme Oxygenase: Comparison to the Cyanide-inhibited, Substrate-bound Complex, J. Biol. Chem. 279, 10195-10205.
35. Otting, G. (1997) NMR studies of water bound to biological molecules, Prog. NMR Spectrosc. 31, 259-285.
36. Koenigs Lightning, L., Huang, H.-W., Moënne-Loccoz, P., Loehr, T. M., Schuller, D. J., Poulos, T. L., and Ortiz de Montellano, P. R. (2001) Disruption of an active site hydrogen bond converts human heme oxygenase-1 into a peroxidase, J. Biol. Chem. 276, 10612-10619.
37. Fujii, H., Zhang, X., Tomita, T., Ikeda-Saito, M., and Yoshida, T. (2001) A role for highly conserved carboxylate, Aspartate-140, in oxygen activation and heme degradation by heme oxygenase-1, J. Am. Chem. Soc. 123, 6475-6484.
38. Sambrook, J., Fritsch, E. F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
39. Lowry, O. H., Rosebrough, N. J., Farr, A. L., and Randall, R. J. (1951) Protein measurement with the folin phenol reagent J. Biol. Chem. 193, 265-275.
40. Johnston, P. D., Figueroa, N., and Redfield, A. G. (1979) Real-time solvent exchange studies of the imino and amino protons of yeast phenylalanine transfer RNA by Fourier transform NMR Proc. Natl. Acad. Sci. U.S.A. 76, 3130-3134.
41. Piotto, M., Sandek, V., and Sklenar, V. (1992) Gradient-tailored excitation for single quantum NMR spectroscopy of aqueous solutions, J. Biomol. NMR 2, 661-666.
42. Gupta, R. K. (1976) Dynamic Range Problem in Fourier Transform NMR. Modified WEFT Pulse Sequence, J. Magn. Reson. 24, 461-465.
43. Jeener, J., Meier, B. H., Bachmann, P., and Ernst, R. R. (1979) Investigation of Exchange Processes by Two-Dimensional NMR Spectroscopy, J. Chem. Phys. 71, 4546-4553.
44. 1H Spin System Identification in Macromolecules, J. Am. Chem. Soc. 110, 7870-7872.
45. Bax, A., and Davis, D. G. (1985) Mlev-17-based two-dimensional homonuclear magnetization transfer spectroscopy, J. Magn. Reson. 65, 355-360.
46. Emerson, S. D., and La Mar, G. N. (1990) Solution Structural Characterization of Cyano Met-Myoglobin: Resonance Assignment of Heme Cavity Residues by 2D NMR, Biochemistry 29, 1545-1555.
47. La Mar, G. N., Satterlee, J. D., and de Ropp, J. S. (1999) in The Porphyrins Handbook (Kadish, K. M., Smith, K. M., and Guilard, R., Eds.) pp 185-298, Academic Press, San Diego.
48. Williams, G., Clayden, N. J., Moore, G. R., and Williams, R. J. P. (1985) Comparison of the Solution and Crystal Structures of Mitochondrial Cytochrome c. Analysis of Paramagnetic Shifts in the Nuclear Magnetic Resonance Spectrum of Ferricytochrome c, J. Mol. Biol. 183, 447-460.
49. 1H NMR Parameters of the Common Amino Acid Residues Measured in Aqueous Solutions of the Linear Tetrapeptides H-Gly-Gly-X-L-Ala-OH, Biopolymers 18, 285-297.
50. Wishart, D. S., Sykes, B. D., and Richards, F. M. (1991) Relationship Between Nuclear Magnetic Resonance Chemical Shift and Protein Secondary Structure, J. Mol. Biol. 222, 311-333.
51. 15N chemical shifts, J. Biomol. NMR 26, 215-240.
52. Cross, K. J., and Wright, P. E. (1985) Calibration of Ring-current Models for the Heme Ring, J. Magn. Reson. 64, 220-231.
53. Hernández, G., Wilks, A., Paolesse, R., Smith, K. M., Ortiz de Montellano, P. R., and La Mar, G. N. (1994) Proton NMR Investigation of Substrate-bound Heme Oxygenase: Evidence for Electronic and Steric Contributions to Stereoselective Heme Cleavage, Biochemistry 33, 6631-6641.
54. 1H NMR Chemical Shifts in Proteins, J. Am. Chem. Soc. 105, 5948-5949.
55. La Mar, G. N., and de Ropp, J. S. (1993) NMR Methodology for Paramagnetic Proteins, Biol. Magn. Reson. 18, 1-79.
56. Wüthrich, K. (1986) NMR of Proteins and Nucleic Acids, Wiley & Sons, New York.
57. 1H NMR Resonance Assignment of Hyperfine-shifted Residues in the Active Site of a Paramagnetic Protein: Application to Aplysia Cyano-metmyoglobin, J. Biomol. NMR 2, 597-618.
58. Shokhirev, N. V., and Walker, F. A. (1998) The Effect of Axial Ligand Plane Orientation on the Contact and Pseudocontact Shifts of Low-spin Ferriheme Proteins, J. Biol. Inorg. Chem. 3, 581-594.
59. 1H Contact Shifts in Low-Spin Fe(III) Model Hemes and Heme Proteins: Explanation of "Curie" and "Anti-Curie" behavior within the Same Molecule, J. Phys. Chem. 99, 17795-17804.
60. 1H NMR characterization of axial interactions of the proximal and distal His in the cyanomet complexes of the isolated chains and 65 kDa intact tetramer of human hemoglobin, J. Am. Chem. Soc. 123, 4266-4274.
61. Nguyen, B. D., Xia, Z., Yeh, D. C., Vyas, K., Deaguero, H., and La Mar, G. (1999) Solution NMR Determination of the Anisotropy and Orientation of the Paramagnetic Susceptibility Tensor as a Function of Temperature for Metmyoglobin Cyanide; Implications for the Population of Excited Electronic States, J. Am. Chem. Soc. 121, 208-217.
62. Emerson, S. D., and La Mar, G. N. (1990) NMR Determination of the Orientation of the Magnetic Susceptibility Tensor in Cyano Met-Myoglobin: A New Probe of Steric Tilt of Bound Ligand, Biochemistry 29, 1556-1566.
63. Caignan, G. A., Deshmukh, R., Wilks, A., Zeng, Y., Huang, H.-w., Moenne-Loccoz, P., Bunce, R. A., Eastman, M. A., and Rivera, M. (2002) Oxidation of heme to β- and δ-biliverdin by Pseudomonas aeruginosa Heme Oxygenase as a Consequence of an Unusual Seating of the Heme, J. Am. Chem. Soc. 124, 14879-14892.
64. Friedman, J., Lad, L., Li, H., Wilks, A., and Poulos, T. L. (2004) Structural Basis for Novel δ-Regioselective Heme Oxygenation in the Opportunistic Pathogen Pseudomonas aeruginosa, Biochemistry 43, 5239-5245.
65. Fujii, H., Zhang, X., and Yoshida, T. (2004) Essential Amino Acid Residues Controlling the Unique Regioselectivity of Heme Oxygenase in Pseudomonas aeruginosa, J. Am. Chem. Soc. 126.
66. Jeffrey, G. A. (1997) An Introduction to Hydrogen Bonding, Oxford University Press, New York.
67. Mildvan, A. S., Harris, T. K., and Abeygunawardana, C. (1999) Nuclear Magnetic Resonance Methods for the Detection and Study of Low-Barrier Hydrogen Bonds on Enzymes, Methods Enzymol. 308, 219-245.
68. Englander, S. W., and Kallenbach, N. R. (1984) Hydrogen exchange and structural dynamics of proteins and nucleic acids, Quart. Rev. Biophys. 16, 521-655.