Structural Basis for Novel δ-Regioselective Heme Oxygenation in the Opportunistic Pathogen Pseudomonas aeruginosa

Biochemistry

Volumn 43, Issue 18, 2004, Pages 5239-5245

  Friedman, Jonathan ^a   Lad, Latesh ^a   Li, Huiying ^a   Wilks, Angela ^b   Poulos, Thomas L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF PHARMACY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; CRYSTAL STRUCTURE; ENZYMES; HYDROPHOBICITY;

OXYGENATION; REGIOSELECTIVITY;

BIOCHEMISTRY;

BACTERIAL ENZYME; BILIVERDIN; HEME; HEME 7 PROPIONATE; HEME DERIVATIVE; HEME OXYGENASE; LYSINE; OXYGEN; PHENYLALANINE; UNCLASSIFIED DRUG; VALINE;

AMINO ACID SEQUENCE; ARTICLE; CRYSTAL STRUCTURE; ENZYME DEGRADATION; ENZYME STABILITY; ENZYME STRUCTURE; GRAM NEGATIVE INFECTION; HYDROGEN BOND; HYDROPHOBICITY; MAMMAL; NONHUMAN; OPPORTUNISTIC INFECTION; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA;

ANIMALS; BACTERIAL PROTEINS; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; HEME; HEME OXYGENASE (DECYCLIZING); HUMANS; HYDROGEN BONDING; HYDROXYLATION; NEISSERIA MENINGITIDIS; OPPORTUNISTIC INFECTIONS; PROPIONATES; PROTEIN STRUCTURE, SECONDARY; PSEUDOMONAS AERUGINOSA; RATS; STRUCTURAL HOMOLOGY, PROTEIN; SUBSTRATE SPECIFICITY;

BACTERIA (MICROORGANISMS); MAMMALIA; NEGIBACTERIA; NEISSERIA; NEISSERIA MENINGITIDIS; PSEUDOMONAS; PSEUDOMONAS AERUGINOSA;

EID: 2442496416     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi049687g     Document Type: Article

References (47)

1. 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.
2. Ortiz de Montellano, P. R. (1998) Heme oxygenase mechanism: evidence for an electrophilic ferric peroxide species, Acc. Chem. Res. 31, 543-549.
3. Sono, M., Roach, M. P., Coulter, E. D., and Dawson, J. H. (1996) Heme-containing Oxygenases, Chem. Rev. 96, 2841-2888.
4. 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.
5. 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.
6. 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 Oxygenase-1, Biochemistry 40, 11552-11558.
7. Hirotsu, S., Chu, G. C., Unno, M., Lee, D. S., Yoshida, T., Park, S.-Y., Shiro, Y., and Ikeda-Saito, M. (2003) The crystal structures of the ferric and ferrous forms of the heme complex of HmuO, a heme oxygenase of Corynebacterium diphtheriae, J. Biol. Chem. (in press).
8. Matera, K. M., Takahashi, S., Fujii, H., Zhou, H., Ishikawa, K., Yoshimura, T., Rousseau, D. L., Yoshida, T., and Ikeda-Saito, M. (1996) Oxygen and one reducing equivalent are both required for the conversion of alpha-hydroxyhemin to verdoheme in heme oxygenase, J. Biol. Chem. 271, 6618-6624.
9. Liu, Y., Moënne-Loccoz, P., Loehr, T. M., and Ortiz de Montellano, P. R. (1997) Heme oxygenase-1, intermediates in verdoheme formation and the requirement for reduction equivalents, J. Biol. Chem. 272, 6909-6917.
10. Liu, Y., and Ortiz de Montellano, P. R. (2000) Reaction intermediates and single turnover rate constants for the oxidation of heme by human heme oxygenase-1, J. Biol. Chem. 275, 5297-5307.
11. Ortiz de Montellano, P. R. (2000) The mechanism of heme oxygenase, Curr. Opin. Chem. Biol. 4, 221-227.
12. Ortiz de Montellano, P. R., and Wilks, A. (2001) in Advances in Inorganic Chemistry, pp 359-407, Academic Press Inc, San Diego, CA.
13. Cornejo, J., Willows, R. D., and Beale, S. I. (1998) Phytobilin biosynthesis: cloning and expression of a gene encoding soluble ferredoxin-dependent heme oxygenase from Synechocystis sp. PCC 6803, Plant J. 15, 99-107.
14. Friebe, A., Schultz, G., and Koesling, D. (1996) Sensitizing soluble guanylyl cyclase to become a highly CO-sensitive enzyme, EMBO J. 15, 6863-6868.
15. Ingi, T., and Ronett, G. V. (1995) Direct demonstration of a physiological role for carbon monoxide in olfactory receptor neurons, J. Neurosci. 15, 8214-8222.
16. Ryter, S. W., Otterbein, L. E., Morse, D., and Choi, A. M. K. (2002) Heme oxygenase/carbon monoxide signaling pathways: Regulation and functional significance, Mol. Cell. Biochem. 234, 249-263.
17. Verma, A., Hirsch, D. J., Glatt, C. E., Ronnett, G. V., and Snyder, S. H. (1993) Carbon monoxide: a putative neural messenger, Science 259, 381-384.
18. Zakhary, R., Poss, K. D., Jaffrey, S. R., Ferris, C. D., Tonegawa, S., and Snyder, S. H. (1997) Targeted gene deletion of heme oxygenase 2 reveals neural role for carbon monoxide, Proc. Natl. Acad. Sci. U.S.A. 94, 14848-14853.
19. Dore, S., Takahashi, M., Ferris, C. D., Hester, L. D., Guastella, D., and Snyder, S. H. (1999) Bilirubin, formed by activation of heme oxygenase-2, protects neurons against oxidative stress injury, Proc. Natl. Acad. Sci. U.S.A. 96, 2445-2450.
20. Stocker, R., Yamamoto, Y., McDonagh, A. F., Glazer, A. N., and Ames, B. N. (1987) Bilirubin is an antioxidant of possible physiological importance, Science 235, 1043-1046.
21. Yachie, A., Niida, Y., Wada, T., Igarashi, N., Kaneda, H., Toma, T., Ohta, K., Kasahara, Y., and Koizumi, S. (1999) Oxidative stress causes enhanced endothelial cell injury in human heme oxygenase-1 deficiency, J. Clin. Invest. 103, 129-135.
22. Zhu, W., Hunt, D. J., Richardson, A. R., and Stojiljkovic, I. (2000) Use of heme compounds as iron sources by pathogenic Neisseriae requires the product of the hemO gene, J. Bacteriol. 182, 439-447.
23. Ratliff, M., Zhu, W. 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.
24. Davies, J. C. (2002) Pseudomonas aeruginosa in cystic fibrosis: pathogenesis and persistance, Paediatr. Respir. Rev. 3, 128-134.
25. Ochsner, U. A., Johnson, Z., and Vasil, M. L. (2000) Genetics and Regulation of Two Distinct Haem-Uptake Systems, Phu and Has, in Pseudomonas aeruginosa, Microbiology 146, 185-198.
26. Vasil, M. L., and Ochsner, U. A. (1999) The response of Pseudomonas aeruginosa to iron: genetics, biochemistry, and virulence, Mol. Microbiol. 34, 399-413.
27. Farnaud, S., and Evans, R. W. (2003) Lactoferrin - a multifunctional protein with antimicrobial properties, Mol. Immunol. 40, 395-405.
28. 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 beta- and delta-Biliverdin by Pseudomonas aeruginosa Heme Oxygenase as a Consequence of an Unusual Seating of the Heme, J. Am. Chem. Soc. 124, 14879-14892.
29. Wilks, A., Black, S. M., Miller, W. L., and Ortiz de Montellano, P. R. (1995) Expression and characterization of truncated human heme oxygenase hHO-1 and a fusion protein of hHO-1 with human cytochrome P450 reductase, Biochemistry 34, 4421-4427.
30. Wilks, A., and Schmitt, M. P. (1998) Expression and characterization of a heme oxygenase (Hmu O) from Corynebacterium diphtheriae, J. Biol. Chem. 273, 837-841.
31. Zhu, W., Wilks, 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.
32. Zhou, H., Migita, C. T., Sato, M., Sun, D., Zhang, X., Ikeda-Saito, M., Fujii, H., and Yoshida, T. (2000) Participation of carboxylate amino acid side chain in regiospecific oxidation of heme by heme oxygenase, J. Am. Chem. Soc. 122, 8311-8312.
33. Otwinowski, Z., and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode, Methods Enzymol. 276, 307-326.
34. Collaborative Computational Project, N. (1994) Acta Crystallogr. D50, 760-767.
35. de La Fortelle, E., and Bricogne, G. (1997) SHARP, Methods Enzymol. 276, 472-494.
36. Jones, T. A., Zou, J. Y., Cowan, S. W., and Kjeldgaard, M. (1991) Improved methods for building protein models in electron density maps and the location of errors in these models, Acta Crystallogr. A47, 110-119.
37. Brunger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J.-S., Kuszewski, R. F., Nilges, M., Pannu, N. S., Read, R. J., Rice, R. J., Rice, L. M., Simonson, T., and Warren, G. L. (1998) Crystallography & NMR System: A new software suite for macromolecular structure determination, Acta Crystallogr. D54, 905-921.
38. Laskowski, R. A., MacArthur, M. W., and Thomton, J. M. (1998) Validation of protein models derived from experiment, Curr. Opin. Struct. Biol. 8, 631-639.
39. Wilks, A. (2002) Heme oxygenase: evolution, structure, and mechanism, Antioxid. Redox Signal. 4, 603-614.
40. Colas, C., and Ortiz de Montellano, P. R. (2003) Autocatalytic radical reactions in physiological prosthetic heme modification, Chem. Rev. 103, 2305-2332.
41. 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.
42. Sugishima, M., Sakamoto, H., Kakuta, Y., Omata, Y., Hayashi, S., Noguchi, M., and Fukuyama, K. (2002) Crystal structure 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.
43. 2 activation, J. Biol. Chem. 278, 34654-34659.
44. Hernandez, 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.
45. 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. (in press).
46. Esnouf, R. M. (1997) An extensively modified version of MolScript that includes greatly enhanced coloring capabilities, J. Mol. Graph. Model. 15, 132-134.
47. Esnouf, R. M. (1999) Further additions to MolScript version 1.4, including reading and contouring of electron-density maps, Acta Crystallogr. D55, 938-940.