Heme oxidation in a chimeric protein of the α-selective Neisseriae meningitidis heme oxygenase with the distal helix of the δ-selective Pseudomonas aeruginosa

Biochemistry

Volumn 44, Issue 42, 2005, Pages 13713-13723

  Deshmukh, Rahul ^d,e   Zeng, Yuhong ^b   Furci, Lena M ^d   Huang, Hong Wei ^a   Morgan, Bailey N ^b   Sander, Suzanne ^b   Alontaga, Aileen Y ^b   Bunce, Richard A ^c   Moënne Loccoz, Pierre ^a   Rivera, Mario ^b   Wilks, Angela ^d  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b UNIVERSITY OF KANSAS   (United States)

^c OKLAHOMA STATE UNIVERSITY   (United States)

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

^e WEST VIRGINIA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; FOURIER TRANSFORM INFRARED SPECTROSCOPY; HYDROGEN BONDS; NUCLEAR MAGNETIC RESONANCE; OXIDATION; RAMAN SPECTROSCOPY;

HELIX RESIDUES; HEME OXYGENASES; PATHOGENS; REGIOSELECTIVITY;

PROTEINS;

ALANINE; BILIVERDIN; BILIVERDIN IX DELTA; CHIMERIC PROTEIN; HEME; HEME OXYGENASE; HEME PROPIONATE; HISTIDINE; LIGAND; LYSINE; METHIONINE; POLYPEPTIDE; PROPIONIC ACID; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; CATALYSIS; HYDROGEN BOND; HYDROXYLATION; INFRARED SPECTROSCOPY; NEISSERIA MENINGITIDIS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; OXIDATION; PRIORITY JOURNAL; PROTEIN CONFORMATION; PSEUDOMONAS AERUGINOSA; RAMAN SPECTROMETRY; REPRODUCIBILITY; SEQUENCE ANALYSIS;

CATALYSIS; HEME; HEME OXYGENASE (DECYCLIZING); MUTAGENESIS, SITE-DIRECTED; NEISSERIA MENINGITIDIS; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN CONFORMATION; PSEUDOMONAS AERUGINOSA; RECOMBINANT FUSION PROTEINS; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; SPECTRUM ANALYSIS, RAMAN;

BACTERIA (MICROORGANISMS); NEISSERIA MENINGITIDIS; NEISSERIAE MENINGITIDIS; PSEUDOMONAS AERUGINOSA;

EID: 27144449927     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi050810t     Document Type: Article

References (37)

1. Ratliff, M., Zhu, W., 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.
2. Zhu, W., Wilks, A., and Stojiljkovic, I. (2000) Degradation of Heme in Gram-Negative Bacteria: The Product of the hemO Gene of Neisseriae meningitidis Is a Heme Oxygenase, J. Bacteriol. 182, 6783-6790.
3. Wilks, A., and Moenne-Loccoz, P. (2000) Identification of the Proximal Ligand His-20 in Heme Oxygenase (Hmu O) from Corynebacterium diphtheriae. Oxidative cleavage of the heme macrocycle does not require the proximal histidine, J. Biol. Chem. 275, 11686-11692.
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. 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 Asp140Ala mutant of human heme oxygenase-1: Catalytic implications, J. Mol. Biol. 330, 527-538.
6. 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.
7. 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. 277, 45086-45090.
8. 2 in HO-1, Biochemistry 42, 9898-9905.
9. 2 activation, J. Biol. Chem. 278, 34654-34659.
10. 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.
11. 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.
12. 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.
13. 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.
14. 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, 4466-4467.
15. Zeng, Y., Deshmukh, R., Caignan, G. A., Bunce, R. A., Rivera, M., and Wilks, A. (2004) Mixed regioselectivity in the Arg-177 mutants of Corynebacterium diphtheriae heme oxygenase as a consequence of in-plane heme disorder, Biochemistry 43, 5222-5238.
16. Sambrook, J., Fritsch, E. F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, Cold Spring Harbor Laboratory Press, Plainview, NY.
17. Yoshida, T., and Kikuchi, G. (1979) Purification and properties of heme oxygenase from rat liver microsomes, J. Biol. Chem. 254, 4487-4491.
18. Wilks, A., and Ortiz de Montellano, P. R. (1993) Rat liver heme oxygenase. High level expression of a truncated soluble form and nature of the meso-hydroxylating species, J. Biol. Chem. 268, 22357-22362.
19. Fuhrop, J. H., and Smith, K. M. (1975) (Smith, K. M., Ed.) pp 804-807, Elsevier, Amsterdam.
20. Wilks, A., and Schmitt, M. P. (1998) Expression and characterization of a heme oxygenase (Hmu O) from Corynebacterium diphtheriae. Iron acquisition requires oxidative cleavage of the heme macrocycle, J. Biol. Chem. 273, 837-841.
21. 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.
22. 13C]-Labeled δ-Aminolevulinic Acid, J. Labelled Compd. Radiopharm. 39, 669-675.
23. Rivera, M., and Walker, F. A. (1995) Biosynthetic Preparation of Isotopically Labeled Heme, Anal. Biochem. 230, 295-302.
24. Warren, M. J., and Scott, A. I. (1990) Tetrapyrrole Assembly and Modification into the Ligands of Biologically Functional Cofactors, Trends Biochem. Sci. 15, 426-431.
25. 12: A Survey of the Last Four Billion Years, Angew. Chem. 32, 1223-1376.
26. 5, J. Biol. Inorg. Chem. 4, 87-98.
27. 12 through the Use of New Two-Dimensional NMR Experiments, J. Am. Chem. Soc. 108, 4285-4294.
28. Patt, S. L., and Sykes, B. D. (1972) Water Eliminated Fourier Transform NMR Spectroscopy, J. Chem. Phys. 56, 3182-3184.
29. Lankhorst, P. P., Wille, G., van Boom, J. H., Altona, C., and Haasnoot, C. A. G. (1983) Conformational Analysis of a Ribopentanucleoside Tetraphosphate in Aqueous Solution, A Two-Dimensional NMR Study at 500 MHz, Nucleic Acids Res. 11, 2839-2856.
30. Jeneer, 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.
31. Kitagawa, T. (1988) in Heme protein structure and the iron-histidine stretching mode (Spiro, T., Ed.) pp 97-131, John Wiley & Sons, New York.
32. Ray, G. B., Li, X.-Y., Ibers, J. A., Sessler, J. L., and Spiro, T. G. (1994) How far can proteins bend the FeCO unit? Distal polar and steric effects in heme proteins and models, J. Am. Chem. Soc. 116, 162-176.
33. Phillips, G. N., Jr., Teodoro, M. L., Li, T., Smith, B., and Olson, J. S. (1999) Bound CO Is A Molecular Probe of Electrostatic Potential in the Distal Pocket of Myoglobin, J. Phys. Chem. B 103, 8817-8829.
34. Li, T., Quillin, M. L., Phillips, G. N., Jr., and Olson, J. S. (1994) Structural determinants of the stretching frequency of CO bound to myoglobin, Biochemistry 33, 1433-1446.
35. 1H NMR characterization of the solution active site structure of substrate-bound, cyanide-inhibited heme oxygenase from Neisseria meningitidis: Comparison to crystal structures, Biochemistry 43, 10112-10126.
36. 13C NMR Spectroscopic Analysis of Paramagnetic Hemes and Heme Proteins, Anal. Bioanal. Chem. 378, 1464-1483.
37. 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.