Role of cysteine residues in heme binding to human heme oxygenase-2 elucidated by two-dimensional NMR spectroscopy

Journal of Biological Chemistry

Volumn 287, Issue 42, 2012, Pages 35181-35191

  Varfaj, Fatbardha ^a   Lampe, Jed N ^a   Ortiz De Montellano, Paul R ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYS RESIDUES; CYSTEINE RESIDUES; FERROUS IRON; HEME BINDING; HEME IRON; HEME OXYGENASE-2; HEME OXYGENASES; INDUCIBLE ENZYME; INTRAMOLECULAR DISULFIDE BONDS; MICROENVIRONMENTS; NADPH-CYTOCHROME P450 REDUCTASE; OXIDIZED STATE; REDOX STATE; REDUCED-STATE; REGULATORY PROCESS; SITE-SPECIFIC; SITE-SPECIFIC MUTAGENESIS;

AMINO ACIDS; COVALENT BONDS; ENZYME ACTIVITY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; TISSUE; TWO DIMENSIONAL;

PORPHYRINS;

APOPROTEIN; CARBON 13; CYSTEINE; HEME; HEME OXYGENASE 2;

ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; DISULFIDE BOND; ENZYME BINDING; HYDROPHILICITY; MOLECULAR INTERACTION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OXIDATION REDUCTION STATE; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; SITE DIRECTED MUTAGENESIS; TWO DIMENSIONAL NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY;

CARBON ISOTOPES; CYSTEINE; HEME; HEME OXYGENASE (DECYCLIZING); HUMANS; ISOTOPE LABELING; MUTAGENESIS, SITE-DIRECTED; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; OXIDATION-REDUCTION; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY;

EID: 84867406948     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.378042     Document Type: Article

References (31)

1. Moore, B. A., Overhaus, M., Whitcomb, J., Ifedigbo, E., Choi, A. M., Otterbein, L. E., and Bauer, A. J. (2005) Brief inhalation of low-dose carbon monoxide protects rodents and swine from postoperative ileus. Crit. Care Med. 33, 1317-1326 (Pubitemid 40827384)
2. Otterbein, L. E., Soares, M. P., Yamashita, K., and Bach, F. H. (2003) Heme oxygenase-1. Unleashing the protective properties of heme. Trends Immunol. 24, 449-455 (Pubitemid 36928103)
3. 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 (Pubitemid 29031171)
4. Trakshel, G. M., Kutty, R. K., and Maines, M. D. (1986) Purification and characterization of the major constitutive form of testicular heme oxygenase. The noninducible isoform. J. Biol. Chem. 261, 11131-11137 (Pubitemid 17216715)
5. Williams, S. E., Wootton, P., Mason, H. S., Bould, J., Iles, D. E., Riccardi, D., Peers, C., and Kemp, P. J. (2004) Hemoxygenase-2 is an oxygen sensor for a calcium-sensitive potassium channel. Science 306, 2093-2097 (Pubitemid 40007661)
6. 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 (Pubitemid 28041463)
7. 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 (Pubitemid 29415179)
8. Bianchetti, C. M., Yi, L., Ragsdale, S. W., and Phillips, G. N., Jr. (2007) Comparison of apo- and heme-bound crystal structures of a truncated human heme oxygenase-2. J. Biol. Chem. 282, 37624-37631
9. Chen, J. J., Throop, M. S., Gehrke, L., Kuo, I., Pal, J. K., Brodsky, M., and London, I. M. (1991) Cloning of the cDNA of the heme-regulated eukaryotic initiation factor 2α (eIF-2α) kinase of rabbit reticulocytes. Homology to yeast GCN2 protein kinase and human double-stranded RNA-dependent eIF-2α kinase. Proc. Natl. Acad. Sci. U.S.A. 88, 7729-7733 (Pubitemid 21915228)
10. Rafie-Kolpin, M., Chefalo, P. J., Hussain, Z., Hahn, J., Uma, S., Matts, R. L., and Chen, J. J. (2000) Two heme-binding domains of heme-regulated eukaryotic initiation factor-2α kinase. N terminus and kinase insertion. J. Biol. Chem. 275, 5171-5178 (Pubitemid 30108920)
11. Creusot, F., Verdière, J., Gaisne, M., and Slonimski, P. P. (1988) CYP1 (HAP1) regulator of oxygen-dependent gene expression in yeast. I. Overall organization of the protein sequence displays several novel structural domains. J. Mol. Biol. 204, 263-276
12. Dumont, M. E., Ernst, J. F., Hampsey, D. M., and Sherman, F. (1987) Identification and sequence of the gene encoding cytochrome c heme lyase in the yeast Saccharomyces cerevisiae. EMBO J. 6, 235-241
13. Steiner, H., Kispal, G., Zollner, A., Haid, A., Neupert, W., and Lill, R. (1996) Heme binding to a conserved Cys-Pro-Val motif is crucial for the catalytic function of mitochondrial heme lyases. J. Biol. Chem. 271, 32605-32611 (Pubitemid 27008680)
14. Drygas, M. E., Lambowitz, A. M., and Nargang, F. E. (1989) Cloning and analysis of the Neurospora crassa gene for cytochrome c heme lyase. J. Biol. Chem. 264, 17897-17906
15. Lathrop, J. T., and Timko, M. P. (1993) Regulation by heme of mitochondrial protein transport through a conserved amino acid motif. Science 259, 522-525 (Pubitemid 23058711)
16. Triggs-Raine, B. L., Doble, B. W., Mulvey, M. R., Sorby, P. A., and Loewen, P. C. (1988) Nucleotide sequence of katG, encoding catalase HPI of Escherichia coli. J. Bacteriol. 170, 4415-4419
17. Yi, L., and Ragsdale, S. W. (2007) Evidence that the heme regulatory motifs in heme oxygenase-2 serve as a thiol/disulfide redox switch regulating heme binding. J. Biol. Chem. 282, 21056-21067 (Pubitemid 47099923)
18. 13C NMR chemical shifts can predict disulfide bond formation. J. Biomol. NMR 18, 165-171
19. Lightning, L. K., Huang, H., Moenne-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 (Pubitemid 38089229)
20. Dierks, E. A., Davis, S. C., and Ortiz de Montellano, P. R. (1998) Glu-320 and Asp-323 are determinants of the CYP4A1 hydroxylation regiospecificity and resistance to inactivation by 1-aminobenzotriazole. Biochemistry 37, 1839-1847 (Pubitemid 28099806)
21. Jiang, Y., Trnka, M. J., Medzihradszky, K. F., Ouellet, H., Wang, Y., and Ortiz de Montellano, P. R. (2009) Covalent heme attachment to the protein in human heme oxygenase-1 with selenocysteine replacing the His-25 proximal iron ligand. J. Inorg. Biochem. 103, 316-325
22. 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 (Pubitemid 23318280)
23. Yoshida, T., and Kikuchi, G. (1978) Purification and properties of heme oxygenase from pig spleen microsomes. J. Biol. Chem. 253, 4224-4229 (Pubitemid 8380644)
24. Rosenfeld, J., Capdevielle, J., Guillemot, J. C., and Ferrara, P. (1992) In-gel digestion of proteins for internal sequence analysis after one- or two-dimensional gel electrophoresis. Anal. Biochem. 203, 173-179
25. Hellman, U., Wernstedt, C., Góñez, J., and Heldin, C. H. (1995) Improvement of an "in-gel" digestion procedure for the micropreparation of internal protein fragments for amino acid sequencing. Anal. Biochem. 224, 451-455
26. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe. A multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6, 277-293
27. Wehrli, F., and Wirthlin, T. (1976) Interpretation of Carbon-13 NMR Spectra, Heyden, London
28. a value of the buried, active-site cysteine on the redox properties of thioredoxin-like oxidoreductases. FEBS Lett. 477, 21-26
29. Gardner, J. D., Yi, L., Ragsdale, S. W., and Brunold, T. C. (2010) Spectroscopic insights into axial ligation and active-site hydrogen bonding in substrate-bound human heme oxygenase-2. J. Biol. Inorg. Chem. 15, 1117-1127
30. Lakowicz, J. R. (2006) Principles of Fluorescence Spectroscopy, 3rd Ed., p. 178, Springer Publishing, New York
31. Sassa, S. (2004) Why heme needs to be degraded to iron, biliverdin IXα, and carbon monoxide? Antioxid. Redox Signal. 6, 819-824