The C-terminal heme regulatory motifs of heme oxygenase-2 are redox-regulated heme binding sites

Biochemistry

Volumn 54, Issue 17, 2015, Pages 2709-2718

  Fleischhacker, Angela S ^a   Sharma, Ajay ^c   Choi, Michelle ^a   Spencer, Andrea M ^a,b   Bagai, Ireena ^a   Hoffman, Brian M ^c   Ragsdale, Stephen W ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

^c NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BINDING SITES; COVALENT BONDS; LIGANDS; SOLS; SPECTROSCOPIC ANALYSIS; SULFUR COMPOUNDS;

CATALYTIC SITES; DISULFIDE BONDS; HEME OXYGENASE-2; HEME REGULATORY MOTIFS; MULTIPLE BINDING SITES; OXIDIZING CONDITIONS; SPECTRAL FEATURE; SPECTROSCOPIC STUDIES;

PORPHYRINS;

HEME; HEME OXYGENASE 2; IRON; MONOMER; FERRIC ION; HEME OXYGENASE; HEME OXYGENASE-2; LIGAND;

ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CATALYSIS; OXIDATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; REGULATORY MECHANISM; CHEMISTRY; ELECTRON SPIN RESONANCE; HUMAN; METABOLISM; OXIDATION REDUCTION REACTION;

BINDING SITES; ELECTRON SPIN RESONANCE SPECTROSCOPY; FERRIC COMPOUNDS; HEME; HEME OXYGENASE (DECYCLIZING); HUMANS; LIGANDS; OXIDATION-REDUCTION;

EID: 84928944743     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/acs.biochem.5b00266     Document Type: Article

References (32)

1. Maines, M. D. (1997) The heme oxygenase system: A regulator of second messenger gases Annu. Rev. Pharmacol. Toxicol. 37, 517-554
2. Maines, M. D., Trakshel, G. M., and Kutty, R. K. (1986) Characterization of two constitutive forms of rat liver microsomal heme oxygenase: Only one molecular species of the enzyme is inducible J. Biol. Chem. 261, 411-419
3. McCoubrey, W. K. and Maines, M. D. (1993) Domains of rat heme oxygenase-2: The amino terminus and histidine-151 are required for heme oxidation Arch. Biochem. Biophys. 302, 402-408
4. 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
5. Schuller, D. J., Wilks, A., de Montellano, P. R. O., and Poulos, T. L. (1999) Crystal structure of human heme oxygenase-l Nat. Struct. Biol. 6, 860-867
6. Yi, L., Jenkins, P. M., Leichert, L. I., Jakob, U., Martens, J. R., and Ragsdale, S. W. (2009) Heme regulatory motifs in heme oxygenase-2 form a thiol/disulfide redox switch that responds to the cellular redox state J. Biol. Chem. 284, 20556-20561
7. 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
8. Varfaj, F., Lampe, J. N., and de Montellano, P. R. O. (2012) Role of cysteine residues in heme binding to human heme oxygenase-2 elucidated by two-dimensional NMR spectroscopy J. Biol. Chem. 287, 35181-35191
9. Bagai, I., Sarangi, R., Fleischhacker, A. S., Sharma, A., Hoffman, B. M., Zuiderweg, E. R. P., and Ragsdale, S. W. (2015) Spectroscopic studies reveal that the heme regulatory motifs of heme oxygenase-2 are dynamically disordered and exhibit redox-dependent interaction with heme Biochemistry 10.1021/bi501489r
10. Gardner, J. D., Yi, L., Ragsdale, S. W., and Brunold, T. C. (2010) Spectroscopic insights into axial ligation and active-site H-bonding in substrate-bound human heme oxygenase-2 JBIC, J. Biol. Inorg. Chem. 15, 1117-1127
11. Ishikawa, H., Kato, M., Hori, H., Ishimori, K., Kirisako, T., Tokunaga, F., and Iwai, K. (2005) Involvement of heme regulatory motif in heme-mediated ubiquitination and degradation of IRP2 Mol. Cell 19, 171-181
12. Ishikawa, H., Nakagaki, M., Bamba, A., Uchida, T., Hori, H., OBrian, M. R., Iwai, K., and Ishimori, K. (2011) Unusual heme binding in the bacterial iron response regulator protein: Spectral characterization of heme binding to the heme regulatory motif Biochemistry 50, 1016-1022
13. Qi, Z. H., Hamza, I., and OBrian, M. R. (1999) Heme is an effector molecule for iron-dependent degradation of the bacterial iron response regulator (Irr) protein Proc. Natl. Acad. Sci. U.S.A. 96, 13056-13061
14. Igarashi, J., Murase, M., Iizuka, A., Pichierri, F., Martinkova, M., and Shimizu, T. (2008) Elucidation of the heme binding site of heme-regulated eukaryotic initiation factor 2 α kinase and the role of the regulatory motif in heme sensing by spectroscopic and catalytic studies of mutant proteins J. Biol. Chem. 283, 18782-18791
15. Miksanova, M., Igarashi, J., Minami, M., Sagami, I., Yamauchi, S., Kurokawa, H., and Shimizu, T. (2006) Characterization of heme-regulated eIF2 α kinase: Roles of the N-terminal domain in the oligomeric state, heme binding, catalysis, and inhibition Biochemistry 45, 9894-9905
16. McCoubrey, W. K., Huang, T. J., and Maines, M. D. (1997) Heme oxygenase-2 is a hemoprotein and binds heme through heme regulatory motifs that are not involved in heme catalysis J. Biol. Chem. 272, 12568-12574
17. Aslanidis, C. and Dejong, P. J. (1990) Ligation-independent cloning of PCR products (LIC-PCR) Nucleic Acids Res. 18, 6069-6074
18. Stols, L., Gu, M. Y., Dieckman, L., Raffen, R., Collart, F. R., and Donnelly, M. I. (2002) A new vector for high-throughput, ligation-independent cloning encoding a tobacco etch virus protease cleavage site Protein Expression Purif. 25, 8-15
19. Zhou, P. and Wagner, G. (2010) Overcoming the solubility limit with solubility-enhancement tags: Successful applications in biomolecular NMR studies J. Biomol. NMR 46, 23-31
20. Spencer, A. L. M., Bagai, I., Becker, D. F., Zuiderweg, E. R. P., and Ragsdale, S. W. (2014) Protein/protein interactions in the mammalian heme degradation pathway: Heme oxygenase-2, cytochrome P450 reductase, and biliverdin reductase J. Biol. Chem. 289, 29836-29858
21. Dawson, R. M. C. (1986) Data for Biochemical Research, 3 rd ed., Clarendon Press, New York.
22. Berry, E. A. and Trumpower, B. L. (1987) Simultaneous determination of hemes a, b, and c from pyridine hemochrome spectra Anal. Biochem. 161, 1-15
23. Hargrove, M. S., Singleton, E. W., Quillin, M. L., Ortiz, L. A., Phillips, G. N., Olson, J. S., and Mathews, A. J. (1994) His64(E7)→Tyr apomyoglobin as a reagent for measuring rates of hemin dissociation J. Biol. Chem. 269, 4207-4214
24. Ascoli, F., Fanelli, M. R., and Antonini, E. (1981) Preparation and properties of apohemoglobin and reconstituted hemoglobins Methods Enzymol. 76, 72-87
25. Owens, C. P., Du, J., Dawson, J. H., and Goulding, C. W. (2012) Characterization of heme ligation properties of Rv0203, a secreted heme binding protein involved in Mycobacterium tuberculosis heme uptake Biochemistry 51, 1518-1531
26. Davydov, R., Sudhamsu, J., Lees, N. S., Crane, B. R., and Hoffman, B. M. (2009) EPR and ENDOR characterization of the reactive intermediates in the generation of NO by cryoreduced oxy-nitric oxide synthase from Geobacillus stearothermophilus J. Am. Chem. Soc. 131, 14493-14507
27. Flanagan, H. L., Gerfen, G. J., Lai, A., and Singel, D. J. (1988) Orientation-selective 14N electron-spin echo envelope modulation (ESEEM): The determination of 14N quadrupole coupling tensor principal axis orientations in orientationally disordered solids J. Chem. Phys. 88, 2162-2168
28. Magliozzo, R. S. and Peisach, J. (1993) Evaluation of nitrogen nuclear hyperfine and quadrupole coupling parameters for the proximal imidazole in myoglobin azide, myoglobin cyanide, and myoglobin mercaptoethanol complexes by electron-spin echo envelope modulation spectroscopy Biochemistry 32, 8446-8456
29. Yukl, E. T., Jepkorir, G., Alontaga, A. Y., Pautsch, L., Rodriguez, J. C., Rivera, M., and Moenne-Loccoz, P. (2010) Kinetic and spectroscopic studies of hemin acquisition in the hemophore HasAp from Pseudomonas aeruginosa Biochemistry 49, 6646-6654
30. Nygaard, T. K., Blouin, G. C., Liu, M., Fukumura, M., Olson, J. S., Fabian, M., Dooley, D. M., and Lei, B. (2006) The mechanism of direct heme transfer from the streptococcal cell surface protein shp to HtsA of the HtsABC transporter J. Biol. Chem. 281, 20761-20771
31. Hargrove, M. S., Barrick, D., and Olson, J. S. (1996) The association rate constant for heme binding to globin is independent of protein structure Biochemistry 35, 11293-11299
32. Ding, Y., McCoubrey, W. K., and Maines, M. D. (1999) Interaction of home oxygenase-2 with nitric oxide donors: Is the oxygenase an intracellular 'sink' for NO? Eur. J. Biochem. 264, 854-861