Heme oxygenase reveals Its strategy for catalyzing three successive oxygenation reactions

Accounts of Chemical Research

Volumn 43, Issue 2, 2010, Pages 240-247

  Matsui, Toshitaka ^a   Masaki, Unno ^a,b   Masao, Ikeda Saito ^a  

^a TOHOKU UNIVERSITY   (Japan)

^b IBARAKI UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

HEME; HEME OXYGENASE; OXYGEN;

ANIMAL; ARTICLE; BIOCATALYSIS; CHEMISTRY; ENZYME SPECIFICITY; HUMAN; METABOLISM; OXIDATION REDUCTION REACTION;

ANIMALS; BIOCATALYSIS; HEME; HEME OXYGENASE (DECYCLIZING); HUMANS; OXIDATION-REDUCTION; OXYGEN; SUBSTRATE SPECIFICITY;

EID: 77249168703     PISSN: 00014842     EISSN: 15204898     Source Type: Journal    
DOI: 10.1021/ar9001685     Document Type: Article

References (67)

1. Tenhunen, R.; Marver, H. S.; Schmid, R. Microsomal heme oxygenase. Characterization of the enzyme. J. Biol. Chem. 1969, 244, 6388-6394.
2. Yoshida, T.; Kikuchi, G. Features of the reaction of heme degradation catalyzed by the reconstituted microsomal heme oxygenase system. J. Biol. Chem. 1978, 253, 4230-4236.
3. Ortiz de Montollano, P. R. Heme oxygenase mechanism - Evidence for an electrophilic, ferric peroxide species. Acc. Chem. Res. 1998, 31, 543-549.
4. Maines, M. D.; Trakshel, G. M.; Kutty, R. K. Characterization of two constitutive forms of rat liver microsomal heme oxygenase. Only one molecular species of the enzyme is inducible. J. Biol. Chem. 1986, 261, 411-419.
5. Schacter, B. A.; Nelson, E. B.; Marver, H. S.; Masters, B. S. S. Immunochemical evidence for an association of heme oxygenase with the microsomal electron transport system. J. Biol. Chem. 1972, 247, 3601-3607.
6. Maines, M. D. The heme oxygenase system: A regulator of second messenger gases. Annu. Rev. Pharmacol. Toxicol. 1997, 37, 517-554.
7. Poss, K. D.; Tonegawa, S. Reduced stress defense in heme oxygenase 1 -deficient cells. Proc. Natl. Acad. Sci. U.S.A. 1997, 94, 10925-10930.
8. Suematsu, M.; Ishimura, Y. The heme oxygenase-carbon monoxide system: A regulator of hepatobiliary function. Hepatology 2000, 31, 3-6.
9. Williams, S. E.; Wootton, P.; Mason, H. S.; Bould, J.; lles, D. E.; Riccardi, D.; Peers, C.; Kemp, P. J. Hemoxygenase-2 is an oxygen sensor for a calcium-sensitive potassium channel. Science 2004, 306, 2093-2097.
10. Cornejo, J.; Willows, R. D.; Beale, S. I. Phytobilin biosynthesis: Cloning and expression of a gene encoding soluble ferredoxin-dependent heme oxygenase from Synechocystis sp. PCC 6803. Plant J. 1998, 15, 99-107.
11. Davis, S. J.; Kurepa, J.; Vierstra, R. D. Arabidopsis thaliana HY1 locus, required for phytochrome-chromophore biosynthesis, encodes a protein related to heme oxygenases. Proc. Natl. Acad. Sci. U.S.A. 1999, 96, 6541-6546.
12. Schmitt, M. P. Utilization of host Iron sources by Corynebacterium diphtheriae: 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. 1997, 179, 838-845.
13. Wandersman, C.; Stojiljkovic, I. Bacterial heme sources: The role of heme, hemoprotein receptors and hemophores. Curr. Opin. Microbiol. 2000, 3, 215-220.
14. Genco, C. A.; Dixon, D. W. Emerging strategies In microbial haem capture. Mol. Microbiol. 2001, 39, 1-11.
15. Colas, C.; Ortiz de Montollano, P. R. Autocatalytic radical reactions in physiological prosthetic heme modification. Chem. Rev. 2003, 103, 2305-2332.
16. Unno, M.; Matsui, T.; Ikeda-Saito, M. Structure and catalytic mechanism of heme oxygenase. Nat. Prod. Rep. 2007, 24, 553-570.
17. 2-dependent verdoheme degradation by heme oxygenase: Reaction mechanisms and potential physiological roles of the dual pathway degradation. J. Biol. Chem. 2005, 280, 36833-36840.
18. Matsui, T.; Omori, K.; Jin, H.; Ikeda-Saito, M. Alkyl peroxides reveal the ring opening mechanism of verdoheme catalyzed by heme oxygenase. J. Am. Chem. Soc. 2008, 130, 4220-4221.
19. Matsui, T.; Kim, S. H.; Jin, H.; Hoffman, B. M.; Ikeda-Saito, M. Compound I of heme oxygenase cannot hydroxylate its heme meso-carbon. J. Am. Chem. Soc. 2006, 128, 1090-1091.
20. Wilks, A.; Ortiz de Montellano, P. R. Rat liver heme oxygenase. High level expression of a truncated soluble form and nature of the meso-hydroxylating species. J. Biol. Chem. 1993, 268, 22357-22362.
21. Wilks, A.; Torpey, J.; Ortiz de Montellano, P. R. Heme oxygenase (HO-1). Evidence for electrophilic oxygen addition to the porphyrin ring in the formation of α-mesohydroxyheme. J. Biol. Chem. 1994, 269, 29553-29556.
22. Davydov, R. M.; Yoshida, T.; Ikeda-Saito, M.; Hoffman, B. M. Hydroperoxy-heme oxygenase generated by cryoreduction catalyzes the formation of α-mesohydroxyheme as detected by EPR and ENDOR. J. Am. Chem. Soc. 1999, 121, 10656-10657.
23. Evans, J. P.; Niemevz, F.; Buldain, G.; Ortiz de Montellano, P. R. Isoporphyrin intermediate In heme oxygenase catalysis: Oxidation of α-meso-phenylheme. J. Biol. Chem. 2008, 283, 19530-19539.
24. Schuller, D. J.; Wilks, A.; Ortiz de Montellano, P. R.; Poulos, T. L Crystal structure of human heme oxygenase-I. Nat. Struct. Biol. 1999, 6, 860-867.
25. Sugishima, M.; Omata, Y.; Kakuta, Y.; Sakamoto, H.; Noguchi, M.; Fukuyama, K. Crystal structure of rat heme oxygenase-1 In complex with heme. FEBS Lett 2000, 471, 61-66.
26. Unno, M.; Matsui, T.; Chu, G. C.; Couture, M.; Yoshida, T.; Rousseau, D. L.; Olson, J. S.; Ikeda-Saito, M. Crystal structure of the dioxygen-bound heme oxygenase from Corynebacterium diphtheriae: Implications for heme oxygenase function. J. Biol. Chem. 2004, 279, 21055-21061. (Pubitemid 38656507)
27. Takahashi, S.; Wang, J.; Rousseau, D. L; Ishikawa, K.; Yoshida, T.; Host, J. R.; Ikeda-Saito, M. Heme-heme oxygenase complex. Structure of the catalytic site and its implication for oxygen activation. J. Biol. Chem. 1994, 269, 1010-1014. (Pubitemid 24981977)
28. Takahashi, S.; Ishikawa, K.; Takeuchi, N.; Ikeda-Saito, M.; Yoshida, T.; Rousseau, D. L Oxygen-bound heme-heme oxygenase complex - Evidence for a highly bent structure of the coordinated oxygen. J. Am. Chem. Soc. 1995, 117, 6002-6006.
29. Hirotsu, S.; Chu, G. C.; Unno, M.; Lee, D. S.; Yoshida, T.; Park S. Y.; Shiro, Y.; Ikeda-Saito, M. The crystal structures of the ferric and ferrous forms of the heme complex of HmuO, a heme oxygenase of Corynebacterium diphtheriae. J. Biol. Chem. 2003, 279, 11937-11947.
30. Fujii, H.; Zhang, X.; Tomita, T.; Ikeda-Saito, M.; Yoshida, T. A role for highly conserved carboxylate, aspartate-140, In oxygen activation and heme degradation by heme oxygenase-1. J. Am. Chem. Soc. 2001, 123, 6475-6484.
31. Lightning, L. K.; Huang, H.; Moenne-Loccoz, P.; Loehr, T. M.; Schuller, D. J.; Poulos, T. L; Ortiz de Montellano, P. R. Disruption of an active site hydrogen bond converts human heme oxygenase-1 into a peroxidase. J. Biol. Chem. 2001, 276, 10612-10619.
32. Schuller, D. J.; Zhu, W.; Stojiljkovic, I.; Wilks, A.; Poulos, T. L Crystal structure of heme oxygenase from the Gram-negative pathogen Neisseria meningitidis and a comparison with mammalian heme oxygenase-1. Biochemistry 2001 ,40,11552-11558.
33. Friedman, J.; Lad, L.; Li, H.; Wilks, A.; Poulos, T. L. Structural basis for novel δ rcgiosolcctive heme oxygenation In the opportunistic pathogen Pseudomonas aeruginosa. Biochemistry 2004, 43, 5239-5245.
34. Matsui, T.; Furukawa, M.; Unno, M.; Tomita, T.; Ikeda-Saito, M. Roles of distal Asp In heme oxygenase from Corynebacterium diphtheriae, HmuO: A water-driven oxygen activation mechanism. J. Biol. Chem. 2005, 280, 2981-2989.
35. 1H NMR investigation of the active site molecular and electronic structures of substratebound, cyanide-inhibited HmuO, a bacterial heme oxygenase from Corynebacterium diphtheriae. J. Biol. Chem. 2003, 278, 6651-6663.
36. Lad, L.; Wang, J.; Li, H.; Friedman, J.; Bhaskar, B.; Ortiz de Montellano, P. R.; Poulos, T. L Crystal structures of the ferric, ferrous, and ferrous-NO forms of the Asp140Ala mutant of human heme oxygenase-1 : Catalytic Implications. J. Mol. Biol. 2003, 330, 527-538.
37. Davydov, R.; Kofman, V.; Fujii, H.; Yoshida, T.; Ikeda-Saito, M.; Hoffman, B. M. Catalytic mechanism of heme oxygenase through EPR and ENDOR of cryoreduced oxy-heme oxygenase and its Asp 140 mutants. J. Am. Chem. Soc. 2002, 124, 1798-1808.
38. Denisov, I. G.; Ikeda-Saito, M.; Yoshida, T.; Silgar, S. G. Cryogenic absorption spectra of hydroperoxo-ferric heme oxygenase, the active intermediate of enzymatic heme oxygenation. FEBS Lett. 2002, 532, 203-206.
39. Garcia-Serres, R.; Davydov, R. M.; Matsui, T.; Ikeda-Saito, M.; Hoffman, B. M.; Huynh, B. H. Distinct reaction pathways followed upon reduction of oxy-heme oxygenase and oxy-myoglobin as characterized by Mössbauer spectroscopy. J. Am. Chem. Soc. 2007, 129, 1402-1412.
40. Davydov, R.; Chemerisov, S.; Werst, D. E.; Rajh, T.; Matsui, T.; Ikeda-Saito, M.; Hoffman, B. M. Proton transfer at helium temperatures during dioxygen activation by heme monooxygenases. J. Am. Chem. Soc. 2004, 126, 15960-15961.
41. Davydov, R.; Makris, T. M.; Kofman, V.; Werst, D. E.; Sligar, S. G.; Hoffman, B. M. Hydroxylation of camphor by reduced oxy-cytochrome P450cam: Mechanistic implications of EPR and ENDOR studies of catalytic intermediates in native and mutant enzymes. J. Am. Chem. Soc. 2001, 123, 1403-1415.
42. Davydov, R.; Matsui, T.; Fujii, H.; Ikeda-Saito, M.; Hoffman, B. M. Kinetic isotope effects on the rate-limiting step of heme oxygenase catalysis Indicate concerted proton transfer/heme hydroxylation. J. Am. Chem. Soc. 2003, 125, 16208-16209.
43. Kumar, D.; de Visser, S. P.; Shaik S. Theory favors a stepwise mechanism of porphyrin degradation by a ferric hydroperoxide model of the active species of heme oxygenase. J. Am. Chem. Soc. 2005, 127, 8204-8213.
44. Kamachi, T.; Yoshizawa, K. Water-assisted oxo mechanism tor heme metabolism. J. Am. Chem. Soc. 2005, 127, 10686-10692.
45. Chen, H.; Moreau, Y.; Derat, E.; Shaik, S. Quantum mechanical/molecular mechanical study of mechanisms of heme degradation by the enzyme heme oxygenase: The strategic function of the water cluster. J. Am. Chem. Soc. 2008, 130, 1953-1965.
46. Mansfield Matera, K.; Takahashi, S.; Fujii, H.; Zhou, H.; Ishikawa, K.; Yoshimura, T.; Rousseau, D. L; Yoshida, T.; Ikeda-Saito, M. Oxygen and one reducing equivalent are both required for the conversion of α-hydroxyhemin to verdoheme in heme oxygenase. J. Biol. Chem. 1996, 271, 6618-6624.
47. Liu, Y.; Moenne-Loccoz, P.; Loehr, T. M.; Ortiz de Montellano, P. R. Heme oxygenase-1, Intermediates in verdoheme formation and the requirement for reduction equivalents. J. Biol. Chem. 1997, 272, 6909-6917.
48. Zhang, X.; Fujii, H.; Mansfield Matera, K.; Migita, C. T.; Sun, D.; Sato, M.; IkedaSaito, M.; Yoshida, T. Stereoselectivity of each of the three steps of the heme oxygenase reaction: hemin to meso-hydroxyhemin, meso-hydroxyhemin to verdoheme, and verdoheme to biliverdin. Biochemistry 2003, 42, 7418-7426.
49. Morishima, I.; Fujii, H.; Shiro, Y.; Sano, S. Studies on the iron(II) meso-oxyporphyrin π-neutral radical as a reaction intermediate in heme catabolism. Inorg. Chem. 1995, 34, 1528-1535.
50. Takahashi, S.; Mansfield Matera, K.; Fujii, H.; Zhou, H.; Ishikawa, K.; Yoshida, T.; Ikeda-Saito, M.; Rousseau, D. L Resonance Raman spectroscopic characterization of α-hydroxyheme and verdoheme complexes of heme oxygenase. Biochemistry 1997, 36,1402-1410.
51. Migita, C. T.; Fujii, H.; Mansfield Matera, K.; Takahashi, S.; Zhou, H.; Yoshida, T. Molecular oxygen oxidizes the porphyrin ring of the ferric α- hydroxyheme In heme oxygenase in the absence of reducing equivalent. Biochim. Biophys. Acta 1999, 1432, 203-213.
52. Sakamoto, H.; Ornate, Y.; Hayashi, S.; Harada, S.; Palmer, G.; Noguchi, M. The reactivity of α-hydroxyhaem and verdohaem bound to haem oxygenase-1 to dioxygen and sodium dithionite. Eur. J. Biochem. 2002, 269, 5231-5239.
53. Sakamoto, H.; Takahashi, K.; Higashimoto, Y.; Harada, S.; Palmer, G.; Noguchi, M. A kinetic study of the mechanism of conversion of α-hydroxyheme to verdoheme while bound to heme oxygenase. Biochem. Biophys. Res. Commun. 2005, 338, 578-583.
54. Liu, Y.; Ortiz de Montellano, P. R. Reaction intermediates and single turnover rate constants tor the oxidation of heme by human heme oxygenase-1. J. Biol. Chem. 2000, 275, 5297-5307.
55. Fuhrhop, J. H.; Kruger, P. 1- or 19-Methoxy-, 1- or 19-amino- and 1- or 19-thiodeoxybiliverdins. Liebigs Ann. Chem. 1977, 360-370.
56. Saito, S.; Itano, H. A. Verdohemochrome IXα: Preparation and oxidorcductive cleavage to biliverdin IXα. Proc. Natl. Acad. Sci. U.S.A. 1982, 79, 1393-1397.
57. Sano, S.; Sano, T.; Morishima, I.; Shiro, Y.; Maeda, Y. On the mechanism of the chemical and enzymic oxygenations of α-oxyprotohemin IX to Fe.biliverdin IXα. Proc. Natl. Acad. Sci. U.S.A. 1986, 83, 531-535.
58. 1H NMR spectra of intermediates from the addition of hydroxide or methoxide with Fe(II) and Fe(III) verdohemes. Inorg. Chem. 2001, 40, 4971-4977.
59. Koemer, R.; Latos-Grazynski, L; Balch, A. L Models for verdoheme hydrolysis. Paramagnetic products from the ring opening of verdohemes, 5-oxaporphyrin complexes of iron(ll), with methoxide ion. J. Am. Chem. Soc. 1998, 120, 9246-9255.
60. Nguyen, K. T.; Rath, S. P.; Latos-Grazynski, L; Olmstead, M. M.; Balch, A. L. Formation of a highly oxidized iron biliverdin complex upon treatment of a fivecoordinate verdoheme with dioxygen. J. Am. Chem. Soc. 2004, 126, 6210-6211.
61. 18O labeling. J Biol. Chem. 1984, 259, 13066-13069.
62. Lad, L.; Ortiz de Montellano, P. R.; Poulos, T. L. Crystal structures of ferrous and ferrous-NO forms of verdoheme In a complex with human heme oxygenase-1 : Catalytic Implications for heme cleavage. J. Inorg. Biochem. 2004, 98, 1686-1695.
63. Damaso, C. O.; Bunce, R. A.; Baybin, M. V.; Wilks, A.; Rivera, M. The ferrous verdoheme-heme oxygenase complex Is six-coordinate and low-spin. J. Am. Chem. Soc. 2005, 127, 17582-17583.
64. Matsui, T.; Unno, M.; Ikeda-Saito, M. Unpublished results.
65. Baranano, D. E.; Rao, M.; Ferris, C. D.; Snyder, S. H. Biliverdin reductase: A major physiologic cytoprotectant. Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 16093-16098.
66. Migita, C. T.; Mansfield Matera, K.; Ikeda-Saito, M.; Olson, J. S.; Fujii, H.; Yoshimura, T.; Zhou, H.; Yoshida, T. The oxygen and carbon monoxide reactions of heme oxygenase. J. Biol. Chem. 1998, 273, 945-949.
67. Matsui, T.; Ikeda-Saito, M. Unpublished results.