Recombinant truncated and microsomal heme oxygenase-1 and -2: Differential sensitivity to inhibitors

Canadian Journal of Physiology and Pharmacology

Volumn 88, Issue 4, 2010, Pages 480-486

  Vukomanovic, Dragic ^a   McLaughlin, Brian ^a   Rahman, Mona N ^a   Vlahakis, Jason Z ^a   Roman, Gheorghe ^a   Dercho, Ryan A ^a   Kinobe, Robert T ^a   Hum, Maaike ^a   Brien, James F ^a   Jia, Zongchao ^a   Szarek, Walter A ^a   Nakatsu, Kanji ^a  

^a QUEEN S UNIVERSITY   (Canada)

Author keywords

Heme oxygenase; Inhibitor; Microsomal; Recombinant truncated human heme oxygenase; Selectivity

Indexed keywords

1,3 DIOXOLANE DERIVATIVE; 2 [2 (4 CHLOROPHENYL)ETHYL] 2 [(1H IMIDAZOL 1 YL)METHYL] 1,3 DIOXOLANE; 4 (4 CHLOROPHENYL) 1 (1H IMIDAZOL 1 YL)BUTAN 2 OL; 4 PHENYL 1 (1H 1,2,4 TRIAZOL 1 YL) 2 BUTANONE; AMINO ACID; HEME OXYGENASE 1; HEME OXYGENASE 2; HEME OXYGENASE INHIBITOR; IMIDAZOLE DERIVATIVE; KETONE DERIVATIVE; MEMBRANE PROTEIN; MICROSOME ENZYME; RECOMBINANT ENZYME; TRIAZOLE DERIVATIVE; UNCLASSIFIED DRUG; 2-(2-(4-CHLOROPHENYL)ETHYL)-2-((1H-IMIDAZOL-1-YL)METHYL)-1,3-DIOXOLANE; 4-(4-CHLOROPHENYL)-1-(1H-IMIDAZOL-1-YL)BUTAN-2-OL; 4-PHENYL-1-(1H-1,2,4-TRIAZOL-1-YL)-2-BUTANONE; ENZYME INHIBITOR; HEME OXYGENASE; HEME OXYGENASE-2; RECOMBINANT PROTEIN;

AMINO ACID SEQUENCE; ANIMAL TISSUE; ARTICLE; BRAIN MICROSOME; CONTROLLED STUDY; DRUG DESIGN; ENZYME CONFORMATION; ENZYME INHIBITION; MALE; MICROSOME; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SPLEEN MICROSOME; ANIMAL; ANTAGONISTS AND INHIBITORS; BRAIN; CHEMISTRY; COMPARATIVE STUDY; ENZYMOLOGY; IN VITRO STUDY; SPLEEN; SPRAGUE DAWLEY RAT;

ANIMALS; BRAIN; ENZYME INHIBITORS; HEME OXYGENASE (DECYCLIZING); HEME OXYGENASE-1; IMIDAZOLES; IN VITRO TECHNIQUES; MALE; MICROSOMES; RATS; RATS, SPRAGUE-DAWLEY; RECOMBINANT PROTEINS; SPLEEN; TRIAZOLES;

EID: 77952028218     PISSN: 00084212     EISSN: None     Source Type: Journal    
DOI: 10.1139/Y10-004     Document Type: Article

References (32)

1. Alam, J. 2002. Heme oxygenase-1: past, present, and future. Antioxid. Redox Signal. 4(4): 559-562. doi:10.1089/15230860260220049. PMID:12230866.
2. Appleton, S.D., Chretien, M.L., McLaughlin, B.E., Vreman, H.J., Stevenson, D.K., Brien, J.F., et al. 1999. Selective inhibition of heme oxygenase, without inhibition of nitric oxide synthase or soluble guanylyl cyclase, by metalloporphyrins at low concentrations. Drug Metab. Dispos. 27(10): 1214-1219. PMID: 10497150.
3. 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(52): 37624-37631. doi:10.1074/jbc.M707396200. PMID:17965015.
4. Braggins, P.E., Trakshel, G.M., Kutty, R.K., and Maines, M.D. 1986. Characterization of two heme oxygenase isoforms in rat spleen: comparison with the hematin-induced and constitutive isoforms of the liver. Biochem. Biophys. Res. Commun. 141(2): 528-533. doi:10.1016/S0006-291X(86)80205-4. PMID:3099789.
5. Chakder, S., Rathi, S., Ma, X.L., and Rattan, S. 1996. Heme oxygenase inhibitor zinc protoporphyrin IX causes an activation of nitric oxide synthase in the rabbit internal anal sphincter. J. Pharmacol. Exp. Ther. 277(3): 1376-1382. PMID:8667200.
6. Cook, M.N., Nakatsu, K., Marks, G.S., McLaughlin, B.E., Vreman, H.J., Stevenson, D.K., and Brien, J.F. 1995. Heme oxygenase activity in the adult rat aorta and liver as measured by carbon monoxide formation. Can. J. Physiol. Pharmacol. 73(4): 515-518. PMID:7671194.
7. Huber, W.J., III, Marohnic, C.C., Peters, M., Alam, J., Reed, J.R., Masters, B.S.S., and Backes, W.L. 2009a. Measurement of membrane-bound human heme oxygenase-1 activity using a chemically defined assay system. Drug Metab. Dispos. 37(4): 857-864. doi:10.1124/dmd.108.025023. PMID:19131520.
8. Huber, W.J., III, Scruggs, B.A., and Backes, W.L. 2009b. C-Terminal membrane spanning region of human heme oxygenase-1 mediates a time-dependent complex formation with cytochrome P450 reductase. Biochemistry, 48(1): 190-197. doi:10.1021/bi801912z. PMID:19123922.
9. Kinobe, R.T., Vlahakis, J.Z., Vreman, H.J., Stevenson, D.K., Brien, J.F., Szarek, W.A., and Nakatsu, K. 2006a. Selectivity of imidazole-dioxolane compounds for in vitro inhibition of microsomal haem oxygenase isoforms. Br. J. Pharmacol. 147(3): 307-315. doi:10.1038/sj.bjp.0706555. PMID:16331285.
10. Kinobe, R.T., Dercho, R.A., Vlahakis, J.Z., Brien, J.F., Szarek, W.A., and Nakatsu, K. 2006b. Inhibition of the enzymatic activity of heme oxygenases by azole-based antifungal drugs. J. Pharmacol. Exp. Ther. 319(1): 277-284. doi:10.1124/jpet.106.102699. PMID:16807364.
11. Kinobe, R.T., Ji, Y., Vlahakis, J.Z., Motterlini, R., Brien, J.F., Szarek, W.A., and Nakatsu, K. 2007. Effectiveness of novel imidazole- dioxolane heme oxygenase inhibitors in renal proximal tubule epithelial cells. J. Pharmacol. Exp. Ther. 323(3): 763-770. doi:10.1124/jpet.107.119800. PMID:17761847.
12. Kinobe, R.T., Dercho, R.A., and Nakatsu, K. 2008. Inhibitors of the heme oxygenase - carbon monoxide system: on the doorstep of the clinic? Can. J. Physiol. Pharmacol. 86(9): 577-599. doi:10.1139/Y08-066.
13. Luo, D., and Vincent, S.R. 1994. Metalloporphyrins inhibit nitric oxidedependent cGMP formation in vivo. Eur. J. Pharmacol. 267(3): 263-267. doi:10.1016/0922-4106(94)90149-X. PMID:7522180.
14. Maines, M.D. 1988. Heme oxygenase: function, multiplicity, regulatory mechanisms, and clinical applications. FASEB J. 2(10): 2557-2568. PMID:3290025.
15. Rahman, M.N., Vlahakis, J.Z., Szarek, W.A., Nakatsu, K., and Jia, Z. 2008. X-ray crystal structure of human heme oxygenase-1 in complex with 1-(adamantan-1-yl)-2-(1H-imidazol-1-yl)ethanone: a common binding mode for imidazole-based heme oxygenase-1 inhibitors. J. Med. Chem. 51(19): 5943-5952. doi:10.1021/jm800505m. PMID:18798608.
16. Rahman, M.N., Vlahakis, J.Z., Vukomanovic, D., Szarek, W.A., Nakatsu, K., and Jia, Z. 2009. X-ray crustal structure of human heme oxygenase-1 with (2R,4S)-2-[2-(4-chlorophenyl)ethyl]-2-[(1H-imidazol-1-yl)methyl] -4[((5-trifluoromethylpyridin-2-yl)thio)methyl]-1,3-dioxolane: a novel inducible binding mode. J. Med. Chem. 52(15): 4946-4950. doi:10.1021/jm900434f. PMID:19601578.
17. Rahman, M.N., Vlahakis, J.Z., Roman, G., Vukomanovic, D., Szarek, W.A., Nakatsu, K., and Jia, Z. 2010. Structural characterization of human heme oxygenase-1 in complex with azole-based inhibitors. J. Inorg. Biochem. 104(3): 324-330. doi:10.1016/j.jinorgbio.2009.10.011. PMID:19917515.
18. Roman, G., Riley, J.G., Vlahakis, J.Z., Kinobe, R.T., Brien, J.F., Nakatsu, K., and Szarek, W.A. 2007. Heme oxygenase inhibition by 2-oxy-substituted 1-(1H-imidazol-1-yl)-4-phenylbutanes: effect of halogen substitution in the phenyl ring. Bioorg. Med. Chem. 15(9): 3225-3234. doi:10.1016/j.bmc.2007.02.034.PMID:17339115.
19. Roman, G., Rahman, M.N., Vukomanovic, D., Jia, Z., Nakatsu, K., and Szarek, W.A. 2010. Heme oxygenase inhibition by 2-oxysubstituted 1-azolyl-4-phenylbutanes: effect of variation of the azole moiety. X-ray crystal structure of human heme oxygenase-1 in complex with 4-phenyl-1-(1H-1,2,4- triazol-1-yl)-2-butanone. Chem. Biol. Drug Des. 75(1): 68-90. doi:10.1111/j.1747-0285.2009.00909.x. PMID:19954435.
20. Ryter, S.W., Alam, J., and Choi, A.M. 2006. Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications. Physiol. Rev. 86(2): 583-650. doi:10.1152/physrev.00011.2005. PMID:16601269.
21. Sugishima, M., Higashimoto, Y., Oishi, T., Takahashi, H., Sakamoto, H., Noguchi, M., and Fukuyama, K. 2007. X-ray crystallographic and biochemical characterization of the inhibitory action of an imidazole-dioxolane compound on heme oxygenase. Biochemistry, 46(7): 1860-1867. doi:10.1021/bi062264p. PMID:17253780.
22. Trakshel, G.M., Kutty, R.K., and Maines, M.D. 1988. Resolution of the rat brain heme oxygenase activity: absence of a detectable amount of the inducible form (HO-1). Arch. Biochem. Biophys. 260(2): 732-739. doi:10.1016/0003-9861(88) 90503-6. PMID:3124761.
23. Vlahakis, J.Z., Kinobe, R.T., Bowers, R.J., Brien, J.F., Nakatsu, K., and Szarek, W.A. 2005. Synthesis and evaluation of azalanstat analogues as heme oxygenase inhibitors. Bioorg. Med. Chem. Lett. 15(5): 1457-1461. doi:10.1016/j.bmcl.2004.12.075. PMID: 15713406.
24. Vlahakis, J.Z., Kinobe, R.T., Bowers, R.J., Brien, J.F., Nakatsu, K., and Szarek, W.A. 2006. Imidazole-dioxolane compounds as isozyme-selective heme oxygenase inhibitors. J. Med. Chem. 49(14): 4437-4441. doi:10.1021/jm0511435. PMID:16821802.
25. Vlahakis, J.Z., Hum, M., Rahman, M.N., Jia, Z., Nakatsu, K., and Szarek, W.A. 2009. Synthesis and evaluation of imidazole-dioxolane compounds as selective heme oxygenase inhibitors: effect of substituents at the 4-position of the dioxolane ring. Bioorg. Med. Chem. 17(6): 2461-2475. doi:10.1016/j.bmc. 2009.01.078. PMID:19268600.
26. Vreman, H.J., and Stevenson, D.K. 1988. Heme oxygenase activity as measured by carbon monoxide production. Anal. Biochem. 168(1): 31-38. doi:10.1016/0003-2697(88)90006-1. PMID:3364715.
27. Vreman, H.J., Ekstrand, B.C., and Stevenson, D.K. 1993. Selection of metalloporphyrin heme oxygenase inhibitors based on potency and photoreactivity. Pediatr. Res. 33(2): 195-200. doi:10.1203/00006450-199302000-00021.
28. Wang, J., Niemevz, F., Lad, L., Huang, L., Alvarez, D.E., Buldain, G., et al. 2004. Human heme oxygenase oxidation of 5- and 15-phenylhemes. J. Biol. Chem. 279(41): 42593-42604. doi:10. 1074/jbc.M406346200. PMID:15297453.
29. 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(30): 22357-22362. PMID:8226746.
30. 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(13): 4421-4427. doi:10.1021/bi00013a034. PMID:7703255.
31. Wilks, A., Medzihradszky, K.F., and Ortiz de Montellano, P.R. 1998. Heme oxygenase active-site residues identified by hemeprotein cross-linking during reduction of CBrCl3. Biochemistry, 37(9): 2889-2896. doi:10.1021/bi972720x. PMID:9485440.
32. 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(29): 21056-21067. doi:10.1074/jbc.M700664200. PMID:17540772.