Evaluation of Imidazole-Based Compounds as Heme Oxygenase-1 Inhibitors

Chemical Biology and Drug Design

Volumn 80, Issue 6, 2012, Pages 876-886

  Sorrenti, Valeria ^a   Guccione, Salvatore ^a   Di Giacomo, Claudia ^a   Modica, Maria N ^a   Pittalà, Valeria ^a   Acquaviva, Rosaria ^a   Basile, Livia ^b   Pappalardo, Morena ^a   Salerno, Loredana ^a  

^a UNIVERSITY OF CATANIA   (Italy)

^b SCUOLA SUPERIORE DI CATANIA   (Italy)

Author keywords

Docking studies; Enzymatic and spectral analyses; HO 1 inhibitors; Imidazole based compounds; Pharmacophoric model

Indexed keywords

1 (2 PHENOXYETHYL) 1H IMIDAZOLE; 1 (4 BROMOPHENYL) 2 (1H IMIDAZOL 1 YL)ETHANONE; 1 (4 BROMOPHENYL) 2 [2 (1 METHYLETHYL) 1H IMIDAZOL 1 YL]ETHANONE; 1 [4 (3 BROMOPHENOXY)BUTYL] 1H IMIDAZOLE; 1 [6 (4 BROMOPHENOXY)EXYL] 1H IMIDAZOLE; 2 (1H IMIDAZOL 1 YL) 1 (4 NITROPHENYL)ETHANOL; HEME; HEME OXYGENASE 1; HEME OXYGENASE INHIBITOR; IMIDAZOLE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; DRUG PROTEIN BINDING; DRUG SCREENING; DRUG STRUCTURE; ENZYME INHIBITION; IC 50; MALE; MOLECULAR DOCKING; NONHUMAN; PHARMACOPHORE; PRIORITY JOURNAL; RAT; SPECTROSCOPY;

ANIMALS; BINDING SITES; ENZYME INHIBITORS; HEME; HEME OXYGENASE-1; HUMANS; IMIDAZOLES; MOLECULAR DOCKING SIMULATION; PHENYL ETHERS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RATS; RECOMBINANT PROTEINS;

RATTUS;

EID: 84868135974     PISSN: 17470277     EISSN: 17470285     Source Type: Journal    
DOI: 10.1111/cbdd.12015     Document Type: Article

References (57)

1. Tenhunen R., Marver H.S., Schmid R. (1968) The enzymatic conversion of heme to bilirubin by microsomal heme oxygenase. Proc Natl Acad Sci USA;61:748-755.
2. Snyder S.H., Baranano D.E. (2001) Heme oxygenase: a font with multiple messengers. Neuropsychopharmacology;25:294-298.
3. De Matteis F., Dawson S.J., Pons N., Pipino S. (2002) Bilirubin and uroporphyrinogen oxidation by induced cytochrome P4501A and cytochrome P4502B: role of polyhalogenated biphenyls of different configuration. Biochem Pharmacol;63:615-624.
4. Maines M.D. (1988) Heme oxygenase: function, multiplicity, regulatory mechanisms, and clinical applications. FASEB J;2:2557-2568.
5. McCoubrey W.K., Huang T.J., Maines M.D. (1997) Isolation and characterization of a cDNA from the rat brain that encodes hemoprotein heme oxygenase-3. Eur J Biochem;247:725-732.
6. Ryter S.W., Alam J., Choi A.M. (2006) Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications. Physiol Rev;86:583-650.
7. Lee T.S., Chau L.Y. (2002) Heme oxygenase-1 mediates the anti-inflammatory effect of interleukin-10 in mice. Nat Med;8:240-246.
8. Lee T.S., Tsai H.L., Chau L.Y. (2003) Induction of heme oxygenase-1 expression in murine macrophages is essential for the anti-inflammatory effect of low dose 15-deoxy-delta 12, 14-prostaglandin J2. J Biol Chem;278:19325-19330.
9. Imuta N., Hori O., Kitao Y., Tabata Y., Yoshimoto T., Matsuyama T., Ogawa S. (2007) Hypoxia-mediated induction of heme oxygenase type I and carbon monoxide release from astrocytes protects nearby cerebral neurons from hypoxia-mediated apoptosis. Antioxid Redox Signal;9:543-552.
10. Deininger M.H., Meyermann R., Trautmann K., Duffner F., Grote E.H., Wickboldt J., Schluesener H.J. (2000) Heme oxygenase (HO)-1 expressing macrophages/microglial cells accumulate during oligodendroglioma progression. Brain Res;882:1-8.
11. McAllister S.C., Hansen S.G., Ruhl R.A., Raggo C.M., DeFilippis V.R., Greenspan D., Fruh K., Moses A.V. (2004) Kaposi sarcoma-associated herpes virus (KSHV) induces heme oxygenase-1 expression and activity in KSHV-infected endothelial cells. Blood;103:3465-3473.
12. Tsuji M.H., Yanagawa T., Iwasa S., Tabuchi K., Onizawa K., Bannai S., Toyooka H., Yoshida H. (1999) Heme oxygenase-1 expression in oral squamous cell carcinoma as involved in lymphnode metastasis. Cancer Lett;138:53-59.
13. Berberat P.O., Dambrauskas Z., Gulbinas A., Giese T., Giese N., Kunzli B., Autschbach F., Meuer S., Buchler M.W., Friess H. (2005) Inhibition of heme oxygenase-1 increases responsiveness of pancreatic cancer cells to anticancer treatment. Clin Cancer Res;11:3790-3798.
14. Fang J., Akaike T., Maeda H. (2004) Antiapoptotic role of heme oxygenase (HO) and the potential of HO as a target in anticancer treatment. Apoptosis;9:27-35.
15. Mayerhofer M., Florian S., Krauth M.T., Aichberger K.J., Bilban M., Marculescu R., Printz D., Fritsch G., Wagner O., Selzer E., Sperr W.R., Valent P., Sillaber C. (2004) Identification of heme oxygenase- 1 as a novel BCR/ABL-dependent survival factor in chronic myeloid leukemia. Cancer Res;64:3148-3154.
16. Fang J., Sawa T., Akaike T., Greish K., Maeda H. (2004) Enhancement of chemotherapeutic response of tumor cells by a heme oxygenase inhibitor, pegylated zinc protoporphyrin. Int J Cancer;109:1-8.
17. Nowis D., Legat M., Grzela T., Niderla J., Wilczek E., Wilczynski G.M., Glodkowska E. et al. (2006) Heme oxygenase-1 protects tumor cells against photodynamic therapy-mediated cytotoxicity. Oncogene;25:3365-3374.
18. Was H., Cichon T., Smolarczyk R., Rudnicka D., Stopa M., Chevalier C., Leger J.J., Lackowska B., Grochot A., Bojkowska K., Ratajska A., Kieda C., Szala S., Dulak J., Jozkowicz A. (2006) Overexpression of heme oxygenase-1 in murine melanoma: increased proliferation and viability of tumor cells, decreased survival of mice. Am J Pathol;169:2181-2198.
19. Johnson R.A., Colombari E., Colombari D.S., Lavesa M., Talman W.T., Nasjletti A. (1997) Role of endogenous carbon monoxide in central regulation of arterial pressure. Hypertension;30:962-967.
20. Tulis D.A., Durante W., Peyton K.J., Evans A.J., Schafer A.I. (2001) Heme oxygenase-1 attenuates vascular remodeling following balloon injury in rat carotid arteries. Atherosclerosis;155:113-122.
21. Doi K., Akaike T., Fujii S., Tanaka S., Ikebe N., Beppu T., Shibahara S., Ogawa M., Maeda H. (1999) Induction of haem oxygenase-1, nitric oxide and ischaemia in experimental solid tumours and implications for tumour growth. Br J Cancer;80:1945-1954.
22. Fang J., Sawa T., Akaike T., Akuta T., Sahoo S.K., Khaled G., Hamada A., Maeda H. (2003) In vivo antitumor activity of pegylated zinc protoporphyrin: targeted inhibition of heme oxygenase in solid tumor. Cancer Res;63:3567-3574.
23. Hirai K., Sasahira T., Ohmori H., Fujii K., Kuniyasu H. (2007) Inhibition of heme oxygenase-1 by zinc protoporphyrin IX reduces tumor growth of LL/2 lung cancer in C57BL mice. Int J Cancer;120:500-505.
24. Luo D., Vincent S.R. (1994) Metalloporphyrins inhibit nitric oxide dependent cGMP formation in vivo. Eur J Pharmacol;267:263-267.
25. Meffert M.K., Haley J.E., Schuman E.M., Schulman H., Madison D.V. (1994) Inhibition of hippocampal heme oxygenase, nitric oxide synthase, and long-term potentiation by metalloporphyrins. Neuron;13:1225-1233.
26. Vlahakis J.Z., Kinobe R.T., Bowers R.J., Brien J.F., Nakatsub K., Szareka W.A. (2005) Synthesis and evaluation of azalanstat analogues as heme oxygenase inhibitors. Bioorg Med Chem Lett;15:1457-1461.
27. Vlahakis J.Z., Kinobe R.T., Bowers R.J., Brien J.F., Nakatsu K., Szarek W.A. (2006) Imidazole-Dioxolane Compounds as Isozyme-Selective Heme Oxygenase Inhibitors. J Med Chem;49:4437-4441.
28. Vlahakis J.Z., Humb M., Rahman M.N., Jia Z., Nakatsu K., 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;17:2461-2475.
29. Roman G., Riley J.G., Vlahakis J.Z., Kinobe R.T., Brien J.F., Nakatsub K., Szarek W.A. (2007) Heme oxygenase inhibition by 2-oxy-substituted 1-(1H-imidazol-1-yl)-4phenylbutanes: effect of halogen substitution in the phenyl ring. Bioorg Med Chem;15:3225-3234.
30. Roman G., Vlahakis J.Z., Vukomanovic D., Nakatsu K., Szarek W.A. (2010) Heme oxygenase inhibition by 1-Aryl-2-(1H-imidazol-1-yl/1H-1, 2, 4-triazol-1yl) ethanones and their derivatives. Chem Med Chem;5:1541-1555.
31. Kinobe R.T., Vlahakis J.Z., Vreman H.J., Stevenson D.K., Brien J.F., Szarek W.A., Nakatsu K. (2006) Selectivity of imidazole-dioxolane compounds for in vitro inhibition of microsomal haem oxygenase isoforms. Br J Pharmacol;147:307-315.
32. Rahman M.N., Vlahakis J.Z., Szarek W.A., Nakatsu K., Jia Z. (2008) X-ray crystal structure of human heme oxygenase-1 in complex with1-(Adamantan-1-yl)-2-(1H-imidazol-1-yl)ethanone: a common binding mode for imidazole-based heme oxygenase-1 inhibitors. J Med Chem;51:5943-5952.
33. Rahman M.N., Vlahakis J.Z., Roman G., Vukomanovic D., Szarek A., Nakatsu K., Jia Z. (2010) Structural characterization of human heme oxygenase-1 in complex with azole-based inhibitors. J Inorg Biochem;104:324-330.
34. Huber W.J. III, Backes W.L. (2007) Expression and characterization of full-length human heme oxygenase-1: the presence of intact membrane-binding region leads to increased binding affinity for NADPH cytochrome P450 reductase. Biochemistry;46:12212-12219.
35. Huber W.J. III, Scruggs B.A., Backes W.L. (2009) C-Terminal membrane spanning region of human heme oxygenase-1 mediates a time-dependent complex formation with cytochrome P450 reductase. Biochemistry;48:190-197.
36. Huber W.J. III, Marohnic C.C., Peters M., Alam J., Reed J.R., Masters B.S. (2009) Measurement of membrane-bound human heme oxygenase-1 activity using a chemically defined assay system. Drug Metab Dispos;37:857-864.
37. Salerno L., Sorrenti V., Guerrera F., Sarvà M.C., Siracusa M.A., Di Giacomo C., Vanella A. (1999) N-substituted-imidazoles as inhibitors of nitric oxide synthase: a preliminary screening. Pharmazie;54:685-690.
38. Salerno L., Sorrenti V., Guerrera F., Sarvà M.C., Siracusa M.A., Di Giacomo C., Vanella A. (1999) 1-[(aryloxy)alkyl]-1H-imidazoles as inhibitors of neuronal nitric oxide synthase. Pharm Pharmacol Commun;5:491-494.
39. Sorrenti V., Di Giacomo C., Salerno L., Siracusa M.A., Guerrera F., Vanella A. (2001) Inhibition of neuronal nitric oxide synthase by N-phenacyl imidazoles. Nitric Oxide;5:32-38.
40. Di Giacomo C., Sorrenti V., Salerno L., Cardile V., Guerrera F., Siracusa M.A., Avitabile M., Vanella A. (2003) Novel inhibitors of neuronal nitric oxide synthase. Exp Biol Med;228:486-490.
41. Sorrenti V., Salerno L., Di Giacomo C., Acquaviva R., Siracusa M.A., Vanella A. (2006) Imidazole derivatives as antioxidants and selective inhibitors of nNOS. Nitric Oxide;14:45-60.
42. Salerno L., Modica M.N., Romeo G., Pittalà V., Siracusa M.A., Amato M.E., Acquaviva R., Di Giacomo C., Sorrenti V. (2012) Novel inhibitors of nitric oxide synthase with antioxidant properties. Eur J Med Chem;49:118-126.
43. Xia Z.W., Cui W.J., Zhang X.H., Shen Q.X., Wang J., Li Y.Z., Chen S.N., Yu S.C. (2002) Analysis of heme oxygenase isomers in rat. World J Gastroenterol;8:1123-1128.
44. Trakshel G.M., Kutty R.K., 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;260:732-739.
45. Ryter S.W., Kvam E., Tyrrell R.M. (2000) Heme oxygenase activity. Current methods and applications. Methods Mol Biol;99:369-391.
46. Lowry O.H., Rosenbrough N.J., Farr A.J., Randall R.G. (1951) Protein measurement with the Folin phenol reagent. J Biol Chem;193:265-275.
47. Kinobe R.T., Dercho R.A., Vlahakis J.Z., Brien J.F., Szarek W.A., Nakatsu K. (2006) Inhibition of the enzymatic activity of heme oxygenases by azole-based antifungal drugs. J Pharmacol Exp Ther;319:277-284.
48. Beaven G.H., Chen S.H., d'Albis A., Gratzer W.B. (1974) A spectroscopic study of the haemin-human-serum-albumin system. Eur J Biochem;41:539-546.
49. Collier G.S., Pratt J.M., De Wet C.R., Tshabalala C.F. (1979) Studies on haemin in dimethyl sulphoxide/water mixture. Biochem J;179:281-289.
50. Thomsen R., Christensen M.H. (2006) MolDock: a new technique for high-accuracy molecular docking. J Med Chem;49:3315-3321.
51. Schüttelkopf W., van Aalten D.M.F. (2004) PRODRG -a tool for high-throughput crystallography of protein-ligand complexes. Acta Crystallogr;60:1355-1363.
52. Wolber G., Langer T. (2005) LigandScout:3-D pharmacophores derived from protein-bound ligands and their use as virtual screening filters. J Chem Inf Comput Sci;45:160-169.
53. Halgren T.A. (1996) Merck molecular force field. V. Extension of MMFF94 using experimental data, additional computational data and empirical rules. J Comp Chem;17:616-641.
54. Vlahakis J.Z., Rahman M.N., Roman G., Jia Z., Nakatsu K., Szarek W.A. (2011) Rapid, convenient method for screening imidazole-containing compounds for heme oxygenase inhibition. J Pharmacol Toxicol Methods;63:79-88.
55. Hu H.B., Wang W., Han L., Zhou W.P., Zhang X.H. (2007) An improved method for purification of recombinant truncated heme oxygenase-1 by expanded bed adsorption and gel filtration. Bioprocess Biosyst Eng;30:87-90.
56. Vukomanovic D., McLaughlin B., Rahman M.N., Vlahakis J.Z., Roman G., Dercho R.A., Kinobe R.T., Hum M., Brien J.F., Jia Z., Szarek W.A., Nakatsu K. (2010) Recombinant truncated and microsomal heme oxygenase-1 and -2: differential sensitivity to inhibitors. Can J Physiol Pharmacol;88:480-486.
57. Rohrig U.F., Grosdidier A., Zoete V., Michielin O. (2009) Docking to heme proteins. J Comput Chem;30:2305-2315.