Structural insights into human heme oxygenase-1 inhibition by potent and selective azole-based compounds

Journal of the Royal Society Interface

Volumn 10, Issue 78, 2013, Pages

  Rahman, Mona N ^a   Vukomanovic, Dragic ^a   Vlahakis, Jason Z ^a   Szarek, Walter A ^a   Nakatsu, Kanji ^a   Jia, Zongchao ^a  

^a QUEEN S UNIVERSITY   (Canada)

Author keywords

Azole; Heme oxygenase; HO 1; Inhibitor; Structure; X ray crystallography

Indexed keywords

CHEMICAL COMPOUNDS; ISOENZYMES; NITRIC OXIDE; SELF ASSEMBLY; STRUCTURE (COMPOSITION); X RAY CRYSTALLOGRAPHY;

AZOLE; BINDING POCKETS; CYTOCHROMES P450; CYTOPROTECTIVE PROPERTIES; DISEASE STATE; HEME OXYGENASE-1; HEME OXYGENASES; HO-1; INHIBITOR; METALLOPORPHYRINS; NITRIC-OXIDE SYNTHASE; SALIENT FEATURES; SELECTIVE INHIBITORS; SIDE EFFECT; STRUCTURAL BASIS; STRUCTURAL INSIGHTS; STRUCTURAL SIMILARITY; SUBSITES; THERAPEUTIC TARGETS;

PORPHYRINS;

(1 ARYL 2 1H IMIDAZOL 1 YL)ETHANONE DERIVATIVE; (1H 1,2,4 TRIAZOL 1 YL )ETHANONE DERIVATIVE; 1 (1H IMIDAZOL 1 YL) 4,4 DIPHENYL 2 BUTANONE; 1 (ADAMANTAN 1 YL) 2 (1H IMIDAZOL 1 YL)ETHANONE; 2 [2 (4 CHLOROPHENYL)ETHYL] 2 [(1H IMIDAZOL 1 YL)METHYL] 1,3 DIOXOLANE; 2 [2 (4 CHLOROPHENYL)ETHYL] 2 [(1H IMIDAZOL 1 YL)METHYL] 4 METHYL 1,3 DIOXOLANE HYDROCHLORIDE; 2 [2 (4 CHLOROPHENYL)ETHYL] 2 [(1H IMIDAZOL 1 YL)METHYL] 4 [[(5 TRIFLUOROMETHYLPYRIDIN 2 YL)THIO]METHYL] 1,3 DIOXOLANE; 2 [3 (2 PIPERIDIN 1 YL)ETHOXYPHENYL]IMIDAZO[1,2 A]PYRIDINE; 4 PHENYL 1 (1,2,4 1H TRIAZOL 1 YL)BUTAN 2 ONE; 5 (2 HYDROXYPHENYL) 2 METHYLPYRROLIDINE 2,3,4 TRICARBOXYLIC ACID 3,4 DIETHYL ESTER; AZALANSTAT; CYTOCHROME P450; DIETHYLSTILBESTROL; HEME OXYGENASE 1; HEME OXYGENASE INHIBITOR; HOLOENZYME; IMIDAZOLE DERIVATIVE; METALLOPORPHYRIN; NITRIC OXIDE SYNTHASE; PYRROLE DERIVATIVE; UNCLASSIFIED DRUG; ENZYME INHIBITOR; HMOX1 PROTEIN, HUMAN;

ANTINEOPLASTIC ACTIVITY; CELL PROTECTION; DRUG BINDING; DRUG DESIGN; DRUG SELECTIVITY; DRUG STRUCTURE; ENZYME INHIBITION; ENZYME STRUCTURE; HUMAN; NONHUMAN; PLASMODIUM YOELII; PROTEIN INTERACTION; REVIEW; STRUCTURE ACTIVITY RELATION; X RAY CRYSTALLOGRAPHY; ANTAGONISTS AND INHIBITORS; CHEMISTRY; CLASSIFICATION; ENZYME ACTIVE SITE;

AZOLES; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; ENZYME INHIBITORS; HEME OXYGENASE-1; HUMANS; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84871316774     PISSN: 17425689     EISSN: 17425662     Source Type: Journal    
DOI: 10.1098/rsif.2012.0697     Document Type: Review

References (96)

1. Tenhunen R, Marver HS, Schmid R. 1969 Microsomal heme oxygenase. Characterization of the enzyme. J. Biol. Chem. 244, 6388-6394.
2. Maines MD. 1997 The heme oxygenase system: a regulator of second messenger gases. Annu. Rev. Pharmacol. Toxicol. 37, 517-554. (doi:10.1146/annurev.pharmtox.37.1.517)
3. Vreman HJ, Wong RJ, Stevenson DK. 2002 Carbon monoxide and cardiovascular function. Boca Raton, FL: CRC Press.
4. Maines MD. 1988 Heme oxygenase: function, multiplicity, regulatory mechanisms, and clinical applications. FASEB J. 2, 2557-2568.
5. Kinobe RT, Dercho RA, Nakatsu K. 2008 Inhibitors of the heme oxygenase-carbon monoxide system: on the doorstep of the clinic? Can. J. Physiol. Pharmacol. 86, 577-599. (doi:10.1139/Y08-066)
6. Poss KD, Tonegawa S. 1997 Reduced stress defense in heme oxygenase 1-deficient cells. Proc. Natl Acad. Sci. USA 94, 10 925-10 930. (doi:10.1073/pnas.94.20.10925)
7. Poss KD, Tonegawa S. 1997 Heme oxygenase 1 is required for mammalian iron reutilization. Proc. Natl Acad. Sci. USA 94, 10 919-10 924. (doi:10.1073/pnas.94.20.10919)
8. Yachie A, Niida Y, Wada T, Igarashi N, Kaneda H, Toma T, Ohta K, Kasahara Y, Koizumi S. 1999 Oxidative stress causes enhanced endothelial cell injury in human heme oxygenase-1 deficiency. J. Clin. Invest. 103, 129-135. (doi:10.1172/JCI4165)
9. Radhakrishnan N, Yadav SP, Sachdeva A, Pruthi PK, Sawhney S, Piplani T, Wada T, Yachie A. 2011 Human heme oxygenase-1 deficiency presenting with hemolysis, nephritis, and asplenia. J. Pediatr. Hematol. Oncol. 33, 74-78. (doi:10.1097/MPH.0b013e3181fd2aae)
10. Radhakrishnan N, Yadav SP, Sachdeva A, Wada T, Yachie A. 2011 An interesting tetrad of asplenia, inflammation, hemolysis, and nephritis. Pediatr. Hematol. Oncol. 28, 723-726. (doi:10.3109/08880018.2011.613979)
11. Lundvig DM, Immenschuh S, Wagener FA. 2012 Heme oxygenase, inflammation, and fibrosis: the good, the bad, and the ugly? Front. Pharmacol. 3, 81. (doi:10.3389/fphar.2012.00081)
12. Ryter SW, Alam J, Choi AM. 2006 Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications. Physiol. Rev. 86, 583-650. (doi:10.1152/physrev.00011.2005)
13. Lee TS, Chau LY. 2002 Heme oxygenase-1 mediates the anti-inflammatory effect of interleukin-10 in mice. Nat. Med. 8, 240-246. (doi:10.1038/nm0302-240)
14. 2. J. Biol. Chem. 278, 19 325-19 330. (doi:10.1074/jbc.M300498200)
15. 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. (doi:10.1089/ars.2006.1519)
16. Stone JR, Marletta MA. 1994 Soluble guanylate cyclase from bovine lung: activation with nitric oxide and carbon monoxide and spectral characterization of the ferrous and ferric states. Biochemistry 33, 5636-5640. (doi:10.1021/bi00184a036)
17. Furchgott RF, Jothianandan D. 1991 Endothelium-dependent and -independent vasodilation involving cyclic GMP: relaxation induced by nitric oxide, carbon monoxide and light. Blood Vessels 28, 52-61.
18. Wang R, Wu L, Wang Z. 1997 The direct effect of carbon monoxide on KCa channels in vascular smooth muscle cells. Pflugers Arch. 434, 285-291. (doi:10.1007/s004240050398)
19. Otterbein LE, Bach FH, Alam J, Soares M, Tao LH, Wysk M, Davis RJ, Flavell RA. 2000 Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway. Nat. Med. 6, 422-428. (doi:10.1038/74680)
20. Amersi F et al. 2002 Ex vivo exposure to carbon monoxide prevents hepatic ischemia/reperfusion injury through p38 MAP kinase pathway. Hepatology 35, 815-823. (doi:10.1053/jhep.2002.32467)
21. Ryter SW, Choi AM. 2005 Heme oxygenase-1: redox regulation of a stress protein in lung and cell culture models. Antioxid. Redox Signal. 7, 80-91. (doi:10.1089/ars.2005.7.80)
22. Wu L, Wang R. 2005 Carbon monoxide: endogenous production, physiological functions, and pharmacological applications. Pharmacol. Rev. 57, 585-630. (doi:10.1124/pr.57.4.3)
23. Farrera JA, Jauma A, Ribo JM, Peire MA, Parellada PP, Roques-Choua S, Bienvenue E, Seta P. 1994 The antioxidant role of bile pigments evaluated by chemical tests. Bioorg. Med. Chem. 2, 181-185. (doi:10.1016/S0968-0896(00)82013- 1)
24. Stocker R, Yamamoto Y, McDonagh AF, Glazer AN, Ames BN. 1987 Bilirubin is an antioxidant of possible physiological importance. Science 235, 1043-1046. (doi:10.1126/science.3029864)
25. Stocker R, Peterhans E. 1989 Antioxidant properties of conjugated bilirubin and biliverdin: biologically relevant scavenging of hypochlorous acid. Free Radic. Res. Commun. 6, 57-66. (doi:10.3109/10715768909073428)
26. Wagner JR, Motchnik PA, Stocker R, Sies H, Ames BN. 1993 The oxidation of blood plasma and low density lipoprotein components by chemically generated singlet oxygen. J. Biol. Chem. 268, 18 502-18 506.
27. Kaur H, Hughes MN, Green CJ, Naughton P, Foresti R, Motterlini R. 2003 Interaction of bilirubin and biliverdin with reactive nitrogen species. FEBS Lett. 543, 113-119. (doi:10.1016/S0014-5793(03)00420-4)
28. Halliwell B, Gutteridge JM. 1992 Biologically relevant metal ion-dependent hydroxyl radical generation: an update. FEBS Lett. 307, 108-112. (doi:10.1016/0014-5793(92)80911-Y)
29. Balla J, Jacob HS, Balla G, Nath K, Eaton JW, Vercellotti GM. 1993 Endothelial-cell heme uptake from heme proteins: induction of sensitization and desensitization to oxidant damage. Proc. Natl Acad. Sci. USA 90, 9285-9289. (doi:10.1073/pnas.90.20.9285)
30. Vile GF, Basu-Modak S, Waltner C, Tyrrell RM. 1994 Heme oxygenase 1 mediates an adaptive response to oxidative stress in human skin fibroblasts. Proc. Natl Acad. Sci. USA 91, 2607-2610. (doi:10.1073/pnas.91.7.2607)
31. Bilban M, Haschemi A, Wegiel B, Chin BY, Wagner O, Otterbein LE. 2008 Heme oxygenase and carbon monoxide initiate homeostatic signaling. J. Mol. Med. (Berl.) 86, 267-279. (doi:10.1007/s00109-007-0276-0)
32. Vile GF, Tyrrell RM. 1993 Oxidative stress resulting from ultraviolet A irradiation of human skin fibroblasts leads to a heme oxygenase-dependent increase in ferritin. J. Biol. Chem. 268, 14 678-14 681.
33. Vogt BA, Alam J, Croatt AJ, Vercellotti GM, Nath KA. 1995 Acquired resistance to acute oxidative stress. Possible role of heme oxygenase and ferritin. Lab. Invest. 72, 474-483.
34. Hentze MW, Kuhn LC. 1996 Molecular control of vertebrate iron metabolism: mRNA-based regulatory circuits operated by iron, nitric oxide, and oxidative stress. Proc. Natl Acad. Sci. USA 93, 8175-8182. (doi:10.1073/pnas.93.16.8175)
35. Domachowske JB. 1997 The role of nitric oxide in the regulation of cellular iron metabolism. Biochem. Mol. Med. 60, 1-7. (doi:10.1006/bmme.1996. 2557)
36. Abraham NG, Kappas A. 2008 Pharmacological and clinical aspects of heme oxygenase. Pharmacol. Rev. 60, 79-127. (doi:10.1124/pr.107.07104)
37. Loboda A, Jazwa A, Grochot-Przeczek A, Rutkowski AJ, Cisowski J, Agarwal A, Jozkowicz A, Dulak J. 2008 Heme oxygenase-1 and the vascular bed: from molecular mechanisms to therapeutic opportunities. Antioxid. Redox Signal. 10, 1767-1812. (doi:10.1089/ars.2008.2043)
38. Hill M et al. 2005 Heme oxygenase-1 inhibits rat and human breast cancer cell proliferation: mutual cross inhibition with indoleamine 2,3-dioxygenase. FASEB J. 19, 1957-1968. (doi:10.1096/fj.05-3875com)
39. Yanagawa T, Omura K, Harada H, Nakaso K, Iwasa S, Koyama Y, Onizawa K, Yusa H, Yoshida H. 2004 Heme oxygenase-1 expression predicts cervical lymph node metastasis of tongue squamous cell carcinomas. Oral Oncol. 40, 21-27. (doi:10.1016/S1368-8375(03)00128-3)
40. Maines MD, Abrahamsson PA. 1996 Expression of heme oxygenase-1 (HSP32) in human prostate: normal, hyperplastic, and tumor tissue distribution. Urology 47, 727-733. (doi:10.1016/S0090-4295(96)00010-6)
41. Berberat PO et al. 2005 Inhibition of heme oxygenase-1 increases responsiveness of pancreatic cancer cells to anticancer treatment. Clin. Cancer Res. 11, 3790-3798. (doi:10.1158/1078-0432.CCR-04-2159)
42. Nowis D et al. 2006 Heme oxygenase-1 protects tumor cells against photodynamic therapy-mediated cytotoxicity. Oncogene 25, 3365-3374. (doi:10.1038/sj.onc.1209378)
43. 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. (doi:10.1023/B:APPT.0000012119.83734.4e)
44. Dulak J et al. 2002 Heme oxygenase activity modulates vascular endothelial growth factor synthesis in vascular smooth muscle cells. Antioxid. Redox Signal. 4, 229-240. (doi:10.1089/152308602753666280)
45. Jozkowicz A, Dulak J. 2003 Effects of protoporphyrins on production of nitric oxide and expression of vascular endothelial growth factor in vascular smooth muscle cells and macrophages. Acta Biochim. Pol. 50, 69-79. (Pubitemid 37034229)
46. Jozkowicz A, Huk I, Nigisch A, Weigel G, Dietrich W, Motterlini R, Dulak J. 2003 Heme oxygenase and angiogenic activity of endothelial cells: stimulation by carbon monoxide and inhibition by tin protoporphyrin-IX. Antioxid. Redox Signal. 5, 155-162. (doi:10.1089/152308603764816514)
47. Li VG, Sacerdoti D, Sangras B, Vanella A, Mezentsev A, Scapagnini G, Falck JR, Abraham NG. 2005 Carbon monoxide signaling in promoting angiogenesis in human microvessel endothelial cells. Antioxid. Redox Signal. 7, 704-710. (doi:10.1089/ars.2005.7.704)
48. Deshane J et al. 2007 Stromal cell-derived factor promotes angiogenesis via a heme oxygenase 1-dependent mechanism. J. Exp. Med. 204, 605-618. (doi:10.1084/jem.20061609)
49. Wong RJ, Vreman HJ, Schulz S, Kalish FS, Pierce NW, Stevenson DK. 2011 In vitro inhibition of heme oxygenase isoenzymes by metalloporphyrins. J. Perinatol. 31(Suppl. 1), S35-S41. (doi:10.1038/jp.2010.173)
50. Fang J, Sawa T, Akaike T, Akuta T, Sahoo SK, 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. (Pubitemid 36793037)
51. 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. (doi:10.1002/ijc.11644)
52. Luo D, Vincent SR. 1994 Metalloporphyrins inhibit nitric oxide-dependent cGMP formation in vivo. Eur. J. Pharmacol. 267, 263-267. (doi:10.1016/0922- 4106(94)90149-X)
53. Meffert MK, Haley JE, Schuman EM, Schulman H, Madison DV. 1994 Inhibition of hippocampal heme oxygenase, nitric oxide synthase, and long-term potentiation by metalloporphyrins. Neuron 13, 1225-1233. (doi:10.1016/0896- 6273(94)90060-4)
54. Grundemar L, Ny L. 1997 Pitfalls using metalloporphyrins in carbon monoxide research. Trends Pharmacol. Sci. 18, 193-195. (doi:10.1016/S0165- 6147(97)01065-1)
55. Appleton SD, Chretien ML, McLaughlin BE, Vreman HJ, Stevenson DK, Brien JF, Nakatsu K, Maurice DH, Marks GS. 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, 1214-1219. (Pubitemid 29463610)
56. Hayashi S, Omata Y, Sakamoto H, Higashimoto Y, Hara T, Sagara Y, Noguchi M. 2004 Characterization of rat heme oxygenase-3 gene. Implication of processed pseudogenes derived from heme oxygenase-2 gene. Gene 336, 241-250. (doi:10.1016/j.gene.2004.04.002)
57. Schrödinger LLC. 2011 PyMOL molecular graphics system, version 1.5.0.4. See http://pymol.org/.
58. Bianchetti CM, Yi L, Ragsdale SW, Phillips Jr GN. 2007 Comparison of apo- and heme-bound crystal structures of a truncated human heme oxygenase-2. J. Biol. Chem. 282, 37 624-37 631. (doi:10.1074/jbc.M707396200)
59. Schuller DJ, Wilks A, Ortiz de Montellano PR, Poulos TL. 1998 Crystallization of recombinant human heme oxygenase-1. Protein Sci. 7, 1836-1838. (doi:10.1002/pro.5560070820)
60. Schuller DJ, Wilks A, Ortiz de Montellano PR, Poulos TL. 1999 Crystal structure of human heme oxygenase-1. Nat. Struct. Biol. 6, 860-867. (doi:10.1038/12319)
61. Lad L, Schuller DJ, Shimizu H, Friedman J, Li H, Ortiz de Montellano PR, Poulos TL. 2003 Comparison of the heme-free and -bound crystal structures of human heme oxygenase-1. J. Biol. Chem. 278, 7834-7843. (doi:10.1074/jbc. M211450200)
62. Qi Z, Hamza I, O'Brian MR. 1999 Heme is an effector molecule for iron-dependent degradation of the bacterial iron response regulator (Irr) protein. Proc. Natl Acad. Sci. USA 96, 13 056-13 061. (doi:10.1073/pnas.96.23. 13056)
63. Huang TJ, McCoubrey Jr WK, Maines MD. 2001 Heme oxygenase-2 interaction with metalloporphyrins: function of heme regulatory motifs. Antioxid. Redox Signal. 3, 685-696. (doi:10.1089/15230860152543023)
64. Yi L, Ragsdale SW. 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, 21 056-21 067. (doi:10.1074/jbc.M700664200)
65. Yi L, Jenkins PM, Leichert LI, Jakob U, Martens JR, Ragsdale SW. 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, 20 556-20 561. (doi:10.1074/jbc.M109.015651)
66. Gardner JD, Yi L, Ragsdale SW, Brunold TC. 2010 Spectroscopic insights into axial ligation and active-site H-bonding in substrate-bound human heme oxygenase-2. J. Biol. Inorg. Chem. 15, 1117-1127. (doi:10.1007/s00775-010-0672- 8)
67. Cuturi MC, Christoph F, Woo J, Iyer S, Brouard S, Heslan JM, Pignon P, Soulillou JP, Buelow R. 1999 RDP1258, a new rationally designed immunosuppressive peptide, prolongs allograft survival in rats: analysis of its mechanism of action. Mol. Med. 5, 820-832. (Pubitemid 32937041)
68. Srivastava P, Pandey VC, Misra AP, Gupta P, Raj K, Bhaduri AP. 1998 Potential inhibitors of plasmodial heme oxygenase; an innovative approach for combating chloroquine resistant malaria. Bioorg. Med. Chem. 6, 181-187. (doi:10.1016/S0968-0896(97)10013-X)
69. Vlahakis JZ, Kinobe RT, Bowers RJ, Brien JF, Nakatsu K, Szarek WA. 2005 Synthesis and evaluation of azalanstat analogues as heme oxygenase inhibitors. Bioorg. Med. Chem. Lett. 15, 1457-1461. (doi:10.1016/j.bmcl.2004.12.075)
70. Kinobe RT, Ji Y, Vlahakis JZ, Motterlini R, Brien JF, Szarek WA, Nakatsu K. 2007 Effectiveness of novel imidazole-dioxolane heme oxygenase inhibitors in renal proximal tubule epithelial cells. J. Pharmacol. Exp. Ther. 323, 763-770. (doi:10.1124/jpet.107.119800)
71. Kinobe RT, Vlahakis JZ, Vreman HJ, Stevenson DK, Brien JF, Szarek WA, Nakatsu K. 2006 Selectivity of imidazole-dioxolane compounds for in vitro inhibition of microsomal haem oxygenase isoforms. Br. J. Pharmacol. 147, 307-315. (doi:10.1038/sj.bjp.0706555)
72. Vlahakis JZ, Kinobe RT, Bowers RJ, Brien JF, Nakatsu K, Szarek WA. 2006 Imidazole-dioxolane compounds as isozyme-selective heme oxygenase inhibitors. J. Med. Chem. 49, 4437-4441. (doi:10.1021/jm0511435)
73. Wilkinson S, Chodak G. 2004 An evaluation of intermediate-dose ketoconazole in hormone refractory prostate cancer. Eur. Urol. 45, 581-584. (doi:10.1016/j.eururo.2003.11.031)
74. Kinobe RT, Dercho RA, Vlahakis JZ, Brien JF, Szarek WA, Nakatsu K. 2006 Inhibition of the enzymatic activity of heme oxygenases by azole-based antifungal drugs. J. Pharmacol. Exp. Ther. 319, 277-284. (doi:10.1124/jpet.106. 102699)
75. Roman G, Riley JG, Vlahakis JZ, Kinobe RT, Brien JF, Nakatsu K, Szarek WA. 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, 3225-3234. (doi:10.1016/j.bmc.2007.02.034)
76. Sugishima M, Higashimoto Y, Oishi T, Takahashi H, Sakamoto H, Noguchi M, Fukuyama K. 2007 X-ray crystallographic and biochemical characterization of the inhibitory action of an imidazole-dioxolane compound on heme oxygenase. Biochemistry 46, 1860-1867. (doi:10.1021/bi062264p)
77. Rahman MN, Vlahakis JZ, Szarek WA, Nakatsu K, 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, 5943-5952. (doi:10.1021/jm800505m)
78. Sorrenti V, Guccione S, Di GC, Modica MN, Pittala V, Acquaviva R, Basile L, Pappalardo M, Salerno L. In press. Evaluation of imidazole-based compounds as heme oxygenase-1 inhibitors. Chem. Biol. Drug Des. (doi:10.1111/cbdd.12015)
79. Collaborative Computational Project N4. 1994 The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D 50, 760-763. (doi:10.1107/ S0907444994003112)
80. Rahman MN, Vlahakis JZ, Vukomanovic D, Szarek WA, Nakatsu K, Jia Z. 2009 X-ray crystal 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, 4946-4950. (doi:10.1021/jm900434f)
81. Roman G, Rahman MN, Vukomanovic D, Jia Z, Nakatsu K, Szarek WA. 2010 Heme oxygenase inhibition by 2-oxy-substituted 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, 68-90. (doi:10.1111/j.1747-0285.2009.00909.x)
82. Vlahakis JZ, Lazar C, Roman G, Vukomanovic D, Nakatsu K, Szarek WA. 2012 Heme oxygenase inhibition by α-(1H-Imidazol-1-yl)-ω-phenylalkanes: effect of introduction of heteroatoms in the alkyl linker. ChemMedChem 16, 897-902. (doi:10.1002/cmdc.201100602)
83. Sun J, Wilks A, Ortiz de Montellano PR, Loehr TM. 1993 Resonance Raman and EPR spectroscopic studies on heme-heme oxygenase complexes. Biochemistry 32, 14 151-14 157. (doi:10.1021/bi00214a012)
84. Sun J, Loehr TM, Wilks A, Ortiz de Montellano PR. 1994 Identification of histidine 25 as the heme ligand in human liver heme oxygenase. Biochemistry 33, 13 734-13 740. (doi:10.1021/bi00250a026)
85. Roman G, Vlahakis JZ, Vukomanovic D, Nakatsu K, Szarek WA. 2010 Heme oxygenase inhibition by 1-aryl-2-(1H-imidazol-1-yl/1H-1,2,4-triazol-1-yl) ethanones and their derivatives. ChemMedChem 5, 1541-1555. (doi:10.1002/cmdc. 201000120)
86. Hum M, McLaughlin BE, Roman G, Vlahakis JZ, Szarek WA, Nakatsu K. 2010 The effects of azole-based heme oxygenase inhibitors on rat cytochromes P450 2E1 and 3A1/2 and human cytochromes P450 3A4 and 2D6. J. Pharmacol. Exp. Ther. 334, 981-987. (doi:10.1124/jpet.110.168492)
87. Vlahakis JZ, Hum M, Rahman MN, Jia Z, Nakatsu K, Szarek WA. 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. (doi:10.1016/j.bmc.2009.01.078)
88. Rahman MN, Vlahakis JZ, Vukomanovic D, Lee W, Szarek WA, Nakatsu K, Jia Z, Uversky VN. 2012 A novel, 'double-clamp' binding mode for human heme oxygenase-1 inhibition. PLoS ONE 7, e29514. (doi:10.1371/journal.pone.0029514)
89. Alaoui-Jamali MA et al. 2009 A novel experimental heme oxygenase-1-targeted therapy for hormone-refractory prostate cancer. Cancer Res. 69, 8017-8024. (doi:10.1158/0008-5472.CAN-09-0419)
90. Di Francesco L et al. 2009 Induction of prostacyclin by steady laminar shear stress suppresses tumor necrosis factor-α biosynthesis via heme oxygenase-1 in human endothelial cells. Circ. Res. 104, 506-513. (doi:10.1161/CIRCRESAHA.108.191114)
91. Csongradi E, Storm MV, Stec DE. 2012 Renal inhibition of heme oxygenase-1 increases blood pressure in angiotensin II-dependent hypertension. Int. J. Hypertens. 2012, 497213. (doi:10.1155/2012/497213)
92. Vukomanovic D et al. 2010 Recombinant truncated and microsomal heme oxygenase-1 and -2: differential sensitivity to inhibitors. Can. J. Physiol. Pharmacol. 88, 480-486. (doi:10.1139/Y10-004)
93. Huber III WJ, Marohnic CC, Peters M, Alam J, Reed JR, Masters BS, Backes WL. 2009 Measurement of membrane-bound human heme oxygenase-1 activity using a chemically defined assay system. Drug Metab. Dispos. 37, 857-864. (doi:10.1124/dmd.108.025023)
94. Huber III WJ, Scruggs BA, Backes WL. 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. (doi:10.1021/ bi801912z)
95. Huber III WJ, Backes WL. 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, 12 212-12 219. (doi:10.1021/bi701496z)
96. Taira J, Sugishima M, Kida Y, Oda E, Noguchi M, Higashimoto Y. 2011 Caveolin-1 is a competitive inhibitor of heme oxygenase-1 (HO-1) with heme: identification of a minimum sequence in caveolin-1 for binding to HO-1. Biochemistry 50, 6824-6831. (doi:10.1021/bi200601t)