Ebselen and congeners inhibit NADPH oxidase 2-dependent superoxide generation by interrupting the binding of regulatory subunits

Chemistry and Biology

Volumn 19, Issue 6, 2012, Pages 752-763

  Smith, Susan M E ^a   Min, Jaeki ^b   Ganesh, Thota ^b   Diebold, Becky ^a   Kawahara, Tsukasa ^a   Zhu, Yerun ^a   McCoy, James ^a   Sun, Aiming ^b   Snyder, James P ^b   Fu, Haian ^a   Du, Yuhong ^a   Lewis, Iestyn ^a   Lambeth, J David ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Department of Chemistry   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EBSELEN; OXIDOREDUCTASE INHIBITOR; PROTEIN P22; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CHEMICAL STRUCTURE; CONGENER; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; FLUORESCENCE POLARIZATION; HIGH THROUGHPUT SCREENING; IN VIVO STUDY; INFLAMMATORY DISEASE; MOUSE; NONHUMAN; PROCESS OPTIMIZATION; PROTEIN DOMAIN; STRUCTURE ACTIVITY RELATION;

AZOLES; BINDING SITES; CELL SURVIVAL; DOSE-RESPONSE RELATIONSHIP, DRUG; HIGH-THROUGHPUT SCREENING ASSAYS; HUMANS; ISOENZYMES; MEMBRANE GLYCOPROTEINS; MOLECULAR STRUCTURE; NADPH OXIDASE; NEUTROPHILS; ORGANOSELENIUM COMPOUNDS; RECOMBINANT PROTEINS; STRUCTURE-ACTIVITY RELATIONSHIP; SUPEROXIDES;

EID: 84862743816     PISSN: 10745521     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chembiol.2012.04.015     Document Type: Article

References (82)

1. B.M. Babior, J.D. Lambeth, and W. Nauseef The neutrophil NADPH oxidase Arch. Biochem. Biophys. 397 2002 342 344
2. B. Banfi, G. Molinar, A. Maturana, K. Steger, B. Hegedus, N. Demaurex, and K.-H. Krause A Ca2+-activated NADPH oxidase in testis, spleen and lymph nodes J. Biol. Chem. 276 2001 27637594 27637601
3. B. Bánfi, R.A. Clark, K. Steger, and K.H. Krause Two novel proteins activate superoxide generation by the NADPH oxidase NOX1 J. Biol. Chem. 278 2003 3510 3513
4. B. Bánfi, B. Malgrange, J. Knisz, K. Steger, M. Dubois-Dauphin, and K.H. Krause NOX3, a superoxide-generating NADPH oxidase of the inner ear J. Biol. Chem. 279 2004 46065 46072
5. S. Carnesecchi, C. Deffert, Y. Donati, O. Basset, B. Hinz, O. Preynat-Seauve, C. Guichard, J.L. Arbiser, B. Banfi, and J.C. Pache A key role for NOX4 in epithelial cell death during development of lung fibrosis Antioxid. Redox Signal. 15 2011 607 619
6. T.C. Chang, M.L. Huang, W.L. Hsu, J.M. Hwang, and L.Y. Hsu Synthesis and biological evaluation of ebselen and its acyclic derivatives Chem. Pharm. Bull. (Tokyo) 51 2003 1413 1416
7. G. Cheng, and J.D. Lambeth NOXO1, regulation of lipid binding, localization, and activation of Nox1 by the Phox homology (PX) domain J. Biol. Chem. 279 2004 4737 4742
8. G. Cheng, Z. Cao, X. Xu, E.G. van Meir, and J.D. Lambeth Homologs of gp91phox: cloning and tissue expression of Nox3, Nox4, and Nox5 Gene 269 2001 131 140
9. G. Cheng, D. Ritsick, and J.D. Lambeth Nox3 regulation by NOXO1, p47phox, and p67phox J. Biol. Chem. 279 2004 34250 34255
10. A. Correa, I. Tellitu, E. Domínguez, and R. SanMartin Novel alternative for the N-S bond formation and its application to the synthesis of benzisothiazol-3-ones Org. Lett. 8 2006 4811 4813
11. I.A. Cotgreave, S.K. Duddy, G.E. Kass, D. Thompson, and P. Moldéus Studies on the anti-inflammatory activity of ebselen. Ebselen interferes with granulocyte oxidative burst by dual inhibition of NADPH oxidase and protein kinase C? Biochem. Pharmacol. 38 1989 649 656
12. J.T. Curnutte, R. Kuver, and B.M. Babior Activation of the respiratory burst oxidase in a fully soluble system from human neutrophils J. Biol. Chem. 262 1987 6450 6452
13. I. Dahan, I. Issaeva, Y. Gorzalczany, N. Sigal, M. Hirshberg, and E. Pick Mapping of functional domains in the p22(phox) subunit of flavocytochrome b(559) participating in the assembly of the NADPH oxidase complex by "peptide walking" J. Biol. Chem. 277 2002 8421 8432
14. X. De Deken, D. Wang, M.C. Many, S. Costagliola, F. Libert, G. Vassart, J.E. Dumont, and F. Miot Cloning of two human thyroid cDNAs encoding new members of the NADPH oxidase family J. Biol. Chem. 275 2000 23227 23233
15. I. de Mendez, A.G. Adams, R.A. Sokolic, H.L. Malech, and T.L. Leto Multiple SH3 domain interactions regulate NADPH oxidase assembly in whole cells EMBO J. 15 1996 1211 1220
16. I. de Mendez, N. Homayounpour, and T.L. Leto Specificity of p47phox SH3 domain interactions in NADPH oxidase assembly and activation Mol. Cell. Biol. 17 1997 2177 2185
17. K. Dohi, H. Ohtaki, T. Nakamachi, S. Yofu, K. Satoh, K. Miyamoto, D. Song, S. Tsunawaki, S. Shioda, and T. Aruga Gp91phox (NOX2) in classically activated microglia exacerbates traumatic brain injury J. Neuroinflammation 7 2010 41
18. K. Ebisu, T. Nagasawa, K. Watanabe, K. Kakinuma, K. Miyano, and M. Tamura Fused p47phox and p67phox truncations efficiently reconstitute NADPH oxidase with higher activity and stability than the individual components J. Biol. Chem. 276 2001 24498 24505
19. M.M. Elahi, Y.X. Kong, and B.M. Matata Oxidative stress as a mediator of cardiovascular disease Oxid. Med. Cell. Longev. 2 2009 259 269
20. E.E. Essick, and F. Sam Oxidative stress and autophagy in cardiac disease, neurological disorders, aging and cancer Oxid. Med. Cell. Longev. 3 2010 168 177
21. A.A. Fatokun, T.W. Stone, and R.A. Smith Oxidative stress in neurodegeneration and available means of protection Front. Biosci. 13 2008 3288 3311
22. G. Gavazzi, B. Banfi, C. Deffert, L. Fiette, M. Schappi, F. Herrmann, and K.H. Krause Decreased blood pressure in NOX1-deficient mice FEBS Lett. 580 2006 497 504
23. M. Geiszt, J.B. Kopp, P. Várnai, and T.L. Leto Identification of renox, an NAD(P)H oxidase in kidney Proc. Natl. Acad. Sci. USA 97 2000 8010 8014
24. D. Gianni, N. Taulet, H. Zhang, C. DerMardirossian, J. Kister, L. Martinez, W.R. Roush, S.J. Brown, G.M. Bokoch, and H. Rosen A novel and specific NADPH oxidase-1 (Nox1) small-molecule inhibitor blocks the formation of functional invadopodia in human colon cancer cells ACS Chem. Biol. 5 2010 981 993
25. Y. Gorin, K. Block, J. Hernandez, B. Bhandari, B. Wagner, J.L. Barnes, and H.E. Abboud Nox4 NAD(P)H oxidase mediates hypertrophy and fibronectin expression in the diabetic kidney J. Biol. Chem. 280 2005 39616 39626
26. H. Grasberger, and S. Refetoff Identification of the maturation factor for dual oxidase. Evolution of an eukaryotic operon equivalent J. Biol. Chem. 281 2006 18269 18272
27. Y. Groemping, K. Lapouge, S.J. Smerdon, and K. Rittinger Molecular basis of phosphorylation-induced activation of the NADPH oxidase Cell 113 2003 343 355
28. L. Hecker, R. Vittal, T. Jones, R. Jagirdar, T.R. Luckhardt, J.C. Horowitz, S. Pennathur, F.J. Martinez, and V.J. Thannickal NADPH oxidase-4 mediates myofibroblast activation and fibrogenic responses to lung injury Nat. Med. 15 2009 1077 1081
29. Y. Imai, K. Kuba, G.G. Neely, R. Yaghubian-Malhami, T. Perkmann, G. van Loo, M. Ermolaeva, R. Veldhuizen, Y.H. Leung, and H. Wang Identification of oxidative stress and Toll-like receptor 4 signaling as a key pathway of acute lung injury Cell 133 2008 235 249
30. D. Jagnandan, J.E. Church, B. Banfi, D.J. Stuehr, M.B. Marrero, and D.J. Fulton Novel mechanism of activation of NADPH oxidase 5(NOX5): Calcium-sensitization via phosphorylation J. Biol. Chem. 282 2007 6494 6507
31. V. Jaquet, L. Scapozza, R.A. Clark, K.H. Krause, and J.D. Lambeth Small-molecule NOX inhibitors: ROS-generating NADPH oxidases as therapeutic targets Antioxid. Redox Signal. 11 2009 2535 2552
32. N. Kashihara, Y. Haruna, V.K. Kondeti, and Y.S. Kanwar Oxidative stress in diabetic nephropathy Curr. Med. Chem. 17 2010 4256 4269
33. T. Kawahara, D. Ritsick, G. Cheng, and J.D. Lambeth Point mutations in the proline-rich region of p22phox are dominant inhibitors of Nox1- and Nox2-dependent reactive oxygen generation J. Biol. Chem. 280 2005 31859 31869
34. T. Kawahara, H.M. Jackson, S.M. Smith, P.D. Simpson, and J.D. Lambeth Nox5 forms a functional oligomer mediated by self-association of its dehydrogenase domain Biochemistry 50 2011 2013 2025
35. B. Laleu, F. Gaggini, M. Orchard, L. Fioraso-Cartier, L. Cagnon, S. Houngninou-Molango, A. Gradia, G. Duboux, C. Merlot, and F. Heitz First in class, potent, and orally bioavailable NADPH oxidase isoform 4 (Nox4) inhibitors for the treatment of idiopathic pulmonary fibrosis J. Med. Chem. 53 2010 7715 7730
36. J.D. Lambeth NOX enzymes and the biology of reactive oxygen Nat. Rev. Immunol. 4 2004 181 189
37. J.D. Lambeth Nox enzymes, ROS, and chronic disease: an example of antagonistic pleiotropy Free Radic. Biol. Med. 43 2007 332 347
38. J.D. Lambeth, G. Cheng, R.S. Arnold, and W.A. Edens Novel homologs of gp91phox Trends Biochem. Sci. 25 2000 459 461
39. J.D. Lambeth, T. Kawahara, and B. Diebold Regulation of Nox and Duox enzymatic activity and expression Free Radic. Biol. Med. 43 2007 319 331
40. J.D. Lambeth, K.H. Krause, and R.A. Clark NOX enzymes as novel targets for drug development Semin. Immunopathol. 30 2008 339 363
41. B. Lassègue, D. Sorescu, K. Szöcs, Q. Yin, M. Akers, Y. Zhang, S.L. Grant, J.D. Lambeth, and K.K. Griendling Novel gp91(phox) homologues in vascular smooth muscle cells: nox1 mediates angiotensin II-induced superoxide formation and redox-sensitive signaling pathways Circ. Res. 88 2001 888 894
42. T. Leto, A. Adams, and I. de Mendez Assembly of the phagocyte NADPH oxidase: binding of Src homology 3 domains to proline-rich targets Proc. Natl. Acad. Sci. U.S.A. 1994 9110650-10654
43. R. Leurs, H. Timmerman, and A. Bast Inhibition of superoxide anion radical production by ebselen (PZ51) and its sulfur analogue (PZ25) in guinea pig alveolar macrophages Biochem. Int. 18 1989 295 299
44. 558 of the human NADPH oxidase leading to defective translocation of the cytosolic proteins p47-phox and p67-phox J. Clin. Invest. 93 1994 2120 2126
45. S. Luxen, D. Noack, M. Frausto, S. Davanture, B.E. Torbett, and U.G. Knaus Heterodimerization controls localization of Duox-DuoxA NADPH oxidases in airway cells J. Cell Sci. 122 2009 1238 1247
46. K. Matsuno, H. Yamada, K. Iwata, D. Jin, M. Katsuyama, M. Matsuki, S. Takai, K. Yamanishi, M. Miyazaki, H. Matsubara, and C. Yabe-Nishimura Nox1 is involved in angiotensin II-mediated hypertension: a study in Nox1-deficient mice Circulation 112 2005 2677 2685
47. B. Mishra, K.I. Priyadarsini, H. Mohan, and G. Mugesh Horseradish peroxidase inhibition and antioxidant activity of ebselen and related organoselenium compounds Bioorg. Med. Chem. Lett. 16 2006 5334 5338
48. A. Müller, E. Cadenas, P. Graf, and H. Sies A novel biologically active seleno-organic compound - I. Glutathione peroxidase-like activity in vitro and antioxidant capacity of PZ 51 (Ebselen) Biochem. Pharmacol. 33 1984 3235 3239
49. National Center for Biotechnology Information. N. PubChem BioAssay Database; AID=1274; AID-1275. http://www.ncbi.nlm.nih.gov/sites/entrez?db= pcassay&term=1274.
50. H. Ouertatani-Sakouhi, F. El-Turk, B. Fauvet, M.K. Cho, D. Pinar Karpinar, D. Le Roy, M. Dewor, T. Roger, J. Bernhagen, and T. Calandra Identification and characterization of novel classes of macrophage migration inhibitory factor (MIF) inhibitors with distinct mechanisms of action J. Biol. Chem. 285 2010 26581 26598
51. M.H. Paclet, S. Berthier, L. Kuhn, J. Garin, and F. Morel Regulation of phagocyte NADPH oxidase activity: identification of two cytochrome b558 activation states FASEB J. 21 2007 1244 1255
52. H.S. Park, S.R. Kim, and Y.C. Lee Impact of oxidative stress on lung diseases Respirology 14 2009 27 38
53. L. Park, P. Zhou, R. Pitstick, C. Capone, J. Anrather, E.H. Norris, L. Younkin, S. Younkin, G. Carlson, B.S. McEwen, and C. Iadecola Nox2-derived radicals contribute to neurovascular and behavioral dysfunction in mice overexpressing the amyloid precursor protein Proc. Natl. Acad. Sci. USA 105 2008 1347 1352
54. C.A. Parkos, R.A. Allen, C.G. Cochrane, and A.J. Jesaitis Purified cytochrome b from human granulocyte plasma membrane is comprised of two polypeptides with relative molecular weights of 91,000 and 22,000 J. Clin. Invest. 80 1987 732 742
55. M.J. Parnham Biological activities and clinical potential of Ebselen Adv. Exp. Med. Biol. 264 1990 193 197
56. M.J. Parnham, and E. Graf Seleno-organic compounds and the therapy of hydroperoxide-linked pathological conditions Biochem. Pharmacol. 36 1987 3095 3102
57. M. Parnham, and H. Sies Ebselen: prospective therapy for cerebral ischaemia Expert Opin. Investig. Drugs 9 2000 607 619
58. M.J. Parnham, S. Leyck, E. Graf, E.J. Dowling, and D.R. Blake The pharmacology of ebselen Agents Actions 32 1991 4 9
59. M.T. Quinn, T. Evans, L.R. Loetterle, A.J. Jesaitis, and G.M. Bokoch Translocation of Rac correlates with NADPH oxidase activation. Evidence for equimolar translocation of oxidase components J. Biol. Chem. 268 1993 20983 20987
60. D.R. Ritsick, W.A. Edens, V. Finnerty, and J.D. Lambeth Nox regulation of smooth muscle contraction Free Radic. Biol. Med. 43 2007 31 38
61. T. Schewe Molecular actions of ebselen - an antiinflammatory antioxidant Gen. Pharmacol. 26 1995 1153 1169
62. C. Schewe, T. Schewe, and A. Wendel Strong inhibition of mammalian lipoxygenases by the antiinflammatory seleno-organic compound ebselen in the absence of glutathione Biochem. Pharmacol. 48 1994 65 74
63. M. Sedeek, G. Callera, A. Montezano, A. Gutsol, F. Heitz, C. Szyndralewiez, P. Page, C.R. Kennedy, K.D. Burns, R.M. Touyz, and R.L. Hébert Critical role of Nox4-based NADPH oxidase in glucose-induced oxidative stress in the kidney: implications in type 2 diabetic nephropathy Am. J. Physiol. Renal Physiol. 299 2010 F1348 F1358
64. J. Shi, C.R. Ross, T.L. Leto, and F. Blecha PR-39, a proline-rich antibacterial peptide that inhibits phagocyte NADPH oxidase activity by binding to Src homology 3 domains of p47 phox Proc. Natl. Acad. Sci. USA 93 1996 6014 6018
65. N. Shimohashi, M. Nakamuta, K. Uchimura, R. Sugimoto, H. Iwamoto, M. Enjoji, and H. Nawata Selenoorganic compound, ebselen, inhibits nitric oxide and tumor necrosis factor-alpha production by the modulation of jun-N-terminal kinase and the NF-kappab signaling pathway in rat Kupffer cells J. Cell. Biochem. 78 2000 595 606
66. A. Shiose, J. Kuroda, K. Tsuruya, M. Hirai, H. Hirakata, S. Naito, M. Hattori, Y. Sakaki, and H. Sumimoto A novel superoxide-producing NAD(P)H oxidase in kidney J. Biol. Chem. 276 2001 1417 1423
67. H. Sies Ebselen, a selenoorganic compound as glutathione peroxidase mimic Free Radic. Biol. Med. 14 1993 313 323
68. H. Sies Ebselen Methods Enzymol. 252 1995 341 342
69. R.J. Snelgrove, L. Edwards, A.J. Rae, and T. Hussell An absence of reactive oxygen species improves the resolution of lung influenza infection Eur. J. Immunol. 36 2006 1364 1373
70. Y.-A. Suh, R.S. Arnold, B. Lassegue, J. Shi, X. Xu, D. Sorescu, A.B. Chung, K.K. Griendling, and J.D. Lambeth Cell transformation by the superoxide-generating oxidase Mox1 Nature 401 1999 79 82
71. H. Sumimoto, Y. Kage, H. Nunoi, H. Sasaki, T. Nose, Y. Fukumaki, M. Ohno, S. Minakami, and K. Takeshige Role of Src homology 3 domains in assembly and activation of the phagocyte NADPH oxidase Proc. Natl. Acad. Sci. USA 91 1994 5345 5349
72. H. Sumimoto, K. Hata, K. Mizuki, T. Ito, Y. Kage, Y. Sakaki, Y. Fukumaki, M. Nakamura, and K. Takeshige Assembly and activation of the phagocyte NADPH oxidase: Specific Interaction of the N-terminal Src homology 3 domain of p47phox with p22phox is required for activation of the NADPH oxidase complex J. Biol. Chem. 36 1996 22152 22158
73. Y. Tabuchi, N. Sugiyama, T. Horiuchi, M. Furusawa, and K. Furuhama Ebselen, a seleno-organic compound, protects against ethanol-induced murine gastric mucosal injury in both in vivo and in vitro systems Eur. J. Pharmacol. 272 1995 195 201
74. I. Takac, K. Schröder, L. Zhang, B. Lardy, N. Anilkumar, J.D. Lambeth, A.M. Shah, F. Morel, and R.P. Brandes The E-loop is involved in hydrogen peroxide formation by the NADPH oxidase Nox4 J. Biol. Chem. 286 2011 13304 13313
75. M. Tamura, M. Takeshita, J.T. Curnutte, D.J. Uhlinger, and J.D. Lambeth Stabilization of human neutrophil NADPH oxidase activated in a cell-free system by cytosolic proteins and by 1-ethyl-3-(3-dimethylaminopropyl) carbodiimide J. Biol. Chem. 267 1992 7529 7538
76. F. Tirone, L. Radu, C.T. Craescu, and J.A. Cox Identification of the binding site for the regulatory calcium-binding domain in the catalytic domain of NOX5 Biochemistry 49 2010 761 771
77. D.J. Uhlinger, K.L. Inge, M.L. Kreck, S.R. Tyagi, N. Neckelmann, and J.D. Lambeth Reconstitution and characterization of the human neutrophil respiratory burst oxidase using recombinant p47-phox, p67-phox and plasma membrane Biochem. Biophys. Res. Commun. 186 1992 509 516
78. P.V. Vignais The superoxide-generating NADPH oxidase: structural aspects and activation mechanism Cell. Mol. Life Sci. 59 2002 1428 1459
79. K. Wakamura, T. Ohtsuka, N. Okamura, S. Ishibashi, and H. Masayasu Mechanism for the inhibitory effect of a seleno-organic compound, Ebselen, and its analogues on superoxide anion production in guinea pig polymorphonuclear leukocytes J. Pharmacobiodyn. 13 1990 421 425
80. J.F. Wang, P. Komarov, H. Sies, and H. de Groot Inhibition of superoxide and nitric oxide release and protection from reoxygenation injury by Ebselen in rat Kupffer cells Hepatology 15 1992 1112 1116
81. S. Yuzawa, N.N. Suzuki, Y. Fujioka, K. Ogura, H. Sumimoto, and F. Inagaki A molecular mechanism for autoinhibition of the tandem SH3 domains of p47phox, the regulatory subunit of the phagocyte NADPH oxidase Genes Cells 9 2004 443 456
82. A. Zembowicz, R.J. Hatchett, W. Radziszewski, and R.J. Gryglewski Inhibition of endothelial nitric oxide synthase by ebselen. Prevention by thiols suggests the inactivation by ebselen of a critical thiol essential for the catalytic activity of nitric oxide synthase J. Pharmacol. Exp. Ther. 267 1993 1112 1118