The 5-lipoxygenase inhibitor RF-22c potently suppresses leukotriene biosynthesis in cellulo and blocks bronchoconstriction and inflammation in vivo

Biochemical Pharmacology

Volumn 112, Issue , 2016, Pages 60-71

  Schaible, Anja M ^a   Filosa, Rosanna ^a,b,h   Krauth, Verena ^a   Temml, Veronika ^c   Pace, Simona ^a   Garscha, Ulrike ^a   Liening, Stefanie ^a   Weinigel, Christina ^d   Rummler, Silke ^d   Schieferdecker, Sebastian ^e   Nett, Markus ^e,f   Peduto, Antonella ^b   Collarile, Selene ^b   Scuotto, Maria ^b   Roviezzo, Fioretina ^g   Spaziano, Giuseppe ^b   De Rosa, Mario ^g   Stuppner, Hermann ^c   Schuster, Daniela ^c   D'Agostino, Bruno ^g   Werz, Oliver ^a   more..

^a FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^b SECOND UNIVERSITY OF NAPLES   (Italy)

^c UNIVERSITY OF INNSBRUCK   (Austria)

^d JENA UNIVERSITY HOSPITAL   (Germany)

^e HANS KNÖLL INSTITUTE   (Germany)

^f TU DORTMUND UNIVERSITY   (Germany)

^g UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^h Consorzio Sannio Tech ^*  (Italy)

Author keywords

5 Lipoxygenase; Benzoquinones; Inflammation; Leukocytes; Leukotriene

Indexed keywords

ANTIINFLAMMATORY AGENT; ARACHIDONIC ACID; CYCLOOXYGENASE 1; CYCLOOXYGENASE 2; LEUKOTRIENE; LIPOXYGENASE INHIBITOR; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; OVALBUMIN; RF 22C; UNCLASSIFIED DRUG; ZILEUTON; ZYMOSAN; 4,5-DIMETHOXY-3-DODECYL-1,2-BENZOQUINONE; ARACHIDONATE 5 LIPOXYGENASE; BENZOQUINONE DERIVATIVE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOSYNTHESIS; CARRAGEENAN-INDUCED PAW EDEMA; CELL FREE SYSTEM; CELL NUCLEUS MEMBRANE; CONTROLLED STUDY; DRUG EFFICACY; DRUG INHIBITION; DRUG POTENCY; DRUG SELECTIVITY; EMBRYO; ENZYME ACTIVATION; EXPERIMENTAL AIR POUCH INFLAMMATION; FEMALE; HEK293 CELL LINE; HUMAN; HUMAN CELL; IC50; IN VIVO STUDY; MOLECULAR DOCKING; MONOCYTE; MOUSE; NEUTROPHIL; NONHUMAN; NORMAL HUMAN; OVALBUMIN-INDUCED BRONCHOCONSTRICTION; PRIORITY JOURNAL; PROTEIN INTERACTION; ANIMAL; BAGG ALBINO MOUSE; BRONCHOCONSTRICTION; CELL CULTURE; DRUG EFFECTS; EDEMA; ENZYMOLOGY; ESCHERICHIA COLI; GENETICS; IMMUNOLOGY; METABOLISM; THROMBOCYTE;

ANIMALS; ANTI-INFLAMMATORY AGENTS; ARACHIDONATE 5-LIPOXYGENASE; BENZOQUINONES; BLOOD PLATELETS; BRONCHOCONSTRICTION; CELLS, CULTURED; EDEMA; ESCHERICHIA COLI; FEMALE; HUMANS; LEUKOTRIENES; LIPOXYGENASE INHIBITORS; MICE, INBRED BALB C; MOLECULAR DOCKING SIMULATION; MONOCYTES; NEUTROPHILS;

EID: 84969247665     PISSN: 00062952     EISSN: 18732968     Source Type: Journal    
DOI: 10.1016/j.bcp.2016.04.019     Document Type: Article

References (56)

1. M. Peters-Golden, and W.R. Henderson Jr. Leukotrienes N. Engl. J. Med. 357 2007 1841 1854
2. A. Di Gennaro, and J.Z. Haeggstrom The leukotrienes: immune-modulating lipid mediators of disease Adv. Immunol. 116 2012 51 92
3. D. Wang, and R.N. Dubois Eicosanoids and cancer Nat. Rev. Cancer 10 2010 181 193
4. O. Radmark, O. Werz, D. Steinhilber, and B. Samuelsson 5-Lipoxygenase, a key enzyme for leukotriene biosynthesis in health and disease Biochim. Biophys. Acta 2015 1851 331 339
5. O. Radmark, O. Werz, D. Steinhilber, and B. Samuelsson 5-Lipoxygenase: regulation of expression and enzyme activity Trends Biochem. Sci. 32 2007 332 341
6. M. Back, W.S. Powell, S.E. Dahlen, J.M. Drazen, J.F. Evans, C.N. Serhan, and et al. International Union of Basic and Clinical Pharmacology. Update on leukotriene, lipoxin and oxoeicosanoid receptors: IUPHAR review 7 Br. J. Pharmacol. 2014
7. J.J. Moreno New aspects of the role of hydroxyeicosatetraenoic acids in cell growth and cancer development Biochem. Pharmacol. 77 2009 1 10
8. O. Werz, and D. Steinhilber Therapeutic options for 5-lipoxygenase inhibitors Pharmacol. Ther. 112 2006 701 718
9. C. Pergola, and O. Werz 5-Lipoxygenase inhibitors: a review of recent developments and patents Expert Opin. Ther. Pat. 20 2010 355 375
10. D. Steinhilber, and B. Hofmann Recent advances in the search for novel 5-lipoxygenase inhibitors Basic Clin. Pharmacol. Toxicol. 114 2014 70 77
11. D. Pettersen, O. Davidsson, and C. Whatling Recent advances for FLAP inhibitors Bioorg. Med. Chem. Lett. 25 2015 2607 2612
12. O. Werz, and D. Steinhilber Development of 5-lipoxygenase inhibitors-lessons from cellular enzyme regulation Biochem. Pharmacol. 70 2005 327 333
13. A.W. Ford-Hutchinson, M. Gresser, and R.N. Young 5-Lipoxygenase Annu. Rev. Biochem. 63 1994 383 417
14. A.M. Schaible, R. Filosa, V. Temml, V. Krauth, M. Matteis, A. Peduto, and et al. Elucidation of the molecular mechanism and the efficacy in vivo of a novel 1,4-benzoquinone that inhibits 5-lipoxygenase Br. J. Pharmacol. 171 2014 2399 2412
15. A.M. Schaible, H. Traber, V. Temml, S.M. Noha, R. Filosa, A. Peduto, and et al. Potent inhibition of human 5-lipoxygenase and microsomal prostaglandin E synthase-1 by the anti-carcinogenic and anti-inflammatory agent embelin Biochem. Pharmacol. 86 2013 476 486
16. B. Hofmann, C.B. Rodl, A.S. Kahnt, T.J. Maier, A.A. Michel, M. Hoffmann, and et al. Molecular pharmacological profile of a novel thiazolinone-based direct and selective 5-lipoxygenase inhibitor Br. J. Pharmacol. 165 2012 2304 2313
17. P.R. Dandawate, A.C. Vyas, S.B. Padhye, M.W. Singh, and J.B. Baruah Perspectives on medicinal properties of benzoquinone compounds Mini Rev. Med. Chem. 10 2010 436 454
18. O. Werz Inhibition of 5-lipoxygenase product synthesis by natural compounds of plant origin Planta Med. 73 2007 1331 1357
19. T. Yoshimoto, C. Yokoyama, K. Ochi, S. Yamamoto, Y. Maki, Y. Ashida, and et al. 2,3,5-Trimethyl-6-(12-hydroxy-5,10-dodecadiynyl)-1,4-benzoquinone (AA861), a selective inhibitor of the 5-lipoxygenase reaction and the biosynthesis of slow-reacting substance of anaphylaxis Biochim. Biophys. Acta 713 1982 470 473
20. R. Filosa, A. Peduto, P. Aparoy, A.M. Schaible, S. Luderer, V. Krauth, and et al. Discovery and biological evaluation of novel 1,4-benzoquinone and related resorcinol derivatives that inhibit 5-lipoxygenase Eur. J. Med. Chem. 67 2013 269 279
21. R. Filosa, A. Peduto, A.M. Schaible, V. Krauth, C. Weinigel, D. Barz, and et al. Novel series of benzoquinones with high potency against 5-lipoxygenase in human polymorphonuclear leukocytes Eur. J. Med. Chem. 94 2015 132 139
22. A.M. Schaible, A. Koeberle, H. Northoff, B. Lawrenz, C. Weinigel, D. Barz, and et al. High capacity for leukotriene biosynthesis in peripheral blood during pregnancy Prostaglandins Leukot. Essent. Fatty Acids 89 2013 245 255
23. O. Scherer, H. Steinmetz, C. Kaether, C. Weinigel, D. Barz, H. Kleinert, and et al. Targeting V-ATPase in primary human monocytes by archazolid potently represses the classical secretion of cytokines due to accumulation at the endoplasmic reticulum Biochem. Pharmacol. 91 2014 490 500
24. D. Steinhilber, T. Herrmann, and H.J. Roth Separation of lipoxins and leukotrienes from human granulocytes by high-performance liquid chromatography with a Radial-Pak cartridge after extraction with an octadecyl reversed-phase column J. Chromatogr. 493 1989 361 366
25. C. Pergola, B. Jazzar, A. Rossi, U. Buehring, S. Luderer, F. Dehm, and et al. Cinnamyl-3,4-dihydroxy-alpha-cyanocinnamate is a potent inhibitor of 5-lipoxygenase J. Pharmacol. Exp. Ther. 338 2011 205 213
26. L. Fischer, D. Szellas, O. Radmark, D. Steinhilber, and O. Werz Phosphorylation- and stimulus-dependent inhibition of cellular 5-lipoxygenase activity by nonredox-type inhibitors FASEB J. 17 2003 949 951
27. C. Pergola, G. Dodt, A. Rossi, E. Neunhoeffer, B. Lawrenz, H. Northoff, and et al. ERK-mediated regulation of leukotriene biosynthesis by androgens: a molecular basis for gender differences in inflammation and asthma Proc. Natl. Acad. Sci. U.S.A. 105 2008 19881 19886
28. T.J. Maier, L. Tausch, M. Hoernig, O. Coste, R. Schmidt, C. Angioni, and et al. Celecoxib inhibits 5-lipoxygenase Biochem. Pharmacol. 76 2008 862 872
29. C. Pergola, B. Jazzar, A. Rossi, H. Northoff, M. Hamburger, L. Sautebin, and et al. On the inhibition of 5-lipoxygenase product formation by tryptanthrin: mechanistic studies and efficacy in vivo Br. J. Pharmacol. 165 2012 765 776
30. J. Gerstmeier, C. Weinigel, S. Rummler, O. Radmark, O. Werz, and U. Garscha Time-resolved in situ assembly of the leukotriene-synthetic 5-lipoxygenase/5-lipoxygenase-activating protein complex in blood leukocytes FASEB J. 30 2016 276 285
31. M.S. Blois Antioxidant determinations by the use of a stable free radical Nature 181 1958 1199 1200
32. B. Schwyn, and J.B. Neilands Universal chemical assay for the detection and determination of siderophores Anal. Biochem. 160 1987 47 56
33. J. Korp, S. Konig, S. Schieferdecker, H.M. Dahse, G.M. Konig, O. Werz, and et al. Harnessing enzymatic promiscuity in myxochelin biosynthesis for the production of 5-lipoxygenase inhibitors ChemBioChem 16 2015 2445 2450
34. D. Albert, I. Zundorf, T. Dingermann, W.E. Muller, D. Steinhilber, and O. Werz Hyperforin is a dual inhibitor of cyclooxygenase-1 and 5-lipoxygenase Biochem. Pharmacol. 64 2002 1767 1775
35. M. Hoffmann, J.J. Lopez, C. Pergola, C. Feisst, S. Pawelczik, P.J. Jakobsson, and et al. Hyperforin induces Ca(2+)-independent arachidonic acid release in human platelets by facilitating cytosolic phospholipase A(2) activation through select phospholipid interactions Biochim. Biophys. Acta 2010 1801 462 472
36. 2+ indicators with greatly improved fluorescence properties J. Biol. Chem. 260 1985 3440 3450
37. G. Jones, P. Willett, R.C. Glen, A.R. Leach, and R. Taylor Development and validation of a genetic algorithm for flexible docking J. Mol. Biol. 267 1997 727 748
38. N.C. Gilbert, S.G. Bartlett, M.T. Waight, D.B. Neau, W.E. Boeglin, A.R. Brash, and et al. The structure of human 5-lipoxygenase Science 331 2011 217 219
39. N. Sullo, F. Roviezzo, M. Matteis, A. Ianaro, G. Calo, R. Guerrini, and et al. Nociceptin/orphanin FQ receptor activation decreases the airway hyperresponsiveness induced by allergen in sensitized mice Am. J. Physiol. Lung Cell. Mol. Physiol. 304 2013 L657 L664
40. A.N. von Bethmann, F. Brasch, R. Nusing, K. Vogt, H.D. Volk, K.M. Muller, and et al. Hyperventilation induces release of cytokines from perfused mouse lung Am. J. Res. Crit. Care Med. 157 1998 263 272
41. D.W. Moss, and A.K. Henderson Clinical enzymology C.A. Burtis, E.R. Ashwood, Tietz Text Book of Clinical Chemistry 3rd ed. 1994 WB Saunders Philadelphia 617 721
42. A. Kaplan, and L.S. Lavernel Clinical chemistry Interpretation and Techniques 2nd ed. 1983 Lea and Febiger Philadelphia 219 296
43. C. Feisst, C. Pergola, M. Rakonjac, A. Rossi, A. Koeberle, G. Dodt, and et al. Hyperforin is a novel type of 5-lipoxygenase inhibitor with high efficacy in vivo Cell. Mol. Life Sci. 66 2009 2759 2771
44. S. Ohkawa, T. Terao, M. Murakami, T. Matsumoto, and G. Goto Reduction of 2,3,5-trimethyl-6-(3-pyridylmethyl)-1,4-benzoquinone by PB-3c cells and biological activity of its hydroquinone Chem. Pharm. Bull. (Tokyo) 39 1991 917 921
45. J.B. Baell, and G.A. Holloway New substructure filters for removal of pan assay interference compounds (PAINS) from screening libraries and for their exclusion in bioassays J. Med. Chem. 53 2010 2719 2740
46. B. D'Agostino, D. Orlotti, G. Calo, N. Sullo, M. Russo, R. Guerrini, and et al. Nociceptin modulates bronchoconstriction induced by sensory nerve activation in mouse lung Am. J. Respir. Cell Mol. Biol. 42 2010 250 254
47. W.J. Chen, S.F. Liaw, C.C. Lin, M.W. Lin, and F.T. Chang Effects of zileuton on airway smooth muscle remodeling after repeated allergen challenge in brown Norway rats Respiration 86 2013 421 429
48. W. Berger, M.T. De Chandt, and C.B. Cairns Zileuton: clinical implications of 5-lipoxygenase inhibition in severe airway disease Int. J. Clin. Pract. 61 2007 663 676
49. A. Rossi, C. Pergola, A. Koeberle, M. Hoffmann, F. Dehm, P. Bramanti, and et al. The 5-lipoxygenase inhibitor, zileuton, suppresses prostaglandin biosynthesis by inhibition of arachidonic acid release in macrophages Br. J. Pharmacol. 161 2010 555 570
50. E.M. Joshi, B.H. Heasley, M.D. Chordia, and T.L. Macdonald In vitro metabolism of 2-acetylbenzothiophene: relevance to zileuton hepatotoxicity Chem. Res. Toxicol. 17 2004 137 143
51. M.E. Surette, R. Palmantier, J. Gosselin, and P. Borgeat Lipopolysaccharides prime whole human blood and isolated neutrophils for the increased synthesis of 5-lipoxygenase products by enhancing arachidonic acid availability: involvement of the CD14 antigen J. Exp. Med. 178 1993 1347 1355
52. J.F. Evans, A.D. Ferguson, R.T. Mosley, and J.H. Hutchinson What's all the FLAP about?: 5-lipoxygenase-activating protein inhibitors for inflammatory diseases Trends Pharmacol. Sci. 29 2008 72 78
53. N.S. Doherty, P. Poubelle, P. Borgeat, T.H. Beaver, G.L. Westrich, and N.L. Schrader Intraperitoneal injection of zymosan in mice induces pain, inflammation and the synthesis of peptidoleukotrienes and prostaglandin E2 Prostaglandins 30 1985 769 789
54. T.R. Jones, M. Labelle, M. Belley, E. Champion, L. Charette, J. Evans, and et al. Pharmacology of montelukast sodium (Singulair), a potent and selective leukotriene D4 receptor antagonist Can. J. Physiol. Pharmacol. 73 1995 191 201
55. A. Rackham, and A.W. Ford-Hutchinson Inflammation and pain sensitivity: effects of leukotrienes D4, B4 and prostaglandin E1 in the rat paw Prostaglandins 25 1983 193 203
56. D.A. Smith, A. Harrison, and P. Morgan Multiple factors govern the association between pharmacology and toxicity in a class of drugs: toward a unification of class effect terminology Chem. Res. Toxicol. 24 2011 463 474