Antifungal activity of cinnamic acid derivatives involves inhibition of benzoate 4-hydroxylase (CYP53)

Journal of Applied Microbiology

Volumn 116, Issue 4, 2014, Pages 955-966

  Korosec B ^a   Sova, M ^b   Turk, S ^b   Krasevec N ^a   Novak, M ^a   Lah, L ^a   Stojan, J ^c   Podobnik, B ^d   Berne, S ^c   Zupanec, N ^a   Bunc, M ^b   Gobec, S ^b   Komel, R ^a,c  

^a NATIONAL INSTITUTE OF CHEMISTRY   (Slovenia)

^b UNIVERSITY OF LJUBLJANA   (Slovenia)

^c UNIVERSITY OF LJUBLJANA   (Slovenia)

^d Lek dd   (Slovenia)

Author keywords

Antifungal activity; Cochliobolus lunatus; CYP53 inhibition; Cytochrome P450 benzoate 4 monooxygenase; Potential antifungal drugs

Indexed keywords

ASPERGILLUS; DETOXIFICATION; PATHOGENS;

ANTIFUNGAL ACTIVITIES; ANTIFUNGAL DRUGS; CINNAMIC ACID DERIVATIVES; CINNAMIC ACIDS; COCHLIOBOLU LUNATU; CYP53 INHIBITION; CYTOCHROME P450 BENZOATE 4-MONOOXYGENASE; CYTOCHROMES P450; MONOOXYGENASES; POTENTIAL ANTIFUNGAL DRUG;

ENZYMES;

1 (4 METHYLPIPERIDIN 1 YL) 3 PHENYLPROP 2 EN 1 ONE; BENZOATE 4 MONOOXYGENASE; CINNAMIC ACID DERIVATIVE; CYTOCHROME P450; UNCLASSIFIED DRUG; ANTIFUNGAL AGENT; CINNAMIC ACID; ENZYME INHIBITOR;

DRUG DEVELOPMENT; ENZYME ACTIVITY; EUKARYOTE; FUNGUS; METABOLISM; PATHOGEN;

ANTIFUNGAL ACTIVITY; ARTICLE; ASPERGILLUS NIGER; CONTROLLED STUDY; CURVULARIA LUNATA; DRUG MECHANISM; DRUG POTENCY; DRUG TARGETING; ENZYME ACTIVE SITE; ENZYME INHIBITION; NONHUMAN; PLEUROTUS OSTREATUS; STRUCTURE ACTIVITY RELATION; ANTAGONISTS AND INHIBITORS; ASCOMYCETES; CHEMISTRY; DRUG EFFECTS; ENZYMOLOGY; FUNGUS; METABOLISM; PLEUROTUS;

ASPERGILLUS NIGER; COCHLIOBOLUS LUNATUS; EUKARYOTA; FUNGI; PLEUROTUS OSTREATUS;

ANTIFUNGAL AGENTS; ASCOMYCOTA; BENZOATE 4-MONOOXYGENASE; CATALYTIC DOMAIN; CINNAMATES; ENZYME INHIBITORS; FUNGI; PLEUROTUS;

EID: 84896119898     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/jam.12417     Document Type: Article

References (46)

1. Barton, D.H.R. and Jones, D.W. (1965) Autoxidation in basic media. Part IV. Hydrocarbon autoxidation. J Chem Soc 3563-3570.
2. Berne, S., Podobnik, B., Zupanec, N., Novak, M., Kraševec, N., Turk, S., Korošec, B., Lah, L. et al. (2012) Virtual screening yields inhibitors of novel antifungal drug target, benzoate 4-monooxygenase. J Chem Inf Model 52, 3053-3063.
3. Bevc, S., Konc, J., Stojan, J., Hodošček, M., Penca, M., Praprotnik, M. and Janežič, D. (2011) ENZO: a web tool for derivation and evaluation of kinetic models of enzyme catalyzed reactions. PLoS ONE 6, e22265.
4. Bisogno, F., Mascoti, L., Sanchez, C., Garibotto, F., Giannini, F., Kurina-Sanz, M. and Enriz, R. (2007) Structure-antifungal activity relationship of cinnamic acid derivatives. J Agric Food Chem 55, 10635-10640.
5. Bos, C.J., Debets, A.J., Swart, K., Huybers, A., Kobus, G. and Slakhorst, S.M. (1988) Genetic analysis and the construction of master strains for assignment of genes to six linkage groups in Aspergillus niger. Curr Genet 14, 437-443.
6. Boström, J., Greenwood, J.R. and Gottfries, J. (2003) Assessing the performance of OMEGA with respect to retrieving bioactive conformations. J Mol Graph Model 21, 449-462.
7. Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72, 248-254.
8. Brennan, N.J., Larsen, L., Lorimer, S.D., Perry, N.B., Chapin, E.L., Werk, T.L., Henry, M.J. and Hahn, D.R. (2006) Fungicidal sesquiterpene dialdehyde cinnamates from Pseudowintera axillaris. J Agric Food Chem 54, 468-473.
9. Chai, X., Zhang, J., Cao, Y., Zou, Y., Wu, Q., Zhang, D., Jiang, Y. and Sun, Q. (2011a) Design, synthesis and molecular docking studies of novel triazole as antifungal agent. Eur J Med Chem 46, 3167-3176.
10. Chai, X., Zhang, J., Cao, Y., Zou, Y., Wu, Q., Zhang, D., Jiang, Y. and Sun, Q. (2011b) New azoles with antifungal activity: design, synthesis, and molecular docking. Bioorg Med Chem Lett 21, 686-689.
11. Chen, H.-C., Li, Q., Shuford, C.M., Liu, J., Muddiman, D.C., Sederoff, R.R. and Chiang, V.L. (2011) Membrane protein complexes catalyze both 4- and 3-hydroxylation of cinnamic acid derivatives in monolignol biosynthesis. Proc Natl Acad Sci USA 108, 21253-21258.
12. Freidlina, R.K., Chukovskaya, E.T. and Englin, B.A. (1965) The influence of ethylene oxide or amines on chain transfer with participation of an intermediate in telomerization of ethylene with carbon tetrachloride. Dokl Akad Nauk SSSR 162, 359-361.
13. Fukuda, H., Nakamura, K., Sukita, E., Ogawa, T. and Fujii, T. (1996) Cytochrome P450rm from Rhodotorula minuta catalyzes 4-hydroxylation of benzoate. J Biochem 119, 314-318.
14. Gobec, S., Sova, M., Kristan, K. and Rizner, T.L. (2004) Cinnamic acid esters as potent inhibitors of fungal 17beta-hydroxysteroid dehydrogenase-a model enzyme of the short-chain dehydrogenase/reductase superfamily. Bioorg Med Chem Lett 14, 3933-3936.
15. Gutierrez, L.J., Mascotti, M.L., Kurina-Sanz, M., Pungitore, C.R., Enriz, R.D. and Giannini, F.A. (2012) Cinnamic acid derivatives acting against Aspergillus fungi. Taq polymerase I a potential molecular target. Nat Prod Commun 7, 1639-1644.
16. Harwood, C.S. and Parales, R.E. (1996) The beta-ketoadipate pathway and the biology of self-identity. Annu Rev Microbiol 50, 553-590.
17. Hawkins, P.C.D. and Nicholls, A. (2012) Conformer generation with OMEGA: learning from the data set and the analysis of failures. J Chem Inf Model 52, 2919-2936.
18. Hawkins, P.C.D., Skillman, A.G., Warren, G.L., Ellingson, B.A. and Stahl, M.T. (2010) Conformer generation with OMEGA: algorithm and validation using high quality structures from the Protein Databank and Cambridge Structural Database. J Chem Inf Model 50, 572-584.
19. Hu, S., Nian, S., Qin, K., Xiao, T., Li, L., Qi, X., Ye, F., Liang, G. et al. (2012) Design, synthesis and inhibitory activities of 8-(substituted styrol-formamido)phenyl-xanthine derivatives on monoamine oxidase B. Chem Pharm Bull 60, 385-390.
20. Ide, M., Ichinose, H. and Wariishi, H. (2012) Molecular identification and functional characterization of cytochrome P450 monooxygenases from the brown-rot basidiomycete Postia placenta. Arch Microbiol 194, 243-253.
21. Jacobson, M., Galetta, S.L., Atlas, S.W., Curtis, M.T. and Wulc, A.W. (1992) Bipolaris-induced orbital cellulitis. J Clin Neuro-ophthalmol 12, 250-256.
22. Jefcoate, C.R. (1978) Measurement of substrate and inhibitor binding to microsomal cytochrome P-450 by optical-difference spectroscopy. In Methods in Enzymology, Vol. 52 ed. Fleischer, S. and Packer, L. pp. 258-279. New York, NY: Academic Press.
23. Jeon, J., Yang, D. and Jun, J. (2011) Selective synthesis of 3, 4-dihydrocoumarins and chalcones from substituted aryl cinnamic esters. Bull Korean Chem Soc 32, 65-70.
24. Katritzky, R.A., Zhang, S. and Soares, M.W. (2001) A facile synthesis of benzyl α, β-unsaturated carboxylic esters. ARKIVOC 10, 54-57.
25. Kim, J.H., Campbell, B.C., Mahoney, N.E., Chan, K.L. and Molyneux, R.J. (2004) Identification of phenolics for control of Aspergillus flavus using Saccharomyces cerevisiae in a model target-gene bioassay. J Agric Food Chem 52, 7814-7821.
26. Kristan, K., Starcević, S., Brunskole, M., Rizner, T.L. and Gobec, S. (2006) Cinnamates and cinnamamides inhibit fungal 17beta-hydroxysteroid dehydrogenase. Mol Cell Endocrinol 248, 239-241.
27. Kristan, K., Bratkovic, T., Sova, M., Gobec, S., Prezelj, A. and Urleb, U. (2009) Novel inhibitors of beta-ketoacyl-ACP reductase from Escherichia coli. Chem Biol Interact 178, 310-316.
28. Lah, L., Podobnik, B., Novak, M., Korošec, B., Berne, S., Vogelsang, M., Kraševec, N., Zupanec, N. et al. (2011) The versatility of the fungal cytochrome P450 monooxygenase system is instrumental in xenobiotic detoxification. Mol Microbiol 81, 1374-1389.
29. Lattanzio, V., Lattanzio, V.M.T., Cardinali, A. and Amendola, V. (2006) Role of phenolics in the resistance mechanisms of plants against fungal pathogens and insects. Phytochem: Adv Res 23-67.
30. Manamgoda, D.S., Cai, L., Bahkali, A.H., Chukeatirote, E. and Hyde, K.D. (2011) Cochliobolus: an overview and current status of species. Fungal Diversity 51, 3-42.
31. Maskin, S.L., Fetchick, R.J., Leone, C.R., Sharkey, P.K. and Rinaldi, M.G. (1989) Bipolaris hawaiiensis-caused phaeohyphomycotic orbitopathy. A devastating fungal sinusitis in an apparently immunocompetent host. Ophthalmology 96, 175-179.
32. Matsuzaki, F. and Wariishi, H. (2005) Molecular characterization of cytochrome P450 catalyzing hydroxylation of benzoates from the white-rot fungus Phanerochaete chrysosporium. Biochem Biophys Res Commun 334, 1184-1190.
33. McGann, M. (2011) FRED pose prediction and virtual screening accuracy. J Chem Inf Model 51, 578-596.
34. Mendoza, J., Torres, T. and Badia, M.D. (1988) On the lead tetraacetate oxidation of 4-amino-1, 2, 4-triazoles, 1-amino- and 2-amino-1, 2, 3-triazoles. Monatshefte für Chemie - Chemical Monthly 119, 1041-1045.
35. Podobnik, B., Stojan, J., Lah, L., Krasevec, N., Seliskar, M., Rizner, T.L., Rozman, D. and Komel, R. (2008) CYP53A15 of Cochliobolus lunatus, a target for natural antifungal compounds. J Med Chem 51, 3480-3486.
36. Rohwedder, J.J. (1979) Disseminated Curvularia lunata infection in a football player. Arch Intern Med 139, 940.
37. Rozman, D., Hennebert, G.L., Kunej, T., Deckock, C. and Komel, R. (1996) Steroid biotransforming strains designated Cochliobolus lunatus m118 and Curvularia lunata AT46 are both Curvularia lunata var. lunata. Mycotaxon 59, 489-498.
38. Saenz, R.E., Brown, W.D. and Sanders, C.V. (2001) Allergic bronchopulmonary disease caused by Bipolaris hawaiiensis presenting as a necrotizing pneumonia: case report and review of literature. Am J Med Sci 321, 209-212.
39. Said, S., Neves, F. and Griffiths, A.J. (2004) Cinnamic acid inhibits the growth of the fungus Neurospora crassa, but is eliminated as acetophenone. Int Biodeterior Biodegradation 54, 1-6.
40. Sangamwar, A.T., Deshpande, U.D. and Pekamwar, S.S. (2008) Antifungals: need to search for a new molecular target. Indian J Pharm Sci 70, 423-430.
41. Sharma, P. (2011) Cinnamic acid derivatives: a new chapter of various pharmacological activities. J Chem Pharm Res 3, 403-423.
42. Sova, M. (2012) Antioxidant and antimicrobial activities of cinnamic acid derivatives. Mini Rev Med Chem 12, 749-767.
43. Sova, M., Perdih, A., Kotnik, M., Kristan, K., Rizner, T.L., Solmajer, T. and Gobec, S. (2006) Flavonoids and cinnamic acid esters as inhibitors of fungal 17beta-hydroxysteroid dehydrogenase: a synthesis, QSAR and modelling study. Bioorg Med Chem 14, 7404-7418.
44. Sova, M., Žižak, D., Stanković, J.A., Prijatelj, M., Turk, S., Juranić, Z.D., Mlinarič-Raščan, I. and Gobec, S. (2013) Cinnamic acid derivatives induce cell cycle arrest in carcinoma cell lines. Med Chem 9, 633-641.
45. Turgeon, B.G. and Baker, S.E. (2007) Genetic and genomic dissection of the Cochliobolus heterostrophus Tox1 locus controlling biosynthesis of the polyketide virulence factor T-toxin. Adv Genet 57, 219-261.
46. Van Gorcom, R.F., Boschloo, J.G., Kuijvenhoven, A., Lange, J., Van Vark, A.J., Bos, C.J., Van Balken, J.A., Pouwels, P.H. et al. (1990) Isolation and molecular characterisation of the benzoate-para-hydroxylase gene (bphA) of Aspergillus niger: a member of a new gene family of the cytochrome P450 superfamily. Mol Gen Genet 223, 192-197.