Characterization of squalene epoxidase of Saccharomyces cerevisiae by applying terbinafine-sensitive variants

Antimicrobial Agents and Chemotherapy

Volumn 51, Issue 1, 2007, Pages 275-284

  Ruckenstuhl, Christoph ^a   Lang, Silvia ^a   Poschenel, Andrea ^a   Eidenberger, Armin ^a   Baral, Pravas Kumar ^a   Kohút, Peter ^b   Hapala, Ivan ^b   Gruber, Karl ^a   Turnowsky, Friederike ^a  

^a UNIVERSITY OF GRAZ   (Austria)

^b INSTITUTE OF CHEMISTRY   (Slovakia)

Author keywords

[No Author keywords available]

Indexed keywords

4 HYDROXYBENZOATE 3 MONOOXYGENASE; ALLYLAMINE; AMINO ACID; ARGININE; ASPARTIC ACID; CYCLOHEXIMIDE; ERGOSTEROL; FLAVINE ADENINE NUCLEOTIDE; FUNGAL ENZYME; FUNGAL PROTEIN; GLYCINE; KETOCONAZOLE; MESSENGER RNA; NAFTIFINE; PHENYLALANINE; PROTEIN ERG1; SERINE; SQUALENE; SQUALENE MONOOXYGENASE; STEROL; TERBINAFINE; TRIACYLGLYCEROL; TRYPTOPHAN; UNCLASSIFIED DRUG;

ALLELE; AMINO ACID SUBSTITUTION; ANTIBIOTIC SENSITIVITY; ARTICLE; BINDING SITE; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME INHIBITION; ERG1 GENE; FUNGAL GENE; FUNGAL STRAIN; GENE EXPRESSION; GENE ISOLATION; IN VITRO STUDY; MOLECULAR MODEL; MUTAGENESIS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN VARIANT; PSEUDOMONAS FLUORESCENS; SACCHAROMYCES CEREVISIAE;

ALLELES; ALLYLAMINE; AMINO ACID SUBSTITUTION; ANTIFUNGAL AGENTS; DRUG RESISTANCE, FUNGAL; FLAVIN-ADENINE DINUCLEOTIDE; NAPHTHALENES; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SQUALENE MONOOXYGENASE; STEROLS; STRUCTURE-ACTIVITY RELATIONSHIP; TEMPERATURE;

EID: 33845977046     PISSN: 00664804     EISSN: None     Source Type: Journal    
DOI: 10.1128/AAC.00988-06     Document Type: Article

References (37)

1. Buurman, E. T., B. Andrews, A. E. Blodgett, J. S. Chavda, and N. F. Schnell. 2005. Utilization of target-specific, hypersensitive strains of Saccharomyces cerevisiae to determine the mode of action of antifungal compounds. Antimicrob. Agents Chemother. 49:2558-2560.
2. Chugh, A., A. Ray, and J. B. Gupta. 2003. Squalene epoxidase as hypocholesterolemic drug target revisited. Prog. Lipid Res. 42:37-50.
3. Devereux, J., P. Haeberli, and O. Smithies. 1984. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 12:387-395.
4. Eppink, M. H., H. A. Schreuder, and W. J. Van Berkel. 1997. Identification of a novel conserved sequence motif in flavoprotein hydroxylases with a putative dual function in FAD/NAD(P)H binding. Protein Sci. 6:2454-2458.
5. Favre, B., and N. S. Ryder. 1996. Characterization of squalene epoxidase activity from the dermatophyte Trichophyton rubrum and its inhibition by terbinafine and other antimycotic agents. Antimicrob. Agents Chemother. 40:443-447.
6. Favre, B., and N. S. Ryder. 1997. Differential inhibition of fungal amd mammalian squalene epoxidases by the benzylamine SDZ SBA 586 in comparison with the allylaminc terbinafine. Arch. Biochem. Biophys. 340:265-269.
7. Gallwitz, D., and I. Sures. 1980. Structure of a split yeast gene: complete nucleotide sequence of the actin gene in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 77:2546-2550.
8. Germann, M., C. Gallo, T. Donahue, R. Shirzadi, J. Stukey, S. Lang, C. Ruckenstuhl, S. Oliaro-Bosso, V. McDonough, F. Turnowsky, G. Balliano, and J. T. Nickels, Jr. 2005. Characterizing sterol defect suppressors uncovers a novel transcriptional signaling pathway regulating zymosterol biosynthesis. J. Biol. Chem. 280:35904-35913.
9. Gietz, R. D., R. H. Schiestl, A. R. Willems, and R. A. Woods. 1995. Studies on the transformation of intact yeast cells by the LiAc/SS-DNA/PEG procedure. Yeast 11:355-360.
10. Horie, M., Y. Tsuchiya, M. Hayashi, Y. Iida, Y. Iwasawa, Y. Nagata, Y. Sawasaki, H. Fukuzumi, K. Kitani, and T. Kamei. 1990. NB-598: a potent competitive inhibitor of squalene epoxidase. J. Biol. Chem. 265:18075- 18078.
11. Jandrositz, A., F. Turnowsky, and G. Hogenauer. 1991. The gene encoding squalene epoxidase from Saccharomyces cerevisiae: cloning and characterization. Gene 107:155-160.
12. Jones, D. T. 1999. GenTHREADER: an efficient and reliable protein fold recognition method for genomic sequences. J. Mol. Biol. 287:797-815.
13. Klobucnikova, V., P. Kohut, R. Leber, S. Fuchsbichler, N. Schweighofer, F. Turnowsky, and I. Hapala. 2003. Terbinafine resistance in a pleiotropic yeast mutant is caused by a single point mutation in the ERG1 gene. Biochem. Biophys. Res. Commun. 309:666-671.
14. Landl, K. M., B. Klosch, and F. Turnowsky. 1996. ERG1, encoding squalene epoxidase, is located on the right arm of chromosome VII of Saccharomyces cerevisiae. Yeast 12:609-613.
15. Leber, R., S. Fuchsbichler, V. Klobucnikova, N. Schweighofer, E. Pitters, K. Wohlfarter, M. Lederer, K. Landl, C. Ruckenstuhl, I. Hapala, and F. Turnowsky. 2003. Molecular mechanism of terbinafine resistance in Saccharomyces cerevisiae. Antimicrob. Agents Chemother. 47:3890-3900.
16. Leber, R., K. Landl, E. Zinser, H. Ahorn, A. Spok, S. D. Kohlwein, F. Turnowsky, and G. Daum. 1998. Dual localization of squalene epoxidase, Erg1p, in yeast reflects a relationship between the endoplasmic reticulum and lipid particles. Mol. Biol. Cell 9:375-386.
17. Leber, R., R. Zenz, K. Schrottner, S. Fuchsbichler, B. Puhringer, and F. Turnowsky. 2001. A novel sequence element is involved in the transcriptional regulation of expression of the ERG1 (squalene epoxidase) gene in Saccharomyces cerevisiae. Eur. J. Biochem. 268:914-924.
18. Lee, H. K., P. Denner-Ancona, J. Sakakibara, T. Ono, and G. D. Prestwich. 2000. Photoaffinity labeling and site-directed mutagenesis of rat squalene epoxidase. Arch. Biochem. Biophys. 381:43-52.
19. Lee, H. K., Y. F. Zheng, X. Y. Xiao, M. Bai, J. Sakakibara, T. Ono, and G. D. Prestwich. 2004. Photoaffinity labeling identifies the substrate-binding site of mammalian squalene epoxidase. Biochem. Biophys. Res. Commun. 315:1-9.
20. Moran, G. R., B. Entsch, B. A. Palfey, and D. P. Ballou. 1996. Evidence for flavin movement in the function of p-hydroxybenzoate hydroxylase from studies of the mutant Arg220Lys. Biochemistry 35:9278-9285.
21. Osborne, C. S., I. Leitner, B. Hofbauer, C. A. Fielding, B. Favre, and N. S. Ryder. 2006. Biological, biochemical, and molecular characterization of a new clinical Trichophyton rubrum isolate resistant to terbinafine. Antimicrob. Agents Chemother. 50:2234-2236.
22. Pasrija, R., T. Prasad, and R. Prasad. 2005. Membrane raft lipid constituents affect drug susceptibilities of Candida albicans. Biochem. Soc. Trans. 33:1219-1223.
23. Rocha, E. M., R. E. Gardiner, S. Park, N. M. Martinez-Rossi, and D. S. Perlin. 2006. A Phe389Leu substitution in ergA confers terbinafine resistance in Aspergillus fumigatus. Antimicrob. Agents Chemother. 50:2533-2536.
24. Ruckenstuhl, C., A. Eidenberger, S. Lang, and F. Turnowsky. 2005. Single amino acid exchanges in FAD-binding domains of squalene epoxidase of Saccharomyces cerevisiae lead to either loss of functionality or terbinafine sensitivity. Biochem. Soc. Trans. 33:1197-1201.
25. Ruckenstuhl, C., R. Leber, and F. Turnowsky. 2005. Squalene epoxidase as drug target. Res. Adv. Antimicrob. Agents Chemother. 5:35-51.
26. Ryder, N. S. 1991. Squalene epoxidase as a target for the allylamines. Biochem. Soc. Trans. 19:774-777.
27. Ryder, N. S., and M. C. Dupont. 1985. Inhibition of squalene epoxidase by allylamine antimycotic compounds. A comparative study of the fungal and mammalian enzymes. Biochem. J. 230:765-770.
28. Sali, A., and T. L. Blundell. 1993. Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 234:779-815.
29. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
30. Sawada, M., K. Washizuka, and H. Okumura. 2004. Synthesis and biological activity of a novel squalene epoxidase inhibitor, FR194738. Bioorg. Med. Chem. Lett. 14:633-637.
31. Schreuder, H. A., P. A. Prick, R. K. Wierenga, G. Vriend, K. S. Wilson, W. G. Hol, and J. Drenth. 1989. Crystal structure of the p-hydroxybenzoate hydroxylase-substrate complex refined at 1.9 Å resolution. Analysis of the enzyme-substrate and enzyme-product complexes. J. Mol. Biol. 208:679-696.
32. Sherman, F. 1991. Getting started with yeast. Methods Enzymol. 194:3-21.
33. Sippl, M. J. 1993. Recognition of errors in three-dimensional structures of proteins. Proteins 17:355-362.
34. Strathern, J. N., and D. R. Higgins. 1991. Recovery of plasmids from yeast into Escherichia coli: shuttle vectors. Methods Enzymol. 194:319-329.
35. Tsai, H. F., M. Bard, K. Izumikawa, A. A. Krol, A. M. Sturm, N. T. Culbertson, C. A. Pierson, and J. E. Bennett. 2004. Candida glabrata erg1 mutant with increased sensitivity to azoles and to low oxygen tension. Antimicrob. Agents Chemother. 48:2483-2489.
36. Wendler, F., H. Bergler, K. Prutej, H. Jungwirth, G. Zisser, K. Kuchler, and G. Hogenauer. 1997. Diazaborine resistance in the yeast Saccharomyces cerevisiae reveals a link between YAP1 and the pleiotropic drug resistance genes PDR1 and PDR3. J. Biol. Chem. 272:27091-27098.
37. Wierenga, R. K., P. Terpstra, and W. G. Hol. 1986. Prediction of the occurrence of the ADP-binding beta alpha beta-fold in proteins, using an amino acid sequence fingerprint. J. Mol. Biol. 187:101-107.