A novel ATP-binding cassette transporter involved in multidrug resistance in the phytopathogenic fungus Penicillium digitatum

Applied and Environmental Microbiology

Volumn 64, Issue 10, 1998, Pages 3983-3988

  Nakaune, Ryoji ^a   Adachi, Kiichi ^a   Nawata, Osamu ^a   Tomiyama, Masamitsu ^b   Akutsu, Katsumi ^c   Hibi, Tadaaki ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

^c IBARAKI UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

4 NITROQUINOLINE 1 OXIDE; ABC TRANSPORTER; ACRIFLAVINE; BITERTANOL; CYCLOHEXIMIDE; FENARIMOL; FUNGAL DNA; FUNGAL RNA; FUNGICIDE; GLYCOPROTEIN P; PYRIFENOX; TRIFLUMIZOLE; UNCLASSIFIED DRUG;

AGRICULTURE; AMINO ACID SEQUENCE; ARTICLE; ASPERGILLUS NIDULANS; CANDIDA ALBICANS; CONTROLLED STUDY; DEMETHYLATION; DNA LIBRARY; MULTIDRUG RESISTANCE; NONHUMAN; NORTHERN BLOTTING; NUCLEOTIDE SEQUENCE; PENICILLIUM; PENICILLIUM DIGITATUM; SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES POMBE; SEQUENCE HOMOLOGY; STEROL SYNTHESIS;

ASPERGILLUS; ATRA; BOTRYOTINIA FUCKELIANA; BOTRYTIS; CANDIDA ALBICANS; EMERICELLA NIDULANS; FUNGI; PENICILLIUM DIGITATUM; SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES POMBE;

EID: 0031663427     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/aem.64.10.3983-3988.1998     Document Type: Article

References (44)

1. Ausbel, F. M., K. Brentand, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl. 1987. Current protocols in molecular biology. Green Publishing Associates and Wiley-Interscience, New York, N.Y.
2. Balzi, E., and A. Goffeau. 1495. Yeast multidrug resistance: the PDR network. J. Bioenerg. Biomembr. 27:71-76.
3. Balzi, E., M. Wang, S. Leterme, L. Van Dyck, and A. Goffeau. 1994. PDR5, a novel yeast multidrug resistance conferring transporter controlled by the transcription regulator PDR1. J. Biol. Chem. 269:2206-2214.
4. Bissinger, P. H., and K. Kuchler. 1994. Molecular cloning and expression of the Saccharomyces cerevisiae STS1 gene product. A yeast ABC transporter conferring mycotoxin resistance. J. Biol. Chem. 269:4180-4186.
5. Delaveau, T., A. Delahodde, E. Carvajal, J. Subik, and C. Jacq. 1994. PDR3, a new yeast regulatory gene, is homologous to PDR1 and controls and multidrug resistance phenomenon. Mol. Gen. Genet. 244:501-511.
6. Del Sorbo, G., A. C. Andrade, J. G. Van Nistelrooy, J. A. Van Kan, E. Balzi, and M. A. De Waard. 1997. Multidrug resistance in Aspergillus nidulans involves novel ATP-binding cassette transporters. Mol. Gen. Genet. 254: 417-426.
7. Delye, C., F. Laigret, and M. F. Corio-Costet. 1997. A mutation in the 14 alpha-demethylase gene of Urcinula necator that correlates with resistance to a sterol biosynthesis inhibitor. Appl. Environ. Microbiol. 63:2966-2970.
8. De Waard, M. A. 1997. Significance of ABC transporters in fungicide sensitivity and resistance. Pectic. Sci. 51:271-275.
9. De Waard, M. A., and J. G. Van Nistelrooy. 1988. Accumulation of SBI fungicide in wild-type and fenarimol-resistant isolates of Penicillium italicum. Pestic. Sci. 22:371-382.
10. De Waard, M. A., and J. G. Van Nistelrooy. 1984. Differential accumulation of fenarimol by a wild type isolate and fenarimol-resistant isolates of Penicillium italicum. Neth. J. Plant Pathol. 90:143-153.
11. De Waard, M. A., and J. G. Van Nistelrooy. 1980. An energy-dependent efflux mechanism for fenarimol in a wild type strain and fenarimol-resistant mutants of Aspergillus nidulans. Pestic. Biochem. Physiol. 13:255-266.
12. De Waard, M. A., and J. G. Van Nistelrooy. 1981. Induction of fenarimol-efflux activity in Aspergillus nidulans by fungicides inhibiting sterol biosynthesis. J. Gen. Microbiol. 126:483-489.
13. De Waard, M. A., and J. G. Van Nistelrooy. 1987. Inhibitors of energy-dependent efflux of fungicide fenarimol by Aspergillus nidulans. Exp. Mycol. 11:1-10.
14. Dexter, D., W. S. Moye-Rowley, A. L. Wu, and J. Golin. 1994. Mutations in the yeast PDR3, PDR4, PDR7 and PDR9 pleiotropic (multiple) drug resistance loci affect the transcript level of an ATP binding cassette transporter encoding gene, PDR5. Genetics 136:505-515.
15. Gottesman, M. M., and I. Pastan. 1993. Biochemistry of multidrug resistance mediated by the multidrug transporter. Annu. Rev. Biochem. 62:385-427.
16. Higgins, C. F. 1992. ABC transporters: from microorganisms to man. Annu. Rev. Cell Biol. 8:67-113.
17. Hirata, D., K. Yano, K. Miyahara, and T. Miyakawa. 1994. Saccharomyces cerevisiae YDR1, which encodes a member of the ATP-binding cassette (ABC) superfamily, is required for multidrug resistance. Curr. Genet. 26: 285-294.
18. Hollomon, D. W. 1993. Resistance to azole fungicides in the field. Biochem. Soc. Trans. 21:1047-1051.
19. Hollomon, D. W., J. Butters, and J. Clark. 1984. Genetic control of triadimenol resistance in barley powdery mildew, p. 477-482. In Proceedings of the British Crop Protection Conference - Pests and Diseases, vol. 2. British Crop Protection Council Publications, Croydon, United Kingdom.
20. Ito, Y., R. Johnson, and B. Scott. 1994. Integrative transformation of the mycotoxin-producing fungus. Penicillium paxilli. Curr. Genet. 25:508-513.
21. Joseph-Horne, T., D. Hollomon, R. S. Loeffler, and S. L. Kelly. 1995. Altered P450 activity associated with direct selection for fungal azole resistance. FEBS Lett. 374:174-178.
22. Katzmann, D. J., P. E. Burnett, J. Golin, Y. Mahe, and W. S. Moye-Rowley. 1994. Transcriptional control of the yeast PDR5 gene by the PDR3 gene product. Mol. Cell. Biol. 14:4653-4661.
23. Katzmann, D. J., T. C. Hallstrom, Y. Mahe, and W. S. Moye-Rowley. 1996. Multiple Pdr1p/Pdr3p binding sites are essential for normal expression of the ATP binding cassette transporter protein-encoding gene PDR5. J. Biol. Chem. 271:23049-23054.
24. Kioka, N., J. Tsubota, Y. Kakehi, T. Komano, M. M. Gottesman, I. Pastan, and K. Ueda. 1989. P-glycoprotein gene (MDR1) cDNA from human adrenal: normal P-glycoprotein carries Gly 185 with an altered pattern of multidrug resistance. Biochem. Biophys. Res. Commun. 162:224-231.
25. Kormanec, J., and M. Farkasovsky. 1994. Isolation of total RNA from yeast and bacteria and detection of rRNA in Northern blots. BioTechniques 17: 838-842.
26. Kyte, J., and R. F. Doolittle. 1982. A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157:105-132.
27. Loffler, J., S. L. Kelly, H. Hebart, U. Schumacher, C. Lass-Florl, and H. Einsele. 1997. Molecular analysis of cyp51 from fluconazole-resistant Candida albicans strains. FEMS Microbiol. Lett. 151:263-268.
28. Mahe, Y., A. Parle-McDermott, A. Nourani, A. Delahodde, A. Lamprecht, and K. Kuchler. 1996. The ATP-binding cassette multidrug transporter Snq2 of Saccharomyces cerevisiae: a novel target for the transcription factors Pdr1 and Pdr3. Mol. Microbiol. 20:109-117.
29. 28a. Nakaune, R., et al. Unpublished data.
30. Prasad, R., P. De Wergifosse, A. Goffeau, and E. Balzi. 1995. Molecular cloning and characterization of a novel gene of Candida albicans, CDR1, conferring multiple resistance to drugs and antifungals. Curr. Genet. 27:320-329.
31. Punt, P. J., R. P. Oliver, M. A. Dingemanse, P. H. Pouwels, and C. A. van den Hondel. 1987. Transformation of Aspergillus based on the hygromycin B resistance marker from Escherichia coli. Gene 56:117-124.
32. Roepe, P. D. 1995. The role of the MDR protein in altered drug translocation across tumor cell membranes. Biochim. Biophys. Acta 1241:385-105.
33. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
34. Sanger, F., S. Nicklen, and A. R. Coulson. 1977. DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. USA 74:5463-5467.
35. Sanglard, D., K. Kuchler, F. Ischer, J. L. Pagani, M. Monod, and J. Bille. 1995. Mechanisms of resistance to azole antifungal agents in Candida albicans isolates from AIDS patients involve specific multidrug transporters. Antimicrob. Agents Chemother. 39:2378-2386.
36. Schinkel, A. H., and P. Borst. 1991. Multidrug resistance mediated by P-glycoproteins. Semin. Cancer Biol. 2:213-226.
37. Servos, J., E. Haase, and M. Brendel. 1993. Gene SNQ2 of Saccharomyces cerevisiae, which confers resistance to 4-nitroquinoline-N-oxide and other chemicals, encodes a 169 kDa protein homologous to ATP-dependent permeases. Mol. Gen. Genet. 236:214-218.
38. Stehmann, C., and M. A. de Waard. 1995. Accumulation of tebuconazole by isolates of Botrytis cinerea differing in sensitivity to sterol demethylation inhibiting fungicides. Pectic. Sci. 45:311-318.
39. Turi, T. G., and J. K. Rose. 1995. Characterization of a novel Schizosaccharomyces pombe multidrug resistance transporter conferring brefeldin A resistance. Biochem. Biophys. Res. Commun. 213:410-418.
40. Van den Brink, H. J., H. J. Van Nistelrooy, M. A. de Waard, C. A. Van den Hondel, and R. F. Van Gorcom. 1996. Increased resistance to 14 alpha-demethylase inhibitors (DMIs) in Aspergillus niger by coexpression of the Penicillium italicum eburicol 14 alpha-demethylase (cyp51) and the A. niger cytochrome P450 reductase (cprA) genes. J. Biotechnol. 49:13-18.
41. Van Nistelrooy, J. G., J. M. Van den Brink, J. A. Van Kan, R. F. Van Gorcom, and M. A. de Waard. 1996. Isolation and molecular characterization of the gene encoding eburicol 14 alpha-demethylase (CYP51) from Penicillium italicum. Mol. Gen. Genet. 250:725-733.
42. Van Tuyl, J. M. 1977. Genetis of fungal resistance to systemic fungicides. Meded. Landbouwhogesch. Wagening. 77:1-136.
43. Walker, J. E., M. Saraste, M. J. Runswick, and N. J. Gay. 1982. Distantly related sequences in the alpha- and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J. 1:945-951.
44. Yoder, O. C. 1988. Cochliobolus heterostrophus, cause of Southern corn leaf blight. Adv. Plant Pathol. 6:93-112.