Physiological functions of multidrug transporters in yeast

Current Science

Volumn 86, Issue 1, 2004, Pages 62-73

  Prasad, Rajendra ^a   Panwar, Snehlata ^a,b  

^a JAWAHARLAL NEHRU UNIVERSITY   (India)

^b UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 4444253790     PISSN: 00113891     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (125)

1. Dassa, E. and Schneider, E., The rise of a protein family, ATP-binding cassette systems. Res. Microbiol., 2001, 152, 203.
2. Higgins, C. F., ABC transporters, physiology, structure and mechanism - an overview. Res. Microbiol., 2001, 152, 205-210.
3. Putman, M., van Veen, H. W. and Konings, W. N., Molecular properties of bacterial multidrug transporters. Microbiol. Mol. Biol. Rev., 2000, 64, 672-693.
4. Van Bambeke, F., Balzi, E. and Tulkens, P. M., Antibiotic efflux pumps. Biochem. Pharmacol., 2000, 60, 457-470.
5. Wolfger, H., Mamnun, Y. M. and Kuchler, K., Fungal ABC proteins, pleiotropic drug resistance, stress response and cellular detoxification. Res. Microbiol., 2001, 152, 375-389.
6. van Veen, H. W. and Konings, W. N., Multidrug transporters from bacteria to man: similarities in structure and function. Semin. Cancer Biol., 1997, 8, 183-191.
7. Borst, P., Zelcer, N. and Helvoort, A. V., ABC transporters in lipid transport. Biochim. Biophys. Acta, 2000, 1486, 128-144.
8. Chakraburtty, K., Translational regulation by ABC systems. Res. Microbiol., 2001, 152, 391-399.
9. Detmers, F. J. M., Lanfermeijer, F. C. and Poolman, B., Peptides and ATP binding cassette peptide transporters. Res. Microbiol., 2001, 152, 245-258.
10. Goldman, B. S. and Kranz, R. G., ABC transporters associated with cytochrome c biogenesis. Res. Microbiol., 2001, 152, 323-329.
11. Liscovitch, M. and Lavie, Y., Multidrug resistance: a role for cholesterol efflux pathways? Trends Biochem. Sci., 2000, 25, 530-537.
12. Mendez, C. and Salas, J. A., The role of ABC transporters in antibiotic-producing organisms: drug secretion and resistance mechanisms. Res. Microbiol., 2001, 152, 341-350.
13. Schinkel, A. H., The physiological function of drug-transporting P-lycoproteins. Semin. Cancer Biol., 1997, 8, 161-170.
14. Decottignies, A. and Goffeau, A., Complete inventory of the yeast ABC proteins. Nature Genet., 1997, 15, 137-145.
15. Taglicht, D. and Michaelis, S., Saccharomyces cerevisiae ABC proteins and their relevance to human health and disease. Methods Enzymol., 1998, 292, 130-162.
16. Hallstrom, T. C. and Moye-Rowley, W. S., Multiple signals from dysfunctional mitochondria activate the pleiotropic drug resistance pathway in Saccharomyces cerevisiae. J. Biol. Chem., 2000, 275, 37347-37356.
17. Del Sorbo, G., Schoonbeek, H. J. and De Waard, M. A., Fungal transporters involved in efflux of natural toxic compounds and fungicides. Fung. Genet. Biol., 2000, 30, 1-15.
18. Ghannoum, M. and Rice, L. B., Antifungal agents: Mode of action, mechanism of resistance, and correlation of these mechanisms with bacterial resistance. Clin. Microbiol, Rev., 1999, 12, 501-512.
19. Marichal, P., Mechanisms of resistance to azole antifungal compounds. Curr. Opin. Anti-infect. Invest. Drugs, 1999, 1, 318-333.
20. Rogers, B., Decottignies, A., Kolaczkowski, M., Carvajal, E., Balzi, E. and Goffeau, A., The pleiotropic drug ABC transporters from Saccharomyces cerevisiae. J. Mol. Microbiol., 2001, Biotechnol., 3, 207-214.
21. St Georgiev, V., Membrane transporters and antifungal drug resistance. Curr. Drug Targets, 2000, 1, 261-284.
22. Vanden Bossche, H., Dromer, F., Improvisi, L., Lozano-Chiu, M., Rex, J. H. and Sanglard, D., Antifungal drug resistance in pathogenic fungi. Med. Mycol., 1998, 36, 119-128.
23. White, T. C., Marr, K. A. and Bowden, R. A., Clinical, cellular and molecular factors that contribute to antifungal drug resistance. Clin. Microbiol. Rev., 1998, 11, 382-402.
24. Decottignies, A. et al., The pleiotropic drug ABC transporters from Saccharomyces cerevisiae., 2002, 155-176.
25. Michaelis, S. and Berkower, C., Sequence comparison of yeast ATP-binding cassette proteins. Cold Spring Harbor Symp. Quant. Biol., LX, 1995, 291-307.
26. Calderone, R. A. and Cihlar, R. L., Fungal Pathogenesis: Principles and Clinical Applications, Marcel Dekker, New York, 2002.
27. Orozco, A. S. et al., Mechanism of fluconazole resistance in Candida krusei. Antimicrob. Agents Chemother., 1998, 42, 2645-2649.
28. Johnstone, R. W., Ruefli, A. A. and Smyth, M. J., Mulitple physiological functions for multidrug transporter P-glycoprotein. Trends Biochem. Sci., 2000, 25, 1-6.
29. Balan, I., Alarco, A. M. and Raymond, M., The Candida albicans CDR3 gene codes for an opaque-phase ABC transporter. J. Bacteriol., 1997, 179, 7210-7218.
30. Franz, R., Michel, S. and Morschhauser, J., A fourth gene from the Candida albicans CDR family of ABC transporters. Gene, 1998, 220, 91-98.
31. McGrath, J. P. and Vershavsky, A., The yeast STE6 gene encodes a homologue of the mammalian multidrug resistance P-glycoprotein. Nature, 1989, 340, 400-404.
32. Prasad, R., Panwar, S. L. and Smriti, Drug resistance in yeast - an emerging scenario. In Advances in Microbial Physiology (ed. Poole, R. K.), Academic Press, 2002, vol. 46, pp. 156-201.
33. Loo, W. T. and Clark, M., Defining the drug binding site in the human multidrug resistance P-glycoprotein using a methanethiosulfonate analog of verapamil, MTS-verapamil. J. Biol. Chem., 2001, 276, 14972-14979.
34. Loo, W. T. and Clark, M., Location of the rhodamine-binding site in the human multidrug resistance P-glycoprotein. J. Biol. Chem., 2002, 277, 44332-44338.
35. Krishnamurthy, S. et al., Deletion of transmembrane domain 12 of CDR1, a multidrug transporter from Candida albicans, leads to altered drug specificity: expression of a yeast multidrug transporter in Baculovirus expression system. Yeast, 1998, 14, 535-550.
36. Egner, R., Rosenthal, F. E., Kralli, A., Sanglard, D. and Kuchler, K., Genetic separation of FK506 susceptibility and drug transport in the yeast Pdr5 ATP-binding cassette multidrug resistance transporter. Mol. Biol. Cell, 1998, 9, 523-543.
37. Egner, R., Bauer, B. E. and Kuchler, K., The transmembrane domain 10 of the yeast Pdr5p ABC antifungal efflux pump determines the substrate specificity and inhibitor susceptibility. Mol. Microbiol., 2000, 35, 1255-1263.
38. Borges-Walmsley, M. I. and Walmsley, A. R., The structure and function of drug pumps. Trends Microbiol., 2001, 9, 71-79.
39. Rosenberg, M. F., Callaghan, R., Ford, R. C. and Higgins, C. F., Structure of the multidrug resistance P-glycoprotein to 2.5 nm resolution determined by electron microscopy and image analysis. J. Biol. Chem., 1997, 272, 10685-10694.
40. Chang, G. and Roth, C. B., Structure of MsbA from E. coli, A homolog of the multidrug resistance ATP binding cassette (ABC) transporters. Science, 2001, 293, 1793-1798.
41. Balzi, E., Wang, M., Leterme, S., Van Dyck, L. and Goffeau, A., PDR5, a novel yeast multidrug resistance conferring transporter controlled by the transcription regulator PDR1. J. Biol. Chem., 1994, 269, 2206-2214.
42. Berkower, C. and Michaelis, S., Mutational analysis of the yeast a-factor transporter STE6, a member of the ATP binding cassette (ABC) protein superfamily. EMBO J., 1991, 10, 3777-3785.
43. Kralli, A., Bohen, S. P. and Yamamoto, K. R., LEM1, an ATP-binding-cassette transporter, selectively modulates the biological potency of steroid hormones. Proc. Natl. Acad. Sci. USA, 1995, 92, 4701-4705.
44. Sanglard, D., Ischer, F., Calabrese, D., de Micheli, M. and Bille, J., Multiple resistance mechanism to azole antifungals in yeast clinical isolates. Drug Resist. Updates, 1998, 1, 255-265.
45. Decottignies, A. et al., Identification and characterisation of SNQ2, a new multidrug ATP binding cassette transporter of the yeast plasma membrane. J. Biol. Chem., 1995, 270, 18150-18157.
46. Katzmann, D. J., Hallstrom, T. C., Voet, M., Wysock, W., Golin, J., Volckert, G. and Moye-Rowley, W. S., Expression of an ATP-binding cassette transporter-encoding gene (YOR1) is required for oligomycin resistance in Saccharomyces cerevisiae. Mol. Cell. Biol., 1995, 15, 6875-6883.
47. Servos, J., Haase, E. and Brendel, M., 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., 1993, 236, 214-218.
48. Szczypca, M. S., Wemmie, J. A., Moye-Rowley, W. S. and Thiele, D. J., A yeast metal resistance protein similar to human cystic fibrosis transmembrane conductance regulator (CFTR) and multidrug resistance-associated protein. J. Biol. Chem., 1994, 269, 22853-22857.
49. Li, Z. S., Szczypka, M., Lu, Y.-P., Thiele, D. J. and Rea, P. A., The yeast cadmium factor protein (YCF1) is a vacuolar glutathione S-conjugate pump. J. Biol. Chem., 1996, 271, 6509-6517.
50. Wemmie, J. A. and Moye-Rowley, W. S., Mutational analysis of the Saccharomyces cerevisiae ATP-binding cassette transporter protein Ycf1p. Mol. Microbiol., 1997, 25, 683-694.
51. Kolaczkowski, M., Kolaczkowska, A., Luczynski, J., Witek, S. and Goffeau, A., In vivo characterization of the drug resistance profile of the major ABC transporters and other components of the yeast pleiotropic drug resistance network. Microb. Drug Resist., 1998, 4, 143-158.
52. Prasad, R., Worgifosse, P. D., Goffeau, A. and Balzi, E., Molecular cloning and characterisation of a novel gene of C. albicans, CDR1, conferring multiple resistance to drugs and antifungals. Curr. Genet., 1995, 27, 320-329.
53. Sanglard, D., Ischer, F., Monod, M. and Bille, J., Cloning of Candida albicans genes conferring resistance to azole antifungal agents, Characterisation of CDR2, a new multidrug ABC transporter gene. Microbiology, 1997, 143, 405-416.
54. Krishnamurthy, S., Gupta, V., Prasad, R., Panwar, S. L. and Prasad, R., Expression of CDR1, a multidrug resistance gene of Candida albicans: In vitro transcriptional activation by heat shock, drugs and human steroid hormones. FEMS Microbiol. Lett., 1998, 160, 191-197.
55. Lyons, C. N. and White, T. C., Transcriptional analyses of antifungal drug resistance in Candida albicans. Antimicrob. Agents Chemother., 2000, 44, 2296-2303.
56. Sanglard, D., Ischer, F., Monod, M., Dogra, S., Prasad R. and Bille, J., ASM Conference on Candida and Candidiasis. Abstr., C27, 1999.
57. Walsh, T. J., Kasai, M., Francesconi, A., Landsman, D. and Chanock, S. J., New evidence that Candida albicans possesses additional ATP-binding cassette MDR-like genes, implications for antifungal azole resistance. J. Med. Vet. Mycol., 1997, 35, 133-137.
58. Egner, R. and Kuchler, K., The yeast multidrug transporter Pdr5 of the plasma membrane is ubiquitinated prior to endocytosis and degradation in the vacuole. FEBS Lett., 1996, 378, 177-181.
59. Piper, P. et al., The Pdr12 ABC transporter is required for the development of weak organic acid resistance in Yeast, EMBO J., 1998, 17, 4257-4265.
60. Holyoak, C. D., Bracey, D., Piper, P. W., Kuchler, K. and Coote, P. J., The Saccharomyces cerevisiae weak-acid-inducible ABC transporter Pdr12 transports fluorescein and preservative anions from the cytosol by an energy-dependent mechanism. J. Bacteriol., 1998, 181, 4644-4652.
61. Holyoak, C. D. et al., Loss of Cmk1 Ca(2+)-calmodulin-dependent protein kinase in yeast results in constitutive weak organic acid resistance, associated with a post-transcriptional activation of the Pdr12 ATP-binding cassette transporter. Mol. Microbiol., 2000, 37, 595-605.
62. Chen, J. X., Bauer, B. E., Kuchler, K. and Clark-Walker, G. D., Positive and negative control of multidrug resistance by the Sit4 protein phosphatase in Kluyveromyces lactis. J. Biol. Chem., 2000, 275, 14865-14872.
63. Wada, S, Niimi, M., Niimi, K., Holmes, A. R., Monk, B. C., Cannon, R. D. and Uehara, Y., Candida glabrata ATP-binding cassette transporters Cdr1p and Pdh1p expressed in a Saccharomyces cerevisiae strain deficient in membrane transporters show phosphorylation-dependent pumping properties. J. Biol. Chem., 2002, 277, 46809-46821.
64. Piper, P., Calderone, C. O., Hatzixanthis, K. and Mollapour, M., Weak acid adaptation: the stress response that confers yeasts with resistance to organic acid food preservatives. Microbiology, 2001, 147, 2635-2642.
65. Ueda, K. et al., Human P-glycoprotein transports cortisol, aldosterone and dexamethasone, but not progesterone. J. Biol. Chem., 1992, 267, 24248-24252.
66. Yang, C. P., Cohen, D., Greenberger, L. M., Hsu, S. I. and Horwitz, S. B., Differential transport properties of two mdr gene products are distinguished by progesterone. J. Biol. Chem., 1990, 265, 10282.
67. Gilbert, D. M., Heery, D. M., Losson, R., Chambon, P. and Lemoine, Y., Estradiol-inducible squelching and cell growth arrest by a chimeric VP16-estrogen receptor expressed in Saccharomyces cerevisiae: suppression by an allele of PDR1. Mol. Cell. Biol., 1993, 13, 462-472.
68. Kolaczkowski, M., van der Rest, M. E., Cybularz-Kolaczkowska, A., Soumillion, J.-P., Konings, W. N. and Goffeau, A., Anticancer drugs, ionophoric peptides, and steroids as substrates of the yeast multidrug transporter Pdr5p. J. Biol. Chem., 1996, 271, 31543-31548.
69. Mahe, Y., Lemoine, Y. and Kuchler, K., The ATP binding cassette transporters Pdr5 and Snq2 of Saccharomyces cerevisiae can mediate transport of steroids in vivo. J. Biol. Chem., 1996, 271, 26167-26172.
70. Krishnamurthy, S., Gupta, V., Snehlata, P. and Prasad, R., Characterisation of human steroid hormone transport mediated by Cdr1p, multidrug transporter of Candida albicans, belonging to the ATP binding cassette super family. FEMS Microbiol. Lett., 1998, 158, 69-74.
71. Kontoyiannis, D. P., Efflux mediated resistance to fluconazole could be modulated by sterol homeostasis in Saccharomyces cerevisiae. J. Antimicrob. Chemother., 2000, 46, 199-203.
72. Kaur, R. and Bachhawat, A. K., The yeast multidrug resistance pump, Pdr5p, confers reduced drug resistance in erg mutants of Saccharomyces cerevisiae. Microbiology, 1999, 145, 809-818.
73. Debry, P., Nash, E. A., Nekalson, D. W. and Metherall, J. E., Role of multidrug resistance P-glycoproteins in cholesterol esterification. J. Biol. Chem., 1997, 272, 1026-1031.
74. Metherall, J. E., Li, H. and Waugh, K., Role of multidrug resistance P-glycoproteins in cholesterol biosynthesis. J. Biol. Chem., 1996, 271, 2634-2640.
75. Wilcox, L. J., Balderes, D. A., Wharton, B., Tinkelenberg, A. H., Rao, G. and Sturley, S. L., Transcriptional profiling identifies two members of the ATP-binding cassette transporter superfamily required for sterol uptake in yeast, J. Biol. Chem., 2002, 277, 32466-32472.
76. Emter, R., Hesse-Peck, A. and Kralli, A., ERG6 and PDR5 regulate small lipophilic drug accumulation in yeast via distinct mechanisms. FEBS Lett., 2002, 521, 57-61.
77. Mukopadhyay, K., Kohli, A. and Prasad, R., Drug susceptibilities of yeast cells are affected by membrane lipids composition. Antimicrob. Agents Chemother., 2002, 46, 3695-3705.
78. Diaz, C. and Schroit, A. J., Role of translocases in the generation of phosphatidylserine asymmetry. J. Membr. Biol., 1996, 151, 1-9.
79. Williamson, P. and Schlegel, R. A., Back and forth: the regulation and function of transbilayer phopholipid movement in eukaryotic cells. Mol. Membr. Biol., 1997, 11, 199-216.
80. Herrmann, A. and Devaux, P. F., Alteration of the aminophospholipid translocase activity during in vivo and artificial aging of human erythrocytes. Biochim. Biophys. Acta, 1990, 1027, 41-46.
81. Toti, F. et al., Another link between phospholipid transmembrane migration and ABC transporter gene family, inferred from a rare inherited disorder of phosphatidylserine externalisation. Biochem. Biophys. Res. Commun., 1997, 241, 548-552.
82. Utsugi, T., Schroit, A. J., Connor, J., Bucana, C. D. and Fidler, I. J., Elevated expression of phosphatidylserine in outer membrane leaflet of human tumour cells and recognition by activated human blood monocytes. Cancer Res., 1991, 51, 3062-3066.
83. Van Helvoort, A., Smith, A. J., Sprong, H., Fritzche, I., Schinkel, A. H., Borst, P. and Van Meer, G., MDR1 P-glycoprotein is a lipid translocase of broad specifity, while MDR3 P-glycoprotein specifically translocates phosphatidylcholine. Cell, 1996, 87, 507-517.
84. Dogra, S., Krishnamurthy, S., Gupta, V., Dixit, B. L., Gupta, C. M., Sanglard, D. and Prasad, R., Asymmetric distribution of phosphatidylethanolamine in C. albicans, possible mediation by CDR1, a multidrug transporter belonging to ATP binding cassette (ABC) superfamily. Yeast, 1999, 15, 111-121.
85. Smriti, Krishnamurthy, S., Dixit, B. L., Gupta, C. M., Milewski, S. and Prasad, R., ABC transporters Cdr1p, Cdr2p and Cdr3p of a human pathogen Candida albicans are general phospholipid translocators. Yeast, 2002, 19, 1-16.
86. Decottignies, A., Grant, A. M., Nichols, J. W., De Wet, H., McIntosh, D. B. and Goffeau, A., ATPase and multidrug transport activities of the overexpressed yeast ABC protein Yor1p. J. Biol. Chem., 1998, 273, 12612-12622.
87. Kean, L. S., Grant, A. M., Angeletti, C., Mahe, Y., Kuchler, K., Fuller, R. S. and Nichols, J. W., Plasma membrane translocation of fluorescent-labeled phosphatidylethanolamine is controlled by transcription regulators, PDR1 and PDR3. J. Cell Biol., 1997, 138, 255-270.
88. Frijters, C. M., Ottenhoff, R., Van Wijland, M. J., Van Nieuwkerk, C. M., Groen, A. K. and Oude Elferink, R. P., Regulation of mdr2 P-glycoprotein expression by bile salts. Biochem. J., 1997, 321, 389-395.
89. Silverman, J. A. and Schrenk, D., Hepatic canalicular membrane 4: expression of the multidrug resistance genes in the liver. FASEB J., 1997, 11, 308-313.
90. Urban, M., Bhargava, T. and Hamer, J. E., An ATP-driven efflux pump is a novel pathogenicity factor in rice blast disease. EMBO J., 1999, 18, 512-521.
91. Raymond, M., Gros, P., Whiteway, M. and Thomas, D. Y., Functional complementation of yeast ste6 by a mammalian multidrug resistance mdr gene. Science, 1992, 256, 232-234.
92. Raymond, M., Ruetz, S., Thomas, D. Y. and Gros, P. 1994, Functional expression of P-glycoprotein in Saccharomyces cerevisiae confers cellular resistance to the immunosuppressive and antifungal agent FK520. Mol. Cell. Biol., 14, 277-286.
93. Raymond, M., Dignard, D., Alarco, A. M., Mainville, N., Magee, B. B. and Thomas, D. Y., A Ste6p/P-glycoprotein homologue from the asexual yeast Candida albicans transports the a-factor mating pheromone in Saccharomyces cerevisiae. Mol. Microbiol., 1998, 27, 587-598.
94. Hull, C. M. and Johnson, A. D., Identification of a mating type-like locus in the asexual pathogenic yeast Candida albicans. Science, 1999, 285, 1271-1275.
95. Hull, C. M., Raisner, R. M. and Johnson, A. D., Evidence for mating of the 'asexual' yeast Candida albicans in a mammalian host. Science, 2000, 289, 307-310.
96. Magee, B. B. and Magee, P. T., Induction of mating in Candida albicans by construction of MTLa and MTLα strains. Science, 2000, 289, 310-313.
97. Wadkins, R. M. and Roepe, P. D., Biophysical aspects of P-glycoprotein-mediated multidrug resistance. Int. Rev. Cytol., 1997, 171, 121-165.
98. Roepe, P. D., The role of the MDR protein in altered drug translocation across tumour cell membranes. Biochim. Biophys. Acta, 1995, 1241, 385-406.
99. i homeostasis in multidrug-resistant (MDR) cells: further characterisation of a series of MDR cell lines expressing different levels of P-glycoprotein. Biochemistry, 1993, 32, 11042-11056.
100. Roepe, P. D., Wei, L., Hoffman, M. M. and Fritz, F., Altered drug translocation mediated by the MDR protein: direct, indirect, or both? J. Bioenerg. Biomembr., 1996, 28, 541-554.
101. Fritz, F., Howard, E. M., Hoffman, M. M. and Roepe, P. D., Evidence for altered ion transport in Saccharomyces cerevisiae overexpressing human MDR1 protein. Biochemistry, 1999, 38, 4214-4226.
102. Hoffman, M. M. and Roepe, P. D., Analysis of ion transport perturbations caused by hu MDR1 protein overexpression. Biochemistry, 1997, 36, 11153-11168.
103. Valverde, M. A., Diaz, M. and Sepulveda, F. V., Volume-regulated chloride channels associated with the human multidrug-resistance P-glycoprotein. Nature, 1992, 355, 830-833.
104. Milewski, S., Mignini, F., Prasad, R. and Borowski, E., Unusual susceptibility of a multidrug-resistance yeast strain to peptidic antifungals. Antimicrob. Agents Chemother., 2001, 45, 223-228.
105. Stella, C. A. and Burgos, H. I., Effect of potassium on Saccharomyces cerevisiae resistance to fluconazole. Antimicrob. Agents Chemother., 2001, 45, 1-2.
106. Bissinger, P. H. and Kuchler, K., Molecular cloning and expression of Saccharomyces cerevisiae STS1 gene product, a yeast ABC transporter conferring mycotoxin resistance. J. Biol. Chem., 1994, 269, 4180-4186.
107. Giaever, G. et al., Functional profiling of the Saccharomyces cerevisiae genome. Nature, 2002, 418, 387-391.
108. Wolfger, H., Mane, Y., Parle-McDermott, A., Delahodde, A. and Kuchler, K., The yeast ATP binding cassette (ABC) protein genes PDR10 and PDR15 are novel targets for the Pdr1 and Pdr3 transcriptional regulators. FEBS Lett., 1997, 418, 269-274.
109. Zhifeng C., Hirata, D., Tsuchiya, E., Osada, H. and Miyakawa, T., The multidrug resistance-associated protein (MRP) subfamily (Yrs1/Yor1) of Saccharomyces cerevisiae is important for the tolerance to a broad range of organic anions. J. Biol. Chem., 1996, 271, 14712-14716.
110. Ortiz, D. F., St Pierre, M. V., Abdulmessih, A. and Arias, I. M., A yeast ATP-binding cassette-type protein mediating ATP-dependent bile acid transport. J. Biol. Chem., 1997, 272, 15358-15365.
111. Leighton, J. and Schatz, G., An ABC transporter in the mitochondrial inner membrane is required for normal growth of Yeast. EMBO J., 1995, 14, 188-195.
112. Dean, M. et al., Mapping and sequencing of two yeast genes belonging to the ATP-binding cassette superfamily. Yeast, 1994, 10, 377-383.
113. Shani, N., Sapag, A. and Valle, D., Characterisation and analysis of conserved motifs in a peroxisomal ATP-binding cassette transporter. J. Biol. Chem., 1996, 271, 8725-8730.
114. +, a novel gene of Schizosaccharomyces pombe which confers brefeldin A resistance, is structurally related to the ATP-binding cassette superfamily. J. Bacteriol., 1995, 177, 1536-1543.
115. Christensen, P. U., Davey, J. and Nielsen, O., The Schizosaccharomyces pombe mam1 gene encodes an ABC transporter mediating secretion of M-factor. Mol. Gen. Genet., 1997, 255, 226-236.
116. Nishi, K., Yoshida, M., Nishimura, M., Nishikawa, M., Nishiyama, M., Horinouchi, S. and Beppu, T., A leptomycin B resistance gene of Schizosaccharomyces pombe encodes a protein similar.to the mammalian P-lycoproteins. Mol. Microbiol., 1992, 6, 761-769.
117. Christensen, P. U., Davis, K., Nielsen, O. and Davey, J., Abc1: a new ABC transporter from the fission yeast Schizosaccharomyces pombe. FEMS Microbiol. Lett., 1997, 147, 97-102.
118. Ortiz, D. F., Ruscitti, T., McCue, K. F. and Ow, D. W., Transport of metal-binding peptides by HMT1, a fission yeast ABC-type vacuolar membrane protein. J. Biol. Chem., 1995, 270, 4721-4728.
119. Ogawa, A., Hashida-Okado, T., Endo, M., Tsuruo, T., Takesako, K. and Kato, I., Role of ABC transporters in aureobasidin A resistance. Antimicrob. Agents Chemother., 1998, 42, 755-761.
120. Theiss, S., Agabian, N. and Kohler, G., ASM Conference on Candida and Candidiasis, Abstr., 1999, pp. 56-57.
121. Sanglard, D., Ischer, F., Calabrese, D., Majcherczyk, P. A. and Bille, J., The ATP binding cassette transporter gene CgCDR1 from Candida glabrata is involved in the resistance of clinical isolates to azole antifungal agents. Antimicrob. Agents Chemother., 1999, 4, 2753-2765.
122. Miyazaki, H. et al., Fluconazole resistance associated with drug efflux and increased transcription of a drug transporter gene, PDH1, in Candida glabrata. Antimicrob. Agents Chemother., 1998, 42, 1695-1701.
123. Sanglard, D., Ischer, F. and Bille, J., ASM Conference on Candida and Candidiasis, Abstr., 1999, p. 55.
124. Moran, G. P., Sanglard, D., Donnelly, S. M., Shanley, D. B., Sullivan, D. J. and Coleman, D. C., Identification and expression of multidrug transporters responsible for fluconazole resistance in Candida dubliniensis. Antimicrob. Agents Chemother., 1998, 42, 1819-1830.
125. Katiyar, S. K. and Edlind, T. D., Identification and expression of multidrug resistance-related ABC transporter gene in Candida krusei. Med. Mycol., 2001, 39, 109-116.