Multidrug resistance transporters Snq2p and Pdr5p mediate caffeine efflux in Saccharomyces cerevisiae

References

• Dews PB. Caffeine. Annu. Rev. Nutr. 1982;2:323–341.10.1146/annurev.nu.02.070182.001543
   PubMed Web of Science ®Google Scholar
• Dews PB, O’Brien CP, Bergman J. Caffeine: behavioral effects of withdrawal and related issues. Food Chem. Toxicol. 2002;40:1257–1261.10.1016/S0278-6915(02)00095-9
   PubMed Web of Science ®Google Scholar
• Ferguson LR, Philpott M. Nutrition and mutagenesis. Annu. Rev. Nutr. 2008;28:313–329.10.1146/annurev.nutr.28.061807.155449
   PubMed Web of Science ®Google Scholar
• Zhou H, Luo Y, Huang S. Updates of mTOR inhibitors. Anticancer Agents Med. Chem. 2010;10:571–81.10.2174/187152010793498663
   PubMed Web of Science ®Google Scholar
• Rockenfeller P1, Madeo F. Ageing and eating. Biochim. Biophys. Acta. 2010;1803(4):499–506.10.1016/j.bbamcr.2010.01.001
   PubMed Web of Science ®Google Scholar
• Paumi CM, Chuk M, Snider J, Stagljar I, Michaelis S. ABC transporters in Saccharomyces cerevisiae and their interactors: New technology advances the biology of the ABCC (MRP) subfamily. Microbiol. Mol. Biol. Rev. 2009;73:577–593.10.1128/MMBR.00020-09
   PubMed Web of Science ®Google Scholar
• Prasad R, Goffeau A. Yeast ATP-binding cassette transporters conferring multidrug resistance. Annu. Rev. Microbiol. 2012;66:39–63.10.1146/annurev-micro-092611-150111
   PubMed Web of Science ®Google Scholar
• Nakajima T, Aoyama T. Polymorphism of drug-metabolizing enzymes in relation to individual susceptibility to industrial chemicals. Ind. Health. 2000;38(2):143–152.10.2486/indhealth.38.143
   PubMed Web of Science ®Google Scholar
• Morel M1, Meux E, Mathieu Y, Thuillier A, Chibani K, Harvengt L, Jacquot JP, Gelhaye E. Xenomic networks variability and adaptation traits in wood decaying fungi. Microbiol. Biotechnol. 2013;6:248–263.10.1111/1751-7915.12015
   Web of Science ®Google Scholar
• Kot M1, Daniel WA. Caffeine as a marker substrate for testing cytochrome P450 activity in human and rat. Pharmacol. Rep. 2008;60:789–797.
   PubMed Web of Science ®Google Scholar
• Haase E, Servos J, Brendel M. Isolation and characterization of additional genes influencing resistance to various mutagens in the yeast Saccharomyces cerevisiae. Curr. Genet. 1992;21:319–324.10.1007/BF00351689
   PubMed Web of Science ®Google Scholar
• Servos J, Haase E, 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;236:214–218.10.1007/BF00277115
   PubMedGoogle Scholar
• Leppert G1, McDevitt R, Falco SC, Van Dyk TK, Ficke MB, Golin J. Cloning by gene amplification of two loci conferring multiple drug resistance in Saccharomyces. Genetics. 1990;125:13–20.
   PubMed Web of Science ®Google Scholar
• Mortimer RK, Johnston JR. Genealogy of principal strains of the yeast genetic stock center. Genetics. 1986;113:35–43.
   PubMed Web of Science ®Google Scholar
• Sikorski RS, Hieter P. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics. 1989;122:19–27.
   PubMed Web of Science ®Google Scholar
• Tsujimoto Y, Takase D, Okano H, Tomari N, Watanabe K, Matsui H. Functional roles of YPT31 and YPT32 in clotrimazole resistance of Saccharomyces cerevisiae through effects on vacuoles and ATP-binding cassette transporter(s). J. Biosci. Bioeng. 2013;115:4–11.10.1016/j.jbiosc.2012.08.011
   PubMed Web of Science ®Google Scholar
• Sambrook J, Fritsch EF, Maniatis T. Molecular cloning: a laboratory manual. 2nd ed. Cold Spring Harbor (NY): Cold Spring Harbor Laboratory Press; 1989.
   Google Scholar
• Burke D, Dawson D, Stearns T. Methods in yeast genetics: a Cold Spring Harbor Laboratory course manual. Cold Spring Harbor (NY): Cold Spring Harbor Laboratory Press; 2000.
   Google Scholar
• Sanger F. Determination of nucleotide sequences in DNA. Science. 1981;214:1205–1210.10.1126/science.7302589
   PubMed Web of Science ®Google Scholar
• Ernst R, Kueppers P, Klein CM, Schwarzmueller T, Kuchler K, Schmitt L. A mutation of the H-loop selectively affects rhodamine transport by the yeast multidrug ABC transporter Pdr5. Proc. Natl. Acad. Sci. USA. 2008;105:5069–5074.10.1073/pnas.0800191105
   PubMed Web of Science ®Google Scholar
• Mahé Y, Lemoine Y, Kuchler K. The ATP binding cassette transporters Pdr5 and Snq2 of Saccharomyces cerevisiae can mediate transport of steroids in Vivo. J. Biol. Chem. 1996;271:25167–25172.10.1074/jbc.271.41.25167
   PubMed Web of Science ®Google Scholar
• Rogers B, Decottignies A, Kolaczkowski M, Carvajal E, Balzi E, Goffeau A. The pleitropic drug ABC transporters from Saccharomyces cerevisiae. J. Mol. Microbiol. Biotechnol. 2001;3:207–214.
   PubMed Web of Science ®Google Scholar
• Golin J, Kon ZN, Wu C-P, Martello J, Hanson L, Supernavage S, Ambudkar SV, Sauna ZE. Complete inhibition of the Pdr5p multidrug efflux pump ATPase activity by its transport substrate clotrimazole suggests that GTP as well as ATP may be used as an energy source. Biochemistry. 2007;46:13109–13119.10.1021/bi701414f
   PubMed Web of Science ®Google Scholar
• Kolaczkowski M, van der Rest M, Cybularz-Kolaczkowska A, Soumillion JP, Konings WN, Goffeau A. Anticancer drugs, ionophoric peptides, and steroids as substrates of the yeast multidrug transporter pdr5p. J Biol. Chem. 1996;271:31543–31548.10.1074/jbc.271.49.31543
   PubMed Web of Science ®Google Scholar
• Hendrych T, Kodedová M, Sigler K, Gásková D. Characterization of the kinetics and mechanisms of inhibition of drugs interacting with the S. cerevisiae multidrug resistance pumps Pdr5p and Snq2p. Biochim. Biophys. Acta. 2009;1788:717–723.10.1016/j.bbamem.2008.12.001
   PubMed Web of Science ®Google Scholar
• Ling H, Chen B, Kang A, Lee JM, Chang MW. Transcriptome response to alkane biofuels in Saccharomyces cerevisiae: Identification of efflux pumps involved in alkane tolerance. Biotechnol. Biofuels. 2013;6:95. doi: 10.1186/1754-6834-6-95.10.1186/1754-6834-6-95
   PubMed Web of Science ®Google Scholar
• Nishida N, Ozato N, Matsui K, Kuroda K, Ueda M. ABC transporters and cell wall proteins involved in organic solvent tolerance in Saccharomyces cerevisiae. J. Biotechnol. 2013;165:145–152.10.1016/j.jbiotec.2013.03.003
   PubMed Web of Science ®Google Scholar
• Furman C, Mehla J, Ananthaswamy N, Arya N, Kulesh B, Kovach I, Ambudkar SV, Golin J. The deviant ATP-binding site of the multidrug efflux pump Pdr5 plays an active role in the transport cycle. J. Biol. Chem. 2013;288:30420–30431.10.1074/jbc.M113.494682
   PubMed Web of Science ®Google Scholar
• Downes MT, Mehla J, Ananthaswamy N, Wakschlag A, Lamonde M, Dine E, Ambudkar SV, Golin J. The transmission interface of the Saccharomyces cerevisiae multidrug transporter Pdr5: Val-656 located in intracellular loop 2 plays a major role in drug resistance. Antimicrob. Agents Chemother. 2013;57:1025–1034.10.1128/AAC.02133-12
   PubMed Web of Science ®Google Scholar
• Kueppers P, Gupta RP, Stindt J, Smits SH, Schmitt L. Functional impact of a single mutation within the transmembrane domain of the multidrug ABC transporter Pdr5. Biochemistry. 2013;52:2184–2195.10.1021/bi3015778
   PubMed Web of Science ®Google Scholar
• Chen Z, Li J, Wang W, Guo X, Li Y, Mao X, Chen X, Guan W. Mutations adjacent to the end of transmembrane helices 6 and 7 independently affect drug efflux capacity of yeast ABC transporter Pdr5p. Biochim. Biophys. Acta. 2014;1838:932–939.10.1016/j.bbamem.2013.12.002
   PubMed Web of Science ®Google Scholar
• Gupta RP, Kueppers P, Hanekop N, Schmitt L. Generating symmetry in the asymmetric ATP-binding cassette (ABC) transporter Pdr5 from Saccharomyces cerevisiae. J. Biol. Chem. 2014;289:15272–15279.10.1074/jbc.M114.553065
   PubMed Web of Science ®Google Scholar
• Wieker HJ, Kuschmitz D, Hess B. Inhibition of yeast mitochondrial F1-ATPase, F0F1-ATPase and submitochondrial particles by rhodamines and ethidium bromide. Biochim. Biophys. Acta. 1987;892:108–117.10.1016/0005-2728(87)90253-2
   PubMed Web of Science ®Google Scholar
• Bullough DA, Ceccarelli EA, Roise D, Allison WS. Inhibition of the bovine-heart mitochondrial F1-ATPase by cationic dyes and amphipathic peptides. Biochim. Biophys. Acta. 1989;975:377–383.10.1016/S0005-2728(89)80346-9
   PubMed Web of Science ®Google Scholar
• Kolaczkowska A, Kolaczkowski M, Goffeau A, Moye-Rowley WS. Compensatory activation of the multidrug transporters Pdr5p, Snq2p, and Yor1p by Pdr1p in Saccharomyces cerevisiae. FEBS Lett. 2008;582:977–983.10.1016/j.febslet.2008.02.045
   PubMed Web of Science ®Google Scholar
• Stein WD. Kinetics of the multidrug transporter (P-glycoprotein) and its reversal. Physiol Rev. 1997;77:545–590.
   PubMed Web of Science ®Google Scholar
• Paynter N, Monda KL, Amin N, Fischer K, Renstrom F, Ngwa JS, Huikari V, Cavadino A, Nolte IM, Teumer A, Yu K, Marques-Vidal P, Rawal R, Manichaikul A, Wojczynski MK, Vink JM, Zhao JH, Burlutsky G, Lahti J, Mikkilä V, Lemaitre RN, Eriksson J, Musani SK, Tanaka T, Geller F, Luan J, Hui J, Mägi R, Dimitriou M, Garcia ME, Ho WK, Wright MJ, Rose LM, Magnusson PK, Pedersen NL, Couper D, Oostra BA, Hofman A, Ikram MA, Tiemeier HW, Uitterlinden AG, van Rooij FJ, Barroso I, Johansson I, Xue L, Kaakinen M, Milani L, Power C, Snieder H, Stolk RP, Baumeister SE, Biffar R, Gu F, Bastardot F, Kutalik Z, Jacobs DR Jr, Forouhi NG, Mihailov E, Lind L, Lindgren C, Michaëlsson K, Morris A, Jensen M, Khaw KT, Luben RN, Wang JJ, Männistö S, Perälä MM, Kähönen M, Lehtimäki T, Viikari J, Mozaffarian D, Mukamal K, Psaty BM, Döring A, Heath AC, Montgomery GW, Dahmen N, Carithers T, Tucker KL, Ferrucci L, Boyd HA, Melbye M, Treur JL, Mellström D, Hottenga JJ, Prokopenko I, Tönjes A, Deloukas P, Kanoni S, Lorentzon M, Houston DK, Liu Y, Danesh J, Rasheed A, Mason MA, Zonderman AB, Franke L, Kristal BS; International parkinson’s disease genomics consortium (IPDGC); North American Brain Expression Consortium (NABEC); UK Brain Expression Consortium (UKBEC), Karjalainen J, Reed DR, Westra HJ, Evans MK, Saleheen D, Harris TB, Dedoussis G, Curhan G, Stumvoll M, Beilby J, Pasquale LR, Feenstra B, Bandinelli S, Ordovas JM, Chan AT, Peters U, Ohlsson C, Gieger C, Martin NG, Waldenberger M, Siscovick DS, Raitakari O, Eriksson JG, Mitchell P, Hunter DJ, Kraft P, Rimm EB, Boomsma DI, Borecki IB, Loos RJ, Wareham NJ, Vollenweider P, Caporaso N, Grabe HJ, Neuhouser ML, Wolffenbuttel BH, Hu FB, Hyppönen E, Järvelin MR, Cupples LA, Franks PW, Ridker PM, van Duijn CM, Heiss G, Metspalu A, North KE, Ingelsson E, Nettleton JA, van Dam RM, Chasman DI. Genome-wide meta-analysis identifies six novel loci associated with habitual coffee consumption. Mol Psychiatry. Forthcoming. doi:10.1038/mp.2014.107.
   PubMed Web of Science ®Google Scholar