Toward understanding the mechanism of action of the yeast multidrug resistance transporter Pdr5p: A molecular modeling study

Journal of Structural Biology

Volumn 173, Issue 2, 2011, Pages 333-344

  Rutledge, Robert M ^a   Esser, Lothar ^a   Ma, Jichun ^a   Xia, Di ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

ABC transporter; Homology modeling; Membrane protein; Nucleotide binding domain; Substrate specificity; Transmembrane domain

Indexed keywords

ABC TRANSPORTER; CLOTRIMAZOLE; MEMBRANE PROTEIN; NUCLEOTIDE BINDING PROTEIN; PLEOTROPIC DRUG RESISTANT PROTEIN 5; UNCLASSIFIED DRUG;

AB INITIO CALCULATION; AMINO ACID SEQUENCE; ANIMAL CELL; ANTIFUNGAL RESISTANCE; ARTICLE; FUNGUS MUTANT; FUNGUS MUTATION; LIPOPHILICITY; MOLECULAR MODEL; MOUSE; NONHUMAN; PRIORITY JOURNAL; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; YEAST;

ATP-BINDING CASSETTE TRANSPORTERS; BLOTTING, WESTERN; MICROBIAL SENSITIVITY TESTS; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SACCHAROMYCES CEREVISIAE PROTEINS;

SACCHAROMYCES CEREVISIAE;

EID: 78751582384     PISSN: 10478477     EISSN: 10958657     Source Type: Journal    
DOI: 10.1016/j.jsb.2010.10.012     Document Type: Article

References (61)

1. Adamian L., Liang J. Prediction of transmembrane helix orientation in polytopic membrane proteins. BMC Struct. Biol. 2006, 6:13.
2. Albrecht M., Tosatto S.C., Lengauer T., Valle G. Simple consensus procedures are effective and sufficient in secondary structure prediction. Protein Eng. 2003, 16:459-462.
3. Aller S.G., Yu J., Ward A., Weng Y., Chittaboina S., Zhuo R., Harrell P.M., Trinh Y.T., Zhang Q., Urbatsch I.L., Chang G. Structure of P-glycoprotein reveals a molecular basis for poly-specific drug binding. Science 2009, 323:1718-1722.
4. Brunger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., Jiang J.S., Kuszewski J., Nilges M., Pannu N.S., Read R.J., Rice L.M., Simonson T., Warren G.L. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 1998, 54:905-921.
5. Chen J.H., Chang X.B., Aleksandrov A.A., Riordan J.R. CFTR is a monomer: biochemical and functional evidence. J. Membr. Biol. 2002, 188:55-71.
6. Claros M.G., von Heijne G. TopPred II: an improved software for membrane protein structure predictions. Comput. Appl. Biosci. 1994, 10:685-686.
7. Davidson A.L., Chen J. ATP-binding cassette transporters in bacteria. Annu. Rev. Biochem. 2004, 73:241-268.
8. Davidson A.L., Maloney P.C. ABC transporters: how small machines do a big job. Trends Microbiol. 2007, 15:448-455.
9. Dawson R.J., Locher K.P. Structure of a bacterial multidrug ABC transporter. Nature 2006, 443:180-185.
10. de Thozee C.P., Cronin S., Goj A., Golin J., Ghislain M. Subcellular trafficking of the yeast plasma membrane ABC transporter, Pdr5, is impaired by a mutation in the N-terminal nucleotide-binding fold. Mol. Microbiol. 2007, 63:811-825.
11. DeGorter M.K., Conseil G., Deeley R.G., Campbell R.L., Cole S.P. Molecular modeling of the human multidrug resistance protein 1 (MRP1/ABCC1). Biochem. Biophys. Res. Commun. 2008, 365:29-34.
12. Egner R., Bauer B.E., Kuchler K. The transmembrane domain 10 of the yeast Pdr5p ABC antifungal efflux pump determines both substrate specificity and inhibitor susceptibility. Mol. Microbiol. 2000, 35:1255-1263.
13. Egner R., Rosenthal F.E., Kralli A., Sanglard D., 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.
14. Ernst R., Kueppers P., Klein C.M., 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.
15. Ferreira-Pereira A., Marco S., Decottignies A., Nader J., Goffeau A., Rigaud J.L. Three-dimensional reconstruction of the Saccharomyces cerevisiae multidrug resistance protein Pdr5p. J. Biol. Chem. 2003, 278:11995-11999.
16. Finn R.D., Mistry J., Schuster-Bockler B., Griffiths-Jones S., Hollich V., Lassmann T., Moxon S., Marshall M., Khanna A., Durbin R., Eddy S.R., Sonnhammer E.L., Bateman A. Pfam: clans, web tools and services. Nucleic Acids Res. 2006, 34:D247-D251.
17. Forrest L.R., Tang C.L., Honig B. On the accuracy of homology modeling and sequence alignment methods applied to membrane proteins. Biophys. J. 2006, 91:508-517.
18. Galperin M.Y. The molecular biology database collection: 2008 update. Nucleic Acids Res. 2008, 36:D2-D4.
19. Gerber S., Comellas-Bigler M., Goetz B.A., Locher K.P. Structural basis of trans-inhibition in a molybdate/tungstate ABC transporter. Science 2008, 321:246-250.
20. Golin J., Ambudkar S.V., Gottesman M.M., Habib A.D., Sczepanski J., Ziccardi W., May L. Studies with novel Pdr5p substrates demonstrate a strong size dependence for xenobiotic efflux. J. Biol. Chem. 2003, 278:5963-5969.
21. Golin J., Kon Z.N., Wu C.P., Martello J., Hanson L., Supernavage S., Ambudkar S.V., Sauna Z.E. 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.
22. Gottesman M.M., Ambudkar S.V. Overview: ABC transporters and human disease. J. Bioenerg. Biomembr. 2001, 33:453-458.
23. Hall T.A. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 1999, 41:95-98.
24. Hanson L., May L., Tuma P., Keeven J., Mehl P., Ferenz M., Ambudkar S.V., Golin J. The role of hydrogen bond acceptor groups in the interaction of substrates with Pdr5p, a major yeast drug transporter. Biochemistry 2005, 44:9703-9713.
25. Hennig L. WinPep 2.11: novel software for PC-based analyses of amino acid sequences. Prep. Biochem. Biotechnol. 2001, 31:201-207.
26. Higgins C.F. ABC transporters: physiology, structure and mechanism - an overview. Res. Microbiol. 2001, 152:205-210.
27. Hirokawa T., Boon-Chieng S., Mitaku S. SOSUI: classification and secondary structure prediction system for membrane proteins. Bioinformatics 1998, 14:378-379.
28. Hofmann K., Stoffel W. TMbase - a database of membrane spanning proteins segments. Biol. Chem. Hoppe-Seyler 1993, 347:166.
29. Jha S., Dabas N., Karnani N., Saini P., Prasad R. ABC multidrug transporter Cdr1p of Candida albicans has divergent nucleotide-binding domains which display functional asymmetry. FEMS Yeast Res. 2004, 5:63-72.
30. Jones T.A., Zou J.Y., Cowan S.W., Kjeldgaard M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A 1991, 47(Pt 2):110-119.
31. Jordan I.K., Kota K.C., Cui G., Thompson C.H., McCarty N.A. Evolutionary and functional divergence between the cystic fibrosis transmembrane conductance regulator and related ATP-binding cassette transporters. Proc. Natl. Acad. Sci. USA 2008, 105:18865-18870.
32. Juretic D., Zoranic L., Zucic D. Basic charge clusters and predictions of membrane protein topology. J. Chem. Inf. Comput. Sci. 2002, 42:620-632.
33. Kolaczkowski M., van der Rest M., Cybularz-Kolaczkowska A., Soumillion J.P., Konings W.N., Goffeau A. Anticancer drugs, ionophoric peptides, and steroids as substrates of the yeast multidrug transporter Pdr5p. J. Biol. Chem. 1996, 271:31543-31548.
34. Krogh A., Larsson B., von Heijne G., Sonnhammer E.L. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 2001, 305:567-580.
35. Laskowski R.A., MacArthur M.W., Moss D.S., Thornton J.M. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Cryst. 1993, 26:283-291.
36. Leppert G., McDevitt R., Falco S.C., Van Dyk T.K., Ficke M.B., Golin J. Cloning by gene amplification of two loci conferring multiple drug resistance in Saccharomyces. Genetics 1990, 125:13-20.
37. Liu H.L., Hsu J.P. Recent developments in structural proteomics for protein structure determination. Proteomics 2005, 5:2056-2068.
38. Loo T.W., Clarke D.M. The minimum functional unit of human P-glycoprotein appears to be a monomer. J. Biol. Chem. 1996, 271:27488-27492.
39. Meller J., Elber R. Linear programming optimization and a double statistical filter for protein threading protocols. Proteins 2001, 45:241-261.
40. Meyers S., Schauer W., Balzi E., Wagner M., Goffeau A., Golin J. Interaction of the yeast pleiotropic drug resistance genes PDR1 and PDR5. Curr. Genet. 1992, 21:431-436.
41. Mishra N.N., Prasad T., Sharma N., Payasi A., Prasad R., Gupta D.K., Singh R. Pathogenicity and drug resistance in Candida albicans and other yeast species. A review. Acta Microbiol. Immunol. Hung. 2007, 54:201-235.
42. Moretti S., Armougom F., Wallace I.M., Higgins D.G., Jongeneel C.V., Notredame C. The M-Coffee web server: a meta-method for computing multiple sequence alignments by combining alternative alignment methods. Nucleic Acids Res 2007, 35:W645-W648.
43. Pettersen E.F., Goddard T.D., Huang C.C., Couch G.S., Greenblatt D.M., Meng E.C., Ferrin T.E. UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 2004, 25:1605-1612.
44. Qin L., Zheng J., Grant C.E., Jia Z., Cole S.P., Deeley R.G. Residues responsible for the asymmetric function of the nucleotide binding domains of multidrug resistance protein 1. Biochemistry 2008, 47:13952-13965.
45. Ravna A.W., Sylte I., Sager G. Molecular model of the outward facing state of the human P-glycoprotein (ABCB1), and comparison to a model of the human MRP5 (ABCC5). Theor. Biol. Med. Model 2007, 4:33.
46. Rea P.A. MRP subfamily ABC transporters from plants and yeast. J. Exp. Biol. 1999, 50:895-913.
47. Riordan J.R. Assembly of functional CFTR chloride channels. Annu. Rev. Physiol. 2005, 67:701-718.
48. Rogers B., Decottignies A., Kolaczkowski M., Carvajal E., Balzi E., Goffeau A. The pleiotropic drug ABC transporters from Saccharomyces cerevisiae. J. Mol. Microbiol. Biotechnol. 2001, 3:207-214.
49. Rost B. PHD: predicting one-dimensional protein structure by profile-based neural networks. Methods Enzymol. 1996, 266:525-539.
50. Rost B., Yachdav G., Liu J. The PredictProtein server. Nucleic Acids Res. 2004, 32:W321-W326.
51. Sauna Z.E., Bohn S.S., Rutledge R., Dougherty M.P., Cronin S., May L., Xia D., Ambudkar S.V., Golin J. Mutations define cross-talk between the N-terminal nucleotide-binding domain and transmembrane helix-2 of the yeast multidrug transporter Pdr5: possible conservation of a signaling interface for coupling ATP hydrolysis to drug transport. J. Biol. Chem. 2008, 283:35010-35022.
52. Schmitt L., Tampe R. Structure and mechanism of ABC transporters. Curr. Opin. Struct. Biol. 2002, 12:754-760.
53. Schmitt L., Benabdelhak H., Blight M.A., Holland I.B., Stubbs M.T. Crystal structure of the nucleotide-binding domain of the ABC-transporter haemolysin B: identification of a variable region within ABC helical domains. J. Mol. Biol. 2003, 330:333-342.
54. Schultz J., Milpetz F., Bork P., Ponting C.P. SMART, a simple modular architecture research tool: identification of signaling domains. Proc. Natl. Acad. Sci. USA 1998, 95:5857-5864.
55. Sharom F.J. ABC multidrug transporters: structure, function and role in chemoresistance. Pharmacogenomics 2008, 9:105-127.
56. Sipos G., Kuchler K. Fungal ATP-binding cassette (ABC) transporters in drug resistance & detoxification. Curr. Drug Targets 2006, 7:471-481.
57. Thompson J.D., Thierry J.C., Poch O. RASCAL: rapid scanning and correction of multiple sequence alignments. Bioinformatics 2003, 19:1155-1161.
58. Tutulan-Cunita A.C., Mikoshi M., Mizunuma M., Hirata D., Miyakawa T. Mutational analysis of the yeast multidrug resistance ABC transporter Pdr5p with altered drug specificity. Genes Cells 2005, 10:409-420.
59. van Geest M., Lolkema J.S. Membrane topology and insertion of membrane proteins: search for topogenic signals. Microbiol. Mol. Biol. Rev. 2000, 64:13-33.
60. von Heijne G. Mitochondrial targeting sequences may form amphiphilic helices. EMBO J. 1986, 5:1335-1342.
61. von Heijne G. Membrane proteins: from sequence to structure. Annu. Rev. Biophys. Biomol. Struct. 1994, 23:167-192.