Chimeras of the ABC drug transporter Cdr1p reveal functional indispensability of transmembrane domains and nucleotide-binding domains, but transmembrane segment 12 is replaceable with the corresponding homologous region of the non-drug transporter Cdr3p

Microbiology

Volumn 152, Issue 5, 2006, Pages 1559-1573

  Saini, Preeti ^a   Gaur, Naseem Akhtar ^a   Prasad, Rajendra ^a  

^a JAWAHARLAL NEHRU UNIVERSITY   (India)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ANISOMYCIN; CELL MEMBRANE PROTEIN; CYCLOHEXIMIDE; FLUCONAZOLE; ITRACONAZOLE; KETOCONAZOLE; MICONAZOLE; NUCLEOTIDE BINDING PROTEIN; PROTEIN CDR1P; PROTEIN CDR3P; RHODAMINE 6G; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; CANDIDA ALBICANS; CARBOXY TERMINAL SEQUENCE; CELL GROWTH; CELL MEMBRANE TRANSPORT; CELL SURFACE; CHIMERA; COMPLEX FORMATION; CONTROLLED STUDY; DRUG SENSITIVITY; DRUG TRANSPORT; ENZYME SUBSTRATE; FUNGAL STRAIN; GENE CONSTRUCT; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; PROTEIN VARIANT; SEQUENCE HOMOLOGY;

ADENOSINE TRIPHOSPHATASES; ANTIFUNGAL AGENTS; CANDIDA ALBICANS; DRUG RESISTANCE, FUNGAL; FLUCONAZOLE; FUNGAL PROTEINS; MEMBRANE PROTEINS; MEMBRANE TRANSPORT PROTEINS; MICROBIAL SENSITIVITY TESTS; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT FUSION PROTEINS; RHODAMINES;

CANDIDA ALBICANS;

EID: 33646813997     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.28471-0     Document Type: Article

References (39)

1. Aleksandrov, L., Aleksandrov, A. A., Chang, X. & Riordan, J. R. (2002). The first nucleotide-binding domain of CFTR is a site of stable nucleotide intercation whereas the second is a site of rapid turnover. J Biol Chem 277, 15419-15425.
2. Balan, I., Alarco, A. M. & Raymond, M. (1997). The Candida albicans CDR3 gene codes for an opaque-phase ABC transporter. J Bacteriol 179, 7210-7218.
3. Beaudet, L. & Gros, P. (1995). Functional dissection of P-glycoprotein nucleotide binding domains in chimeric and mutant proteins. J Biol Chem 270, 17159-17170.
4. Braun, B. R., Hoog, M. V. H., d'Enfert, C. & 40 other authors (2005). A human curated annotation of Candida albicans genome. PLoS Genet 1, 36-57.
5. Dogra, S., Krishnamurthy, S., Gupta, V., Dixit, B. L., Gupta, C. M., Sanglard, D. & Prasad, R. (1999). Asymmetric distribution of phosphatidylethanolamine in C. albicans: possible mediation by CDR1, A multidrug transporter belonging to ATP binding cassette (ABC) superfamily. Yeast 15, 111-121.
6. Franz, R., Michel, S. & Morschhauser, J. (1998). A fourth gene from the Candida albicans CDR family of ABC transporters. Gene 220, 91-98.
7. Gao, M., Cui, H. R., Loe, D. W., Grant, C. E., Almquist, K. C., Cole, S. P. C. & Deeley, R. G. (2000). Comparison of the functional characteristics of the nucleotide binding domains of the multidrug resistance protein 1. J Biol Chem 275, 13098-13108.
8. Gaur, M., Devapriya, C. & Prasad, R. (2005). The complete inventory of ABC proteins in human pathogenic yeast, Candida albicans. J Mol Microbiol Biotechnol 9, 3-15.
9. Henriksen, U., Gather, U. & Litman, T. (2005). Effect of Walker A mutation (K86M) on oligomerization and surface targeting of the multidrug resistance transporter ABCG2. J Cell Sci 118, 1417-1426.
10. Hrycyna, C. A., Ramachandra, M., Germann, U. A., Chang, P., Wu, Pastan, I. & Gottesman, M. M. (1999). Both ATP sites of human P-glycoprotein are essential but not symmetric. Biochemistry 38, 13887-13899.
11. Jha, S., Karnani, N., Dhar, S. K., Mukhopadhyay, K., Shukla, S., Saini, P., Mukhopadhyay, G. & Prasad, R. (2003a). Purification and charaterization of N-terminal nucleotide binding domain of an ABC drug transporter of Candida albicans- uncommon cysteine 193 of Walker A is critical for ATP hydrolysis. Biochemistry 42, 10822-10832.
12. Jha, S., Karnani, N., Lynn, A. M. & Prasad, R. (2003b). Covalent modification of cysteine 193 impairs ATPase function of nucleotide-binding domain of a Candida drug efflux pump. Biochem Biophys Res Commun 310, 869-875.
13. Jha, S., Dabas, N., Karnani, N., Saini, P. & Prasad, R. (2004). ABC multidrug transporter Cdr1p of Candida albicans has divergent nucleotide-binding domains which display functional asymmetry. FEMS Yeast Res 5, 63-72.
14. Kohli, A., Smriti, Mukhopadhyay, K, Rattan, A. & Prasad, R. (2002). In vitro low-level resistance to azoles in Candida albicans is associated with changes in membrane lipid fluidity and asymmetry. Antimicrob Agents Chermother 46, 1046-1052.
15. Krishnamurthy, S., Gupta, V., Snehlata, P. & Prasad, R. (1998a). 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 158, 69-74.
16. Krishnamurthy, S., Chatterjee, U., Gupta, V., Prasad, R., Das, P., Snehlata, P., Hasnain, S. E. & Prasad, R. (1998b). 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 14, 535-550.
17. Loo, T. W. & Clarke, D. M. (1997). Correction of defective protein kinesis of human P-glycoprotein mutants by substrates and modulators. J Biol Chem 272, 709-712.
18. Morello, J.-P., Petaja-Repo, U. E, Bichet D. G. & Bouvier, M. (2000). Pharmacological chaperones: a new twist on receptor folding. Trends Pharmacol Sci 21, 466-468.
19. Mukhopadhyay, K., Kohli, A. K. & Prasad, R. (2002). Drug susceptibilities of yeast cells are affected by membrane lipid composition. Antimicrob Agents Chemother 46, 3695-3705.
20. Nakamura, K., Niimi, M., Niimi, K., Holmes, A. R., Yates, J. E., Decottignies, A., Monk B. C., Goffeau, A. & Cannon, R. D. (2002). Functional expression of Candida albicans drug efflux pump Cdr1p in a Saccharomyces cerevisiae strain deficient in membrane transporters. Antimicrob Agents Chemother 45, 3366-3374.
21. Ng, W. F., Sarangi, F., Zastawny, R. L., Veinot-Drebot, L. & Ling, V. (1989). Identification of members of the P-glycoprotein multigene family. Mol Cell Biol 9, 1224-1232.
22. Nikaido, K. & Ames, G. F. L. (1999). One intact ATP-binding subunit is sufficient to support ATP hydrolysis and translocation in an ABC transporter, the histidine permease. J Biol Chem 274, 26727-26735.
23. Pollet J.-F., Geffel, J. V., Stevens, E. V., Geffel, R. V., Beauwens, R., Bollen, A. & Jacobs, P. (2000). Expression and intraceflular processing of chimeric and mutant CFTR molecules. Biochim Biophys Acta 1500, 59-69.
24. Prasad, R., Worgifosse, P. D., Goffeau, A. & Balzi, E. (1995). Molecular cloning and characterisation of a novel gene of C. albicans, CDR1, conferring multiple resistance to drugs and antifungals. Curr Genet 27, 320-329.
25. Prasad, R., Krishnamurthy, S., Gupta, V. & Panwar, S. L. (1998). Multidrug transporters of Candida albicans. Folia Microbiol 43, 228.
26. Rice, P., Longden, I. & Bleasby, A. (2000). EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet 16, 276-277.
27. Ruetz, S. & Gros, P. (1994). Phosphatidylcholine translocase: a physiological role for the mdr2 gene. Cell 77, 1071-1081.
28. Sanglard, D., Kuchler, K., Ischer, F., Pagani, J.-L., Monod, M. & Bille, J. (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.
29. Sanglard, D., Ischer, F., Monod, M. & Bille, J. (1997). Cloning of Candida albicans genes conferring resistance to azole antifungal agents: characterization of CDR2, a new multidrug ABC transporter gene. Microbiology 143, 405-416.
30. Sanglard, D., Ischer, F., Monod, M., Dogra, S., Prasad, R. & Bille, J. (1999). Analysis of the ATP-binding cassette (ABC)-transporter gene CDR4 from Candida albicans. In ASM Conference on Candida and Candidiasis, Charleston, SC, USA, March 1-4, p. 56.
31. Shukla, S., Saini, P., Smriti, Jha, S., Ambudkar, S. V. & Prasad, R. (2003). Functional characterization of Candida albicans ABC transporter Cdr1p. Eukaryot Cell 2, 1361-1375.
32. Shukla, S., Ambudkar, S. V. & Prasad, R. (2004). Substitution of threonine-1351 in the multidrug transporter Cdr1p of Candida albicans results in hypersusceptibility to antifungal agents and threonine-1351 is essential for synergic effects of calcineurin inhibitor FK520. J Antimicrob Chemother 54, 38-45.
33. Smit, J. J., Schinkel, A. H., Oude Elferink, R. P. J. & 11 other authors (1993). Homozygous disruption of the murine mdr2 P-glycoprotein gene leads to complete absence of phospholipid from bile and to liver disease. Cell 75, 451-462.
34. Smriti, Krishnamurthy, S., Dixit, B. L., Gupta, C. M., Milewski, S. & Prasad, R. (2002). ABC transporters Cdr1p, Cdr2p and Cdr3p of a human pathogen Candida albicans are general phospholipid translocators. Yeast 19, 303-318.
35. Tusnady, G. E. & Simon, I. (1998). Principles governing amino acid composition of integral membrane proteins: applications to topology prediction. J Mol Biol 283, 489-506.
36. Tusnady, G. E. & Simon, I. (2001). The HMMTOP transmembrane topology prediction server. Bioinformatics 17, 849-850.
37. Walmsley, M. B., Mckeegan, K. S. & Walmsley, A. R. (2003). Structure and function in efflux pumps that confer resistance to drugs. Biochem J 376, 313-338.
38. White, T. C., Marr, K. A. & Bowden, R. A. (1998). Clinical, cellular, and molecular factors that contribute to antifungal drug resistance. Clin Microbiol Rev 11, 382-402.
39. Zhou, Y., Gottesman, M. M. & Pastan, I. (1999). Domain exchangeability between the multidrug transporter (MDRI) and phosphatidylcholine flippase (MDR2). Mol Pharmacol 56, 997-1004.