- About this Journal ·
- Abstracting and Indexing ·
- Aims and Scope ·
- Article Processing Charges ·
- Author Guidelines ·
- Bibliographic Information ·
- Citations to this Journal ·
- Contact Information ·
- Editorial Board ·
- Editorial Workflow ·
- Free eTOC Alerts ·
- Publication Ethics ·
- Recently Accepted Articles ·
- Reviewers Acknowledgment ·
- Submit a Manuscript ·
- Subscription Information ·
- Table of Contents
Journal of Amino Acids
Volume 2011 (2011), Article ID 531412, 12 pages
Functionally Relevant Residues of Cdr1p: A Multidrug ABC Transporter of Human Pathogenic Candida albicans
Membrane Biology Laboratory, School of Life Sciences, Jawaharlal Nehru University, New Delhi 110067, India
Received 24 December 2010; Accepted 21 February 2011
Academic Editor: Faizan Ahmad
Copyright © 2011 Rajendra Prasad et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
- H. Vanden Bossche, F. Dromer, I. Improvisi, M. Lozano-Chiu, J. H. Rex, and D. Sanglard, “Antifungal drug resistance in pathogenic fungi,” Medical Mycology, vol. 36, no. 1, pp. 119–128, 1998.
- M. A. Ghannoum and L. B. Rice, “Antifungal agents: mode of action, mechanisms of resistance, and correlation of these mechanisms with bacterial resistance,” Clinical Microbiology Reviews, vol. 12, no. 4, pp. 501–517, 1999.
- T. C. White, K. A. Marr, and R. A. Bowden, “Clinical, cellular, and molecular factors that contribute to antifungal drug resistance,” Clinical Microbiology Reviews, vol. 11, no. 2, pp. 382–402, 1998.
- H. V. Bossche, P. Marichal, and F. C. Odds, “Molecular mechanisms of drug resistance in fungi,” Trends in Microbiology, vol. 2, no. 10, pp. 393–400, 1994.
- F. C. Odds, Candida and Candidosis: A Review and Bibliography, Ballière Tindall, London, UK, 1988.
- R. Prasad and K. Kapoor, “Multidrug resistance in yeast Candida,” International Review of Cytology, vol. 242, pp. 215–248, 2004.
- R. Prasad, P. Snehlata, and S. Krishnamurthy, “Drug resistance mechanisms of human pathogenic fungi,” in Fungal Pathogenesis: Principles and Clinical Applications, R. A. Calderone and R. L. Cihlar, Eds., vol. 14, pp. 601–631, Marcel Dekker, New York, NY, USA, 2002.
- S. L. Kelly, D. C. Lamb, L. Juergen, H. Einsele, and D. E. Kelly, “The G464S amino acid substitution in Candida albicans sterol 14α-demethylase causes fluconazole resistance in the clinic through reduced affinity,” Biochemical and Biophysical Research Communications, vol. 262, no. 1, pp. 174–179, 1999.
- D. C. Lamb, D. E. Kelly, T. C. White, and S. L. Kelly, “The R467K amino acid substitution in Candida albicans sterol 14α- demethylase causes drug resistance through reduced affinity,” Antimicrobial Agents and Chemotherapy, vol. 44, no. 1, pp. 63–67, 2000.
- J. Morschhäuser, “The genetic basis of fluconazole resistance development in Candida albicans,” Biochimica et Biophysica Acta, vol. 1587, no. 2-3, pp. 240–248, 2002.
- C. F. Higgins, “ABC transporters: physiology, structure and mechanism—an overview,” Research in Microbiology, vol. 152, no. 3-4, pp. 205–210, 2001.
- C. F. Higgins and K. J. Linton, “The ATP switch model for ABC transporters,” Nature Structural and Molecular Biology, vol. 11, no. 10, pp. 918–926, 2004.
- R. Prasad, P. D. Worgifosse, A. Goffeau, and E. Balzi, “Molecular cloning and characterisation of a novel gene of Candida albicans, CDR1, conferring multiple resistance to drugs and antifungals,” Current Genetics, vol. 27, pp. 320–329, 1995.
- D. Sanglard, F. Ischer, M. Monod, and J. Bille, “Cloning of Candida albicans genes conferring resistance to azole antifungal agents: characterization of CDR2, a new multidrug ABC transporter gene,” Microbiology, vol. 143, no. 2, pp. 405–416, 1997.
- R. Franz, S. Michel, and J. Morschhäuser, “A fourth gene from the Candida albicans CDR family of ABC transporters,” Gene, vol. 220, no. 1-2, pp. 91–98, 1998.
- S. Krishnamurthy, U. Chatterjee, V. Gupta 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, vol. 14, no. 6, pp. 535–550, 1998.
- N. Puri, M. Gaur, M. Sharma, S. Shukla, S. V. Ambudkar, and R. Prasad, “The amino acid residues of transmembrane helix 5 of multidrug resistance protein CaCdr1p of Candida albicans are involved in substrate specificity and drug transport,” Biochimica et Biophysica Acta, vol. 1788, no. 9, pp. 1752–1761, 2009.
- P. Saini, T. Prasad, N. A. Gaur et al., “Alanine scanning of transmembrane helix 11 of Cdr1p ABC antifungal efflux pump of Candida albicans: identification of amino acid residues critical for drug efflux,” Journal of Antimicrobial Chemotherapy, vol. 56, no. 1, pp. 77–86, 2005.
- K. Nakamura, M. Niimi, K. Niimi et al., “Functional expression of Candida albicans drug efflux pump Cdr1p in a Saccharomyces cerevisiae strain deficient in membrane transporters,” Antimicrobial Agents and Chemotherapy, vol. 45, no. 12, pp. 3366–3374, 2001.
- A. Decottignies, A. M. Grant, J. W. Nichols, H. De Wet, D. B. McIntosh, and A. Goffeau, “ATPase and multidrug transport activities of the overexpressed yeast ABC protein Yor1p,” Journal of Biological Chemistry, vol. 273, no. 20, pp. 12612–12622, 1998.
- S. Shukla, P. Saini, S. Smriti, S. Jha, S. V. Ambudkar, and R. Prasad, “Functional characterization of Candida albicans ABC transporter Cdr1p,” Eukaryotic Cell, vol. 2, no. 6, pp. 1361–1375, 2003.
- R. Pasrija, D. Banerjee, and R. Prasad, “Structure and function analysis of CaMdr1p, a major facilitator superfamily antifungal efflux transporter protein of Candida albicans: identification of amino acid residues critical for drug/H+ transport,” Eukaryotic Cell, vol. 6, no. 3, pp. 443–453, 2007.
- J. E. Walker, M. Saraste, M. J. Runswick, and N. J. Gay, “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 Journal, vol. 1, no. 8, pp. 945–951, 1982.
- E. Schneider and S. Hunke, “ATP-binding-cassette (ABC) transport systems: functional and structural aspects of the ATP-hydrolyzing subunits/domains,” FEMS Microbiology Reviews, vol. 22, no. 1, pp. 1–20, 1998.
- A. Kumar, S. Shukla, A. Mandal, S. Shukla, S. V. Ambudkar, and R. Prasad, “Divergent signature motifs of nucleotide binding domains of ABC multidrug transporter, CaCdr1p of pathogenic Candida albicans, are functionally asymmetric and noninterchangeable,” Biochimica et Biophysica Acta, vol. 1798, no. 9, pp. 1757–1766, 2010.
- S. Jha, N. Karnani, S. K. Dhar et al., “Purification and characterization of the 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, vol. 42, no. 36, pp. 10822–10832, 2003.
- P. Saini, N. A. Gaur, and R. Prasad, “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, vol. 152, no. 5, pp. 1559–1573, 2006.
- C. A. Hrycyna, M. Ramachandra, U. A. Germann, P. W. Cheng, I. Pastan, and M. M. Gottesman, “Both ATP sites of human P-glycoprotein are essential but not symmetric,” Biochemistry, vol. 38, no. 42, pp. 13887–13899, 1999.
- I. L. Urbatsch, B. Sankaran, S. Bhagat, and A. E. Senior, “Both P-glycoprotein nucleotide-binding sites are catalytically active,” Journal of Biological Chemistry, vol. 270, no. 45, pp. 26956–26961, 1995.
- G. Szakács, C. Özvegy, E. Bakos, B. Sarkadi, and A. Váradi, “Role of glycine-534 and glycine-1179 of human multidrug resistance protein (MDR1) in drug-mediated control of ATP hydrolysis,” Biochemical Journal, vol. 356, no. 1, pp. 71–75, 2001.
- I. L. Urbatsch, K. Gimi, S. Wilke-Mounts, and A. E. Senior, “Investigation of the role of glutamine-471 and glutamine-1114 in the two catalytic sites of P-glycoprotein,” Biochemistry, vol. 39, no. 39, pp. 11921–11927, 2000.
- Z. E. Sauna, M. Müller, X. H. Peng, and S. V. Ambudkar, “Importance of the conserved walker B glutamate residues, 556 and 1201, for the completion of the catalytic cycle of ATP hydrolysis by human P-glycoprotein (ABCB1),” Biochemistry, vol. 41, no. 47, pp. 13989–14000, 2002.
- M. Azzaria, E. Schurr, and P. Gros, “Discrete mutations introduced in the predicted nucleotide-binding sites of the mdr1 gene abolish its ability to confer multidrug resistance,” Molecular and Cellular Biology, vol. 9, no. 12, pp. 5289–5297, 1989.
- V. Rai, S. Shukla, S. Jha, S. S. Komath, and R. Prasad, “Functional characterization of N-terminal nucleotide binding domain (NBD-1) of a major ABC drug transporter Cdr1p of Candida albicans: uncommon but conserved Trp326 of walker B is important for ATP binding,” Biochemistry, vol. 44, no. 17, pp. 6650–6661, 2005.
- E. Procko, I. Ferrin-O'Connell, S. L. Ng, and R. Gaudet, “Distinct structural and functional properties of the ATPase sites in an asymmetric ABC transporter,” Molecular Cell, vol. 24, no. 1, pp. 51–62, 2006.
- P. Melin, V. Thoreau, C. Norez, F. Bilan, A. Kitzis, and F. Becq, “The cystic fibrosis mutation G1349D within the signature motif LSHGH of NBD2 abolishes the activation of CFTR chloride channels by genistein,” Biochemical Pharmacology, vol. 67, no. 12, pp. 2187–2196, 2004.
- M. Chen, R. Abele, and R. Tampé, “Functional non-equivalence of ATP-binding cassette signature motifs in the transporter associated with antigen processing (TAP),” Journal of Biological Chemistry, vol. 279, no. 44, pp. 46073–46081, 2004.
- B. L. Browne, V. McClendon, and D. M. Bedwell, “Mutations within the first LSGGQ motif of Ste6p cause defects in a-factor transport and mating in Saccharomyces cerevisiae,” Journal of Bacteriology, vol. 178, no. 6, pp. 1712–1719, 1996.
- Z. Szentpétery, A. Kern, K. Liliom, B. Sarkadi, A. Váradi, and E. Bakos, “The role of the conserved glycines of ATP-binding cassette signature motifs of MRP1 in the communication between the substrate-binding site and the catalytic centers,” Journal of Biological Chemistry, vol. 279, no. 40, pp. 41670–41678, 2004.
- O. Ramaen, C. Sizun, O. Pamlard, E. Jacquet, and J. Y. Lallemand, “Attempts to characterize the NBD heterodimer of MRP1: transient complex formation involves Gly771 of the ABC signature sequence but does not enhance the intrinsic ATPase activity,” Biochemical Journal, vol. 391, no. 3, pp. 481–490, 2005.
- G. Schmees, A. Stein, S. Hunke, H. Landmesser, and E. Schneider, “Functional consequences of mutations in the conserved ‘signature sequence’ of the ATP-binding-cassette protein MalK,” European Journal of Biochemistry, vol. 266, no. 2, pp. 420–430, 1999.
- K. P. Hopfner, A. Karcher, D. S. Shin et al., “Structural biology of Rad50 ATPase: ATP-driven conformational control in DNA double-strand break repair and the ABC-ATPase superfamily,” Cell, vol. 101, no. 7, pp. 789–800, 2000.
- P. C. Smith, N. Karpowich, L. Millen et al., “ATP binding to the motor domain from an ABC transporter drives formation of a nucleotide sandwich dimer,” Molecular Cell, vol. 10, no. 1, pp. 139–149, 2002.
- G. Verdon, S. V. Albers, N. Van Oosterwijk, B. W. Dijkstra, A. J. M. Driessen, and A. M. W. H. Thunnissen, “Formation of the productive ATP-Mg2+-bound dimer of GlcV, an ABC-ATPase from Sulfolobus solfataricus,” Journal of Molecular Biology, vol. 334, no. 2, pp. 255–267, 2003.
- R. J. P. Dawson and K. P. Locher, “Structure of a bacterial multidrug ABC transporter,” Nature, vol. 443, no. 7108, pp. 180–185, 2006.
- J. Zaitseva, C. Oswald, T. Jumpertz et al., “A structural analysis of asymmetry required for catalytic activity of an ABC-ATPase domain dimer,” EMBO Journal, vol. 25, no. 14, pp. 3432–3443, 2006.
- M. L. Oldham, D. Khare, F. A. Quiocho, A. L. Davidson, and J. Chen, “Crystal structure of a catalytic intermediate of the maltose transporter,” Nature, vol. 450, no. 7169, pp. 515–521, 2007.
- H. A. Lewis, S. G. Buchanan, S. K. Burley et al., “Structure of nucleotide-binding domain 1 of the cystic fibrosis transmembrane conductance regulator,” EMBO Journal, vol. 23, no. 2, pp. 282–293, 2004.
- R. Ernst, P. Kueppers, C. M. Klein, T. Schwarzmueller, K. Kuchler, and L. Schmitt, “A mutation of the H-loop selectively affects rhodamine transport by the yeast multidrug ABC transporter Pdr5,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 13, pp. 5069–5074, 2008.
- R. Ernst, P. Kueppers, J. Stindt, K. Kuchler, and L. Schmitt, “Multidrug efflux pumps: substrate selection in ATP-binding cassette multidrug efflux pumps-first come, first served?” FEBS Journal, vol. 277, no. 3, pp. 540–549, 2010.
- S. Shukla, V. Rai, D. Banerjee, and R. Prasad, “Characterization of Cdr1p, a major multidrug efflux protein of Candida albicans: purified protein is amenable to intrinsic fluorescence analysis,” Biochemistry, vol. 45, no. 7, pp. 2425–2435, 2006.
- C. Gauthier, S. Weber, A. M. Alarco et al., “Functional similarities and differences between Candida albicans Cdr1p and Cdr2p transporters,” Antimicrobial Agents and Chemotherapy, vol. 47, no. 5, pp. 1543–1554, 2003.
- N. Puri, O. Prakash, R. Manoharlal, M. Sharma, I. Ghosh, and R. Prasad, “Analysis of physico-chemical properties of substrates of ABC and MFS multidrug transporters of pathogenic Candida albicans,” European Journal of Medicinal Chemistry, vol. 45, no. 11, pp. 4813–4826, 2010.
- M. Sharma, R. Manoharlal, S. Shukla et al., “Curcumin modulates efflux mediated by yeast ABC multidrug transporters and is synergistic with antifungals,” Antimicrobial Agents and Chemotherapy, vol. 53, no. 8, pp. 3256–3265, 2009.
- A. R. Holmes, Y. H. Lin, K. Niimi et al., “ABC transporter Cdr1p contributes more than Cdr2p does to fluconazole efflux in fluconazole-resistant Candida albicans clinical isolates,” Antimicrobial Agents and Chemotherapy, vol. 52, no. 11, pp. 3851–3862, 2008.
- K. Tanabe, E. Lamping, K. Adachi et al., “Inhibition of fungal ABC transporters by unnarmicin A and unnarmicin C, novel cyclic peptides from marine bacterium,” Biochemical and Biophysical Research Communications, vol. 364, no. 4, pp. 990–995, 2007.
- S. Shukla, Z. E. Sauna, R. Prasad, and S. V. Ambudkar, “Disulfiram is a potent modulator of multidrug transporter Cdr1p of Candida albicans,” Biochemical and Biophysical Research Communications, vol. 322, no. 2, pp. 520–525, 2004.