Cysteine-scanning mutagenesis provides no evidence for the extracellular accessibility of the nucleotide-binding domains of the multidrug resistance transporter P-glycoprotein

EMBO Journal

Volumn 18, Issue 23, 1999, Pages 6800-6808

  Blott, Emma J ^a   Higgins, Christopher F ^a   Linton, Kenneth J ^a  

^a NONE

Author keywords

ABC transporter; Cysteine scanning mutagenesis; Multidrug resistance; Nucleotide binding domain; P glycoprotein

Indexed keywords

ABC TRANSPORTER; CYSTEINE; GLYCOPROTEIN P; MULTIDRUG RESISTANCE PROTEIN; NUCLEOTIDE BINDING PROTEIN; TRANSMEMBRANE CONDUCTANCE REGULATOR;

ARTICLE; MUTAGENESIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; SALMONELLA TYPHIMURIUM;

NEGIBACTERIA; SALMONELLA TYPHIMURIUM; TYPHIMURIUM;

EID: 0033485546     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/18.23.6800     Document Type: Article

References (33)

1. Al-Shawi, M.K. and Senoir, A.E. (1993) Characterization of the adenosine triphosphatase activity of Chinese hamster P-glycoprotein. J. Biol. Chem., 268, 4179-4206.
2. Ames, G.F.-L. (1986) Bacterial periplasmic transport systems: structure, mechanism and evolution. Annu. Rev. Biochem., 55, 397-425.
3. Ames, G.F.-L., and Spudich, E.N. (1976) Protein-protein interaction: periplasmic histidine-binding protein J interacts with P protein. Proc. Natl Acad. Sci. USA, 73, 1877-1881.
4. Baichwal, V., Liu, D. and Ames, G.F.-L. (1993) The ATP-binding component of a prokaryotic traffic ATPase is exposed to the periplasmic (external) surface. Proc. Natl Acad. Sci. USA, 90, 620-624.
5. Bell, A.W., Buckel, S.D., Groarke, J.M., Hope, J.N., Kingsley, D.H. and Hermodson, M.A. (1986) The nucleotide sequences of the rbsD, rbsA and rbsC genes of Escherichia coli K12.J. Biol. Chem., 261, 7652-7658.
6. Bliss, J.M. and Silver, R.P. (1997) Evidence that KpsT, the ATP-binding component of an ATP-binding cassette transporter, is exposed to the periplasm and associates with polymer during translocation of the polysialic acid capsule of Escherichia coli K1. J. Bacteriol., 179, 1400-1403.
7. Bosch, I. and Croop, J. (1996) P-glycoprotein multidrug resistance and cancer. Biochim. Biophys. Acta, 1288, 37-54.
8. Clancy, J.P., Hong, J.S., Bebok, Z., King, S.A., Demolombe, S., Bedwell, D.M. and Sorcher, E.J. (1998) Cystic fibrosis transmembrane conductance regulator (CFTR) nucleotide-binding domain 1 (NBD1) and CFTR truncated within NBD1 target to the epithelial plasma membrane and increase anion permeability. Biochemistry, 37, 15222-15230.
9. Davidson, A.L., Shuman, H.A. and Nikaido, H. (1992) Mechanism of maltose transport in Escherichia coli: transmembrane signaling by periplasmic binding proteins. Proc. Natl Acad. Sci. USA, 89, 2360-2364.
10. Eichler, J. and Wickner, W. (1998) The SecA subunit of Escherichia coli preprotein translocase is exposed to the periplasm. J. Bacteriol., 180, 5776-5779.
11. Gallagher, M.P., Pearce, S.R. and Higgins, C.F. (1989) Identification and localization of the membrane-associated, ATP-binding subunit of the oligopeptide permease of Salmonella typhimurium. Eur. J. Biochem., 180, 133-141.
12. Gottesman, M.M. and Pastan, I. (1993) Biochemistry of multidrug resistance mediated by the multidrug transporter. Annu. Rev. Biochem., 62, 385-427.
13. Gruis, D.B. and Price, E.M. (1997) The nucleotide-binding folds of the cystic fibrosis transmembrane conductance regulator are extracellularly accessible. Biochemistry, 36, 7739-7745.
14. Higgins, C.F. (1992) ABC transporters: from microorganisms to man. Annu. Rev. Cell Biol., 8, 67-113.
15. Higgins, C.F., Haag, P.D., Nikaido, K., Ardeshir, F., Garcia, G. and Ames, G.F. (1982) Complete nucleotide sequence and identification of membrane components of the histidine transport operon of S. typhimurium. Nature, 298, 723-727.
16. Higgins, C.F. et al. (1986) A family of related ATP-binding subunits coupled to many distinct biological processes in bacteria. Nature, 323, 448-450.
17. Hung, L.-W., Wang, I.X., Nikaido, K., Liu, P.-Q., Ames, G.F.-L. and Kim, S.-H. (1998) Crystal structure of the ATP-binding subunit of an ABC transporter. Nature, 396, 703-707.
18. Hyde, S.C. et al. (1990) Structural model of ATP-binding proteins associated with cystic fibrosis, multidrug resistance and bacterial transport. Nature, 346, 362-365.
19. Kerppola, R.E., Shyamala, V.K., Klebba, P. and Ames, G.F.-L. (1991) The membrane-bound proteins of periplasmic permeases form a complex. J. Biol. Chem., 266, 9857-9865.
20. Kim, Y.J., Rajapandi, T. and Oliver, D. (1994) SecA protein is exposed to the periplasmic surface of the Escherichia coli inner membrane in its active state. Cell, 78, 845-853.
21. Ko, Y.H., Delannoy, M. and Pedersen, P.L. (1997) Cystic fibrosis transmembrane conductance regulator: the first nucleotide binding fold targets the membrane with retention of its ATP binding function. Biochemistry, 36, 5053-5064.
22. Loo, T.W. and Clarke, D.M. (1995) Membrane topology of a cysteine-less mutant of human P-glycoprotein. J. Biol. Chem., 270, 843-848.
23. Nikaido, H. and Hall, J.A. (1998) Overview of bacterial ABC transporters. Methods Enzymol., 292, 3-20.
24. Petronilli, V. and Ames, G.F. (1991) Binding protein-independent histidine permease mutants. Uncoupling of ATP hydrolysis from transmembrane signaling. J. Biol, Chem., 266, 16293-16296.
25. Ramamurthy, V. and Oliver, D. (1997) Topology of the integral membrane form of the Escherichia coli SecA protein reveals multiple periplasmically exposed regions and modulation by ATP binding. J. Biol. Chem., 272, 23239-23246.
26. Rosenberg, M.F., Callaghan, R., Ford, R.C. and Higgins, C.F. (1997) Structure of the multidrug resistance P-glycoprotein to 2.5 nm resolution. J. Biol. Chem., 272, 10685-10694.
27. Saier, M.H., Jr (1996) Phylogenetic approaches to the identification and characterization of protein families and superfamilies. Microb. Comp. Genomics. 1, 129-150.
28. Sarkadi, B., Price, E.M., Boucher, R.C, Germann, U.A. and Scarborough, G.A. (1992) Expression of the human multidrug resistance cDNA in insect cells generates a high activity drug-stimulated membrane ATPase. J. Biol. Chem., 262, 4854-4858.
29. Schneider, E., Hunke, S. and Tebbe, S. (1995) The MalK protein of the ATP-binding cassette transporter for maltose of Escherichia coli is accessible from the periplasmic side of the membrane. J. Bacteriol., 177, 5364-5367.
30. Shen, D.W., Fojo, A., Chin, J.E., Roninson, I.B., Richert, N., Pastan, I. and Gottesman, M. M. (1986) Human multidrug-resistant cell lines: increased mdr 1 expression can precede gene amplification. Science, 232, 643-645.
31. Thiebaut, F., Currier, S.J., Whitaker, J., Haugland, R.P., Gottesman, M.M., Pastan, I. and Willingham, M.C. (1990) Activity of the mutidrug transporter results in alkalization of the cytosol: measurement of cytosolic pH by microinjection of a pH sensitive dye. J. Histochem. Cytochem., 38, 685-690.
32. van der Does, C., den Blaauwen, T., de Wit, J.G., Manting, E.H., Groot, N.A., Fekkes, P. and Driessen, A.J.M. (1996) SecA is an intrinsic subunit of the Escherichia coli preprotein translocase and exposes its carboxyl terminus to the periplasm. Mol. Microbiol., 22, 619-629.
33. Wickner, W. (1976) Fractionation of membrane vesicles from coliphage M13-infected Escherichia coli. J. Bacteriaol., 127, 162-167.