Providing a molecular mechanism for P-glycoprotein; Why would i bother?

Biochemical Society Transactions

Volumn 43, Issue , 2015, Pages 995-1002

  Callaghan, Richard ^a  

^a AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

Author keywords

ATP binding cassette (ABC) protein; Cancer chemotherapy; Membrane transport; Molecular mechanism; Multi drug resistance; Permeability (P) glycoprotein

Indexed keywords

ADENOSINE TRIPHOSPHATE; ANTINEOPLASTIC AGENT; CYCLOSPORIN A; DOXORUBICIN; FLUPENTIXOL; MEMBRANE PROTEIN; MULTIDRUG RESISTANCE ASSOCIATED PROTEIN 1; MULTIDRUG RESISTANCE PROTEIN; RHODAMINE 123; VINBLASTINE; DRUG; PROTEIN BINDING;

ALLOSTERISM; ARTICLE; CANCER CELL LINE; CANCER CHEMOTHERAPY; CANCER RESISTANCE; CELL TRANSPORT; CRYSTAL STRUCTURE; DIMERIZATION; DRUG BINDING SITE; DRUG PROTEIN BINDING; HUMAN; MOLECULAR DYNAMICS; PHARMACOPHORE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE; PROTEIN TRANSPORT; CHEMISTRY; DRUG RESISTANCE; METABOLISM; MULTIDRUG RESISTANCE; NEOPLASM; PATHOLOGY; TRANSPORT AT THE CELLULAR LEVEL; X RAY CRYSTALLOGRAPHY;

ADENOSINE TRIPHOSPHATE; BIOLOGICAL TRANSPORT; CRYSTALLOGRAPHY, X-RAY; DRUG RESISTANCE, MULTIPLE; DRUG RESISTANCE, NEOPLASM; HUMANS; NEOPLASMS; P-GLYCOPROTEIN; PHARMACEUTICAL PREPARATIONS; PROTEIN BINDING;

EID: 84947273468     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST20150131     Document Type: Article

References (54)

1. Kartner, N. and Ling, V. (1989) Multidrug resistance in cancer. Sci. Am. 260, 44-51 CrossRef PubMed
2. Dano, K. (1973) Active outward transport of daunomycin in resistant Ehrlich ascites tumor cells. Biochim. Biophys. Acta 323, 466-483 CrossRef PubMed
3. Juliano, R.L. and Ling, V. (1976) A surface glycoprotein modulating drug permeability in Chinese hamster ovary cell mutants. Biochim. Biophys. Acta 455, 152-162 CrossRef PubMed
4. Kartner, N., Riordan, J.R. and Ling, V. (1983) Cell surface P-glycoprotein associated with multidrug resistance in mammalian cell lines. Science 221, 1285-1288 CrossRef PubMed
5. Chambers, T.C., McAvoy, E.M., Jacobs, J.W. and Eilon, G. (1990) Protein kinase C phosphorylates P-glycoprotein in multidrug resistant human KB carcinoma cells. J. Biol. Chem. 265, 7679-7686 PubMed
6. Ichikawa, M., Yoshimura, A., Furukawa, T., Sumizawa, T., Nakazima, Y. and Akiyama, S. (1991) Glycosylation of P-glycoprotein in a multidrug-resistant KB cell line, and in the human tissues. Biochim. Biophys. Acta 1073, 309-315 CrossRef PubMed
7. Richert, N.D., Aldwin, L., Nitecki, D., Gottesman, M.M. and Pastan, I. (1988) Stability and covalent modification of P-glycoprotein in multidrugresistant KB cells. Biochemistry 27, 7607-7613 CrossRef PubMed
8. Riordan, J.R. and Ling, V. (1979) Purification of P-glycoprotein from plasma membrane vesicles of chinese hamster ovary cell mutants with reduced colchicine permeability. J. Biol. Chem. 254, 12701-12705 PubMed
9. Hamada, H. and Tsuruo, T. (1988) Purification of the 170- to 180-kilodalton membrane glycoprotein associated with multidrug resistance. 170- to 180-kilodalton membrane glycoprotein is an ATPase. J. Biol. Chem. 263, 1454-1458 PubMed
10. Taylor, A.M., Storm, J., Soceneantu, L., Linton, K.J., Gabriel, M., Martin, C., Woodhouse, J., Blott, E., Higgins, C.F. and Callaghan, R. (2001) Detailed characterization of cysteine-less P-glycoprotein reveals subtle pharmacological differences in function from wild-type protein. Br. J. Pharmacol. 134, 1609-1618 CrossRef PubMed
11. Ambudkar, S.V., Lelong, I.H., Zhang, J., Cardarelli, C.O., Gottesman, M.M. and Pastan, I. (1992) Partial purification and reconstitution of the human multidrug- resistance pump: characterization of the drug-stimulatable ATP hydrolysis. Proc. Natl. Acad. Sci. U.S.A. 89, 8472-8476 CrossRef PubMed
12. Doige, C.A., Yu, X. and Sharom, F.J. (1992) ATPase activity of partially purified P-glycoprotein from multidrug-resistant Chinese hamster ovary cells. Biochim. Biophys. Acta 1109, 149-160 CrossRef PubMed
13. Rigaud, J.L., Paternostre, M.T. and Bluzat, A. (1988) Mechanisms of membrane protein insertion into liposomes during reconstitution procedures involving the use of detergents. 2. Incorporation of the light-driven proton pump bacteriorhodopsin. Biochemistry 27, 2677-2688 CrossRef PubMed
14. Callaghan, R., Berridge, G., Ferry, D.R. and Higgins, C.F. (1997) The functional purification of P-glycoprotein is dependent on maintenance of a lipid-protein interface. Biochim. Biophys. Acta 1328, 109-124 CrossRef PubMed
15. Loo, T.W. and Clarke, D.M. (1995) Rapid purification of human P-glycoprotein mutants expressed transiently in HEK 293 cells by nickel-chelate chromatography and characterization of their drug stimulated ATPase activities. J. Biol. Chem. 270, 21449-21452 CrossRef PubMed
16. al-Shawi, M.K. and Senior, A.E. (1993) Characterization of the adenosine triphosphatase activity of Chinese hamster P-glycoprotein. J. Biol. Chem. 268, 4197-4206 PubMed
17. al-Shawi, M.K., Urbatsch, I.L. and Senior, A.E. (1994) Covalent inhibitors of P-glycoprotein ATPase activity. J. Biol. Chem. 269, 8986-8992 PubMed
18. Tombline, G., Bartholomew, L.A., Urbatsch, I.L. and Senior, A.E. (2004). Combined mutation of catalytic glutamate residues in the two nucleotide binding domains of P-glycoprotein generates a conformation that binds ATP and ADP tightly. J. Biol. Chem. 279, 31212-31220 CrossRef PubMed
19. Jones, P.M., O'Mara, M.L. and George, A.M. (2009) ABC transporters: a riddle wrapped in a mystery inside an enigma. Trends Biochem. Sci. 34, 520-531 CrossRef PubMed
20. Diedrichs, K., Diez, J., Greller, G., Muller, C., Breed, J., Schnell, C., Vonrhein, C., Boos, W. and Welte, W. (2000) Crystal structure of MalK, the ATPase subunit of the trehalose/maltose ABC transporter of the archeon Thermococcus litoralis. EMBO J. 19, 5951-5961 CrossRef PubMed
21. Hopfner, K.P., Karcher, A., Shin, D.S., Craig, L., Arthur, L.M., Carney, J.P. and Tainer, J.A. (2000) Structural biology of Rad50 ATPase: ATP-driven conformational control in DNA double-strand break repair and the ABC-ATPase superfamily. Cell 101, 789-800 CrossRef PubMed
22. Hung, L.W., Wang, I.X., Nikaido, K., Liu, P.Q., Ames, G.F. and Kim, S.H. (1998) Crystal structure of the ATP-binding subunit of an ABC transporter. Nature 396, 703-707 CrossRef PubMed
23. Dawson, R.J. and Locher, K.P. (2006) Structure of a bacterial multidrug ABC transporter. Nature 443, 180-185 CrossRef PubMed
24. Cole, S.P.C., Bhardwaj, G., Gerlach, J.H., Mackie, J.E., Grant, C.E., Almquist, K.C., Stewart, A.J., Kurz, E.U., Duncan, A.M.V. and Deeley, R.G. (1992). Overexpression of a transporter gene in a multidrug resistant human lung cancer cell line. Science 258, 1650-1654 CrossRef PubMed
25. Doyle, L.A., Yang, W., Abruzzo, L.V., Krogmann, T., Gao, Y., Rishi, A.K. and Ross, D.D. (1998) A multidrug resistance transporter from human MCF-7 breast cancer cells. Proc. Natl. Acad. Sci. U.S.A. 95, 15665-15670 CrossRef PubMed
26. Higgins, C.F. and Gottesman, M.M. (1992) Is the multidrug transporter a flippase? Trends Biochem. Sci. 17, 18-21 CrossRef PubMed
27. Raviv, Y., Pollard, H.B., Bruggemann, E.P., Pastan, I. and Gottesman, M.M. (1990) Photosensitized labeling of a functional multidrug transporter in living drug-resistant tumor cells. J. Biol. Chem. 265, 3975-3980 PubMed
28. Homolya, L., Hollo, Z., Germann, U.A., Pastan, I., Gottesman, M.M. and Sarkadi, B. (1993) Fluorescent cellular indicators are extruded by the multidrug resistance protein. J. Biol. Chem. 268, 21493-21496 PubMed
29. Tamai, I. and Safa, A.R. (1991) Azidopine noncompetitively interacts with vinblastine and cyclosporin A binding to P-glycoprotein in multidrug resistant cells. J. Biol. Chem. 266, 16796-16800 PubMed
30. Dey, S., Ramachandra, M., Pastan, I., Gottesman, M.M. and Ambudkar, S.V. (1997) Evidence for two nonidentical drug-interaction sites in the human P- glycoprotein. Proc. Natl. Acad. Sci. U.S.A. 94, 10594-10599 CrossRef PubMed
31. Greenberger, L.M. (1993) Major photoaffinity drug labeling sites for iodoaryl azidoprazosin in P-glycoprotein are within, or immediately C-terminal to, transmembrane domains 6 and 12. J. Biol. Chem. 268, 11417-11425 PubMed
32. Safa, A.R. (1992) Photoaffinity labelling of P-glycoprotein in multidrug resistant cells. Cancer Invest. 10, 295-305 CrossRef
33. Pleban, K., Kopp, S., Csaszar, E., Peer, M., Hrebicek, T., Rizzi, A., Ecker, G.F. and Chiba, P. (2005) P-glycoprotein substrate binding domains are located at the transmembrane domain/transmembrane domain interfaces: a combined photoaffinity labeling-protein homology modeling approach. Mol. Pharmacol. 67, 365-374 CrossRef PubMed
34. Ferry, D.R., Russell, M.A. and Cullen, M.H. (1992) P-glycoprotein possesses a 1,4-dihydropyridine selective drug acceptor site which is allosterically coupled to a vinca alkaloid selective binding site. Biochem. Biophys. Res. Commun. 188, 440-445 CrossRef PubMed
35. Martin, C., Berridge, G., Higgins, C.F., Mistry, P., Charlton, P. and Callaghan, R. (2000) Communication between multiple drug binding sites on P-glycoprotein. Mol. Pharmacol. 58, 624-632 PubMed
36. Martin, C., Berridge, G., Mistry, P., Higgins, C., Charlton, P. and Callaghan, R. (1999) The molecular interaction of the high affinity reversal agent XR9576 with P-glycoprotein. Br. J. Pharmacol. 128, 403-411 CrossRef PubMed
37. Shapiro, A.B. and Ling, V. (1997) Positively cooperative sites for drug transport by P-glycoprotein with distinct drug specificities. Eur. J. Biochem. 250, 130-137 CrossRef PubMed
38. Garrigos, M., Mir, L.M. and Orlowski, S. (1997) Competitive and non-competitive inhibition of the multidrug-resistance-associated P-glycoprotein ATPase. Further experimental evidence for a multisite model. Eur. J. Biochem. 244, 664-673 CrossRef PubMed
39. Pascaud, C., Garrigos, M. and Orlowski, S. (1998) Multidrug resistance transporter P-glycoprotein has distinct but interacting binding sites for cytotoxic drugs and reversing agents. Biochem. J. 333, 351-358 PubMed
40. Chen, C.J., Chin, J.E., Ueda, K., Clark, D.P., Pastan, I., Gottesman, M.M. and Roninson, I.B. (1986) Internal duplication and homology with bacterial transport proteins in the mdr1 (P-glycoprotein) gene from multidrug-resistant human cells. Cell 47, 381-389 CrossRef PubMed
41. Gros, P., Croop, J. and Houseman, D.E. (1986) Mammalian multidrug resistance gene: complete cDNA sequence indicates strong homology to bacterial transport proteins. Cell 47, 371-380 CrossRef PubMed
42. 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 CrossRef PubMed
43. 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 determined by electron microscopy and image analysis. J. Biol. Chem. 272, 10685-10694 CrossRef PubMed
44. Rosenberg, M.F., Velarde, G., Ford, R.C., Martin, C., Berridge, G., Kerr, I.D., Callaghan, R., Schmidlin, A., Wooding, C., Linton, K.J. and Higgins, C.F. (2001) Repacking of the transmembrane domains of P-glycoprotein during the transport ATPase cycle. EMBO J. 20, 5615-5625 CrossRef PubMed
45. Sonveaux, N., Vigano, C., Shapiro, A.B., Ling, V. and Ruysschaert, J.M. (1999) Ligand-mediated tertiary structure changes of reconstituted Pglycoprotein. A tryptophan fluorescence quenching analysis. J. Biol. Chem. 274, 17649-17654 CrossRef PubMed
46. Vigano, C., Julien, M., Carrier, I., Gros, P. and Ruysschaert, J.M. (2002). Structural and functional asymmetry of the nucleotide-binding domains of P-glycoprotein investigated by attenuated total reflection Fourier transform infrared spectroscopy. J. Biol. Chem. 277, 5008-5016 CrossRef PubMed
47. Martin, C., Higgins, C.F. and Callaghan, R. (2001) The vinblastine binding site adopts high- and low-affinity conformations during a transport cycle of P-glycoprotein. Biochemistry 40, 15733-15742 CrossRef PubMed
48. Rothnie, A., Callaghan, R., Deeley, R.G. and Cole, S.P. (2006) Role of GSH in estrone sulfate binding and translocation by the multidrug resistance protein 1 (MRP1/ABCC1). J. Biol. Chem. 281, 13906-13914 CrossRef PubMed
49. Clark, R., Kerr, I.D. and Callaghan, R. (2006) Multiple drug-binding sites on the R482G isoform of the ABCG2 transporter. Br. J. Pharmacol. 149, 506-515 CrossRef PubMed
50. Rosenberg, M.F., Callaghan, R., Modok, S., Higgins, C.F. and Ford, R.C. (2005) Three-dimensional Structure of P-glycoprotein: the transmembrane regions adopt an asymmetric configuration in the nucleotide-bound state. J. Biol. Chem. 280, 2857-2862 CrossRef PubMed
51. Aller, S.G., Yu, J., Ward, A., Weng, Y., Chittaboina, S., Zhuo, R., Harrell, P.M., Trinh, Y.T., Zhang, Q., Urbatsch, I.L. and Chang, G. (2009) Structure of P-glycoprotein reveals a molecular basis for poly-specific drug binding. Science 323, 1718-1722 CrossRef PubMed
52. Jin, M.S., Oldham, M.L., Zhang, Q. and Chen, J. (2012) Crystal structure of the multidrug transporter P-glycoprotein from Caenorhabditis elegans. Nature 490, 566-569 CrossRef PubMed
53. Li, J., Jaimes, K.F. and Aller, S.G. (2014) Refined structures of mouse P-glycoprotein. Protein Sci. 23, 34-46 CrossRef PubMed
54. O'Mara, M.L. and Mark, A.E. (2014) Structural characterization of two metastable ATP-bound states of P-glycoprotein. PLoS One 9, e91916 CrossRef PubMed