Structure of the multidrug resistance P-glycoprotein

Seminars in Cancer Biology

Volumn 8, Issue 3, 1997, Pages 135-142

  Higgins, Christopher F ^a   Callaghan, Richard ^a   Linton, Kenneth J ^a   Rosenberg, Mark F ^b   Ford, Robert C ^b  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

ABC transporters; Membrane protein; P glycoprotein; Protein structure

Indexed keywords

ABC TRANSPORTER; GLYCOPROTEIN P; MEMBRANE PROTEIN; MULTIDRUG RESISTANCE PROTEIN;

BINDING SITE; CONFERENCE PAPER; DRUG PROTEIN BINDING; ELECTRON MICROSCOPY; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; PROTEIN DOMAIN; PROTEIN STRUCTURE; PROTEIN TERTIARY STRUCTURE;

EID: 0031160951     PISSN: 1044579X     EISSN: None     Source Type: Journal    
DOI: 10.1006/scbi.1997.0067     Document Type: Conference Paper

References (54)

1. 1. Valverde MA, Bond TD, Hardy SP, Taylor JC, Higgins CF, Altamirano J, Alvarez-Leefmans FJ (1996) The multidrug resistance P-glycoprotein modulates cell regulatory volume decrease. EMBO J 15:4460-4468
2. 2. Valverde MA, Diaz M, Sepulveda FV, Gill DR, Hyde SC, Higgins CF (1992) Volume-regulated chloride channels associated with the human multidrug-resistance P-glycoprotein. Nature 355:830-833
3. 3. Rosenberg MF, Callaghan R, Ford RC, Higgins CF (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
4. 4. Chen C-J, Chin JE, Ueda K, Clark DP, Pastan I, Gottesman MMIB (1986) Internal duplication and homology with bacterial transport proteins in the mdr1 (P-glycoprotein) gene from multidrug-resistant human cells. Cell 47:381-389
5. 5. Gerlach JH, Endicott JA, Juranka PF, Henderson G, Sarangi F, Deuchars KL, Ling V (1986) Homology between P-glycoprotein and a bacterial haemolysin transport protein suggests a model for multidrug resistance. Nature 324:485-489
6. 6. Gros P, Croop J, Housmann D (1986) Mammalian multidrug resistance gene: complete cDNA sequence indicates strong homology to bacterial transport proteins. Cell 47:371-380
7. 7. Chambers TC, Pohl J, Raynor RL, Kuo JF (1993) Identification of specific sites in human P-glycoprotein phosphorylated by protein-kinase-C. J Biol Chem 268:4592-4595
8. 8. Goodfellow HR, Sardini A, Ruetz S, Callaghan R, Gros P, McNaughton PA, Higgins CF (1996) Protein kinase C-mediated phosphorylation does not regulate drug transport by the human multidrug resistance P-glycoprotein. J Biol Chem 271:13668-13674
9. 9. Germann UA, Chambers TC, Ambudkar SV, Licht T, Cardarelli CO, Pastan I, Gottesman MM (1996) Characterization of phosphorylation-defective mutants of human P-glycoprotein expressed in mammalian cells. J Biol Chem 271:1708-1716
10. 10. Hardy SP, Goodfellow HR, Valverde MA, Gill DR, Sepulveda FV, Higgins CF (1995) Protein kinase C-mediated phosphorylation of the human multidrug resistance P-glycoprotein regulates cell volume-activated chloride channels. EMBO J 14:68-75
11. 11. Kast C, Canfield V, Levenson R, Gros P (1995) Membrane topology of P-glycoprotein as determined by epitope insertion - transmembrane organization of the N-terminal domain of mdr3. Biochemistry 34:4402-4411
12. 12. Loo TW, Clarke DM (1995) Membrane topology of a cysteineless mutant of human P-glycoprotein. J Biol Chem 270:843-848
13. 13. Georges E, Tsuruo T, Ling V (1993) Topology of P-glycoprotein as determined by epitope mapping of MRK-16 monoclonal antibody. J Biol Chem 268:1792-1798
14. 14. Cianfriglia M, Willingham MC, Tombes M, Scagliotti GV, Frasca G, Chersi A (1994) P-glycoprotein epitiope mapping. I. Identification of a linear human-specific epitope in the fourth loop of the P-glycoprotein extracellular domain by MM4.17 murine monoclonal antibody to human multidrug-resistant cells. Int J Cancer 56:153-160
15. 15. Cianfriglia M, Romagnoli G, Tombesi M, Poloni F, Falasca G, Di Modugno F, Castagna M, Chersi A (1995) P-glycoprotein epitope mapping. II. The murine monoclonal antibody MM6.15 to human multidrug-resistant cells binds with three distinct loops in the MDR1-P-glycoprotein extracellular domain. Int J Cancer 61:142-147
16. 16. Zhang J-T, Ling V (1991) Study of membrane orientation and glycosylated extracellular loops of mouse P-glycoprotein by in vitro translation. J Biol Chem 266:18224-18232
17. 17. Zhang J-T, Duthie M, Ling V (1993) Membrane topology of the N-terminal half of the hamster P-glycoprotein molecule. J Biol Chem 268:15101-15110
18. 18. Skach WR, Calayag MC, Lingappa VR (1993) Evidence for an alternate model of human P-glycoprotein structure and biogenesis. J Biol Chem 268:6903-6908
19. 19. Skach WR, Lingappa VR (1994) Transmembrane orientation and topogenesis of the 3rd and 4th membrane-spanning regions of human P-glycoprotein (MDR1). Cancer Res 54:3202-3209
20. 20. Bibi E, Beja O (1994) Membrane topology of multidrug-resistance protein expressed in Escherichia-coli N-terminal domain. J Biol Chem 269:19910-19915
21. 21. Beja O, Bibi E (1995) Multidrug-resistance protein (MDR)-alkaline phosphatase hybrids in Escherichia-coli suggest a major revision in the topology of the C-terminal half of MDR. J Biol Chem 270:12351-12354
22. 22. Linton KJ, Higgins CF (1997) Topological analysis of the human multidrug resistance P-glycoprotein using β-lactamase fusions in Escherichia coli. Biochem J. Submitted
23. 23. Sonveaux N, Shapiro AB, Goormaghtigh E, Ling V, Ruysschaert J-M (1996) Secondary and tertiary structure changes of reconstituted P-glycoprotein. J Biol Chem 271:24617-24624
24. 24. Bruggeman EP, Germann UA, Gottesman MM, Pastan I (1989) Two different regions of phosphoglycoprotein are photoaffinity labelled by azidopine. J Biol Chem 264:15483-15488
25. 25. Greenberger LM, Lisanti CJ, Silva JT, Horwitz SB (1991) Domain mapping of the photoaffinity drug binding sites in P-glycoprotein encoded by mouse mdr1b. J Biol Chem 266:20744-20751
26. 26. Ferry DR, Russell MA, Cullen MH (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
27. 3H]vinblastine binding to P-glycoprotein of CCRF ADR5000 cells. Eur J Pharmacol 288:105-114
28. 28. Martin C, Berridge G, Higgins CF, Callaghan R (1997) The multidrug resistance reversal agent SR33557 modulates vinca alkaloid binding to P-glycoprotein by an allosteric interaction. Br J Pharmacol (in press)
29. 29. Tame JRH, Murshudov GN, Dodson EJ, Neil TK, Dodson GG, Higgins CF, Wilkson AJ (1994) The structural basis of sequence-independent peptide binding by OppA protein. Science 264:1578-1581
30. 30. Tame JRH, Sleigh SH, Wilkinson AJ, Ladbury JE (1996) The role of water in sequence-independent ligand binding by an oligopeptide transporter protein. Nature Structural Biology 3:998-1001
31. 31. Bianchet MA, Bains G, Pelosi P, Pevsner J, Snyder SH, Monaco HL, Amzel LM (1996) The three-dimensional structure of bovine odorant binding protein and its mechanism of odor recognition. Nature Structural Biology 3:934-939
32. 32. Higgins CF, Gottesman MM (1992) Is the multidrug transporter a flippase? TIBS 17:18-21
33. 33. Sarkadi B, Price EM, Boucher RC, Germann UA, Scarborough GA (1992) Expression of the human multidrug resistance cDNA in insect cells generates a high-activity drug-stimulated membrane ATPase. J Biol Chem 267:4854-4858
34. 34. Ambudkar SV, Lelong IH, Zhang J, Cardarelli CO, Gottesman MM, Pastan I (1992) Partial purification and reconstitution of the human multidrug-resistance pump: characterisation of the drug-stimulatable ATP hydrolysis. Proc Natl Acad Sci (USA) 89:8472-8476
35. 35. Loo TW, Clarke DM (1996) Inhibition of oxidative cross-linking between engineered cysteine residues at position-332 in predicted transmembrane segments (TM) 6 and (TM) 975 in predicted TM12 of human P-glycoprotein by drug substrates. J Biol Chem 271:27482-27487
36. 36. Hyde SC, Emsley P, Hartshorn MJ, Mimmack MM, Gileadi U, Pearce SR, Gallagher MP, Gill DR, Hubbard RE, Higgins CF (1990) Structural model of ATP-binding proteins associated with cystic fibrosis, multidrug resistance and bacterial transport. Nature 346:362-365
37. 37. Mimura CS, Holbrook SR, Ames GF-L (1991) Structural model of the nucleotide-binding conserved component of periplasmic permeases. Proc Natl Acad Sci (USA) 88:84-88
38. 38. Baichwal V, Lui D, Ames GF-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
39. 39. Schneider E, Hunke S, Tebbe S (1995) The MalK protein of the ATP-binding cassette transporter for maltose of Escherichia coli is accessible to protease digestion from the periplasmic side of the membrane. J Bacteriol 177:5364-5367
40. 40. Bliss JM, Silver RP (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
41. 41. Loo TW, Clarke DM (1996) The minimum functional unit of human P-glycoprotein appears to be a monomer. J Biol Chem 271:27488-27492
42. 42. Boscoboinik D, Debanne MT, Stafford AR, Jung CY, Gupta RS, Epand RM (1990) Dimerization of the P-glycoprotein in membranes. Biochim Biophys Acta 1027:225-228
43. 43. Naito M, Tsuruo T (1992) Functionally active homodimer of P-glycoprotein in multidrug-resistant tumor cells. Biochem Biophys Res Commun 185:284-290
44. 44. Poruchynsky MS, Ling V (1994) Detection of oligomeric and monomeric forms of P-glycoprotein in multidrug-resistant cells. Biochemistry 33:4163-4174
45. 45. Raviv Y, Pollard HB, Bruggemann EP, Pastan I, Gottesman MM (1990) Photosensitized labelling of a functional multidrug transporter in living drug-resistant tumour cells. J Biol Chem 265:3975-3980
46. 46. Homolya L, Hollo Z, Germann UA, Pastan I, Gottesman MM, Sarkadi B (1993) Fluorescent cellular indicators are extruded by the multidrug-resistance protein. J Biol Chem 268:21493-21496
47. 47. Malkhandi J, Ferry DR, Boer R, Callaghan R, Russell M, Ulrich W-R (1997) Localisation of the 1,4-dehydropyridine drug acceptor of P-glycoprotein to an intracellular domain. J Biol Chem. Submitted
48. 48. Greenberger LM (1993) Major photoaffinity drug labelling sites for iodoaryl azidoprazosin in P-glycoprotein are within, or immediately C-terminal to, transmembrane domain-6 and domain-12. J Biol Chem 268:11417-11425
49. 49. Safa AR, Stern RK, Choi K, Agresti M, Tamai I, Mehta ND, Roninson JB (1990) Molecular basis of preferential resistance to colchicine in multidrug-resistant human cells conferred by gly-185-val-185 substitution in P-glycoprotein. Proc Natl Acad Sci (USA) 87:7225-7229
50. 50. Choi K, Chen C-J, Kriegler M, Roninson IB (1988) An altered pattern of cross-resistance in multidrug-resistant human cells results from spontaneous mutations in the MDR1 (P-glycoprotein) gene. Cell 53:519-529.
51. 51. Luecke H, Chang BT, Mailliard WS, Schaepfer DD, Haigler HT (1995) Crystal-structure of the annexin-xii hexamer and implications for bilayer insertion. Nature 378:512-515
52. 52. Hamman BD, Chen J-C, Johnson EE, Johnson AE (1997) The aqueous pore through the translocon has a diameter of 40-60 Å during cotranslational protein translocation at the ER membrane. Cell 89:535-544
53. 53. Higgins CF (1992) ABC transporters: from microorganisms to man. Ann Rev Cell Biol 8:67-113
54. 54. Akabas MH, Kaufmann C, Cook TA, Archdeacon P (1994) Amino acid residues lining the chloride channel of the cystic fibrosis transmembrane conductance regulator. J Biol Chem 269:148-14868