Improved expression and purification of human multidrug resistance protein MDR1 from baculovirus-infected insect cells

Protein Expression and Purification

Volumn 66, Issue 1, 2009, Pages 7-14

  Kodan, Atsushi ^a,c,d   Shibata, Hiroyuki ^a   Matsumoto, Takashi ^a   Terakado, Kanako ^a,b   Sakiyama, Keita ^a,b   Matsuo, Michinori ^d   Ueda, Kazumitsu ^c,d   Kato, Hiroaki ^a,b  

^a RIKEN HARIMA INSTITUTE   (Japan)

^b KYOTO UNIVERSITY   (Japan)

^c KYOTO UNIVERSITY   (Japan)

^d KYOTO UNIVERSITY   (Japan)

Author keywords

Baculovirus; Expression; Insect cell; Membrane proteins; Purification

Indexed keywords

BUFFER; GLYCOPROTEIN P;

ANIMAL; ARTICLE; BACULOVIRUS; CELL LINE; CELL MEMBRANE; CHEMISTRY; ENZYME STABILITY; GENETICS; HUMAN; INSECT; ISOLATION AND PURIFICATION; METABOLISM;

ANIMALS; BACULOVIRIDAE; BUFFERS; CELL LINE; CELL MEMBRANE; ENZYME STABILITY; HUMANS; INSECTS; P-GLYCOPROTEIN;

HEXAPODA;

EID: 63649083045     PISSN: 10465928     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pep.2009.02.010     Document Type: Article

References (51)

1. Ueda K., Cardarelli C., Gottesman M.M., and Pastan I. Expression of a full-length cDNA for the human MDR1 gene confers resistance to colchicine, doxorubicin, and vinblastine. Proc. Natl. Acad. Sci. USA 84 (1987) 3004-3008
2. Chen C.J., Chin J.E., Ueda K., Clark D.P., Pastan I., Gottesman M.M., and Roninson I.B. Internal duplication and homology with bacterial transport proteins in the mdr1 (P-glycoprotein) gene from multidrug-resistant human cells. Cell 47 (1986) 381-389
3. Sharom F.J. The P-glycoprotein efflux pump: how does it transport drugs?. J. Membr. Biol. 160 (1997) 161-175
4. Endicott J.A., and Ling V. The biochemistry of P-glycoprotein-mediated multidrug resistance. Annu. Rev. Biochem. 58 (1989) 137-171
5. Senior A.E., al-Shawi, I.L. Urbatsch M.K., and Urbatsch I.L. The catalytic cycle of P-glycoprotein. FEBS Lett. 377 (1995) 285-289
6. Ambudkar S.V., Dey S., Hrycyna C.A., Ramachandra M., Pastan I., and Gottesman M.M. Biochemical, cellular, and pharmacological aspects of the multidrug transporter. Annu. Rev. Pharmacol. Toxicol. 39 (1999) 361-398
7. Loo T.W., and Clarke D.M. Quality control by proteases in the endoplasmic reticulum. Removal of a protease-sensitive site enhances expression of human P-glycoprotein. J. Biol. Chem. 273 (1998) 32373-32376
8. Schinkel A.H., Kemp S., Dolle M., Rudenko G., and Wagenaar E. N-glycosylation and deletion mutants of the human MDR1 P-glycoprotein. J. Biol. Chem. 268 (1993) 7474-7481
9. Ueda K., Shimabuku A.M., Konishi H., Fujii Y., Takebe S., Nishi K., Yoshida M., Beppu T., and Komano T. Functional expression of human P-glycoprotein in Schizosaccharomyces pombe. FEBS Lett. 330 (1993) 279-282
10. Evans G.L., Ni B., Hrycyna C.A., Chen D., Ambudkar S.V., Pastan I., Germann U.A., and Gottesman M.M. Heterologous expression systems for P-glycoprotein: E. coli, yeast, and baculovirus. J. Bioenerg. Biomembr. 27 (1995) 43-52
11. Kuchler K., and Thorner J. Functional expression of human mdr1 in the yeast Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 89 (1992) 2302-2306
12. Ambudkar S.V., Lelong I.H., Zhang J., Cardarelli C.O., Gottesman M.M., and Pastan I. Partial purification and reconstitution of the human multidrug-resistance pump: characterization of the drug-stimulatable ATP hydrolysis. Proc. Natl. Acad. Sci. USA 89 (1992) 8472-8476
13. Gottesman M.M., Pastan I., and Ambudkar S.V. P-glycoprotein and multidrug resistance. Curr. Opin. Genet. Dev. 6 (1996) 610-617
14. Ramachandra M., Ambudkar S.V., Gottesman M.M., Pastan I., and Hrycyna C.A. Functional characterization of a glycine 185-to-valine substitution in human P-glycoprotein by using a vaccinia-based transient expression system. Mol. Biol. Cell 7 (1996) 1485-1498
15. 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. Repacking of the transmembrane domains of P-glycoprotein during the transport ATPase cycle. EMBO J. 20 (2001) 5615-5625
16. Rosenberg M.F., Kamis A.B., Callaghan R., Higgins C.F., and Ford R.C. Three-dimensional structures of the mammalian multidrug resistance P-glycoprotein demonstrate major conformational changes in the transmembrane domains upon nucleotide binding. J. Biol. Chem. 278 (2003) 8294-8299
17. Lee J.Y., Urbatsch I.L., Senior A.E., and Wilkens S. Nucleotide-induced structural changes in P-glycoprotein observed by electron microscopy. J. Biol. Chem. 283 (2008) 5769-5779
18. Rosenberg M.F., Callaghan R., Ford R.C., and Higgins C.F. Structure of the multidrug resistance P-glycoprotein to 2.5 nm resolution determined by electron microscopy and image analysis. J. Biol. Chem. 272 (1997) 10685-10694
19. Dawson R.J., and Locher K.P. Structure of a bacterial multidrug ABC transporter. Nature 443 (2006) 180-185
20. Ward A., Reyes C.L., Yu J., Roth C.B., and Chang G. Flexibility in the ABC transporter MsbA: alternating access with a twist. Proc. Natl. Acad. Sci. USA 104 (2007) 19005-19010
21. Velamakanni S., Yao Y., Gutmann D.A., and van Veen H.W. Multidrug transport by the ABC transporter Sav1866 from Staphylococcus aureus. Biochemistry 47 (2008) 9300-9308
22. Cai J., and Gros P. Overexpression, purification, and functional characterization of ATP-binding cassette transporters in the yeast, Pichia pastoris. Biochim. Biophys. Acta 1610 (2003) 63-76
23. Germann U.A. Baculovirus-mediated expression of human multidrug resistance cDNA in insect cells and functional analysis of recombinant P-glycoprotein. Methods Enzymol. 292 (1998) 427-441
24. Figler R.A., Omote H., Nakamoto R.K., and Al-Shawi M.K. Use of chemical chaperones in the yeast Saccharomyces cerevisiae to enhance heterologous membrane protein expression: high-yield expression and purification of human P-glycoprotein. Arch. Biochem. Biophys. 376 (2000) 34-46
25. Urbatsch I.L., Wilke-Mounts S., Gimi K., and Senior A.E. Purification and characterization of N-glycosylation mutant mouse and human P-glycoproteins expressed in Pichia pastoris cells. Arch. Biochem. Biophys. 388 (2001) 171-177
26. Kerr K.M., Sauna Z.E., and Ambudkar S.V. Correlation between steady-state ATP hydrolysis and vanadate-induced ADP trapping in human P-glycoprotein. Evidence for ADP release as the rate-limiting step in the catalytic cycle and its modulation by substrates. J. Biol. Chem. 276 (2001) 8657-8664
27. Loo T.W., and Clarke D.M. The minimum functional unit of human P-glycoprotein appears to be a monomer. J. Biol. Chem. 271 (1996) 27488-27492
28. McDevitt C.A., Shintre C.A., Grossmann J.G., Pollock N.L., Prince S.M., Callaghan R., and Ford R.C. Structural insights into P-glycoprotein (ABCB1) by small angle X-ray scattering and electron crystallography. FEBS Lett. 582 (2008) 2950-2956
29. Valiyaveetil F.I., Zhou Y., and MacKinnon R. Lipids in the structure, folding, and function of the KcsA K+ channel. Biochemistry 41 (2002) 10771-10777
30. Lee A.G. Lipid-protein interactions in biological membranes: a structural perspective. Biochim. Biophys. Acta 1612 (2003) 1-40
31. Guan L., Smirnova I.N., Verner G., Nagamori S., and Kaback H.R. Manipulating phospholipids for crystallization of a membrane transport protein. Proc. Natl. Acad. Sci. USA 103 (2006) 1723-1726
32. Zhang H., Kurisu G., Smith J.L., and Cramer W.A. A defined protein-detergent-lipid complex for crystallization of integral membrane proteins: the cytochrome b6f complex of oxygenic photosynthesis. Proc. Natl. Acad. Sci. USA 100 (2003) 5160-5163
33. Smith G.E., Foellmer H.G., Knell J., DeBartolomeis J., and Voznesensky A.I. Spodoptera frugiperda single cell suspension cell line in serum-free media, methods of producing and using. Protein Sciences Corporation (Meriden, CT) (2000)
34. Kimura Y., Shibasaki S., Morisato K., Ishizuka N., Minakuchi H., Nakanishi K., Matsuo M., Amachi T., Ueda M., and Ueda K. Microanalysis for MDR1 ATPase by high-performance liquid chromatography with a titanium dioxide column. Anal. Biochem. 326 (2004) 262-266
35. Chifflet S., Torriglia A., Chiesa R., and Tolosa S. A method for the determination of inorganic phosphate in the presence of labile organic phosphate and high concentrations of protein: application to lens ATPases. Anal. Biochem. 168 (1988) 1-4
36. Bligh E.G., and Dyer W.J. A rapid method of total lipid extraction and purification. Can. J. Med. Sci. 37 (1959) 911-917
37. Cogan E.B., Birrell G.B., and Griffith O.H. A robotics-based automated assay for inorganic and organic phosphates. Anal. Biochem. 271 (1999) 29-35
38. Rao V.V., Chiu M.L., Kronauge J.F., and Piwnica-Worms D. Expression of recombinant human multidrug resistance P-glycoprotein in insect cells confers decreased accumulation of technetium-99m-sestamibi. J. Nucl. Med. 35 (1994) 510-515
39. Ramachandra M., Ambudkar S.V., Chen D., Hrycyna C.A., Dey S., Gottesman M.M., and Pastan I. Human P-glycoprotein exhibits reduced affinity for substrates during a catalytic transition state. Biochemistry 37 (1998) 5010-5019
40. Weiss H.M., and Grisshammer R. Purification and characterization of the human adenosine A(2a) receptor functionally expressed in Escherichia coli. Eur. J. Biochem. 269 (2002) 82-92
41. Garrigues A., Escargueil A.E., and Orlowski S. The multidrug transporter, P-glycoprotein, actively mediates cholesterol redistribution in the cell membrane. Proc. Natl. Acad. Sci. USA 99 (2002) 10347-10352
42. Loo T.W., and Clarke D.M. 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 (1995) 21449-21452
43. Engel C.K., Chen L., and Prive G.G. Stability of the lactose permease in detergent solutions. Biochim. Biophys. Acta 1564 (2002) 47-56
44. Boulter J.M., and Wang D.N. Purification and characterization of human erythrocyte glucose transporter in decylmaltoside detergent solution. Protein Expr. Purif. 22 (2001) 337-348
45. Loo T.W., and Clarke D.M. Mutational analysis of human P-glycoprotein. Methods Enzymol. 292 (1998) 480-492
46. Nuti S.L., Mehdi A., and Rao U.S. Activation of the human P-glycoprotein ATPase by trypsin. Biochemistry 39 (2000) 3424-3432
47. Dong M., Penin F., and Baggetto L.G. Efficient purification and reconstitution of P-glycoprotein for functional and structural studies. J. Biol. Chem. 271 (1996) 28875-28883
48. Jiang Y., Lee A., Chen J., Cadene M., Chait B.T., and MacKinnon R. Crystal structure and mechanism of a calcium-gated potassium channel. Nature 417 (2002) 515-522
49. Sharom F.J., Yu X., Chu J.W., and Doige C.A. Characterization of the ATPase activity of P-glycoprotein from multidrug-resistant Chinese hamster ovary cells. Biochem. J. 308 Pt 2 (1995) 381-390
50. Ravaud S., Do Cao M.A., Jidenko M., Ebel C., Le Maire M., Jault J.M., Di Pietro A., Haser R., and Aghajari N. The ABC transporter BmrA from Bacillus subtilis is a functional dimer when in a detergent-solubilized state. Biochem. J. 395 (2006) 345-353
51. Poolman B., Doeven M.K., Geertsma E.R., Biemans-Oldehinkel E., Konings W.N., and Rees D.C. Functional analysis of detergent-solubilized and membrane-reconstituted ATP-binding cassette transporters. Methods Enzymol. 400 (2005) 429-459