Reconstitution and partial characterization of phospholipid flippase activity from detergent extracts of the Bacillus subtilis cell membrane

Journal of Bacteriology

Volumn 182, Issue 15, 2000, Pages 4198-4206

  Hrafnsdóttir, Sigrún ^a   Menon, Anant K ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MEMBRANE PROTEIN; DETERGENT; GLYCEROL; LIPOSOME; PHOSPHOLIPASE A2; PHOSPHOLIPID DERIVATIVE; PHOSPHOLIPID FLIPPASE; UNCLASSIFIED DRUG;

ARTICLE; BACILLUS SUBTILIS; BACTERIAL MEMBRANE; CELL MEMBRANE TRANSPORT; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME RECONSTITUTION; LIPID BILAYER; LIPID COMPOSITION; LIPID VESICLE; MEMBRANE STRUCTURE; NONHUMAN; PHOSPHOLIPID TRANSFER; PRIORITY JOURNAL; PROTEIN MODIFICATION; PROTEOLIPOSOME; TRANSPORT KINETICS;

ATP-BINDING CASSETTE TRANSPORTERS; BACILLUS SUBTILIS; BIOLOGICAL TRANSPORT, ACTIVE; CARRIER PROTEINS; CELL MEMBRANE; DETERGENTS; DRUG RESISTANCE, MULTIPLE; OCTOXYNOL; P-GLYCOPROTEINS; PHOSPHATIDYLCHOLINES; PHOSPHOLIPIDS; PROTEOLIPIDS; SOLUBILITY;

EID: 0033927123     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.182.15.4198-4206.2000     Document Type: Article

References (45)

1. 2+-dependent transbilayer movement of phospholipid. J. Biol. Chem. 271:17205-17210.
2. Bell, R. M., R. D. Mavis, M. J. Osborn, and P. R. Vagelos. 1971. Enzymes of phospholipid metabolism: localization in the cytoplasmic and outer membrane of the cell envelope of Escherichia coli and Salmonella typhimurium. Biochim. Biophys. Acta 249:628-635.
3. Bishop, W. R., and R. M. Bell. 1985. Assembly of the endoplasmic reticulum phospholipid bilayer: the phosphatidylcholine transporter. Cell 42:51-60.
4. Bligh, E. G., and W. J. Dyer. 1959. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37:911-917.
5. Buton, X., G. Morrot, P. Fellmann, and M. Seigneuret. 1996. Ultrafast glycerophospholipid-selective transbilayer motion mediated by a protein in the endoplasmic reticulum membrane. Biochim. Biophys. Acta 249:636-642.
6. Daleke, D. L., and W. H. Huestis. 1985. Incorporation and translocation of aminophospholipids in human erythrocytes. Biochemistry 24:5406-5416.
7. Devaux, P. F. 1993. Lipid transmembrane asymmetry and flip-flop in biological membranes and in lipid bilayers. Curr. Opin. Struct. Biol. 3:489-494.
8. Dolis, D., C. Moreau, A. Zachowski, and P. F. Devaux. 1997. Aminophospholipid translocase and proteins involved in transmembrane phospholipid traffic. Biophys. Chem. 68:221-231.
9. Fattal, E., S. Nir, R. A. Parente, and F. C. Szoka, Jr. 1994. Pore-forming peptides induce rapid phospholipid flip-flop in membranes. Biochemistry 33:6721-6731.
10. Gupta, C. M., R. Radhakrishnan, and H. G. Khorana. 1977. Glycerophospholipid synthesis: improved general method and new analogs containing photoactivable groups. Proc. Natl. Acad. Sci. USA 74:4315-4319.
11. Hrafnsdóttir, S., J. W. Nichols, and A. K. Menon. 1997. Transbilayer movement of fluorescent phospholipids in Bacillus megaterium membrane vesicles. Biochemistry 36:4969-4978.
12. 6-NBD-labeled phospholipids across the inner membrane of Escherichia coli. Biochim. Biophys. Acta 1280:41-50.
13. Huijbregts, R. P. H., A. I. P. M. de Kroon, and B. de Kruijff. 1998. Rapid transmembrane movement of newly synthesized phosphatidylethanolamine across the inner membrane of Escherichia coli. J. Biol. Chem. 273:18936-18942.
14. Huijbregts, R. P. H., A. I. P. M. de Kroon, and B. de Kruijff. 2000. Topology and transport of membrane lipids in bacteria. Biochim. Biophys. Acta 1469: 43-61.
15. Hutson, J. L., and J. A. Higgins. 1982. Asymmetric synthesis followed by transmembrane movement of phosphatidylethanolamine in rat liver endoplasmic reticulum. Biochim. Biophys. Acta 687:247-256.
16. Kates, M. 1986. Techniques of lipidology. Elsevier. Amsterdam. The Netherlands.
17. Konings, W. N., A. Bisschop, M. Veenhuis, and C. A. Vermeulen. 1973. New procedure for the isolation of membrane vesicles of Bacillus subtilis and an electron microscopy study of their ultrastructure. J. Bacteriol. 116:1456-1465.
18. Kornberg, R. D., and H. M. McConnell, 1971. Inside-outside transitions of phospholipids in vesicle membranes. Biochemistry 10:1111-1120.
19. Kramer, R. M., H. Hasselbach, and G. Semenza. 1981. Rapid transmembrane movement of phosphatidylcholine in small unilamellar lipid vesicles formed by detergent removal. Biochim. Biophys. Acta 643:233-242.
20. Langley, K. E., and E. P. Kennedy. 1979. Energetics of rapid transmembrane movement and of compositional asymmetry of phosphatidylethanolamine in membranes of Bacillus megaterium. Proc. Natl. Acad. Sci. USA 76:6245-6249.
21. Levy, D., A. Bluzat, M. Seigneuret, and J.-L. Rigaud. 1990. A systematic study of liposome reconstitution involving Bio-Bead-mediated Triton X-100 removal. Biochim. Biophys. Acta 1025:179-190.
22. Margolles, A., M. Putman, H. van Veen, and W. N. Konings. 1999. The purified and functionally reconstituted multidrug transporter LmrA of Lactococcus lactis mediates the transbilayer movement of specific fluorescent phospholipids. Biochemistry 38:16298-16306.
23. Martin, O. C., and R. E. Pagano. 1987. Transbilayer movement of fluorescent analogs of phosphatidylserine and phosphatidylethanolamine at the plasma membrane of cultured cells. J. Biol. Chem. 262:5890-5898.
24. Matsuzaki, K., S. Yoneyama, O. Murase, and K. Miyajima. 1996. Transbilayer transport of ions and lipids coupled with mastroparan X translocation. Biochemistry 35:8450-8456.
25. Matsuzaki, K., O. Murase, N. Fujii, and K. Miyajima. 1996. An antimicrobial peptide, magainin 2, induces rapid flip-flop of phospholipids couples with pore formation and peptide translocation. Biochemistry 35:11361-11368.
26. Menon, A. K. 1995. Flippases. Trends Cell Biol. 5:355-360.
27. Mimms, L. T., G. Zampighi, Y. Nozaki, C. Tanford, and J. A. Reynolds. 1981. Phospholipid vesicle formation and transmembrane protein incorporation using octyl glucoside. Biochemistry 20:833-840.
28. Moll, G. N., W. N. Konings, and A. J. M. Driessen. 1998. The lantibiotic nisin induces transmembrane movement of a fluorescent phospholipid. J. Bacteriol. 180:6565-6570.
29. Patterson, P. H., and W. J. Lennarz. 1971. Studies on the membranes of bacilli. I. Phospholipid biosynthesis. J. Biol. Chem. 246:1062-1072.
30. Polissi, A., and C. Georgopoulos. 1996. Mutational analysis and properties of the msbA gene of Escherichia coli, coding for an essential ABC family transporter. Mol. Microbiol. 20:1221-1233.
31. Raggers, R. J., A. van Helvoort, R. Evers, and G. van Meer. 1999. The human multidrug resistance protein MRP1 translocates sphingolipid analogs across the plasma membrane. J. Cell Sci. 112:415-422.
32. Rothman, J. E., and E. P. Kennedy. 1977. Rapid transmembrane movement of newly synthesizes phospholipids during membrane assembly. Proc. Natl. Acad. Sci. USA 74:1821-1825.
33. Rouser, G., S. Fleischer, and A. Yamamoto. 1970. Two dimensional thin layer chromatographic separation of polar lipids and determination of phospholipids by phosphorus analysis of spots. Lipids 5:494-496.
34. Ruetz, S., and P. Gros. 1994. Phosphatidylcholine translocase: a physiological role for the mdr2 gene. Cell 77:1071-1081.
35. Saier, M. H., Jr., I. T. Paulsen, M. K. Sliwinski, S. S. Pao, R. A. Skurray, and H. Nikaido. 1998. Evolutionary origins of multidrug and drug-specific efflux pumps in bacteria. FASEB J. 12:265-274.
36. Seigneuret, M., and P. F. Devaux. 1984. ATP-dependent asymmetric distribution of spin-labeled phospholipids in the erythrocyte membrane: relation to shape changes. Proc. Natl. Acad. Sci. USA 81:3751-3755.
37. Shai, Y. 1999. Mechanism of the binding, insertion and destabilization of phospholipid bilayer membranes by α-helical antimicrobial and cell non-selective membrane-lytic peptides. Biochim. Biophys. Acta 1462:55-70.
38. Smith, A. J., J. L. P. M. Timmermans-Hereijgers, B. Roelofsen, K. W. A. Wirtz, W. J. van Blitterswijk, J. J. M. Smit, A. H. Schinkel, and P. Borst. 1994. The human MDR3 P-glycoprotein promotes translocation of phosphatidylcholine through the plasma membrane of fibroblasts from transgenic mice. FEBS Lett. 354:263-266.
39. van Helvoort, A., A. J. Smith, H. Sprong, I. Fritzsche, A. H. Schinkel, P. Borst, and G. van Meer. 1996. MDR1 P-glycoprotein is a lipid translocase of broad specificity, while MDR3 P-glycoprotein specifically translocates phosphatidylcholine. Cell 87:507-517.
40. van Veen, H., and W. N. Konings. 1998. The ABC family of multidrug transporters in microorganisms. Biochim. Biophys. Acta 1365:31-36.
41. Wessel, D., and U. I. Flügge. 1984. A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Anal. Biochem. 138:141-143.
42. White, D. A., F. R. Albright, W. J. Lennarz, and C. A. Schaitman. 1971. Distribution of phospholipid-synthesizing enzymes in the wall and membrane subfractions of the envelope of Escherichia coli. Biochim. Biophys. Acta 249:636-642.
43. Zachowski, A. 1993. Phospholipids in animal eukaryotic membranes: transverse asymmetry and movement. Biochem. J. 294:1-14.
44. Zhou, Q., J. Zhao, J. G. Stout, R. A. Luhm, T. Wiedmer, and P. J. Sims. 1997. Molecular cloning of human plasma membrane phospholipid scramblase. J. Biol. Chem. 272:18240-18244.
45. Zhou, Z., K. A. White, A. Polissi, C. Georgopoulos, and C. R. H. Raetz. 1998. Function of Escherichia coli MsbA, and essential ABC family transporter, in lipid A and phospholipid biosynthesis. J. Biol. Chem. 273:12466-12475.