Sorting of lipids and transmembrane peptides between detergent-soluble bilayers and detergent-resistant rafts

Biophysical Journal

Volumn 85, Issue 3, 2003, Pages 1656-1666

  McIntosh, Thomas J ^a   Vidal, Adriana ^a   Simon, Sidney A ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLESTEROL; DETERGENT; DIOLEOYLPHOSPHATIDYLCHOLINE; MEMBRANE PROTEIN; SPHINGOMYELIN; TRITON X 100;

ARTICLE; BILAYER MEMBRANE; CELL MEMBRANE; CONTROLLED STUDY; HYDROPHOBICITY; LIPID COMPOSITION; NONHUMAN; PROTEIN ANALYSIS; PROTEIN LOCALIZATION; TEMPERATURE DEPENDENCE;

EID: 0041821501     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(03)74595-0     Document Type: Article

References (73)

1. Ahmed, S. N., D. A. Brown, and E. London. 1997. On the origin of sphingolipid/cholesterol-rich detergent-insoluble cell membranes: physiological concentrations of cholesterol and sphingolipid induce formation of a detergent-insoluble, liquid-ordered lipid phase in model membranes. Biochemistry. 36:10944-10953.
2. Allende, D., A. Vidal, S. A. Simon, and T. J. McIntosh. 2003. Bilayer interfacial properties modulate the binding of amphipathic peptides. Chem. Phys. Lipids. 122:65-76.
3. Arreaza, G., and D. A. Brown. 1995. Sorting and intracellular trafficking of a glycosylphosphatidylinositol-anchored protein and two hybrid proteins with the same ectodomain in MDCK kidney epithelial cell. J. Biol. Chem. 270:23641-23647.
4. Baird, B., E. D. Sheets, and D. Holowka. 1999. How does the plasma membrane participate in cellular signaling by receptors for immunoglobulin E? Biophys. Chem. 82:109-119.
5. Banfield, D. K., M. J. Lewis, C. Rabouille, G. Warren, and H. R. B. Pelham. 1994. Localization of Sed5, a putative vesicle targeting molecule, to the cis-Golgi network involves both its transmembrane and cytoplasmic domains. J. Cell Biol. 127:357-371.
6. Ben-Shaul, A., N. Ben-Tal, and B. Honig. 1996. Statistical thermodynamic analysis of peptide and protein insertion into lipid membranes. Biophys. J. 71:130-137.
7. Bretscher, M. S., and S. Munro. 1993. Cholesterol and the Golgi apparatus. Science. 261:1280-1281.
8. Brown, D. A., and E. London. 1998. Functions of lipid rafts in biological membranes. Annu. Rev. Cell Dev. Biol. 14:111-136.
9. Brown, D. A., and E. London. 2000. Structure and function of sphingolipid-and cholesterol-rich membrane rafts. J. Biol. Chem. 275:17221-17224.
10. Brown, R. E. 1998. Sphingolipid organization in biomembranes: what physical studies of model membranes reveal. J. Cell Sci. 111:1-9.
11. Chamberlain, L. H., R. D. Burgoyne, and G. W. Gould. 2001. SNARE proteins are highly enriched in lipid rafts in PC12 cells: implications for the spatial control of exocytosis. Proc. Natl. Acad. Sci. USA. 98:5619-5624.
12. Chen, P. S., Jr., T. Y. Toribara, and H. Warner. 1956. Microdetermination of phosphorous. Anal. Chem. 28:1756-1758,
13. Cole, N. B., J. Ellenberg, J. Song, D. Dieuliis, and J. Lippincott-Schwartz. 1998. Retrograde transport of Golgi-localized proteins to the ER. J. Cell Biol. 140:1-15.
14. DePlanque, M. R. R., E. Goormaghigh, D. V. Greathouse, R. E. Koeppe, J. A. W. Kruijtzer, R. M. J. Liskamp, B. Dekruijff, and J. A. Killian. 2001. Sensitivity of single membrane-spanning alpha-helical peptides to hydrophobic mismatch with a lipid bilayer: effects of backbone structure, orientation, and extent of membrane incorporation. Biochemistry. 40:5000-5010.
15. DePlanque, M. R. R., J. A. W. Kruijtzer, R. A. Liskamp, D. Marsh, D. V. Greathouse, R. E. Koeppe, B. Dekruijff, and J. A. Killian. 1999. Different membrane anchoring positions of tryptophan and lysine in synthetic transmembrane alpha-helical peptides. J. Biol. Chem. 274:20839-20846.
16. Dietrich, C., L. A. Bagatolli, Z. N. Volovyk, N. L. Thompson, M. Levi, K. Jacobson, and E. Gratton. 2001. Lipid rafts reconstituted in model membranes. Biophys. J. 80:1417-1428.
17. Edidin, M. 1998. Lipid microdomains in cell surface membranes. Curr. Opin. Struct. Biol. 7:528-532.
18. Evans, E., and D. Needham. 1987. Physical properties of surfactant bilayer membranes: thermal transitions, elasticity, rigidity, cohesion, and colloidal interactions. J. Phys. Chem. 91:4219-4228.
19. Evans, E. A., and W. Rawicz. 1990. Entropy-driven tension and bending elasticity in condensed-fluid membranes. Phys. Rev. Lett. 64:2094-2097.
20. Field, K. A., D. Holowka, and B. Baird. 1997. Compartmentalized activation of the high affinity immunoglobulin E receptor within membrane domains. J. Biol. Chem. 272:4276-4280.
21. Fridriksson, E. K., P. A. Shipkova, E. D. Sheets, D. Holowka, B. Baird, and F. W. Mclafferty. 1999. Quantitative analysis of phospholipids in functionally important membrane domains from RBL-2H3 mast cells using tandem high-resolution mass spectrometry. Biochemistry. 38:8056-8063.
22. Galbiati, F., B. Razani, and M. P. Lisanti. 2001. Emerging themes in lipid rafts and caveolae. Cell. 106:403-411.
23. Gandhavadi, M., D. Allende, A. Vidal, S. A. Simon, and T. J. McIntosh. 2002. Structure, composition, and peptide binding properties of detergent soluble bilayers and detergent resistant rafts. Biophys. J. 82:1469-1482.
24. Gkantiragas, I., B. Brugger, E. Stuven, D. Kaloyanova, X.-Y. Li, K. Lohr, F. Lottspeich, F. T. Wieland, and J. B. Helms. 2001. Sphingomyelin-enriched microdomains at the Golgi complex. Mol. Biol. Cell. 12:1819-1833.
25. Hanada, K., M. Nishijima, Y. Akamatsu, and R. E. Pagano. 1995. Both sphingolipids and cholesterol participate in the detergent insolubility of alkaline-phosphatase, a glycosylphosphatidylinositol-anchored protein, in mammalian membranes. J. Biol. Chem. 270:6254-6260.
26. Heerklotz, H. 2002. Triton promotes domain formation in lipid raft mixtures. Biophys. J. 83:2693-2701.
27. Holthuis, J. C., T. Pomorski, R. J. Raggers, H. Sprong, and G. Van Meer. 2001. The organizing potential of sphingolipids in intracellular membrane transport. Physiol. Rev. 81:1689-1723.
28. Hunt, J., P. Rath, K. J. Rothschild, and D. M. Engelman. 1997. Spontaneous, pH-dependent membrane insertion of a transbilayer alpha-helix. Biochemistry. 36:15177-15192.
29. Ikonen, E. 2001. Roles of lipid rafts in membrane transport. Curr. Opin. Cell Biol. 13:470-477.
30. Kabouridis, P. S., J. Janzen, A. L. Agee, and S. C. Ley. 2000. Cholesterol depletion disrupts lipid rafts and modulates the activity of multiple signaling pathways in T lymphocytes. Eur. J. Immunol. 30:954-963.
31. Kawabuchi, M., Y. Satomi, T. Takao, Y. Shimonishi, S. Nada, K. Nagai, A. Tarakhovsky, and M. Okada. 2000. Transmembrane phosphoprotein Chp regulates the activity of Src-family of tyrosine kinase. Nature. 404:999-1003.
32. Kenworthy, A. K., and M. Edidin. 1998. Distribution of glycosylphosphatidylinositol-anchored protein at the apical surface of MDCK cells examined at a resolution of <100 Å using imaging fluorescence resonance energy transfer. J. Cell Biol. 142:69-84.
33. Lafont, F., P. Verkade, T. Galli, C. Wimmer, D. Louvard, and K. Simons, 1999. Raft association of SNAP receptors acting in apical trafficking in Madin-Darby canine kidney cells. Proc. Natl. Acad. Sci. USA. 96:3734-3738.
34. Lakowicz, J. R. 1983. Principles of Fluorescence Spectroscopy. Plenum Press, New York.
35. Lang, T., D. Bruns, D. Wenzel, D. Riedel, P. Holroyd, C. Thiele, and R. Jahn. 2001. SNAREs are concentrated in cholesterol-dependent clusters that define docking and fusion sites for exocytosis. EMBO J. 20:2202-2213.
36. Ledesma, M. D., B. Brugger, C. Bunning, F. T. Wieland, and C. G. Dotti. 1999. Maturation of the axonal plasma membrane requires upregulation of sphingomyelin synthesis and formation of protein-lipid complexes. EMBO J. 18:1761-1771.
37. Li, X.-M., M. M. Momsen, J. M. Smaby, H. L. Brockman, and R. E. Brown. 2001. Cholesterol decreases the interfacial elasticity and detergent solubility of sphingomyelins. Biochemistry. 40:5954-5963.
38. London, E., and D. A. Brown. 2000. Insolubility of lipids in Triton X-100: physical origin and relationship to sphingolipid/cholesterol membrane domains (rafts). Biochim. Biophys. Acta. 1508:182-195.
39. Lundbaek, J. A., O. S. Andersen, T. Werge, and C. Nielsen. 2003. Cholesterol-induced protein sorting. An analysis of energetic feasibility. Biophys. J. 84:2080-2089.
40. Macdonald, R. I. 1980 Action of detergents on membranes: differences between lipid extracted from red cell ghosts and from red cell lipid vesicles by Triton X-100. Biochemistry. 19:1916-1922.
41. Masibay, A. S., P. V. Balaji, E. E. Boeggeman, and P. K. Qasba. 1993. Mutational analysis of the Golgi retention signal of bovine beta-1,4-galactosyltransferase. J. Biol. Chem. 268:9908-9916.
42. McIntosh, T. J., and S. A. Simon. 1986. The hydration force and bilayer deformation: a reevaluation. Biochemistry. 25:4058-4066.
43. McIntosh, T. J., S. A. Simon, D. Needham, and C.-H. Huang. 1992. Structure and cohesive properties of sphingomyelin:cholesterol bilayers. Biochemistry. 31:2012-2020.
44. Melkonian, K. A., A. G. Ostermeyer, J. Z. Chen, M. G. Roth, and D. A. Brown. 1999. Role of lipid modifications in targeting proteins to detergent-resistant membrane rafts. Many raft proteins are acylated, while few are prenylated. J. Biol. Chem. 274:3910-3917.
45. Mesquita, R. M. R. S., E. Melo, T. E. Thompson, and W. L. C. Vaz. 2000. Partitioning of amphiphiles between coexisting ordered and disordered phases in two-phase lipid bilayer membranes. Biophys. J. 78:3019-3025.
46. Moffett, S., D. A. Brown, and M. E. Linder. 2000. Lipid-dependent targeting of G proteins into rafts. J. Biol. Chem. 275:2191-2198.
47. Morein, S., J. A. Killian, and M. M. Sperotto. 2002. Characterization of the thermotropic behavior and lateral organization of lipid-peptide mixtures by a combined experimental and theoretical approach: effect of hydrophobic mismatch and role of flanking residues. Biophys. J. 82:1405-1417.
48. Munro, S. 1991. Sequences within and adjacent to the transmembrane segment of 2,6-sialytransferase specify Golgi retention. EMBO J. 10:3577-3588.
49. Munro, S. 1995. An investigation of the role of transmembrane domains in Golgi protein retention. EMBO J. 14:4695-4704.
50. Needham, D., and R. S. Nunn. 1990. Elastic deformation and failure of lipid bilayer membranes containing cholesterol. Biophys. J. 58:997-1009.
51. Nilsson, T., J. M. Lucocq, D. Mackay, and G. Warren. 1991. The membrane spanning domain of β-1,4-galactosytransferase specifies trans Golgi localization. EMBO J. 10:3567-3575.
52. Niu, S. L., and B. J. Litman. 2002. Determination of membrane cholesterol partition coefficient using a lipid vesicle-cyclodextrin binary system: effect of phospholipid acyl chain unsaturation and headgroup composition. Biophys. J. 83:3408-3415.
53. Petrache, H. I., D. M. Zuckerman, J. N. Sachs, J. A. Killian, R. E. Koeppe, and T. B. Woolf. 2002. Hydrophobic matching mechanism investigated by molecular dynamics simulations. Langmuir. 18:1340-1351.
54. Prinetti, A., V. Chigorno, G. Tettamanti, and S. Sonnino. 2000. Sphingolipid-enriched membrane domains from rat cerebellar granule cells differentiated in culture, a compositional study. J. Biol. Chem. 275:11658-11665.
55. Rayner, J. C., and H. R. B. Pelham. 1997. Transmembrane domain-dependent sorting of proteins in the ER and plasma membrane in yeast. EMBO J. 16:1832-1841.
56. Ren, J., S. Lew, J. Wang, and E. London. 1999a. Control of the transmembrane orientation and interhelical interactions within membranes by hydrophobic helix length. Biochemistry. 38:5905-5912.
57. Ren, J., S. Lew, Z. Wang, and E. London. 1997. Transmembrane orientation of hydrophobic alpha-helices is regulated both by relationship of helix length to bilayer thickness and by the cholesterol concentration. Biochemistry. 36:10213-10220.
58. Ren, J., J. C. Sharpe, R. J. Collier, and E. London. 1999b. Membrane translocation of charged residues at the tips of hydrophobic helices in the T domain of diphtheria toxin. Biochemistry. 38:976-984.
59. Ridder, A. N. J. A., W. Van De Hoef, J. Stam, A. Kuhn, B. De Kruijff, and J. A. Killian. 2002. Importance of hydrophobic matching for spontaneous insertion of a single-spanning membrane protein. Biochemistry. 41:4946-4952.
60. Rinia, H. A., M. M. E. Snel, J. P. J. M. Van Der Eerden, and B. Dekruijff. 2001. Visualizing detergent resistant domains in model membranes with atomic force microscopy. FEBS Lett. 501:92-96.
61. Rodgers, W., B. Crise, and J. K. Rose. 1994. Signals determining protein tyrosine kinase and glycosyl-phosphatidylinositol-anchored proteins targeting to a glycolipid-enriched membrane fraction. Mol. Cell. Biol. 14:5384-5391.
62. Samsonov, A. V., I. Mihalyov, and F. S. Cohen. 2001. Characterization of cholesterol-sphingomyelin domains and their dynamics in bilayer membranes. Biophys. J. 81:1486-1500.
63. Scheiffele, P., M. G. Roth, and K. Simons. 1997. Interaction of influenza virus haemagglutinin with sphingolipid-cholesterol membrane domains via its transmembrane domain. EMBO J. 16:5501-5508.
64. Simon, S. A., S. Advani, and T. J. McIntosh. 1995. Temperature dependence of the repulsive pressure between phosphatidylcholine bilayers. Biophys. J. 69:1473-1483.
65. Simons, K., and E. Ikonen. 1997. Functional rafts in cell membranes. Nature. 387:569-572.
66. Simons, K., and E. Ikonen. 2000. How cells handle cholesterol. Science. 290:1721-1726.
67. Simons, K., and D. Toomre. 2000. Lipid rafts and signal transduction. Nat. Rev. Mol. Cell Biol. 1:31-39.
68. Simons, K., and G. Van Meer. 1988. Lipid sorting in epithelial cells. Biochemistry. 27:6197-6202.
69. Strandberg, E., S. Morein, D. T. Rijkers, R. M. Liskamp, P. C. Van Der Wel, and J. A. Killian. 2002. Lipid dependence of membrane anchoring properties and snorkeling behavior of aromatic and charged residues in transmembrane peptides. Biochemistry. 41:7190-7198.
70. Swift, A. M., and C. E. Machamer. 1991. A Golgi retention signal in a membrane-spanning domain of coronavirus E1 protein. J. Cell Biol. 115:19-30.
71. van Duyl, B. Y., D. T. Rijkers, B. De Kruijff, and J. A. Killian. 2002. Influence of hydrophobic mismatch and palmitoylation on the association of transmembrane alpha-helical peptides with detergent-resistant membranes. FEBS Lett. 523:79-84.
72. Webb, R. J., J. M. East, R. P. Sarma, and A. G. Lee. 1998. Hydrophobic mismatch and the incorporation of peptides into lipid bilayers: a possible mechanism for retention in the Golgi. Biochemistry. 37:673-679.
73. Zacharias, D. A., J. D. Violin, A. C. Newton, and R. Y. Tsien. 2002. Partitioning of lipid-modified monomeric GFPs into membrane microdomains of live cells. Science. 296:913-916.