Cholesterol depletion induces solid-like regions in the plasma membrane

Biophysical Journal

Volumn 90, Issue 3, 2006, Pages 927-938

  Nishimura, Stefanie Y ^a   Vrljic, Marija ^a   Klein, Lawrence O ^a   McConnell, Harden M ^a   Moerner, W E ^a  

^a STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLESTEROL; GLYCOSYLPHOSPHATIDYLINOSITOL; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; PHOSPHOETHANOLAMINE;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; CYTOSKELETON; DIFFUSION COEFFICIENT; FEMALE; IMAGING; MOLECULAR INTERACTION; MOLECULAR PROBE; NONHUMAN; SOLID STATE; TEMPERATURE DEPENDENCE;

ANIMALIA;

EID: 33646205852     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.105.070524     Document Type: Article

References (70)

1. Subramanian, S., and H. M. McConnell. 1987. Critical mixing in monolayer mixtures of phospholipid and cholesterol. J. Phys. Chem. 91:1715-1718.
2. 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.
3. Dietrich, C., Z. N. Volovyk, M. Levi, N. L. Thompson, and K. Jacobson. 2001. Partitioning of Thy-1, GM1, and cross-linked phospholipid analogs into lipid rafts reconstituted in supported model membrane monolayers. Proc. Natl. Acad. Sci. USA. 98:10642-10647.
4. 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.
5. Veatch, S. L., and S. L. Keller. 2002. Organization in lipid membranes containing cholesterol. Phys. Rev. Lett. 89:2681011-2681014.
6. Veatch, S. L., and S. L. Keller. 2003. Separation of liquid phases in giant vesicles of ternary mixtures of phospholipids and cholesterol. Biophys. J. 85:3074-3083.
7. Bagatolli, L. A., and E. Gratton. 2000. Two photon fluorescence microscopy of coexisting lipid domains in giant unilamellar vesicles of binary phospholipid mixtures. Biophys. J. 78:290-305.
8. Korlach, J., P. Schwille, W. W. Webb, and G. W. Feigenson. 1999. Characterization of lipid bilayer phases by confocal microscopy and fluorescence correlation spectroscopy. Proc. Natl. Acad. Sci. USA. 96:8461-8466.
9. Feigenson, G. W., and J. T. Buboltz. 2001. Ternary phase diagram of dipalmitoyl-PC/dilauroyl-PC/cholesterol: nanoscopic domain formation driven by cholesterol. Biophys. J. 80:2775-2788.
10. Vist, M. R., and J. H. Davis. 1990. Phase equilibria of cholesterol/dipalmitoylphosphatidylcholine mixtures: 2H nuclear magnetic resonance and differential scanning calorimetry. Biochemistry. 29:451-464.
11. Veatch, S. L., I. V. Polozov, K. Gawrisch, and S. L. Keller. 2004. Liquid domains in vesicles investigated by NMR and fluorescence microscopy. Biophys. J. 86:2910-2922.
12. Radhakrishnan, A., and H. M. McConnell. 1999. Cholesterol-phospholipid complexes in membranes. J. Am. Chem. Soc. 121:486-487.
13. Radhakrishnan, A., and H. M. McConnell. 1999. Condensed complexes of cholesterol and phospholipids. Biophys. J. 77:1507-1517.
14. McConnell, H. 2005. Complexes in ternary cholesterol-phospholipid mixtures. Biophys. J. 88:L23-L25.
15. McConnell, H. M., and A. Radhakrishnan. 2003. Condensed complexes of cholesterol and phospholipids. Biochim. Biophys. Acta. 1610:159-173.
16. McConnell, H. M., and M. Vrljic. 2003. Liquid-liquid immiscibility in membranes. Annu. Rev. Biophys. Biomol. Struct. 32:469-492.
17. Keller, S. L., W. H. Pitcher III, W. H. Huestis, and H. M. McConnell. 1998. Red blood cell lipids form immiscible liquids. Phys. Rev. Lett. 81:5019-5022.
18. Simons, K., and E. Ikonen. 1997. Functional rafts in cell membranes. Nature. 387:569-572.
19. Brown, D. A., and J. K. Rose. 1992. Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell. 68:533-544.
20. Schroeder, R., E. London, and D. Brown. 1994. Interactions between saturated acyl chains confer detergent resistance on lipids and glycosylphosphatidylinositol (GPI)-anchored proteins: GPI-anchored proteins in liposomes and cells show similar behavior. Proc. Natl. Acad. Sci. USA. 91:12130-12134.
21. Brown, D. A., and E. London. 2000. Structure and function of sphingolipid- and cholesterol-rich membrane rafts. J. Biol. Chem. 275:17221-17224.
22. Heerklotz, H., H. Szadkowska, T. Anderson, and J. Seelig. 2003. The sensitivity of lipid domains to small perturbations demonstrated by the effect of triton. J. Mol. Biol. 329:793-799.
23. Harder, T., P. Scheiffele, P. Verkade, and K. Simons. 1998. Lipid domain structure of the plasma membrane revealed by patching of membrane components. J. Cell Biol. 141:929-942.
24. Mayor, S., K. G. Rothberg, and F. R. Maxfield. 1994. Sequestration of GPI-anchored proteins in caveolae triggered by cross-linking. Science. 264:1948-1951.
25. Vrljic, M., S. Y. Nishimura, S. Brasselet, W. E. Moerner, and H. M. McConnell. 2002. Translational diffusion of individual class II MHC membrane proteins in cells. Biophys. J. 83:2681-2692.
26. Vrljic, M., S. Y. Nishimura, W. E. Moerner, and H. M. McConnell. 2005. Cholesterol depletion suppresses the translational diffusion of class II major histocompatibility complex proteins in the plasma membrane. Biophys. J. 88:334-347.
27. Anderson, R. G. W., and K. Jacobson. 2002. A role for lipid shells in targeting proteins to caveolae, rafts and other lipid domains. Science. 296:1821-1825.
28. Hao, M., S. Mukherjee, and F. R. Maxfield. 2001. Cholesterol depletion induces large scale domain segregation in living cell membranes. Proc. Natl. Acad. Sci. USA. 98:13072-13077.
29. Lommerse, P. H. M., H. P. Spaink, and T. Schmidt. 2004. In vivo plasma membrane organization: results of biophysical approaches. Biochim. Biophys. Acta. 1664:119-131.
30. Edidin, M. 2003. The state of lipid rafts: from model membranes to cells. Annu. Rev. Biophys. Biomol. Struct. 32:257-283.
31. Xavier, R., T. Brennan, Q. Li, C. McCormack, and B. Seed. 1998. Membrane compartmentation is required for efficient T cell activation. Immunity. 8:723-732.
32. Field, K., D. Holowka, and B. Baird. 1997. Compartmentalized activation of the high affinity immunoglobulin E receptor within membrane domains. J. Biol. Chem. 272:4276-4280.
33. Sheets, E. D., D. Holowka, and B. Baird. 1999. Critical role for cholesterol in Lyn-mediated tyrosine phosphorylation of FcεRI and their association with detergent-resistant membranes. J. Cell Biol. 145:877-887.
34. Vidalain, P. O., O. Azocar, C. Servet-Delprat, C. Rabourdin-Combe, D. Gerlier, and S. Manie. 2000. CD40 signaling in human dendritic cells is initiated within membrane rafts. EMBO J. 19:3304-3313.
35. Kwik, J., S. Boyle, D. Fooksman, L. Margolis, M. P. Sheetz, and M. Edidin. 2003. Membrane cholesterol, lateral mobility, and the phosphatidylinositol 4,5-bisphosphate-dependent organization of cell actin. Proc. Natl. Acad. Sci. USA. 100:13964-13969.
36. Shvartsman, D. E., M. Kotler, R. D. Tall, M. G. Roth, and Y. I. Henis. 2003. Differently anchored influenza hemagglutinin mutants display distinct interaction dynamics with mutual rafts. J. Cell Biol. 163:879-888.
37. Sooksawate, T., and M. A. Simmonds. 2001. Effects of membrane cholesterol on the sensitivity of the GABA(A) receptor to GABA in acutely dissociated rat hippocampal neurones. Neuropharmacology. 40:178-184.
38. Kenworthy, A. K., B. J. Nichols, C. L. Remmert, G. M. Hendrix, M. Kumar, J. Zimmerberg, and J. Lippincott-Schwartz. 2004. Dynamics of putative raft-associated proteins at the cell surface. J. Cell Biol. 165:735-746.
39. Bacia, K., D. Scherfeld, N. Kahya, and P. Schwille. 2004. Fluorescence correlation spectroscopy relates rafts in model and native membranes. Biophys. J. 87:1034-1043.
40. Wettstein, D. A., J. J. Boniface, P. A. Reay, H. Schild, and M. M. Davis. 1991. Expression of a class II major histocompatibility complex (MHC) heterodimer in a lipid-linked form with enhanced peptide/soluble MHC complex formation at low pH. J. Exp. Med. 174:219-228.
41. Murase, K., T. Fujiwara, Y. Umemura, K. Suzuki, R. Iino, H. Yamashita, M. Saito, H. Murakoshi, K. Ritchie, and A. Kusumi. 2004. Ultrafine membrane compartments for molecular diffusion as revealed by single molecule techniques. Biophys. J. 86:4075-4093.
42. Rotsch, C., and M. Radmacher. 2000. Drug-induced changes of cytoskeletal structure and mechanics in fibroblasts: an atomic microscopy study. Biophys. J. 78:520-535.
43. Huby, R. D. J., A. Weiss, and S. C. Ley. 1998. Nocodazole inhibits signal transduction by the T cell antigen receptor. J. Biol. Chem. 273:12024-12031.
44. Wakatsuki, T., B. Schwab, N. C. Thompson, and E. L. Elson. 2000. Effects of cytochalasin D and latranculin B on mechanical properties of cells. J. Cell Sci. 114:1025-1036.
45. Saxton, M. J. 1994. Anomalous diffusion due to obstacles: a Monte Carlo study. Biophys. J. 66:394-401.
46. Smith, P. R., I. E. G. Morrison, K. M. Wilson, N. Fernandez, and R. J. Cherry. 1999. Anomalous diffusion of major histocompatibility complex class I molecules on HeLa cells determined by single particle tracking. Biophys. J. 76:3331-3344.
47. Feder, T. J., I. Brust-Mascher, J. P. Slattery, B. Baird, and W. W. Webb. 1996. Constrained diffusion of immobile fraction on cell surfaces: a new interpretation. Biophys. J. 70:2767-2773.
48. Qian, H., M. P. Sheetz, and E. L. Elson. 1991. Single particle tracking. Analysis of diffusion and flow in two-dimensional systems. Biophys. J. 60:910-921.
49. Schütz, G. J., H. Schindler, and T. Schmidt. 1997. Single-molecule microscopy on model membranes reveals anomalous diffusion. Biophys. J. 73:1073-1080.
50. Wolf, D. E. 1985. Determination of the sidedness of carbocyanine dye labeling of membranes. Biochemistry. 24:582-586.
51. Schwiegelshohn, B., J. F. Presley, M. Gorecki, T. Vogel, Y. A. Carpentier, F. R. Maxfield, and R. J. Deckelbaum. 1995. Effects of apoprotein E on intracellular metabolism of model triglyceride-rich particles are distinct from effects on cell particle uptake. J. Biol. Chem. 270:1761-1769.
52. Murakoshi, H., R. Iino, T. Kobayashi, T. Fujiwara, C. Ohshima, A. Yoshimura, and A. Kusumi. 2004. Single-molecule imaging analysis of Ras activation in living cells. Proc. Natl. Acad. Sci. USA. 101:7317-7322.
53. Tamm, L. K., and H. M. McConnell. 1985. Supported phospholipid bilayers. Biophys. J. 47:105-113.
54. Vaz, W. L., Z. I. Derzko, and K. A. Jacobson. 1982. Photobleaching measurements of the lateral diffusion of lipids and proteins in artificial phospholipid bilayer membranes. In Membrane Reconstitution. G. Poste and G. L. Nicolson, editors. Elsevier Biomedical Press, Amsterdam. 83-136.
55. Smith, B. A., and H. M. McConnell. 1978. Determination of molecular motion in membranes using periodic pattern photobleaching. Proc. Natl. Acad. Sci. USA. 75:2759-2763.
56. Saxton, M. J. 1993. Lateral diffusion in an archipelago. Single-particle diffusion. Biophys. J. 64:1766-1780.
57. Devaux, P. F. 1992. Protein involvement in transmembrane lipid asymmetry. Annu. Rev. Biophys. Biomol. Struct. 21:417-439.
58. Myher, J. J., A. Kuksis, and S. Pind. 1989. Molecular species of glycerophospholipids and sphingomyelins of human erythrocytes improved methods of analysis. Lipids. 24:396-407.
59. Hullin, F., M.-J. Bossant, and N. Salem Jr. 1991. Aminophospholipid molecular species asymmetry in the human erythrocyte plasma membrane. Biochim. Biophys. Acta. 1061:15-25.
60. Morrot, G., S. Cribier, P. F. Devaux, D. Geldwerth, J. Davoust, J. F. Bureau, P. Fellmann, P. Herve, and B. Frilley. 1986. Asymmetric lateral mobility of phospholipids in the human erythrocyte membrane. Proc. Natl. Acad. Sci. USA. 83:6863-6867.
61. Chahine, J., S. Cribier, and P. Devaux. 1993. Phospholipid transmembrane domains and lateral diffusion in fibroblasts. Proc. Natl. Acad. Sci. USA. 90:447-451.
62. Julien, M., J.-F. Tournier, and J.-F. Tocanne. 1993. Differences in the transbilayer and lateral motions of fluorescent analogs of phosphatidylcholine and phosphatidylethanolamine in the apical plasma membrane of bovine aortic endothelial cells. Exp. Cell Res. 208:387-397.
63. Steck, T. L., J. Ye, and Y. Lange. 2002. Probing red cell membrane cholesterol movement with cyclodextrin. Biophys. J. 83:2118-2125.
64. Schroeder, F., G. Nemecz, W. Gibson Wood, C. Joiner, G. Morrot, M. Ayraut-Jarrier, and P. F. Devaux. 1991. Transmembrane distribution of sterol in the human erythrocyte. Biochim. Biophys. Acta. 1066:183-192.
65. Muller, P., and A. Herrmann. 2002. Rapid transbilayer movement of spin-labeled steroids in human erythrocytes and in liposomes. Biophys. J. 82:1418-1428.
66. Derzko, Z. I., and K. A. Jacobson. 1980. Comparative lateral diffusion of fluorescent lipid analogues in phospholipid multibilayers. Biochemistry. 19:6050-6057.
67. Tsukagoshi, N., and C. F. Fox. 1973. Transport system assembly and the mobility of membrane lipids in Escherichia coli. Biochemistry. 12:2822-2829.
68. Linden, C. D., K. L. Wright, H. M. McConnell, and C. F. Fox. 1973. Lateral phase separations in membrane lipids and the mechanism of sugar transport in Escherichia coli. Proc. Natl. Acad. Sci. USA. 70:2271-2275.
69. Saffman, P. G., and M. Delbruck. 1975. Brownian motion in biological membranes. Proc. Natl. Acad. Sci. USA. 72:3111-3113.
70. Hughes, B. D., B. A. Pailthorpe, and L. R. White. 1981. The translational and rotational drag on a cylinder moving in a membrane. J. Fluid Mech. 110:349-372.