Protein-Lipid Interactions in the Formation of Raft Microdomains in Biological Membranes

Protein-Lipid Interactions: From Membrane Domains to Cellular Networks

Volumn , Issue , 2006, Pages 305-336

  Kusumi, Akihiro ^a   Suzuki, Kenichi ^a   Kondo, Junko ^a   Morone, Nobuhiro ^b   Umemura, Yasuhiro ^a  

^a KYOTO UNIVERSITY   (Japan)

^b NATIONAL INSTITUTE OF MENTAL HEALTH   (Japan)

Author keywords

Membrane skeleton based compartments; Microdomains; Molecular complexes; Protein lipid interactions in the formation of raft microdomains; Raft domains; Raft hypothesis

Indexed keywords

EID: 33751220398     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1002/3527606769.ch13     Document Type: Chapter

References (96)

1. Anderson, R. G., K. Jacobson. 2002. A role for lipid shells in targeting proteins to caveolae, rafts, and other lipid domains. Science 296, 1821-1825.
2. Anderson, T. G., H.M. McConnell. 2001. Condensed complexes and the calorimetry of cholesterol-phospholipid bilayers. Biophys. J. 81, 2774-2785.
3. Anderson, T. G., H.M. McConnell. 2002. A thermodynamic model for extended complexes of cholesterol and phospholipid. Biophys. J. 83, 2039-2052.
4. Baird, B., E.D. Sheets, D. Holowka. 1999. How does the plasma membrane participate in cellular signaling by receptors for immunoglobulin E? Biophys. Chem. 82, 109-119.
5. Bretscher, M. S., S. Munro. 1993. Cholesterol and the Golgi apparatus. Science 261, 1280-1281.
6. Brown, D. A., E. London. 1998. Functions of lipid rafts in biological membranes. Annu. Rev. Cell Dev. Biol. 14, 111-136.
7. Brugger, B., C. Graham, I. Leibrecht, E. Mombelli, A. Jen, F. Wieland, R. Morris. 2004. The membrane domains occupied by glycosylphosphatidylinositol-anchored prion protein and Thy-1 differ in lipid composition. J. Biol. Chem. 279, 7530- 7536.
8. Cherukuri, A., R.H. Carter, S. Brooks, W. Bornmann, R. Finn, C. S. Dowd, S. K. Pierce. 2004a. B cell signaling is regulated by induced palmitoylation of CD81. J. Biol. Chem. 279, 31973-31982.
9. Cherukuri, A., T. Shoham, H. W. Sohn, S. Levy, S. Brooks, R. Carter, S. K. Pierce. 2004b. The tetraspanin CD81 is necessary for partitioning of coligated CD19/CD21- B cell antigen receptor complexes into signaling- active lipid rafts. J. Immunol. 172, 370-380.
10. Crane, J. M., L. K. Tamm. 2004. Role of cholesterol in the formation and nature of lipid rafts in planar and spherical model membranes. Biophys. J. 86, 2965-2979.
11. de Backer, M., S. McSweeney, H.B. Rasmussen, B.W. Rise, P. Lindley, E. Hough. 2002. The 1.9 Å crystal structure of heatlabile shrimp alkaline phosphatase. J. Mol. Biol. 318, 1265-1274.
12. Dietrich, C., Z.N. Volovyk, M. Levi, N.L. Thompson, K. Jacobson. 2001. Partitioning of Thy-1, GM1, and cross-linked phospho lipid analogs into lipid rafts reconstituted in supported model membrane monolayers. Proc. Natl Acad. Sci. USA 98, 10642-10647.
13. Dietrich, C., B. Yang, T. Fujiwara, A. Kusumi, K. Jacobson. 2002. Relationship of lipid rafts to transient confinement zones detected by single particle tracking. Biophys. J. 82, 274-284.
14. Dykstra, M., A. Cherukuri, H.W. Sohn, S. J. Tzeng, S. K. Pierce. 2003. Location is everything: lipid rafts and immune cell signaling. Annu. Rev. Immunol. 21, 457- 481.
15. East, J. M., D. Melville, A. G. Lee. 1985. Exchange rates and numbers of annular lipids for the calcium and magnesium ion dependent adenosine triphosphatase. Biochemistry 24, 2615-2623.
16. Feder, T. J., I. Brust-Mascher, J.P. Slattery, B. Baird, W.W. Webb. 1996. Constrained diffusion or immobile fraction on cell surfaces: a new interpretation. Biophys. J. 70, 2767-2773.
17. Field, K. A., D. Holowka, B. Baird. 1995. Fc epsilon RI-mediated recruitment of p53/56lyn to detergent-resistant membrane domains accompanies cellular signaling. Proc. Natl Acad. Sci. USA 92, 9201-9205.
18. Field, K. A., D. Holowka, B. Baird. 1997. Compartmentalized activation of the high affinity immunoglobulin E receptor within membrane domains. J. Biol. Chem. 272, 4276-4280.
19. Fra, A. M., E. Williamson, K. Simons, R. G. Parton. 1994. Detergent-insoluble glycolipid microdomains in lymphocytes in the absence of caveolae. J. Biol. Chem. 269, 30745-30748.
20. Gaidarov, I., F. Santini, R. A. Warren, J.H. Keen. 1999. Spatial control of coated-pit dynamics in living cells. Nat. Cell Biol. 1, 1-7.
21. Gil, T., J.H. Ipsen, O.G. Mouritsen, M.C. Sabra, M.M. Sperotto, M.J. Zuckermann. 1998. Theoretical analysis of protein organization in lipid membranes. Biochim. Biophys. Acta 1376, 245-266.
22. Glebov, O. O., B. J. Nichols. 2004. Lipid raft proteins have a random distribution during localized activation of the T-cell receptor. Nat. Cell Biol. 6, 238-243.
23. Hancock, J. F. 2003. Ras proteins: different signals from different locations. Nat. Rev. Mol. Cell Biol. 4, 373-384.
24. Harder, T., P. Scheiffele, P. Verkade, K. Simons. 1998. Lipid domain structure of the plasma membrane revealed by patching of membrane components. J. Cell Biol. 141, 929-942.
25. Heerklotz, H. 2002. Triton promotes domain formation in lipid raft mixtures. Biophys. J. 83, 2693-2701.
26. Heerklotz, H., H. Szadkowska, T. Anderson, J. Seelig. 2003. The sensitivity of lipid domains to small perturbations demonstrated by the effect of Triton. J. Mol. Biol. 329, 793-799.
27. Horvath, L. I., P. J. Brophy, D. Marsh. 1988. Exchange rates at the lipid-protein interface of myelin proteolipid protein studied by spin-label electron spin resonance. Biochemistry 27, 46-52.
28. Iino, R., I. Koyama, A. Kusumi. 2001. Single molecule imaging of green fluorescent proteins in living cells: E-cadherin forms oligomers on the free cell surface. Biophys. J. 80, 2667-2677.
29. Janes, P.W., S.C. Ley, A. I. Magee. 1999. Aggregation of lipid rafts accompanies signaling via the T cell antigen receptor. J. Cell Biol. 147, 447-461.
30. Jordan, B. A., L. A. Devi. 1999. G-proteincoupled receptor heterodimerization modulates receptor function. Nature 399, 697- 700.
31. Kawasaki, K., J. J. Yin, W. K. Subczynski, J. S. Hyde, A. Kusumi. 2001. Pulse EPR detection of lipid exchange between protein- rich raft and bulk domains in the membrane: methodology development and its application to studies of influenza viral membrane. Biophys. J. 80, 738-748.
32. Kenworthy, A. K., M. Edidin. 1998. Distribution of a 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. Kenworthy, A. K., N. Petranova, M. Edidin. 2000. High-resolution FRET microscopy of cholera toxin B-subunit and GPI-anchored proteins in cell plasma membranes. Mol. Biol. Cell 11, 1645-1655.
34. Kenworthy, A. K., B. J. Nichols, C. L. Remmert G.M. Hendrix, M. Kumar, J. Zimmerberg, J. Lippincott-Schwartz. 2004. Dynamics of putative raft-associated proteins at the cell surface. J. Cell Biol. 165, 735-746.
35. Koyama-Honda, I., K. Ritchie, T. Fujiwara, R. Iino, H. Murakoshi, R. S. Kasai, A. Kusumi. 2005. Fluorescence imaging for monitoring the colocalization of two single molecules in living cells. Biophys. J. 88, 2126-2136.
36. Kusumi, A., J. S. Hyde. 1982. Spin-label saturation- transfer electron spin resonance detection of transient association of rhodopsin in reconstituted membranes. Biochemistry 21, 5978-5983.
37. Kusumi, A., I. Koyama-Honda, K. Suzuki. 2004. Molecular dynamics and interactions for creation of stimulation-induced stabilized rafts from small unstable steady-state rafts. Traffic 5, 213-230.
38. Lai, E. C. 2003. Lipid rafts make for slippery platforms. J. Cell Biol. 162, 365-370.
39. Le Du, M.H., T. Stigbrand, M.J. Taussig, A. Menez, E. A. Stura. 2001. Crystal structure of alkaline phosphatase from human placenta at 18 Å resolution. Implication for a substrate specificity. J. Biol. Chem. 276, 9158-9165.
40. Lehto, M.T., F. J. Sharom. 2002. Proximity of the protein moiety of a GPI-anchored protein to the membrane surface: a FRET study. Biochemistry 41, 8368-8376.
41. London, E., 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.
42. Lukacik, P., P. Roversi, J. White, D. Esser, G. P. Smith, J. Billington, P. A. Williams, P.M. Rudd, M.R. Wormald, D.J. Harvey, M.D. Crispin, C.M. Radcliffe, R. A. Dwek, D.J. Evans, B. P. Morgan, R.A. Smith, S.M. Lea. 2004. Complement regulation at the molecular level: the structure of decayaccelerating factor. Proc. Natl Acad. Sci. USA 101, 1279-1284.
43. Manes, S., R. Ana Lacalle, C. Gomez-Mouton, A. C. Martinez. 2003. From rafts to crafts: membrane asymmetry in moving cells. Trends. Immunol. 24, 320-326.
44. Marwali, M.R., J. Rey-Ladino, L. Dreolini, D. Shaw, F. Takei. 2003. Membrane cholesterol regulates LFA-1 function and lipid raft heterogeneity. Blood 102, 215-222.
45. Maxfield, F. R. 2002. Plasma membrane microdomains. Curr. Opin. Cell Biol. 14, 483-487.
46. Mayor, S., M. Rao. 2004. Rafts: scale-dependent, active lipid organization at the cell surface. Traffic 5, 231-240.
47. Mayor, S., K. G. Rothberg, F. R. Maxfield. 1994. Sequestration of GPI-anchored proteins in caveolae triggered by cross-linking. Science 264, 1948-1951.
48. McConnell, H.M., A. Radhakrishnan. 2003. Condensed complexes of cholesterol and phospholipids. Biochim. Biophys. Acta 1610, 159-173.
49. McConnell, H.M., M. Vrljic. 2003. Liquid- liquid immiscibility in membranes. Annu. Rev. Biophys. Biomol. Struct. 32, 469-492.
50. Mitchell, J. S., O. Kanca, B.W. McIntyre. 2002. Lipid microdomain clustering induces a redistribution of antigen recognition and adhesion molecules on human T lymphocytes. J. Immunol. 168, 2737-2744.
51. Mukherjee, S., F. R. Maxfield. 2004. Membrane domains. Annu. Rev. Cell Dev. Biol. 20, 839-866.
52. Nagle, J. F. 1992. Long tail kinetics in biophysics? Biophys. J. 63, 366-370.
53. Nichols, B. J. 2003. GM1-containing lipid rafts are depleted within clathrin-coated pits. Curr. Biol. 13, 686-690.
54. Okonogi, T. M., A. Radhakrishnan, H.M. McConnell. 2002. Two fatty acids can replace one phospholipid in condensed complexes with cholesterol. Biochim. Biophys. Acta 1564, 1-4.
55. Paladino, S., D. Sarnataro, R. Pillich, S. Tivodar, L. Nitsch, C. Zurzolo. 2004. Protein oligomerization modulates raft partitioning and apical sorting of GPI-anchored proteins. J. Cell Biol. 167, 699-709.
56. Parmryd, I., J. Adler, R. Patel, A. I. Magee. 2003. Imaging metabolism of phosphatidylinositol 4,5-bisphosphate in T-cell GM1- enriched domains containing Ras proteins. Exp. Cell Res. 285, 27-38.
57. Parton, R. G., J. F. Hancock. 2001. Caveolin and Ras function. Methods Enzymol. 333, 172-183.
58. Parton, R. G., J. F. Hancock. 2004. Lipid rafts and plasma membrane microorganization: insights from Ras. Trends Cell Biol. 14, 141-147.
59. Pasdar, M., W. J. Nelson. 1988a. Kinetics of desmosome assembly in Madin-Darby canine kidney epithelial cells: temporal and spatial regulation of desmoplakin organization and stabilization upon cell-cell contact. I. Biochemical analysis. J. Cell Biol. 106, 677-685.
60. Pasdar, M., W. J. Nelson. 1988b. Kinetics of desmosome assembly in Madin-Darby canine kidney epithelial cells: temporal and spatial regulation of desmoplakin organization and stabilization upon cell-cell contact. II. Morphological analysis. J. Cell Biol. 106, 687-695.
61. Pasdar, M., W. J. Nelson. 1989. Regulation of desmosome assembly in epithelial cells: kinetics of synthesis, transport, and stabilization of desmoglein I, a major protein of the membrane core domain. J. Cell Biol. 109, 163-177.
62. Pasenkiewicz-Gierula, M., W. K. Subczynski, A. Kusumi. 1991. Influence of phospholipid unsaturation on the cholesterol distribution in membranes. Biochimie 73, 1311- 1316.
63. Peters, R., R. J. Cherry. 1982. Lateral and rotational diffusion of bacteriorhodopsin in lipid bilayers: experimental test of the Saffman- Delbruck equations. Proc. Natl Acad. Sci. USA 79, 4317-4321.
64. Pierce, S. K. 2002. Lipid rafts and B-cell activation. Nat. Rev. Immunol. 2, 96-105.
65. Pierini, L. M., F. R. Maxfield. 2001. Flotillas of lipid rafts fore and aft. Proc. Natl Acad. Sci. USA 98, 9471-9473.
66. Pierini, L. M., R. J. Eddy, M. Fuortes, S. Seveau, C. Casulo, F. R. Maxfield. 2003. Membrane lipid organization is critical for human neutrophil polarization. J. Biol. Chem. 278, 10831-10841.
67. Pralle, A., P. Keller, E. L. Florin, K. Simons, J. K. Horber. 2000. Sphingolipid-cholesterol rafts diffuse as small entities in the plasma membrane of mammalian cells. J. Cell Biol. 148, 997-1008.
68. Pribluda, V. S., C. Pribluda, H. Metzger. 1994. Transphosphorylation as the mechanism by which the high-affinity receptor for IgE is phosphorylated upon aggregation. Proc. Natl Acad. Sci. USA 91, 11246- 11250.
69. Prior, I. A., C. Muncke, R. G. Parton, J. F. Hancock. 2003. Direct visualization of Ras proteins in spatially distinct cell surface microdomains. J. Cell Biol. 160, 165-170.
70. Radhakrishnan, A., T.G. Anderson, H.M. McConnell. 2000. Condensed complexes, rafts, and the chemical activity of cholesterol in membranes. Proc. Natl Acad. Sci. USA 97, 12422-12427.
71. Radhakrishnan, A., X.M. Li, R. E. Brown, H. M. McConnell. 2001. Stoichiometry of cholesterol-sphingomyelin condensed complexes in monolayers. Biochim. Biophys. Acta 1511, 1-6.
72. Rudd, P. M., B. P. Morgan, M.R. Wormald, D.J. Harvey, C.W. van den Berg, S. J. Davis, M.A. Ferguson, R. A. Dwek. 1997. The glycosylation of the complement regulatory protein, human erythrocyte CD59. J. Biol. Chem. 272, 7229-7244.
73. Saffman, P. G., M. Delbrück. 1975. Brownian motion in biological membranes. Proc. Natl Acad. Sci. USA 72, 3111-3113.
74. Schroeder, R. J., S. N. Ahmed, Y. Zhu, E. London, D.A. Brown. 1998. Cholesterol and sphingolipid enhance the Triton X-100 insolubility of glycosylphosphatidylinositolanchored proteins by promoting the formation of detergent-insoluble ordered membrane domains. J. Biol. Chem. 273, 1150-1157.
75. Sharma, P., R. Varma, R. C. Sarasij, Ira, K. Gousset, G. Krishnamoorthy, M. Rao, S. Mayor. 2004. Nanoscale organization of multiple GPI-anchored proteins in living cell membranes. Cell 116, 577-589.
76. Sheets, E. D., G.M. Lee, R. Simson, K. Jacobson. 1997. Transient confinement of a glycosylphosphatidylinositol-anchored protein in the plasma membrane. Biochemistry 36, 12449-12458.
77. Sheets, E. D., D. Holowka, B. Baird. 1999. Critical role for cholesterol in Lyn-mediated tyrosine phosphorylation of FcepsilonRI and their association with detergent-resistant membranes. J. Cell Biol. 145, 877- 887.
78. Shvartsman, D.E., M. Kotler, R.D. Tall, M.G. Roth, Y. I. Henis. 2003. Differently anchored influenza hemagglutinin mutants display distinct interaction dynamics with mutual rafts. J. Cell Biol. 163, 879-888.
79. Simons, K., E. Ikonen. 1997. Functional rafts in cell membranes. Nature 387, 569- 572.
80. Simons, K., D. Toomre. 2000. Lipid rafts and signal transduction. Nat. Rev. Mol. Cell Biol. 1, 31-39.
81. Simons, K., G. van Meer. 1988. Lipid sorting in epithelial cells. Biochemistry 27, 6197- 6202.
82. Simons, K., W. L. Vaz. 2004. Model systems, lipid rafts, and cell membranes. Annu. Rev. Biophys. Biomol. Struct 33, 269-295.
83. Singer, S. J., G. L. Nicolson. 1972. The fluid mosaic model of the structure of cell membranes. Science 175, 720-731.
84. Stoddart, A., M.L. Dykstra, B. K. Brown, W. Song, S. K. Pierce, F.M. Brodsky. 2002. Lipid rafts unite signaling cascades with clathrin to regulate BCR internalization. Immunity 17, 451-462.
85. Subczynski, W. K., A. Kusumi. 2003. Dynamics of raft molecules in the cell and artificial membranes: approaches by pulse EPR spin labeling and single molecule optical microscopy. Biochim. Biophys. Acta 1610, 231-243.
86. Subczynski, W. K., W. E. Antholine, J. S. Hyde, A. Kusumi. 1990. Microimmiscibility and three-dimensional dynamic structures of phosphatidylcholine-cholesterol membranes: translational diffusion of a copper complex in the membrane. Biochemistry 29, 7936-7945.
87. Suzuki, K., F. Sanematsu, T. Fujiwara, M. Edidin, A. Kusumi. 2001. Rapid, continual formation/dispersion of raft-like domains in the resting cell membrane. Mol. Biol. Cell 12, 470a.
88. Suzuki, K., F. Sanematsu, T. Fujiwara, M. Edidin, A. Kusumi. 2002. Stimulation-induced formation of temporal but stabilized rafts. Biophys. J. 82, 348a.
89. Suzuki, K., F. Sanematsu, T. Fujiwara, K. Ritchie, M. Edidin, A. Kusumi. 2003. Crosslinking of a GPI-anchored protein creates signaling rafts from smaller, transient, lipid rafts. Biophys. J. 84, 487a.
90. Tavano, R., G. Gri, B. Molon, B. Marinari, C. E. Rudd, L. Tuosto, A. Viola. 2004. CD28 and lipid rafts coordinate recruitment of Lck to the immunological synapse of human T lymphocytes. J. Immunol. 173, 5392-5397.
91. Thomas, J. L., D. Holowka, B. Baird, W.W. Webb. 1994. Large-scale co-aggregation of fluorescent lipid probes with cell surface proteins. J. Cell Biol. 125, 795-802.
92. Varma, R., S. Mayor. 1998. GPI-anchored proteins are organized in submicron domains at the cell surface. Nature 394, 798-801.
93. Vaz, W. L., M. Criado, V.M. Madeira, G. Schoellmann, T.M. Jovin. 1982. Size dependence of the translational diffusion of large integral membrane proteins in liquid- crystalline phase lipid bilayers. A study using fluorescence recovery after photobleaching. Biochemistry 21, 5608-5612.
94. Vrljic, M., S.Y. Nishimura, S. Brasselet, W. E. Moerner, H.M. McConnell. 2002. Translational diffusion of individual class II MHC membrane proteins in cells. Biophys. J. 83, 2681-2692.
95. Wu, M., D. Holowka, H.G. Craighead, B. Baird. 2004. Visualization of plasma membrane compartmentalization with patterned lipid bilayers. Proc. Natl Acad. Sci. USA 101, 13798-13803.
96. Young, R. M., D. Holowka, B. Baird. 2003. A lipid raft environment enhances Lyn kinase activity by protecting the active site tyrosine from dephosphorylation. J. Biol. Chem. 278, 20746-20752.