Abstract
Lipid rafts are membrane microdomains that are enriched in cholesterol and glycosphingolipids. They have been implicated in processes as diverse as signal transduction, endocytosis and cholesterol trafficking. Recent evidence suggests that this diversity of function is accompanied by a diversity in the composition of lipid rafts. The rafts in cells appear to be heterogeneous both in terms of their protein and their lipid content, and can be localized to different regions of the cell. This review summarizes the data supporting the concept of heterogeneity among lipid rafts and outlines the evidence for cross-talk between raft components. Based on differences in the ways in which proteins interact with rafts, the Induced-Fit Model of Raft Heterogeneity is proposed to explain the establishment and maintenance of heterogeneity within raft populations.
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- Abrami L., Fivaz M., Kobayashi T., Kinoshita T., Parton R. G., van der Goot F. G. Cross-talk between caveolae and glycosylphosphatidylinositol-rich domains. J Biol Chem. 2001 Jun 13;276(33):30729–30736. doi: 10.1074/jbc.M102039200. [DOI] [PubMed] [Google Scholar]
- Anderson Richard G. W., Jacobson Ken. A role for lipid shells in targeting proteins to caveolae, rafts, and other lipid domains. Science. 2002 Jun 7;296(5574):1821–1825. doi: 10.1126/science.1068886. [DOI] [PubMed] [Google Scholar]
- Arni S., Keilbaugh S. A., Ostermeyer A. G., Brown D. A. Association of GAP-43 with detergent-resistant membranes requires two palmitoylated cysteine residues. J Biol Chem. 1998 Oct 23;273(43):28478–28485. doi: 10.1074/jbc.273.43.28478. [DOI] [PubMed] [Google Scholar]
- Bagnat Michel, Simons Kai. Cell surface polarization during yeast mating. Proc Natl Acad Sci U S A. 2002 Oct 8;99(22):14183–14188. doi: 10.1073/pnas.172517799. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bodin S., Giuriato S., Ragab J., Humbel B. M., Viala C., Vieu C., Chap H., Payrastre B. Production of phosphatidylinositol 3,4,5-trisphosphate and phosphatidic acid in platelet rafts: evidence for a critical role of cholesterol-enriched domains in human platelet activation. Biochemistry. 2001 Dec 18;40(50):15290–15299. doi: 10.1021/bi0109313. [DOI] [PubMed] [Google Scholar]
- Brown D. A., London E. Structure and function of sphingolipid- and cholesterol-rich membrane rafts. J Biol Chem. 2000 Jun 9;275(23):17221–17224. doi: 10.1074/jbc.R000005200. [DOI] [PubMed] [Google Scholar]
- Brown D. A., London E. Structure and origin of ordered lipid domains in biological membranes. J Membr Biol. 1998 Jul 15;164(2):103–114. doi: 10.1007/s002329900397. [DOI] [PubMed] [Google Scholar]
- Brown D. A., Rose J. K. Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell. 1992 Feb 7;68(3):533–544. doi: 10.1016/0092-8674(92)90189-j. [DOI] [PubMed] [Google Scholar]
- Chatterjee S., Mayor S. The GPI-anchor and protein sorting. Cell Mol Life Sci. 2001 Dec;58(14):1969–1987. doi: 10.1007/PL00000831. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cinek T., Horejsí V. The nature of large noncovalent complexes containing glycosyl-phosphatidylinositol-anchored membrane glycoproteins and protein tyrosine kinases. J Immunol. 1992 Oct 1;149(7):2262–2270. [PubMed] [Google Scholar]
- Drevot Philippe, Langlet Claire, Guo Xiao-Jun, Bernard Anne-Marie, Colard Odile, Chauvin Jean-Paul, Lasserre Rémi, He Hai-Tao. TCR signal initiation machinery is pre-assembled and activated in a subset of membrane rafts. EMBO J. 2002 Apr 15;21(8):1899–1908. doi: 10.1093/emboj/21.8.1899. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Edidin Michael. The state of lipid rafts: from model membranes to cells. Annu Rev Biophys Biomol Struct. 2003 Jan 16;32:257–283. doi: 10.1146/annurev.biophys.32.110601.142439. [DOI] [PubMed] [Google Scholar]
- Foster Leonard J., De Hoog Carmen L., Mann Matthias. Unbiased quantitative proteomics of lipid rafts reveals high specificity for signaling factors. Proc Natl Acad Sci U S A. 2003 Apr 30;100(10):5813–5818. doi: 10.1073/pnas.0631608100. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fra A. M., Williamson E., Simons K., Parton R. G. De novo formation of caveolae in lymphocytes by expression of VIP21-caveolin. Proc Natl Acad Sci U S A. 1995 Sep 12;92(19):8655–8659. doi: 10.1073/pnas.92.19.8655. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fridriksson E. K., Shipkova P. A., Sheets E. D., Holowka D., Baird B., McLafferty F. W. Quantitative analysis of phospholipids in functionally important membrane domains from RBL-2H3 mast cells using tandem high-resolution mass spectrometry. Biochemistry. 1999 Jun 22;38(25):8056–8063. doi: 10.1021/bi9828324. [DOI] [PubMed] [Google Scholar]
- Friedrichson T., Kurzchalia T. V. Microdomains of GPI-anchored proteins in living cells revealed by crosslinking. Nature. 1998 Aug 20;394(6695):802–805. doi: 10.1038/29570. [DOI] [PubMed] [Google Scholar]
- Furuchi T., Anderson R. G. Cholesterol depletion of caveolae causes hyperactivation of extracellular signal-related kinase (ERK). J Biol Chem. 1998 Aug 14;273(33):21099–21104. doi: 10.1074/jbc.273.33.21099. [DOI] [PubMed] [Google Scholar]
- García-Cardeña G., Oh P., Liu J., Schnitzer J. E., Sessa W. C. Targeting of nitric oxide synthase to endothelial cell caveolae via palmitoylation: implications for nitric oxide signaling. Proc Natl Acad Sci U S A. 1996 Jun 25;93(13):6448–6453. doi: 10.1073/pnas.93.13.6448. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gómez-Móuton C., Abad J. L., Mira E., Lacalle R. A., Gallardo E., Jiménez-Baranda S., Illa I., Bernad A., Mañes S., Martínez-A C. Segregation of leading-edge and uropod components into specific lipid rafts during T cell polarization. Proc Natl Acad Sci U S A. 2001 Aug 7;98(17):9642–9647. doi: 10.1073/pnas.171160298. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hancock J. F., Magee A. I., Childs J. E., Marshall C. J. All ras proteins are polyisoprenylated but only some are palmitoylated. Cell. 1989 Jun 30;57(7):1167–1177. doi: 10.1016/0092-8674(89)90054-8. [DOI] [PubMed] [Google Scholar]
- Hansen G. H., Immerdal L., Thorsen E., Niels-Christiansen L. L., Nystrøm B. T., Demant E. J., Danielsen E. M. Lipid rafts exist as stable cholesterol-independent microdomains in the brush border membrane of enterocytes. J Biol Chem. 2001 Jun 1;276(34):32338–32344. doi: 10.1074/jbc.M102667200. [DOI] [PubMed] [Google Scholar]
- Harder T., Scheiffele P., Verkade P., Simons K. Lipid domain structure of the plasma membrane revealed by patching of membrane components. J Cell Biol. 1998 May 18;141(4):929–942. doi: 10.1083/jcb.141.4.929. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hope H. R., Pike L. J. Phosphoinositides and phosphoinositide-utilizing enzymes in detergent-insoluble lipid domains. Mol Biol Cell. 1996 Jun;7(6):843–851. doi: 10.1091/mbc.7.6.843. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Huo Hairong, Guo Xuemin, Hong Shangyu, Jiang Manrong, Liu Xinyuan, Liao Kan. Lipid rafts/caveolae are essential for insulin-like growth factor-1 receptor signaling during 3T3-L1 preadipocyte differentiation induction. J Biol Chem. 2003 Jan 21;278(13):11561–11569. doi: 10.1074/jbc.M211785200. [DOI] [PubMed] [Google Scholar]
- Ichikawa S., Sakiyama H., Suzuki G., Hidari K. I., Hirabayashi Y. Expression cloning of a cDNA for human ceramide glucosyltransferase that catalyzes the first glycosylation step of glycosphingolipid synthesis. Proc Natl Acad Sci U S A. 1996 May 14;93(10):4638–4643. doi: 10.1073/pnas.93.10.4638. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ikonen E., Parton R. G. Caveolins and cellular cholesterol balance. Traffic. 2000 Mar;1(3):212–217. doi: 10.1034/j.1600-0854.2000.010303.x. [DOI] [PubMed] [Google Scholar]
- Ilangumaran S., Arni S., van Echten-Deckert G., Borisch B., Hoessli D. C. Microdomain-dependent regulation of Lck and Fyn protein-tyrosine kinases in T lymphocyte plasma membranes. Mol Biol Cell. 1999 Apr;10(4):891–905. doi: 10.1091/mbc.10.4.891. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Iwabuchi K., Handa K., Hakomori S. Separation of "glycosphingolipid signaling domain" from caveolin-containing membrane fraction in mouse melanoma B16 cells and its role in cell adhesion coupled with signaling. J Biol Chem. 1998 Dec 11;273(50):33766–33773. doi: 10.1074/jbc.273.50.33766. [DOI] [PubMed] [Google Scholar]
- Janes P. W., Ley S. C., Magee A. I. Aggregation of lipid rafts accompanies signaling via the T cell antigen receptor. J Cell Biol. 1999 Oct 18;147(2):447–461. doi: 10.1083/jcb.147.2.447. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kasahara K., Watanabe K., Takeuchi K., Kaneko H., Oohira A., Yamamoto T., Sanai Y. Involvement of gangliosides in glycosylphosphatidylinositol-anchored neuronal cell adhesion molecule TAG-1 signaling in lipid rafts. J Biol Chem. 2000 Nov 3;275(44):34701–34709. doi: 10.1074/jbc.M003163200. [DOI] [PubMed] [Google Scholar]
- Kimura A., Baumann C. A., Chiang S. H., Saltiel A. R. The sorbin homology domain: a motif for the targeting of proteins to lipid rafts. Proc Natl Acad Sci U S A. 2001 Jul 31;98(16):9098–9103. doi: 10.1073/pnas.151252898. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Koziak K., Kaczmarek E., Kittel A., Sévigny J., Blusztajn J. K., Schulte Am Esch J., 2nd, Imai M., Guckelberger O., Goepfert C., Qawi I. Palmitoylation targets CD39/endothelial ATP diphosphohydrolase to caveolae. J Biol Chem. 2000 Jan 21;275(3):2057–2062. doi: 10.1074/jbc.275.3.2057. [DOI] [PubMed] [Google Scholar]
- Le Phuong U., Guay Ginette, Altschuler Yoram, Nabi Ivan R. Caveolin-1 is a negative regulator of caveolae-mediated endocytosis to the endoplasmic reticulum. J Biol Chem. 2001 Nov 27;277(5):3371–3379. doi: 10.1074/jbc.M111240200. [DOI] [PubMed] [Google Scholar]
- Luhrs C. A., Slomiany B. L. A human membrane-associated folate binding protein is anchored by a glycosyl-phosphatidylinositol tail. J Biol Chem. 1989 Dec 25;264(36):21446–21449. [PubMed] [Google Scholar]
- Madore N., Smith K. L., Graham C. H., Jen A., Brady K., Hall S., Morris R. Functionally different GPI proteins are organized in different domains on the neuronal surface. EMBO J. 1999 Dec 15;18(24):6917–6926. doi: 10.1093/emboj/18.24.6917. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mayor S., Maxfield F. R. Insolubility and redistribution of GPI-anchored proteins at the cell surface after detergent treatment. Mol Biol Cell. 1995 Jul;6(7):929–944. doi: 10.1091/mbc.6.7.929. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mayor S., Rothberg K. G., Maxfield F. R. Sequestration of GPI-anchored proteins in caveolae triggered by cross-linking. Science. 1994 Jun 24;264(5167):1948–1951. doi: 10.1126/science.7516582. [DOI] [PubMed] [Google Scholar]
- McCabe J. B., Berthiaume L. G. N-terminal protein acylation confers localization to cholesterol, sphingolipid-enriched membranes but not to lipid rafts/caveolae. Mol Biol Cell. 2001 Nov;12(11):3601–3617. doi: 10.1091/mbc.12.11.3601. [DOI] [PMC free article] [PubMed] [Google Scholar]
- McConville M. J., Menon A. K. Recent developments in the cell biology and biochemistry of glycosylphosphatidylinositol lipids (review). Mol Membr Biol. 2000 Jan-Mar;17(1):1–16. doi: 10.1080/096876800294443. [DOI] [PubMed] [Google Scholar]
- Melkonian K. A., Ostermeyer A. G., Chen J. Z., Roth M. G., Brown D. A. Role of lipid modifications in targeting proteins to detergent-resistant membrane rafts. Many raft proteins are acylated, while few are prenylated. J Biol Chem. 1999 Feb 5;274(6):3910–3917. doi: 10.1074/jbc.274.6.3910. [DOI] [PubMed] [Google Scholar]
- Milhiet Pierre-Emmanuel, Giocondi Marie-Cécile, Baghdadi Omid, Ronzon Frédéric, Roux Bernard, Le Grimellec Christian. Spontaneous insertion and partitioning of alkaline phosphatase into model lipid rafts. EMBO Rep. 2002 Apr 18;3(5):485–490. doi: 10.1093/embo-reports/kvf096. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mitsuda Teruhiko, Furukawa Keiko, Fukumoto Satoshi, Miyazaki Hiroshi, Urano Takeshi, Furukawa Koichi. Overexpression of ganglioside GM1 results in the dispersion of platelet-derived growth factor receptor from glycolipid-enriched microdomains and in the suppression of cell growth signals. J Biol Chem. 2002 Jan 8;277(13):11239–11246. doi: 10.1074/jbc.M107756200. [DOI] [PubMed] [Google Scholar]
- Moffett S., Brown D. A., Linder M. E. Lipid-dependent targeting of G proteins into rafts. J Biol Chem. 2000 Jan 21;275(3):2191–2198. doi: 10.1074/jbc.275.3.2191. [DOI] [PubMed] [Google Scholar]
- Munro S. An investigation of the role of transmembrane domains in Golgi protein retention. EMBO J. 1995 Oct 2;14(19):4695–4704. doi: 10.1002/j.1460-2075.1995.tb00151.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nabi Ivan R., Le Phuong U. Caveolae/raft-dependent endocytosis. J Cell Biol. 2003 May 26;161(4):673–677. doi: 10.1083/jcb.200302028. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nezil F. A., Bloom M. Combined influence of cholesterol and synthetic amphiphillic peptides upon bilayer thickness in model membranes. Biophys J. 1992 May;61(5):1176–1183. doi: 10.1016/S0006-3495(92)81926-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ng G. Y., George S. R., Zastawny R. L., Caron M., Bouvier M., Dennis M., O'Dowd B. F. Human serotonin1B receptor expression in Sf9 cells: phosphorylation, palmitoylation, and adenylyl cyclase inhibition. Biochemistry. 1993 Nov 2;32(43):11727–11733. doi: 10.1021/bi00094a032. [DOI] [PubMed] [Google Scholar]
- O'Brien P. J., Zatz M. Acylation of bovine rhodopsin by [3H]palmitic acid. J Biol Chem. 1984 Apr 25;259(8):5054–5057. [PubMed] [Google Scholar]
- O'Dowd B. F., Hnatowich M., Caron M. G., Lefkowitz R. J., Bouvier M. Palmitoylation of the human beta 2-adrenergic receptor. Mutation of Cys341 in the carboxyl tail leads to an uncoupled nonpalmitoylated form of the receptor. J Biol Chem. 1989 May 5;264(13):7564–7569. [PubMed] [Google Scholar]
- Oh P., Schnitzer J. E. Immunoisolation of caveolae with high affinity antibody binding to the oligomeric caveolin cage. Toward understanding the basis of purification. J Biol Chem. 1999 Aug 13;274(33):23144–23154. doi: 10.1074/jbc.274.33.23144. [DOI] [PubMed] [Google Scholar]
- Oh P., Schnitzer J. E. Segregation of heterotrimeric G proteins in cell surface microdomains. G(q) binds caveolin to concentrate in caveolae, whereas G(i) and G(s) target lipid rafts by default. Mol Biol Cell. 2001 Mar;12(3):685–698. doi: 10.1091/mbc.12.3.685. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ostermeyer A. G., Beckrich B. T., Ivarson K. A., Grove K. E., Brown D. A. Glycosphingolipids are not essential for formation of detergent-resistant membrane rafts in melanoma cells. methyl-beta-cyclodextrin does not affect cell surface transport of a GPI-anchored protein. J Biol Chem. 1999 Nov 26;274(48):34459–34466. doi: 10.1074/jbc.274.48.34459. [DOI] [PubMed] [Google Scholar]
- Panasiewicz Mirosława, Domek Hanna, Hoser Grazyna, Kawalec Maciej, Pacuszka Tadeusz. Structure of the ceramide moiety of GM1 ganglioside determines its occurrence in different detergent-resistant membrane domains in HL-60 cells. Biochemistry. 2003 Jun 3;42(21):6608–6619. doi: 10.1021/bi0206309. [DOI] [PubMed] [Google Scholar]
- Parton Robert G., Richards Ayanthi A. Lipid rafts and caveolae as portals for endocytosis: new insights and common mechanisms. Traffic. 2003 Nov;4(11):724–738. doi: 10.1034/j.1600-0854.2003.00128.x. [DOI] [PubMed] [Google Scholar]
- Peiró S., Comella J. X., Enrich C., Martín-Zanca D., Rocamora N. PC12 cells have caveolae that contain TrkA. Caveolae-disrupting drugs inhibit nerve growth factor-induced, but not epidermal growth factor-induced, MAPK phosphorylation. J Biol Chem. 2000 Dec 1;275(48):37846–37852. doi: 10.1074/jbc.M000487200. [DOI] [PubMed] [Google Scholar]
- Pike L. J., Miller J. M. Cholesterol depletion delocalizes phosphatidylinositol bisphosphate and inhibits hormone-stimulated phosphatidylinositol turnover. J Biol Chem. 1998 Aug 28;273(35):22298–22304. doi: 10.1074/jbc.273.35.22298. [DOI] [PubMed] [Google Scholar]
- Pike Linda J., Han Xianlin, Chung Koong-Nah, Gross Richard W. Lipid rafts are enriched in arachidonic acid and plasmenylethanolamine and their composition is independent of caveolin-1 expression: a quantitative electrospray ionization/mass spectrometric analysis. Biochemistry. 2002 Feb 12;41(6):2075–2088. doi: 10.1021/bi0156557. [DOI] [PubMed] [Google Scholar]
- Pike Linda J. Lipid rafts: bringing order to chaos. J Lipid Res. 2003 Feb 1;44(4):655–667. doi: 10.1194/jlr.R200021-JLR200. [DOI] [PubMed] [Google Scholar]
- Prinetti A., Chigorno V., Tettamanti G., Sonnino S. Sphingolipid-enriched membrane domains from rat cerebellar granule cells differentiated in culture. A compositional study. J Biol Chem. 2000 Apr 21;275(16):11658–11665. doi: 10.1074/jbc.275.16.11658. [DOI] [PubMed] [Google Scholar]
- Prior I. A., Harding A., Yan J., Sluimer J., Parton R. G., Hancock J. F. GTP-dependent segregation of H-ras from lipid rafts is required for biological activity. Nat Cell Biol. 2001 Apr;3(4):368–375. doi: 10.1038/35070050. [DOI] [PubMed] [Google Scholar]
- Prior Ian A., Muncke Cornelia, Parton Robert G., Hancock John F. Direct visualization of Ras proteins in spatially distinct cell surface microdomains. J Cell Biol. 2003 Jan 13;160(2):165–170. doi: 10.1083/jcb.200209091. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rajendran Lawrence, Masilamani Madhan, Solomon Samuel, Tikkanen Ritva, Stuermer Claudia A. O., Plattner Helmut, Illges Harald. Asymmetric localization of flotillins/reggies in preassembled platforms confers inherent polarity to hematopoietic cells. Proc Natl Acad Sci U S A. 2003 Jun 25;100(14):8241–8246. doi: 10.1073/pnas.1331629100. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ralton J. E., McConville M. J. Delineation of three pathways of glycosylphosphatidylinositol biosynthesis in Leishmania mexicana. Precursors from different pathways are assembled on distinct pools of phosphatidylinositol and undergo fatty acid remodeling. J Biol Chem. 1998 Feb 13;273(7):4245–4257. doi: 10.1074/jbc.273.7.4245. [DOI] [PubMed] [Google Scholar]
- Roberts W. L., Myher J. J., Kuksis A., Low M. G., Rosenberry T. L. Lipid analysis of the glycoinositol phospholipid membrane anchor of human erythrocyte acetylcholinesterase. Palmitoylation of inositol results in resistance to phosphatidylinositol-specific phospholipase C. J Biol Chem. 1988 Dec 15;263(35):18766–18775. [PubMed] [Google Scholar]
- Rothberg K. G., Heuser J. E., Donzell W. C., Ying Y. S., Glenney J. R., Anderson R. G. Caveolin, a protein component of caveolae membrane coats. Cell. 1992 Feb 21;68(4):673–682. doi: 10.1016/0092-8674(92)90143-z. [DOI] [PubMed] [Google Scholar]
- Roy S., Luetterforst R., Harding A., Apolloni A., Etheridge M., Stang E., Rolls B., Hancock J. F., Parton R. G. Dominant-negative caveolin inhibits H-Ras function by disrupting cholesterol-rich plasma membrane domains. Nat Cell Biol. 1999 Jun;1(2):98–105. doi: 10.1038/10067. [DOI] [PubMed] [Google Scholar]
- Röper K., Corbeil D., Huttner W. B. Retention of prominin in microvilli reveals distinct cholesterol-based lipid micro-domains in the apical plasma membrane. Nat Cell Biol. 2000 Sep;2(9):582–592. doi: 10.1038/35023524. [DOI] [PubMed] [Google Scholar]
- Sargiacomo M., Sudol M., Tang Z., Lisanti M. P. Signal transducing molecules and glycosyl-phosphatidylinositol-linked proteins form a caveolin-rich insoluble complex in MDCK cells. J Cell Biol. 1993 Aug;122(4):789–807. doi: 10.1083/jcb.122.4.789. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Saslowsky David E., Lawrence Jared, Ren Xiaoyan, Brown Deborah A., Henderson Robert M., Edwardson J. Michael. Placental alkaline phosphatase is efficiently targeted to rafts in supported lipid bilayers. J Biol Chem. 2002 May 14;277(30):26966–26970. doi: 10.1074/jbc.M204669200. [DOI] [PubMed] [Google Scholar]
- Scheiffele P., Roth M. G., Simons K. Interaction of influenza virus haemagglutinin with sphingolipid-cholesterol membrane domains via its transmembrane domain. EMBO J. 1997 Sep 15;16(18):5501–5508. doi: 10.1093/emboj/16.18.5501. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schnitzer J. E., McIntosh D. P., Dvorak A. M., Liu J., Oh P. Separation of caveolae from associated microdomains of GPI-anchored proteins. Science. 1995 Sep 8;269(5229):1435–1439. doi: 10.1126/science.7660128. [DOI] [PubMed] [Google Scholar]
- Schuck Sebastian, Honsho Masanori, Ekroos Kim, Shevchenko Andrej, Simons Kai. Resistance of cell membranes to different detergents. Proc Natl Acad Sci U S A. 2003 Apr 29;100(10):5795–5800. doi: 10.1073/pnas.0631579100. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shaul P. W., Smart E. J., Robinson L. J., German Z., Yuhanna I. S., Ying Y., Anderson R. G., Michel T. Acylation targets emdothelial nitric-oxide synthase to plasmalemmal caveolae. J Biol Chem. 1996 Mar 15;271(11):6518–6522. doi: 10.1074/jbc.271.11.6518. [DOI] [PubMed] [Google Scholar]
- Shenoy-Scaria A. M., Dietzen D. J., Kwong J., Link D. C., Lublin D. M. Cysteine3 of Src family protein tyrosine kinase determines palmitoylation and localization in caveolae. J Cell Biol. 1994 Jul;126(2):353–363. doi: 10.1083/jcb.126.2.353. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shenoy-Scaria A. M., Gauen L. K., Kwong J., Shaw A. S., Lublin D. M. Palmitylation of an amino-terminal cysteine motif of protein tyrosine kinases p56lck and p59fyn mediates interaction with glycosyl-phosphatidylinositol-anchored proteins. Mol Cell Biol. 1993 Oct;13(10):6385–6392. doi: 10.1128/mcb.13.10.6385. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shogomori Hidehiko, Brown Deborah A. Use of detergents to study membrane rafts: the good, the bad, and the ugly. Biol Chem. 2003 Sep;384(9):1259–1263. doi: 10.1515/BC.2003.139. [DOI] [PubMed] [Google Scholar]
- Simons K., Toomre D. Lipid rafts and signal transduction. Nat Rev Mol Cell Biol. 2000 Oct;1(1):31–39. doi: 10.1038/35036052. [DOI] [PubMed] [Google Scholar]
- Simons M., Friedrichson T., Schulz J. B., Pitto M., Masserini M., Kurzchalia T. V. Exogenous administration of gangliosides displaces GPI-anchored proteins from lipid microdomains in living cells. Mol Biol Cell. 1999 Oct;10(10):3187–3196. doi: 10.1091/mbc.10.10.3187. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Singer S. J., Nicolson G. L. The fluid mosaic model of the structure of cell membranes. Science. 1972 Feb 18;175(4023):720–731. doi: 10.1126/science.175.4023.720. [DOI] [PubMed] [Google Scholar]
- Slimane Tounsia Aït, Trugnan Germain, Van IJzendoorn Sven C. D., Hoekstra Dick. Raft-mediated trafficking of apical resident proteins occurs in both direct and transcytotic pathways in polarized hepatic cells: role of distinct lipid microdomains. Mol Biol Cell. 2003 Feb;14(2):611–624. doi: 10.1091/mbc.E02-08-0528. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Smart E. J., Graf G. A., McNiven M. A., Sessa W. C., Engelman J. A., Scherer P. E., Okamoto T., Lisanti M. P. Caveolins, liquid-ordered domains, and signal transduction. Mol Cell Biol. 1999 Nov;19(11):7289–7304. doi: 10.1128/mcb.19.11.7289. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Smart E. J., Ying Y. S., Mineo C., Anderson R. G. A detergent-free method for purifying caveolae membrane from tissue culture cells. Proc Natl Acad Sci U S A. 1995 Oct 24;92(22):10104–10108. doi: 10.1073/pnas.92.22.10104. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Song K. S., Li Shengwen, Okamoto T., Quilliam L. A., Sargiacomo M., Lisanti M. P. Co-purification and direct interaction of Ras with caveolin, an integral membrane protein of caveolae microdomains. Detergent-free purification of caveolae microdomains. J Biol Chem. 1996 Apr 19;271(16):9690–9697. doi: 10.1074/jbc.271.16.9690. [DOI] [PubMed] [Google Scholar]
- Stan R. V., Roberts W. G., Predescu D., Ihida K., Saucan L., Ghitescu L., Palade G. E. Immunoisolation and partial characterization of endothelial plasmalemmal vesicles (caveolae). Mol Biol Cell. 1997 Apr;8(4):595–605. doi: 10.1091/mbc.8.4.595. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Thorn Hans, Stenkula Karin G., Karlsson Margareta, Ortegren Unn, Nystrom Fredrik H., Gustavsson Johanna, Stralfors Peter. Cell surface orifices of caveolae and localization of caveolin to the necks of caveolae in adipocytes. Mol Biol Cell. 2003 Jul 11;14(10):3967–3976. doi: 10.1091/mbc.E03-01-0050. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Walmsley Adrian R., Zeng Fanning, Hooper Nigel M. The N-terminal region of the prion protein ectodomain contains a lipid raft targeting determinant. J Biol Chem. 2003 Jul 14;278(39):37241–37248. doi: 10.1074/jbc.M302036200. [DOI] [PubMed] [Google Scholar]
- Walter E. I., Roberts W. L., Rosenberry T. L., Ratnoff W. D., Medof M. E. Structural basis for variations in the sensitivity of human decay accelerating factor to phosphatidylinositol-specific phospholipase C cleavage. J Immunol. 1990 Feb 1;144(3):1030–1036. [PubMed] [Google Scholar]
- Wang Xiao-Qi, Sun Ping, Paller Amy S. Ganglioside induces caveolin-1 redistribution and interaction with the epidermal growth factor receptor. J Biol Chem. 2002 Sep 26;277(49):47028–47034. doi: 10.1074/jbc.M208257200. [DOI] [PubMed] [Google Scholar]
- Watson R. T., Shigematsu S., Chiang S. H., Mora S., Kanzaki M., Macara I. G., Saltiel A. R., Pessin J. E. Lipid raft microdomain compartmentalization of TC10 is required for insulin signaling and GLUT4 translocation. J Cell Biol. 2001 Aug 13;154(4):829–840. doi: 10.1083/jcb.200102078. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Westover Emily J., Covey Douglas F., Brockman Howard L., Brown Rhoderick E., Pike Linda J. Cholesterol depletion results in site-specific increases in epidermal growth factor receptor phosphorylation due to membrane level effects. Studies with cholesterol enantiomers. J Biol Chem. 2003 Oct 6;278(51):51125–51133. doi: 10.1074/jbc.M304332200. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Westover Emily J., Covey Douglas F. First synthesis of ent-desmosterol and its conversion to ent-deuterocholesterol. Steroids. 2003 Feb;68(2):159–166. doi: 10.1016/s0039-128x(02)00174-5. [DOI] [PubMed] [Google Scholar]
- Xu X., Bittman R., Duportail G., Heissler D., Vilcheze C., London E. Effect of the structure of natural sterols and sphingolipids on the formation of ordered sphingolipid/sterol domains (rafts). Comparison of cholesterol to plant, fungal, and disease-associated sterols and comparison of sphingomyelin, cerebrosides, and ceramide. J Biol Chem. 2001 Jun 29;276(36):33540–33546. doi: 10.1074/jbc.M104776200. [DOI] [PubMed] [Google Scholar]
- Yamabhai Montarop, Anderson Richard G. W. Second cysteine-rich region of epidermal growth factor receptor contains targeting information for caveolae/rafts. J Biol Chem. 2002 May 21;277(28):24843–24846. doi: 10.1074/jbc.C200277200. [DOI] [PubMed] [Google Scholar]
- Zacharias David A., Violin Jonathan D., Newton Alexandra C., Tsien Roger Y. Partitioning of lipid-modified monomeric GFPs into membrane microdomains of live cells. Science. 2002 May 3;296(5569):913–916. doi: 10.1126/science.1068539. [DOI] [PubMed] [Google Scholar]
- Zhang W., Trible R. P., Samelson L. E. LAT palmitoylation: its essential role in membrane microdomain targeting and tyrosine phosphorylation during T cell activation. Immunity. 1998 Aug;9(2):239–246. doi: 10.1016/s1074-7613(00)80606-8. [DOI] [PubMed] [Google Scholar]
- Zurzolo C., van't Hof W., van Meer G., Rodriguez-Boulan E. VIP21/caveolin, glycosphingolipid clusters and the sorting of glycosylphosphatidylinositol-anchored proteins in epithelial cells. EMBO J. 1994 Jan 1;13(1):42–53. doi: 10.1002/j.1460-2075.1994.tb06233.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- von Haller P. D., Donohoe S., Goodlett D. R., Aebersold R., Watts J. D. Mass spectrometric characterization of proteins extracted from Jurkat T cell detergent-resistant membrane domains. Proteomics. 2001 Aug;1(8):1010–1021. doi: 10.1002/1615-9861(200108)1:8<1010::AID-PROT1010>3.0.CO;2-L. [DOI] [PubMed] [Google Scholar]