Temperature-dependent localization of GPI-anchored intestinal alkaline phosphatase in model rafts†
Marie-Cécile Giocondi
Institut National de la Santé et de la Recherche Médicale, Unité 554, Montpellier, France
Université de Montpellier, Centre National de la Recherche Scientifique, UMR 5048, Centre de Biochimie Structurale, Montpellier, France
Search for more papers by this authorFrançoise Besson
ICBMS, Institut de Chimie et Biochimie Moléculaires et Supramoléculaires, 43 boulevard du 11 novembre 1918, Villeurbanne, F-69622, France
CNRS, UMR 5246, Villeurbanne, F-69622, France
Université de Lyon, Lyon, F-69003, France
Université Lyon 1, F-69003, France
Search for more papers by this authorPatrice Dosset
Institut National de la Santé et de la Recherche Médicale, Unité 554, Montpellier, France
Université de Montpellier, Centre National de la Recherche Scientifique, UMR 5048, Centre de Biochimie Structurale, Montpellier, France
Search for more papers by this authorPierre-Emmanuel Milhiet
Institut National de la Santé et de la Recherche Médicale, Unité 554, Montpellier, France
Université de Montpellier, Centre National de la Recherche Scientifique, UMR 5048, Centre de Biochimie Structurale, Montpellier, France
Search for more papers by this authorCorresponding Author
Christian Le Grimellec
Institut National de la Santé et de la Recherche Médicale, Unité 554, Montpellier, France
Université de Montpellier, Centre National de la Recherche Scientifique, UMR 5048, Centre de Biochimie Structurale, Montpellier, France
Nanostructures and Membrane Complexes, C.B.S., 29 rue de Navacelles, 34090 Montpellier Cedex, France.Search for more papers by this authorMarie-Cécile Giocondi
Institut National de la Santé et de la Recherche Médicale, Unité 554, Montpellier, France
Université de Montpellier, Centre National de la Recherche Scientifique, UMR 5048, Centre de Biochimie Structurale, Montpellier, France
Search for more papers by this authorFrançoise Besson
ICBMS, Institut de Chimie et Biochimie Moléculaires et Supramoléculaires, 43 boulevard du 11 novembre 1918, Villeurbanne, F-69622, France
CNRS, UMR 5246, Villeurbanne, F-69622, France
Université de Lyon, Lyon, F-69003, France
Université Lyon 1, F-69003, France
Search for more papers by this authorPatrice Dosset
Institut National de la Santé et de la Recherche Médicale, Unité 554, Montpellier, France
Université de Montpellier, Centre National de la Recherche Scientifique, UMR 5048, Centre de Biochimie Structurale, Montpellier, France
Search for more papers by this authorPierre-Emmanuel Milhiet
Institut National de la Santé et de la Recherche Médicale, Unité 554, Montpellier, France
Université de Montpellier, Centre National de la Recherche Scientifique, UMR 5048, Centre de Biochimie Structurale, Montpellier, France
Search for more papers by this authorCorresponding Author
Christian Le Grimellec
Institut National de la Santé et de la Recherche Médicale, Unité 554, Montpellier, France
Université de Montpellier, Centre National de la Recherche Scientifique, UMR 5048, Centre de Biochimie Structurale, Montpellier, France
Nanostructures and Membrane Complexes, C.B.S., 29 rue de Navacelles, 34090 Montpellier Cedex, France.Search for more papers by this authorPaper presented as part of a special issue of papers from the AFMBiomed conference, Barcelona 2007.
Abstract
In plasma membranes, most of glycosylphosphatidylinositol (GPI)-anchored proteins would be associated with rafts, a category of ordered microdomains enriched in sphingolipids and cholesterol (Ch). They would be also concentrated in the detergent resistant membranes (DRMs), a plasma membrane fraction extracted at low temperature. Preferential localization of GPI-anchored proteins in these membrane domains is essentially governed by their high lipid order, as compared to their environment. Changes in the temperature are expected to modify the membrane lipid order, suggesting that they could affect the distribution of GPI-anchored proteins between membrane domains. Validity of this hypothesis was examined by investigating the temperature-dependent localization of the GPI-anchored bovine intestinal alkaline phophatase (BIAP) into model raft made of palmitoyloleoylphosphatidylcholine/sphingomyelin/cholesterol (POPC/SM/Chl) supported membranes. Atomic force microscopy (AFM) shows that the inserted BIAP is localized in the SM/Chl enriched ordered domains at low temperature. Above 30°C, BIAP redistributes and is present in both the ‘fluid’ POPC enriched and the ordered SM/Chl domains. These data strongly suggest that in cells the composition of plasma membrane domains at low temperature differs from that at physiological temperature. Copyright © 2007 John Wiley & Sons, Ltd.
REFERENCES
- Ahmed SN, Brown DA, London E. 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.
- Bassereau P, Brodbreck D, Russell TP, Brown HR, Shull KR. 1993. Topological coarsening of symmetric diblock copolymer films: model 2D systems. Phys. Rev. Lett. 71: 1716–1719.
- Benting J, Rietveld A, Ansorge I, Simons K. 1999. Acyl and alkyl chain length of GPI-anchors is critical for raft association in vitro. FEBS Lett. 462: 47–50.
- Booth AG, Kenny AJ. 1974. A rapid method for the preparation of microvilli from rabbit kidney. Biochem. J. 142: 575–581.
- Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72: 248–254.
- Brasitus TA, Schachter D. 1980. Lipid dynamics and lipid-protein interactions in rat enterocyte basolateral and microvillus membranes. Biochemistry 19: 2763–2769.
- Brown DA, London E. 2000. Structure and function of sphingolipid- and cholesterol-rich membrane rafts. J. Biol. Chem. 275: 17221–17224.
- Brown DA, Rose JK. 1992. Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell 68: 533–544.
- Bublitz R, Armesto J, Hoffmann-Blume E, Schulze M, Rhode H, Horn A, Aulwurm S, Hannappel E, Fischer W. 1993. Heterogeneity of glycosylphosphatidylinositol-anchored alkaline phosphatase of calf intestine. Eur. J. Biochem. 217: 199–207.
- Chiantia S, Ries J, Kahya N, Schwille P. 2006. Combined AFM and two-focus SFCS study of Raft-exhibiting model membranes. Chem. Phys. Chem. 7: 2409–2418.
- Cyboron GW, Wuthier RE. 1981. Purification and initial characterization of intrinsic membrane-bound alkaline phosphatase from chicken epiphyseal cartilage. J. Biol. Chem. 256: 7262–7268.
- de Almeida RF, Fedorov A, Prieto M. 2003. Sphingomyelin/phosphatidylcholine/cholesterol phase diagram: boundaries and composition of lipid rafts. Biophys. J. 85: 2406–2416.
- Dietrich C, Volovyk ZN, Levi M, Thompson NL, Jacobson K. 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.
- Ferguson MA. 1999. The structure, biosynthesis and functions of glycosylphosphatidylinositol anchors, and the contribution of trypanosome research. J. Cell. Sci. 112: 2799–2809.
- Giocondi MC, Le Grimellec C. 1989. Temperature dependence of plasma membrane physical state in living Madin-Darby canine kidney cells. Biochem. Biophys. Res. Commun. 162: 1004–1009.
- Giocondi MC, Le Grimellec C. 2004. Temperature dependence of the surface topography in dimyristoylphosphatidylcholine/distearoylphosphatidylcholine multibilayers. Biophys. J. 86: 2218–2230.
- Giocondi MC, Vié V, Lesniewska E, Milhiet PE, Zinke-Allmang M, Le Grimellec C. 2001. Phase topology and growth of single domains in lipid bilayers. Langmuir 17: 1653–1659.
- Giocondi MC, Boichot S, Plenat T, Le Grimellec CC. 2004a. Structural diversity of sphingomyelin microdomains. Ultramicroscopy 100: 135–143.
- Giocondi MC, Milhiet PE, Dosset P, Le Grimellec C. 2004b. Use of cyclodextrin for AFM monitoring of model raft formation. Biophys. J. 86: 861–869.
- Hooper NM, Turner AJ. 1988. Ectoenzymes of the kidney microvillar membrane. Biochem. J. 250: 865–869.
- Jacobson K, Mouritsen OG, Anderson RG. 2007. Lipid rafts: at a crossroad between cell biology and physics. Nat. Cell. Biol. 9: 7–14.
- Johnson SJ, Bayerl TM, McDermott DC, Adam GW, Rennie AR, Thomas RK, Sackmann E. 1991. Structure of an adsorbed dimyristoylphosphatidylcholine bilayer measured with specular reflection of neutrons. Biophys. J. 59: 289–294.
- Kahya N, Brown DA, Schwille P. 2005. Raft partitioning and dynamic behavior of human placental alkaline phosphatase in giant unilamellar vesicles. Biochemistry 44: 7479–7489.
- Karim A, Douglas JF, Sung LP, Ermi BD. 2002. Self-assembly by phase separation in polymer thin films. In Encyclopedia of Materials: Science and Technology, KHJ Buschow, RW Cahn, MC Flemings, B Ilschner, EJ Kramer, S Mahajan (eds). NIST ed. Elsevier Science Ltd: Amsterdam, the Netherlands; 8319–8322.
- Karnovsky MJ, Kleinfeld AM, Hoover RL, Klausner RD. 1982. The concept of lipid domains in membranes. J. Cell. Biol. 94: 1–6.
- Le Du MH, Stigbrand T, Taussig MJ, Menez A, Stura EA. 2001. Crystal structure of alkaline phosphatase from human placenta at 1.8 A resolution. Implication for a substrate specificity. J. Biol. Chem. 276: 9158–9165.
- Le Grimellec C, Giocondi MC, Carriere B, Carriere S, Cardinal J. 1982. Membrane fluidity and enzyme activities in brush border and basolateral membranes of the dog kidney. Am. J. Physiol. 242: F246–F253.
- Lichtenberg D, Goni FM, Heerklotz H. 2005. Detergent-resistant membranes should not be identified with membrane rafts. Trends. Biochem. Sci. 30: 430–436.
- Low MG. 1989. The glycosyl-phosphatidylinositol anchor of membrane proteins. Biochim. Biophys. Acta 988: 427–454.
- Meder D, Moreno MJ, Verkade P, Vaz WL, Simons K. 2006. Phase coexistence and connectivity in the apical membrane of polarized epithelial cells. Proc. Natl. Acad. Sci. USA 103: 329–334.
- Milhiet P-E, Giocondi M-C, Baghdadi O, Ronzon F, Le Grimellec C, Roux B. 2002a. AFM Detection of GPI protein insertion into DOPC/DPPC model membranes. Single. Mol. 3: 135–140.
- Milhiet PE, Giocondi MC, Baghdadi O, Ronzon F, Roux B, Le Grimellec C. 2002b. Spontaneous insertion and partitioning of alkaline phosphatase into model lipid rafts. EMBO Rep. 3: 485–490.
- Morrisett JD, Pownall HJ, Plumlee RT, Smith LC, Zehner ZE. 1975. Multiple thermotropic phase transitions in Escherichia coli membranes and membrane lipids. A comparison of results obtained by nitroxyl stearate paramagnetic resonance, pyrene excimer fluorescence, and enzyme activity measurements. J. Biol. Chem. 250: 6969–6976.
- Mrsny RJ, Volwerk JJ, Griffith OH. 1986. A simplified procedure for lipid phosphorus analysis shows that digestion rates vary with phospholipid structure. Chem. Phys. Lipids 39: 185–191.
- Redman CA, Thomas-Oates JE, Ogata S, Ikehara Y, Ferguson MA. 1994. Structure of the glycosylphosphatidylinositol membrane anchor of human placental alkaline phosphatase. Biochem. J. 302(Pt 3): 861–865.
- Ronzon F, Desbat B, Buffeteau T, Mingotaud C, Chauvet J-P, Roux B. 2002. Structure and orientation of a glycosylphosphatidyl Inositol anchored protein at the air/water interface. J. Phys. Chem. B 106: 3307–3315.
- Saslowsky DE, Lawrence J, Ren X, Brown DA, Henderson RM, Edwardson JM. 2002. Placental alkaline phosphatase is efficiently targeted to rafts in supported lipid bilayers. J. Biol. Chem. 277: 26966–26970.
- Simons K, Ikonen E. 1997. Functional rafts in cell membranes. Nature 387: 569–572.
- Sung L, Karim A, Douglas JF, Han CC. 1996. Dimensional crossover in the phase separation kinetics of thin polymer blend films. Phys. Rev. Lett. 76: 4368–4371.
- Tsamaloukas A, Szadkowska H, Heerklotz H. 2006. Thermodynamic comparison of the interactions of cholesterol with unsaturated phospholipid and sphingomyelins. Biophys. J. 90: 4479–4487.
- Veatch SL, Keller SL. 2005. Miscibility phase diagrams of giant vesicles containing sphingomyelin. Phys. Rev. Lett. 94: 148101.
- Wang Y, Tsui O. 2006. Mean-field description of spinodal growth of surface waves on rupturing films. J. Non-Crystal Sol. 325: 4977–4982.
- White D. 1973. In The Phospholipid Composition of Mammalian Tissues, In Form and Function of Phospholipids, G Ansell, J Hawthorne, R Dawson (eds). Elsevier: Amsterdam.
- Wilfong RF, Neville DM Jr. 1970. The isolation of a brush border membrane fraction from rat kidney. J. Biol. Chem. 245: 6106–6112.
