The prion protein and lipid rafts (Review)

References

• Zahn R, Liu A, Luhrs T, Riek R, von Schroetter C, Lopez Garcia F, Billeter M, Calzolai L, Wider G, Wuthrich K. NMR solution structure of the human prion protein. Proc Natl Acad Sci USA 2000; 97: 145–150
   PubMed Web of Science ®Google Scholar
• Prusiner SB. Prions. Proc Natl Acad Sci USA 1998; 95: 13363–13383
   PubMed Web of Science ®Google Scholar
• Bueler H, Aguzzi A, Sailer A, Greiner RA, Autenried P, Aguet M, Weissmann C. Mice devoid of PrP are resistant to scrapie. Cell 1993; 73: 1339–1347
   PubMed Web of Science ®Google Scholar
• Milhavet O, Lehmann S. Oxidative stress and the prion protein in transmissible spongiform encephalopathies. Brain Res Brain Res Rev 2002; 38: 328–339
   PubMed Web of Science ®Google Scholar
• Mouillet-Richard S, Ermonval M, Chebassier C, Laplanche JL, Lehmann S, Launay JM, Kellermann O. Signal transduction through prion protein. Science 2000; 289: 1925–1928
   PubMed Web of Science ®Google Scholar
• Pauly PC, Harris DA. Copper stimulates endocytosis of the prion protein. J Biol Chem 1998; 273: 33107–33110
   PubMed Web of Science ®Google Scholar
• Watt NT, Hooper NM. The prion protein and neuronal zinc homeostasis. Trends Biochem Sci 2003; 28: 406–410
   Google Scholar
• Collinge J, Whittington MA, Sidle KC, Smith CJ, Palmer MS, Clarke AR, Jefferys JG. Prion protein is necessary for normal synaptic function. Nature 1994; 370: 295–297
   PubMed Web of Science ®Google Scholar
• Lichtenberg D, Goni FM, Heerklotz H. Detergent-resistant membranes should not be identified with membrane rafts. Trends Biochem Sci 2005; 30: 430–436
   PubMed Web of Science ®Google Scholar
• Stahl N, Borchelt DR, Hsiao K, Prusiner SB. Scrapie prion protein contains a phosphatidylinositol glycolipid. Cell 1987; 51: 229–240
   PubMed Web of Science ®Google Scholar
• Stahl N, Baldwin MA, Hecker R, Pan K-M, Burlingame AL, Prusiner SB. Glycosylinositol phospholipid anchors of the scrapie and cellular prion proteins contain sialic acid. Biochemistry 1992; 31: 5043–5053
   PubMed Web of Science ®Google Scholar
• Brewis IA, Ferguson MAJ, Mehlert A, Turner AJ, Hooper NM. Structures of the glycosyl-phosphatidylinositol anchors of porcine and human membrane dipeptidase. Interspecies comparison of the glycan core structures and further structural studies on the porcine anchor. J Biol Chem 1995; 270: 22946–22956
   PubMed Web of Science ®Google Scholar
• Meri S, Lehto T, Sutton CW, Tyynela J, Baumann M. Structural composition and functional characterization of soluble CD59: heterogeneity of the oligosaccharide and glycophosphoinositol (GPI) anchor revealed by laser-desorption mass spectrometric analysis. Biochem J 1996; 316: 923–935
   PubMed Web of Science ®Google Scholar
• Brown DA, London E. Functions of lipid rafts in biological membranes. Annu Rev Cell Dev Biol 1998; 14: 111–136
   PubMed Web of Science ®Google Scholar
• Brown DA, London E. Structure and function of sphingolipid- and cholesterol-rich membrane rafts. J Biol Chem 2000; 275: 17221–17224
   PubMed Web of Science ®Google Scholar
• Brown DA, Rose JK. Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell 1992; 68: 533–544
   PubMed Web of Science ®Google Scholar
• Taraboulos A, Scott M, Semenov A, Avraham D, Laszlo L, Prusiner SB. Cholesterol depletion and modification of COOH-terminal targeting sequence of the prion protein inhibit formation of the scrapie isoform. J Cell Biol 1995; 129: 121–132
   PubMed Web of Science ®Google Scholar
• Vey M, Pilkuhn S, Wille H, Nixon R, DeArmond SJ, Smart EJ, Anderson RGW, Taraboulos A, Prusiner SB. Subcellular colocalization of the cellular and scrapie prion proteins in caveolae-like membranous domains. Proc Natl Acad Sci USA 1996; 93: 14945–14949
   PubMed Web of Science ®Google Scholar
• Naslavsky N, Stein R, Yanai A, Friedlander G, Taraboulos A. Characterization of detergent-insoluble complexes containing the cellular prion protein and its scrapie isoform. J Biol Chem 1997; 272: 6324–6331
   PubMed Web of Science ®Google Scholar
• Sarnataro D, Campana V, Paladino S, Stornaiuolo M, Nitsch L, Zurzolo C. PrP(C) association with lipid rafts in the early secretory pathway stabilizes its cellular conformation. Mol Biol Cell 2004; 15: 4031–4042
   PubMed Web of Science ®Google Scholar
• Simons K, Ikonen E. Functional rafts in cell membranes. Nature 1997; 387: 569–572
   PubMed Web of Science ®Google Scholar
• Pang S, Urquhart P, Hooper NM. N-Glycans, not the GPI anchor, mediate the apical targeting of a naturally glycosylated, GPI-anchored protein in polarised epithelial cells. J Cell Sci 2004; 117: 5079–5086
   Google Scholar
• Sarnataro D, Paladino S, Campana V, Grassi J, Nitsch L, Zurzolo C. PrPC is sorted to the basolateral membrane of epithelial cells independently of its association with rafts. Traffic 2002; 3: 810–821
   Google Scholar
• Uelhoff A, Tatzelt J, Aguzzi A, Winklhofer KF, Haass C. A Pathogenic PrP Mutation and Doppel Interfere with Polarized Sorting of the Prion Protein. J Biol Chem 2005; 280: 5137–5140
   Google Scholar
• Walmsley AR, Zeng F, Hooper NM. The N-terminal region of the prion protein ectodomain contains a lipid raft targeting determinant. J Biol Chem 2003; 278: 37241–37248
   Google Scholar
• Baron GS, Caughey B. Effect of glycosylphosphatidylinositol anchor-dependent and -independent prion protein association with model raft membranes on conversion to the protease-resistant isoform. J Biol Chem 2003; 278: 14883–14892
   PubMed Web of Science ®Google Scholar
• Lee KS, Linden R, Prado MA, Brentani RR, Martins VR. Towards cellular receptors for prions. Rev Med Virol 2003; 13: 399–408
   PubMed Web of Science ®Google Scholar
• Mahfoud R, Garmy N, Maresca M, Yahi N, Puigserver A, Fantini J. Identification of a common sphingolipid-binding domain in Alzheimer, prion, and HIV-1 proteins. J Biol Chem 2002; 277: 11292–11296
   PubMed Web of Science ®Google Scholar
• Rosenmann H, Talmor G, Halimi M, Yanai A, Gabizon R, Meiner Z. Prion protein with an E200K mutation displays properties similar to those of the cellular isoform PrP(C). J Neurochem 2001; 76: 1654–1662
   Google Scholar
• Madore N, Smith KL, Graham CH, Jen A, Brady K, Hall S, Morris R. Functionally different GPI proteins are organised in different domains on the neuronal surface. EMBO J 1999; 19: 6917–6926
   Google Scholar
• Brugger B, Graham C, Leibrecht I, Mombelli E, Jen A, Wieland F, Morris R. The membrane domains occupied by glycosylphosphatidylinositol-anchored prion protein and Thy-1 differ in lipid composition. J Biol Chem 2004; 279: 7530–7536
   PubMed Web of Science ®Google Scholar
• Moore RC, Lee IY, Silverman GL, Harrison PM, Strome R, Heinrich C, Karunaratne A, Pasternak SH, Chishti MA, Liang Y, Mastrangelo P, Wang K, Smit AF, Katamine S, Carlson GA, Cohen FE, Prusiner SB, Melton DW, Tremblay P, Hood LE, Westaway D. Ataxia in prion protein (PrP)-deficient mice is associated with upregulation of the novel PrP-like protein doppel. J Mol Biol 1999; 292: 797–817
   PubMed Web of Science ®Google Scholar
• Shaked Y, Hijazi N, Gabizon R. Doppel and PrP(C) do not share the same membrane microenvironment. FEBS Lett 2002; 530: 85–88
   Google Scholar
• Massimino ML, Ballarin C, Bertoli A, Casonato S, Genovesi S, Negro A, Sorgato MC. Human Doppel and prion protein share common membrane microdomains and internalization pathways. Int J Biochem Cell Biol 2004; 36: 2016–2031
   Google Scholar
• Pike LJ. Lipid rafts: heterogeneity on the high seas. Biochem J 2004; 378: 281–292
   PubMed Web of Science ®Google Scholar
• Shyng S-L, Huber MT, Harris DA. A prion protein cycles between the cell surface and an endocytic compartment in cultured neuroblastoma cells. J Biol Chem 1993; 268: 15922–15928
   PubMed Web of Science ®Google Scholar
• Shyng SL, Heuser JE, Harris DA. A glycolipid-anchored prion protein is endocytosed via clathrin-coated pits. J Cell Biol 1994; 125: 1239–1250
   PubMed Web of Science ®Google Scholar
• Harmey JH, Doyle D, Brown V, Rogers MS. The cellular isoform of the prion protein, PrPc, is associated with caveolae in mouse neuroblastoma (N2a) cells. Biochem Biophys Res Commun 1995; 210: 753–759
   PubMedGoogle Scholar
• Kaneko K, Vey M, Scott M, Pilkuhn S, Cohen FE, Prusiner SB. COOH-terminal sequence of the cellular prion protein directs subcellular trafficking and controls conversion into the scapie isoform. Proc Natl Acad Sci USA 1997; 94: 2333–2338
   PubMed Web of Science ®Google Scholar
• Anderson RGW. The caveolae membrane system. Annu Rev Biochem 1998; 67: 199–225
   PubMed Web of Science ®Google Scholar
• Parpal S, Karlsson M, Thorn H, Stralfors P. Cholesterol depletion disrupts caveolae and insulin receptor signaling for metabolic control via insulin receptor substrate-1, but not for mitogen-activated protein kinase control. J Biol Chem 2001; 276: 9670–9678
   PubMed Web of Science ®Google Scholar
• Peters PJ, Mironov A, Jr, Peretz D, van Donselaar E, Leclerc E, Erpel S, DeArmond SJ, Burton DR, Williamson RA, Vey M, Prusiner SB. Trafficking of prion proteins through a caveolae-mediated endosomal pathway. J Cell Biol 2003; 162: 703–717
   PubMed Web of Science ®Google Scholar
• Marella M, Lehmann S, Grassi J, Chabry J. Filipin prevents pathological prion protein accumulation by reducing endocytosis and inducing cellular PrP release. J Biol Chem 2002; 277: 25457–25464
   PubMed Web of Science ®Google Scholar
• Parkin ET, Watt NT, Turner AJ, Hooper NM. Dual mechanisms for shedding of the cellular prion protein. J Biol Chem 2004; 279: 11170–11178
   PubMedGoogle Scholar
• Gorodinsky A, Harris DA. Glycolipid-anchored proteins in neuroblastoma cells form detergent-resistant complexes without caveolin. J Cell Biol 1995; 129: 619–627
   PubMed Web of Science ®Google Scholar
• Parkin ET, Hussain I, Turner AJ, Hooper NM. The amyloid precursor protein is not enriched in caveolae-like, detergent-insoluble membrane microdomains. J Neurochem 1997; 69: 2179–2188
   PubMedGoogle Scholar
• Kirchhausen T. Clathrin. Annu Rev Biochem 2000; 69: 699–727
   PubMed Web of Science ®Google Scholar
• Harris DA. Cellular biology of prion diseases. Clin Microbiol Rev 1999; 12: 429–444
   PubMed Web of Science ®Google Scholar
• Conese M, Nykjaer A, Petersen CM, Cremona O, Pardi R, Andreasen PA, Gliemann J, Christensen EI, Blasi F. Alpha-2 Macroglobulin receptor/Ldl receptor-related protein(Lrp)-dependent internalization of the urokinase receptor. J Cell Biol 1995; 131: 1609–1622
   PubMed Web of Science ®Google Scholar
• Sunyach C, Jen A, Deng J, Fitzgerald KT, Frobert Y, Grassi J, McCaffrey MW, Morris R. The mechanism of internalization of glycosylphosphatidylinositol-anchored prion protein. EMBO J 2003; 22: 3591–3601
   PubMed Web of Science ®Google Scholar
• Nichols B. Caveosomes and endocytosis of lipid rafts. J Cell Sci 2003; 116: 4707–4714
   PubMed Web of Science ®Google Scholar
• Magalhaes AC, Silva JA, Lee KS, Martins VR, Prado VF, Ferguson SS, Gomez MV, Brentani RR, Prado MA. Endocytic intermediates involved with the intracellular trafficking of a fluorescent cellular prion protein. J Biol Chem 2002; 277: 33311–33318
   Google Scholar
• Stockel J, Safar J, Wallacen AC, Cohen FE, Prusiner SB. Prion protein selectively binds copper(II) ions. Biochemistry 1998; 37: 7185–7193
   PubMed Web of Science ®Google Scholar
• Viles JH, Cohen FE, Prusiner SB, Goodin DB, Wright PE, Dyson HJ. Copper binding to the prion protein: structural implications of four identical cooperative binding sites. Proc Natl Acad Sci USA 1999; 96: 2042–2047
   PubMed Web of Science ®Google Scholar
• Perera WSS, Hooper NM. Ablation of the metal ion-induced endocytosis of the prion protein by disease-associated mutation of the octarepeat region. Curr Biol 2001; 11: 519–523
   PubMed Web of Science ®Google Scholar
• Taylor, DR, Watt, NT, Perera, WSS, Hooper, NM. Assigning functions to distinct regions of the N-terminus of the prion protein that are involved in its copper-stimulated, clathrin-dependent endocytosis. J Cell Sci 2005;118:5141–5153.
   Google Scholar
• Shyng S-L, Moulder KL, Lesko A, Harris DA. The N-terminal domain of a glycolipid-anchored prion protein is essential for its endocytosis via clathrin-coated pits. J Biol Chem 1995; 270: 14793–14800
   PubMed Web of Science ®Google Scholar
• Kiachopoulos S, Heske J, Tatzelt J, Winklhofer KF. Misfolding of the prion protein at the plasma membrane induces endocytosis, intracellular retention and degradation. Traffic 2004; 5: 426–436
   Google Scholar
• Nunziante M, Gilch S, Schatzl HM. Essential role of the prion protein N terminus in subcellular trafficking and half-life of cellular prion protein. J Biol Chem 2003; 278: 3726–3734
   PubMedGoogle Scholar
• Zahn R. The octapeptide repeats in mammalian prion protein constitute a pH-dependent folding and aggregation site. J Mol Biol 2003; 334: 477–488
   PubMed Web of Science ®Google Scholar
• Tsui-Pierchala BA, Encinas M, Milbrandt J, Johnson EM, Jr. Lipid rafts in neuronal signaling and function. Trends Neurosci 2002; 25: 412–417
   PubMed Web of Science ®Google Scholar
• Horejsi V, Drbal K, Cebecauer M, Cerny J, Brdicka T, Angelisova P, Stockinger H. GPI-microdomains: a role in signalling via immunoreceptors. Immunology Today 1999; 20: 356–361
   PubMedGoogle Scholar
• Mouillet-Richard S, Pietri M, Schneider B, Vidal C, Mutel V, Launay J-M, Kellermann O. Modulation of serotonergic receptor signaling and cross-talk by prion protein. J Biol Chem 2005; 280: 4592–4601
   PubMed Web of Science ®Google Scholar
• Spielhaupter C, Schatzl HM. PrPC Directly interacts with proteins involved in signaling pathways. J Biol Chem 2001; 276: 44604–44612
   PubMed Web of Science ®Google Scholar
• Mattei V, Garofalo T, Misasi R, Gizzi C, Mascellino MT, Dolo V, Pontieri GM, Sorice M, Pavan A. Association of cellular prion protein with gangliosides in plasma membrane microdomains of neural and lymphocytic cells. Neurochem Res 2002; 27: 743–749
   PubMed Web of Science ®Google Scholar
• Mattei V, Garofalo T, Misasi R, Circella A, Manganelli V, Lucania G, Pavan A, Sorice M. Prion protein is a component of the multimolecular signaling complex involved in T cell activation. FEBS Lett 2004; 560: 14–18
   Google Scholar
• Stuermer CA, Langhorst MF, Wiechers MF, Legler DF, Von Hanwehr SH, Guse AH, Plattner H. PrPc capping in T cells promotes its association with the lipid raft proteins reggie-1 and reggie-2 and leads to signal transduction. FASEB J 2004; 18: 1731–1733
   Google Scholar
• Zanata SM, Lopes MH, Mercadante AF, Hajj GN, Chiarini LB, Nomizo R, Freitas AR, Cabral AL, Lee KS, Juliano MA, de Oliveira E, Jachieri SG, Burlingame A, Huang L, Linden R, Brentani RR, Martins VR. Stress-inducible protein 1 is a cell surface ligand for cellular prion that triggers neuroprotection. EMBO J 2002; 21: 3307–3316
   PubMed Web of Science ®Google Scholar
• Chiarini LB, Freitas AR, Zanata SM, Brentani RR, Martins VR, Linden R. Cellular prion protein transduces neuroprotective signals. EMBO J 2002; 21: 3317–3326
   PubMed Web of Science ®Google Scholar
• Santuccione A, Sytnyk V, Leshchyns'ka I, Schachner M. Prion protein recruits its neuronal receptor NCAM to lipid rafts to activate p59fyn and to enhance neurite outgrowth. J Cell Biol 2005; 169: 341–354
   PubMed Web of Science ®Google Scholar
• Monnet C, Gavard J, Mege RM, Sobel A. Clustering of cellular prion protein induces ERK1/2 and stathmin phosphorylation in GT1-7 neuronal cells. FEBS Lett 2004; 576: 114–118
   PubMed Web of Science ®Google Scholar
• Mineo C, James GL, Smart EJ, Anderson RGW. Localization of epidermal growth factor-stimulated Ras/Raf-1 interaction to caveolae membrane. J Biol Chem 1996; 271: 11930–11935
   PubMed Web of Science ®Google Scholar
• Mineo C, Gill GN, Anderson RG. Regulated migration of epidermal growth factor receptor from caveolae. J Biol Chem 1999; 274: 30636–30643
   PubMed Web of Science ®Google Scholar
• Vassallo N, Herms J, Behrens C, Krebs B, Saeki K, Onodera T, Windl O, Kretzschmar HA. Activation of phosphatidylinositol 3-kinase by cellular prion protein and its role in cell survival. Biochem Biophys Res Commun 2005; 332: 75–82
   Google Scholar
• Solforosi L, Criado JR, McGavern DB, Wirz S, Sanchez-Alavez M, Sugama S, DeGiorgio LA, Volpe BT, Wiseman E, Abalos G, Masliah E, Gilden D, Oldstone MB, Conti B, Williamson RA. Cross-linking cellular prion protein triggers neuronal apoptosis in vivo. Science 2004; 303: 1514–1516
   PubMed Web of Science ®Google Scholar
• Botto L, Masserini M, Cassetti A, Palestini P. Immunoseparation of prion protein-enriched domains from other detergent-resistant membrane fractions, isolated from neuronal cells. FEBS Lett 2004; 557: 143–147
   PubMed Web of Science ®Google Scholar
• Hugel B, Martinez MC, Kunzelmann C, Blattler T, Aguzzi A, Freyssinet JM. Modulation of signal transduction through the cellular prion protein is linked to its incorporation in lipid rafts. Cell Mol Life Sci 2004; 61: 2998–3007
   Google Scholar
• Anderson RG, Jacobson K. A role for lipid shells in targeting proteins to caveolae, rafts, and other lipid domains. Science 2002; 296: 1821–1825
   PubMed Web of Science ®Google Scholar
• Mayor S, Rao M. Rafts: scale-dependent, active lipid organization at the cell surface. Traffic 2004; 5: 231–240
   PubMed Web of Science ®Google Scholar
• Campana V, Sarnataro D, Zurzolo C. The highways and byways of prion protein trafficking. Trends Cell Biol 2005; 15: 102–111
   PubMed Web of Science ®Google Scholar
• Bate C, Salmona M, Diomede L, Williams A. Squalestatin cures prion-infected neurons and protects against prion neurotoxicity. J Biol Chem 2004; 279: 14983–14990
   PubMed Web of Science ®Google Scholar
• Baron GS, Wehrly K, Dorward DW, Chesebro B, Caughey B. Conversion of raft associated prion protein to the protease-resistant state requires insertion of PrP-res (PrP(Sc)) into contiguous membranes. EMBO J 2002; 21: 1031–1040
   PubMed Web of Science ®Google Scholar
• Nishina K, Deleault NR, Lucassen RW, Supattapone S. In vitro prion protein conversion in detergent-solubilized membranes. Biochemistry 2004; 43: 2613–2621
   Google Scholar
• Sanghera N, Pinheiro TJ. Binding of prion protein to lipid membranes and implications for prion conversion. J Mol Biol 2002; 315: 1241–1256
   PubMed Web of Science ®Google Scholar
• Kazlauskaite J, Sanghera N, Sylvester I, Venien-Bryan C, Pinheiro TJ. Structural changes of the prion protein in lipid membranes leading to aggregation and fibrillization. Biochemistry 2003; 42: 3295–3304
   PubMed Web of Science ®Google Scholar
• Critchley P, Kazlauskaite J, Eason R, Pinheiro TJ. Binding of prion proteins to lipid membranes. Biochem Biophys Res Commun 2004; 313: 559–567
   PubMed Web of Science ®Google Scholar
• Kanu N, Imokawa Y, Drechsel DN, Williamson RA, Birkett CR, Bostock CJ, Brockes JP. Transfer of scrapie prion infectivity by cell contact in culture. Curr Biol 2002; 12: 523–530
   PubMed Web of Science ®Google Scholar
• Fevrier B, Vilette D, Archer F, Loew D, Faigle W, Vidal M, Laude H, Raposo G. Cells release prions in association with exosomes. Proc Natl Acad Sci USA 2004; 101: 9683–9688
   PubMed Web of Science ®Google Scholar
• Liu T, Li R, Pan T, Liu D, Petersen RB, Wong BS, Gambetti P, Sy MS. Intercellular transfer of the cellular prion protein. J Biol Chem 2002; 277: 47671–47678
   PubMed Web of Science ®Google Scholar
• Chesebro B, Trifilo M, Race R, Meade-White K, Teng C, LaCasse R, Raymond L, Favara C, Baron G, Priola S, Caughey B, Masliah E, Oldstone M. Anchorless prion protein results in infectious amyloid disease without clinical scrapie. Science 2005; 308: 1435–1439
   PubMed Web of Science ®Google Scholar
• Aguzzi A. Cell biology. Prion toxicity: all sail and no anchor. Science 2005; 308: 1420–1421
   PubMed Web of Science ®Google Scholar
• Russelakis-Carneiro M, Hetz C, Maundrell K, Soto C. Prion replication alters the distribution of synaptophysin and caveolin 1 in neuronal lipid rafts. Am J Pathol 2004; 165: 1839–1848
   PubMed Web of Science ®Google Scholar