The membrane environment of endogenous cellular prion protein in primary rat cerebellar neurons

Journal of Neurochemistry

Volumn 95, Issue 3, 2005, Pages 771-783

  Loberto, Nicoletta ^a   Prioni, Simona ^a   Bettiga, Arianna ^a   Chigorno, Vanna ^a   Prinetti, Alessandro ^a,b   Sonnino, Sandro ^a  

^a UNIVERSITY OF MILAN   (Italy)

^b Dipartimento di Chimica   (Italy)

Author keywords

Detergent resistant membrane domains; Gangliosides; GPI anchored proteins; Neuronal cells; Prion protein; Sphingolipids

Indexed keywords

CELL PROTEIN; CHOLESTEROL; GANGLIOSIDE; GLYCOSPHINGOLIPID; GLYCOSYLPHOSPHATIDYLINOSITOL; MEMBRANE PROTEIN; MONOCLONAL ANTIBODY; PHOSPHATIDYLCHOLINE; PRION PROTEIN; PROTEIN KINASE FYN; PROTEIN KINASE LYN; SPHINGOLIPID; SPHINGOMYELIN; THY 1 ANTIGEN;

ANIMAL CELL; ARTICLE; BIOTINYLATION; CELL SURFACE; CEREBELLUM; CONTROLLED STUDY; COVALENT BOND; ENVIRONMENT; EXPOSURE; FLOTATION; IN VITRO STUDY; LIPID MEMBRANE; NERVE CELL DIFFERENTIATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN INTERACTION; RAT; SEPARATION TECHNIQUE; SUCROSE GRADIENT;

ANIMALS; CELL FRACTIONATION; CELL MEMBRANE; CELLS, CULTURED; CEREBELLUM; DETERGENTS; GANGLIOSIDES; IMMUNOPRECIPITATION; MEMBRANE LIPIDS; MEMBRANE PROTEINS; NEURONS; NEUTRAL GLYCOSPHINGOLIPIDS; OCTOXYNOL; PLANT OILS; POLYETHYLENE GLYCOLS; PRIONS; PROTO-ONCOGENE PROTEINS C-FYN; RATS; RATS, SPRAGUE-DAWLEY; SPHINGOMYELINS; SRC-FAMILY KINASES;

ANIMALIA;

EID: 27644593331     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2005.03397.x     Document Type: Article

References (69)

1. Altin J. G. and Pagler E. B. (1995) A one-step procedure for biotinylation and chemical cross-linking of lymphocyte surface and intracellular membrane-associated molecules. Anal. Biochem. 224, 382-389.
2. Ami S., Ilangumaran S., van Echten-Deckert G., Sandhoff K., Poincelet M., Briol A., Rungger-Brandle E. and Hoessli D. C. (1996) Differential regulation of Src-family protein kinase in GPI domains of T lymphocyte plasma membranes. Biochem. Biophys. Res. 225, 801-807.
3. Balasz R., Gallo V. and Kingsbury A. (1988) Effect of depolarization on the maturation of cerebellar granule cells in culture. Brain Res. 468, 269-276.
4. Baron G. S., Wehrly K., Dorward D. W., Chesebro B. and Caughey B. (2002) Conversion of raft-associated prion protein to the protease-resistant state requires insertion of PrP-res (PrP(Sc)) into contiguous membranes. EMBO J. 21, 1031-1040.
5. Borchelt D. L., Scott M., Taraboulos A., Stahl N. and Prusiner S. B. (1990) Scrapie and cellular prion proteins differ in their kinetics of synthesis and topology in cultured cells. J. Cell Biol. 110, 743-752.
6. Botto L., Masserini M., Cassetti A. and Palestini P. (2004) Immunoseparation of prion protein-enriched domains from other detergent-resistant membrane fractions, isolated from neuronal cells. FEBS Lett. 557, 143-147.
7. Brown D. A. (1994) GPI-anchored proteins and detergent-resistant membrane domains. Braz. J. Med. Biol. Res. 27, 309-315.
8. Brown D. A. and London E. (1998) Functions of lipid rafts in biological membranes. Annu. Rev. Cell Dev. Biol. 14, 11-136.
9. Brown D. A. and Rose J. K. (1992) Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell 68, 533-544.
10. Brugger B., Graham C. H., Leibrecht I., Mombelli E., Jen A., Wieland F. and Morris R. (2004) The membrane domains occupied by glycosylphosphatidylinositol-anchored prion protein and Thy-1 differ in lipid composition. J. Biol. Chem. 279, 7530-7536.
11. Carter H. E., Rothfus J. A. and Gigg R. (1961) Biochemistry of the sphingolipids. XII. Conversion of cerebrosides to ceramides and sphingosine; structure of Gaucher cerebroside. J. Lipid Res. 2, 228-234.
12. Cole S. R., Ashman L. K. and Ev P. L. (1987) Biotinylation: an alternative to radioiodination for the identification of cell surface antigens in immunoprecipitates. Mol. Immunol. 24, 699-705.
13. Faivre-Sarrailh C., Gauthier F., Denisenko-Nehrbass N., Le Bivic A., Rougon G. and Girault J. A. (2000) The glycosylphosphatidyl inosithol-anchored adhesion molecule F3/contactin is required for surface transport of paranodin/contactin-associated protein (caspr). J. Cell Biol. 149, 491-502.
14. Fra A. M., Williamson E., Simons K. and Parton R. G. (1994) Detergent-insoluble glycolipid microdomains in lymphocytes in the absence of caveolae. J. Biol. Chem. 269, 30 745-30 748.
15. Gallo V., Ciotti M. T., Coletti A., Aloisi F. and Levi G. (1982) Selective release of glutamate from cerebellar granule cells differentiating in culture. Proc. Natl Acad. Sci. USA 79, 7919-7923.
16. Harder T. and Simons K. (1997) Caveolae, DIGs, and the dynamics of sphingolipid-cholesterol microdomains. Curr. Opin. Cell Biol. 9, 534-542.
17. Harris D. A. (1999) Cellular biology of prion diseases. Clin. Microbiol. Rev. 12, 429-444.
18. Henke R. C., Seeto G. S. and Jeffrey P. L. (1997) Thy-1 and AvGp50 signal transduction complex in the avian nervous system: c-Fyn and G α in protein association and activation of signaling pathways. J. Neurosci. Res. 49, 655-670.
19. Hornshaw M. P., McDermott J. R., Candy J. M. and Lakey J. H. (1995) Copper binding to the N-terminal tandem repeat region of mammalian and avian prion protein: structural studies using synthetic peptides.
20. IUPAC-IUBMB Joint Commission on Biochemical Nomenclature. (1997) Nomenclature of glycolipids. Pure Appl. Chem. 69, 2475-2487;
21. (1998) Carbohydr. Res. 312, 167-175.
22. Kaneko K., Vey M., Scott M., Pikuhn S., Cohen F. E. and Prusiner S. B. (1997) COOH-terminal sequence of the cellular prion protein directs subcellular trafficking and controls conversion into the scrapie isoform. Proc. Natl Acad. Sci. USA 94, 2333-2338.
23. Kasahara K. and Sanai Y. (1999) Possible roles of glycosphingolipids in lipid rafts. Bioph. Chem. 82, 121-127.
24. Kasahara K. and Sanai Y. (2000) Functional roles of glycosphingolipids in signal transduction via lipid rafts. Glycoconjugate J. 17, 153-162.
25. Kasahara K., Watanabe Y., Yamamoto T. and Sanai Y. (1997) Association of Src family tyrosine kinase Lyn with ganglioside GD3 in rat brain. Possible regulation of Lyn by glycosphingolipid in caveolae-like domains. J. Biol. Chem. 272, 29 947-29 953.
26. Kasahara K., Watanabe K., Takeuchi K., Kaneko H., Oohira A., Yamamoto T. and Sanai Y. (2000) Involvement of gangliosides in glycosylphosphatidylinositol- anchored neuronal cell adhesion molecule TAG-1 signaling in lipid rafts. J. Biol. Chem. 275, 34 701-34 709.
27. Kasahara K., Watanabe K., Kozutsumi Y., Oohira A., Yamamoto T. and Sanai Y. (2002) Association of GPI-anchored protein TAG-1 with Src-family kinase Lyn in lipid rafts of cerebellar granule cells. Neurochem. Res. 27, 823-829.
28. Keshet G. I., Bar-Peled O., Yaffe D., Nudel U. and Gabizon R. (2000) The cellular prion protein co-localizes with the dystroglycan complex in the brain. J. Neurochem. 75, 1889-1897.
29. Kramer E. M., Klein C., Koch T., Boytinck M. and Trotter J. (1999) Compartmentation of Fyn kinase with glycosylphosphatidylinositol-anchored molecules in oligodendrocytes facilitates kinase activation during myelination. J. Biol. Chem. 274, 29 042-29 049.
30. Kretzschmar H. A., Prusiner S. B., Stowring L. E. and DeArmond S. J. (1986) Scrapie prion proteins are synthesized in neurons. Am. J. Pathol. 122, 1-5.
31. Liang X., Nazarian A., Erdjument-Bromage H., Bornmann W., Tempst P. and Resh M. D. (2001) Heterogeneous fatty acylation of Src family kinases with polyunsaturated fatty acids regulates raft localization and signal transduction. J. Biol. Chem. 276, 30 987-30 994.
32. Loberto N., Prioni S., Prinetti A., Ottico E., Chigorno V., Karagogeos D. and Sonnino S. (2003) The adhesion protein TAG-1 has a ganglioside environment in the sphingolipid-enriched membrane domains of neuronal surface. J. Neurochem. 85, 224-233.
33. Madore N., Smith K. L., Graham C. H., Jen A., Brady K., Hall S. and Morris R. (1999) Functionally different GPI proteins are organized in different domains on the neuronal surface. EMBO J. 18, 6917-6926.
34. Mahfoud R., Garmy N., Maresca M., Yahi N., Puigserver A. and Fantini J. (2002) Identification of a common sphingolipid-binding domain in Alzheimer, prion, and HIV-1 proteins. J. Biol. Chem. 277, 11 292-11 296.
35. Mangé A., Milhavet O., McMahon H. E., Cassanova D. and Lehmann S. (2000) Effect of amphotericin on wild-type and mutated prion proteins in cultured cells: putative mechanism of action in transmissible spongiform encephalopathies. J. Neurochem. 74, 754-762.
36. Mangé A., Milhavet O., Umlauf D., Harris D. and Lehmann S. (2002) PrP-dependent cell adhesion in N2a neuroblastoma cells. FEBS Lett. 514, 159-162.
37. Morris R. (1992) Thy-1, the enigmatic extrovert on the neuronal surface. Bioassays 14, 715-722.
38. Mouillet-Richard S., Ermonval M., Chebassier C., Laplanche J. L., Lehmann S., Launay J. M. and Kellermann O. (2000) Signal transduction through prion protein. Science 289, 1925-1928.
39. Mujheriee A., Arnaud L. and Cooper J. A. (2003) Lipid-dependent recruitment of neuronal Src to lipid rafts. J. Biol. Chem. 278, 40 806-40 814.
40. Muniz M. and Riezman H. (2000) Intracellular transport of GPI-anchored proteins. EMBO J. 19, 10-15.
41. Nagai Y. and Tsuji S. (1994) Significance of ganglioside-mediated glycosignal transduction in neuronal differentiation and development. Prog. Brain Res. 101, 119-126.
42. Naslavsky N., Stein R., Yanai A., Friedlander G. and Taraboulos A. (1997) Characterization of detergent-insoluble complexes containing the cellular prion protein and its scrapie isoform. J. Biol. Chem. 272, 6324-6331.
43. Naslavsky N., Shmeeda H., Friedlander G., Yanai A., Futerman A. H., Barenholz Y. and Taraboulos A. (1999) Sphingolipid depletion increases formation of the scrapie prion protein in neuroblastoma cells infected with prions. J. Biol. Chem. 274, 20 763-20 771.
44. Ottico E., Prinetti A., Prioni S., Giannotta C., Basso L., Chigorno V. and Sonnino S. (2003) Dynamics of membrane lipid domains in neuronal granule cells differentiated in culture. J. Lipid Res. 44, 2142-2151.
45. Paladino S., Samataro D. and Zurzolo C. (2002) Detergent-resistant membrane microdomains and apical sorting of GPI-anchored proteins in polarized epithelial cells. Int. J. Med. 29, 439-445.
46. Pauly P. C. and Harris D. A. (1998) Copper stimulates endocytosis of the prion protein. J. Biol. Chem. 273, 33 107-33 110.
47. Prinetti A., Chigorno V., Tettamanti G. and Sonnino S. (2000a) Sphingolipid-enriched membrane domains from rat cerebellar granule cells differentiated in culture. A compositional study. J. Biol. Chem. 275, 11 658-11 665.
48. Prinetti A., Marano N., Prioni S., Chigorno V., Mauri L., Casellato R., Tettamanti G. and Sonnino S. (2000b) Association of Src-family protein tyrosine kinases with sphingolipids in rat cerebellar granule cells differentiated in culture. Glycoconjugate J. 17, 223-232.
49. Prinetti A., Prioni S., Chigorno S., Karagogeos D., Tettamanti G. and Sonnino S. (2001a) Immunoseparation of sphingolipid-enriched membrane domains enriched in Src family protein tyrosine kinases and in the neuronal adhesion molecule TAG-1 by anti-GD3 ganglioside monoclonal antibody. J. Neurochem. 78, 1162-1167.
50. Prinetti A., Chigorno V., Prioni S., Loberto N., Marano N., Tettamanti G. and Sonnino S. (2001b) Changes in the lipid turnover, composition and organization, as sphingolipid-enriched membrane domains, in rat cerebellar granule cells developing in vitro. J. Biol. Chem. 276, 21 136-21 145.
51. Prusiner S. B. (1991) Molecular biology of prion diseases. Science 252, 1515-1522.
52. Prusiner S. B. (1998) Prions. Proc. Natl Acad. Sci. USA 95, 13 363-13 383.
53. Robinson P. J. (1997) Signal transduction via GPI-anchored membrane proteins. Adv. Exp. Med. Biol. 419, 365-370.
54. Sanghera N. and Pinheiro T. J. T. (2002) Binding of prion protein to lipid membranes and implications for prion conversion. J. Mol. Biol. 315, 1241-1256.
55. c association with lipid rafts in the early secretory pathway stabilizes its cellular conformation. Mol. Biol. Cell 15, 4031-4042.
56. Shyng S. L., Huber M. T. and Harris D. A. (1993) A prion protein cycles between the cell surface and an endocytic compartment in cultured neuroblastoma cells. J. Biol. Chem. 268, 15 922-15 928.
57. Simons K. and Ikonen E. (1997) Functional rafts in cell membranes. Nature 387, 569-572.
58. Spielhauter C. and Schaltz H. M. (2001) PrPc directly interacts with proteins involved in signaling pathways. J. Biol. Chem. 276, 44 604-44 612.
59. Stahl N., Borchelt D. R., Hsiao K. and Prusiner S. B. (1987) Scrapie prion protein contains a phosphatidylinositol glycolipid. Cell 51, 229-240.
60. Stockel J., Safar J., Wallace A. C., Cohen F. E. and Prusiner S. B. (1998) Prion protein selectively binds copper (II) ions. Biochemistry 37, 7185-7193.
61. Sunyach C., Jen A., Deng J., Fitzgerald K., Frobert Y., McCaffrey M. and Morris R. J. (2003) The mechanism of internalization of glycosylphosphatidylinositol-anchored prion protein. EMBO J. 22, 3591-3601.
62. Svennerholm L. (1980) Ganglioside designation. Adv. Exp. Med. Biol. 125, 11.
63. Taraboulos A., Scott M., Semenov A., Avraham D., Laszlo L. and Prusiner S. B. (1995) Cholesterol depletion and modification of COOH-terminal targeting sequence of the prion protein inhibit formation of the scrapie isoform. J. Cell Biol. 129, 121-132.
64. Tettamanti G., Bonali F., Marchesini S. and Zambotti V. (1973) Parallelism of subcellular location of major particulate neuroaminidase and ganglioside in rabbit brain cortex. Biochim. Biophys. Acta 296, 160-170.
65. 3H. J. Labeled Compd. Radiopharm. 29, 567-574.
66. Varma R. and Mayor S. (1998) GPI-anchored proteins are organized in submicron domains at the cell surface. Nature 394, 798-801.
67. Vaskovsky V. E. and Kostetsky E. Y. (1968) Modified spray for the detection of phospholipids on thin-layer chromatograms. J. Lipid Res. 9, 396.
68. Vey M., Pikuhn S., Wille H., Nixon R., DeArmond S. J., Smart E. J., Anderson R. G., Taraboulos A. and Prusiner S. B. (1996) Subcellular localization of the cellular and scrapie prion proteins in caveolae-like membranous domains. Proc. Natl Acad. Sci. USA 93, 14 945-14 949.
69. Wu C., Butz S., Ying Y. and Anderson R. G. W. (1997) Tyrosine kinase receptors concentrated in caveolae-like domains from neuronal plasma membrane. J. Biol. Chem. 272, 3554-3559.