Dynamics of membrane lipid domains in neuronal cells differentiated in culture

Journal of Lipid Research

Volumn 44, Issue 11, 2003, Pages 2142-2151

  Ottico, Elena ^a   Prinetti, Alessandro ^a   Prioni, Simona ^a   Giannotta, Claudia ^a   Basso, Luisa ^a   Chigorno, Vanna ^a   Sonnino, Sandro ^a  

^a UNIVERSITY OF MILAN   (Italy)

Author keywords

Cholesterol; Cyclodextrin; Ganglioside; Sphingolipid enriched membrane domain; Sphingomyelin

Indexed keywords

C SRC PROTEIN; CHOLESTEROL; LIPID; MEMBRANE LIPID; METHYL BETA CYCLODEXTRIN; PHOSPHATIDYLCHOLINE; PROTEIN; PROTEIN KINASE LYN; SPHINGOLIPID; TRITON X 100; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DEATH; CELL DIFFERENTIATION; CEREBELLUM CORTEX; CHOLESTEROL TRANSPORT; CONTROLLED STUDY; DOSE TIME EFFECT RELATION; GRANULE CELL; LIPID ANALYSIS; LIPID DOMAIN; MEMBRANE DOMAIN; MEMBRANE LIPID DOMAIN; MEMBRANE PERMEABILITY; NERVE CELL CULTURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN TARGETING; RAT; SIGNAL TRANSDUCTION;

ANIMALS; BETA-CYCLODEXTRINS; CELL DIFFERENTIATION; CELL SURVIVAL; CELLS, CULTURED; CEREBELLUM; CHOLESTEROL; CYCLODEXTRINS; GLYCEROPHOSPHOLIPIDS; GLYCOSPHINGOLIPIDS; NEURONS; PHOSPHATIDYLCHOLINES; PROTEIN TRANSPORT; RATS; RATS, SPRAGUE-DAWLEY;

EID: 0345098359     PISSN: 00222275     EISSN: None     Source Type: Journal    
DOI: 10.1194/jlr.M300247-JLR200     Document Type: Article

References (50)

1. Simons, K., and D. Toomre. 2000. Lipid rafts and signal transduction. Nat. Rev. Mol. Cell Biol. 1: 31-39.
2. Hakomori, S., K. Handa, K. Iwabuchi, S. Yamamura, and A. Prinetti. 1998. New insights in glycosphingolipid function: "glycosignaling domain," a cell surface assembly of glycosphingolipids with signal transducer molecules, involved in cell adhesion coupled with signaling. Glycobiology. 8: xi-xix.
3. Brown, D. A., and E. London. 1998. Functions of lipid rafts in biological membranes. Annu. Rev. Cell Dev. Biol. 14: 111-136.
4. Prinetti, A., K. Iwabuchi, and S. Hakomori. 1999. Glycosphingolipid-enriched signaling domain in mouse neuroblastoma Neuro2a cells. Mechanism of ganglioside-dependent neuritogenesis. J. Biol. Chem. 274: 20916-20924.
5. Madore, N., K. L. Smith, C. H. Graham, A. Jen, K. Brady, S. Hall, and R. Morris. 1999. Functionally different GPI proteins are organized in different domains on the neuronal surface. EMBO J. 18: 6917-6926.
6. Bilderback, T. R., V. R. Gazula, M. P. Lisanti, and R. T. Dobrowsky. 1999. Caveolin interacts with Trk A and p75NTR and regulates neurotrophin signaling pathways. J. Biol. Chem. 274: 257-263.
7. Prinetti, A., N. Marano, S. Prioni, V. Chigorno, L. Mauri, R. Casellato, G. Tettamanti, and S. Sonnino. 2000. Association of Src-family protein tyrosine kinases with sphingolipids in rat cerebellar granule cells differentiated in culture. Glycoconj. J. 17: 223-232.
8. Prinetti, A., V. Chigorno, G. Tettamanti, and S. Sonnino. 2000. Sphingolipid-enriched membrane domains from rat cerebellar granule cells differentiated in culture. A compositional study. J. Biol. Chem. 275: 11658-11665.
9. Prinetti, A., V. Chigorno, S. Prioni, N. Loberto, N. Marano, G. Tettamanti, and S. Sonnino. 2001. 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: 21136-21145.
10. Prinetti, A., S. Prioni, S. Chigorno, D. Karagogeos, G. Tettamanti, and S. Sonnino. 2001. 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.
11. Loberto, N., S. Prioni, A. Prinetti, E. Ottico, S. Chigorno, D. Karagogeos, and S. Sonnino. 2003. The adhesion protein TAG-1 has a ganglioside environment in the sphingolipid-enriched membrane domains of neuronal cells in culture. J. Neurochem. 85: 224-233.
12. Prioni, S., N. Loberto, A. Prinetti, S. Chigorno, F. Guzzi, R. Maggi, M. Parenti, and S. Sonnino. 2002. Sphingolipid metabolism and caveolin expression in gonadotropin-releasing hormone-expressing GN11 and gonadotropin-releasing hormone-secreting GT1-7 neuronal cells. Neurochem. Res. 27: 831-840.
13. Kasahara, K., Y. Watanabe, T. Yamamoto, and Y. Sanai. 1997. Caveolin interacts with Trk A and p75NTR and regulates neurotrophin signaling pathways. J. Biol. Chem. 272: 29947-29953.
14. Kasahara, K., Y. Watanabe, K. Takeuchi, H. Kaneko, A. Ooohira, T. Yamamoto, and Y. Sanai. 2000. 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. 275: 34701-34709.
15. 1-induced sphingolipid depletion inhibits vitamin uptake via the glycosylphosphatidylinositol-anchored folate receptor. J. Biol. Chem. 272: 18020-18024.
16. Naslavsky, N., H. Shmeeda, G. Friedlander, A. Yanai, A. H. Futerman, Y. Barenholz, and A. Taraboulos. 1999. Sphingolipid depletion increases formation of the scrapie prion protein in neuroblastoma cells infected with prions. J. Biol. Chem. 274: 20763-20771.
17. Sheets, E. D., G. M. Lee, R. Simson, and K. Jacobson. 1997. Transient confinement of a glycosylphosphatidylinositol-anchored protein in the plasma membrane. Biochemistry. 36: 12449-12458.
18. Inokuchi, J., S. Uemura, K. Kabayama, and Y. Igarashi. 2000. Glycosphingolipid deficiency affects functional microdomain formation in Lewis lung carcinoma cells. Glycoconj. J. 17: 239-246.
19. Taraboulos, A., M. Scott, A. Semenov, D. Avraham, L. Laszlo, and S. B. Prusiner. 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.
20. Ledesma, M. D., K. Simons, and C. G. Dotti. 1998. Neuronal polarity: essential role of protein-lipid complexes in axonal sorting. Proc. Natl. Acad. Sci. USA. 95: 3966-3971.
21. Simons, M., P. Keller, B. De Strooper, K. Beyreuther, C. G. Dotti, and K. Simons. 1998. Cholesterol depletion inhibits the generation of beta-amyloid in hippocampal neurons. Proc. Natl. Acad. Sci. USA. 95: 6460-6464.
22. Neufeld, E. B., A. M. Cooney, J. Pitha, E. A. Dawidowicz, N. K. Dwyer, P. G. Pentchev, and E.J. Blanchette-Mackie. 1996. Intracellular trafficking of cholesterol monitored with a cyclodextrin. J. Biol. Chem. 271: 21604-21613.
23. Furuchi, T., and R. G. W. Anderson. 1998. Cholesterol depletion of caveolae causes hyperactivation of extracellular signal-related kinase ERK. J. Biol. Chem. 273: 21099-21104.
24. Ilangumaran, S., and D. C. Hoessli. 1998. Effects of cholesterol depletion by cyclodextrin on the sphingolipid microdomains of the plasma membrane. Biochem. J. 335: 433-440.
25. Sheets, E. D., D. Holowka, and 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.
26. Fukasawa, M., M. Nishijima, H. Itabe, T. Takano, and K. Hanada. 2000. Reduction of sphingomyelin level without accumulation of ceramide in Chinese hamster ovary cells affects detergent-resistant membrane domains and enhances cellular cholesterol efflux to methyl-beta-cyclodextrin. J. Biol. Chem. 275: 34028-34034.
27. Shogomori, H., and A. H. Futerman. 2001. Cholera toxin is found in detergent-insoluble rafts/domains at the cell surface of hippocampal neurons but is internalized via a raft-independent mechanism. J. Biol. Chem. 276: 9182-9188.
28. Mendez, A. J., G. Lin, D. P. Wade, R. M. Lawn, and J. F. Oram. 2001. Membrane lipid domains distinct from cholesterol/sphingomyelin-rich rafts are involved in the ACA1-mediated lipid secretory pathway. J. Biol. Chem. 276: 3158-3166.
29. Kilsdonk, E. P. C., P. G. Yancey, G. W. Stoudt, F. W. Bangerter, W. J. Johnson, M. C. Phillips, and G. H. Rothblat. 1995. Cellular cholesterol efflux mediated by cyclodextrins. J. Biol. Chem. 270: 17250-17256.
30. Hansen, G. H., L. Immerdal, E. Thorsen, L-L. Niels-Christiansen, B. T. Nystrom, E. J. F. Demant, and E. M. Danielsen. 2001. Lipid rafts exist as stable cholesterol-independent microdomains in the brush border membrane of enterocytes. J. Biol. Chem. 276: 32338-32344.
31. Singh, I., and Y. Kishimoto. 1983. Effect of cyclodextrins on the solubilization of lignoceric acid, ceramide, and cerebroside, and on the enzymatic reactions involving these compounds. J. Lipid Res. 24: 662-665.
32. Casu, B., A. Grenni, A. Naggi, G. Torri, M. Virtuani, and B. Focher. 1990. Interaction of cyclodextrinscyclomalto-oligosaccharides with glycolipids: N.M.R. studies of aqueous system of cyclomaltohexaose and alkyl glycosides. Carbohydr. Res. 200: 101-109.
33. Shiraishi, T., M. Hiraiwa, and Y. Uda. 1993. Effects of cyclodextrins on the hydrolysis of ganglioside GM1 by acid beta-galactosidases. Glycoconj. J. 10: 170-174.
34. Carter, H. E., J. A. Rothfus, and R. Gigg. 1961. Biochemistry of the sphingolipids: XII. Conversion of cerebrosides to ceramides and sphingosine; structure of Gaucher cerebroside. J. Lipid Res. 2: 228-234.
35. Tettamanti, G., F. Bonali, S. Marchesini, and V. Zambotti. 1973. Parallelism of subcellular location of major particulate neuraminidase and gangliosides in rabbit brain cortex. Biochim. Biophys. Acta. 296: 160-170.
36. 3H. J. Label. Compd. Radiopharm. 29: 567-574.
37. Gallo, V., M. Ciotti, A. Coletti, F. Aloisi, and G. Levi. 1982. Selective release of glutamate from cerebellar granule cells differentiating in culture. Proc. Natl. Acad. Sci. USA. 79: 7919-7923.
38. Thangnipon, W., A. Kingsbury, M. Webb, and R. Balazs. 1983. Observations on rat cerebellar cells in vitro: influence of substratum, potassium concentration and relationship between neurones and astrocytes. Brain Res. 11: 177-189.
39. Kingsbury, A. E., V. Gallo, P. L. Woodhams, and R. Balazs. 1985. Survival, morphology and adhesion properties of cerebellar interneurones cultured in chemically defined and serum-supplemented medium. Brain Res. 17: 17-25.
40. Balasz, R., V. Gallo, and A. Kingsbury. 1988. Effect of depolarization on the maturation of cerebellar granule cells in culture. Brain Res. 468: 269-276.
41. Rizzardini, M., M. Lupi, S. Bernasconi, A. Mangolini, and L. Cantoni. 2002. Mitochondrial dysfunction and death in motor neurons exposed to the glutathione-depleting agent ethacrynic acid. J. Neurol. Sci. 207: 51-58.
42. van Echten, G., H. Iber, H. Stotz, A. Takatsuki, and K. Sandhoff. 1990. Uncoupling of ganglioside biosynthesis by Brefeldin A. Eur. J. Cell Biol. 51: 135-139.
43. Vaskovsky, V. E., and E. Y. Kostetsky. 1968. Modified spray for the detection of phospholipids on thin-layer chromatograms. J. Lipid Res. 9: 396.
44. Klein, T. R., D. Kirsch, R. Kaufmann, and D. Riesner. 1998. Prion rods contain small amounts of two host sphingolipids as revealed by thin-layer chromatography and mass spectrometry. Biol. Chem. 379: 655-666.
45. Lowry, O. H., N. J. Rosebrough, A. L. Farr, and R. J. Randall. 1951. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193: 265-275.
46. Ahmed, S. M., B. Casu, A. Cedro, M. Guerrini, E. Lanzarotti, D. Moltrasio, A. Naggi, and G. Torri. 1994. Disruption of micellar aggregates of ganglioside GM-1 by complexation with α-cyclodextrin. Int. J. Pharm. 109: 99-106.
47. Pascher, I. 1976. Molecular arrangements in sphingolipids. Conformation and hydrogen bonding of ceramide and their implication on membrane stability and permeability. Biochim. Biophys. Acta. 455: 433-451.
48. Riboni, L., R. Bassi, A. Prinetti, and G. Tettamanti. 1996. Salvage of catabolic products in ganglioside metabolism: a study on rat cerebellar granule cells in culture. FEBS Lett. 391: 336-340.
49. Ladisch, S., R. Li, and E. Olson. 1994. Ceramide structure predicts tumor ganglioside immunosuppressive activity. Proc. Natl. Acad. Sci. USA. 91: 1974-1978.
50. Sonnino, S., L. Cantù, M. Corti, D. Acquotti, and B. Venerando. 1994. Aggregative properties of gangliosides in solution. Chem. Phys. Lipids. 71: 21-45.