Two types of detergent-insoluble, glycosphingolipid/cholesterol-rich membrane domains from isolated myelin

Journal of Neurochemistry

Volumn 94, Issue 6, 2005, Pages 1696-1710

  Arvanitis, Dina N ^a,b   Min, Weixian ^b   Gong, Yanping ^a,b   Heng, Yew M ^b   Boggs, Joan M ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b HOSPITAL FOR SICK CHILDREN   (Canada)

Author keywords

Caveolin; Cerebroside sulfate; Cytoskeleton; Galactosylceramide; Oligodendrocytes; Rafts

Indexed keywords

ACTIN; CAVEOLIN; CHOLESTEROL; CYTOSKELETON PROTEIN; DETERGENT; EDETIC ACID; FLOTILLIN 1; GALACTOSYLCERAMIDE; GLYCOSPHINGOLIPID; ISOPROTEIN; MYELIN; MYELIN BASIC PROTEIN; NERVE CELL ADHESION MOLECULE; NERVE CELL ADHESION MOLECULE 120; PHOSPHOTRANSFERASE; SODIUM CHLORIDE; SODIUM DIHYDROGEN PHOSPHATE; SULFATIDE; TRITON X 100; TROMETAMOL; TUBULIN; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOSKELETON; ENZYME ACTIVITY; EXTRACTION; LIPID ANALYSIS; LIPID RAFT; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN LIPID INTERACTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; SOLUBILITY; SUCROSE DENSITY GRADIENT CENTRIFUGATION;

ACTINS; ANIMALS; AXONS; BRAIN; CATTLE; CAVEOLIN 1; CAVEOLINS; CHOLESTEROL; CYTOSKELETON; DETERGENTS; G(M1) GANGLIOSIDE; GALACTOSYLCERAMIDES; GLYCOSPHINGOLIPIDS; MEMBRANE MICRODOMAINS; MEMBRANE PROTEINS; MICROSCOPY, ELECTRON, TRANSMISSION; MYELIN SHEATH; NEURAL CELL ADHESION MOLECULES; OCTOXYNOL; SIGNAL TRANSDUCTION; SOLUBILITY; SUBCELLULAR FRACTIONS; TUBULIN;

EID: 24944525686     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2005.03331.x     Document Type: Article

References (89)

1. Anderson R. G. (1993) Caveolae: where incoming and outgoing messengers meet. Curr. Opin. Cell Biol. 5, 647-652.
2. Arvanitis D. N. (2004) Protein and lipid assemblies in bovine brain myelin. PhD Thesis. University of Toronto, Toronto.
3. Arvanitis D. N., Yang W. and Boggs J. M. (2002) Myelin proteolipid protein, basic protein, the small isoform of myelin-associated glycoprotein, and p42MAPK are associated in the Triton X-100 extract of central nervous system myelin. J. Neurosci. Res. 70, 8-23.
4. Arvanitis D. N., Wang H., Bagshaw R. D., Callahan J. W. and Boggs J. M. (2004) Membrane-associated estrogen receptor and caveolin-1 are present in central nervous system myelin. J. Neurosci. Res. 75, 603-613.
5. Bading H. and Greenberg M. E. (1991) Stimulation of protein tyrosine phosphorylation by NMDA receptor activation. Science 253, 912-914.
6. Baird B., Sheets E. D. and Holowka D. (1999) How does the plasma membrane participate in cellular signalling by receptors for immunoglobulin E? Biophys. Chem. 82, 109-119.
7. Bambrick L. L. and Braun P. E. (1991) Phosphorylation of myelin-associated glycoprotein in cultured oligodendrocytes. Dev. Neurosci. 13, 412-416.
8. Berkelman T. and Stenstedt T. (1998) 2-D Electrophoresis Using Immobilized pH Gradients. Principles and Methods. Amersham Pharmacia Biotech Inc., Piscataway.
9. Bhat N. R. and Zhang P. (1996) Activation of mitogen-activated protein kinases in oligodendrocytes. J. Neurochem. 66, 1986-1994.
10. Bickel P. E., Scherer P. E., Schnitzer J. E., Oh P., Lisanti M. P. and Lodish H. F. (1997) Flotillin and epidermal surface antigen define a new family of caveolae-associated integral membrane proteins. J. Biol. Chem. 272, 13 793-13 802.
11. Boggs J. M., Wood D. D., Moscarello M. A. and Papahadjopoulos D. (1977) Lipid phase separation induced by a hydrophobic protein in phosphatidylserine- phosphatidylcholine vesicles. Biochemistry 16, 2325-2329.
12. Boggs J. M., Hashim G. A., Day E. D. and Moscarello M. A. (1985) Lipid-induced recognition of a conformational determinant (residues 65-83) in myelin basic protein. J. Immunol. 135, 2617-2622.
13. Boulton T. G., Nye S. H., Robbins D. J., Ip N. Y., Radziejewska E., Morgenbesser S. D., DePinho R. A., Panayotatos N., Cobb M. H. and Yancopoulos G. D. (1991) ERKs: a family of protein-serine/ threonine kinases that are activated and tyrosine phosphorylated in response to insulin and NGF. Cell 65, 663-675.
14. Braccia A., Villani M., Immerdal L., Niels-Christiansen L. L., Nystrom B. T., Hansen G. H. and Danielsen E. M. (2003) Microvillar membrane microdomains exist at physiological temperature. Role of galectin-4 as lipid raft stabilizer revealed by 'superrafts'. J. Biol. Chem. 278, 15 679-15 684.
15. 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.
16. Brown M. C., Moreno M. B., Bongarzone E. R., Cohen P. D., Soto E. F. and Pasquini J. M. (1993) Vesicular transport of myelin proteolipid and cerebroside sulfates to the myelin membrane. J. Neurosci. Res. 35, 402-408.
17. Cabrera O. E. E., Bongiovanni G., Hallak M., Soto E. F. and Pasquini J. M. (2000) The cytoskeletal components of the myelin fraction are affected by a single intracranial injection of apotransferrin in young rats. Neurochem. Res. 25, 669-676.
18. De Angelis D. A. and Braun P. E. (1994) Isoprenylation of brain 2′,3′-cyclic nucleotide 3′-phosphodiesterase modulates cell morphology. J. Neurosci. Res. 39, 386-397.
19. Drevot P., Langlet C., Guo X.-J., Bernard A.-M., Colard O., Chauvin J.-P., Lasserre R. and He H.-T. (2002) TCR signal initiation machinery is pre-assembled and activated in a subset of membrane rafts. EMBO J. 21, 1899-1908.
20. Erickson A. K., Payne D. M., Martino P. A., Rossomando A. J., Shabanowitz J., Weber M. J., Hunt D. F. and Sturgill T. W. (1990) Identification by mass spectrometry of threonine 97 in bovine myelin basic protein as a specific phosphorylation site for mitogen-activated protein kinase. J. Biol. Chem. 265, 19 728-19 735.
21. Foger N., Marhaba R. and Zoller M. (2000) CD44 supports T cell proliferation and apoptosis by apposition of protein kinases. Eur. J. Immunol. 10, 2888-2899.
22. Geiger B. and Bershadsky A. (2001) Assembly and mechanosensory function of focal contacts. Curr. Opin. Cell Biol. 13, 584-592.
23. Gillespie C. S., Wilson R., Davidson A. and Brophy P. J. (1989) Characterization of a cytoskeletal matrix associated with myelin from rat brain. Biochem. J. 260, 689-696.
24. Gomez-Mouton C., Abad J. L., Mira E., Lacalle R. A., Gallardo E., Jimenez-Baranda S., Ilia L, Bernad A., Manes S. and Martinez A. C. (2001) Segregation of leading-edge and uropod components into specific lipid rafts during T cell polarization. Proc. Natl Acad. Sci. USA 98, 9642-9647.
25. Gudz T. I., Schneider T. E., Haas T. A. and Macklin W. B. (2002) Myelin proteolipid protein forms a complex with integrins and may participate in integrin receptor signaling in oligodendrocytes. J. Neurosci. 22, 7398-7407.
26. van der Haar M. E., Visser H. W., de Vries H. and Hoekstra D. (1998) Transport of proteolipid protein to the plasma membrane does not depend on glycosphingolipid cotransport in oligodendrocyte cultures. J. Neurosci. Res. 51, 371-381.
27. Hakomori S. (2000) Cell adhesion/recognition and signal transduction through glycosphingolipid microdomain. Glycoconj. J. 17, 143-151.
28. 2+. Biochim. Biophys. Acta 1223, 375-382.
29. Harder T. and Simons K. (1997) Caveolae, DIGs, and the dynamics of sphingolipid-cholesterol microdomains. Curr. Opin. Cell Biol. 4, 534-542.
30. He Q. and Meiri K. F. (2002) Isolation and characterization of detergent-resistant microdomains responsive to NCAM-mediated signaling from growth cones. Mol. Cell. Neurosci. 19, 18-31.
31. Holowka D., Sheets E. D. and Baird B. (2000) Interactions between Fc(epsilon) RI and lipid raft components are regulated by the actin cytoskeleton. J. Cell Sci. 113, 1009-1019.
32. Horvath L. I., Brophy P. J. and Marsh D. (1990) Influence of polar residue deletions on lipid-protein interactions with the myelin proteolipid protein. Spin-label ESR studies with DM-20/lipid recombinants. Biochemistry 29, 2635-2638.
33. Iwabuchi K., Handa K. and Hakomori S. (1998) 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. 273, 33 766-33 773.
34. James M., Nuttall A., Ilsley J. L., Ottersbach K., Tinsley J. M., Sudol M. and Winder S. J. (2000) Adhesion-dependent tyrosine phosphorylation of (beta)-dystroglycan regulates its interaction with utrophin. J. Cell Sci. 113, 1717-1726.
35. Jaramillo M. L., Afar D. E., Almazan G. and Bell J. C. (1994) Identification of tyrosine 620 as the major phosphorylation site of myelin-associated glycoprotein and its implication in interacting with signalling molecules. J. Biol. Chem. 269, 27 240-27 245.
36. Johns T. G. and Bernard C. C. (1999) The structure and function of myelin oligodendrocyte glycoprotein. J. Neurochem. 72, 1-9.
37. Karthigasan J., Kosaras B., Nguyen J. and Kirschner D. A. (1994) Protein and lipid composition of radial component-enriched CNS myelin. J. Neurochem. 62, 1203-1213.
38. Kim . P., Lee J. Y., Jeong J. K., Bae S. W., Lee H. K. and Jo I. (1999) Nongenomic stimulation of nitric oxide release by estrogen is mediated by estrogen receptor alpha localized in caveolae. Biochem. Biophys. Res. Commun. 263, 257-262.
39. Kim T. and Pfeiffer S. E. (1999) Myelin glycosphingolipid/cholesterol- enriched microdomains selectively sequester the non-compact myelin proteins CNP and MOG. J. Neurocytol. 28, 281-293.
40. Klein C., Kramer E. M., Gardine A. M., Schraven B., Brandt R. and Trotter J. (2002) Process outgrowth of oligodendrocytes is promoted by interaction of fyn kinase with the cytoskeletal protein tau. J. Neurosci. 22, 698-707.
41. Kramer E. M., Koch T., Niehaus A. and Trotter J. (1997) Oligodendrocytes direct glycosyl phosphatidylinositol-anchored proteins to the myelin sheath in glycosphingolipid-rich complexes. J. Biol. Chem. 272, 8937-8945.
42. 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.
43. Kursula P., Lehto V. P. and Heape A. M. (2001) The small myelin-associated glycoprotein binds to tubulin and microtubules. Mol. Brain Res. 87, 22-30.
44. Laemmli U.K., Beuin F. and Gujer-Kellenberger G. (1970) A factor preventing the major head protein of bacteriophage T4 from random aggregation. J. Mol. Biol. 47, 69-85.
45. Larocca J. N. and Almazan G. (1997) Acetylcholine agonists stimulate mitogen-activated protein kinase in oligodendrocyte progenitors by muscarinic receptors. J. Neurosci. Res. 50, 743-754.
46. Levin E. R. (2002) Cellular functions of plasma membrane estrogen receptors. Steroids 67, 471-475.
47. Lisanti M. P., Scherer P. E., Viugirene J., Tang Z., Hermanowski-Vosatka A., Tu Y.-H., Cook R. F. and Sargiacomo M. (1994) Characterization of caveolin-rich membrane domains isolated from an endothelial-rich source: implications for human disease. J. Cell Biol. 126, 111-126.
48. Liu H. N., Larocca J. N. and Almazan G. (1999) Molecular pathways mediating activation by kainate of mitogen-activated protein kinase in oligodendrocyte progenitors. Brain Res. Mol. Brain Res. 66, 50-61.
49. London E. and Brown D. A. (2000) Insolubility of lipids in triton X-100: physical origin and relationship to sphingolipid/cholesterol membrane domains (rafts). Biochim. Biophys. Acta 1508, 182-195.
50. 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, 6917-6912.
51. Marta C. B., Ortiz E. H., Hallak M., Baron B., Guillou F., Zakin M. M., Soto E. F. and Pasquini J. M. (2002) Changes in the expression of cytoskeletal proteins in the CNS of transferrin transgenic mice. Dev. Neurosci. 24, 242-251.
52. Marta C. B., Taylor C. M., Coetzee T., Kim T., Winkler S., Bansal R. and Pfeiffer S. E. (2003) Antibody cross-linking of myelin oligodendrocyte glycoprotein leads to its rapid repartitioning into detergent-insoluble fractions, and altered protein phosphorylation and cell morphology. J. Neurosci. 23, 5461-5471.
53. Martenson R. E., Law M. J. and Deibler G. E. (1983) Identification of multiple in vivo phosphorylation sites in rabbit myelin basic protein. J. Biol. Chem. 258, 930-937.
54. Maruyama M., Sudo T., Kasuya Y., Shiga T., Hu B. and Osada H. (2000) Immunolocalization of p38 MAP kinase in mouse brain. Brain Res. 887, 350-358.
55. Melkonian K. A., Ostermeyer A. G., Chen J. Z., Roth M. G. and Brown D. A. (1999) Role of lipid modifications in targeting proteins to detergent-resistant membrane rafts. Many raft proteins are acylated, while few are prenylated. J. Biol. Chem. 274, 3910-3917.
56. Messier A. M. and Bizzozero O. A. (2000) Conserved fatty acid composition of proteolipid protein during brain development and in myelin subfractions. Neurochem. Res. 25, 449-455.
57. Mimik J. and Braun P. E. (1996) Differential intracellular sorting of the myelin-associated glycoprotein isoforms. J. Neurosci. Res. 44, 411-420.
58. Morell P. and Quarles R. H. (1999) Myelin formation, structure, and biochemistry, in Basic Neurochemistry: Molecular, Cellular, and Medical Aspects, 6th edn (Siegel G. J., editor-in-chief), pp. 70-90. Lippincott-Raven, New York.
59. Monta K., Sasaki H., Fujimoto K., Furuse M. and Tsukita S. (1999) Claudin-11/OSP-based tight junctions of myelin sheaths in brain and Sertoli cells in testis. J. Cell Biol. 145, 579-588.
60. Nebl T., Pestonjamasp K. N., Leszyk J. D., Crowley J. L., Oh S. W. and Luna E. J. (2002) Proteomic analysis of a detergent-resistant membrane skeleton from neutrophil plasma membranes. J. Biol. Chem. 277, 43 399-43 409.
61. Niethammer P., Delling M., Sytnyk V., Dityatev A., Fukami K. and Schachner M. (2002) Cosignalling of NCAM via lipid rafts and the FGF receptor is required for neuritogenesis. J. Cell Biol. 157, 521-532.
62. Norton W. T. (1977) Isolation and characterization of myelin, in Myelin (Morell P., ed.), pp. 161-200. Plenum Press, New York.
63. Norton W. T. and Poduslo S. E. (1973) Myelination in rat brain: method of myelin isolation. J. Neurochem. 4, 749-757.
64. O'Neill R. C. and Braun P. E. (2000) Selective synthesis of 2′,3′-cyclic nucleotide 3′-phosphodiesterase isoform 2 and identification of specifically phosphorylated serine residues. J. Neurochem. 74, 540-546.
65. Oliferenko S., Paiha K., Harder T., Gerke V., Schwarzler C., Schwarz H., Beug H., Gunthert U. and Huber L. A. (1999) Analysis of CD44-containing lipid rafts: recruitment of annexin II and stabilization by the actin cytoskeleton. J. Cell Biol. 4, 843-854.
66. Olive S., Dubois C., Schachner M. and Rougon G. (1995) The F3 neuronal glycosylphosphatidylinositol-linked molecule is localized to glycolipid-enriched membrane subdomains and interacts with L1 and Fyn kinase in cerebellum. J. Neurochem. 65, 2307-2317.
67. Parkin E. T., Turner A. J. and Hooper N. M. (1996) Isolation and characterization of two distinct low-density, Triton-insoluble, complexes from porcine lung membranes. Biochem. J. 319, 887-896.
68. Parton R. G. and Simons K. (1995) Digging into caveolae. Science 269, 1398-1399.
69. Pedraza L., Owens G. C., Green L. A. and Salzer J. L. (1990) The myelin-associated glycoproteins: membrane disposition, evidence of a novel disulfide linkage between immunoglobulin-like domains, and posttranslational palmitylation. J. Cell Biol. 111, 2651-2661.
70. Pereyra P. M., Horvath E. and Braun P. E. (1988) Triton X-100 extractions of central nervous system myelin indicate a possible role for the minor myelin proteins in the stability in lamellae. Neurochem. Res. 13, 583-595.
71. Peterson G. L. (1977) A simplification of the protein assay method of Lowry et al. which is more generally applicable. Anal. Biochem. 83, 346-356.
72. 2+-calmodulin regulated effectors of microtubule stability in bovine brain. Biochemistry 31, 8849-8855.
73. Quarles R. H. (2002) Myelin sheaths: glycoproteins involved in their formation, maintenance and degeneration. Cell. MoI. Life Sci. 59, 1851-1871.
74. Roper K., Corbeil D. and Huttner W. B. (2000) Retention of prominin in microvilli reveals distinct cholesterol-based lipid micro-domains in the apical plasma membrane. Nat. Cell Biol. 2, 582-592.
75. Schachner M. and Bartsch U. (2000) Multiple functions of the myelin-associated glycoprotein MAG (siglec-4a) in formation and maintenance of myelin. Glia 29, 154-165.
76. Schnitzer J. E., Liu J. and Oh P. (1995a) Endothelial caveolae have the molecular transport machinery for vesicle budding, docking, and fusion including VAMP, NSF, SNAP, annexins, and GTPases. J. Biol. Chem. 270, 14 399-14 404.
77. Schnitzer J. E., McIntosh D. P., Dvorak A. M., Liu J. and Oh P. (1995b) Separation of caveolae from associated microdomains of GPI-anchored proteins. Science 269, 1435-1439.
78. Simons K. and Ikonen E. (1997) Functional rafts in cell membranes. Nature 387, 569-572.
79. Simons M., Kramer E. M., Thiele C., Stoffel W. and Trotter J. (2000) Assembly of myelin by association of proteolipid protein with cholesterol- and galactosylceramide-rich membrane domains. J. Cell Biol. 151, 143-154.
80. Stahlhut M. and van Deurs B. (2000) Identification of filamin as a novel ligand for caveolin-1: evidence for the organization of caveolin-1-associated membrane domains by the actin cytoskeleton. Mol. Biol. Cell 11, 325-337.
81. Stariha R. L. and Kim S. U. (2001) Protein kinase C and mitogen-activated protein kinase signalling in oligodendrocytes. Microsc. Res. Techn. 52, 680-688.
82. Stecca B., Southwood C. M., Gragerov A., Kelley K. A., Friedrich V. L. Jr and Gow A. (2000) The evolution of lipophilin genes from invertebrates to tetrapods: DM-20 cannot replace proteolipid protein in CNS myelin. J. Neurosci. 20, 4002-4010.
83. Taylor C. M., Coetzee T. and Pfeiffer S. E. (2002) Detergent-insoluble glycosphingolipid/cholesterol microdomains of the myelin membrane. J. Neurochem. 81, 993-1004.
84. Umemori H., Sato S., Yagi T., Aizawa S. and Yamamoto T. (1994) Initial events of myelination involve Fyn tyrosine kinase signalling. Nature 367, 572-576.
85. Vinson M., Rausch O., Maycox P. R. et al. (2003) Lipid rafts mediate the interaction between myelin-associated glycoprotein (MAG) on myelin and MAG-receptors on neurons. Mol. Cell. Neurosci. 22, 344-352.
86. Wilson R. and Brophy P. J. (1987) Identification of myelin proteins in association with the cytoskeleton in extracts of purified myelin and cultured oligodendrocytes. Biochem. Soc. Trans. 15, 853-854.
87. Wilson R. and Brophy P. J. (1989) Role for the oligodendrocyte cytoskeleton in myelination. J. Neurosci. Res. 22, 439-448.
88. Xavier R. and Seed B. (1999) Membrane compartmentation and the response to antigen. Curr. Opin. Immunol. 11, 265-269.
89. Yamamoto Y., Yoshikawa H., Nagano S., Kondoh G., Sadahiro S., Gotow T., Yanagihara T. and Sakoda S. (1999) Myelin-associated oligodendrocytic basic protein is essential for normal arrangement of the radial component in CNS myelin. Eur. J. Neurosci. 11, 847-855.