Partitioning of myelin basic protein into membrane microdomains in a spontaneously demyelinating mouse model for multiple sclerosis

Biochemistry and Cell Biology

Volumn 84, Issue 6, 2006, Pages 993-1005

  DeBruin, Lillian S ^a,b   Haines, Jeffery D ^a,c   Bienzle, Dorothee ^a   Harauz, George ^a  

^a UNIVERSITY OF GUELPH   (Canada)

^b WILFRID LAURIER UNIVERSITY   (Canada)

^c MCGILL UNIVERSITY   (Canada)

Author keywords

Detergent resistant membranes; Lipid rafts; Membrane microdomains; Multiple sclerosis; Myelin; Myelin basic protein; Post translational modifications

Indexed keywords

CELL MEMBRANES; CHEMICAL MODIFICATION; DISEASES; LIPIDS; PHOSPHORYLATION;

DETERGENT RESISTANT MEMBRANES; LIPID RAFTS; MEMBRANE MICRODOMAINS; MULTIPLE SCLEROSIS; MYELIN; MYELIN BASIC PROTEIN; POST TRANSLATIONAL MODIFICATIONS;

PROTEINS;

3 [(3 CHOLAMIDOPROPYL)DIMETHYLAMMONIO] 1 PROPANESULFONIC ACID; MITOGEN ACTIVATED PROTEIN KINASE; MYELIN; MYELIN BASIC PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; CONFERENCE PAPER; CONTROLLED STUDY; DEMYELINATING DISEASE; DISEASE COURSE; EXPERIMENTAL MODEL; HISTOPATHOLOGY; LIPID RAFT; MOUSE; MULTIPLE SCLEROSIS; MYELIN SHEATH; NONHUMAN; PROTEIN PROCESSING; WESTERN BLOTTING;

AGING; ANIMALS; CELL FRACTIONATION; CHOLIC ACIDS; DETERGENTS; DISEASE MODELS, ANIMAL; MEMBRANE MICRODOMAINS; MICE; MICE, INBRED STRAINS; MICE, TRANSGENIC; MULTIPLE SCLEROSIS; MYELIN BASIC PROTEINS; PHOSPHORYLATION; PROTEIN ISOFORMS; PROTEIN PROCESSING, POST-TRANSLATIONAL; SEVERITY OF ILLNESS INDEX; SILVER STAINING; SUBCELLULAR FRACTIONS; THREONINE;

MURINAE; MUS;

EID: 33947371742     PISSN: 08298211     EISSN: None     Source Type: Journal    
DOI: 10.1139/O06-180     Document Type: Conference Paper

References (111)

1. Arnaiz, S.L., D'Amico, G., Paglia, N., Arismendi, M., Basso, N., and Rosario Lores, A.M. 2004. Enriched environment, nitric oxide production and synaptic plasticity prevent the aging-dependent impairment of spatial cognition. Mol. Aspects Med. 25: 91-101.
2. Arvanitis, D.N., Min, W., Gong, Y., Heng, Y.M., and Boggs, J.M. 2005. Two types of detergent-insoluble, glycosphingolipid/cholesterol-rich membrane domains from isolated myelin. J. Neurochem. 94: 1696-1710. doi:10.1111/j.1471-4159.2005.03331.x.
3. Atkins, C.M., Yon, M., Groome, N.P., and Sweatt, J.D. 1999. Regulation of myelin basic protein phosphorylation by mitogen-activated protein kinase during increased action potential firing in the hippocampus. J. Neurochem. 73: 1090-1097. doi:10.1046/j.1471-4159.1999.0731090.x.
4. Baron, W., Decker, L., Colognato, H., and Ffrench-Constant, C. 2003. Regulation of integrin growth factor interactions in oligodendrocytes by lipid raft microdomains. Curr. Biol. 13: 151-155. doi:10.1016/S0960-9822(02) 01437-9.
5. Baron, W., Colognato, H., and Ffrench-Constant, C. 2005. Integrin-growth factor interactions as regulators of oligodendroglial development and function. Glia, 49: 467-479. doi:10.1002/glia.20132.
6. Barrese, N., Mak, B., Fisher, L., and Moscarello, M.A. 1998. Mechanism of demyelination in DM20 transgenic mice involves increased fatty acylation. J. Neurosci. Res. 53: 143-152. doi:10.1002/(SICI)1097-4547(19980715)53: 2〈143::AID-JNR3〉3.0. CO;2-7.
7. Boggs, J.M. 2006. Myelin basic protein: a multifunctional protein. Cell. Mol. Life Sci. 63: 1945-1961. doi:10.1007/s00018-006-6094-7.
8. Boggs, J.M., and Rangaraj, G. 2000. Interaction of lipid-bound myelin basic protein with actin filaments and calmodulin. Biochemistry, 39: 7799-7806. doi:10.1021/bi0002129.
9. Boggs, J.M., Wang, H., Gao, W., Arvanitis, D.N., Gong, Y., and Min, W. 2004. A glycosynapse in myelin? Glycoconj. J. 21: 97-110. doi:10.1023/B:GLYC0000044842.34958.f8.
10. Boggs, J.M., Rangaraj, G., Hill, C.M.D., Bates, I.R., Heng, Y.M., and Harauz, G. 2005. Effect of arginine loss in myelin basic protein, as occurs in its deiminated charge isoform, on mediation of actin polymerization and actin binding to a lipid membrane in vitro. Biochemistry, 44: 3524-3534. doi:10.1021/bi0473760.
11. Boggs, J.M., Rangaraj, G., Gao, W., and Heng, Y.M. 2006. Effect of phosphorylation of myelin basic protein by MAPK on its interactions with actin and actin binding to a lipid membrane in vitro. Biochemistry, 45: 391-401. doi:10.1021/bi0519194.
12. Bouwknecht, J.A., and Paylor, R. 2002. Behavioral and physiological mouse assays for anxiety: a survey in nine mouse strains. Behav. Brain Res. 136: 489-501. doi:10.1016/S0166-4328(02)00200-0.
13. Campagnoni, A.T. 1988. Molecular biology of myelin proteins from the central nervous system. J. Neurochem. 51: 1-14.
14. Campagnoni, A.T., and Campagnoni, C. 2004. Myelin basic protein gene. In Myelin biology and disorders. Edited by R.A. Lazzarini, J.W. Griffin, H. Lassman, K.-A. Nave, R.H. Miller, and B.D. Trapp. Elsevier Academic Press, San Diego. Pp. 387-400.
15. Campagnoni, A.T., Pribyl, T.M., Campagnoni, C.W., Kampf, K., Amur-Umarjee, S., Landry, C.F., et al. 1993. Structure and developmental regulation of Golli-mbp, a 105-kilobase gene that encompasses the myelin basic protein gene and is expressed in cells in the oligodendrocyte lineage in the brain. J. Biol. Chem. 268: 4930-4938.
16. Capello, E., Voskuhl, R.R., McFarland, H.F., and Raine, C.S. 1997. Multiple sclerosis: re-expression of a developmental gene in chronic lesions correlates with remyelination. Ann. Neurol. 41: 797-805. doi:10.1002/ana.410410616.
17. Cerghet, M., Skoff, R.P., Bessert, D., Zhang, Z., Mullins, C., and Ghandour, M.S. 2006. Proliferation and death of oligodendrocytes and myelin proteins are differentially regulated in male and female rodents. J. Neurosci. 26: 1439-1447. doi:10.1523/JNEUROSCI.2219-05.2006.
18. Chanderkar, L.P., Paik, W.K., and Kim, S. 1986. Studies on myelin basic protein methylation during mouse brain development. Biochem. J. 240: 471-479.
19. Chaudhuri, A., and Behan, P.O. 2004. Multiple sclerosis is not an autoimmune disease. Arch. Neurol. 61: 1610-1612. doi:10.1001/archneur.61. 10.1610.
20. Chaudhuri, A., and Behan, P.O. 2005. Multiple sclerosis: looking beyond autoimmunity. J. R. Soc. Med. 98: 303-306. doi:10.1258/jrsm.98.7.303.
21. Dasgupta, S., Jana, M., Liu, X., and Pahan, K. 2005. Myelin basic protein-primed T cells of female but not male mice induce nitric-oxide synthase and proinflammatory cytokines in microglia: implications for gender bias in multiple sclerosis. J. Biol. Chem. 280: 32609-32617. doi:10.1074/jbc. M500299200.
22. DeBruin, L.S., and Harauz, G. 2006. White matter rafting - membrane microdomains in myelin. Neurochem. Res., In press. doi:10.1007/s11064-006-9137- 4.
23. DeBruin, L.S., Haines, J.D., Wellhauser, L.A., Radeva, G., Schonmann, V., Bienzle, D., and Harauz, G. 2005. Developmental partitioning of myelin basic protein into membrane microdomains. J. Neurosci. Res. 80: 211-225. doi:10.1002/jnr.20452.
24. Decker, L., Baron, W., and Ffrench-Constant, C. 2004. Lipid rafts: microenvironments for integrin-growth factor interactions in neural development. Biochem. Soc. Trans. 32: 426-430. doi:10.1042/BST0320426.
25. Dubois-Dalcq, M., Ffrench-Constant, C., and Franklin, R.J. 2005. Enhancing central nervous system remyelination in multiple sclerosis. Neuron, 48: 9-12.
26. Duncan, I.D., Grever, W.E., and Zhang, S.C. 1997. Repair of myelin disease: strategies and progress in animal models. Mol. Med. Today, 3: 554-561.
27. Dyer, C.A. 2002. The structure and function of myelin: from inert membrane to perfusion pump. Neurochem. Res. 27: 1279-1292. doi:10.1023/A:1021611430052.
28. Dyer, C.A., and Benjamins, J.A. 1989a. Organization of oligodendroglial membrane sheets. I: Association of myelin basic protein and 2′,3′-cyclic nucleotide 3′-phosphohydrolase with cytoskeleton. J. Neurosci. Res. 24: 201-211. doi:10.1002/jnr.490240211.
29. Dyer, C.A., and Benjamins, J.A. 1989b. Organization of oligodendroglial membrane sheets: II. Galactocerebroside: antibody interactions signal changes in cytoskeleton and myelin basic protein. J. Neurosci. Res. 24: 212-221. doi:10.1002/jnr.490240212.
30. Dyer, C.A., and Benjamins, J.A. 1990. Glycolipids and transmembrane signaling: antibodies to galactocerebroside cause an influx of calcium in oligodendrocytes. J. Cell Biol. 111: 625-633. doi:10.1083/jcb.111.2.625.
31. Dyer, C.A., Philibotte, T.M., Billings-Gagliardi, S., and Wolf, M.K. 1995. Cytoskeleton in myelin-basic-protein-deficient shiverer oligodendrocytes. Dev. Neurosci. 17: 53-62.
32. Dyer, C.A., Philibotte, T., Wolf, M.K., and Billings-Gagliardi, S. 1997. Regulation of cytoskeleton by myelin components: studies on shiverer oligodendrocytes carrying an Mbp transgene. Dev. Neurosci. 19: 395-409.
33. Eichberg, J., and Iyer, S. 1996. Phosphorylation of myelin protein: recent advances. Neurochem. Res. 21: 527-535.
34. Fields, R.D. 2005. Myelination: an overlooked mechanism of synaptic plasticity? Neuroscientist, 11: 528-531. doi:10.1177/ 1073858405282304.
35. Gielen, E., Baron, W., Vandeven, M., Steels, P., Hoekstra, D., and Ameloot, M. 2006. Rafts in oligodendrocytes: evidence and structure-function relationship. Glia, 54: 499-512. doi:10.1002/glia.20406.
36. Givogri, M.I., Bongarzone, E.R., Schonmann, V., and Campagnoni, A.T. 2001. Expression and regulation of golli products of myelin basic protein gene during in vitro development of oligodendrocytes. J. Neurosci. Res. 66: 679-690. doi:10.1002/jnr.10031.
37. Golub, T., Wacha, S., and Caroni, P. 2004. Spatial and temporal control of signaling through lipid rafts. Curr. Opin. Neurobiol. 14: 542-550. doi:10.1016/j.conb.2004.08.003.
38. Gravel, M., Peterson, J., Yong, V.W., Kottis, V., Trapp, B., and Braun, P.E. 1996. Overexpression of 2′,3′-cyclic nucleotide 3′-phosphodiesterase in transgenic mice alters oligodendrocyte development and produces aberrant myelination. Mol. Cell. Neurosci. 7: 453-166. doi:10.1006/mcne.1996.0033.
39. Griffin, R.J., Moloney, A., Kelliher, M., Johnston, J.A., Ravid, R., Dockery, P., O'Connor, R., and O'Neill, C. 2005. Activation of Akt/PKB, increased phosphorylation of Akt substrates and loss and altered distribution of Akt and PTEN are features of Alzheimer's disease pathology. J. Neurochem. 93: 105-117. doi:10.1111/j.1471-4159.2004.02949.x.
40. Hancock, J.F. 2006. Lipid rafts: contentious only from simplistic standpoints. Nat. Rev. Mol. Cell Biol. 7: 456-462. doi:10.1038/ nrm1925.
41. Harauz, G., and Musse, A.A. 2006. A tale of two citrullines - structural and functional aspects of myelin basic protein deimination in health and disease. Neurochem. Res., In press. doi:10.1007/s11064-006-9108-9.
42. Harauz, G., Ishiyama, N., Hill, C.M.D., Bates, I.R., Libich, D.S., and Farès, C. 2004. Myelin basic protein-diverse conformational states of an intrinsically unstructured protein and its roles in myelin assembly and multiple sclerosis. Micron, 35: 503-542. doi:10.1016/j.micron.2004.04.005.
43. Hill, C.M.D., and Harauz, G. 2005. Charge effects modulate actin assembly by classic myelin basic protein isoforms. Biochem. Biophys. Res. Commun. 329: 362-369. doi:10.1016/j.bbrc.2005.01.151.
44. Hill, C.M.D., Libich, D.S., and Harauz, G. 2005. Assembly of tubulin by classic myelin basic protein isoforms and regulation by post-translational modification. Biochemistry, 44: 16672-16683. doi:10.1021/bi050646+.
45. Jacobs, E.C., Pribyl, T.M., Kampf, K., Campagnoni, C., Colwell, C.S., Reyes, S.D., et al. 2005. Region-specific myelin pathology in mice lacking the golli products of the myelin basic protein gene. J. Neurosci. 25: 7004-7013. doi:10.1523/JNEUROSCI. 0288-05.2005.
46. Jimenez, C.R., Stam, F.J., Li, K.W., Gouwenberg, Y., Hornshaw, M.P., De Winter, F., Verhaagen, J., and Smit, A.B. 2005. Proteomics of the injured rat sciatic nerve reveals protein expression dynamics during regeneration. Mol. Cell. Proteomics, 4: 120-132.
47. Johnson, R.S., Roder, J.C., and Riordan, J.R. 1995. Over-expression of the DM-20 myelin proteolipid causes central nervous system demyelination in transgenic mice. J. Neurochem. 64: 967-976.
48. Kagawa, T., Ikenaka, K., Inoue, Y., Kuriyama, S., Tsujii, T., Nakao, J., et al. 1994. Glial cell degeneration and hypomyelination caused by overexpression of myelin proteolipid protein gene. Neuron, 13: 427-442. doi:10.1016/0896-6273(94)90358-1.
49. Karthigasan, J., Garvey, J.S., Ramamurthy, G.V., and Kirschner, D.A. 1996. Immunolocalization of 17 and 21.5 kDa MBP isoforms in compact myelin and radial component. J. Neurocytol. 25: 1-7. doi:10.1007/BF02284781.
50. Kim, S., Chanderkar, L.P., Ghosh, S.K., Park, J.O., and Paik, W.K. 1988. Enzymatic methylation of arginine residue in myelin basic protein. Adv. Exp. Med. Biol. 231: 327-340.
51. Kim, J.K., Mastronardi, F.G., Wood, D.D., Lubman, D.M., Zand, R., and Moscarello, M.A. 2003. Multiple sclerosis: an important role for post-translational modifications of myelin basic protein in pathogenesis. Mol. Cell. Proteomics, 2: 453-462.
52. Kosaras, B., and Kirschner, D.A. 1990. Radial component of CNS myelin: junctional subunit structure and supramolecular assembly. J. Neurocytol. 19: 187-199. doi:10.1007/BF01217297.
53. Krämer, 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.
54. Krämer, 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: 29042-29049. doi:10.1074/jbc.274.41.29042.
55. Kramer, E.M., Schardt, A., and Nave, K.A. 2001. Membrane traffic in myelinating oligodendrocytes. Microsc. Res. Tech. 52: 656-671.
56. Krieger, C., Hu, J.H., and Pelech, S. 2003. Aberrant protein kinases and phosphoproteins in amyotrophic lateral sclerosis. Trends Pharmacol. Sci. 24: 535-541. doi:10.1016/j.tips.2003.08.003.
57. Landry, C.F., Ellison, J.A., Pribyl, T.M., Campagnoni, C., Kampf, K., and Campagnoni, A.T. 1996. Myelin basic protein gene expression in neurons: developmental and regional changes in protein targeting within neuronal nuclei, cell bodies, and processes. J. Neurosci. 16: 2452-2462.
58. Lassmann, H. 2004. Cellular damage and repair in multiple sclerosis. In Myelin biology and disorders. Edited by R.A. Lazzarini, J.W. Griffin, H. Lassman, K.-A. Nave, R.H. Miller, and B.D. Trapp. Elsevier Academic Press, San Diego. pp. 733-762.
59. Lassmann, H., Brack, W., and Lucchinetti, C. 2001. Heterogeneity of multiple sclerosis pathogenesis: implications for diagnosis and therapy. Trends Mol. Med. 7: 115-121. doi:10.1016/S1471-4914(00)01909-2.
60. Le Corre, S., Klafki, H.W., Plesnila, N., Hubinger, G., Obermeier, A., Sahagun, H., et al. 2006. An inhibitor of tau hyperphosphorylation prevents severe motor impairments in tau transgenic mice. Proc. Natl. Acad. Sci. U.S.A. 103: 9673-9678. doi:10.1073/pnas.0602913103.
61. Lee, J., Gravel, M., Zhang, R., Thibault, P., and Braun, P.E. 2005. Process outgrowth in oligodendrocytes is mediated by CNP, a novel microtubule assembly myelin protein. J. Cell Biol. 170: 661-673. doi:10.1083/jcb. 200411047.
62. Li, L., and Tang, B.L. 2005. Environmental enrichment and neurodegenerative diseases. Biochem. Biophys. Res. Commun. 334: 293-297. doi:10.1016/j.bbrc.2005.05.162.
63. Lichtenberg, D., Goni, F.M., and Heerklotz, H. 2005. Detergent-resistant membranes should not be identified with membrane rafts. Trends Biochem. Sci. 30: 430-436. doi:10.1016/j.tibs.2005.06.004.
64. Lucchinetti, C., Brack, W., Parisi, J., Scheithauer, B., Rodriguez, M., and Lassmann, H. 1999. A quantitative analysis of oligodendrocytes in multiple sclerosis lesions. A study of 113 cases. Brain, 122: 2279-2295. doi:10.1093/brain/122.12.2279.
65. Maggio, B., Rosetti, CM., Borioli, G.A., Fanani, M.L., and Del Boca, M. 2005. Protein-mediated surface structuring in biomembranes. Braz. J. Med. Biol. Res. 38: 1735-1748.
66. Makhlouf, K., Imitola, J., and Khoury, S.J. 2002. Experimental autoimmune encephalomyelitis and multiple sclerosis: from bench to bedside. In Disorders of myelin in the central and peripheral nervous systems. Edited by F. Dangond. Butterworth/ Heinemann, Woburn. pp. 155-164.
67. Mastronardi, F.G., and Moscarello, M.A. 2005. Molecules affecting myelin stability: a novel hypothesis regarding the pathogenesis of multiple sclerosis. J. Neurosci. Res. 80: 301-308. doi:10.1002/jnr.20420.
68. Mastronardi, F.G., Ackerley, C.A., Arsenault, L., Roots, B.I., and Moscarello, M.A. 1993. Demyelination in a transgenic mouse: a model for multiple sclerosis. J. Neurosci. Res. 36: 315-324. doi:10.1002/jnr.490360309.
69. Mastronardi, F.G., Ackerley, C.A., Roots, B.I., and Moscarello, M.A. 1996a. Loss of myelin basic protein cationicity in DM20 transgenic mice is dosage dependent. J. Neurosci. Res. 44: 301-307. doi:10.1002/(SICI) 1097-4547(19960515)44:4〈301::AID-JNR1〉3.0.CO;2-G.
70. Mastronardi, F.G., al-Sabbagh, A., Nelson, P.A., Rego, J., Roots, B.I., and Moscarello, M.A. 1996b. Myelin basic protein in experimental allergic encephalomyelitis is not affected at the posttranslational level: implications for demyelinating disease. J. Neurosci. Res. 44: 344-349. doi:10.1002/(SICI)1097-4547(19960515)44:4〈344::AID-JNR5〉3.0.CO;2-C.
71. Mastronardi, F.G., Mak, B., Ackerley, C.A., Roots, B.I., and Moscarello, M.A. 1996c. Modifications of myelin basic protein in DM20 transgenic mice are similar to those in myelin basic protein from multiple sclerosis. J. Clin. Invest. 97: 349-358.
72. Musse, A.A., Boggs, J.M., and Harauz, G. 2006. Deimination of membrane-bound myelin basic protein in multiple sclerosis exposes an immunodominant epitope. Proc. Natl. Acad. Sci. U.S.A. 103: 4422-4427. doi:10.1073/pnas.0509158103.
73. Nakajima, K., Ikenaka, K., Kagawa, T., Aruga, J., Nakao, J., Nakahira, K., et al. 1993. Novel isoforms of mouse myelin basic protein predominantly expressed in embryonic stage. J. Neurochem. 60: 1554-1563.
74. Norton, W.T., and Poduslo, S.E. 1973. Myelination in rat brain: method of myelin isolation. J. Neurochem. 21: 749-757.
75. Patil, A., and Nakamura, H. 2006. Disordered domains and high surface charge confer hubs with the ability to interact with multiple proteins in interaction networks. FEBS Lett. 580: 2041-2045. doi:10.1016/j.febslet. 2006.03.003.
76. Pedraza, L., Fidler, L., Staugaitis, S.M., and Colman, D.R. 1997. The active transport of myelin basic protein into the nucleus suggests a regulatory role in myelination. Neuron, 18: 579-589. doi:10.1016/S0896-6273(00) 80299-8.
77. Pike, L.J. 2004. Lipid rafts: heterogeneity on the high seas. Biochem. J. 378: 281-292. doi:10.1042/BJ20031672.
78. Pike, L.J. 2006. Rafts defined: a report on the Keystone Symposium on Lipid Rafts and Cell Function. J. Lipid Res. 47: 1597-1598.
79. Pritzker, L.B., Joshi, S., Harauz, G., and Moscarello, M.A. 2000. Deimination of myelin basic protein. 2. Effect of methylation of MBP on its deimination by peptidylarginine deiminase. Biochemistry, 39: 5382-5388. doi:10.1021/bi9925571.
80. Quarles, R.H. 1980. The biochemical and morphological heterogeneity of myelin and myelin-related membranes. In Biochemistry of brain. Edited by S. Kumar. Pergamon, Oxford. pp. 81-102.
81. Quest, A.F., Leyton, L., and Parraga, M. 2004. Caveolins, caveolae, and lipid rafts in cellular transport, signaling, and disease. Biochem. Cell Biol. 82: 129-144. doi:10.1139/o03-071.
82. Radeva, G., and Sharom, F.J. 2004. Isolation and characterization of lipid rafts with different properties from RBL-2H3 (rat basophilic leukaemia) cells. Biochem. J. 380: 219-230. doi:10.1042/BJ20031348.
83. Rajendran, L., and Simons, K. 2005. Lipid rafts and membrane dynamics. J. Cell Sci. 118: 1099-1102. doi:10.1242/jcs.01681.
84. Rawal, N., Lee, Y.J., Paik, W.K., and Kim, S. 1992. Studies on NG-methylarginine derivatives in myelin basic protein from developing and mutant mouse brain. Biochem. J. 287: 929-935.
85. Riccio, P., Simone, S.M., Cibelli, G., De Santis, A., Bobba, A., Livrea, P., and Quagliariello, E. 1983. Solubilization of myelin proteins by detergents. In Structure and function of membrane proteins. Edited by E. Quagliariello and F. Palmieri. Elsevier Science Publishers B.V., Amsterdam. pp. 361-364.
86. Riccio, P., Rosenbusch, J.P., and Quagliariello, E. 1984. A new procedure for the isolation of the brain myelin basic protein in a lipid-bound form. FEBS Lett. 177: 236-240. doi:10.1016/0014-5793(84)81290-9.
87. Ro, H.A., and Carson, J.H. 2004. pH microdomains in oligodendrocytes. J. Biol. Chem. 279: 37115-37123. doi:10.1074/jbc.M403099200.
88. Rosenbluth, J., Nave, K.A., Mierzwa, A., and Schiff, R. 2006. Subtle myelin defects in PLP-null mice. Glia, 54: 172-182. doi:10.1002/glia. 20370.
89. Saito, Y., Suzuki, K., Hulette, C.M., and Murayama, S. 2004. Aberrant phosphorylation of alpha-synuclein in human Niemann-Pick type C1 disease. J. Neuropathol. Exp. Neurol. 63: 323-328.
90. Schuck, S., Honsho, M., Ekroos, K., Shevchenko, A., and Simons, K. 2003. Resistance of cell membranes to different detergents. Proc. Natl. Acad. Sci. U.S.A. 100: 5795-5800. doi:10.1073/pnas.0631579100.
91. Shanshiashvili, L.V., Suknidze, N.C., Machaidze, G.G., Mikeladze, D.G., and Ramsden, J.J. 2003. Adhesion and clustering of charge isomers of myelin basic protein at model myelin membranes. Arch. Biochem. Biophys. 419: 170-177. doi:10.1016/j.abb.2003.09.020.
92. Simons, K., and Ehehalt, R. 2002. Cholesterol, lipid rafts, and disease. J. Clin. Invest. 110: 597-603. doi:10.1172/JCI200216390.
93. Simons, K., and Ikonen, E. 1997. Functional rafts in cell membranes. Nature (London), 387: 569-572. doi:10.1038/42408.
94. 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. doi:10.1083/jcb.151.1.143.
95. Sperber, B.R., and McMorris, F.A. 2001. Fyn tyrosine kinase regulates oligodendroglial cell development but is not required for morphological differentiation of oligodendrocytes. J. Neurosci. Res. 63: 303-312. doi:10.1002/1097-4547(20010215)63:4〈303::AID-JNR1024〉3.0.CO;2-A.
96. Sperber, B.R., Boyle-Walsh, E.A., Engleka, M.J., Gadue, P., Peterson, A.C., Stein, P.L., Scherer, S.S., and McMorris, F.A. 2001. A unique role for Fyn in CNS myelination. J. Neurosci. 21: 2039-2047.
97. Sriram, S., and Steiner, I. 2005. Experimental allergic encephalomyelitis: a misleading model of multiple sclerosis. Ann. Neurol. 58: 939-945. doi:10.1002/ana.20743.
98. Stariha, R.L., and Kim, S.U. 2001a. Mitogen-activated protein kinase signalling in oligodendrocytes: a comparison of primary cultures and CG-4. Int. J. Dev. Neurosci. 19: 427-437.
99. Stariha, R.L., and Kim, S.U. 2001b. Protein kinase C and mitogen-activated protein kinase signalling in oligodendrocytes. Microsc. Res. Tech. 52: 680-688. doi:10.1002/jemt.1052.
100. Stariha, R.L., Kikuchi, S., Siow, Y.L., Pelech, S.L., Kim, M., and Kim, S.U. 1997. Role of extracellular signal-regulated protein kinases 1 and 2 in oligodendroglial process extension. J. Neurochem. 68: 945-953.
101. Szuchet, S., Polak, P.E., Yim, S.H., and Lange, Y. 1988. Plasma membrane of cultured oligodendrocytes: II. Possible structural and functional domains. Glia, 1: 54-63. doi:10.1002/glia.440010107.
102. Taylor, C.M., Coetzee, T., and Pfeiffer, S.E. 2002. Detergent-insoluble glycosphingolipid/cholesterol microdomains of the myelin membrane. J. Neurochem. 81: 993-1004. doi:10.1046/j.1471-4159.2002.00884.x.
103. Tompa, P. 2005. The interplay between structure and function in intrinsically unstructured proteins. FEBS Lett. 579: 3346-3354. doi:10.1016/j.febslet.2005.03.072.
104. Tompa, P., Szasz, C., and Buday, L. 2005. Structural disorder throws new light on moonlighting. Trends Biochem. Sci. 30: 484-489. doi:10.1016/j.tibs.2005.07.008.
105. Trapp, B.D., and Kidd, G.J. 2004. Structure of the myelinated axon. In Myelin Biology and Disorders. Edited by R.A. Lazzarini, J.W. Griffin, H. Lassman, K. Nave, R.H. Miller, and B.D. Trapp. Elsevier Academic Press, San Diego. pp. 3-27.
106. Ulmer, J.B., and Braun, P.E. 1983. In vivo phosphorylation of myelin basic proteins in developing mouse brain: evidence that phosphorylation is an early event in myelin formation. Dev. Neurosci. 6: 345-355.
107. Vartanian, T., Szuchet, S., Dawson, G., and Campagnoni, A.T. 1986. Oligodendrocyte adhesion activates protein kinase C-mediated phosphorylation of myelin basic protein. Science (Washington, D.C.), 234: 1395-1398.
108. Wight, P.A., and Dobretsova, A. 2004. Where, when and how much: regulation of myelin proteolipid protein gene expression. Cell. Mol. Life Sci. 61: 810-821.
109. Wilson, R., and Brophy, P.J. 1989. Role for the oligodendrocyte cytoskeleton in myelination. J. Neurosci. Res. 22: 4390-448. doi:10.1002/jnr.490220409.
110. Zajchowski, L.D., and Robbins, S.M. 2002. Lipid rafts and little caves. Compartmentalized signalling in membrane microdomains. Eur. J. Biochem. 269: 737-752. doi:10.1046/j.0014-2956.2001.02715.x.
111. Zand, R., Li, M.X., Jin, X., and Lubman, D. 1998. Determination of the sites of posttranslational modifications in the charge isomers of bovine myelin basic protein by capillary electrophoresis-mass spectroscopy. Biochemistry, 37: 2441-2449. doi:10.1021/ bi972347t.