Myelin architecture: zippering membranes tightly together

Cellular and Molecular Life Sciences

Volumn 71, Issue 7, 2014, Pages 1265-1277

  Bakhti, Mostafa ^a,b,c   Aggarwal, Shweta ^a,b   Simons, Mikael ^a,b  

^a MAX PLANCK INSTITUTE OF EXPERIMENTAL MEDICINE   (Germany)

^b UNIVERSITY OF GÖTTINGEN   (Germany)

^c INSTITUTE OF EPIDEMIOLOGY   (Germany)

Author keywords

Myelin; Myelin basic protein; Oligodendrocytes; Proteolipid protein

Indexed keywords

MYELIN; MYELIN BASIC PROTEIN; PROTEOLIPID PROTEIN;

AXON; BILAYER MEMBRANE; BOVINE; CELL MEMBRANE; CENTRAL NERVOUS SYSTEM; CHICKEN; CYTOPLASM; DOGFISH; DOWN REGULATION; GUINEA PIG; HUMAN; LEPORIDAE; MOUSE; MYELIN SHEATH; NERVE CONDUCTION; NONHUMAN; OLIGODENDROGLIA; PIG; POLYMERIZATION; PROTEIN DEGRADATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; RAT; REVIEW; SHARK; XENOPUS; AMINO ACID SEQUENCE; BIOLOGICAL MODEL; CHEMISTRY; CYTOLOGY; DEMYELINATING DISEASE; METABOLISM; MOLECULAR GENETICS; PATHOLOGY; PHYSIOLOGY; SEQUENCE ALIGNMENT; ULTRASTRUCTURE;

AMINO ACID SEQUENCE; CELL MEMBRANE; DEMYELINATING DISEASES; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; MYELIN BASIC PROTEIN; MYELIN PROTEOLIPID PROTEIN; MYELIN SHEATH; OLIGODENDROGLIA; SEQUENCE ALIGNMENT;

EID: 84902084169     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-013-1492-0     Document Type: Review

References (160)

1. Hartline DK, Colman DR (2007) Rapid conduction and the evolution of giant axons and myelinated fibers. Curr Biol 17:R29–R35
2. Sherman DL, Brophy PJ (2005) Mechanisms of axon ensheathment and myelin growth. Nat Rev Neurosci 6:683–690
3. Baumann N, Pham-Dinh D (2001) Biology of oligodendrocyte and myelin in the mammalian central nervous system. Physiol Rev 81:871–927
4. Aggarwal S, Yurlova L, Simons M (2011) Central nervous system myelin: structure, synthesis and assembly. Trends Cell Biol 21:585–593
5. Piper RC, Katzmann DJ (2007) Biogenesis and function of multivesicular bodies. Annu Rev Cell Dev Biol 23:519–547
6. Platt FM, Boland B, Van Der Spoel AC (2012) The cell biology of disease: lysosomal storage disorders: the cellular impact of lysosomal dysfunction. J Cell Biol 199:723–734
7. Schmitz G, Müller G (1991) Structure and function of lamellar bodies, lipid–protein complexes involved in storage and secretion of cellular lipids. J Lipid Res 32:1539–1570
8. Weinbaum S, Tarbell JM, Damiano ER (2007) The structure and function of the endothelial glycocalyx layer. Annu Rev Biomed Eng 9:121–167
9. Harauz G, Ladizhansky V, Boggs JM (2009) Structural polymorphism and multifunctionality of myelin basic protein. Biochemistry 48:8094–8104
10. Harauz G, Ishiyama N, Hill CMD et al (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
11. Hill CM, Bates IR, White GF et al (2002) Effects of the osmolyte trimethylamine-N-oxide on conformation, self-association, and two-dimensional crystallization of myelin basic protein. J Struct Biol 139:13–26
12. Tompa P (2002) Intrinsically unstructured proteins. Trends Biochem Sci 27:527–533
13. Tompa P (2009) Structure and function of intrinsically disordered proteins. Matrix 331
14. Dyson HJ, Wright PE (2005) Intrinsically unstructured proteins and their functions. Nat Rev Mol Cell Biol 6:197–208
15. Tompa P, Bánki P, Bokor M et al (2006) Protein–water and protein–buffer interactions in the aqueous solution of an intrinsically unstructured plant dehydrin: NMR Intensity and DSC aspects. Biophys J 91:2243–2249
16. Mouillon J-M, Eriksson SK, Harryson P (2008) Mimicking the plant cell interior under water stress by macromolecular crowding: disordered dehydrin proteins are highly resistant to structural collapse. Plant Physiol 148:1925–1937
17. Polverini E, Coll EP, Tieleman DP, Harauz G (2011) Conformational choreography of a molecular switch region in myelin basic protein–molecular dynamics shows induced folding and secondary structure type conversion upon threonyl phosphorylation in both aqueous and membrane-associated environments. Biochim Biophys Acta 1808:674–683
18. Smith GST, Chen L, Bamm VV et al (2010) The interaction of zinc with membrane-associated 18.5 kDa myelin basic protein: an attenuated total reflectance-Fourier transform infrared spectroscopic study. Amino Acids 39:739–750
19. Vassall KA, Bessonov K, De Avila M et al (2013) The effects of threonine phosphorylation on the stability and dynamics of the central molecular switch region of 18.5-kDa myelin basic protein. PloS one 8:e68175
20. Chernoff GF (1981) Shiverer: an autosomal recessive mutant mouse with myelin deficiency. J Hered 72:128
21. Roach A, Boylan K, Horvath S et al (1983) Characterization of cloned cDNA representing rat myelin basic protein: absence of expression in brain of shiverer mutant mice. Cell 34:799–806
22. Aggarwal S, Snaidero N, Pähler G et al (2013) Myelin membrane assembly is driven by a phase transition of myelin basic proteins into a cohesive protein meshwork. PLoS Biol 11:e1001577
23. Smith R (1992) The basic protein of CNS myelin: its structure and ligand binding. J Neurochem 59:1589–1608
24. Kattnig DR, Bund T, Boggs JM et al (2012) Lateral self-assembly of 18.5-kDa myelin basic protein (MBP) charge component-C1 on membranes. Biochim Biophys Acta, pp 1–12
25. Hyman AA, Brangwynne CP (2011) Beyond stereospecificity: liquids and mesoscale organization of cytoplasm. Dev Cell 21:14–16
26. Weber SC, Brangwynne CP (2012) Getting RNA and protein in phase. Cell 149:1188–1191
27. Hyman AA, Simons K (2012) Beyond oil and water—phase transitions in cells. Science 337:1047–1049
28. Brangwynne CP, Eckmann CR, Courson DS et al (2009) Germline P granules are liquid droplets that localize by controlled dissolution/condensation. Science 324:1729–1732
29. Kato M, Han TW, Xie S et al (2012) Cell-free formation of RNA granules: low complexity sequence domains form dynamic fibers within hydrogels. Cell 149:753–767
30. Li P, Banjade S, Cheng H-C et al (2012) Phase transitions in the assembly of multivalent signalling proteins. Nature 483:336–340
31. Frey S, Richter RP, Görlich D (2006) FG-rich repeats of nuclear pore proteins form a three-dimensional meshwork with hydrogel-like properties. Science 314:815–817
32. Bund T, Boggs JM, Harauz G et al (2010) Copper uptake induces self-assembly of 18.5 kDa myelin basic protein (MBP). Biochem J 99:3020–3028
33. Ishiyama N, Bates IR, Hill CM et al (2001) The effects of deimination of myelin basic protein on structures formed by its interaction with phosphoinositide-containing lipid monolayers. J Struct Biol 136:30–45
34. Smith R (1985) The encephalitogenic protein of myelin forms hexamers in which the polypeptides have a pleated-sheet structure. FEBS Lett 183:331–334
35. Harauz G, Libich DS (2009) The classic basic protein of myelin–conserved structural motifs and the dynamic molecular barcode involved in membrane adhesion and protein–protein interactions. Curr Protein Pept Sci 10:196–215
36. Bates IR, Boggs JM, Feix JBHG (2003) Membrane-anchoring and charge effects in the interaction of myelin basic protein with lipid bilayers studied by site-directed spin labeling. J Biol Chem 278:29041–29047
37. Bates IR, Feix JB, Boggs JM, Harauz G (2004) An immunodominant epitope of myelin basic protein is an amphipathic alpha-helix. J Biol Chem 279:5757–5764
38. 11C]-2-(4′-methylaminophenyl)-6-hydroxybenzothiazole. Ann Neurol 69:673–680
39. Fowler DM, Koulov AV, Balch WE, Kelly JW (2007) Functional amyloid—from bacteria to humans. Trends Biochem Sci 32:217–224
40. Chiti F, Dobson CM (2006) Protein misfolding, functional amyloid, and human disease. Annu Rev Biochem 75:333–366
41. Alberti S, Halfmann R, King O et al (2009) A systematic survey identifies prions and illuminates sequence features of prionogenic proteins. Cell 137:146–158
42. Smith R (1982) Self-association of myelin basic protein: enhancement by detergents and lipids. Biochemistry 21:2697–2701
43. Ader C, Frey S, Maas W et al (2010) Amyloid-like interactions within nucleoporin FG hydrogels. Proc Natl Acad Sci USA 107:6281–6285
44. Maji SK, Perrin MH, Sawaya MR et al (2009) Functional amyloids as natural storage of peptide hormones in pituitary secretory granules. Science 325:328–332
45. Uversky VN, Oldfield CJ, Dunker AK (2008) Intrinsically disordered proteins in human diseases: introducing the D2 concept. Annu Rev Biophys 37:215–246
46. Chivet M, Hemming F, Pernet-Gallay K et al (2012) Emerging role of neuronal exosomes in the central nervous system. Frontiers Physiol 3:145
47. Emery B, Agalliu D, Cahoy JD et al (2009) Myelin gene regulatory factor is a critical transcriptional regulator required for CNS myelination. Cell 138:172–185
48. Bujalka H, Koenning M, Jackson S et al (2013) MYRF is a membrane-associated transcription factor that autoproteolytically cleaves to directly activate myelin genes. PLoS Biol 11:e1001625. doi:10.1371/journal.pbio.1001625
49. Li Z, Park Y, Marcotte EM (2013) A bacteriophage tailspike domain promotes self-cleavage of a human membrane-bound transcription factor, the myelin regulatory factor MYRF. PLoS Biol 11:e1001624. doi:10.1371/journal.pbio.1001624
50. Wake H, Lee PR, Fields RD (2011) Control of local protein synthesis and initial events in myelination by action potentials. Science 333:1647–1651
51. Lyons DA, Naylor SG, Scholze A, Talbot WS (2009) Kif1b is essential for mRNA localization in oligodendrocytes and development of myelinated axons. Nat Genet 41:854–858
52. Laursen LS, Chan CW, Ffrench-Constant C (2011) Translation of myelin basic protein mRNA in oligodendrocytes is regulated by integrin activation and hnRNP-K. J Cell Biol 192:797–811
53. White R, Gonsior C, Krämer-Albers E-M et al (2008) Activation of oligodendroglial Fyn kinase enhances translation of mRNAs transported in hnRNP A2-dependent RNA granules. J Cell Biol 181:579–586
54. Kosturko LD, Maggipinto MJ, D’Sa C et al (2005) The microtubule-associated protein tumor overexpressed gene binds to the RNA trafficking protein heterogeneous nuclear ribonucleoprotein A2. Mol Biol Cell 16:1938–1947
55. Kosturko LD, Maggipinto MJ, Korza G et al (2006) Heterogeneous nuclear ribonucleoprotein (hnRNP) E1 binds to hnRNP A2 and inhibits translation of A2 response element mRNAs. Mol Biol Cell 17:3521–3533
56. White R, Gonsior C, Bauer NM et al (2011) HnRNP F is a novel component of oligodendroglial RNA transport granules contributing to the regulation of MBP protein synthesis. J Biol Chem 287:1742–1754
57. Bauer NM, Moos C, van Horssen J et al (2012) Myelin basic protein synthesis is regulated by small non-coding RNA 715. EMBO Rep 13:827–834
58. Kim JK, Mastronardi FG, Wood DD et al (2003) Multiple sclerosis: an important role for post-translational modifications of myelin basic protein in pathogenesis. Mol Cell Proteomics 2:453–462
59. Zhang C, Walker AK, Zand R et al (2012) Myelin basic protein undergoes a broader range of modifications in mammals than in lower vertebrates. J Proteome Res 11:4791–4802. doi:10.1021/pr201196e
60. Boggs JM (2006) Myelin basic protein: a multifunctional protein. Cell Mol Life Sci 63:1945–1961
61. Ozkirimli E, Yadav SS, Miller WT, Post CB (2008) An electrostatic network and long-range regulation of Src kinases. Protein Sci 17:1871–1880
62. McLaughlin S, Aderem A (1995) The myristoyl-electrostatic switch: a modulator of reversible protein-membrane interactions. Trends Biochem Sci 20:272–276
63. Ahmed MAM, De Avila M, Polverini E et al (2012) Solution NMR structure and molecular dynamics simulations of murine 18.5-kDa myelin basic protein segment (S72-S107) in association with dodecylphosphocholine micelles. Biochemistry. doi:10.1021/bi300998x
64. Homchaudhuri L, De Avila M, Nilsson SB et al (2010) Secondary structure and solvent accessibility of a calmodulin-binding C-terminal segment of membrane-associated myelin basic protein. Biochemistry 49:8955–8966
65. Bamm VV, De Avila M, Smith GST et al (2011) Structured functional domains of myelin basic protein: cross talk between actin polymerization and Ca(2+)-dependent calmodulin interaction. Biophys J 101:1248–1256
66. Goldbaum O, Richter-Landsberg C (2001) Stress proteins in oligodendrocytes: differential effects of heat shock and oxidative stress. J Neurochem 78:1233–1242
67. Aquino DA, Peng D, Lopez C, Farooq M (1998) The constitutive heat shock protein-70 is required for optimal expression of myelin basic protein during differentiation of oligodendrocytes. Neurochem Res 23:413–420
68. Cwiklinska H, Mycko MP, Luvsannorov O et al (2003) Heat shock protein 70 associations with myelin basic protein and proteolipid protein in multiple sclerosis brains. Int Immunol 15:241–249
69. Riccio P, Giovannelli S, Bobba A et al (1995) Specificity of zinc binding to myelin basic protein. Neurochem Res 20:1107–1113
70. Smeyers-Verbeke J, Defrise-Gussenhoven E, Ebinger G, Löwenthal AMD (1974) Distribution of Cu and Zn in human brain tissue. Clin Chim Acta 51:309–314
71. Earl C, Chantry A, Mohammad N, Glynn P (1988) Zinc ions stabilise the association of basic protein with brain myelin membranes. J Neurochem 51:718–724
72. Liuzzi GM, Ventola A, Rizzo T et al (1991) Zinc as an inhibitor of myelin basic protein proteolytic breakdown in the central nervous system. Acta Neurol 13:153–161
73. Berlet HH, Bischoff H, Weinhardt F (1994) Divalent metals of myelin and their differential binding by myelin basic protein of bovine central nervous system. Neurosci Lett 179:75–78
74. Cavatorta P, Giovanelli S, Bobba A et al (1994) Myelin basic protein interaction with zinc and phosphate: fluorescence studies on the water-soluble form of the protein. Biophys J 66:1174–1179
75. Tsang D, Tsang YS, Ho WK, Wong RN (1997) Myelin basic protein is a zinc-binding protein in brain: possible role in myelin compaction. Neurochem Res 22:811–819
76. Nuzzo S, Meneghini C, Mobilioo S et al (2002) An X-ray absorption spectroscopy study of the zinc environment in Langmuir-Blodgett phospholipid multilayers. Biophys J 83:3507–3512
77. Tsutsui S, Stys PK (2012) Metabolic injury to axons and myelin. Exp Neurol. doi:10.1016/j.expneurol.2012.04.016
78. Nawaz S, Kippert A, Saab AS et al (2009) Phosphatidylinositol 4,5-bisphosphate-dependent interaction of myelin basic protein with the plasma membrane in oligodendroglial cells and its rapid perturbation by elevated calcium. J Neurosci 29:4794–4807
79. Musse AA, Gao W, Homchaudhuri L et al (2008) Myelin basic protein as a “PI(4,5)P2-modulin”: a new biological function for a major central nervous system protein. Biochemistry 47:10372–10382
80. Musse AA, Gao W, Rangaraj G et al (2009) Myelin basic protein co-distributes with other PI(4,5)P2-sequestering proteins in Triton X-100 detergent-resistant membrane microdomains. Neurosci Lett 450:32–36
81. Lamensa JW, Moscarello MA (1993) Deimination of human myelin basic protein by a peptidylarginine deiminase from bovine brain. J Neurochem 61:987–996
82. Smith GST, Paez PM, Spreuer V et al (2011) Classical 18.5-and 21.5-kDa isoforms of myelin basic protein inhibit calcium influx into oligodendroglial cells, in contrast to golli isoforms. J Neurosci Res 89:467–480
83. Aggarwal S, Yurlova L, Snaidero N et al (2011) A size barrier limits protein diffusion at the cell surface to generate lipid-rich myelin-membrane sheets. Dev Cell 21:445–456
84. Dyer CA, Philibotte TM, Billings-Gagliardi S, Wolf MK (1995) Cytoskeleton in myelin-basic-protein-deficient shiverer oligodendrocytes. Dev Neurosci 17:53–62
85. Dyer CA, Phillbotte T, Wolf MK, Billings-Gagliardi S (1997) Regulation of cytoskeleton by myelin components: studies on shiverer oligodendrocytes carrying an Mbp transgene. Dev Neurosci 19:395–409
86. Ishiyama N, Hill CM, Bates IR, Harauz G (2006) The formation of helical tubular vesicles by binary monolayers containing a nickel-chelating lipid and phosphoinositides in the presence of basic polypeptides. Chem Phys Lipids 114:103–111
87. Zuchero JB, Barres B (2011) Between the sheets: a molecular sieve makes myelin membranes. Dev Cell 21:385–386
88. Hülsmann BB, Labokha AA, Görlich D (2012) The permeability of reconstituted nuclear pores provides direct evidence for the selective phase model. Cell 150:738–751
89. Singer SJ, Nicolson GL (1972) The fluid mosaic model of the structure of cell membranes. Science 175:720–731
90. Fitzner D, Schneider A, Kippert A et al (2006) Myelin basic protein-dependent plasma membrane reorganization in the formation of myelin. EMBO J 25:5037–5048
91. Yurlova L, Kahya N, Aggarwal S et al (2011) Self-segregation of myelin membrane lipids in model membranes. Biophys J 101:2713–2720
92. Boggs JM, Moscarello M, Papahadjopoulos D (1977) Phase separation of acidic and neutral phospholipids induced by human myelin basic protein. Biochemistry 16:5420–5426
93. Min Y, Kristiansen K, Boggs JM et al (2009) Interaction forces and adhesion of supported myelin lipid bilayers modulated by myelin basic protein. Proc Natl Acad Sci USA 106:3154–3159
94. Rosetti CM, Maggio B, Wilke N (2010) Micron-scale phase segregation in lipid monolayers induced by myelin basic protein in the presence of a cholesterol analog. Biochim Biophys Acta 1798:498–505
95. Rosetti CM, Maggio B, Oliveira RG (2008) The self-organization of lipids and proteins of myelin at the membrane interface. Molecular factors underlying the microheterogeneity of domain segregation. Biochim Biophys Acta 1778:1665–1675
96. Ter Beest MB, Hoekstra D (1993) Interaction of myelin basic protein with artificial membranes. Parameters governing binding, aggregation and dissociation. Eur J Biochem 211:689–696
97. Jo E, Boggs JM (1995) Aggregation of acidic lipid vesicles by myelin basic protein: dependence on potassium concentration. Biochemistry 34:13705–13716
98. Mac Millan SV, Ishiyama N, White GF et al (2000) Myelin basic protein component C1 in increasing concentrations can elicit fusion, aggregation, and fragmentation of myelin-like membranes. Eur J Cell Biol 79:327–335
99. Hu Y, Israelachvili J (2008) Lateral reorganization of myelin lipid domains by myelin basic protein studied at the air–water interface. Colloids Surf B Biointerface 62:22–30
100. Debruin LS, Harauz G (2007) White matter rafting–membrane microdomains in myelin. Neurochem Res 32:213–228
101. DeBruin LS, Haines JD, Wellhauser LA et al (2005) Developmental partitioning of myelin basic protein into membrane microdomains. J Neurosci Res 80:211–225
102. Sackmann E, Goennenwein S (2006) Cell adhesion as dynamic interplay of lock-and-key, generic and elastic forces. Prog Theor Phys Supp 165:78–99
103. Sackmann E, Bruinsma RF (2002) Cell adhesion as wetting transition? ChemPhysChem 3:262–269
104. Rodríguez-Fernández JL, Riol-Blanco L, Delgado-Martín C (2010) What is an immunological synapse? Microbes Infect 12:438–445
105. Reichardt P, Dornbach B, Gunzer M (2010) APC, T cells, and the immune synapse. Curr Top Microbiol Immunol 340:229–249
106. Foa C, Soler M, Benoliel A-M, Bongrand P (1996) Steric stabilization and cell adhesion. J Mater Sci Mater Med 7:141–148
107. Bell GI, Dembo M, Bongrand P (1984) Cell adhesion. Competition between nonspecific repulsion and specific bonding. Biophys J 45:1051–1064
108. Sabri S, Soler M, Foa C et al (2000) Glycocalyx modulation is a physiological means of regulating cell adhesion. J Cell Sci 113:1589–1600
109. Morris JE (1993) Proteoglycans and the modulation of cell adhesion by steric exclusion. Dev Dyn 196:246–251
110. Dugas JC, Tai YC, Speed TP et al (2006) Functional genomic analysis of oligodendrocyte differentiation. J Neurosci 26:10967–10983
111. Nishiyama A, Komitova M, Suzuki R, Zhu X (2009) Polydendrocytes (NG2 cells): multifunctional cells with lineage plasticity. Nat Rev Neurosci 10:9–22
112. Bouvier-Labit C, Liprandi A, Monti G et al (2002) CD44H is expressed by cells of the oligodendrocyte lineage and by oligodendrogliomas in humans. J Neurooncol 60:127–134
113. Tuohy TMF, Wallingford N, Liu Y et al (2004) CD44 overexpression by oligodendrocytes: a novel mouse model of inflammation-independent demyelination and dysmyelination. Glia 47:335–345
114. Nait Oumesmar B, Vignais L, Duhamel-Clérin E et al (1995) Expression of the highly polysialylated neural cell adhesion molecule during postnatal myelination and following chemically induced demyelination of the adult mouse spinal cord. Eur J Neurosci 7:480–491
115. Stoykova LI, Beesley JS, Grinspan JB, Glick MC (2001) ST8Sia IV mRNA corresponds with the biosynthesis of alpha2,8 sialyl polymers but not oligomers in rat oligodendrocytes. J Neurosci Res 66:497–505
116. Fewou SN, Ramakrishnan H, Büssow H et al (2007) Down-regulation of polysialic acid is required for efficient myelin formation. J Biol Chem 282:16700–16711
117. Winkler S, Stahl RC, Carey DJ, Bansal R (2002) Syndecan-3 and perlecan are differentially expressed by progenitors and mature oligodendrocytes and accumulate in the extracellular matrix. J Neurosci Res 69:477–487
118. Saito M, Yu RK (1986) Further characterization of a myelin-associated neuraminidase: properties and substrate specificity. J Neurochem 47:632–641
119. Saito M, Yu RK (1993) Possible role of myelin-associated neuraminidase in membrane adhesion. J Neurosci Res 36:127–132
120. Bakhti M, Snaidero N, Schneider D et al (2013) Loss of electrostatic cell-surface repulsion mediates myelin membrane adhesion and compaction in the central nervous system. Proc Natl Acad Sci USA 110:3143–3148
121. Möbius W, Patzig J, Nave K-A, Werner HB (2008) Phylogeny of proteolipid proteins: divergence, constraints, and the evolution of novel functions in myelination and neuroprotection. Neuron Glia Biol 4:111–127
122. Popot JL, Pham Dinh D, Dautigny A (1991) Major myelin proteolipid: the 4-alpha-helix topology. J Membr Biol 123:278
123. Boison D, Büssow H, D’Urso D et al (1995) Adhesive properties of proteolipid protein are responsible for the compaction of CNS myelin sheaths. J Neurosci 15:5502–5513
124. Klugmann M, Schwab MH, Pühlhofer A et al (1997) Assembly of CNS myelin in the absence of proteolipid protein. Neuron 18:59–70
125. Griffiths I, Klugmann M, Anderson T et al (1998) Axonal swellings and degeneration in mice lacking the major proteolipid of myelin. Science 280:1610–1613
126. Rosenbluth J, Schiff R, Lam P (2009) Effects of osmolality on PLP-null myelin structure: implications re axon damage. Brain Res 1253:191–197
127. Rosenbluth J, Nave K-A, Mierzwa A, Schiff R (2006) Subtle myelin defects in PLP-null mice. Glia 54:172–182
128. Palaniyar N, Semotok JL, Wood DD et al (1998) Human proteolipid protein (PLP) mediates winding and adhesion of phospholipid membranes but prevents their fusion. Biochim Biophys Acta 1415:85–100
129. Coetzee T, Suzuki K, Nave KA, Popko B (1999) Myelination in the absence of galactolipids and proteolipid proteins. Mol Cell Neurosci 14:41–51
130. Gow A, Southwood CM, Li JS et al (1999) CNS myelin and sertoli cell tight junction strands are absent in Osp/claudin-11 null mice. Cell 99:649–659
131. Kosaras B, Kirschner DA (1990) Radial component of CNS myelin: junctional subunit structure and supramolecular assembly. J Neurocytol 19:187–199
132. Karthigasan J, Kosaras B, Nguyen J, Kirschner DA (1994) Protein and lipid composition of radial component-enriched CNS myelin. J Neurochem 62:1203–1213
133. Chow E, Mottahedeh J, Prins M et al (2005) Disrupted compaction of CNS myelin in an OSP/Claudin-11 and PLP/DM20 double knockout mouse. Mol Cell Neurosci 29:405–413
134. Jackman N, Ishii A, Bansal R (2009) Oligodendrocyte development and myelin biogenesis: parsing out the roles of glycosphingolipids. Physiology 24:290–297
135. Chrast R, Saher G, Nave K-A, Verheijen MHG (2011) Lipid metabolism in myelinating glial cells: lessons from human inherited disorders and mouse models. J Lipid Res 52:419–434
136. Boggs JM, Gao W, Zhao J et al (2010) Participation of galactosylceramide and sulfatide in glycosynapses between oligodendrocyte or myelin membranes. FEBS Lett 584:1771–1778
137. Boggs JM, Menikh A, Rangaraj G (2000) Trans interactions between galactosylceramide and cerebroside sulfate across apposed bilayers. Biophys J 78:874–885
138. Boggs JM, Gao W, Hirahara Y (2008) Myelin glycosphingolipids, galactosylceramide and sulfatide, participate in carbohydrate–carbohydrate interactions between apposed membranes and may form glycosynapses between oligodendrocyte and/or myelin membranes. Biochim Biophys Acta 1780:445–455
139. Kulkarni K, Snyder DS, McIntosh TJ (1999) Adhesion between cerebroside bilayers. Biochemistry 38:15264–15271
140. Cochran FB, Yu RK, Ledeen RW (1982) Myelin gangliosides in vertebrates. J Neurochem 39:773–779
141. Vital C, Brechenmacher C, Reiffers J et al (1983) Uncompacted myelin lamellae in two cases of peripheral neuropathy. Acta Neuropathol 60:252–256
142. Vallat JM, Leboutet MJ, Jauberteau MO et al (1994) Widenings of the myelin lamellae in a typical Guillain-Barré syndrome. Muscle Nerve 17:378–380
143. Roy K, Murtie JC, El-Khodor BF et al (2007) Loss of erbB signaling in oligodendrocytes alters myelin and dopaminergic function, a potential mechanism for neuropsychiatric disorders. Proc Natl Acad Sci USA 104:8131–8136
144. Pollock M, Calder C, Allpress S (1993) Peripheral nerve abnormality in multiple sclerosis. Ann Neurol 2:1–5
145. Sospedra M, Martin R (2005) Immunology of multiple sclerosis. Annu Rev Immunol 23:683–747
146. Payne SC, Bartlett C, Harvey AR et al (2012) Myelin sheath decompaction, axon swelling, and functional loss during chronic secondary degeneration in rat optic nerve. Invest Ophthalmol Vis Sci 53:6093–6101
147. Raine CS, Cannella B, Hauser SL, Genain CP (1999) Demyelination in primate autoimmune encephalomyelitis and acute multiple sclerosis lesions: a case for antigen-specific antibody mediation. Ann Neurol 46:144–160
148. Kettenmann H, Sonnhof U, Schachner M (1983) Exclusive potassium dependence of the membrane potential in cultured mouse oligodendrocytes. J Neurosci 3:500–505
149. Ro H, Carson JH (2004) pH microdomains in oligodendrocytes. J Biol Chem 279:37115–37123
150. Boggs JM, Yip PM, Rangaraj G, Jo E (1997) Effect of posttranslational modifications to myelin basic protein on its ability to aggregate acidic lipid vesicles. Biochemistry 36:5065–5071
151. Beniac DR, Wood DD, Palaniyar N et al (2000) Cryoelectron microscopy of protein-lipid complexes of human myelin basic protein charge isomers differing in degree of citrullination. J Struct Biol 84:80–95
152. Musse AA, Boggs JM, Harauz G (2006) Deimination of membrane-bound myelin basic protein in multiple sclerosis exposes an immunodominant epitope. Proc Natl Acad Sci USA 103:4422–4427
153. Moscarello MA, Pritzker L, Mastronardi FG, Wood DD (2002) Peptidylarginine deiminase: a candidate factor in demyelinating disease. J Neurochem 81:335–343
154. Imgrund S, Hartmann D, Farwanah H et al (2009) Adult ceramide synthase 2 (CERS2)-deficient mice exhibit myelin sheath defects, cerebellar degeneration, and hepatocarcinomas. J Biol Chem 284:33549–33560
155. Ben-David O, Pewzner-Jung Y, Brenner O, Laviad EL, Kogot-Levin A, Weissberg I, Biton IE, Pienik R, Wang E, Kelly S, Alroy J, Raas-Rothschild A, Friedman A, Brügger B, Merrill AH Jr, Futerman AH (2011) Encephalopathy caused by ablation of very long acyl chain ceramide synthesis may be largely due to reduced galactosylceramide levels. J Biol Chem 286(34):30022–30033
156. Young KM, Psachoulia K, Tripathi RB et al (2013) Oligodendrocyte dynamics in the healthy adult CNS: evidence for myelin remodeling. Neuron 77:873–885
157. Czopka T, Ffrench-Constant C, Lyons DA (2013) Individual oligodendrocytes have only a few hours in which to generate new myelin sheaths in vivo. Dev Cell 25:599–609
158. Mangin J-M, Li P, Scafidi J, Gallo V (2012) Experience-dependent regulation of NG2 progenitors in the developing barrel cortex. Nat Neurosci 15:1192–1194
159. Makinodan M, Rosen KM, Ito S, Corfas G (2012) A critical period for social experience-dependent oligodendrocyte maturation and myelination. Science 337:1357–1360
160. Liu J, Dietz K, DeLoyht JM et al (2012) Impaired adult myelination in the prefrontal cortex of socially isolated mice. Nat Neurosci 15:1621–1623