Central nervous system myelin: Structure, synthesis and assembly

Trends in Cell Biology

Volumn 21, Issue 10, 2011, Pages 585-593

  Aggarwal, Shweta ^a   Yurlova, Larisa ^a   Simons, Mikael ^a,b  

^a MAX PLANCK INSTITUTE OF EXPERIMENTAL MEDICINE   (Germany)

^b UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

MYELIN; MYELIN BASIC PROTEIN; MYELIN OLIGODENDROCYTE GLYCOPROTEIN;

CELL MEMBRANE; CENTRAL NERVOUS SYSTEM; CYTOLOGY; GENE EXPRESSION; GENETIC TRANSCRIPTION; HUMAN; MICROTUBULE; MULTIPLE SCLEROSIS; MYELIN SHEATH; MYELINATION; NERVE CELL; NERVE FIBER; NONHUMAN; OLIGODENDROGLIA; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN STABILITY; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; REGULATORY MECHANISM; REMYELINIZATION; REVIEW; SCHWANN CELL; SIGNAL TRANSDUCTION;

ANIMALS; AXONS; CELL MEMBRANE; CENTRAL NERVOUS SYSTEM; DEMYELINATING DISEASES; HUMANS; MICE; MYELIN SHEATH; OLIGODENDROGLIA;

EID: 80053109845     PISSN: 09628924     EISSN: 18793088     Source Type: Journal    
DOI: 10.1016/j.tcb.2011.06.004     Document Type: Review

References (82)

1. Hartline D.K., Colman D.R. Rapid conduction and the evolution of giant axons and myelinated fibers. Curr. Biol. 2007, 17:R29-R35.
2. Simons M., Trotter J. Wrapping it up: the cell biology of myelination. Curr. Opin. Neurobiol. 2007, 17:533-540.
3. Sherman D.L., Brophy P.J. Mechanisms of axon ensheathment and myelin growth. Nat. Rev. Neurosci. 2005, 6:683-690.
4. Baumann N., Pham-Dinh D. Biology of oligodendrocyte and myelin in the mammalian central nervous system. Physiol. Rev. 2001, 81:871-927.
5. Waxman S.G. Axonal conduction and injury in multiple sclerosis: the role of sodium channels. Nat. Rev. Neurosci. 2006, 7:932-941.
6. Singer S.J., Nicolson G.L. The fluid mosaic model of the structure of cell membranes. Science 1972, 175:720-731.
7. Hartline D.K. What is myelin?. Neuron Glia Biol. 2008, 4:153-163.
8. Mobius W., et al. Electron microscopy of the mouse central nervous system. Methods Cell Biol. 2010, 96:475-512.
9. Velumian A.A., et al. Visualization of cytoplasmic diffusion within living myelin sheaths of CNS white matter axons using microinjection of the fluorescent dye Lucifer Yellow. Neuroimage 2010, 56:27-34.
10. Maglione M., et al. Oligodendrocytes in mouse corpus callosum are coupled via gap junction channels formed by connexin47 and connexin32. Glia 2010, 58:1104-1117.
11. Kamasawa N., et al. Connexin-47 and connexin-32 in gap junctions of oligodendrocyte somata, myelin sheaths, paranodal loops and Schmidt-Lanterman incisures: implications for ionic homeostasis and potassium siphoning. Neuroscience 2005, 136:65-86.
12. Mierzwa A., et al. Permeability of the paranodal junction of myelinated nerve fibers. J. Neurosci. 2010, 30:15962-15968.
13. Shroff S., et al. Paranodal permeability in 'myelin mutants'. Glia 2011, 59:1447-1457.
14. Hall S.M., Williams P.L. Studies on the 'incisures' of Schmidt and Lanterman. J. Cell Sci. 1970, 6:767-791.
15. Taveggia C., et al. Neuregulin-1 type III determines the ensheathment fate of axons. Neuron 2005, 47:681-694.
16. Michailov G.V., et al. Axonal neuregulin-1 regulates myelin sheath thickness. Science 2004, 304:700-703.
17. Piaton G., et al. Axon-oligodendrocyte interactions during developmental myelination, demyelination and repair. J. Neurochem. 2010, 114:1243-1260.
18. Taveggia C., et al. Signals to promote myelin formation and repair. Nat. Rev. Neurol. 2010, 6:276-287.
19. Chong S.Y., Chan J.R. Tapping into the glial reservoir: cells committed to remaining uncommitted. J. Cell Biol. 2010, 188:305-312.
20. Emery B. Regulation of oligodendrocyte differentiation and myelination. Science 2010, 330:779-782.
21. Dugas J.C., et al. Dicer1 and miR-219 are required for normal oligodendrocyte differentiation and myelination. Neuron 2010, 65:597-611.
22. Zhao X., et al. MicroRNA-mediated control of oligodendrocyte differentiation. Neuron 2010, 65:612-626.
23. Shin D., et al. Dicer ablation in oligodendrocytes provokes neuronal impairment in mice. Annu. Neurol. 2009, 66:843-857.
24. Kim J.Y., et al. HDAC1 nuclear export induced by pathological conditions is essential for the onset of axonal damage. Nat. Neurosci. 2010, 13:180-189.
25. Budde H., et al. Control of oligodendroglial cell number by the miR-17-92 cluster. Development 2010, 137:2127-2132.
26. Liu J., Casaccia P. Epigenetic regulation of oligodendrocyte identity. Trends Neurosci. 2010, 33:193-201.
27. Fancy S.P., et al. Dysregulation of the Wnt pathway inhibits timely myelination and remyelination in the mammalian CNS. Genes Dev. 2009, 23:1571-1585.
28. Tawk M., et al. Wnt/β-catenin signaling is an essential and direct driver of myelin gene expression and myelinogenesis. J. Neurosci. 2011, 31:3729-3742.
29. Emery B., et al. Myelin gene regulatory factor is a critical transcriptional regulator required for CNS myelination. Cell 2009, 138:172-185.
30. Howng S.Y., et al. ZFP191 is required by oligodendrocytes for CNS myelination. Genes Dev. 2010, 24:301-311.
31. Baron W., Hoekstra D. On the biogenesis of myelin membranes: sorting, trafficking and cell polarity. FEBS Lett. 2010, 584:1760-1770.
32. Aggarwal, S. et al. (2011) A size barrier limits protein diffusion at the cell surface to generate lipid-rich myelin-membrane sheets. Dev. Cell. In press. doi:10.1016/j.devcel.2011.08.001.
33. White R., et al. Activation of oligodendroglial Fyn kinase enhances translation of mRNAs transported in hnRNP A2-dependent RNA granules. J. Cell Biol. 2008, 181:579-586.
34. Lyons D.A., et al. Kif1b is essential for mRNA localization in oligodendrocytes and development of myelinated axons. Nat. Genet. 2009, 41:854-858.
35. Laursen L.S., et al. Translation of myelin basic protein mRNA in oligodendrocytes is regulated by integrin activation and hnRNP-K. J. Cell Biol. 2011, 192:797-811.
36. Karsenti E. Self-organization in cell biology: a brief history. Nat. Rev. Mol. Cell Biol. 2008, 9:255-262.
37. Millor J., et al. Self-organized defensive behavior in honeybees. Proc. Natl. Acad. Sci. U.S.A. 1999, 96:12611-12615.
38. Misteli T. The concept of self-organization in cellular architecture. J. Cell Biol. 2001, 155:181-185.
39. Whitesides G.M., Grzybowski B. Self-assembly at all scales. Science 2002, 295:2418-2421.
40. Traka M., et al. A genetic mouse model of adult-onset, pervasive central nervous system demyelination with robust remyelination. Brain 2010, 133:3017-3029.
41. Pohl H.B., et al. Genetically induced adult oligodendrocyte cell death is associated with poor myelin clearance, reduced remyelination, and axonal damage. J. Neurosci. 2011, 31:1069-1080.
42. Saher G., Simons M. Cholesterol and myelin biogenesis. Subcell. Biochem. 2010, 51:489-508.
43. Alderson N.L., et al. The human FA2H gene encodes a fatty acid 2-hydroxylase. J. Biol. Chem. 2004, 279:48562-48568.
44. Eckhardt M., et al. A mammalian fatty acid hydroxylase responsible for the formation of alpha-hydroxylated galactosylceramide in myelin. Biochem. J. 2005, 388(Pt 1):245-254.
45. Zoller I., et al. Absence of 2-hydroxylated sphingolipids is compatible with normal neural development but causes late-onset axon and myelin sheath degeneration. J. Neurosci. 2008, 28:9741-9754.
46. O'Brien J.S. Stability of the myelin membrane. Science 1965, 147:1099-1107.
47. Coetzee T., et al. Myelination in the absence of galactocerebroside and sulfatide: normal structure with abnormal function and regional instability. Cell 1996, 86:209-219.
48. Bosio A., et al. Functional breakdown of the lipid bilayer of the myelin membrane in central and peripheral nervous system by disrupted galactocerebroside synthesis. Proc. Natl. Acad. Sci. U.S.A. 1996, 93:13280-13285.
49. Saadat L., et al. Absence of oligodendroglial glucosylceramide synthesis does not result in CNS myelin abnormalities or alter the dysmyelinating phenotype of CGT-deficient mice. Glia 2010, 58:391-398.
50. Meixner M., et al. Myelination in the absence of UDP-galactose:ceramide galactosyl-transferase and fatty acid 2 -hydroxylase. BMC Neurosci. 2011, 12:22.
51. Potter K.A., et al. Central nervous system dysfunction in a mouse model of Fa2h deficiency. Glia 2011, 59:1009-1021.
52. Imgrund S., et al. Adult ceramide synthase 2 (CERS2)-deficient mice exhibit myelin sheath defects, cerebellar degeneration, and hepatocarcinomas. J. Biol. Chem. 2009, 284:33549-33560.
53. Pewzner-Jung Y., et al. A critical role for ceramide synthase 2 in liver homeostasis. I. Alterations in lipid metabolic pathways. J. Biol. Chem. 2010, 285:10902-10910.
54. Pewzner-Jung Y., et al. A critical role for ceramide synthase 2 in liver homeostasis. II. Insights into molecular changes leading to hepatopathy. J. Biol. Chem. 2010, 285:10911-10923.
55. Hess M.W., et al. 5000-year-old myelin: uniquely intact in molecular configuration and fine structure. Curr. Biol. 1998, 8:R512-R513.
56. Teigler A., et al. Defects in myelination, paranode organization and Purkinje cell innervation in the ether lipid-deficient mouse cerebellum. Hum. Mol. Genet. 2009, 18:1897-1908.
57. Rodemer C., et al. Inactivation of ether lipid biosynthesis causes male infertility, defects in eye development and optic nerve hypoplasia in mice. Hum. Mol. Genet. 2003, 12:1881-1895.
58. Harauz G., et al. Myelin basic protein-diverse conformational states of an intrinsically unstructured protein and its roles in myelin assembly and multiple sclerosis. Micron 2004, 35:503-542.
59. Nawaz S., et al. 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. 2009, 29:4794-4807.
60. Musse A.A., et al. Myelin basic protein as a 'PI(4,5)P2-modulin': a new biological function for a major central nervous system protein. Biochemistry 2008, 47:10372-10382.
61. Bates I.R., et al. Membrane-anchoring and charge effects in the interaction of myelin basic protein with lipid bilayers studied by site-directed spin labeling. J. Biol. Chem. 2003, 278:29041-29047.
62. Bates I.R., et al. An immunodominant epitope of myelin basic protein is an amphipathic alpha-helix. J. Biol. Chem. 2004, 279:5757-5764.
63. Musse A.A., et al. Deimination of membrane-bound myelin basic protein in multiple sclerosis exposes an immunodominant epitope. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:4422-4427.
64. Hu Y., et al. Synergistic interactions of lipids and myelin basic protein. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:13466-13471.
65. McLaurin J., et al. Localization of basic proteins in human myelin. J. Neurosci. Res. 1993, 35:618-628.
66. Min Y., et al. Interaction forces and adhesion of supported myelin lipid bilayers modulated by myelin basic protein. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:3154-3159.
67. Klugmann M., et al. Assembly of CNS myelin in the absence of proteolipid protein. Neuron 1997, 18:59-70.
68. Winterstein C., et al. Distinct endocytic recycling of myelin proteins promotes oligodendroglial membrane remodeling. J. Cell Sci. 2008, 121:834-842.
69. Kippert A., et al. Rho regulates membrane transport in the endocytic pathway to control plasma membrane specialization in oligodendroglial cells. J. Neurosci. 2007, 27:3560-3570.
70. Trajkovic K., et al. Neuron to glia signaling triggers myelin membrane exocytosis from endosomal storage sites. J. Cell Biol. 2006, 172:937-948.
71. Bakhti M., et al. Inhibition of myelin membrane sheath formation by oligodendrocyte-derived exosome-like vesicles. J. Biol. Chem. 2011, 286:787-796.
72. Hsu C., et al. Regulation of exosome secretion by Rab35 and its GTPase-activating proteins TBC1D10A-C. J. Cell Biol. 2010, 189:223-232.
73. Kramer-Albers E.M., et al. Oligodendrocytes secrete exosomes containing major myelin and stress-protective proteins: trophic support for axons?. Proteomics Clin. Appl. 2007, 1:1446-1461.
74. Fitzner D., et al. Selective transfer of exosomes from oligodendrocytes to microglia by macropinocytosis. J. Cell Sci. 2011, 124(Pt 3):447-458.
75. Novak N., et al. N-WASP is required for membrane wrapping and myelination by Schwann cells. J. Cell Biol. 2011, 192:243-250.
76. Dupree J.L., Popko B. Genetic dissection of myelin galactolipid function. J. Neurocytol. 1999, 28:271-279.
77. Werner H.B., et al. Proteolipid protein is required for transport of sirtuin 2 into CNS myelin. J. Neurosci. 2007, 27:7717-7730.
78. Dhaunchak A.S., et al. A proteome map of axoglial specializations isolated and purified from human central nervous system. Glia 2010, 58:1949-1960.
79. Ishii A., et al. Human myelin proteome and comparative analysis with mouse myelin. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:14605-14610.
80. Larocca J.N., Norton W.T. Isolation of myelin. Curr. Protoc. Cell Biol. 2007, Chapter 3:Unit3.25.
81. Chrast R., et al. Lipid metabolism in myelinating glial cells: lessons from human inherited disorders and mouse models. J. Lipid Res. 2011, 52:419-434.
82. Parasassi T., et al. Phase fluctuation in phospholipid membranes revealed by Laurdan fluorescence. Biophys. J. 1990, 57:1179-1186.