Wrapping it up: the cell biology of myelination

Current Opinion in Neurobiology

Volumn 17, Issue 5, 2007, Pages 533-540

  Simons, Mikael ^a,b   Trotter, Jacqueline ^c  

^a Institute for Biochemistry and Molecular Cell Biology   (Germany)

^b MAX PLANCK INSTITUTE OF EXPERIMENTAL MEDICINE   (Germany)

^c JOHANNES GUTENBERG UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

MYELIN; MYELIN BASIC PROTEIN; MYELIN PROTEIN;

CELL MEMBRANE; CYTOLOGY; LIPID COMPOSITION; MYELINATION; NERVE CONDUCTION; NERVE FIBER; NERVE POTENTIAL; NERVE SHEATH; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; OLIGODENDROGLIA; PERIPHERAL NERVOUS SYSTEM; POLARIZATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; REVIEW; SCHWANN CELL;

ANIMALS; BIOLOGY; MODELS, BIOLOGICAL; MYELIN BASIC PROTEINS; MYELIN PROTEINS; SCHWANN CELLS;

EID: 37549007582     PISSN: 09594388     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.conb.2007.08.003     Document Type: Review

References (58)

1. Yin X., Baek R.C., Kirschner D.A., Peterson A., Fujii Y., Nave K.A., Macklin W.B., and Trapp B.D. Evolution of a neuroprotective function of central nervous system myelin. J Cell Biol 172 (2006) 469-478
2. Lappe-Siefke C., Goebbels S., Gravel M., Nicksch E., Lee J., Braun P.E., Griffiths I.R., and Nave K.A. Disruption of Cnp1 uncouples oligodendroglial functions in axonal support and myelination. Nat Genet 33 (2003) 366-374
3. Griffiths I., Klugmann M., Anderson T., Yool D., Thomson C., Schwab M.H., Schneider A., Zimmermann F., McCulloch M., Nadon N., et al. Axonal swellings and degeneration in mice lacking the major proteolipid of myelin. Science 280 (1998) 1610-1613
4. Schafer D.P., and Rasband M.N. Glial regulation of the axonal membrane at nodes of Ranvier. Curr Opin Neurobiol 16 (2006) 508-514
5. Barres B.A., and Raff M.C. Axonal control of oligodendrocyte development. J Cell Biol 147 (1999) 1123-1128
6. Sherman D.L., and Brophy P.J. Mechanisms of axon ensheathment and myelin growth. Nat Rev Neurosci 6 (2005) 683-690
7. Kramer E.M., Schardt A., and Nave K.A. Membrane traffic in myelinating oligodendrocytes. Microsc Res Tech 52 (2001) 656-671
8. Simons M., and Trajkovic K. Neuron-glia communication in the control of oligodendrocyte function and myelin biogenesis. J Cell Sci 119 (2006) 4381-4389
9. Jessen K.R., and Mirsky R. The origin and development of glial cells in peripheral nerves. Nat Rev Neurosci 6 (2005) 671-682
10. Taveggia C., Zanazzi G., Petrylak A., Yano H., Rosenbluth J., Einheber S., Xu X., Esper R.M., Loeb J.A., Shrager P., et al. Neuregulin-1 type III determines the ensheathment fate of axons. Neuron 47 (2005) 681-694. This study identifies neuregulin-1 type III on the axon as the crucial factor in determining whether a Schwann cell will form myelin or not.
11. Michailov G.V., Sereda M.W., Brinkmann B.G., Fischer T.M., Haug B., Birchmeier C., Role L., Lai C., Schwab M.H., and Nave K.A. Axonal neuregulin-1 regulates myelin sheath thickness. Science 304 (2004) 700-703
12. Chen Z.L., and Strickland S. Laminin gamma1 is critical for Schwann cell differentiation, axon myelination, and regeneration in the peripheral nerve. J Cell Biol 163 (2003) 889-899
13. Yu W.M., Feltri M.L., Wrabetz L., Strickland S., and Chen Z.L. Schwann cell-specific ablation of laminin gamma1 causes apoptosis and prevents proliferation. J Neurosci 25 (2005) 4463-4472
14. Yang D., Bierman J., Tarumi Y.S., Zhong Y.P., Rangwala R., Proctor T.M., Miyagoe-Suzuki Y., Takeda S., Miner J.H., Sherman L.S., et al. Coordinate control of axon defasciculation and myelination by laminin-2 and -8. J Cell Biol 168 (2005) 655-666
15. Grove M., Komiyama N.H., Nave K.A., Grant S.G., Sherman D.L., and Brophy P.J. FAK is required for axonal sorting by Schwann cells. J Cell Biol 176 (2007) 277-282
16. Li S., Liquari P., McKee K.K., Harrison D., Patel R., Lee S., and Yurchenco P.D. Laminin-sulfatide binding initiates basement membrane assembly and enables receptor signaling in Schwann cells and fibroblasts. J Cell Biol 169 (2005) 179-189
17. Feltri M.L., Graus Porta D., Previtali S.C., Nodari A., Migliavacca B., Cassetti A., Littlewood-Evans A., Reichardt L.F., Messing A., Quattrini A., et al. Conditional disruption of beta 1 integrin in Schwann cells impedes interactions with axons. J Cell Biol 156 (2002) 199-209
18. Benninger Y., Thurnherr T., Pereira J.A., Krause S., Wu X., Chrostek-Grashoff A., Herzog D., Nave K.A., Franklin R.J., Meijer D., et al. Essential and distinct roles for cdc42 and rac1 in the regulation of Schwann cell biology during peripheral nervous system development. J Cell Biol 177 (2007) 1051-1061
19. Nodari A., Zambroni D., Quattrini A., Court F.A., D'Urso A., Recchia A., Tybulewicz V.L., Wrabetz L., and Feltri M.L. {beta}1 integrin activates Rac1 in Schwann cells to generate radial lamellae during axonal sorting and myelination. J Cell Biol 177 (2007) 1063-1075
20. Spiegel I., Adamsky K., Eshed Y., Milo R., Sabanay H., Sarig-Nadir O., Horresh I., Scherer S.S., Rasband M.N., and Peles E. A central role for Necl4 (SynCAM4) in Schwann cell-axon interaction and myelination. Nat Neurosci 10 (2007) 861-869. These two studies identify Necl4 (SynCAM4) on Schwann cells and Necl1 (SynCAM3) on the axon as an essential pair of proteins in mediating the glia-axon interactions necessary for myelination.
21. Maurel P., Einheber S., Galinska J., Thaker P., Lam I., Rubin M.B., Scherer S.S., Murakami Y., Gutmann D.H., and Salzer J.L. Nectin-like proteins mediate axon-Schwann cell interactions along the internode and are essential for myelination. J Cell Biol 178 (2007) 861-874. These two studies identify Necl4 (SynCAM4) on Schwann cells and Necl1 (SynCAM3) on the axon as an essential pair of proteins in mediating the glia-axon interactions necessary for myelination.
22. Tait S., Gunn-Moore F., Collinson J.M., Huang J., Lubetzki C., Pedraza L., Sherman D.L., Colman D.R., and Brophy P.J. An oligodendrocyte cell adhesion molecule at the site of assembly of the paranodal axo-glial junction. J Cell Biol 150 (2000) 657-666
23. Traka M., Dupree J.L., Popko B., and Karagogeos D. The neuronal adhesion protein TAG-1 is expressed by Schwann cells and oligodendrocytes and is localized to the juxtaparanodal region of myelinated fibers. J Neurosci 22 (2002) 3016-3024
24. Eshed Y., Feinberg K., Poliak S., Sabanay H., Sarig-Nadir O., Spiegel I., Bermingham Jr. J.R., and Peles E. Gliomedin mediates Schwann cell-axon interaction and the molecular assembly of the nodes of Ranvier. Neuron 47 (2005) 215-229
25. Eshed Y., Feinberg K., Carey D.J., and Peles E. Secreted gliomedin is a perinodal matrix component of peripheral nerves. J Cell Biol 177 (2007) 551-562
26. Salzer J.L. Polarized domains of myelinated axons. Neuron 40 (2003) 297-318
27. Knust E., and Bossinger O. Composition and formation of intercellular junctions in epithelial cells. Science 298 (2002) 1955-1959
28. Chan J.R., Jolicoeur C., Yamauchi J., Elliott J., Fawcett J.P., Ng B.K., and Cayouette M. The polarity protein Par-3 directly interacts with p75NTR to regulate myelination. Science 314 (2006) 832-836. This work establishes an important link between the Par polarity complex and the process of myelination. Par-3 was shown to directly associate and recruit the p75 neurotrophin receptor to the axon-glial junction, forming a complex necessary for myelination.
29. Hartline D.K., and Colman D.R. Rapid conduction and the evolution of giant axons and myelinated fibers. Curr Biol 17 (2007) R29-R35
30. Edenfeld G., Volohonsky G., Krukkert K., Naffin E., Lammel U., Grimm A., Engelen D., Reuveny A., Volk T., and Klambt C. The splicing factor crooked neck associates with the RNA-binding protein HOW to control glial cell maturation in Drosophila. Neuron 52 (2006) 969-980. A genetic screen in Drosophila identifies a novel function of two regulators of mRNA splicing. Crooked neck and held out wings in peripheral glial were shown to be necessary for the ensheathment of peripheral axons. These splicing components translocate to the nucleus to promote the splicing of genes involved in the assembly of cellular junctions.
31. Ebersole T.A., Chen Q., Justice M.J., and Artzt K. The quaking gene product necessary in embryogenesis and myelination combines features of RNA binding and signal transduction proteins. Nat Genet 12 (1996) 260-265
32. Bhat M.A. Molecular organization of axo-glial junctions. Curr Opin Neurobiol 13 (2003) 552-559
33. Colognato H., and ffrench-Constant C. Mechanisms of glial development. Curr Opin Neurobiol 14 (2004) 37-44
34. Kessaris N., Fogarty M., Iannarelli P., Grist M., Wegner M., and Richardson W.D. Competing waves of oligodendrocytes in the forebrain and postnatal elimination of an embryonic lineage. Nat Neurosci 9 (2006) 173-179
35. Kirby B.B., Takada N., Latimer A.J., Shin J., Carney T.J., Kelsh R.N., and Appel B. In vivo time-lapse imaging shows dynamic oligodendrocyte progenitor behavior during zebrafish development. Nat Neurosci 9 (2006) 1506-1511. This is the first extensive in vivo time-lapse microscopy study of oligodendroglial cells. Using zebrafish as a model system, this study shows that OPCs continuously extend and retract numerous filopodium-like processes. These dynamic processes seem to sense nearby OPCs necessary to regulate the uniform spacing of oligodendrocytes.
36. Kim H.J., DiBernardo A.B., Sloane J.A., Rasband M.N., Solomon D., Kosaras B., Kwak S.P., and Vartanian T.K. WAVE1 is required for oligodendrocyte morphogenesis and normal CNS myelination. J Neurosci 26 (2006) 5849-5859
37. Bacon C., Lakics V., Machesky L., and Rumsby M. N-WASP regulates extension of filopodia and processes by oligodendrocyte progenitors, oligodendrocytes, and Schwann cells - implications for axon ensheathment at myelination. Glia 55 (2007) 844-858
38. Osterhout D.J., Wolven A., Wolf R.M., Resh M.D., and Chao M.V. Morphological differentiation of oligodendrocytes requires activation of Fyn tyrosine kinase. J Cell Biol 145 (1999) 1209-1218
39. Klein C., Kramer E.M., Cardine A.M., Schraven B., Brandt R., and Trotter J. Process outgrowth of oligodendrocytes is promoted by interaction of fyn kinase with the cytoskeletal protein tau. J Neurosci 22 (2002) 698-707
40. Liang X., Draghi N.A., and Resh M.D. Signaling from integrins to Fyn to Rho family GTPases regulates morphologic differentiation of oligodendrocytes. J Neurosci 24 (2004) 7140-7149
41. Kippert A., Trajkovic K., Rajendran L., Ries J., and Simons M. Rho regulates membrane transport in the endocytic pathway to control plasma membrane specialization in oligodendroglial cells. J Neurosci 27 (2007) 3560-3570
42. Mi S., Miller R.H., Lee X., Scott M.L., Shulag-Morskaya S., Shao Z., Chang J., Thill G., Levesque M., Zhang M., et al. LINGO-1 negatively regulates myelination by oligodendrocytes. Nat Neurosci 8 (2005) 745-751
43. Lee X., Yang Z., Shao Z., Rosenberg S.S., Levesque M., Pepinsky R.B., Qiu M., Miller R.H., Chan J.R., and Mi S. NGF regulates the expression of axonal LINGO-1 to inhibit oligodendrocyte differentiation and myelination. J Neurosci 27 (2007) 220-225
44. Brockschnieder D., Sabanay H., Riethmacher D., and Peles E. Ermin, a myelinating oligodendrocyte-specific protein that regulates cell morphology. J Neurosci 26 (2006) 757-762
45. Shi S.H., Jan L.Y., and Jan Y.N. Hippocampal neuronal polarity specified by spatially localized mPar3/mPar6 and PI 3-kinase activity. Cell 112 (2003) 63-75
46. Anitei M., Ifrim M., Ewart M.A., Cowan A.E., Carson J.H., Bansal R., and Pfeiffer S.E. A role for Sec8 in oligodendrocyte morphological differentiation. J Cell Sci 119 (2006) 807-818
47. Trajkovic K., Dhaunchak A.S., Goncalves J.T., Wenzel D., Schneider A., Bunt G., Nave K.A., and Simons M. Neuron to glia signaling triggers myelin membrane exocytosis from endosomal storage sites. J Cell Biol 172 (2006) 937-948. This study shows that neurons control membrane trafficking in oligodendrocytes. Neurons reduce the rate of endocytosis in oligodendrocytes and promote the exocytosis of membrane from endosomal storage pools.
48. Perens E.A., and Shaham S. C. elegans daf-6 encodes a patched-related protein required for lumen formation. Dev Cell 8 (2005) 893-906
49. Lubarsky B., and Krasnow M.A. Tube morphogenesis: making and shaping biological tubes. Cell 112 (2003) 19-28
50. Simons M., Kramer E.M., Thiele C., Stoffel W., and Trotter J. Assembly of myelin by association of proteolipid protein with cholesterol- and galactosylceramide-rich membrane domains. J Cell Biol 151 (2000) 143-154
51. Taylor C.M., Coetzee T., and Pfeiffer S.E. Detergent-insoluble glycosphingolipid/cholesterol microdomains of the myelin membrane. J Neurochem 81 (2002) 993-1004
52. Erne B., Sansano S., Frank M., and Schaeren-Wiemers N. Rafts in adult peripheral nerve myelin contain major structural myelin proteins and myelin and lymphocyte protein (MAL) and CD59 as specific markers. J Neurochem 82 (2002) 550-562
53. Krämer E.M., Koch T., Niehaus A., and Trotter J. Oligodendrocytes direct glycosyl phosphatidylinositol-anchored proteins to the myelin sheath in glycosphingolipid-rich complexes. J Biol Chem 272 (1997) 8937-8945
54. Barbarese E., Brumwell C., Kwon S., Cui H., and Carson J.H. RNA on the road to myelin. J Neurocytol 28 (1999) 263-270
55. Harauz G., Ishiyama N., Hill C.M., Bates I.R., Libich D.S., and Fares C. Myelin basic protein-diverse conformational states of an intrinsically unstructured protein and its roles in myelin assembly and multiple sclerosis. Micron 35 (2004) 503-542
56. Fitzner D., Schneider A., Kippert A., Mobius W., Willig K.I., Hell S.W., Bunt G., Gaus K., and Simons M. Myelin basic protein-dependent plasma membrane reorganization in the formation of myelin. EMBO J 25 (2006) 5037-5048. This paper shows that neurons increase the lipid packing of the myelin-forming bilayer in oligodendrocytes and that MBP is involved in this process of plasma membrane rearrangement. MBP seems to act as a clustering agent bringing together the myelin membrane components at the plasma membrane.
57. Saher G., Brugger B., Lappe-Siefke C., Mobius W., Tozawa R., Wehr M.C., Wieland F., Ishibashi S., and Nave K.A. High cholesterol level is essential for myelin membrane growth. Nat Neurosci 8 (2005) 468-475. This study reports that oligodendrocytes with a conditional knockout of squalene synthetase, an enzyme required for cholesterol biosynthesis, are viable. Compensation occurs by uptake of cholesterol from an external source, thereby maintaining the stoichiometry of myelin components.
58. Coetzee T., Fujita N., Dupree J., Shi R., Blight A., Suzuki K., Suzuki K., and Popko B. Myelination in the absence of galactocerebroside and sulfatide: normal structure with abnormal function and regional instability. Cell 86 (1996) 209-219