Cell polarity in myelinating glia: From membrane flow to diffusion barriers

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1821, Issue 8, 2012, Pages 1146-1153

  Simons, Mikael ^a,b   Snaidero, Nicolas ^a   Aggarwal, Shweta ^a  

^a MAX PLANCK INSTITUTE OF EXPERIMENTAL MEDICINE   (Germany)

^b UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

Myelin; Neuron; Oligodendrocyte; Polarity

Indexed keywords

LIPID; MYELIN;

CELL MEMBRANE; CELL POLARITY; CELL VACUOLE; CYTOPLASM; GLIA; HUMAN; MEMBRANE TRANSPORT; MYELINATION; NONHUMAN; PRIORITY JOURNAL; REVIEW;

ANIMALS; BIOLOGICAL TRANSPORT; CELL MEMBRANE; CELL POLARITY; CYTOPLASM; DIFFUSION; EXOCYTOSIS; HUMANS; LIPID METABOLISM; MEMBRANE PROTEINS; MODELS, MOLECULAR; MYELIN SHEATH; NEURONS; SCHWANN CELLS; TRANSPORT VESICLES;

EID: 84862164961     PISSN: 13881981     EISSN: 18792618     Source Type: Journal    
DOI: 10.1016/j.bbalip.2012.01.011     Document Type: Review

References (84)

1. D.L. Sherman, and P.J. Brophy Mechanisms of axon ensheathment and myelin growth Nat. Rev. Neurosci. 6 2005 683 690 (Pubitemid 43160317)
2. S. Aggarwal, L. Yurlova, and M. Simons Central nervous system myelin: structure, synthesis and assembly Trends Cell Biol. 21 2011 585 593
3. W. Baron, and D. Hoekstra On the biogenesis of myelin membranes: sorting, trafficking and cell polarity FEBS Lett. 584 2010 1760 1770
4. E.J. Arroyo, and S.S. Scherer On the molecular architecture of myelinated fibers Histochem. Cell Biol. 113 2000 1 18 (Pubitemid 30164404)
5. J.L. Salzer Polarized domains of myelinated axons Neuron 40 2003 297 318 (Pubitemid 37244097)
6. J.L. Salzer, P.J. Brophy, and E. Peles Molecular domains of myelinated axons in the peripheral nervous system Glia 56 2008 1532 1540
7. I. Mellman, and W.J. Nelson Coordinated protein sorting, targeting and distribution in polarized cells Nat. Rev. Mol. Cell Biol. 9 2008 833 845
8. K. Mostov, T. Su, and M. ter Beest Polarized epithelial membrane traffic: conservation and plasticity Nat. Cell Biol. 5 2003 287 293 (Pubitemid 36432292)
9. N. Baumann, and D. Pham-Dinh Biology of oligodendrocyte and myelin in the mammalian central nervous system Physiol. Rev. 81 2001 871 927 (Pubitemid 32267079)
10. R. Chrast, G. Saher, K.A. Nave, and M.H. Verheijen Lipid metabolism in myelinating glial cells: lessons from human inherited disorders and mouse models J. Lipid Res. 52 2011 419 434
11. P. Wood, F. Moya, C. Eldridge, G. Owens, B. Ranscht, M. Schachner, M. Bunge, and R. Bunge Studies of the initiation of myelination by Schwann cells Ann. N. Y. Acad. Sci. 605 1990 1 14
12. K.R. Jessen, and R. Mirsky The origin and development of glial cells in peripheral nerves Nat. Rev. Neurosci. 6 2005 671 682 (Pubitemid 43160316)
13. K.A. Nave, and J.L. Salzer Axonal regulation of myelination by neuregulin 1 Curr. Opin. Neurobiol. 16 2006 492 500 (Pubitemid 44466397)
14. P. Maurel, S. Einheber, J. Galinska, P. Thaker, I. Lam, M.B. Rubin, S.S. Scherer, Y. Murakami, D.H. Gutmann, and J.L. Salzer Nectin-like proteins mediate axon Schwann cell interactions along the internode and are essential for myelination J. Cell Biol. 178 2007 861 874 (Pubitemid 47347369)
15. I. Spiegel, K. Adamsky, Y. Eshed, R. Milo, H. Sabanay, O. Sarig-Nadir, I. Horresh, S.S. Scherer, M.N. Rasband, and E. Peles A central role for Necl4 (SynCAM4) in Schwann cell-axon interaction and myelination Nat. Neurosci. 10 2007 861 869 (Pubitemid 47013431)
16. M.A. Chernousov, W.M. Yu, Z.L. Chen, D.J. Carey, and S. Strickland Regulation of Schwann cell function by the extracellular matrix Glia 56 2008 1498 1507
17. F.A. Court, L. Wrabetz, and M.L. Feltri Basal lamina: Schwann cells wrap to the rhythm of space-time Curr. Opin. Neurobiol. 16 2006 501 507 (Pubitemid 44479837)
18. A. Nodari, D. Zambroni, A. Quattrini, F.A. Court, A. D'Urso, A. Recchia, V.L. Tybulewicz, L. Wrabetz, and M.L. Feltri {beta}1 integrin activates Rac1 in Schwann cells to generate radial lamellae during axonal sorting and myelination J. Cell Biol. 177 2007 1063 1075 (Pubitemid 46955710)
19. J.A. Pereira, Y. Benninger, R. Baumann, A.F. Goncalves, M. Ozcelik, T. Thurnherr, N. Tricaud, D. Meijer, R. Fassler, U. Suter, and J.B. Relvas Integrin-linked kinase is required for radial sorting of axons and Schwann cell remyelination in the peripheral nervous system J. Cell Biol. 185 2009 147 161
20. Y. Benninger, T. Thurnherr, J.A. Pereira, S. Krause, X. Wu, A. Chrostek-Grashoff, D. Herzog, K.A. Nave, R.J. Franklin, D. Meijer, C. Brakebusch, U. Suter, and J.B. Relvas 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 (Pubitemid 46955709)
21. M. Grove, N.H. Komiyama, K.A. Nave, S.G. Grant, D.L. Sherman, and P.J. Brophy FAK is required for axonal sorting by Schwann cells J. Cell Biol. 176 2007 277 282 (Pubitemid 46184879)
22. J.R. Chan, C. Jolicoeur, J. Yamauchi, J. Elliott, J.P. Fawcett, B.K. Ng, and M. Cayouette The polarity protein Par-3 directly interacts with p75NTR to regulate myelination Science 314 2006 832 836 (Pubitemid 44706652)
23. K.A. Lewallen, Y.A. Shen, A.R. De la Torre, B.K. Ng, D. Meijer, and J.R. Chan Assessing the role of the cadherin/catenin complex at the Schwann cell-axon interface and in the initiation of myelination J. Neurosci. 31 2011 3032 3043
24. B. Beirowski, J. Gustin, S.M. Armour, H. Yamamoto, A. Viader, B.J. North, S. Michan, R.H. Baloh, J.P. Golden, R.E. Schmidt, D.A. Sinclair, J. Auwerx, and J. Milbrandt Sir-two-homolog 2 (Sirt2) modulates peripheral myelination through polarity protein Par-3/atypical protein kinase C (aPKC) signaling Proc. Natl. Acad. Sci. U. S. A. 108 2011 E952 E961
25. K. Susuki, A.R. Raphael, Y. Ogawa, M.C. Stankewich, E. Peles, W.S. Talbot, and M.N. Rasband Schwann cell spectrins modulate peripheral nerve myelination Proc. Natl. Acad. Sci. U. S. A. 108 2011 8009 8014
26. K.D. McCarthy, and J. de Vellis Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue J. Cell Biol. 85 1980 890 902 (Pubitemid 10007455)
27. S. Szuchet, P.E. Polak, and S.H. Yim Mature oligodendrocytes cultured in the absence of neurons recapitulate the ontogenic development of myelin membranes Dev. Neurosci. 8 1986 208 221 (Pubitemid 17009469)
28. S.Y. Chong, and J.R. Chan Tapping into the glial reservoir: cells committed to remaining uncommitted J. Cell Biol. 188 2010 305 312
29. C. Taveggia, M.L. Feltri, and L. Wrabetz Signals to promote myelin formation and repair Nat. Rev. Neurosci. 6 2010 276 287 1
30. G. Piaton, R.M. Gould, and C. Lubetzki Axon-oligodendrocyte interactions during developmental myelination, demyelination and repair J. Neurochem. 114 2010 1243 1260
31. B. Emery Regulation of oligodendrocyte differentiation and myelination Science 330 2010 779 782
32. B. Sobottka, U. Ziegler, A. Kaech, B. Becher, and N. Goebels CNS live imaging reveals a new mechanism of myelination: the liquid croissant model Glia 2011 10.1002/glia.21228 Sep 1.
33. C.A. Dyer, and J.A. Benjamins Organization of oligodendroglial membrane sheets: II. Galactocerebroside:antibody interactions signal changes in cytoskeleton and myelin basic protein J. Neurosci. Res. 24 1989 212 221 (Pubitemid 19261872)
34. S. Aggarwal, L. Yurlova, N. Snaidero, C. Reetz, S. Frey, J. Zimmermann, G. Pahler, A. Janshoff, J. Friedrichs, D.J. Muller, C. Goebel, and M. Simons A size barrier limits protein diffusion at the cell surface to generate lipid-rich myelin-membrane sheets Dev. Cell 21 2011 445 456
35. M. Simons, E.M. Kramer, C. Thiele, W. Stoffel, and J. Trotter Assembly of myelin by association of proteolipid protein with cholesterol- and galactosylceramide-rich membrane domains J. Cell Biol. 151 2000 143 154
36. C. Winterstein, J. Trotter, and E.M. Kramer-Albers Distinct endocytic recycling of myelin proteins promotes oligodendroglial membrane remodeling J. Cell Sci. 121 2008 834 842 (Pubitemid 351578119)
37. A. Feldmann, J. Amphornrat, M. Schonherr, C. Winterstein, W. Mobius, T. Ruhwedel, L. Danglot, K.A. Nave, T. Galli, D. Bruns, J. Trotter, and E.M. Kramer-Albers Transport of the major myelin proteolipid protein is directed by VAMP3 and VAMP7 J. Neurosci. 31 2011 5659 5672
38. K. Trajkovic, A.S. Dhaunchak, J.T. Goncalves, D. Wenzel, A. Schneider, G. Bunt, K.A. Nave, and M. Simons Neuron to glia signaling triggers myelin membrane exocytosis from endosomal storage sites J. Cell Biol. 172 2006 937 948
39. M. Bakhti, C. Winter, and M. Simons Inhibition of myelin membrane sheath formation by oligodendrocyte-derived exosome-like vesicles J. Biol. Chem. 286 2011 787 796
40. L. Pedraza, J.K. Huang, and D.R. Colman Organizing principles of the axoglial apparatus Neuron 30 2001 335 344 (Pubitemid 32530579)
41. L. Cotter, M. Ozcelik, C. Jacob, J.A. Pereira, V. Locher, R. Baumann, J.B. Relvas, U. Suter, and N. Tricaud Dlg1-PTEN interaction regulates myelin thickness to prevent damaging peripheral nerve overmyelination Science 328 2010 1415 1418
42. M. Ozcelik, L. Cotter, C. Jacob, J.A. Pereira, J.B. Relvas, U. Suter, and N. Tricaud Pals1 is a major regulator of the epithelial-like polarization and the extension of the myelin sheath in peripheral nerves J. Neurosci. 30 2010 4120 4131
43. A. Bolis, S. Coviello, I. Visigalli, C. Taveggia, A. Bachi, A.H. Chishti, T. Hanada, A. Quattrini, S.C. Previtali, A. Biffi, and A. Bolino Dlg1, Sec8, and Mtmr2 regulate membrane homeostasis in Schwann cell myelination J. Neurosci. 29 2009 8858 8870
44. F. Caudron, and Y. Barral Septins and the lateral compartmentalization of eukaryotic membranes Dev. Cell 16 2009 493 506
45. D.L. Sherman, S. Tait, S. Melrose, R. Johnson, B. Zonta, F.A. Court, W.B. Macklin, S. Meek, A.J. Smith, D.F. Cottrell, and P.J. Brophy Neurofascins are required to establish axonal domains for saltatory conduction Neuron 48 2005 737 742 (Pubitemid 41759425)
46. A.M. Pillai, C. Thaxton, A.L. Pribisko, J.G. Cheng, J.L. Dupree, and M.A. Bhat Spatiotemporal ablation of myelinating glia-specific neurofascin (Nfasc NF155) in mice reveals gradual loss of paranodal axoglial junctions and concomitant disorganization of axonal domains J. Neurosci. Res. 87 2009 1773 1793
47. J. Devaux, and A. Gow Tight junctions potentiate the insulative properties of small CNS myelinated axons J. Cell Biol. 183 2008 909 921
48. A. Gow, C.M. Southwood, J.S. Li, M. Pariali, G.P. Riordan, S.E. Brodie, J. Danias, J.M. Bronstein, B. Kachar, and R.A. Lazzarini CNS myelin and sertoli cell tight junction strands are absent in Osp/claudin-11 null mice Cell 99 1999 649 659 (Pubitemid 30004640)
49. T. Miyamoto, K. Morita, D. Takemoto, K. Takeuchi, Y. Kitano, T. Miyakawa, K. Nakayama, Y. Okamura, H. Sasaki, Y. Miyachi, M. Furuse, and S. Tsukita Tight junctions in Schwann cells of peripheral myelinated axons: a lesson from claudin-19 deficient mice J. Cell Biol. 169 2005 527 538 (Pubitemid 40686702)
50. D.A. Lyons, S.G. Naylor, A. Scholze, and W.S. Talbot Kif1b is essential for mRNA localization in oligodendrocytes and development of myelinated axons Nat. Genet. 41 2009 854 858
51. S.J. Singer, and G.L. Nicolson The fluid mosaic model of the structure of cell membranes Science 175 1972 720 731
52. B. Winckler, P. Forscher, and I. Mellman A diffusion barrier maintains distribution of membrane proteins in polarized neurons Nature 397 1999 698 701
53. T. Kobayashi, B. Storrie, K. Simons, and C.G. Dotti A functional barrier to movement of lipids in polarized neurons Nature 359 1992 647 650
54. M.N. Rasband The axon initial segment and the maintenance of neuronal polarity Nat. Rev. Neurosci. 11 2010 552 562
55. C. Nakada, K. Ritchie, Y. Oba, M. Nakamura, Y. Hotta, R. Iino, R.S. Kasai, K. Yamaguchi, T. Fujiwara, and A. Kusumi Accumulation of anchored proteins forms membrane diffusion barriers during neuronal polarization Nat. Cell Biol. 5 2003 626 632 (Pubitemid 36818084)
56. A. Kusumi, K.G. Suzuki, R.S. Kasai, K. Ritchie, and T.K. Fujiwara Hierarchical mesoscale domain organization of the plasma membrane Trends Biochem. Sci. 36 2011 604 615
57. J. Saarikangas, and Y. Barral The emerging functions of septins in metazoans EMBO Rep. 12 2011 1118 1126
58. M.V. Nachury, E.S. Seeley, and H. Jin Trafficking to the ciliary membrane: how to get across the periciliary diffusion barrier? Annu. Rev. Cell Dev. Biol. 26 2010 59 87
59. Q. Hu, L. Milenkovic, H. Jin, M.P. Scott, M.V. Nachury, E.T. Spiliotis, and W.J. Nelson A septin diffusion barrier at the base of the primary cilium maintains ciliary membrane protein distribution Science 329 2010 436 439
60. C.L. Williams, C. Li, K. Kida, P.N. Inglis, S. Mohan, L. Semenec, N.J. Bialas, R.M. Stupay, N. Chen, O.E. Blacque, B.K. Yoder, and M.R. Leroux MKS and NPHP modules cooperate to establish basal body/transition zone membrane associations and ciliary gate function during ciliogenesis J. Cell Biol. 192 2011 1023 1041
61. B. Craige, C.C. Tsao, D.R. Diener, Y. Hou, K.F. Lechtreck, J.L. Rosenbaum, and G.B. Witman CEP290 tethers flagellar transition zone microtubules to the membrane and regulates flagellar protein content J. Cell Biol. 190 2010 927 940
62. S.S. Francis, J. Sfakianos, B. Lo, and I. Mellman A hierarchy of signals regulates entry of membrane proteins into the ciliary membrane domain in epithelial cells J. Cell Biol. 193 2011 219 233
63. S. Frey, and D. Gorlich A saturated FG-repeat hydrogel can reproduce the permeability properties of nuclear pore complexes Cell 130 2007 512 523 (Pubitemid 47208521)
64. G. Harauz, V. Ladizhansky, and J.M. Boggs Structural polymorphism and multifunctionality of myelin basic protein Biochemistry 48 2009 8094 8104
65. Y. Hu, and J. Israelachvili Lateral reorganization of myelin lipid domains by myelin basic protein studied at the air-water interface Colloids Surf. B Biointerfaces 62 2008 22 30 (Pubitemid 351179232)
66. D. Fitzner, A. Schneider, A. Kippert, W. Mobius, K.I. Willig, S.W. Hell, G. Bunt, K. Gaus, and M. Simons Myelin basic protein-dependent plasma membrane reorganization in the formation of myelin EMBO J. 25 2006 5037 5048 (Pubitemid 44658522)
67. I. Sommer, and M. Schachner Monoclonal antibodies (O1 to O4) to oligodendrocyte cell surfaces: an immunocytological study in the central nervous system Dev. Biol. 83 1981 311 327
68. R. Schiff, and J. Rosenbluth Distribution of myelin lipid antigens in adult and developing rat spinal cord Brain Res. 686 1995 143 149
69. E. Kirschning, G. Rutter, and H. Hohenberg High-pressure freezing and freeze-substitution of native rat brain: suitability for preservation and immunoelectron microscopic localization of myelin glycolipids J. Neurosci. Res. 53 1998 465 474 (Pubitemid 28363208)
70. T. Coetzee, N. Fujita, J. Dupree, R. Shi, A. Blight, K. Suzuki, and B. Popko Myelination in the absence of galactocerebroside and sulfatide: normal structure with abnormal function and regional instability Cell 86 1996 209 219 (Pubitemid 26286104)
71. A. Bosio, E. Binczek, and W. Stoffel 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. 93 1996 13280 13285 (Pubitemid 26382807)
72. J.L. Dupree, T. Coetzee, A. Blight, K. Suzuki, and B. Popko Myelin galactolipids are essential for proper node of Ranvier formation in the CNS J. Neurosci. 18 1998 1642 1649 (Pubitemid 28103072)
73. L.Y. Yurlova, K. Kahya, S. Aggarwal, H.-J. Kaiser, S. Chiantia, M. Bakhti, Y. Pewzner-Jung, O. Ben-David, A.H. Futerman, B. Brügger, and M. Simons Self-segregation of myelin membrane lipids in model membranes Biophys. J. 101 2011 2713 2720
74. C.M. Rosetti, B. Maggio, and R.G. Oliveira 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 2008 1665 1675 (Pubitemid 351843440)
75. H.M. McConnell, and M. Vrljic Liquid-liquid immiscibility in membranes Annu. Rev. Biophys. Biomol. Struct. 32 2003 469 492 (Pubitemid 37056238)
76. L.A. Bagatolli, J.H. Ipsen, A.C. Simonsen, and O.G. Mouritsen An outlook on organization of lipids in membranes: searching for a realistic connection with the organization of biological membranes Prog. Lipid Res. 49 2010 378 389
77. T.A. Watkins, B. Emery, S. Mulinyawe, and B.A. Barres Distinct stages of myelination regulated by gamma-secretase and astrocytes in a rapidly myelinating CNS coculture system Neuron 60 2008 555 569
78. H. Zhang, A.A. Jarjour, A. Boyd, and A. Williams Central nervous system remyelination in culture - a tool for multiple sclerosis research Exp. Neurol. 230 2011 138 148
79. A.A. Jarjour, H. Zhang, N. Bauer, C. Ffrench-Constant, and A. Williams In vitro modeling of central nervous system myelination and remyelination Glia 2011 10.1002/glia.21231
80. T. Czopka, and D.A. Lyons Dissecting mechanisms of myelinated axon formation using zebrafish Methods Cell Biol. 105 2011 25 62
81. K.R. Monk, K. Oshima, S. Jors, S. Heller, and W.S. Talbot Gpr126 is essential for peripheral nerve development and myelination in mammals Development 138 2011 2673 2680
82. B.B. Kirby, N. Takada, A.J. Latimer, J. Shin, T.J. Carney, R.N. Kelsh, and B. Appel In vivo time-lapse imaging shows dynamic oligodendrocyte progenitor behavior during zebrafish development Nat. Neurosci. 9 2006 1506 1511 (Pubitemid 44862658)
83. J.K. Huang, A.A. Jarjour, B. Nait Oumesmar, C. Kerninon, A. Williams, W. Krezel, H. Kagechika, J. Bauer, C. Zhao, A.B. Evercooren, P. Chambon, C. Ffrench-Constant, and R.J. Franklin Retinoid X receptor gamma signaling accelerates CNS remyelination Nat. Neurosci. 14 2011 45 53
84. J.B. Zuchero, and B.A. Barres Between the sheets: a molecular sieve makes myelin membranes Dev. Cell 13 2011 385 386