Neuroscience Bulletin

, Volume 29, Issue 2, pp 177–188 | Cite as

Myelin-based inhibitors of oligodendrocyte myelination: clues from axonal growth and regeneration

Review

Abstract

The differentiation of and myelination by oligodendrocytes (OLs) are exquisitely regulated by a series of intrinsic and extrinsic mechanisms. As each OL can make differing numbers of myelin segments with variable lengths along similar axon tracts, myelination can be viewed as a graded process shaped by inhibitory/inductive cues during development. Myelination by OLs is a prime example of an adaptive process determined by the microenvironment and architecture of the central nervous system (CNS). in this review, we discuss how myelin formation by OLs may be controlled by the heterogeneous microenvironment of the CNS. Then we address recent findings demonstrating that neighboring OLs may compete for available axon space, and highlight our current understanding of myelin-based inhibitors of axonal regeneration that are potentially responsible for the reciprocal dialogue between OLs and determine the numbers and lengths of myelin internodes. Understanding the mechanisms that control the spatiotemporal regulation of myelinogenic potential during development may provide valuable insight into therapeutic strategies for promoting remyelination in an inhibitory microenvironment.

Keywords

differentiation myelin nogo-A LINGO-1 semaphorin ephrin netrin-1 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. [1]
    Nave KA. Myelination and support of axonal integrity by glia. Nature 2010, 468: 244–252.PubMedCrossRefGoogle Scholar
  2. [2]
    Lee Y, Morrison BM, Li Y, Lengacher S, Farah MH, Hoffman PN, et al. Oligodendroglia metabolically support axons and contribute to neurodegeneration. Nature 2012, 487: 443–448.PubMedCrossRefGoogle Scholar
  3. [3]
    Miller RH. Regulation of oligodendrocyte development in the vertebrate CNS. Prog Neurobiol 2002, 67: 451–467.PubMedCrossRefGoogle Scholar
  4. [4]
    Richardson WD, Kessaris N, Pringle N. Oligodendrocyte wars. Nat Rev Neurosci 2006, 7: 11–18.PubMedCrossRefGoogle Scholar
  5. [5]
    Franklin RJM, Ffrench-Constant C. Remyelination in the CNS: from biology to therapy. Nat Rev Neurosci 2008, 9: 839–855.PubMedCrossRefGoogle Scholar
  6. [6]
    Chang A, Nishiyama A, Peterson J, Prineas J, Trapp BD. NG2-positive oligodendrocyte progenitor cells in adult human brain and multiple sclerosis lesions. J Neurosci 2000, 20: 6404–6412.PubMedGoogle Scholar
  7. [7]
    Wolswijk G. Oligodendrocyte precursor cells in the demyelinated multiple sclerosis spinal cord. Brain 2002, 125: 338–349.PubMedCrossRefGoogle Scholar
  8. [8]
    Wolswijk G. Oligodendrocyte survival, loss and birth in lesions of chronic-stage multiple sclerosis. Brain 2000, 123: 105–115.PubMedCrossRefGoogle Scholar
  9. [9]
    Patrikios P, Stadelmann C, Kutzelnigg A, Rauschka H, Schmidbauer M, Laursen H. Remyelination is extensive in a subset of multiple sclerosis patients. Brain 2006, 129: 3165–3172.PubMedCrossRefGoogle Scholar
  10. [10]
    Kuhlmann T, Miron V, Cui Q, Cuo Q, Wegner C, Antel J, et al. Differentiation block of oligodendroglial progenitor cells as a cause for remyelination failure in chronic multiple sclerosis. Brain 2008, 131: 1749–1758.PubMedCrossRefGoogle Scholar
  11. [11]
    Lu QR, Sun T, Zhu Z, Ma N, Garcia M, Stiles CD, et al. Common developmental requirement for Olig Function indicates a Motor Neuron / Oligodendrocyte Connection. Cell 2002, 109: 75–86.PubMedCrossRefGoogle Scholar
  12. [12]
    Zhou Q, Wang S, Anderson DJ. Identification of a novel family of oligodendrocyte lineage-specific basic helix-loop-helix transcription factors. Neuron 2000, 25: 331–343.PubMedCrossRefGoogle Scholar
  13. [13]
    Lu QR, Yuk D, Alberta J, Zhu Z, Pawlitzky I, Chan J, et al. Sonic hedgehog—regulated oligodendrocyte lineage genes encoding bHLH proteins in the mammalian central nervous system. Neuron 2000, 25: 317–329.PubMedCrossRefGoogle Scholar
  14. [14]
    Zhou Q, Choi G, Anderson DJ. The bHLH transcription factor Olig2 promotes oligodendrocyte differentiation in collaboration with Nkx2.2. Neuron 2001, 31: 791–807.PubMedCrossRefGoogle Scholar
  15. [15]
    Zhou Q, Anderson DJ. The bHLH transcription factors OLIG2 and OLIG1 couple neuronal and glial subtype specification. Cell 2002, 109: 61–73.PubMedCrossRefGoogle Scholar
  16. [16]
    Takebayashi H, Nabeshima Y, Yoshida S, Chisaka O, Ikenaka K, Nabeshima Y. The basic helix-loop-helix factor olig2 is essential for the development of motoneuron and oligodendrocyte lineages. Curr Biol 2002, 12: 1157–1163.PubMedCrossRefGoogle Scholar
  17. [17]
    Fancy SP, Baranzini SE, Zhao C, Yuk DI, Irvine KA, Kaing S, et al. Dysregulation of the Wnt pathway inhibits timely myelination and remyelination in the mammalian CNS. Genes Dev 2009, 23: 1571–1585.PubMedCrossRefGoogle Scholar
  18. [18]
    Li H, He Y, Richardson WD, Casaccia P. Two-tier transcriptional control of oligodendrocyte differentiation. Curr Opin Neurol 2009, 19: 479–485.CrossRefGoogle Scholar
  19. [19]
    Chang A, Tourtellotte WW, Rudick R, Trapp BD. Premyelinating oligodendrocytes in chronic lesions of multiple sclerosis. N Engl J Med 2002, 346: 165–173.PubMedCrossRefGoogle Scholar
  20. [20]
    Rivers LE, Young KM, Rizzi M, Jamen F, Psachoulia K, Wade A, et al. PDGFRA/NG2 glia generate myelinating oligodendrocytes and piriform projection neurons in adult mice. Nat Neurosci 2008, 11: 1392–1401.PubMedCrossRefGoogle Scholar
  21. [21]
    Horner PJ, Power a E, Kempermann G, Kuhn HG, Palmer TD, Winkler J, et al. Proliferation and differentiation of progenitor cells throughout the intact adult rat spinal cord. J Neurosci 2000, 20: 2218–2228.PubMedGoogle Scholar
  22. [22]
    Gensert JM, Goldman JE. Demyelinated Axons in the Adult CNS. Neuron 1997, 19: 197–203.PubMedCrossRefGoogle Scholar
  23. [23]
    Windrem MS, Nunes MC, Rashbaum WK, Schwartz TH, Goodman R A, McKhann G, et al. Fetal and adult human oligodendrocyte progenitor cell isolates myelinate the congenitally dysmyelinated brain. Nat Med 2004, 10: 93–97.PubMedCrossRefGoogle Scholar
  24. [24]
    Chong SYC, Chan JR: Tapping into the glial reservoir: cells committed to remaining uncommitted. J Cell Biol 2010, 188: 305–12.PubMedCrossRefGoogle Scholar
  25. [25]
    Chong SYC, Rosenberg SS, Fancy SPJ, Zhao C, Shen YA, Hahn AT, et al. Neurite outgrowth inhibitor Nogo-A establishes spatial segregation and extent of oligodendrocyte myelination. Proc Natl Acad Sci U S A 2012, 109: 1299–1304.PubMedCrossRefGoogle Scholar
  26. [26]
    Kessaris N, Fogarty M, Iannarelli P, Grist M, Wegner M, Richardson WD. Competing waves of oligodendrocytes in the forebrain and postnatal elimination of an embryonic lineage. Nat Neurosci 2006, 9: 173–179.PubMedCrossRefGoogle Scholar
  27. [27]
    Dawson M. NG2-expressing glial progenitor cells: an abundant and widespread population of cycling cells in the adult rat CNS. Mol Cell Neurosci 2003, 24: 476–488.PubMedCrossRefGoogle Scholar
  28. [28]
    Kirby BB, Takada N, Latimer AJ, Shin J, Carney TJ, Kelsh RN, et al. In vivo time-lapse imaging shows dynamic oligodendrocyte progenitor behavior during zebrafish development. Nat Neurosci 2006, 9: 1506–1511.PubMedCrossRefGoogle Scholar
  29. [29]
    Ye F, Chen Y, Hoang T, Montgomery RL, Zhao X, Bu H, et al. HDAC1 and HDAC2 regulate oligodendrocyte differentiation by disrupting the beta-catenin-TCF interaction. Nat Neurosci 2009, 12: 829–838.PubMedCrossRefGoogle Scholar
  30. [30]
    Shen S, Sandoval J, Swiss V, Li J, Dupree J, Franklin RJM, et al. Age-dependent epigenetic control of differentiation inhibitors is critical for remyelination efficiency. Nat Neurosci 2008, 11: 1024–1034.PubMedCrossRefGoogle Scholar
  31. [31]
    Popko B. Epigenetic control of myelin repair. Nat Neurosci 2008, 11: 987–988.PubMedCrossRefGoogle Scholar
  32. [32]
    Marin-Husstege M, Muggironi M, Liu A, Casaccia-Bonnefil P. Histone deacetylase activity is necessary for oligodendrocyte lineage progression. J Neurosci 2002, 22: 10333–10345.PubMedGoogle Scholar
  33. [33]
    Shen S, Li J, Casaccia-Bonnefil P. Histone modifications affect timing of oligodendrocyte progenitor differentiation in the developing rat brain. J Cell Biol 2005, 169: 577–589.PubMedCrossRefGoogle Scholar
  34. [34]
    Ruckh JM, Zhao JW, Shadrach JL, Van Wijngaarden P, Rao TN, Wagers AJ, et al. Rejuvenation of regeneration in the aging central nervous system. Cell Stem Cell 2012, 10: 96–103.PubMedCrossRefGoogle Scholar
  35. [35]
    Redmond S, Chan JR. Neuroscience. Revitalizing remyelination—the answer is circulating. Science 2012, 336: 161–162.PubMedCrossRefGoogle Scholar
  36. [36]
    Lee S, Leach MK, Redmond SA, Chong SYC, Mellon SH, Tuck SJ, et al. A culture system to study oligodendrocyte myelination processes using engineered nanofibers. Nat Methods 2012, 9: 917–922.PubMedCrossRefGoogle Scholar
  37. [37]
    Voyvodic JT. Target size regulates calibre and myelination of sympathetic axons. Nature 1989, 342: 430–433.PubMedCrossRefGoogle Scholar
  38. [38]
    Lee X, Yang Z, Shao Z, Rosenberg SS, Levesque M, Pepinsky RB, et al. NGF regulates the expression of axonal LINGO-1 to inhibit oligodendrocyte differentiation and myelination. J Neurosci 2007, 27: 220–225.PubMedCrossRefGoogle Scholar
  39. [39]
    Jepson S, Vought B, Gross CH, Gan L, Austen D, Frantz JD, et al. LINGO-1, a transmembrane signaling protein, inhibits oligodendrocyte differentiation and myelination through intercellular self-interactions. J Cell Biol 2012, 287: 22184–22195.Google Scholar
  40. [40]
    Charles P, Hernandez MP, Stankoff B, Aigrot MS, Colin C, Rougon G, et al. Negative regulation of central nervous system myelination by polysialylated-neural cell adhesion molecule. Proc Natl Acad Sci U S A 2000, 97: 7585–7590.PubMedCrossRefGoogle Scholar
  41. [41]
    Charles P, Reynolds R, Seilhean D, Rougon G, Aigrot MS, Niezgoda A, et al. Re-expression of PSA-NCAM by demyelinated axons: an inhibitor of remyelination in multiple sclerosis? Brain 2002, 125: 1972–1979.PubMedCrossRefGoogle Scholar
  42. [42]
    Barres B, Raff MC. Axonal control of oligodendrocyte development. J Cell Biol 1999, 147: 1123–1128.PubMedCrossRefGoogle Scholar
  43. [43]
    Clarke LE, Young KM, Hamilton NB, Li H, Richardson WD, Attwell D. Properties and fate of oligodendrocyte progenitor cells in the corpus callosum, motor cortex, and piriform cortex of the mouse. J Neurosci 2012, 32: 8173–8185.PubMedCrossRefGoogle Scholar
  44. [44]
    Cammermeyer J. The distribution of oligodendrocytes in cerebral gray and white matter of several mammals. Am J Anat 1960, 107: 107–127.PubMedCrossRefGoogle Scholar
  45. [45]
    Hahn AT, Chan JR. A collaboration conducive to conduction: matching axonal density to oligodendroglial number (Commentary on Kawai et al.). Eur J Neurosci 2009, 30: 2029.PubMedCrossRefGoogle Scholar
  46. [46]
    Kawai K, Itoh T, Itoh A, Horiuchi M, Wakayama K, Bannerman P, et al. Maintenance of the relative proportion of oligodendrocytes to axons even in the absence of BAX and BAK. Eur J Neurosci 2009, 30: 2030–2041.PubMedCrossRefGoogle Scholar
  47. [47]
    Rosenberg SS, Kelland EE, Tokar E, De la Torre AR, Chan JR. The geometric and spatial constraints of the microenvironment induce oligodendrocyte differentiation. Proc Natl Acad Sci U S A 2008, 105: 14662–14667.PubMedCrossRefGoogle Scholar
  48. [48]
    Baer AS, Syed YA, Kang SU, Mitteregger D, Vig R, Ffrench-Constant C, et al. Myelin-mediated inhibition of oligodendrocyte precursor differentiation can be overcome by pharmacological modulation of Fyn-RhoA and protein kinase C signalling. Brain 2009, 132: 465–481.PubMedCrossRefGoogle Scholar
  49. [49]
    Kotter MR, Li WW, Zhao C, Franklin RJM. Myelin impairs CNS remyelination by inhibiting oligodendrocyte precursor cell differentiation. J Neurosci 2006, 26: 328–332.PubMedCrossRefGoogle Scholar
  50. [50]
    Domeniconi M, Zampieri N, Spencer T, Hilaire M, Mellado W, Chao M V, et al. MAG induces regulated intramembrane proteolysis of the p75 neurotrophin receptor to inhibit neurite outgrowth. Neuron 2005, 46: 849–855.PubMedCrossRefGoogle Scholar
  51. [51]
    Wang KC, Koprivica V, Kim JA, Sivasankaran R, Guo Y, Neve RL, et al. Oligodendrocyte-myelin glycoprotein is a Nogo receptor ligand that inhibits neurite outgrowth. Nature 2002, 417: 941–944.PubMedCrossRefGoogle Scholar
  52. [52]
    Kottis V, Thibault P, Mikol D, Xiao ZC, Zhang R, Dergham P, et al. Oligodendrocyte-myelin glycoprotein (OMgp) is an inhibitor of neurite outgrowth. J Neurochem 2002, 82: 1566–1569.PubMedCrossRefGoogle Scholar
  53. [53]
    Caroni P, Schwab ME. Two membrane protein fractions from rat central myelin with inhibitory properties for neurite growth and fibroblast spreading. J Cell Biol 1988, 106: 1281–1288.PubMedCrossRefGoogle Scholar
  54. [54]
    Filbin MT. Myelin-associated inhibitors of axonal regeneration in the adult mammalian CNS. Nat Rev Neurosci 2003, 4: 703–713.PubMedCrossRefGoogle Scholar
  55. [55]
    Schwab ME. Nogo and axon regeneration. Curr Opin Neurol 2004, 14: 118–124.CrossRefGoogle Scholar
  56. [56]
    Dickson BJ. Molecular mechanisms of axon guidance. Science 2002, 298: 1959–1964.PubMedCrossRefGoogle Scholar
  57. [57]
    Yu TW, Bargmann CI. Dynamic regulation of axon guidance. Nat Neurosci 2001, 4Suppl: 1169–1176.PubMedCrossRefGoogle Scholar
  58. [58]
    Giger RJ, Hollis ER, Tuszynski MH. Guidance molecules in axon regeneration. Cold Spring Harb Perspect Biol 2010, 2: a001867.PubMedCrossRefGoogle Scholar
  59. [59]
    Fox M, Afshari F, Alexander J, Colello R, Fuss B. Growth conelike sensorimotor structures are characteristic features of postmigratory, premyelinating oligodendrocytes. Glia 2005, 566: 563–566.Google Scholar
  60. [60]
    Jarjour A, Kennedy TE. Oligodendrocyte precursors on the move: mechanisms directing migration. Neuroscientist 2004, 10: 99–105.PubMedCrossRefGoogle Scholar
  61. [61]
    Sloane J, Vartanian TK. Myosin Va controls oligodendrocyte morphogenesis and myelination. J Neurosci 2007, 27: 11366–11375.PubMedCrossRefGoogle Scholar
  62. [62]
    Huber AB, Weinmann O, Brösamle C, Oertle T, Schwab ME. Patterns of Nogo mRNA and protein expression in the developing and adult rat and after CNS lesions. J Neurosci 2002, 22: 3553–3567.PubMedGoogle Scholar
  63. [63]
    Chen MS, Huber B, Van der Haar ME, Frank M, Schnell L, Spillmann A, et al. Nogo-A is a myelin-associated neurite outgrowth inhibitor and an antigen for monoclonal antibody IN-1. Nature 2000, 403: 434–439.PubMedCrossRefGoogle Scholar
  64. [64]
    Hu F, Strittmatter SM. The N-terminal domain of Nogo-A inhibits cell adhesion and axonal outgrowth by an integrinspecific mechanism. J Neurosci 2008, 28: 1262–1269.PubMedCrossRefGoogle Scholar
  65. [65]
    Mimura F, Yamagishi S, Arimura N, Fujitani M, Kubo T, Kaibuchi K, et al. Myelin-associated glycoprotein inhibits microtubule assembly by a Rho-kinase-dependent mechanism. J Cell Biol 2006, 281: 15970–15979.Google Scholar
  66. [66]
    Fournier AE, Takizawa BT, Strittmatter SM. Rho kinase inhibition enhances axonal regeneration in the injured CNS. J Neurosci 2003, 23: 1416–1423.PubMedGoogle Scholar
  67. [67]
    Fournier AE, Grandpre T, Strittmatter SM. Identification of a receptor mediating Nogo-66 inhibition of axonal regeneration. Nature 2001, 409: 341–346.PubMedCrossRefGoogle Scholar
  68. [68]
    Mi YJ, Hou B, Liao QM, Ma Y, Luo Q, Dai YK, et al. Amino-Nogo-A antagonizes reactive oxygen species generation and protects immature primary cortical neurons from oxidative toxicity. Cell Differ Dev 2012, 19: 1175–1186.CrossRefGoogle Scholar
  69. [69]
    Wong ST, Henley JR, Kanning KC, Huang K, Bothwell M, Poo M. A p75(NTR) and Nogo receptor complex mediates repulsive signaling by myelin-associated glycoprotein. Nat Neurosci 2002, 5: 1302–1308.PubMedCrossRefGoogle Scholar
  70. [70]
    Shao Z, Browning JL, Lee X, Scott ML, Shulga-Morskaya S, Allaire N, et al. TAJ/TROY, an orphan TNF receptor family member, binds Nogo-66 receptor 1 and regulates axonal regeneration. Neuron 2005, 45: 353–359.PubMedCrossRefGoogle Scholar
  71. [71]
    Mi S, Lee X, Shao Z, Thill G, Ji B, Relton J, et al. LINGO-1 is a component of the Nogo-66 receptor/p75 signaling complex. Nat Neurosci 2004, 7: 221–228.PubMedCrossRefGoogle Scholar
  72. [72]
    Park JB, Yiu G, Kaneko S, Wang J, Chang J, He XL, et al. A TNF receptor family member, TROY, is a coreceptor with Nogo receptor in mediating the inhibitory activity of myelin inhibitors. Neuron 2005, 45: 345–351.PubMedCrossRefGoogle Scholar
  73. [73]
    Mi S, Miller RH, Lee X, Scott ML, Shulag-Morskaya S, Shao Z, et al. LINGO-1 negatively regulates myelination by oligodendrocytes. Nat Neurosci 2005, 8: 745–751.PubMedCrossRefGoogle Scholar
  74. [74]
    Mi S, Hu B, Hahm K, Luo Y, Kam Hui ES, Yuan Q, et al. LINGO-1 antagonist promotes spinal cord remyelination and axonal integrity in MOG-induced experimental autoimmune encephalomyelitis. Nature Med 2007, 13: 1228–1233.PubMedCrossRefGoogle Scholar
  75. [75]
    Mi S, Sandrock A, Miller RH. LINGO-1 and its role in CNS repair. Int J Biochem Cell B 2008, 40: 1971–1978.CrossRefGoogle Scholar
  76. [76]
    Mi S, Miller RH, Tang W, Lee X, Hu B, Wu W, et al. Promotion of central nervous system remyelination by induced differentiation of oligodendrocyte precursor cells. Ann Neurol 2009, 65: 304–315.PubMedCrossRefGoogle Scholar
  77. [77]
    Zhao XH, Jin WL, Ju G. An in vitro study on the involvement of LINGO-1 and Rho GTPases in Nogo-A regulated differentiation of oligodendrocyte precursor cells. Mol Cell Neurosci 2007, 36: 260–269.PubMedCrossRefGoogle Scholar
  78. [78]
    Ji B, Li M, Wu WT, Yick LW, Lee X, Shao Z, et al. LINGO-1 antagonist promotes functional recovery and axonal sprouting after spinal cord injury. Mol Cell Neurosci 2006, 33: 311–320.PubMedCrossRefGoogle Scholar
  79. [79]
    Jalink K, Van Corven EJ, Hengeveld T, Morii N, Narumiya S, Moolenaar WH. Inhibition of lysophosphatidate- and thrombin-induced neurite retraction and neuronal cell rounding by ADP ribosylation of the small GTP-binding protein Rho. J Cell Biol 1994, 126: 801–810.PubMedCrossRefGoogle Scholar
  80. [80]
    Liang X, Draghi N, Resh MD. Signaling from integrins to Fyn to Rho family GTPases regulates morphologic differentiation of oligodendrocytes. J Neurosci 2004, 24: 7140–7149.PubMedCrossRefGoogle Scholar
  81. [81]
    Nikolic M. The role of Rho GTPases and associated kinases in regulating neurite outgrowth. Int J Biochem Cell B 2002, 34: 731–745.CrossRefGoogle Scholar
  82. [82]
    Kruger RP, Aurandt J, Guan KL. Semaphorins command cells to move. Nat Rev Mol Cell Bio 2005, 6: 789–800.CrossRefGoogle Scholar
  83. [83]
    Dewit J, Verhaagen J. Role of semaphorins in the adult nervous system. Prog Neurobiol 2003, 71: 249–267.CrossRefGoogle Scholar
  84. [84]
    Huber AB, Kolodkin AL, Ginty DD, Cloutier JF. Signaling at the growth cone: ligand-receptor complexes and the control of axon growth and guidance. Ann Rev Neurosci 2003, 26: 509–563.PubMedCrossRefGoogle Scholar
  85. [85]
    Koeberle PD, Bähr M. Growth and guidance cues for regenerating axons: where have they gone? J Neurobiol 2004, 59: 162–180.PubMedCrossRefGoogle Scholar
  86. [86]
    Giraudon P, Vincent P, Vuaillat C, Verlaeten O, Cartier L, Marie-Cardine A, et al. Semaphorin CD100 from activated T lymphocytes induces process extension collapse in oligodendrocytes and death of immature neural cells. J immunol 2004, 172: 1246–1255.PubMedGoogle Scholar
  87. [87]
    Moreau-Fauvarque C, Kumanogoh A, Camand E, Jaillard C, Barbin G, Boquet I, et al. The transmembrane semaphorin Sema4D/CD100, an inhibitor of axonal growth, is expressed on oligodendrocytes and upregulated after CNS lesion. J Neurosci 2003, 23: 9229–9239.PubMedGoogle Scholar
  88. [88]
    Yamaguchi W, Tamai R, Kageura M, Furuyama T, Inagaki S. Sema4D as an inhibitory regulator in oligodendrocyte development. Mol Cell Neurosci 2012, 49: 290–299.PubMedCrossRefGoogle Scholar
  89. [89]
    Bernard F, Moreau-Fauvarque C, Heitz-Marchaland C, Zagar Y, Dumas L, Fouquet S, et al. Role of transmembrane semaphorin Sema6A in oligodendrocyte differentiation and myelination. Glia 2012, 60: 1590–1604.PubMedCrossRefGoogle Scholar
  90. [90]
    Goldberg JL, Vargas ME, Wang JT, Mandemakers W, Oster SF, Sretavan DW, et al. An oligodendrocyte lineage-specific semaphorin, Sema5A, inhibits axon growth by retinal ganglion cells. J Neurosci 2004, 24: 4989–4999.PubMedCrossRefGoogle Scholar
  91. [91]
    Leslie JR, Imai F, Fukuhara K, Takegahara N, Rizvi T, Friedel RH, et al. Ectopic myelinating oligodendrocytes in the dorsal spinal cord as a consequence of altered semaphorin 6D signaling inhibit synapse formation. Development 2011, 138: 4085–4095.PubMedCrossRefGoogle Scholar
  92. [92]
    Prestoz L, Chatzopoulou E, Lemkine G, Spassky N, Lebras B, Kagawa T, et al. Control of axonophilic migration of oligodendrocyte precursor cells by Eph-ephrin interaction. Neuron Glia Biol 2004, 1: 73–83.PubMedCrossRefGoogle Scholar
  93. [93]
    Worzfeld T, Rauch P, Karram K, Trotter J, Kuner R, Offermanns S. Mice lacking Plexin-B3 display normal CNS morphology and behaviour. Mol Cell Neurosci 2009, 42: 372–381.PubMedCrossRefGoogle Scholar
  94. [94]
    Benson MD, Romero MI, Lush ME, Lu QR, Henkemeyer M, Parada LF. Ephrin-B3 is a myelin-based inhibitor of neurite outgrowth. Proc Natl Acad Sci U S A 2005, 102: 10694–10699.PubMedCrossRefGoogle Scholar
  95. [95]
    Round J, Stein E. Netrin signaling leading to directed growth cone steering. Curr Opin Neurol 2007, 17: 15–21.CrossRefGoogle Scholar
  96. [96]
    Killeen MT, Sybingco SS. Netrin, Slit and Wnt receptors allow axons to choose the axis of migration. Dev Biol 2008, 323: 143–151.PubMedCrossRefGoogle Scholar
  97. [97]
    Löw K, Culbertson M, Bradke F, Tessier-Lavigne M, Tuszynski MH. Netrin-1 is a novel myelin-associated inhibitor to axon growth. J Neurosci 2008, 28: 1099–1108.PubMedCrossRefGoogle Scholar
  98. [98]
    Jarjour A, Bull SJ, Almasieh M, Rajasekharan S, Baker KA, Mui J, et al. Maintenance of axo-oligodendroglial paranodal junctions requires DCC and netrin-1. J Neurosci 2008, 28: 11003–11014.PubMedCrossRefGoogle Scholar
  99. [99]
    Tsai HH, Macklin WB, Miller RH. Netrin-1 is required for the normal development of spinal cord oligodendrocytes. J Neurosci 2006, 26: 1913–1922.PubMedCrossRefGoogle Scholar
  100. [100]
    Rajasekharan S, Baker KA, Horn KE, Jarjour A, Antel JP, Kennedy TE. Netrin 1 and Dcc regulate oligodendrocyte process branching and membrane extension via Fyn and RhoA. Development 2009, 136: 415–426.PubMedCrossRefGoogle Scholar
  101. [101]
    Tsai HH. Netrin 1 mediates spinal cord oligodendrocyte precursor dispersal. Development 2003, 130: 2095–2105.PubMedCrossRefGoogle Scholar
  102. [102]
    Rajasekharan S, Bin JM, Antel JP, Kennedy TE. A central role for RhoA during oligodendroglial maturation in the switch from netrin-1-mediated chemorepulsion to process elaboration. J Neurochem 2010, 113: 1589–1597.PubMedGoogle Scholar
  103. [103]
    Manitt C, Colicos M, Thompson KM, Rousselle E, Peterson C, Kennedy TE. Widespread expression of netrin-1 by neurons and oligodendrocytes in the adult mammalian spinal cord. J Neurosci 2001, 21: 3911–3922.PubMedGoogle Scholar
  104. [104]
    Serafini T, Colamarino S, Leonardo ED, Wang H, Beddington R, Skarnes WC, et al. Netrin-1 is required for commissural axon guidance in the developing vertebrate nervous system. Cell 1996, 87: 1001–1014.PubMedCrossRefGoogle Scholar
  105. [105]
    Deiner MS, Sretavan DW. Altered midline axon pathways and ectopic neurons in the developing hypothalamus of netrin-1- and DCC-deficient mice. J Neurosci 1999, 19: 9900–9912.PubMedGoogle Scholar
  106. [106]
    Sherman DL, Brophy PJ. Mechanisms of axon ensheathment and myelin growth. Nat Rev Neurosci 2005, 6: 683–690.PubMedCrossRefGoogle Scholar
  107. [107]
    Dou CL, Levine JM. Identification of a neuronal cell surface receptor for a growth inhibitory chondroitin sulfate proteoglycan (NG2). J Neurochem 1997, 68: 1021–1030.PubMedCrossRefGoogle Scholar
  108. [108]
    Llorens F, Gil V, Del Río JA. Emerging functions of myelinassociated proteins during development, neuronal plasticity, and neurodegeneration. FASEB 2011, 25: 463–475.CrossRefGoogle Scholar
  109. [109]
    Wang H, Tewari A, Einheber S, Salzer JL, Melendez-Vasquez C V. Myosin ii has distinct functions in PNS and CNS myelin sheath formation. J Cell Biol 2008, 182: 1171–1184.PubMedCrossRefGoogle Scholar
  110. [110]
    Sun F, Park KK, Belin S, Wang D, Lu T, Chen G, et al. Sustained axon regeneration induced by co-deletion of PTEN and SoCS3. Nature 2011, 480: 372–375.PubMedCrossRefGoogle Scholar
  111. [111]
    Narayanan SP, Flores AI, Wang F, Macklin WB. Akt signals through the mammalian target of rapamycin pathway to regulate CNS myelination. J Neurosci 2009, 29: 6860–6870.PubMedCrossRefGoogle Scholar
  112. [112]
    Harrington EP, Zhao C, Fancy SPJ, Kaing S, Franklin RJM, Rowitch DH, et al. Oligodendrocyte PTEN is required for myelin and axonal integrity, not remyelination. Ann Neurol 2010, 68: 703–716.PubMedCrossRefGoogle Scholar
  113. [113]
    Tyler W, Gangoli N, Gokina P, Kim H, Covey M, Levison SW, et al. Activation of the mammalian target of rapamycin (mToR) is essential for oligodendrocyte differentiation. J Neurosci 2009, 29: 6367–6378.PubMedCrossRefGoogle Scholar
  114. [114]
    Rosenberg SS, Chan JR. Modulating myelination: knowing when to say Wnt. Genes Dev 2009, 23: 1487–1493.PubMedCrossRefGoogle Scholar

Copyright information

© Shanghai Institutes for Biological Sciences, CAS and Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Feng Mei
    • 1
  • S. Y. Christin Chong
    • 1
  • Jonah R. Chan
    • 1
  1. 1.Department of Neurology, Program in Neuroscience and the MS Research GroupUniversity of CaliforniaSan FranciscoUSA

Personalised recommendations