Contactin-1 regulates myelination and nodal/paranodal domain organization in the central nervous system

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 3, 2014, Pages

  Çolakoǧlu, Gülsen ^a   Bergstrom Tyrberg, Ulrika ^a,b   Berglund, Erik O ^a,c   Ranscht, Barbara ^a  

^a BURNHAM INSTITUTE   (United States)

^b KAROLINSKA INSTITUTE   (Sweden)

^c GILEAD SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CONTACTIN 1; POTASSIUM CHANNEL KV1.2; PROTEIN NODAL; PROTEOLIPID PROTEIN; SODIUM CHANNEL;

ARTICLE; CELL MATURATION; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; ELECTRON MICROSCOPY; IN VIVO STUDY; MOUSE; MYELIN SHEATH; MYELINATION; NERVE FIBER; NONHUMAN; OLIGODENDROGLIA; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS;

ANIMALS; AXONS; CELL DIFFERENTIATION; CENTRAL NERVOUS SYSTEM; CONTACTIN 1; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GREEN FLUORESCENT PROTEINS; KV1.2 POTASSIUM CHANNEL; MICE; MICE, KNOCKOUT; MYELIN SHEATH; OLIGODENDROGLIA; OPTIC NERVE; PHENOTYPE; TIME FACTORS;

EID: 84892934317     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1313769110     Document Type: Article

References (63)

1. Baumann N, Pham-Dinh D (2001) Biology of oligodendrocyte and myelin in the mammalian central nervous system. Physiol Rev 81(2):871-927.
2. Nave KA (2010) Myelination and support of axonal integrity by glia. Nature 468(7321):244-252.
3. Miller RH (2002) Regulation of oligodendrocyte development in the vertebrate CNS. Prog Neurobiol 67(6):451-467.
4. Sherman DL, Brophy PJ (2005) Mechanisms of axon ensheathment and myelin growth. Nat Rev Neurosci 6(9):683-690.
5. Dutta R, Trapp BD (2011) Mechanisms of neuronal dysfunction and degeneration in multiple sclerosis. Prog Neurobiol 93(1):1-12.
6. Ben-Hur T, Goldman SA (2008) Prospects of cell therapy for disorders of myelin. Ann N Y Acad Sci 1142(1):218-249.
7. Franklin RJ, Ffrench-Constant C (2008) Remyelination in the CNS: From biology to therapy. Nat Rev Neurosci 9(11):839-855.
8. Ranscht B (1988) Sequence of contactin, a 130-kD glycoprotein concentrated in areas of interneuronal contact, defines a new member of the immunoglobulin supergene family in the nervous system. J Cell Biol 107(4):1561-1573.
9. Gennarini G, Cibelli G, Rougon G, Mattei MG, Goridis C (1989) The mouse neuronal cell surface protein F3: A phosphatidylinositol-anchored member of the immunoglobulin superfamily related to chicken contactin. J Cell Biol 109(2):775-788.
10. Berglund EO, et al. (1999) Ataxia and abnormal cerebellar microorganization in mice with ablated contactin gene expression. Neuron 24(3):739-750.
11. Rios JC, et al. (2000) Contactin-associated protein (Caspr) and contactin form a complex that is targeted to the paranodal junctions during myelination. J Neurosci 20(22):8354-8364.
12. Boyle ME, et al. (2001) Contactin orchestrates assembly of the septate-like junctions at the paranode in myelinated peripheral nerve. Neuron 30(2):385-397.
13. Faivre-Sarrailh C, et al. (2000) The glycosylphosphatidyl inositol-anchored adhesion molecule F3/contactin is required for surface transport of paranodin/contactin-associated protein (caspr). J Cell Biol 149(2):491-502.
14. Sherman DL, et al. (2005) Neurofascins are required to establish axonal domains for saltatory conduction. Neuron 48(5):737-742.
15. Salzer JL, Brophy PJ, Peles E (2008) Molecular domains of myelinated axons in the peripheral nervous system. Glia 56(14):1532-1540.
16. Kazarinova-Noyes K, et al. (2001) Contactin associates with Na+ channels and increases their functional expression. J Neurosci 21(19):7517-7525.
17. Koch T, Brugger T, Bach A, Gennarini G, Trotter J (1997) Expression of the immunoglobulin superfamily cell adhesion molecule F3 by oligodendrocyte- lineage cells. Glia 19(3):199-212.
18. White R, et al. (2008) Activation of oligodendroglial Fyn kinase enhances translation of mRNAs transported in hnRNP A2-dependent RNA granules. J Cell Biol 181(4):579-586.
19. Laursen LS, Chan CW, ffrench-Constant C (2009) An integrin-contactin complex regulates CNS myelination by differential Fyn phosphorylation. J Neurosci 29(29):9174-9185.
20. Godement P, Salaün J, Imbert M (1984) Prenatal and postnatal development of retinogeniculate and retinocollicular projections in the mouse. J Comp Neurol 230(4):552-575.
21. Huberman AD, et al. (2008) Architecture and activity-mediated refinement of axonal projections from a mosaic of genetically identified retinal ganglion cells. Neuron 59(3):425-438.
22. Shaw G, Weber K (1982) Differential expression of neurofilament triplet proteins in brain development. Nature 298(5871):277-279.
23. Brady ST, et al. (1999) Formation of compact myelin is required for maturation of the axonal cytoskeleton. J Neurosci 19(17):7278-7288.
24. Murtie JC, Macklin WB, Corfas G (2007) Morphometric analysis of oligodendrocytes in the adult mouse frontal cortex. J Neurosci Res 85(10):2080-2086.
25. Mallon BS, Shick HE, Kidd GJ, Macklin WB (2002) Proteolipid promoter activity distinguishes two populations of NG2-positive cells throughout neonatal cortical development. J Neurosci 22(3):876-885.
26. Wang H, Kunkel DD, Martin TM, Schwartzkroin PA, Tempel BL (1993) Heteromultimeric K+ channels in terminal and juxtaparanodal regions of neurons. Nature 365(6441):75-79.
27. Boiko T, et al. (2001) Compact myelin dictates the differential targeting of two sodium channel isoforms in the same axon. Neuron 30(1):91-104.
28. Kaplan MR, et al. (2001) Differential control of clustering of the sodium channels Na (v) 1.2 and Na (v) 1.6 at developing CNS nodes of Ranvier. Neuron 30(1):105-119.
29. Krämer-Albers E-M, White R (2011) From axon-glial signalling to myelination: The integrating role of oligodendroglial Fyn kinase. Cell Mol Life Sci 68(12):2003-2012.
30. Seiwa C, Sugiyama I, Yagi T, Iguchi T, Asou H (2000) Fyn tyrosine kinase participates in the compact myelin sheath formation in the central nervous system. Neurosci Res 37(1):21-31.
31. Perge JA, Koch K, Miller R, Sterling P, Balasubramanian V (2009) How the optic nerve allocates space, energy capacity, and information. J Neurosci 29(24):7917-7928.
32. Brümmendorf T, et al. (1993) The axonal recognition molecule F11 is a multifunctional protein: Specific domains mediate interactions with Ng-CAM and restrictin. Neuron 10(4):711-727.
33. Morales G, et al. (1993) Induction of axonal growth by heterophilic interactions between the cell surface recognition proteins F11 and Nr-CAM/Bravo. Neuron 11(6):1113-1122.
34. Volkmer H, Zacharias U, Nörenberg U, Rathjen FG (1998) Dissection of complex molecular interactions of neurofascin with axonin-1, F11, and tenascin-R, which promote attachment and neurite formation of tectal cells. J Cell Biol 142(4):1083-1093.
35. Zeng L, D'Alessandri L, Kalousek MB, Vaughan L, Pallen CJ (1999) Protein tyrosine phosphatase α (PTPalpha) and contactin form a novel neuronal receptor complex linked to the intracellular tyrosine kinase fyn. J Cell Biol 147(4):707-714.
36. Barres BA, Raff MC (1999) Axonal control of oligodendrocyte development. J Cell Biol 147(6):1123-1128.
37. Wake H, Lee PR, Fields RD (2011) Control of local protein synthesis and initial events in myelination by action potentials. Science 333(6049):1647-1651.
38. Chatzopoulou E, et al. (2008) Structural requirement of TAG-1 for retinal ganglion cell axons and myelin in the mouse optic nerve. J Neurosci 28(30):7624-7636.
39. Yu T, Lieberman AP (2013) Npc1 acting in neurons and glia is essential for the formation and maintenance of CNS myelin. PLoS Genet 9(4):e1003462.
40. de Waegh SM, Lee VM, Brady ST (1992) Local modulation of neurofilament phosphorylation, axonal caliber, and slow axonal transport by myelinating Schwann cells. Cell 68(3):451-463.
41. Hsieh ST, et al. (1994) Regional modulation of neurofilament organization by myelination in normal axons. J Neurosci 14(11 Pt 1):6392-6401.
42. Sánchez I, Hassinger L, Paskevich PA, Shine HD, Nixon RA (1996) Oligodendroglia regulate the regional expansion of axon caliber and local accumulation of neurofilaments during development independently of myelin formation. J Neurosci 16(16):5095-5105.
43. Câmara J, et al. (2009) Integrin-mediated axoglial interactions initiate myelination in the central nervous system. J Cell Biol 185(4):699-712.
44. Dupree JL, Girault J-A, Popko B (1999) Axo-glial interactions regulate the localization of axonal paranodal proteins. J Cell Biol 147(6):1145-1152.
45. Bhat MA, et al. (2001) Axon-glia interactions and the domain organization of myelinated axons requires neurexin IV/Caspr/Paranodin. Neuron 30(2):369-383.
46. Rios JC, et al. (2003) Paranodal interactions regulate expression of sodium channel subtypes and provide a diffusion barrier for the node of Ranvier. J Neurosci 23(18):7001-7011.
47. Dupree JL, Coetzee T, Blight A, Suzuki K, Popko B (1998) Myelin galactolipids are essential for proper node of Ranvier formation in the CNS. J Neurosci 18(5):1642-1649.
48. Susuki K, et al. (2013) Three mechanisms assemble central nervous system nodes of Ranvier. Neuron 78(3):469-482.
49. Rasband MN, et al. (1999) Dependence of nodal sodium channel clustering on paranodal axoglial contact in the developing CNS. J Neurosci 19(17):7516-7528.
50. Rosenbluth J, Dupree JL, Popko B (2003) Nodal sodium channel domain integrity depends on the conformation of the paranodal junction, not on the presence of transverse bands. Glia 41(3):318-325.
51. Peles E, et al. (1995) The carbonic anhydrase domain of receptor tyrosine phosphatase β is a functional ligand for the axonal cell recognition molecule contactin. Cell 82(2):251-260.
52. Nörenberg U, Hubert M, Brümmendorf T, Tárnok A, Rathjen FG (1995) Characterization of functional domains of the tenascin-R (restrictin) polypeptide: cell attachment site, binding with F11, and enhancement of F11-mediated neurite outgrowth by tenascin-R. J Cell Biol 130(2):473-484.
53. Rigato F, et al. (2002) Tenascin-C promotes neurite outgrowth of embryonic hippocampal neurons through the alternatively spliced fibronectin type III BD domains via activation of the cell adhesion molecule F3/contactin. J Neurosci 22(15):6596-6609.
54. Rush AM, et al. (2005) Contactin regulates the current density and axonal expression of tetrodotoxin-resistant but not tetrodotoxin-sensitive sodium channels in DRG neurons. Eur J Neurosci 22(1):39-49.
55. Brackenbury WJ, et al. (2008) Voltage-gated Na+ channel beta1 subunit-mediated neurite outgrowth requires Fyn kinase and contributes to postnatal CNS development in vivo. J Neurosci 28(12):3246-3256.
56. Barres BA, Raff MC (1993) Proliferation of oligodendrocyte precursor cells depends on electrical activity in axons. Nature 361(6409):258-260.
57. Demerens C, et al. (1996) Induction of myelination in the central nervous system by electrical activity. Proc Natl Acad Sci USA 93(18):9887-9892.
58. Malone M, et al. (2013) Neuronal activity promotes myelination via a cAMP pathway. Glia 61(6):843-854.
59. Stevens B, Porta S, Haak LL, Gallo V, Fields RD (2002) Adenosine: A neuron-glial transmitter promoting myelination in the CNS in response to action potentials. Neuron 36(5):855-868.
60. Kazarinova-Noyes K, Shrager P (2002) Molecular constituents of the node of Ranvier. Mol Neurobiol 26(2-3):167-182.
61. Rothe C, et al. (2008) The human combinatorial antibody library HuCAL GOLD combines diversification of all six CDRs according to the natural immune system with a novel display method for efficient selection of high-affinity antibodies. J Mol Biol 376(4):1182-1200.
62. Gallyas F (1979) Silver staining of myelin by means of physical development. Neurol Res 1(2):203-209.
63. Friedrich VL, Mugnaini E (1981) Preparation of neural tissues for electron microscopy. Neuroanatomical Tract-Tracing Methods, eds Heimer L, Robards MJ (Plenum, New York), pp 345-375.