Composition, assembly, and maintenance of excitable membrane domains in myelinated axons

Seminars in Cell and Developmental Biology

Volumn 22, Issue 2, 2011, Pages 178-184

  Rasband, Matthew N ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Action potential; Cell adhesion molecule; Neuron glia interaction

Indexed keywords

CELL ADHESION MOLECULE; ION CHANNEL; SCAFFOLD PROTEIN;

EXCITABLE MEMBRANE; EXTRACELLULAR MATRIX; HUMAN; MYELINATED NERVE; NERVE CELL PLASTICITY; NERVE FIBER; NERVE FUNCTION; NEUROTRANSMISSION; NONHUMAN; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN DOMAIN; RANVIER NODE; REVIEW;

EID: 79953176267     PISSN: 10849521     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.semcdb.2010.09.010     Document Type: Review

References (88)

1. Hill A.S., Nishino A., Nakajo K., Zhang G., Fineman J.R., Selzer M.E., et al. Ion channel clustering at the axon initial segment and node of ranvier evolved sequentially in early chordates. PLoS Genet 2008, 4(12):e1000317.
2. Hille B. Ionic channels of excitable membranes 2001, Sinauer Associates, Inc., Sunderland, MA. 3rd ed.
3. Lorincz A., Nusser Z. Molecular identity of dendritic voltage-gated sodium channels. Science 2010, 328(5980):906-909.
4. Kole M.H., Ilschner S.U., Kampa B.M., Williams S.R., Ruben P.C., Stuart G.J. Action potential generation requires a high sodium channel density in the axon initial segment. Nat Neurosci 2008, 11(2):178-186.
5. Caldwell J.H., Schaller K.L., Lasher R.S., Peles E., Levinson S.R. Sodium channel Na(v)1.6 is localized at nodes of ranvier, dendrites, and synapses. Proc Natl Acad Sci U S A 2000, 97(10):5616-5620.
6. Duflocq A., Le Bras B., Bullier E., Couraud F., Davenne M. Nav1.1 is predominantly expressed in nodes of Ranvier and axon initial segments. Mol Cell Neurosci 2008.
7. Boiko T., Rasband M.N., Levinson S.R., Caldwell J.H., Mandel G., Trimmer J.S., et al. Compact myelin dictates the differential targeting of two sodium channel isoforms in the same axon. Neuron 2001, 30(1):91-104.
8. Schafer D.P., Custer A.W., Shrager P., Rasband M.N. Early events in node of Ranvier formation during myelination and remyelination in the PNS. Neuron Glia Biol 2006, 2(2):69-79.
9. Hu W., Tian C., Li T., Yang M., Hou H., Shu Y. Distinct contributions of Na(v)1.6 and Na(v)1.2 in action potential initiation and backpropagation. Nat Neurosci 2009, 12(8):996-1002.
10. Van Wart A., Trimmer J.S., Matthews G. Polarized distribution of ion channels within microdomains of the axon initial segment. J Comp Neurol 2007, 500(2):339-352.
11. Brackenbury W.J., Calhoun J.D., Chen C., Miyazaki H., Nukina N., Oyama F., et al. Functional reciprocity between Na+ channel Nav1.6 and beta1 subunits in the coordinated regulation of excitability and neurite outgrowth. Proc Natl Acad Sci U S A 2010, 107(5):2283-2288.
12. Lorincz A., Nusser Z. Cell-type-dependent molecular composition of the axon initial segment. J Neurosci 2008, 28(53):14329-14340.
13. Ogiwara I., Miyamoto H., Morita N., Atapour N., Mazaki E., Inoue I., et al. Na(v)1.1 localizes to axons of parvalbumin-positive inhibitory interneurons: a circuit basis for epileptic seizures in mice carrying an Scn1a gene mutation. J Neurosci 2007, 27(22):5903-5914.
14. Devaux J.J., Kleopa K.A., Cooper E.C., Scherer S.S. KCNQ2 is a Nodal K+ channel. J Neurosci 2004, 24(5):1236-1244.
15. Brown D.A., Passmore G.M., Neural KCNQ (Kv7) channels. Br J Pharmacol 2009, 156(8):1185-1195.
16. Schwarz J.R., Glassmeier G., Cooper E.C., Kao T.C., Nodera H., Tabuena D., et al. KCNQ channels mediate IKs, a slow K+ current regulating excitability in the rat node of Ranvier. J Physiol 2006, 573(Pt 1):17-34.
17. Cooper E.C. Made for "anchorin" Kv7.2/7.3 (KCNQ2/KCNQ3) channels and the modulation of neuronal excitability in vertebrate axons. Semin Cell Dev Biol 2010.
18. Ogawa Y., Horresh I., Trimmer J.S., Bredt D.S., Peles E., Rasband M.N. Postsynaptic density-93 clusters Kv1 channels at axon initial segments independently of Caspr2. J Neurosci 2008, 28(22):5731-5739.
19. Inda M.C., Defelipe J., Munoz A. Voltage-gated ion channels in the axon initial segment of human cortical pyramidal cells and their relationship with chandelier cells. Proc Natl Acad Sci U S A 2006.
20. Wang H., Kunkel D.D., Martin T.M., Schwartzkroin P.A., Tempel B.L. Heteromultimeric K+ channels in terminal and juxtaparanodal regions of neurons. Nature 1993, 365(6441):75-79.
21. Vabnick I., Trimmer J.S., Schwarz T.L., Levinson S.R., Risal D., Shrager P. Dynamic potassium channel distributions during axonal development prevent aberrant firing patterns. J Neurosci 1999, 19(2):747-758.
22. Rasband M.N. It's 'juxta' potassium channel. J Neurosci Res 2004, 76:749-757.
23. Kole M.H., Letzkus J.J., Stuart G.J. Axon initial segment Kv1 channels control axonal action potential waveform and synaptic efficacy. Neuron 2007, 55:633-647.
24. Goldberg E.M., Clark B.D., Zagha E., Nahmani M., Erisir A., Rudy B. K+ channels at the axon initial segment dampen near-threshold excitability of neocortical fast-spiking GABAergic interneurons. Neuron 2008, 58(3):387-400.
25. Garrido J.J., Giraud P., Carlier E., Fernandes F., Moussif A., Fache M.P., et al. A targeting motif involved in sodium channel clustering at the axonal initial segment. Science 2003, 300(5628):2091-2094.
26. Pan Z., Kao T., Horvath Z., Lemos J., Sul J.-Y., Cranstoun S.D., et al. A common ankyrin-G-based mechanism retains KCNQ and Nav channels at electrically active domains of the axon. J Neurosci 2006, 26:2599-2613.
27. Bréchet A., Fache M.P., Brachet A., Ferracci G., Baude A., Irondelle M., et al. Protein kinase CK2 contributes to the organization of sodium channels in axonal membranes by regulating their interaction with ankyrin G. J Cell Biol 2008, 183:1101-1114.
28. Leterrier C., Brachet A., Dargent B., Vacher H. Determinants of voltage-gated sodium channel clustering in neurons. Semin Cell Dev Biol 2010.
29. Berghs S., Aggujaro D., Dirkx R., Maksimova E., Stabach P., Hermel J.M., et al. betaIV spectrin, a new spectrin localized at axon initial segments and nodes of ranvier in the central and peripheral nervous system. J Cell Biol 2000, 151(5):985-1002.
30. Yang Y., Ogawa Y., Hedstrom K.L., Rasband M.N. {beta}IV spectrin is recruited to axon initial segments and nodes of Ranvier by ankyrinG. J Cell Biol 2007, 176(4):509-519.
31. Komada M., Soriano P. [Beta]IV-spectrin regulates sodium channel clustering through ankyrin-G at axon initial segments and nodes of Ranvier. J Cell Biol 2002, 156(2):337-348.
32. Lacas-Gervais S., Guo J., Strenzke N., Scarfone E., Kolpe M., Jahkel M., et al. BetaIVSigma1 spectrin stabilizes the nodes of Ranvier and axon initial segments. J Cell Biol 2004, 166(7):983-990.
33. Zhou D., Lambert S., Malen P.L., Carpenter S., Boland L.M., Bennett V. AnkyrinG is required for clustering of voltage-gated Na channels at axon initial segments and for normal action potential firing. J Cell Biol 1998, 143(5):1295-1304.
34. Hedstrom K.L., Xu X., Ogawa Y., Frischknecht R., Seidenbecher C.I., Shrager P., et al. Neurofascin assembles a specialized extracellular matrix at the axon initial segment. J Cell Biol 2007, 178(5):875-886.
35. Dzhashiashvili Y., Zhang Y., Galinska J., Lam I., Grumet M., Salzer J.L. Nodes of Ranvier and axon initial segments are ankyrin G-dependent domains that assemble by distinct mechanisms. J Cell Biol 2007, 177(5):857-870.
36. Rasband M.N., Park E.W., Zhen D., Arbuckle M.I., Poliak S., Peles E., et al. Clustering of neuronal potassium channels is independent of their interaction with PSD-95. J Cell Biol 2002, 159:663-672.
37. Horresh I., Poliak S., Grant S., Bredt D., Rasband M.N., Peles E. Multiple molecular interactions determine the clustering of Caspr2 and Kv1 channels in myelinated axons. J Neurosci 2008, 28(52):14213-14222.
38. Poliak S., Gollan L., Salomon D., Berglund E.O., Ohara R., Ranscht B., et al. Localization of Caspr2 in myelinated nerves depends on axon-glia interactions and the generation of barriers along the axon. J Neurosci 2001, 21(19):7568-7575.
39. Ogawa Y., Schafer D.P., Horresh I., Bar V., Hales K., Yang Y., et al. Spectrins and ankyrinB constitute a specialized paranodal cytoskeleton. J Neurosci 2006, 26(19):5230-5239.
40. Horresh I., Bar V., Kissil J.L., Peles E. Organization of myelinated axons by Caspr and Caspr2 requires the cytoskeletal adapter protein 4.1B. J Neurosci 2010, 30(7):2480-2489.
41. Ogawa Y., Oses-Prieto J., Kim M.Y., Horresh I., Peles E., Burlingame A.L., et al. ADAM22, a Kv1 channel-interacting protein, recruits membrane-associated guanylate kinases to juxtaparanodes of myelinated axons. J Neurosci 2010, 30:1038-1048.
42. Davis J.Q., Bennett V. Ankyrin binding activity shared by the neurofascin/L1/NrCAM family of nervous system cell adhesion molecules. J Biol Chem 1994, 269(44):27163-27166.
43. Jenkins S.M., Bennett V. Ankyrin-G coordinates assembly of the spectrin-based membrane skeleton, voltage-gated sodium channels, and L1 CAMs at Purkinje neuron initial segments. J Cell Biol 2001, 155(5):739-746.
44. Burkarth N., Kriebel M., Kranz E.U., Volkmer H. Neurofascin regulates the formation of gephyrin clusters and their subsequent translocation to the axon hillock of hippocampal neurons. Mol Cell Neurosci 2007, 36(1):59-70.
45. Ango F., di Cristo G., Higashiyama H., Bennett V., Wu P., Huang Z.J. Ankyrin-based subcellular gradient of neurofascin, an immunoglobulin family protein, directs GABAergic innervation at purkinje axon initial segment. Cell 2004, 119(2):257-272.
46. Zweier C., de Jong E.K., Zweier M., Orrico A., Ousager L.B., Collins A.L., et al. CNTNAP2 and NRXN1 are mutated in autosomal-recessive Pitt-Hopkins-like mental retardation and determine the level of a common synaptic protein in Drosophila. Am J Hum Genet 2009, 85(5):655-666.
47. Strauss K.A., Puffenberger E.G., Huentelman M.J., Gottlieb S., Dobrin S.E., Parod J.M., et al. Recessive symptomatic focal epilepsy and mutant contactin-associated protein-like 2. N Engl J Med 2006, 354(13):1370-1377.
48. Alarcon M., Abrahams B.S., Stone J.L., Duvall J.A., Perederiy J.V., Bomar J.M., et al. Linkage, association, and gene-expression analyses identify CNTNAP2 as an autism-susceptibility gene. Am J Hum Genet 2008, 82(1):150-159.
49. John N., Krugel H., Frischknecht R., Smalla K.H., Schultz C., Kreutz M.R., et al. Brevican-containing perineuronal nets of extracellular matrix in dissociated hippocampal primary cultures. Mol Cell Neurosci 2006.
50. Bekku Y., Rauch U., Ninomiya Y., Oohashi T. Brevican distinctively assembles extracellular components at the large diameter nodes of Ranvier in the CNS. J Neurochem 2009, 108(5):1266-1276.
51. Dours-Zimmerman M.T., Maurer K., Rauch U., Stoffel W., Fassler R., Zimmermann D.R. Versican V2 assembles the extracellular matrix surrounding the nodes of Ranvier in the central nervous system. J Neurosci 2009, 29:7731-7742.
52. Bekku Y., Vargova L., Goto Y., Vorisek I., Dmytrenko L., Narasaki M., et al. Bral1: its role in diffusion barrier formation and conduction velocity in the CNS. J Neurosci 2010, 30(8):3113-3123.
53. Weber P., Bartsch U., Rasband M.N., Czaniera R., Lang Y., Bluethmann H., et al. Mice deficient for tenascin-R display alterations of the extracellular matrix and decreased axonal conduction velocities in the CNS. J Neurosci 1999, 19(11):4245-4262.
54. Susuki K., Rasband M.N. Molecular mechanisms of node of Ranvier formation. Curr Opin Cell Biol 2008, 20(6):616-623.
55. Eshed Y., Feinberg K., Carey D.J., Peles E. Secreted gliomedin is a perinodal matrix component of peripheral nerves. J Cell Biol 2007, 177(3):551-562.
56. Feinberg K., Eshed-Eisenbach Y., Frechter S., Amor V., Salomon D., Sabanay H., et al. A glial signal consisting of gliomedin and NrCAM clusters axonal Na+ channels during the formation of nodes of Ranvier. Neuron 2010, 65(4):490-502.
57. Sagane K., Ishihama Y., Sugimoto H. LGI1 and LGI4 bind to ADAM22, ADAM23 and ADAM11. Int J Biol Sci 2008, 4(6):387-396.
58. Eshed Y., Feinberg K., Poliak S., Sabanay H., Sarig-Nadir O., Spiegel I., et al. Gliomedin mediates Schwann cell-axon interaction and the molecular assembly of the nodes of ranvier. Neuron 2005, 47(2):215-229.
59. Rasband M.N., Peles E., Trimmer J.S., Levinson S.R., Lux S.E., Shrager P. Dependence of nodal sodium channel clustering on paranodal axoglial contact in the developing CNS. J Neurosci 1999, 19(17):7516-7528.
60. Custer A.W., Kazarinova-Noyes K., Sakurai T., Xu X., Simon W., Grumet M., et al. The role of the ankyrin-binding protein NrCAM in node of Ranvier formation. J Neurosci 2003, 23(31):10032-10039.
61. Bhat M.A., Rios J.C., Lu Y., Garcia-Fresco G.P., Ching W., St Martin M., et al. Axon-glia interactions and the domain organization of myelinated axons requires neurexin IV/Caspr/Paranodin. Neuron 2001, 30(2):369-383.
62. Zonta B., Tait S., Melrose S., Anderson H., Harroch S., Higginson J., et al. Glial and neuronal isoforms of Neurofascin have distinct roles in the assembly of nodes of Ranvier in the central nervous system. J Cell Biol 2008, 181(7):1169-1177.
63. Dupree J.L., Girault J.-A., Popko B. Axo-glial interactions regulate the localization of axonal paranodal proteins. J Cell Biol 1999, 147(6):1145-1151.
64. Boyle M.E., Berglund E.O., Murai K.K., Weber L., Peles E., Ranscht B. Contactin orchestrates assembly of the septate-like junctions at the paranode in myelinated peripheral nerve. Neuron 2001, 30(2):385-397.
65. Poliak S., Salomon D., Elhanany H., Sabanay H., Kiernan B., Pevny L., et al. Juxtaparanodal clustering of Shaker-like K+ channels in myelinated axons depends on Caspr2 and TAG-1. J Cell Biol 2003, 162(6):1149-1160.
66. Traka M., Goutebroze L., Denisenko N., Bessa M., Nifli A., Havaki S., et al. Association of TAG-1 with Caspr2 is essential for the molecular organization of juxtaparanodal regions of myelinated fibers. J Cell Biol 2003, 162(6):1161-1172.
67. Hedstrom K.L., Ogawa Y., Rasband M.N. AnkyrinG is required for maintenance of the axon initial segment and neuronal polarity. J Cell Biol 2008, 183(4):635-640.
68. Nakada C., Ritchie K., Oba Y., Nakamura M., Hotta Y., Iino R., et al. Accumulation of anchored proteins forms membrane diffusion barriers during neuronal polarization. Nat Cell Biol 2003, 5(7):626-632.
69. Winckler B., Forscher P., Mellman I. A diffusion barrier maintains distribution of membrane proteins in polarized neurons. Nature 1999, 397(6721):698-701.
70. Sobotzik J.M., Sie J.M., Politi C., Del Turco D., Bennett V., Deller T., et al. AnkyrinG is required to maintain axo-dendritic polarity in vivo. Proc Natl Acad Sci U S A 2009, 106(41):17564-17569.
71. Song A.H., Wang D., Chen G., Li Y., Luo J., Duan S., et al. A selective filter for cytoplasmic transport at the axon initial segment. Cell 2009, 136(6):1148-1160.
72. Hirokawa N., Takemura R. Molecular motors and mechanisms of directional transport in neurons. Nat Rev Neurosci 2005, 6(3):201-214.
73. Rasband M.N. The axon initial segment and the maintenance of neuronal polarity. Nat Rev Neurosci 2010.
74. Grubb M.S., Burrone J. Activity-dependent relocation of the axon initial segment fine-tunes neuronal excitability. Nature 2010.
75. Kuba H., Oichi Y., Ohmori H. Presynaptic activity regulates Na(+) channel distribution at the axon initial segment. Nature 2010.
76. Dugandzija-Novakovic S., Koszowski A.G., Levinson S.R., Shrager P. Clustering of Na+ channels and node of Ranvier formation in remyelinating axons. J Neurosci 1995, 15(1 Pt 2):492-503.
77. Rasband M.N., Trimmer J.S., Schwarz T.L., Levinson S.R., Ellisman M.H., Schachner M., et al. Potassium channel distribution, clustering, and function in remyelinating rat axons. J Neurosci 1998, 18(1):36-47.
78. Rios J.C., Rubin M., St Martin M., Downey R.T., Einheber S., Rosenbluth J., et al. Paranodal interactions regulate expression of sodium channel subtypes and provide a diffusion barrier for the node of Ranvier. J Neurosci 2003, 23(18):7001-7011.
79. Coman I., Aigrot M.S., Seilhean D., Reynolds R., Girault J.A., Zalc B., et al. Nodal, paranodal and juxtaparanodal axonal proteins during demyelination and remyelination in multiple sclerosis. Brain 2006, 129(Pt 12):3186-3195.
80. Craner M.J., Newcombe J., Black J.A., Hartle C., Cuzner M.L., Waxman S.G. Molecular changes in neurons in multiple sclerosis: altered axonal expression of Nav1.2 and Nav1.6 sodium channels and Na+/Ca2+ exchanger. Proc Natl Acad Sci U S A 2004, 101(21):8168-8173.
81. Rasband M.N., Kagawa T., Park E.W., Ikenaka K., Trimmer J.S. Dysregulation of axonal sodium channel isoforms after adult-onset chronic demyelination. J Neurosci Res 2003, 73(4):465-470.
82. Devaux J.J., Scherer S.S. Altered ion channels in an animal model of Charcot-Marie-Tooth disease type IA. J Neurosci 2005, 25(6):1470-1480.
83. Windrem M.S., Schanz S.J., Guo M., Tian G.F., Washco V., Stanwood N., et al. Neonatal chimerization with human glial progenitor cells can both remyelinate and rescue the otherwise lethally hypomyelinated shiverer mouse. Cell Stem Cell 2008, 2(6):553-565.
84. Susuki K., Rasband M.N., Tohyama K., Koibuchi K., Okamoto S., Funakoshi K., et al. Anti-GM1 antibodies cause complement-mediated disruption of sodium channel clusters in peripheral motor nerve fibers. J Neurosci 2007, 27(15):3956-3967.
85. Mathey E.K., Derfuss T., Storch M.K., Williams K.R., Hales K., Woolley D.R., et al. Neurofascin as a novel target for autoantibody-mediated axonal injury. J Exp Med 2007, 204(10):2363-2372.
86. Schafer D.P., Jha S., Liu F., Akella T., McCullough L.D., Rasband M.N. Disruption of the axon initial segment cytoskeleton is a new mechanism for neuronal injury. J Neurosci 2009, 29(42):13242-13254.
87. von Reyn C.R., Spaethling J.M., Mesfin M.N., Ma M., Neumar R.W., Smith D.H., et al. Calpain mediates proteolysis of the voltage-gated sodium channel alpha-subunit. J Neurosci 2009, 29(33):10350-10356.
88. Reeves T.M., Greer J.E., Vanderveer A.S., Phillips L.L. Proteolysis of submembrane cytoskeletal proteins ankyrin-G and alphaII-spectrin following diffuse brain injury: a role in white matter vulnerability at nodes of ranvier. Brain Pathol 2010.