Submembranous cytoskeletons stabilize nodes of Ranvier

Experimental Neurology

Volumn 283, Issue , 2016, Pages 446-451

  Susuki, Keiichiro ^a   Otani, Yoshinori ^a   Rasband, Matthew N ^b  

^a WRIGHT STATE UNIVERSITY   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Ankyrin; Node of Ranvier; Paranode; Protein 4.1; Spectrin

Indexed keywords

ANKYRIN; ANKYRIN 3 NODE OF RANVIER; BETA III SPECTRIN; CYTOSKELETON PROTEIN; ERYTHROCYTE BAND 4.1 PROTEIN; MEMBRANE PROTEIN; POTASSIUM CHANNEL KCNQ2; POTASSIUM CHANNEL KCNQ3; SHAW POTASSIUM CHANNEL; SODIUM CHANNEL NAV1.6; SPECTRIN; SPECTRIN ALPHA NON ERYTHROCYTIC 1; UNCLASSIFIED DRUG; VOLTAGE GATED SODIUM CHANNEL; ION CHANNEL;

ANK3 GENE; AXON; BETA III SPECTRIN GENE; CELL ADHESION; CELL INTERACTION; CELL JUNCTION; COMPLEX FORMATION; GENE; GENE MUTATION; GLIA; JUXTAPARANODE; NERVE CONDUCTION; NERVOUS SYSTEM; NERVOUS SYSTEM INJURY; NEUROLOGIC DISEASE; NONHUMAN; PARANODE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; RANVIER NODE; REVIEW; SCHWANN CELL; SIGNAL TRANSDUCTION; SPTAN1 GENE; ANIMAL; CELL MEMBRANE; CYTOSKELETON; GAP JUNCTION; HUMAN; METABOLISM; PHYSIOLOGY;

ANIMALS; ANKYRINS; CELL MEMBRANE; CYTOSKELETON; GAP JUNCTIONS; HUMANS; ION CHANNELS; RANVIER'S NODES; SPECTRIN;

EID: 84957100256     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2015.11.012     Document Type: Review

References (71)

1. Arancibia-Carcamo, I.L., Attwell, D., The node of Ranvier in CNS pathology. Acta Neuropathol. 128 (2014), 161–175.
2. Armbrust, K.R., Wang, X., Hathorn, T.J., Cramer, S.W., Chen, G., Zu, T., Kangas, T., Zink, A.N., Öz, G., Ebner, T.J., Ranum, L.P., Mutant β-III spectrin causes mGluR1α mislocalization and functional deficits in a mouse model of spinocerebellar ataxia type 5. J. Neurosci. 34 (2014), 9891–9904.
3. Baines, A.J., The spectrin–ankyrin-4.1–adducin membrane skeleton: adapting eukaryotic cells to the demands of animal life. Protoplasma 244 (2010), 99–131.
4. Baines, A.J., Lu, H.C., Bennett, P.M., The protein 4.1 family: hub proteins in animals for organizing membrane proteins. Biochim. Biophys. Acta 1838 (2014), 605–619.
5. Bennett, V., Healy, J., Membrane domains based on ankyrin and spectrin associated with cell–cell interactions. Cold Spring Harb. Perspect. Biol., 1, 2009, a003012.
6. Berghs, S., Aggujaro, D., Dirkx, R. Jr., Maksimova, E., Stabach, P., Hermel, J.M., Zhang, J.P., Philbrick, W., Slepnev, V., Ort, T., Solimena, M., βIV spectrin, a new spectrin localized at axon initial segments and nodes of Ranvier in the central and peripheral nervous system. J. Cell Biol. 151 (2000), 985–1002.
7. Bhat, M.A., Rios, J.C., Lu, Y., Garcia-Fresco, G.P., Ching, W., St. Martin, M., Li, J., Einheber, S., Chesler, M., Rosenbluth, J., Salzer, J.L., Bellen, H.J., Axon-glia interactions and the domain organization of myelinated axons requires neurexin IV/caspr/paranodin. Neuron 30 (2001), 369–383.
8. Boiko, T., Rasband, M.N., Levinson, S.R., Caldwell, J.H., Mandel, G., Trimmer, J.S., Matthews, G., Compact myelin dictates the differential targeting of two sodium channel isoforms in the same axon. Neuron 30 (2001), 91–104.
9. 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 30 (2001), 385–397.
10. Buttermore, E.D., Dupree, J.L., Cheng, J., An, X., Tessarollo, L., Bhat, M.A., The cytoskeletal adaptor protein band 4.1B is required for the maintenance of paranodal axoglial septate junctions in myelinated axons. J. Neurosci. 31 (2011), 8013–8024.
11. 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. 97 (2000), 5616–5620.
12. Chang, K.J., Zollinger, D.R., Susuki, K., Sherman, D.L., Makara, M.A., Brophy, P.J., Cooper, E.C., Bennett, V., Mohler, P.J., Rasband, M.N., Glial ankyrins facilitate paranodal axoglial junction assembly. Nat. Neurosci. 17 (2014), 1673–1681.
13. Cifuentes-Diaz, C., Chareyre, F., Garcia, M., Devaux, J., Carnaud, M., Levasseur, G., Niwa-Kawakita, M., Harroch, S., Girault, J.A., Giovannini, M., Goutebroze, L., Protein 4.1B contributes to the organization of peripheral myelinated axons. PLoS One, 6, 2011, e25043.
14. Czogalla, A., Sikorski, A.F., Spectrin and calpain: a ‘target’ and a ‘sniper’ in the pathology of neuronal cells. Cell. Mol. Life Sci. 62 (2005), 1913–1924.
15. Denisenko-Nehrbass, N., Oguievetskaia, K., Goutebroze, L., Galvez, T., Yamakawa, H., Ohara, O., Carnaud, M., Girault, J.A., Protein 4.1B associates with both Caspr/paranodin and Caspr2 at paranodes and juxtaparanodes of myelinated fibres. Eur. J. Neurosci. 17 (2003), 411–416.
16. Devaux, J., Alcaraz, G., Grinspan, J., Bennett, V., Joho, R., Crest, M., Scherer, S.S., Kv3.1b is a novel component of CNS nodes. J. Neurosci. 23 (2003), 4509–4518.
17. + channel. J. Neurosci. 24 (2004), 1236–1244.
18. Duflocq, A., Chareyre, F., Giovannini, M., Couraud, F., Davenne, M., Characterization of the axon initial segment (AIS) of motor neurons and identification of a para-AIS and a juxtapara-AIS, organized by protein 4.1B. BMC Biol., 9, 2011, 66.
19. 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. 177 (2007), 857–870.
20. Einheber, S., Meng, X., Rubin, M., Lam, I., Mohandas, N., An, X., Shrager, P., Kissil, J., Maurel, P., Salzer, J.L., The 4.1B cytoskeletal protein regulates the domain organization and sheath thickness of myelinated axons. Glia 61 (2013), 240–253.
21. Eshed-Eisenbach, Y., Peles, E., The making of a node: a co-production of neurons and glia. Curr. Opin. Neurobiol. 23 (2013), 1049–1056.
22. Faivre-Sarrailh, C., Devaux, J.J., Neuro-glial interactions at the nodes of Ranvier: implication in health and diseases. Front. Cell. Neurosci., 7, 2013, 196.
23. + channels during the formation of nodes of Ranvier. Neuron 65 (2010), 490–502.
24. Galiano, M.R., Jha, S., Ho, T.S., Zhang, C., Ogawa, Y., Chang, K.J., Stankewich, M.C., Mohler, P.J., Rasband, M.N., A distal axonal cytoskeleton forms an intra-axonal boundary that controls axon initial segment assembly. Cell 149 (2012), 1125–1139.
25. Garcia-Fresco, G.P., Sousa, A.D., Pillai, A.M., Moy, S.S., Crawley, J.N., Tessarollo, L., Dupree, J.L., Bhat, M.A., Disruption of axo-glial junctions causes cytoskeletal disorganization and degeneration of Purkinje neuron axons. Proc. Natl. Acad. Sci. U. S. A. 103 (2006), 5137–5142.
26. Gasser, A., Ho, T.S., Cheng, X., Chang, K.J., Waxman, S.G., Rasband, M.N., Dib-Hajj, S.D., An ankyrinG-binding motif is necessary and sufficient for targeting Nav1.6 sodium channels to axon initial segments and nodes of Ranvier. J. Neurosci. 32 (2012), 7232–7243.
27. Gollan, L., Sabanay, H., Poliak, S., Berglund, E.O., Ranscht, B., Peles, E., Retention of a cell adhesion complex at the paranodal junction requires the cytoplasmic region of Caspr. J. Cell Biol. 157 (2002), 1247–1256.
28. Gollan, L., Salomon, D., Salzer, J.L., Peles, E., Caspr regulates the processing of contactin and inhibits its binding to neurofascin. J. Cell Biol. 163 (2003), 1213–1218.
29. Ho, T.S., Zollinger, D.R., Chang, K.J., Xu, M., Cooper, E.C., Stankewich, M.C., Bennett, V., Rasband, M.N., A hierarchy of ankyrin–spectrin complexes clusters sodium channels at nodes of Ranvier. Nat. Neurosci. 17 (2014), 1664–1672.
30. 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. 30 (2010), 2480–2489.
31. Ikeda, Y., Dick, K.A., Weatherspoon, M.R., Gincel, D., Armbrust, K.R., Dalton, J.C., Stevanin, G., Dürr, A., Zühlke, C., Bürk, K., Clark, H.B., Brice, A., Rothstein, J.D., Schut, L.J., Day, J.W., Ranum, L.P., Spectrin mutations cause spinocerebellar ataxia type 5. Nat. Genet. 38 (2006), 184–190.
32. Iqbal, Z., Vandeweyer, G., van der Voet, M., Waryah, A.M., Zahoor, M.Y., Besseling, J.A., Roca, L.T., Vulto-van Silfhout, A.T., Nijhof, B., Kramer, J.M., Van der Aa, N., Ansar, M., Peeters, H., Helsmoortel, C., Gilissen, C., Vissers, L.E., Veltman, J.A., de Brouwer, A.P., Frank Kooy, R., Riazuddin, S., Schenck, A., van Bokhoven, H., Rooms, L., Homozygous and heterozygous disruptions of ANK3: at the crossroads of neurodevelopmental and psychiatric disorders. Hum. Mol. Genet. 22 (2013), 1960–1970.
33. Ivanovic, A., Horresh, I., Golan, N., Spiegel, I., Sabanay, H., Frechter, S., Ohno, S., Terada, N., Möbius, W., Rosenbluth, J., Brose, N., Peles, E., The cytoskeletal adapter protein 4.1G organizes the internodes in peripheral myelinated nerves. J. Cell Biol. 196 (2012), 337–344.
34. Jenkins, P.M., Kim, N., Jones, S.L., Tseng, W.C., Svitkina, T.M., Yin, H.H., Bennett, V., Giant ankyrin-G: a critical innovation in vertebrate evolution of fast and integrated neuronal signaling. Proc. Natl. Acad. Sci. U. S. A. 112 (2015), 957–964.
35. Komada, M., Soriano, P., βIV-spectrin regulates sodium channel clustering through ankyrin-G at axon initial segments and nodes of Ranvier. J. Cell Biol. 156 (2002), 337–348.
36. Kordeli, E., Lambert, S., Bennett, V., AnkyrinG. A new ankyrin gene with neural-specific isoforms localized at the axonal initial segment and node of Ranvier. J. Biol. Chem. 270 (1995), 2352–2359.
37. Leussis, M.P., Madison, J.M., Petryshen, T.L., Ankyrin 3: genetic association with bipolar disorder and relevance to disease pathophysiology. Biol. Mood Anxiety Disord., 2, 2012, 18.
38. Machnicka, B., Czogalla, A., Hryniewicz-Jankowska, A., Bogusławska, D.M., Grochowalska, R., Heger, E., Sikorski, A.F., Spectrins: a structural platform for stabilization and activation of membrane channels, receptors and transporters. Biochim. Biophys. Acta 1838 (2014), 620–634.
39. Mondello, S., Robicsek, S.A., Gabrielli, A., Brophy, G.M., Papa, L., Tepas, J., Robertson, C., Buki, A., Scharf, D., Jixiang, M., Akinyi, L., Muller, U., Wang, K.K., Hayes, R.L., αII-spectrin breakdown products (SBDPs): diagnosis and outcome in severe traumatic brain injury patients. J. Neurotrauma 27 (2010), 1203–1213.
40. Normand, E.A., Rasband, M.N., Subcellular patterning: axonal domains with specialized structure and function. Dev. Cell 32 (2015), 459–468.
41. Ogawa, Y., Schafer, D.P., Horresh, I., Bar, V., Hales, K., Yang, Y., Susuki, K., Peles, E., Stankewich, M.C., Rasband, M.N., Spectrins and ankyrinB constitute a specialized paranodal cytoskeleton. J. Neurosci. 26 (2006), 5230–5239.
42. Ohara, R., Yamakawa, H., Nakayama, M., Ohara, O., Type II brain 4.1 (4.1B/KIAA0987), a member of the protein 4.1 family, is localized to neuronal paranodes. Brain Res. Mol. Brain Res. 85 (2000), 41–52.
43. Ohno, N., Terada, N., Yamakawa, H., Komada, M., Ohara, O., Trapp, B.D., Ohno, S., Expression of protein 4.1G in Schwann cells of the peripheral nervous system. J. Neurosci. Res. 84 (2006), 568–577.
44. Pan, Z., Kao, T., Horvath, Z., Lemos, J., Sul, J.Y., Cranstoun, S.D., Bennett, V., Scherer, S.S., Cooper, E.C., A common ankyrin-G-based mechanism retains KCNQ and Nav channels at electrically active domains of the axon. J. Neurosci. 26 (2006), 2599–2613.
45. NF155) in mice reveals gradual loss of paranodal axoglial junctions and concomitant disorganization of axonal domains. J. Neurosci. Res. 87 (2009), 1773–1793.
46. + channels in myelinated axons depends on Caspr2 and TAG-1. J. Cell Biol. 162 (2003), 1149–1160.
47. Reeves, T.M., Greer, J.E., Vanderveer, A.S., Phillips, L.L., Proteolysis of submembrane cytoskeletal proteins ankyrin-G and αII-spectrin following diffuse brain injury: a role in white matter vulnerability at nodes of Ranvier. Brain Pathol. 20 (2010), 1055–1068.
48. Rosenbluth, J., Multiple functions of the paranodal junction of myelinated nerve fibers. J. Neurosci. Res. 87 (2009), 3250–3258.
49. Saatman, K.E., Creed, J., Raghupathi, R., Calpain as a therapeutic target in traumatic brain injury. Neurotherapeutics 7 (2010), 31–42.
50. 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. 29 (2009), 13242–13254.
51. Sherman, D.L., Tait, S., Melrose, S., Johnson, R., Zonta, B., Court, F.A., Macklin, W.B., Meek, S., Smith, A.J., Cottrell, D.F., Brophy, P.J., Neurofascins are required to establish axonal domains for saltatory conduction. Neuron 48 (2005), 737–742.
52. Shi, L., Zhang, X., Golhar, R., Otieno, F.G., He, M., Hou, C., Kim, C., Keating, B., Lyon, G.J., Wang, K., Hakonarson, H., Whole-genome sequencing in an autism multiplex family. Mol. Autism, 4, 2013, 8.
53. Shields, D.C., Schaecher, K.E., Saido, T.C., Banik, N.L., A putative mechanism of demyelination in multiple sclerosis by a proteolytic enzyme, calpain. Proc. Natl. Acad. Sci. U. S. A. 96 (1999), 11486–11491.
54. Smith, K.R., Kopeikina, K.J., Fawcett-Patel, J.M., Leaderbrand, K., Gao, R., Schürmann, B., Myczek, K., Radulovic, J., Swanson, G.T., Penzes, P., Psychiatric risk factor ANK3/ankyrin-G nanodomains regulate the structure and function of glutamatergic synapses. Neuron 84 (2014), 399–415.
55. Sun, X.Y., Takagishi, Y., Okabe, E., Chishima, Y., Kanou, Y., Murase, S., Mizumura, K., Inaba, M., Komatsu, Y., Hayashi, Y., Peles, E., Oda, S., Murata, Y., A novel Caspr mutation causes the shambling mouse phenotype by disrupting axoglial interactions of myelinated nerves. J. Neuropathol. Exp. Neurol. 68 (2009), 1207–1218.
56. Susuki, K., Node of Ranvier disruption as a cause of neurological diseases. ASN Neuro 5 (2013), 209–219.
57. Susuki, K., Raphael, A.R., Ogawa, Y., Stankewich, M.C., Peles, E., Talbot, W.S., Rasband, M.N., Schwann cell spectrins modulate peripheral nerve myelination. Proc. Natl. Acad. Sci. U. S. A. 108 (2011), 8009–8014.
58. Susuki, K., Chang, K.J., Zollinger, D.R., Liu, Y., Ogawa, Y., Eshed-Eisenbach, Y., Dours-Zimmermann, M.T., Oses-Prieto, J.A., Burlingame, A.L., Seidenbecher, C.I., Zimmermann, D.R., Oohashi, T., Peles, E., Rasband, M.N., Three mechanisms assemble central nervous system nodes of Ranvier. Neuron 78 (2013), 469–482.
59. Terada, N., Saitoh, Y., Ohno, N., Komada, M., Saitoh, S., Peles, E., Ohno, S., Essential function of protein 4.1G in targeting of membrane protein palmitoylated 6 into Schmidt–Lanterman incisures in myelinated nerves. Mol. Cell. Biol. 32 (2012), 199–205.
60. Tohyama, J., Nakashima, M., Nabatame, S., Gaik-Siew, C., Miyata, R., Rener-Primec, Z., Kato, M., Matsumoto, N., Saitsu, H., SPTAN1 encephalopathy: distinct phenotypes and genotypes. J. Hum. Genet. 60 (2015), 167–173.
61. Traka, M., Goutebroze, L., Denisenko, N., Bessa, M., Nifli, A., Havaki, S., Iwakura, Y., Fukamauchi, F., Watanabe, K., Soliven, B., Girault, J.A., Karagogeos, D., Association of TAG-1 with Caspr2 is essential for the molecular organization of juxtaparanodal regions of myelinated fibers. J. Cell Biol. 162 (2003), 1161–1172.
62. Tseng, W.C., Jenkins, P.M., Tanaka, M., Mooney, R., Bennett, V., Giant ankyrin-G stabilizes somatodendritic GABAergic synapses through opposing endocytosis of GABAA receptors. Proc. Natl. Acad. Sci. U. S. A. 112 (2015), 1214–1219.
63. Voas, M.G., Lyons, D.A., Naylor, S.G., Arana, N., Rasband, M.N., Talbot, W.S., αII-spectrin is essential for assembly of the nodes of Ranvier in myelinated axons. Curr. Biol. 17 (2007), 562–568.
64. + channels in terminal and juxtaparanodal regions of neurons. Nature 365 (1993), 75–79.
65. Xu, M., Cooper, E.C., An ankyrin-G N-terminal gate and protein kinase CK2 dually regulate binding of voltage-gated sodium and KCNQ2/3 potassium channels. J. Biol. Chem. 290 (2015), 16619–16632.
66. Yan, X.X., Jeromin, A., Jeromin, A., Spectrin breakdown products (SBDPs) as potential biomarkers for neurodegenerative diseases. Curr. Transl. Geriatr. Exp. Gerontol. Rep. 1 (2012), 85–93.
67. Yang, Y., Lacas-Gervais, S., Morest, D.K., Solimena, M., Rasband, M.N., βIV spectrins are essential for membrane stability and the molecular organization of nodes of Ranvier. J. Neurosci. 24 (2004), 7230–7240.
68. Yang, Y., Ogawa, Y., Hedstrom, K.L., Rasband, M.N., βIV spectrin is recruited to axon initial segments and nodes of Ranvier by ankyrinG. J. Cell Biol. 176 (2007), 509–519.
69. Yuan, A., Yi, Z., Wang, Q., Sun, J., Li, Z., Du, Y., Zhang, C., Yu, T., Fan, J., Li, H., Yu, S., ANK3 as a risk gene for schizophrenia: new data in Han Chinese and meta analysis. Am. J. Med. Genet. B Neuropsychiatr. Genet. 159B (2012), 997–1005.
70. Zhang, C., Susuki, K., Zollinger, D.R., Dupree, J.L., Rasband, M.N., Membrane domain organization of myelinated axons requires βII spectrin. J. Cell Biol. 203 (2013), 437–443.
71. Zonta, B., Tait, S., Melrose, S., Anderson, H., Harroch, S., Higginson, J., Sherman, D.L., Brophy, P.J., Glial and neuronal isoforms of neurofascin have distinct roles in the assembly of nodes of Ranvier in the central nervous system. J. Cell Biol. 181 (2008), 1169–1177.