Assembly and Maintenance of Nodes of Ranvier Rely on Distinct Sources of Proteins and Targeting Mechanisms

Neuron

Volumn 73, Issue 1, 2012, Pages 92-107

  Zhang, Yanqing ^a   Bekku, Yoko ^a   Dzhashiashvili, Yulia ^a   Armenti, Stephen ^a   Meng, Xiaosong ^a   Sasaki, Yo ^b   Milbrandt, Jeffrey ^b   Salzer, James L ^a  

^a NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BREFELDIN A; CELL ADHESION MOLECULE; CYTOSKELETON PROTEIN; GLYCOPROTEIN; ION CHANNEL; NERVE CELL ADHESION MOLECULE; NEUROFASCIN 186; NICOTINAMIDE MONONUCLEOTIDE ADENYLYL TRANSFERASE 1; NICOTINAMIDE NUCLEOTIDE ADENYLYLTRANSFERASE; PROTEIN CASPR; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BIOACCUMULATION; CELLULAR DISTRIBUTION; CHANNEL GATING; CONTROLLED STUDY; DIFFUSION; IN VITRO STUDY; MOUSE; MYELINATION; NERVE DEGENERATION; NERVE FIBER; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN TARGETING; PROTEIN TRANSPORT; RANVIER NODE; RAT; REGULATORY MECHANISM; SCHWANN CELL; TRANSGENIC MOUSE;

ANIMALS; BIOTINYLATION; CELL ADHESION MOLECULES; CELLS, CULTURED; COCULTURE TECHNIQUES; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; GANGLIA, SPINAL; GENE EXPRESSION REGULATION; GREEN FLUORESCENT PROTEINS; INTERCELLULAR ADHESION MOLECULE-1; MICE; MICE, TRANSGENIC; MICROSCOPY, CONFOCAL; MODELS, BIOLOGICAL; MYELIN BASIC PROTEINS; NERVE GROWTH FACTORS; NERVE TISSUE PROTEINS; NEURONS; RANVIER'S NODES; RATS; SCHWANN CELLS; TRANSFECTION;

EID: 84862908261     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2011.10.016     Document Type: Article

References (61)

1. Aigner L., Arber S., Kapfhammer J.P., Laux T., Schneider C., Botteri F., Brenner H.R., Caroni P. Overexpression of the neural growth-associated protein GAP-43 induces nerve sprouting in the adult nervous system of transgenic mice. Cell 1995, 83:269-278.
2. Alix J.J., Dolphin A.C., Fern R. Vesicular apparatus, including functional calcium channels, are present in developing rodent optic nerve axons and are required for normal node of Ranvier formation. J.Physiol. 2008, 586:4069-4089.
3. Anderson E., Maday S., Sfakianos J., Hull M., Winckler B., Sheff D., Fölsch H., Mellman I. Transcytosis of NgCAM in epithelial cells reflects differential signal recognition on the endocytic and secretory pathways. J. Cell Biol. 2005, 170:595-605.
4. Armstrong R., Toews A.D., Morell P. Axonal transport through nodes of Ranvier. Brain Res. 1987, 412:196-199.
5. Beckett D., Kovaleva E., Schatz P.J. A minimal peptide substrate in biotin holoenzyme synthetase-catalyzed biotinylation. Protein Sci. 1999, 8:921-929.
6. 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., et al. Axon-glia interactions and the domain organization of myelinated axons requires neurexin IV/Caspr/Paranodin. Neuron 2001, 30:369-383.
7. 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 2001, 30:91-104.
8. Boiko T., Vakulenko M., Ewers H., Yap C.C., Norden C., Winckler B. Ankyrin-dependent and -independent mechanisms orchestrate axonal compartmentalization of L1 family members neurofascin and L1/neuron-glia cell adhesion molecule. J.Neurosci. 2007, 27:590-603.
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 2001, 30:385-397.
10. Campenot R.B., Soin J., Blacker M., Lund K., Eng H., MacInnis B.L. Block of slow axonal transport and axonal growth by brefeldin A in compartmented cultures of rat sympathetic neurons. Neuropharmacology 2003, 44:1107-1117.
11. Chung H.J., Jan Y.N., Jan L.Y. Polarized axonal surface expression of neuronal KCNQ channels is mediated by multiple signals in the KCNQ2 and KCNQ3 C-terminal domains. Proc. Natl. Acad. Sci. USA 2006, 103:8870-8875.
12. Devaux J.J. The C-terminal domain of ßIV-spectrin is crucial for KCNQ2 aggregation and excitability at nodes of Ranvier. J.Physiol. 2010, 588:4719-4730.
13. Dityatev A., Seidenbecher C.I., Schachner M. Compartmentalization from the outside: the extracellular matrix and functional microdomains in the brain. Trends Neurosci. 2010, 33:503-512.
14. 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, 177:857-870.
15. Edwards C., Frisch H.L. A model for the localization of acetylcholine receptors at the muscle endplate. J.Neurobiol. 1976, 7:377-381.
16. Einheber S., Milner T.A., Giancotti F., Salzer J.L. Axonal regulation of Schwann cell integrin expression suggests a role for alpha 6 beta 4 in myelination. J. Cell Biol. 1993, 123:1223-1236.
17. Eshed Y., Feinberg K., Poliak S., Sabanay H., Sarig-Nadir O., Spiegel I., Bermingham J.R., Peles E. Gliomedin mediates Schwann cell-axon interaction and the molecular assembly of the nodes of Ranvier. Neuron 2005, 47:215-229.
18. Fache M.P., Moussif A., Fernandes F., Giraud P., Garrido J.J., Dargent B. Endocytotic elimination and domain-selective tethering constitute a potential mechanism of protein segregation at the axonal initial segment. J. Cell Biol. 2004, 166:571-578.
19. Feinberg K., Eshed-Eisenbach Y., Frechter S., Amor V., Salomon D., Sabanay H., Dupree J.L., Grumet M., Brophy P.J., Shrager P., Peles E. A glial signal consisting of gliomedin and NrCAM clusters axonal Na+ channels during the formation of nodes of Ranvier. Neuron 2010, 65:490-502.
20. Feng G., Mellor R.H., Bernstein M., Keller-Peck C., Nguyen Q.T., Wallace M., Nerbonne J.M., Lichtman J.W., Sanes J.R. Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 2000, 28:41-51.
21. Geng L., Zhang H.L., Peng H.B. The formation of acetylcholine receptor clusters visualized with quantum dots. BMC Neurosci. 2009, 10:80.
22. Goldstein A.Y., Wang X., Schwarz T.L. Axonal transport and the delivery of pre-synaptic components. Curr. Opin. Neurobiol. 2008, 18:495-503.
23. Howarth M., Takao K., Hayashi Y., Ting A.Y. Targeting quantum dots to surface proteins in living cells with biotin ligase. Proc. Natl. Acad. Sci. USA 2005, 102:7583-7588.
24. Jin Y., Garner C.C. Molecular mechanisms of presynaptic differentiation. Annu. Rev. Cell Dev. Biol. 2008, 24:237-262.
25. Kaplan M.R., Cho M.H., Ullian E.M., Isom L.L., Levinson S.R., Barres B.A. Differential control of clustering of the sodium channels Na(v)1.2 and Na(v)1.6 at developing CNS nodes of Ranvier. Neuron 2001, 30:105-119.
26. Klausner R.D., Donaldson J.G., Lippincott-Schwartz J. Brefeldin A: insights into the control of membrane traffic and organelle structure. J. Cell Biol. 1992, 116:1071-1080.
27. Lai H.C., Jan L.Y. The distribution and targeting of neuronal voltage-gated ion channels. Nat. Rev. Neurosci. 2006, 7:548-562.
28. Lambert S., Davis J.Q., Bennett V. Morphogenesis of the node of Ranvier: co-clusters of ankyrin and ankyrin-binding integral proteins define early developmental intermediates. J.Neurosci. 1997, 17:7025-7036.
29. Lee A., Goldin A.L. Role of the terminal domains in sodium channel localization. Channels (Austin) 2009, 3:171-180.
30. Lonigro A., Devaux J.J. Disruption of neurofascin and gliomedin at nodes of Ranvier precedes demyelination in experimental allergic neuritis. Brain 2009, 132:260-273.
31. Lustig M., Erskine L., Mason C.A., Grumet M., Sakurai T. Nr-CAM expression in the developing mouse nervous system: ventral midline structures, specific fiber tracts, and neuropilar regions. J.Comp. Neurol. 2001, 434:13-28.
32. McEwen D.P., Isom L.L. Heterophilic interactions of sodium channel beta1 subunits with axonal and glial cell adhesion molecules. J.Biol. Chem. 2004, 279:52744-52752.
33. Opazo P., Choquet D. A three-step model for the synaptic recruitment of AMPA receptors. Mol. Cell. Neurosci. 2011, 46:1-8.
34. 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. 2006, 26:2599-2613.
35. Pedraza L., Huang J.K., Colman D.R. Organizing principles of the axoglial apparatus. Neuron 2001, 30:335-344.
36. Pillai A.M., Thaxton C., Pribisko A.L., Cheng J.G., Dupree J.L., Bhat M.A. 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. 2009, 87:1773-1793.
37. Rasband M.N. The axon initial segment and the maintenance of neuronal polarity. Nat. Rev. Neurosci. 2010, 11:552-562.
38. Rasband M.N., Taylor C.M., Bansal R. Paranodal transverse bands are required for maintenance but not initiation of Nav1.6 sodium channel clustering in CNS optic nerve axons. Glia 2003, 44:173-182.
39. Ratcliffe C.F., Westenbroek R.E., Curtis R., Catterall W.A. Sodium channel beta1 and beta3 subunits associate with neurofascin through their extracellular immunoglobulin-like domain. J. Cell Biol. 2001, 154:427-434.
40. Rios J.C., Melendez-Vasquez C.V., Einheber S., Lustig M., Grumet M., Hemperly J., Peles E., Salzer J.L. Contactin-associated protein (Caspr) and contactin form a complex that is targeted to the paranodal junctions during myelination. J.Neurosci. 2000, 20:8354-8364.
41. Rios J.C., Rubin M., St Martin M., Downey R.T., Einheber S., Rosenbluth J., Levinson S.R., Bhat M., Salzer J.L. Paranodal interactions regulate expression of sodium channel subtypes and provide a diffusion barrier for the node of Ranvier. J.Neurosci. 2003, 23:7001-7011.
42. Rosenbluth J. Multiple functions of the paranodal junction of myelinated nerve fibers. J.Neurosci. Res. 2009, 87:3250-3258.
43. Salzer J.L. Clustering sodium channels at the node of Ranvier: close encounters of the axon-glia kind. Neuron 1997, 18:843-846.
44. Salzer J.L. Polarized domains of myelinated axons. Neuron 2003, 40:297-318.
45. Salzer J.L., Brophy P.J., Peles E. Molecular domains of myelinated axons in the peripheral nervous system. Glia 2008, 56:1532-1540.
46. Sasaki Y., Araki T., Milbrandt J. Stimulation of nicotinamide adenine dinucleotide biosynthetic pathways delays axonal degeneration after axotomy. J.Neurosci. 2006, 26:8484-8491.
47. Sasaki Y., Vohra B.P., Baloh R.H., Milbrandt J. Transgenic mice expressing the Nmnat1 protein manifest robust delay in axonal degeneration invivo. J.Neurosci. 2009, 29:6526-6534.
48. 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 2005, 48:737-742.
49. Shin K.J., Wall E.A., Zavzavadjian J.R., Santat L.A., Liu J., Hwang J.I., Rebres R., Roach T., Seaman W., Simon M.I., Fraser I.D. A single lentiviral vector platform for microRNA-based conditional RNA interference and coordinated transgene expression. Proc. Natl. Acad. Sci. USA 2006, 103:13759-13764.
50. Siggia E.D., Lippincott-Schwartz J., Bekiranov S. Diffusion in inhomogeneous media: theory and simulations applied to whole cell photobleach recovery. Biophys. J. 2000, 79:1761-1770.
51. Snapp E.L., Altan N., Lippincott-Schwartz J. Measuring protein mobility by photobleaching GFP chimeras in living cells. Curr. Protoc. Cell Biol. 2003, Chapter 21. Unit 21.1.
52. Susuki K., Rasband M.N. Molecular mechanisms of node of Ranvier formation. Curr. Opin. Cell Biol. 2008, 20:616-623.
53. Taylor A.M., Blurton-Jones M., Rhee S.W., Cribbs D.H., Cotman C.W., Jeon N.L. A microfluidic culture platform for CNS axonal injury, regeneration and transport. Nat. Methods 2005, 2:599-605.
54. Thaxton C., Pillai A.M., Pribisko A.L., Dupree J.L., Bhat M.A. Nodes of Ranvier act as barriers to restrict invasion of flanking paranodal domains in myelinated axons. Neuron 2011, 69:244-257.
55. Tzoumaka E.E., Novaković S.D., Levinson S.R., Shrager P. Na+ channel aggregation in remyelinating mouse sciatic axons following transection. Glia 1995, 15:188-194.
56. Wisco D., Anderson E.D., Chang M.C., Norden C., Boiko T., Fölsch H., Winckler B. Uncovering multiple axonal targeting pathways in hippocampal neurons. J. Cell Biol. 2003, 162:1317-1328.
57. Woods I.G., Lyons D.A., Voas M.G., Pogoda H.M., Talbot W.S. nsf is essential for organization of myelinated axons in zebrafish. Curr. Biol. 2006, 16:636-648.
58. Zhang C.L., Ho P.L., Kintner D.B., Sun D., Chiu S.Y. Activity-dependent regulation of mitochondrial motility by calcium and Na/K-ATPase at nodes of Ranvier of myelinated nerves. J.Neurosci. 2010, 30:3555-3566.
59. Zhang J., Bal M., Bierbower S., Zaika O., Shapiro M.S. AKAP79/150 signal complexes in G-protein modulation of neuronal ion channels. J.Neurosci. 2011, 31:7199-7211.
60. Zimmermann H. Accumulation of synaptic vesicle proteins and cytoskeletal specializations at the peripheral node of Ranvier. Microsc. Res. Tech. 1996, 34:462-473.
61. Zonta B., Desmazieres A., Rinaldi A., Tait S., Sherman D.L., Nolan M.F., Brophy P.J. A critical role for Neurofascin in regulating action potential initiation through maintenance of the axon initial segment. Neuron 2011, 69:945-956.