Three mechanisms assemble central nervous system nodes of Ranvier
Open accessAbstract
Rapid action potential propagation in myelinated axons requires Na⁺ channel clustering at nodes of Ranvier. However, the mechanism of clustering at CNS nodes remains poorly understood. Here, we show that the assembly of nodes of Ranvier in the CNS involves three mechanisms: a glia-derived extracellular matrix (ECM) complex containing proteoglycans and adhesion molecules that cluster NF186, paranodal axoglial junctions that function as barriers to restrict the position of nodal proteins, and axonal cytoskeletal scaffolds (CSs) that stabilize nodal Na⁺ channels. We show that while mice with a single disrupted mechanism had mostly normal nodes, disruptions of the ECM and paranodal barrier, the ECM and CS, or the paranodal barrier and CS all lead to juvenile lethality, profound motor dysfunction, and significantly reduced Na⁺ channel clustering. Our results demonstrate that ECM, paranodal, and axonal cytoskeletal mechanisms ensure robust CNS nodal Na⁺ channel clustering.
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CNS nodal ECMs do not play a primary role in recruiting Na+ channels at the nodes, but play a compensating role in assembling nodes or are important for stabilizing the nodes.
“CNS nodal ECMs do not play a primary role to recruit Na + channels at the nodes, but play a compensating mechanism for assembling nodes or are important for stabilizing the nodes.”
From The hyaluronan and proteoglycan link proteins: Organizers of the brain extracellular matrix and key molecules for neuronal function and plasticity (2015) · cites this paper as Susuki et al., 2013
Susuki et al. demonstrated a hierarchy between three mechanisms: paranodal junction barriers, axonal cytoskeletal scaffolds, and NF186-binding ECM proteins.
“They demonstrate the existence of hierarchy between three mechanisms.”
From The hyaluronan and proteoglycan link proteins: Organizers of the brain extracellular matrix and key molecules for neuronal function and plasticity (2015) · cites this paper as Susuki et al., 2013
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Self-citationAn αII Spectrin-Based Cytoskeleton Protects Large-Diameter Myelinated Axons from Degeneration
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Self-citationNode of Ranvier Disruption as a Cause of Neurological Diseases
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Self-citationMyelination induces axonal hotspots of synaptic vesicle fusion that promote sheath growth
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CNS myelination requires VAMP2/3-mediated membrane expansion in oligodendrocytes
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Self-citationNeural ECM molecules in axonal and synaptic homeostatic plasticity
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Self-citationCytoskeletal control of axon domain assembly and function
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Self-citationMurcia‐Belmonte, V., Esteban, P. F., Hernández, J. M., Gruart, A., Luján, R., Delgado-Garcia, J. M., & de Castro, F. (2015) · Brain Structure and Function · doi:10.1007/s00429-014-0977-4 · Cited by 50 · see citing works
Regulation and dysregulation of axon infrastructure by myelinating glia
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The making of a node: a co-production of neurons and glia
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Self-citationNrCAM is a marker for substrate‐selective activation of ADAM10 in Alzheimer's disease
Brummer, T., Müller, S. A., Pan-Montojo, F. J., Yoshida, F., Fellgiebel, A., Tomita, T., Endres, K., & Lichtenthaler, S. F. (2019) · EMBO Molecular Medicine · doi:10.15252/emmm.201809695 · Cited by 48 · see citing works
Caspr and Caspr2 Are Required for Both Radial and Longitudinal Organization of Myelinated Axons
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Excitable Domains of Myelinated Nerves
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Self-citationColombelli, C., Palmisano, M., Eshed‐Eisenbach, Y., Zambroni, D., Pavoni, E., Ferri, C., Saccucci, S., Nicole, S., Soininen, R., McKee, K. K., et al. (2015) · The Journal of Cell Biology · doi:10.1083/jcb.201403111 · Cited by 42 · see citing works
Self-citationAxonal Spectrins: Nanoscale Organization, Functional Domains and Spectrinopathies
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NuMA1 promotes axon initial segment assembly through inhibition of endocytosis
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Glial βII Spectrin Contributes to Paranode Formation and Maintenance
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Self-citationSubcellular Patterning: Axonal Domains with Specialized Structure and Function
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Self-citationReassembly of Excitable Domains after CNS Axon Regeneration
Marin, M. A., de Lima, S., Gilbert, H.-Y., Giger, R. J., Benowitz, L. I., & Rasband, M. N. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.1747-16.2016 · Cited by 33 · see citing works
Self-citationFunctional and structural properties of ion channels at the nerve terminal depends on compact myelin
Berret, E., Kim, S. E., Lee, S. Y., Kushmerick, C., & Kim, J. H. (2016) · The Journal of Physiology · doi:10.1113/jp272205 · Cited by 32 · see citing works
Saifetiarova, J., Taylor, A. M., & Bhat, M. A. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.2661-16.2017 · Cited by 31 · see citing works
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Submembranous cytoskeletons stabilize nodes of Ranvier
Susuki, K., Otani, Y., & Rasband, M. N. (2016) · Experimental Neurology · doi:10.1016/j.expneurol.2015.11.012 · Cited by 31 · see citing works
Self-citationMurcia‐Belmonte, V., Esteban, P. F., Hernández, J. M., Gruart, A., Luján, R., Delgado-Garcia, J. M., & de Castro, F. (2015) · Brain Structure and Function · doi:10.1007/s00429-015-1016-9 · Cited by 30 · see citing works
Neuron–Oligodendrocyte Communication in Myelination of Cortical GABAergic Cells
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The clustering of voltage‐gated sodium channels in various excitable membranes
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Self-citationNodal β spectrins are required to maintain Na+ channel clustering and axon integrity
Liu, C., Stevens, S. R., Teliska, L. H., Stankewich, M. C., Mohler, P. J., Hund, T. J., & Rasband, M. N. (2020) · eLife · doi:10.7554/elife.52378 · Cited by 26 · see citing works
Self-citationHapln2 in Neurological Diseases and Its Potential as Therapeutic Target
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β spectrin-dependent and domain specific mechanisms for Na+ channel clustering
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Self-citationThe Ins and Outs of Polarized Axonal Domains
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Self-citationAssembly and Function of the Juxtaparanodal Kv1 Complex in Health and Disease
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A view of the genetic and proteomic profile of extracellular matrix molecules in aging and stroke
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LGI3/2–ADAM23 interactions cluster Kv1 channels in myelinated axons to regulate refractory period
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Chronic peripheral nerve compression disrupts paranodal axoglial junctions
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Self-citationFormation and disruption of functional domains in myelinated CNS axons
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Activity-dependent regulation of excitable axonal domains
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Glial M6B stabilizes the axonal membrane at peripheral nodes of Ranvier
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Two distinct types of nodes of Ranvier support auditory nerve function in the mouse cochlea
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- Authors
- 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.
- Affiliations
- Baylor College of Medicine (US)
- University of California, San Francisco (US)
- Leibniz Institute for Neurobiology (DE)
- University Hospital Zurich (CH)
- Okayama University (JP)
- Weizmann Institute of Science (IL)
- Corresponding author
- Rasband, Matthew N.
- ORCID
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2013-05
- Volume
- 78
- Issue
- 3
- Pages
- 469-482
- ISSN
- 0896-6273 (ISSN-L)
- PMC
- PMC3756512
- OpenAlex
- W2056897764
- Cited by
- 186
- References
- 54
- Citations by year
- 2026: 8 · 2025: 16 · 2024: 13 · 2023: 13 · 2022: 8 · 2021: 14 · 2020: 17 · 2019: 14 · 2018: 14 · 2017: 11 · 2016: 12 · 2015: 21 · 2014: 17 · 2013: 8
- FWCI
- 8.66
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- Zurich Open Repository and Archive (University of Zurich) (acceptedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Zurich Open Repository and Archive (University of Zurich) (submittedVersion)
- Zurich Open Repository and Archive (University of Zurich)
- Funders
- Dr. Miriam and Sheldon G. Adelson Medical Research Foundation
- Ministry of Education, Culture, Sports, Science and Technology (24107516)
- United States-Israel Binational Science Foundation
- National Institutes of Health (NS044916, NS069688, NS50220)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion channel regulation and function
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion Transport and Channel Regulation
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Hereditary Neurological Disorders
- Keywords
- nodes of Ranvier, myelinated axons, action potential propagation, extracellular matrix, proteoglycans, adhesion molecules, central nervous system myelination, motor impairment
- MeSH terms
- Action Potentials, Animals, Axons, Central Nervous System, Cytoskeleton, Extracellular Matrix, Myelin Sheath, Proteoglycans, Ranvier's Nodes, Sodium Channels, Cell Adhesion Molecules, Mice, Knockout, Mice
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