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Title: The membrane periodic skeleton is an actomyosin network that regulates axonal diameter and conduction

Journal Article · · eLife
DOI:https://doi.org/10.7554/eLife.55471· OSTI ID:1607599
 [1];  [2];  [1]; ORCiD logo [3];  [4];  [5];  [1];  [1];  [1]; ORCiD logo [6];  [6];  [7];  [8];  [9];  [10]; ORCiD logo [11]; ORCiD logo [4]; ORCiD logo [1]
  1. Nerve Regeneration Group, Porto, Portugal, i3S- Instituto de Investigação e Inovação em Saúde, Universidade do Porto, Porto, Portugal
  2. Nerve Regeneration Group, Porto, Portugal, i3S- Instituto de Investigação e Inovação em Saúde, Universidade do Porto, Porto, Portugal, ICBAS- Instituto de Ciências Biomédicas Abel Salazar, Universidade do Porto, Porto, Portugal
  3. i3S- Instituto de Investigação e Inovação em Saúde, Universidade do Porto, Porto, Portugal, ICBAS- Instituto de Ciências Biomédicas Abel Salazar, Universidade do Porto, Porto, Portugal, Neuroengineering and Computational Neuroscience Group, INEB- Instituto de Engenharia Biomédica, Universidade do Porto, Porto, Portugal
  4. i3S- Instituto de Investigação e Inovação em Saúde, Universidade do Porto, Porto, Portugal, Neuroengineering and Computational Neuroscience Group, INEB- Instituto de Engenharia Biomédica, Universidade do Porto, Porto, Portugal
  5. Nerve Regeneration Group, Porto, Portugal, i3S- Instituto de Investigação e Inovação em Saúde, Universidade do Porto, Porto, Portugal, ICBAS- Instituto de Ciências Biomédicas Abel Salazar, Universidade do Porto, Porto, Portugal, Neuroengineering and Computational Neuroscience Group, INEB- Instituto de Engenharia Biomédica, Universidade do Porto, Porto, Portugal
  6. Department of Orthopaedic Surgery, Johns Hopkins University School of Medicine, The Solomon H. Snyder Department of Neuroscience, Johns Hopkins University School of Medicine, Baltimore, United States
  7. i3S- Instituto de Investigação e Inovação em Saúde, Universidade do Porto, Porto, Portugal, Chromosome Instability and Dynamics Group, Porto, Portugal
  8. i3S- Instituto de Investigação e Inovação em Saúde, Universidade do Porto, Porto, Portugal, Advanced Light Microscopy, IBMC- Instituto de Biologia Molecular e Celular, Universidade do Porto, Porto, Portugal
  9. Stowers Institute for Medical Research, Kansas City, United States
  10. International Iberian Nanotechnology Laboratory, Braga, Portugal
  11. Advanced Light Microscopy Facility, EMBL, Heidelberg, Germany
+ Show Author Affiliations

Neurons have a membrane periodic skeleton (MPS) composed of actin rings interconnected by spectrin. Here, combining chemical and genetic gain- and loss-of-function assays, we show that in rat hippocampal neurons the MPS is an actomyosin network that controls axonal expansion and contraction. Using super-resolution microscopy, we analyzed the localization of axonal non-muscle myosin II (NMII). We show that active NMII light chains are colocalized with actin rings and organized in a circular periodic manner throughout the axon shaft. In contrast, NMII heavy chains are mostly positioned along the longitudinal axonal axis, being able to crosslink adjacent rings. NMII filaments can play contractile or scaffolding roles determined by their position relative to actin rings and activation state. We also show that MPS destabilization through NMII inactivation affects axonal electrophysiology, increasing action potential conduction velocity. In summary, our findings open new perspectives on axon diameter regulation, with important implications in neuronal biology.

Sponsoring Organization:
USDOE Office of Nuclear Energy (NE), Nuclear Fuel Cycle and Supply Chain
Grant/Contract Number:
SFRH/BPD/114912/2016; SFRH/BD/136760/2018; PD/BD/135491/2018
OSTI ID:
1607599
Alternate ID(s):
OSTI ID: 1607600
Journal Information:
eLife, Journal Name: eLife Vol. 9; ISSN 2050-084X
Publisher:
eLife Sciences Publications, Ltd.Copyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 33 works
Citation information provided by
Web of Science

References (29)

The Regulation of Axon Diameter: From Axonal Circumferential Contractility to Activity-Dependent Axon Swelling journal September 2018
Actin/Myosin-V- and Activity-Dependent Inter-synaptic Vesicle Exchange in Central Neurons journal February 2017
Axons break in animals lacking β-spectrin journal January 2007
Sequential Treatment of SH-SY5Y Cells with Retinoic Acid and Brain-Derived Neurotrophic Factor Gives Rise to Fully Differentiated, Neurotrophic Factor-Dependent, Human Neuron-Like Cells journal September 2000
Determinants of conduction velocity in myelinated nerve fibers journal March 1980
Dissecting Temporal and Spatial Control of Cytokinesis with a Myosin II Inhibitor journal March 2003
Signaling by Neuronal Swelling journal January 2011
Coupled circumferential and axial tension driven by actin and myosin influences in vivo axon diameter journal October 2017
Localized Myosin II Activity Regulates Assembly and Plasticity of the Axon Initial Segment journal February 2018
A note on conduction velocity journal July 1954
Nonmuscle Myosin II Isoforms Coassemble in Living Cells journal May 2014
Calyculin A and okadaic acid: Inhibitors of protein phosphatase activity journal March 1989
Irregular geometries in normal unmyelinated axons: A 3D serial EM analysis journal December 1990
Myosin II has distinct functions in PNS and CNS myelin sheath formation journal September 2008
Interfacing Microfluidics with Microelectrode Arrays for Studying Neuronal Communication and Axonal Signal Propagation journal January 2018
Culturing hippocampal neurons journal December 2006
Myosin phosphatase target subunit: Many roles in cell function journal April 2008
The Physiological Molecular Shape of Spectrin: A Compact Supercoil Resembling a Chinese Finger Trap journal June 2015
Characterization of Three Full-length Human Nonmuscle Myosin II Paralogs journal September 2013
Actin, Spectrin, and Associated Proteins Form a Periodic Cytoskeletal Structure in Axons journal December 2012
Subdiffraction-Resolution Fluorescence Imaging with Conventional Fluorescent Probes journal August 2008
Ultrastructure of the axonal periodic scaffold reveals a braid-like organization of actin rings journal December 2019
Myosin IIA Heavy Chain Phosphorylation Mediates Adhesion Maturation and Protrusion in Three Dimensions journal January 2017
Fluorescence nanoscopy by ground-state depletion and single-molecule return journal September 2008
A major role for the Rho-associated coiled coil forming protein kinase in G-protein-mediated Ca 2+ sensitization through inhibition of myosin phosphatase in rabbit trachea journal October 1999
A Myosin V Inhibitor Based on Privileged Chemical Scaffolds journal September 2010
Non-muscle myosin II takes centre stage in cell adhesion and migration journal November 2009
µSpikeHunter: An advanced computational tool for the analysis of neuronal communication and action potential propagation in microfluidic platforms journal April 2019
The Actin-Binding Protein α-Adducin Is Required for Maintaining Axon Diameter journal April 2016

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