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Cited by 118Axon Guidance and Neuronal SignalingCellular Mechanics and InteractionsNeurogenesis and neuroplasticity mechanisms

An Integrated Cytoskeletal Model of Neurite Outgrowth

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Miller, Kyle E., Suter, Daniel M.·2018·Frontiers in Cellular Neuroscience
DOI 10.3389/fncel.2018.00447PMC PMC6275320
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Abstract

Understanding neurite outgrowth is important because it underlies the wiring of the nervous system during development and regeneration following trauma and disease. Despite a significant body of research, the underlying cytoskeletal and mechanical mechanisms of growth and guidance are still not fully understood. Here, we bring together quantitative data to develop an integrated mechanical model of axonal elongation. The strength of this approach is that by focusing on forces rather than individual processes in a quantitative framework, the relative contributions of different processes to neurite growth can be impartially considered. We begin this review by discussing the structural organization of neurons focusing on the actin and microtubule (MT) cytoskeletons. Then, recent studies on the biophysics of growth cones and axons are covered to develop a more integrated model of neurite growth. With this foundation, some of the “controversial” findings in this field are discussed. A central idea that develops is that neurons appear to be active fluids, which generate strong contractile forces in the growth cone and weaker contractile forces along the axon. As a result of subcellular gradients in forces and material properties, actin flows rapidly rearwards in the growth cone periphery and MTs flow forward in bulk along the axon. From this a picture emerges that a growth cone is much like a migrating cell coupled to the cell body by the axon. Forces and cytoskeletal dynamics in the growth cone control its advance, whereas the axon acts to restrain and support growth cone motility. The major difference of the present integrated model to previous models is that the growth cone moves forward as a coherent structure and pulls the adjacent axon along, instead of advancing by the assembly of MTs at the tip of the axon. With this perspective, new approaches for promoting neuronal regeneration are discussed.

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  • Similar cytoskeletal processes are instrumental to neurite outgrowth, which depends on mechanical forces by opposing migration of actin and microtubule cytoskeletal components.

    “Similar cytoskeletal processes are instrumental to neurite outgrowth, which depends on the generation of mechanical forces by the opposing migration of actin and microtubule cytoskeletal components [107].”

    From Rlip76: An Unexplored Player in Neurodegeneration and Alzheimer’s Disease? (2022) · cites this paper as [107]

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Authors
Miller, K. E., & Suter, D. M.
Affiliations
  • Michigan State University (US)
  • Purdue University West Lafayette (US)
Corresponding author
  • Miller, Kyle E.
  • Suter, Daniel M.
ORCID
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Frontiers in Cellular Neuroscience
Publisher
Frontiers Media SA
Published
2018-11-26
Volume
12
Pages
447-447
ISSN
1662-5102 (ISSN-L)
DOI
10.3389/fncel.2018.00447
PMC
PMC6275320
OpenAlex
W2902217021
Cited by
118
References
3
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en
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Locations
  • Frontiers in Cellular Neuroscience (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
Foundation for the National Institutes of Health
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Axon Guidance and Neuronal Signaling
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular Mechanics and Interactions
  • Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
Keywords
neurite outgrowth, axon elongation, growth cones, actin cytoskeleton, microtubules, cytoskeleton mechanics, contractile force, growth cone motility, neuronal regeneration, neuronal development, cell migration

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

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