Mechanosensing is critical for axon growth in the developing brain
Open accessAbstract
During nervous system development, neurons extend axons along well-defined pathways. The current understanding of axon pathfinding is based mainly on chemical signaling. However, growing neurons interact not only chemically but also mechanically with their environment. Here we identify mechanical signals as important regulators of axon pathfinding. In vitro, substrate stiffness determined growth patterns of Xenopus retinal ganglion cell axons. In vivo atomic force microscopy revealed a noticeable pattern of stiffness gradients in the embryonic brain. Retinal ganglion cell axons grew toward softer tissue, which was reproduced in vitro in the absence of chemical gradients. To test the importance of mechanical signals for axon growth in vivo, we altered brain stiffness, blocked mechanotransduction pharmacologically and knocked down the mechanosensitive ion channel piezo1. All treatments resulted in aberrant axonal growth and pathfinding errors, suggesting that local tissue stiffness, read out by mechanosensitive ion channels, is critically involved in instructing neuronal growth in vivo.
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The gene PIEZO1 is involved in axon pathfinding and harbors a high-scoring nonsynonymous mutation.
“Axon pathfinding is another process suggested to have been targeted by human-specific changes; the gene PIEZO1 is involved in this process (47) and harbors a high-scoring nonsynonymous mutation.”
From An ancestral recombination graph of human, Neanderthal, and Denisovan genomes (2021) · cites this paper as [47]
PIEZO1 carries a non-synonymous change that is almost fixed in modern humans and is another factor in axon guidance.
“PIEZO1, which carries a non-synonymous change that is almost fixed in modern humans, is another factor in axon guidance100”
From A catalog of single nucleotide changes distinguishing modern humans from archaic hominins (2019) · cites this paper as [100]
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- Authors
- Koser, D. E., Thompson, A. J., Foster, S. K., Dwivedy, A., Pillai, E. K., Sheridan, G. K., Svoboda, H., Viana, M., Costa, L. D. F., Guck, J., Holt, C. E., & Franze, K.
- Affiliations
- University of Cambridge (GB)
- Universidade de São Paulo (BR)
- Corresponding author
- Franze, Kristian
- ORCID
- Venue
- Nature Neuroscience
- Published
- 2016-09-19
- Volume
- 19
- Issue
- 12
- Pages
- 1592-1598
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- PMC
- PMC5531257
- OpenAlex
- W2522174175
- Cited by
- 649
- References
- 62
- Citations by year
- 2026: 53 · 2025: 68 · 2024: 82 · 2023: 58 · 2022: 85 · 2021: 81 · 2020: 76 · 2019: 55 · 2018: 52 · 2017: 36 · 2016: 1
- FWCI
- 26.79
- Type
- journal article
- Language
- en
- Open access
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Apollo (University of Cambridge) (acceptedVersion)
- PubMed Central (acceptedVersion)
- University of Brighton Repository (University of Brighton) (submittedVersion, other-oa)
- Repository@Nottingham (University of Nottingham) (submittedVersion)
- Repository@Nottingham (University of Nottingham) (submittedVersion, cc-by)
- MPG.PuRe (Max Planck Society) (submittedVersion)
- Apollo
- Funders
- Alexander von Humboldt-Stiftung
- Winston Churchill Foundation of the United States
- Wellcome Trust (322817, 085314/Z/08/Z, WT085314)
- Fundação de Amparo à Pesquisa do Estado de São Paulo (11/50761-2)
- Conselho Nacional de Desenvolvimento Científico e Tecnológico (307333/2013‐2)
- Studienstiftung des Deutschen Volkes
- National Institutes of Health (11/50761-2)
- University at Buffalo
- Medical Research Council
- Biotechnology and Biological Sciences Research Council (BB/M021394/1)
- National Institute of Child Health and Human Development
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (R21HD080585)
- FP7 Ideas: European Research Council (322817)
- 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
- mechanosensing, axon guidance, tissue stiffness, mechanotransduction, Piezo1, retinal ganglion cells, neuronal growth, embryonic brain development, stiffness gradient, Xenopus
- MeSH terms
- Animals, Axons, Brain, Retina, Retinal Ganglion Cells, Visual Pathways, Xenopus laevis, Zebrafish, Mechanotransduction, Cellular, Neurogenesis
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