Leading-process actomyosin coordinates organelle positioning and adhesion receptor dynamics in radially migrating cerebellar granule neurons
Abstract
During brain development, neurons migrate from germinal zones to their final positions to assemble neural circuits. A unique saltatory cadence involving cyclical organelle movement (e.g., centrosome motility) and leading-process actomyosin enrichment prior to nucleokinesis organizes neuronal migration. While functional evidence suggests that leading-process actomyosin is essential for centrosome motility, the role of the actin-enriched leading process in globally organizing organelle transport or traction forces remains unexplored. Our results show that myosin ii motors and F-actin dynamics are required for Golgi apparatus positioning before nucleokinesis in cerebellar granule neurons (CGNs) migrating along glial fibers. Moreover, we show that primary cilia are motile organelles, localized to the leading-process F-actin-rich domain and immobilized by pharmacological inhibition of myosin ii and F-actin dynamics. Finally, leading process adhesion dynamics are dependent on myosin ii and F-actin. In conclusion, we propose that actomyosin coordinates the overall polarity of migrating CGNs by controlling asymmetric organelle positioning and cell-cell contacts as these cells move along their glial guides.
- Authors:
-
- St. Jude Children's Research Hospital, Memphis, TN (United States). Dept. of Developmental Neurobiology
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
- Publication Date:
- Research Org.:
- Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
- Sponsoring Org.:
- USDOE; Work for Others (WFO); American Lebanese Syrian Associated Charities (ALSAC); National Inst. of Neurological Disorders (NINDS)
- OSTI Identifier:
- 1286758
- Grant/Contract Number:
- AC05-00OR22725; 1-FY12-455; 1R01NS066936
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Neural Development
- Additional Journal Information:
- Journal Volume: 9; Journal Issue: 1; Journal ID: ISSN 1749-8104
- Publisher:
- BioMed Central
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Cerebellar granule neuron
Citation Formats
Trivedi, Niraj, Ramahi, Joseph S., Karakaya, Mahmut, Howell, Danielle, Kerekes, Ryan A., and Solecki, David J. Leading-process actomyosin coordinates organelle positioning and adhesion receptor dynamics in radially migrating cerebellar granule neurons. United States: N. p., 2014.
Web. doi:10.1186/1749-8104-9-26.
Trivedi, Niraj, Ramahi, Joseph S., Karakaya, Mahmut, Howell, Danielle, Kerekes, Ryan A., & Solecki, David J. Leading-process actomyosin coordinates organelle positioning and adhesion receptor dynamics in radially migrating cerebellar granule neurons. United States. https://doi.org/10.1186/1749-8104-9-26
Trivedi, Niraj, Ramahi, Joseph S., Karakaya, Mahmut, Howell, Danielle, Kerekes, Ryan A., and Solecki, David J. Tue .
"Leading-process actomyosin coordinates organelle positioning and adhesion receptor dynamics in radially migrating cerebellar granule neurons". United States. https://doi.org/10.1186/1749-8104-9-26. https://www.osti.gov/servlets/purl/1286758.
@article{osti_1286758,
title = {Leading-process actomyosin coordinates organelle positioning and adhesion receptor dynamics in radially migrating cerebellar granule neurons},
author = {Trivedi, Niraj and Ramahi, Joseph S. and Karakaya, Mahmut and Howell, Danielle and Kerekes, Ryan A. and Solecki, David J.},
abstractNote = {During brain development, neurons migrate from germinal zones to their final positions to assemble neural circuits. A unique saltatory cadence involving cyclical organelle movement (e.g., centrosome motility) and leading-process actomyosin enrichment prior to nucleokinesis organizes neuronal migration. While functional evidence suggests that leading-process actomyosin is essential for centrosome motility, the role of the actin-enriched leading process in globally organizing organelle transport or traction forces remains unexplored. Our results show that myosin ii motors and F-actin dynamics are required for Golgi apparatus positioning before nucleokinesis in cerebellar granule neurons (CGNs) migrating along glial fibers. Moreover, we show that primary cilia are motile organelles, localized to the leading-process F-actin-rich domain and immobilized by pharmacological inhibition of myosin ii and F-actin dynamics. Finally, leading process adhesion dynamics are dependent on myosin ii and F-actin. In conclusion, we propose that actomyosin coordinates the overall polarity of migrating CGNs by controlling asymmetric organelle positioning and cell-cell contacts as these cells move along their glial guides.},
doi = {10.1186/1749-8104-9-26},
journal = {Neural Development},
number = 1,
volume = 9,
place = {United States},
year = {Tue Dec 02 00:00:00 EST 2014},
month = {Tue Dec 02 00:00:00 EST 2014}
}
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Reelin, Rap1 and N-cadherin orient the migration of multipolar neurons in the developing neocortex
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Par6α signaling controls glial-guided neuronal migration
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Plexin-A2 and its ligand, Sema6A, control nucleus-centrosome coupling in migrating granule cells
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Cytoskeletal coordination during neuronal migration
journal, September 2005
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Microtubule-based nuclear movement occurs independently of centrosome positioning in migrating neurons
journal, October 2007
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- Proceedings of the National Academy of Sciences, Vol. 104, Issue 41
SynCAM 1 participates in axo-dendritic contact assembly and shapes neuronal growth cones
journal, April 2010
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Polarization of the Golgi apparatus and the microtubule-organizing center in cultured fibroblasts at the edge of an experimental wound.
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- Proceedings of the National Academy of Sciences, Vol. 79, Issue 8
Polarization of the Golgi apparatus and the microtubule-organizing center within cloned natural killer cells bound to their targets.
journal, December 1983
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- Proceedings of the National Academy of Sciences, Vol. 80, Issue 23
Myosin at the apical pole of ciliated epithelial cells as revealed by a monoclonal antibody.
journal, August 1986
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- Journal of Cell Biology, Vol. 103, Issue 2
Recycling of Golgi-resident Glycosyltransferases through the ER Reveals a Novel Pathway and Provides an Explanation for Nocodazole-induced Golgi Scattering
journal, December 1998
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Lis1 and doublecortin function with dynein to mediate coupling of the nucleus to the centrosome in neuronal migration
journal, June 2004
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Optineurin links myosin VI to the Golgi complex and is involved in Golgi organization and exocytosis
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