Rapid induction of dendritic spine morphogenesis by trans-synaptic ephrinB-EphB receptor activation of the Rho-GEF kalirin

Peter Penzes; Alexander Beeser; Jonathan Chernoff; Martin R. Schiller; Betty A. Eipper; Richard E. Mains; Richard L. Huganir

doi:10.1016/S0896-6273(02)01168-6

Rapid induction of dendritic spine morphogenesis by trans-synaptic ephrinB-EphB receptor activation of the Rho-GEF kalirin

Peter Penzes, Alexander Beeser, Jonathan Chernoff, Martin R. Schiller, Betty A. Eipper, Richard E. Mains, Richard L. Huganir^*

^*Corresponding author for this work

Neuroscience

Research output: Contribution to journal › Article › peer-review

396 Scopus citations

Abstract

The morphogenesis of dendritic spines, the major sites of excitatory synaptic transmission in the brain, is important in synaptic development and plasticity. We have identified an ephrinB-EphB receptor trans-synaptic signaling pathway which regulates the morphogenesis and maturation of dendritic spines in hippocampal neurons. Activation of the EphB receptor induces translocation of the Rho-GEF kalirin to synapses and activation of Rac1 and its effector PAK. Overexpression of dominant-negative EphB receptor, catalytically inactive kalirin, or dominant-negative Rac1, or inhibition of PAK eliminates ephrin-induced spine development. This novel signal transduction pathway may be critical for the regulation of the actin cytoskeleton controlling spine morphogenesis during development and plasticity.

Original language	English (US)
Pages (from-to)	263-274
Number of pages	12
Journal	Neuron
Volume	37
Issue number	2
DOIs	https://doi.org/10.1016/S0896-6273(02)01168-6
State	Published - Jan 23 2003

Funding

We would like to thank Chun He and Lin Ding for the neuronal cultures, Drs. Rita Sattler and Gavin Rumbaugh for help with cultures and microscopy, and Dr. Gareth Thomas for critically reading the manuscript. We are grateful for the reagents provided by Drs. Michael Greenberg, Matthew Dalva, and Jeanine Zieg (Harvard Medical School, Cambridge, MA), and Anthony Pawson (University of Toronto, Toronto, ON, Canada). This work was supported by The Howard Hughes Medical Institute, MH 61873, and DA 00266.

ASJC Scopus subject areas

General Neuroscience

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title = "Rapid induction of dendritic spine morphogenesis by trans-synaptic ephrinB-EphB receptor activation of the Rho-GEF kalirin",

abstract = "The morphogenesis of dendritic spines, the major sites of excitatory synaptic transmission in the brain, is important in synaptic development and plasticity. We have identified an ephrinB-EphB receptor trans-synaptic signaling pathway which regulates the morphogenesis and maturation of dendritic spines in hippocampal neurons. Activation of the EphB receptor induces translocation of the Rho-GEF kalirin to synapses and activation of Rac1 and its effector PAK. Overexpression of dominant-negative EphB receptor, catalytically inactive kalirin, or dominant-negative Rac1, or inhibition of PAK eliminates ephrin-induced spine development. This novel signal transduction pathway may be critical for the regulation of the actin cytoskeleton controlling spine morphogenesis during development and plasticity.",

author = "Peter Penzes and Alexander Beeser and Jonathan Chernoff and Schiller, {Martin R.} and Eipper, {Betty A.} and Mains, {Richard E.} and Huganir, {Richard L.}",

note = "Funding Information: We would like to thank Chun He and Lin Ding for the neuronal cultures, Drs. Rita Sattler and Gavin Rumbaugh for help with cultures and microscopy, and Dr. Gareth Thomas for critically reading the manuscript. We are grateful for the reagents provided by Drs. Michael Greenberg, Matthew Dalva, and Jeanine Zieg (Harvard Medical School, Cambridge, MA), and Anthony Pawson (University of Toronto, Toronto, ON, Canada). This work was supported by The Howard Hughes Medical Institute, MH 61873, and DA 00266.",

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doi = "10.1016/S0896-6273(02)01168-6",

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T1 - Rapid induction of dendritic spine morphogenesis by trans-synaptic ephrinB-EphB receptor activation of the Rho-GEF kalirin

AU - Penzes, Peter

AU - Beeser, Alexander

AU - Chernoff, Jonathan

AU - Schiller, Martin R.

AU - Eipper, Betty A.

AU - Mains, Richard E.

AU - Huganir, Richard L.

N1 - Funding Information: We would like to thank Chun He and Lin Ding for the neuronal cultures, Drs. Rita Sattler and Gavin Rumbaugh for help with cultures and microscopy, and Dr. Gareth Thomas for critically reading the manuscript. We are grateful for the reagents provided by Drs. Michael Greenberg, Matthew Dalva, and Jeanine Zieg (Harvard Medical School, Cambridge, MA), and Anthony Pawson (University of Toronto, Toronto, ON, Canada). This work was supported by The Howard Hughes Medical Institute, MH 61873, and DA 00266.

PY - 2003/1/23

Y1 - 2003/1/23

N2 - The morphogenesis of dendritic spines, the major sites of excitatory synaptic transmission in the brain, is important in synaptic development and plasticity. We have identified an ephrinB-EphB receptor trans-synaptic signaling pathway which regulates the morphogenesis and maturation of dendritic spines in hippocampal neurons. Activation of the EphB receptor induces translocation of the Rho-GEF kalirin to synapses and activation of Rac1 and its effector PAK. Overexpression of dominant-negative EphB receptor, catalytically inactive kalirin, or dominant-negative Rac1, or inhibition of PAK eliminates ephrin-induced spine development. This novel signal transduction pathway may be critical for the regulation of the actin cytoskeleton controlling spine morphogenesis during development and plasticity.

AB - The morphogenesis of dendritic spines, the major sites of excitatory synaptic transmission in the brain, is important in synaptic development and plasticity. We have identified an ephrinB-EphB receptor trans-synaptic signaling pathway which regulates the morphogenesis and maturation of dendritic spines in hippocampal neurons. Activation of the EphB receptor induces translocation of the Rho-GEF kalirin to synapses and activation of Rac1 and its effector PAK. Overexpression of dominant-negative EphB receptor, catalytically inactive kalirin, or dominant-negative Rac1, or inhibition of PAK eliminates ephrin-induced spine development. This novel signal transduction pathway may be critical for the regulation of the actin cytoskeleton controlling spine morphogenesis during development and plasticity.

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Rapid induction of dendritic spine morphogenesis by trans-synaptic ephrinB-EphB receptor activation of the Rho-GEF kalirin

Abstract

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