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Published 30 January 2006. doi:10.1083/jcb.200506136
The Rockefeller University Press, 0021-9525 $8.00
JCB, Volume 172, Number 3, 453-467
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Article

Localized recruitment and activation of RhoA underlies dendritic spine morphology in a glutamate receptor–dependent manner



Vanessa Schubert1, Jorge Santos Da Silva1, and Carlos G. Dotti1,2,3

1 Cavalieri Ottolenghi Scientific Institute, Universita Degli Studi di Torino, Azienda Ospedaliera San Luigi Gonzaga, Regione Gonzole 10, 10043 Orbassano (Torino), Italy
2 Department of Human Genetics, Catholic University of Leuven, 3000 Leuven, Belgium
3 Flanders Interuniversity Institute of Biotechnology, 3000 Leuven, Belgium

Actin is the major cytoskeletal source of dendritic spines, which are highly specialized protuberances on the neuronal surface where excitatory synaptic transmission occurs (Harris, K.M., and S.B. Kater. 1994. Annu. Rev. Neurosci. 17:341–371; Yuste, R., and D.W. Tank. 1996. Neuron. 16:701–716). Stimulation of excitatory synapses induces changes in spine shape via localized rearrangements of the actin cytoskeleton (Matus, A. 2000. Science. 290:754–758; Nagerl, U.V., N. Eberhorn, S.B. Cambridge, and T. Bonhoeffer. 2004. Neuron. 44:759–767). However, what remains elusive are the precise molecular mechanisms by which different neurotransmitter receptors forward information to the underlying actin cytoskeleton. We show that in cultured hippocampal neurons as well as in whole brain synaptosomal fractions, RhoA associates with glutamate receptors (GluRs) at the spine plasma membrane. Activation of ionotropic GluRs leads to the detachment of RhoA from these receptors and its recruitment to metabotropic GluRs. Concomitantly, this triggers a local reduction of RhoA activity, which, in turn, inactivates downstream kinase RhoA-specific kinase, resulting in restricted actin instability and dendritic spine collapse. These data provide a direct mechanistic link between neurotransmitter receptor activity and the changes in spine shape that are thought to play a crucial role in synaptic strength.

J.S. Da Silva's present address is Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724.

Abbreviations used in this paper: Dia1, Diaphanous 1; F-actin, filamentous actin; GDP, guanosine diphosphate; GluR, glutamate receptor; iGluR, iono-tropic GluR; mGluR, metabotropic GluR; NMDA, N-methyl-D-asparate; NMDAR, NMDA receptor; PIIa, profilinIIa; PSD, postsynaptic density; ROCK, RhoA-specific kinase; ST, synaptotagmin.


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