Proneural transcription factors regulate different steps of cortical neuron migration through Rnd-mediated inhibition of RhoA signalling

Emilie Pacary; Julian Heng; Roberta Azzarelli; Philippe Riou; Diogo Castro; Melanie Lebel-Potter; Carlos Parras; Donald M. Bell; Anne J. Ridley; Madeline Parsons; Francois Guillemot

doi:10.1016/j.neuron.2011.02.018

Proneural transcription factors regulate different steps of cortical neuron migration through Rnd-mediated inhibition of RhoA signalling

Emilie Pacary, Julian Heng, Roberta Azzarelli, Philippe Riou, Diogo Castro, Melanie Lebel-Potter, Carlos Parras, Donald M. Bell, Anne J. Ridley, Madeline Parsons, Francois Guillemot

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

172 Citations (Scopus)

Abstract

Little is known of the intracellular machinery that controls the motility of newborn neurons. We have previously shown that this proneural protein Neurog2 promotes the migration of nascent cortical neurons by inducing the expression of the atypical Rho GTPase Rnd2. Here, we show that another proneural factor, Ascl1, promotes neuronal migration in the cortex through direct regulation of a second Rnd family member, Rnd3. Both Rnd2 and Rnd3 promote neuronal migration by inhibiting RhoA signaling, but they control distinct steps of the migratory process, multipolar to bipolar transition in the intermediate zone and locomotion in the cortical plate, respectively. Interestingly, these divergent functions directly result from the distinct subcellular distributions of the two Rnd proteins. Because Rnd proteins also regulate progenitor divisions and neurite outgrowth, we propose that proneural factors, through spatiotemporal regulation of Rnd proteins, integrate the process of neuronal migration with other events in the neurogenic program.

Original language	English
Pages (from-to)	1069-1084
Number of pages	16
Journal	Neuron
Volume	69
Issue number	6
DOIs	https://doi.org/10.1016/j.neuron.2011.02.018
Publication status	Published - 24 Mar 2011

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title = "Proneural transcription factors regulate different steps of cortical neuron migration through Rnd-mediated inhibition of RhoA signalling",

abstract = "Little is known of the intracellular machinery that controls the motility of newborn neurons. We have previously shown that this proneural protein Neurog2 promotes the migration of nascent cortical neurons by inducing the expression of the atypical Rho GTPase Rnd2. Here, we show that another proneural factor, Ascl1, promotes neuronal migration in the cortex through direct regulation of a second Rnd family member, Rnd3. Both Rnd2 and Rnd3 promote neuronal migration by inhibiting RhoA signaling, but they control distinct steps of the migratory process, multipolar to bipolar transition in the intermediate zone and locomotion in the cortical plate, respectively. Interestingly, these divergent functions directly result from the distinct subcellular distributions of the two Rnd proteins. Because Rnd proteins also regulate progenitor divisions and neurite outgrowth, we propose that proneural factors, through spatiotemporal regulation of Rnd proteins, integrate the process of neuronal migration with other events in the neurogenic program.",

author = "Emilie Pacary and Julian Heng and Roberta Azzarelli and Philippe Riou and Diogo Castro and Melanie Lebel-Potter and Carlos Parras and Bell, {Donald M.} and Ridley, {Anne J.} and Madeline Parsons and Francois Guillemot",

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T1 - Proneural transcription factors regulate different steps of cortical neuron migration through Rnd-mediated inhibition of RhoA signalling

AU - Pacary, Emilie

AU - Heng, Julian

AU - Azzarelli, Roberta

AU - Riou, Philippe

AU - Castro, Diogo

AU - Lebel-Potter, Melanie

AU - Parras, Carlos

AU - Bell, Donald M.

AU - Ridley, Anne J.

AU - Parsons, Madeline

AU - Guillemot, Francois

PY - 2011/3/24

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N2 - Little is known of the intracellular machinery that controls the motility of newborn neurons. We have previously shown that this proneural protein Neurog2 promotes the migration of nascent cortical neurons by inducing the expression of the atypical Rho GTPase Rnd2. Here, we show that another proneural factor, Ascl1, promotes neuronal migration in the cortex through direct regulation of a second Rnd family member, Rnd3. Both Rnd2 and Rnd3 promote neuronal migration by inhibiting RhoA signaling, but they control distinct steps of the migratory process, multipolar to bipolar transition in the intermediate zone and locomotion in the cortical plate, respectively. Interestingly, these divergent functions directly result from the distinct subcellular distributions of the two Rnd proteins. Because Rnd proteins also regulate progenitor divisions and neurite outgrowth, we propose that proneural factors, through spatiotemporal regulation of Rnd proteins, integrate the process of neuronal migration with other events in the neurogenic program.

AB - Little is known of the intracellular machinery that controls the motility of newborn neurons. We have previously shown that this proneural protein Neurog2 promotes the migration of nascent cortical neurons by inducing the expression of the atypical Rho GTPase Rnd2. Here, we show that another proneural factor, Ascl1, promotes neuronal migration in the cortex through direct regulation of a second Rnd family member, Rnd3. Both Rnd2 and Rnd3 promote neuronal migration by inhibiting RhoA signaling, but they control distinct steps of the migratory process, multipolar to bipolar transition in the intermediate zone and locomotion in the cortical plate, respectively. Interestingly, these divergent functions directly result from the distinct subcellular distributions of the two Rnd proteins. Because Rnd proteins also regulate progenitor divisions and neurite outgrowth, we propose that proneural factors, through spatiotemporal regulation of Rnd proteins, integrate the process of neuronal migration with other events in the neurogenic program.

U2 - 10.1016/j.neuron.2011.02.018

DO - 10.1016/j.neuron.2011.02.018

M3 - Article

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SP - 1069

EP - 1084

JO - Neuron

JF - Neuron

IS - 6

ER -

Proneural transcription factors regulate different steps of cortical neuron migration through Rnd-mediated inhibition of RhoA signalling

Abstract

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