Lpd Depletion Reveals That SRF Specifies Radial Versus Tangential Migration of Pyramidal Neurons

Overview

Journal Nat Cell Biol

Specialty Cell Biology

Date 2011 Jul 26

PMID 21785421

Citations 21

Authors

Elaine M Pinheiro

Zhigang Xie

Amy L Norovich

Marina Vidaki

Li-Huei Tsai

Frank B Gertler

Affiliations

Soon will be listed here.

Abstract

During corticogenesis, pyramidal neurons (∼80% of cortical neurons) arise from the ventricular zone, pass through a multipolar stage to become bipolar and attach to radial glia, and then migrate to their proper position within the cortex. As pyramidal neurons migrate radially, they remain attached to their glial substrate as they pass through the subventricular and intermediate zones, regions rich in tangentially migrating interneurons and axon fibre tracts. We examined the role of lamellipodin (Lpd), a homologue of a key regulator of neuronal migration and polarization in Caenorhabditis elegans, in corticogenesis. Lpd depletion caused bipolar pyramidal neurons to adopt a tangential, rather than radial-glial, migration mode without affecting cell fate. Mechanistically, Lpd depletion reduced the activity of SRF, a transcription factor regulated by changes in the ratio of polymerized to unpolymerized actin. Therefore, Lpd depletion exposes a role for SRF in directing pyramidal neurons to select a radial migration pathway along glia rather than a tangential migration mode.

Citing Articles

F-BAR proteins CIP4 and FBP17 function in cortical neuron radial migration and process outgrowth.

English L, Taylor R, Cameron C, Broker E, Dent E bioRxiv. 2024; .

PMID: 39484544 PMC: 11527352. DOI: 10.1101/2024.10.25.620310.

MKL/SRF and Bcl6 mutual transcriptional repression safeguards the fate and positioning of neocortical progenitor cells mediated by RhoA.

Cossard A, Stam K, Smets A, Jossin Y Sci Adv. 2023; 9(46):eadd0676.

PMID: 37967194 PMC: 10651131. DOI: 10.1126/sciadv.add0676.

Comprehensive characterization of migration profiles of murine cerebral cortical neurons during development using FlashTag labeling.

Yoshinaga S, Shin M, Kitazawa A, Ishii K, Tanuma M, Kasai A iScience. 2021; 24(4):102277.

PMID: 33851097 PMC: 8022222. DOI: 10.1016/j.isci.2021.102277.

MicroRNA-934 is a novel primate-specific small non-coding RNA with neurogenic function during early development.

Prodromidou K, Vlachos I, Gaitanou M, Kouroupi G, Hatzigeorgiou A, Matsas R Elife. 2020; 9.

PMID: 32459171 PMC: 7295570. DOI: 10.7554/eLife.50561.

Brain specific Lamellipodin knockout results in hyperactivity and increased anxiety of mice.

Bodo C, Fernandes C, Krause M Sci Rep. 2017; 7(1):5365.

PMID: 28710397 PMC: 5511208. DOI: 10.1038/s41598-017-05043-3.

References

Xie Z, Moy L, Sanada K, Zhou Y, Buchman J, Tsai L . Cep120 and TACCs control interkinetic nuclear migration and the neural progenitor pool. Neuron. 2007; 56(1):79-93. PMC: 2642594. DOI: 10.1016/j.neuron.2007.08.026. View

Elias L, Wang D, Kriegstein A . Gap junction adhesion is necessary for radial migration in the neocortex. Nature. 2007; 448(7156):901-7. DOI: 10.1038/nature06063. View

Michael M, Vehlow A, Navarro C, Krause M . c-Abl, Lamellipodin, and Ena/VASP proteins cooperate in dorsal ruffling of fibroblasts and axonal morphogenesis. Curr Biol. 2010; 20(9):783-91. PMC: 2946563. DOI: 10.1016/j.cub.2010.03.048. View

Lafuente E, van Puijenbroek A, Krause M, Carman C, Freeman G, Berezovskaya A . RIAM, an Ena/VASP and Profilin ligand, interacts with Rap1-GTP and mediates Rap1-induced adhesion. Dev Cell. 2004; 7(4):585-95. DOI: 10.1016/j.devcel.2004.07.021. View

Marin O, Rubenstein J . Cell migration in the forebrain. Annu Rev Neurosci. 2003; 26:441-83. DOI: 10.1146/annurev.neuro.26.041002.131058. View

Miralles F, Posern G, Zaromytidou A, Treisman R . Actin dynamics control SRF activity by regulation of its coactivator MAL. Cell. 2003; 113(3):329-42. DOI: 10.1016/s0092-8674(03)00278-2. View

Johansen F, Prywes R . Identification of transcriptional activation and inhibitory domains in serum response factor (SRF) by using GAL4-SRF constructs. Mol Cell Biol. 1993; 13(8):4640-7. PMC: 360090. DOI: 10.1128/mcb.13.8.4640-4647.1993. View

Sanchez-Alcaniz J, Haege S, Mueller W, Pla R, Mackay F, Schulz S . Cxcr7 controls neuronal migration by regulating chemokine responsiveness. Neuron. 2011; 69(1):77-90. DOI: 10.1016/j.neuron.2010.12.006. View

Posern G, Treisman R . Actin' together: serum response factor, its cofactors and the link to signal transduction. Trends Cell Biol. 2006; 16(11):588-96. DOI: 10.1016/j.tcb.2006.09.008. View

10.

Adler C, Fetter R, Bargmann C . UNC-6/Netrin induces neuronal asymmetry and defines the site of axon formation. Nat Neurosci. 2006; 9(4):511-8. PMC: 2613020. DOI: 10.1038/nn1666. View

11.

Lyulcheva E, Taylor E, Michael M, Vehlow A, Tan S, Fletcher A . Drosophila pico and its mammalian ortholog lamellipodin activate serum response factor and promote cell proliferation. Dev Cell. 2008; 15(5):680-90. PMC: 2691947. DOI: 10.1016/j.devcel.2008.09.020. View

12.

Quinn C, Pfeil D, Chen E, Stovall E, Harden M, Gavin M . UNC-6/netrin and SLT-1/slit guidance cues orient axon outgrowth mediated by MIG-10/RIAM/lamellipodin. Curr Biol. 2006; 16(9):845-53. DOI: 10.1016/j.cub.2006.03.025. View

13.

MANSER J, Wood W . Mutations affecting embryonic cell migrations in Caenorhabditis elegans. Dev Genet. 1990; 11(1):49-64. DOI: 10.1002/dvg.1020110107. View

14.

Yokota Y, Gashghaei H, Han C, Watson H, Campbell K, Anton E . Radial glial dependent and independent dynamics of interneuronal migration in the developing cerebral cortex. PLoS One. 2007; 2(8):e794. PMC: 1950908. DOI: 10.1371/journal.pone.0000794. View

15.

Fode C, Ma Q, Casarosa S, Ang S, Anderson D, Guillemot F . A role for neural determination genes in specifying the dorsoventral identity of telencephalic neurons. Genes Dev. 2000; 14(1):67-80. PMC: 316337. View

16.

Hand R, Bortone D, Mattar P, Nguyen L, Heng J, Guerrier S . Phosphorylation of Neurogenin2 specifies the migration properties and the dendritic morphology of pyramidal neurons in the neocortex. Neuron. 2005; 48(1):45-62. DOI: 10.1016/j.neuron.2005.08.032. View

17.

Geneste O, Copeland J, Treisman R . LIM kinase and Diaphanous cooperate to regulate serum response factor and actin dynamics. J Cell Biol. 2002; 157(5):831-8. PMC: 2173419. DOI: 10.1083/jcb.200203126. View

18.

Ayala R, Shu T, Tsai L . Trekking across the brain: the journey of neuronal migration. Cell. 2007; 128(1):29-43. DOI: 10.1016/j.cell.2006.12.021. View

19.

Han J, Lim C, Watanabe N, Soriani A, Ratnikov B, Calderwood D . Reconstructing and deconstructing agonist-induced activation of integrin alphaIIbbeta3. Curr Biol. 2006; 16(18):1796-806. DOI: 10.1016/j.cub.2006.08.035. View

20.

Posern G, Sotiropoulos A, Treisman R . Mutant actins demonstrate a role for unpolymerized actin in control of transcription by serum response factor. Mol Biol Cell. 2002; 13(12):4167-78. PMC: 138624. DOI: 10.1091/mbc.02-05-0068. View