Spatial Distribution of the Full-length Members of the Grg Family During Embryonic Neurogenesis Reveals a "Grg-mediated Repression Map" in the Mouse Telencephalon

Overview

Journal PLoS One

Specialties General Medicine
Science

Date 2018 Dec 21

PMID 30571765

Citations 2

Authors

Charalampos Chrysovalantis Chytoudis-Peroudis

Nikistratos Siskos

Konstantinos Kalyviotis

Ioannis Fysekis

Petros Ypsilantis

Constantinos Simopoulos

George Skavdis

Maria E Grigoriou

Affiliations

Soon will be listed here.

Abstract

The full-length members of the Groucho/Transducin-like Enhancer of split gene family, namely Grg1-4, encode nuclear corepressors that act either directly, via interaction with transcription factors, or indirectly by modifying histone acetylation or chromatin structure. In this work we describe a detailed expression analysis of Grg1-4 family members during embryonic neurogenesis in the developing murine telencephalon. Grg1-4 presented a unique, complex yet overlapping expression pattern; Grg1 and Grg3 were mainly detected in the proliferative zones of the telencephalon, Grg2 mainly in the subpallium and finally, Grg4 mainly in the subpallial post mitotic neurons. In addition, comparative analysis of the expression of Grg1-4 revealed that, at these stages, distinct telencephalic progenitor domains or structures are characterized by the presence of different combinations of Grg repressors, thus forming a "Grg-mediated repression map".

Citing Articles

Characterization of the Abracl-Expressing Cell Populations in the Embryonic Mammalian Telencephalon.

Troumpoukis D, Vasileiou A, Siskos N, Stylianopoulou E, Ypsilantis P, Skavdis G Biomolecules. 2023; 13(9).

PMID: 37759737 PMC: 10527439. DOI: 10.3390/biom13091337.

Roles of transducin-like enhancer of split (TLE) family proteins in tumorigenesis and immune regulation.

Yu G, Chen Y, Hu Y, Zhou Y, Ding X, Zhou X Front Cell Dev Biol. 2022; 10:1010639.

PMID: 36438567 PMC: 9692235. DOI: 10.3389/fcell.2022.1010639.

References

Zhao Y, Marin O, Hermesz E, Powell A, Flames N, Palkovits M . The LIM-homeobox gene Lhx8 is required for the development of many cholinergic neurons in the mouse forebrain. Proc Natl Acad Sci U S A. 2003; 100(15):9005-10. PMC: 166428. DOI: 10.1073/pnas.1537759100. View

Wang D, Kriegstein A . Defining the role of GABA in cortical development. J Physiol. 2009; 587(Pt 9):1873-9. PMC: 2689328. DOI: 10.1113/jphysiol.2008.167635. View

Agarwal M, Kumar P, Mathew S . The Groucho/Transducin-like enhancer of split protein family in animal development. IUBMB Life. 2015; 67(7):472-81. PMC: 7015701. DOI: 10.1002/iub.1395. View

Fragkouli A, Verhey van Wijk N, Lopes R, Kessaris N, Pachnis V . LIM homeodomain transcription factor-dependent specification of bipotential MGE progenitors into cholinergic and GABAergic striatal interneurons. Development. 2009; 136(22):3841-51. PMC: 2766344. DOI: 10.1242/dev.038083. View

Patel S, Bhumbra S, Paknikar R, Dressler G . Epigenetic mechanisms of Groucho/Grg/TLE mediated transcriptional repression. Mol Cell. 2011; 45(2):185-95. PMC: 3268830. DOI: 10.1016/j.molcel.2011.11.007. View

Sekiya T, Zaret K . Repression by Groucho/TLE/Grg proteins: genomic site recruitment generates compacted chromatin in vitro and impairs activator binding in vivo. Mol Cell. 2007; 28(2):291-303. PMC: 2083644. DOI: 10.1016/j.molcel.2007.10.002. View

Grbavec D, Lo R, Liu Y, Stifani S . Transducin-like Enhancer of split 2, a mammalian homologue of Drosophila Groucho, acts as a transcriptional repressor, interacts with Hairy/Enhancer of split proteins, and is expressed during neuronal development. Eur J Biochem. 1999; 258(2):339-49. DOI: 10.1046/j.1432-1327.1998.2580339.x. View

Bajoghli B . Evolution of the Groucho/Tle gene family: gene organization and duplication events. Dev Genes Evol. 2007; 217(8):613-8. DOI: 10.1007/s00427-007-0167-y. View

Long J, Swan C, Liang W, Cobos I, Potter G, Rubenstein J . Dlx1&2 and Mash1 transcription factors control striatal patterning and differentiation through parallel and overlapping pathways. J Comp Neurol. 2008; 512(4):556-72. PMC: 2761428. DOI: 10.1002/cne.21854. View

10.

Jennings B, Ish-Horowicz D . The Groucho/TLE/Grg family of transcriptional co-repressors. Genome Biol. 2008; 9(1):205. PMC: 2395242. DOI: 10.1186/gb-2008-9-1-205. View

11.

Flandin P, Zhao Y, Vogt D, Jeong J, Long J, Potter G . Lhx6 and Lhx8 coordinately induce neuronal expression of Shh that controls the generation of interneuron progenitors. Neuron. 2011; 70(5):939-50. PMC: 3153409. DOI: 10.1016/j.neuron.2011.04.020. View

12.

Mallo M, Franco del Amo F, Gridley T . Cloning and developmental expression of Grg, a mouse gene related to the groucho transcript of the Drosophila Enhancer of split complex. Mech Dev. 1993; 42(1-2):67-76. DOI: 10.1016/0925-4773(93)90099-j. View

13.

Stylianopoulou E, Skavdis G, Grigoriou M . Zinc-based fixation for high-sensitivity in situ hybridization: a nonradioactive colorimetric method for the detection of rare transcripts on tissue sections. Methods Mol Biol. 2014; 1211:125-38. DOI: 10.1007/978-1-4939-1459-3_11. View

14.

Arce L, Pate K, Waterman M . Groucho binds two conserved regions of LEF-1 for HDAC-dependent repression. BMC Cancer. 2009; 9:159. PMC: 2701438. DOI: 10.1186/1471-2407-9-159. View

15.

Cai Y, Brophy P, Levitan I, Stifani S, Dressler G . Groucho suppresses Pax2 transactivation by inhibition of JNK-mediated phosphorylation. EMBO J. 2003; 22(20):5522-9. PMC: 213790. DOI: 10.1093/emboj/cdg536. View

16.

Flames N, Pla R, Gelman D, Rubenstein J, Puelles L, Marin O . Delineation of multiple subpallial progenitor domains by the combinatorial expression of transcriptional codes. J Neurosci. 2007; 27(36):9682-95. PMC: 4916652. DOI: 10.1523/JNEUROSCI.2750-07.2007. View

17.

Pinto M, Lobe C . Products of the grg (Groucho-related gene) family can dimerize through the amino-terminal Q domain. J Biol Chem. 1996; 271(51):33026-31. DOI: 10.1074/jbc.271.51.33026. View

18.

Reiter F, Wienerroither S, Stark A . Combinatorial function of transcription factors and cofactors. Curr Opin Genet Dev. 2017; 43:73-81. DOI: 10.1016/j.gde.2016.12.007. View

19.

Cinnamon E, Paroush Z . Context-dependent regulation of Groucho/TLE-mediated repression. Curr Opin Genet Dev. 2008; 18(5):435-40. DOI: 10.1016/j.gde.2008.07.010. View

20.

Fedorova E, Zink D . Nuclear architecture and gene regulation. Biochim Biophys Acta. 2008; 1783(11):2174-84. DOI: 10.1016/j.bbamcr.2008.07.018. View