Transcriptional control of GABAergic neuronal subtype identity in the thalamus

Neural Development

Alessio Delogu²  Andrew G Lumsden¹  Verena Zyka¹  Katherine Sellers² 

[1] MRC Centre for Developmental Neurobiology, King’s College London, London SE1 1UL, UK;Present address: Department of Neuroscience, Institute of Psychiatry, King’s College London, London SE5 9NU, UK

关键词: Diencephalon;    Neurogenesis;    GABAergic thalamus;    Sox14;    Dlx2;    Helt;   

Others  :  802409
DOI  :  10.1186/1749-8104-9-14

 received in 2014-01-10, accepted in 2014-06-02,  发布年份 2014

【 摘 要 】

Background

The thalamus is often defined as the ‘gateway to consciousness’, a feature that is supported by the specific connectivity and electrophysiological properties of its neurons. Inhibitory GABAergic neurons are required for the dynamic gating of information passing through the thalamus. The high degree of heterogeneity among thalamic GABA neurons suggests that, during embryonic development, alternative differentiation programmes exist to guide the acquisition of inhibitory neuron subtype identity.

Results

Taking advantage of the accessibility of the developing chick embryo, we have used in ovo manipulations of gene expression to test the role of candidate transcription factors in controlling GABAergic neuronal subtype identity in the developing thalamus.

Conclusions

In this study, we describe two alternative differentiation programmes for GABAergic neurogenesis in the thalamus and identify Helt and Dlx2 as key transcription factors that are sufficient to direct neuronal progenitors along a specific differentiation pathway at the expense of alternative lineage choices. Furthermore, we identify Calb2, a gene encoding for the GABA subtype marker calretinin as a target of the transcription factor Sox14. This work is a step forward in our understanding of how GABA neuron diversity in the thalamus is achieved during development and will help future investigation of the molecular mechanisms that lead up to the acquisition of different synaptic targets and electrophysiological features of mature thalamic inhibitory neurons.

【 授权许可】

   
2014 Sellers et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

【 参考文献 】

• [1]Steriade M: The corticothalamic system in sleep. Front Biosci 2003, 8:d878-d899.
• [2]Behrendt RP: Dysregulation of thalamic sensory ‘transmission’ in schizophrenia: neurochemical vulnerability to hallucinations. J Psychopharmacol 2006, 20:356-372.
• [3]Steriade M: Sleep, epilepsy and thalamic reticular inhibitory neurons. Trends Neurosci 2005, 28:317-324.
• [4]De Biasi S, Arcelli P, Spreafico R: Parvalbumin immunoreactivity in the thalamus of guinea pig: light and electron microscopic correlation with gamma-aminobutyric acid immunoreactivity. J Comp Neurol 1994, 348:556-569.
• [5]Cobos I, Broccoli V, Rubenstein JL: The vertebrate ortholog of Aristaless is regulated by Dlx genes in the developing forebrain. J Comp Neurol 2005, 483:292-303.
• [6]Delogu A, Sellers K, Zagoraiou L, Bocianowska-Zbrog A, Mandal S, Guimera J, Rubenstein JL, Sugden D, Jessell T, Lumsden A: Subcortical visual shell nuclei targeted by ipRGCs develop from a Sox14+-GABAergic progenitor and require Sox14 to regulate daily activity rhythms. Neuron 2012, 75:648-662.
• [7]Vue TY, Aaker J, Taniguchi A, Kazemzadeh C, Skidmore JM, Martin DM, Martin JF, Treier M, Nakagawa Y: Characterization of progenitor domains in the developing mouse thalamus. J Comp Neurol 2007, 505:73-91.
• [8]Kiecker C, Lumsden A: Hedgehog signaling from the ZLI regulates diencephalic regional identity. Nat Neurosci 2004, 7:1242-1249.
• [9]Scholpp S, Wolf O, Brand M, Lumsden A: Hedgehog signalling from the zona limitans intrathalamica orchestrates patterning of the zebrafish diencephalon. Development 2006, 133:855-864.
• [10]Vue TY, Bluske K, Alishahi A, Yang LL, Koyano-Nakagawa N, Novitch B, Nakagawa Y: Sonic hedgehog signaling controls thalamic progenitor identity and nuclei specification in mice. J Neurosci 2009, 29:4484-4497.
• [11]Bluske KK, Vue TY, Kawakami Y, Taketo MM, Yoshikawa K, Johnson JE, Nakagawa Y: beta-Catenin signaling specifies progenitor cell identity in parallel with Shh signaling in the developing mammalian thalamus. Development 2012, 139:2692-2702.
• [12]Kataoka A, Shimogori T: Fgf8 controls regional identity in the developing thalamus. Development 2008, 135:2873-2881.
• [13]Robertshaw E, Matsumoto K, Lumsden A, Kiecker C: Irx3 and Pax6 establish differential competence for Shh-mediated induction of GABAergic and glutamatergic neurons of the thalamus. Proc Natl Acad Sci U S A 2013, 110:E3919-E3926.
• [14]Scholpp S, Delogu A, Gilthorpe J, Peukert D, Schindler S, Lumsden A: Her6 regulates the neurogenetic gradient and neuronal identity in the thalamus. Proc Natl Acad Sci U S A 2009, 106:19895-19900.
• [15]Hashimoto-Torii K, Motoyama J, Hui C-C, Kuroiwa A, Nakafuku M, Shimamura K: Differential activities of Sonic hedgehog mediated by Gli transcription factors define distinct neuronal subtypes in the dorsal thalamus. Mech Dev 2003, 120:1097-1111.
• [16]Kitamura K, Miura H, Yanazawa M, Miyashita T, Kato K: Expression patterns of Brx1 (Rieg gene), Sonic hedgehog, Nkx2.2, Dlx1 and Arx during zona limitans intrathalamica and embryonic ventral lateral geniculate nuclear formation. Mech Dev 1997, 67:83-96.
• [17]Jeong Y, Dolson DK, Waclaw RR, Matise MP, Sussel L, Campbell K, Kaestner KH, Epstein DJ: Spatial and temporal requirements for sonic hedgehog in the regulation of thalamic interneuron identity. Development 2011, 138:531-541.
• [18]Virolainen SM, Achim K, Peltopuro P, Salminen M, Partanen J: Transcriptional regulatory mechanisms underlying the GABAergic neuron fate in different diencephalic prosomeres. Development 2012, 139:3795-3805.
• [19]Nakatani T, Minaki Y, Kumai M, Ono Y: Helt determines GABAergic over glutamatergic neuronal fate by repressing Ngn genes in the developing mesencephalon. Development 2007, 134:2783-2793.
• [20]Guimera J, Weisenhorn DV, Wurst W: Megane/Heslike is required for normal GABAergic differentiation in the mouse superior colliculus. Development 2006, 133:3847-3857.
• [21]Miyoshi G, Bessho Y, Yamada S, Kageyama R: Identification of a novel basic helix-loop-helix gene, Heslike, and its role in GABAergic neurogenesis. J Neurosci 2004, 24:3672-3682.
• [22]Anderson SA, Eisenstat DD, Shi L, Rubenstein JL: Interneuron migration from basal forebrain to neocortex: dependence on Dlx genes. Science 1997, 278:474-476.
• [23]Stühmer T, Anderson SA, Ekker M, Rubenstein JLR: Ectopic expression of the Dlx genes induces glutamic acid decarboxylase and Dlx expression. Development 2002, 129:245-252.
• [24]Long JE, Swan C, Liang WS, Cobos I, Potter GB, Rubenstein JL: Dlx1&2 and Mash1 transcription factors control striatal patterning and differentiation through parallel and overlapping pathways. J Comp Neurol 2009, 512:556-572.
• [25]Das RM, Van Hateren NJ, Howell GR, Farrell ER, Bangs FK, Porteous VC, Manning EM, McGrew MJ, Ohyama K, Sacco MA: A robust system for RNA interference in the chicken using a modified microRNA operon. Dev Biol 2006, 294:554-563.
• [26]Uchikawa M, Kamachi Y, Kondoh H: Two distinct subgroups of Group B Sox genes for transcriptional activators and repressors: their expression during embryonic organogenesis of the chicken. Mech Dev 1999, 84:103-120.
• [27]Yoon MS, Puelles L, Redies C: Formation of cadherin-expressing brain nuclei in diencephalic alar plate divisions. J Comp Neurol 2000, 427:461-480.
• [28]Muller K, Hirano S, Puelles L, Redies C: OL-protocadherin expression in the visual system of the chicken embryo. J Comp Neurol 2004, 470:240-255.
• [29]Strahle U, Blader P, Adam J, Ingham PW: A simple and efficient procedure for non-isotopic in situ hybridization to sectioned material. Trends Genet 1994, 10:75-76.