Prox1 regulates the subtype-specific development of caudal ganglionic eminence-derived GABAergic cortical interneurons

Goichi Miyoshi, Allison Young, Timothy Petros, Theofanis Karayannis, Melissa Mc Kenzie Chang, Alfonso Lavado, Tomohiko Iwano, Miho Nakajima, Hiroki Taniguchi, Z. Josh Huang, Nathaniel Heintz, Guillermo Oliver, Fumio Matsuzaki, Robert P. Machold, Gordon Fishell

    Research output: Contribution to journalArticle

    Abstract

    Neurogliaform (RELN+) and bipolar (VIP+) GABAergic interneurons of the mammalian cerebral cortex provide critical inhibition locally within the superficial layers. While these subtypes are known to originate from the embryonic caudal ganglionic eminence (CGE), the specific genetic programs that direct their positioning, maturation, and integration into the cortical network have not been elucidated. Here, we report that in mice expression of the transcription factor Prox1 is selectively maintained in postmitotic CGE-derived cortical interneuron precursors and that loss of Prox1 impairs the integration of these cells into superficial layers. Moreover, Prox1 differentially regulates the postnatal maturation of each specific subtype originating from the CGE (RELN, Calb2/VIP, and VIP). Interestingly, Prox1 promotes the maturation of CGE-derived interneuron subtypes through intrinsic differentiation programs that operate in tandem with extrinsically driven neuronal activity-dependent pathways. Thus Prox1 represents the first identified transcription factor specifically required for the embryonic and postnatal acquisition of CGE-derived cortical interneuron properties.

    Original languageEnglish (US)
    Pages (from-to)12869-12889
    Number of pages21
    JournalJournal of Neuroscience
    Volume35
    Issue number37
    DOIs
    StatePublished - Sep 16 2015

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    Interneurons
    Transcription Factors
    Cerebral Cortex

    Keywords

    • Bipolar
    • Mouse genetics
    • Neurogliaform
    • RELN
    • Transcription
    • VIP

    ASJC Scopus subject areas

    • Neuroscience(all)

    Cite this

    Miyoshi, G., Young, A., Petros, T., Karayannis, T., Chang, M. M. K., Lavado, A., ... Fishell, G. (2015). Prox1 regulates the subtype-specific development of caudal ganglionic eminence-derived GABAergic cortical interneurons. Journal of Neuroscience, 35(37), 12869-12889. https://doi.org/10.1523/JNEUROSCI.1164-15.2015

    Prox1 regulates the subtype-specific development of caudal ganglionic eminence-derived GABAergic cortical interneurons. / Miyoshi, Goichi; Young, Allison; Petros, Timothy; Karayannis, Theofanis; Chang, Melissa Mc Kenzie; Lavado, Alfonso; Iwano, Tomohiko; Nakajima, Miho; Taniguchi, Hiroki; Josh Huang, Z.; Heintz, Nathaniel; Oliver, Guillermo; Matsuzaki, Fumio; Machold, Robert P.; Fishell, Gordon.

    In: Journal of Neuroscience, Vol. 35, No. 37, 16.09.2015, p. 12869-12889.

    Research output: Contribution to journalArticle

    Miyoshi, G, Young, A, Petros, T, Karayannis, T, Chang, MMK, Lavado, A, Iwano, T, Nakajima, M, Taniguchi, H, Josh Huang, Z, Heintz, N, Oliver, G, Matsuzaki, F, Machold, RP & Fishell, G 2015, 'Prox1 regulates the subtype-specific development of caudal ganglionic eminence-derived GABAergic cortical interneurons', Journal of Neuroscience, vol. 35, no. 37, pp. 12869-12889. https://doi.org/10.1523/JNEUROSCI.1164-15.2015
    Miyoshi, Goichi ; Young, Allison ; Petros, Timothy ; Karayannis, Theofanis ; Chang, Melissa Mc Kenzie ; Lavado, Alfonso ; Iwano, Tomohiko ; Nakajima, Miho ; Taniguchi, Hiroki ; Josh Huang, Z. ; Heintz, Nathaniel ; Oliver, Guillermo ; Matsuzaki, Fumio ; Machold, Robert P. ; Fishell, Gordon. / Prox1 regulates the subtype-specific development of caudal ganglionic eminence-derived GABAergic cortical interneurons. In: Journal of Neuroscience. 2015 ; Vol. 35, No. 37. pp. 12869-12889.
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