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The Journal of Neuroscience, March 31, 2004, 24(13):3355-3369; doi:10.1523/JNEUROSCI.3860-03.2004

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Cellular/Molecular
Dual Control of Neurogenesis by PC3 through Cell Cycle Inhibition and Induction of Math1

Daniela Canzoniere,^1 * Stefano Farioli-Vecchioli,^1 * Filippo Conti,¹ Maria Teresa Ciotti,¹ Ada Maria Tata,³ Gabriella Augusti-Tocco,³ Elisabetta Mattei,² Madepalli K. Lakshmana,¹ Valery Krizhanovsky,⁴ Steven A. Reeves,⁵ Roberto Giovannoni,⁶ Francesca Castano,⁶ Antonio Servadio,⁶ Nissim Ben-Arie,⁴ and Felice Tirone¹

¹Istituto Neurobiologia e Medicina Molecolare and ²Istituto Biologia e Patologia Molecolare, Consiglio Nazionale delle Ricerche, 00156 Rome, Italy, ³Dipartimento Biologia Cellulare e dello Sviluppo, Università Sapienza, 00185 Rome, Italy, ⁴Department of Cell and Animal Biology, The Hebrew University of Jerusalem, Jerusalem 91904, Israel, ⁵Central Nervous System Signaling Laboratory, Center for Aging, Genetics, and Neurodegeneration, Massachusetts General Hospital, Harvard Medical School, Charlestown, Massachusetts 02129, and ⁶Telethon Institute of Genetics and Medicine, 00161 Naples, Italy

Growing evidence indicates that cell cycle arrest and neurogenesis are highly coordinated and interactive processes, governed by cell cycle genes and neural transcription factors. The gene PC3 (Tis21/BTG2) is expressed in the neuroblast throughout the neural tube and inhibits cell cycle progression at the G₁ checkpoint by repressing cyclin D1 transcription. We generated inducible mouse models in which the expression of PC3 was upregulated in neuronal precursors of the neural tube and of the cerebellum. These mice exhibited a marked increase in the production of postmitotic neurons and impairment of cerebellar development. Cerebellar granule precursors of PC3 transgenic mice displayed inhibition of cyclin D1 expression and a strong increase in the expression of Math1, a transcription factor required for their differentiation. Furthermore, PC3, encoded by a recombinant adenovirus, also induced Math1 in postmitotic granule cells in vitro and stimulated the Math1 promoter activity. In contrast, PC3 expression was unaffected in the cerebellar primordium of Math1 null mice, suggesting that PC3 acts upstream to Math1. As a whole, our data suggest that cell cycle exit of cerebellar granule cell precursors and the onset of cerebellar neurogenesis are coordinated by PC3 through transcriptional control of cyclin D1 and Math1, respectively.

Key words: cyclin D1; Math1; NeuroD1; nestin; neuroepithelia; tet-on/off

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Received Aug 19, 2003; revised January 19, 2004; accepted January 21, 2004.

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