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The Journal of Neuroscience, March 24, 2004, 24(12):3104-3114; doi:10.1523/JNEUROSCI.4444-03.2004

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Development/Plasticity/Repair
Barhl1 Regulates Migration and Survival of Cerebellar Granule Cells by Controlling Expression of the Neurotrophin-3 Gene

Shengguo Li,¹ Feng Qiu,¹ Anlong Xu,² Sandy M. Price,¹ and Mengqing Xiang¹

¹Center for Advanced Biotechnology and Medicine and Department of Pediatrics, University of Medicine and Dentistry of New Jersey-Robert Wood Johnson Medical School, Piscataway, New Jersey 08854, and ²Department of Biochemistry, College of Life Sciences, Sun Yat-sen University, Guangzhou 510275, China

The neurons generated at the germinal rhombic lip undergo long distance migration along divergent pathways to settle in widely dispersed locations within the hindbrain, giving rise to cerebellar granule cells and precerebellar nuclei. Neurotrophin-3 (NT-3) signaling has been shown to be required for proper migration and survival of cerebellar granule cells. The molecular bases that govern NT-3 expression within the cerebellum, however, remain unknown at present. Here we report that, during early mouse neurogenesis, the Barhl1 homeobox gene is highly expressed by the rhombic lip and rhombic lip-derived migratory neurons. Its expression is later restricted to cerebellar granule cells and precerebellar neurons extending mossy fibers, two groups of neurons that synaptically connect in the adult cerebellar system. Loss of Barhl1 function causes cerebellar phenotypes with a striking similarity to those of NT-3 conditional null mice, which include attenuated cerebellar foliation as well as defective radial migration and increased apoptotic death of granule cells. Correlating with these defects, we find that NT-3 expression is dramatically downregulated in granule cells of the posterior lobe of Barhl1^–/– cerebella. Moreover, in the precerebellar system of Barhl1^–/– mice, all five nuclei that project mossy fibers fail to form correctly because of aberrant neuronal migration and elevated apoptosis. These results suggest that Barhl1 plays an essential role in the migration and survival of cerebellar granule cells and precerebellar neurons and functionally link Barhl1 to the NT-3 signaling pathway during cerebellar development.

Key words: Barhl1; homeobox gene; neurotrophin-3; cerebellum; neuronal migration; apoptosis; rhombic lip; pontine gray nucleus

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Received Sep 30, 2003; revised January 21, 2004; accepted February 13, 2004.

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