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The Journal of Neuroscience, June 11, 2008, 28(24):6092-6103; doi:10.1523/JNEUROSCI.0677-08.2008

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Development/Plasticity/Repair
Genomic Analysis of Drosophila Neuronal Remodeling: A Role for the RNA-Binding Protein Boule as a Negative Regulator of Axon Pruning

Eric D. Hoopfer,^1,2 * Andrea Penton,^1 * Ryan J. Watts,¹ and Liqun Luo^1,2

¹Department of Biology and ²Neurosciences Program, Howard Hughes Medical Institute, Stanford University, Stanford, California 94305

Correspondence should be addressed to Liqun Luo at the above address. Email: lluo{at}stanford.edu

Drosophila mushroom body (MB) neurons undergo axon pruning during metamorphosis through a process of localized degeneration of specific axon branches. Developmental axon degeneration is initiated by the steroid hormone ecdysone, acting through a nuclear receptor complex composed of USP (ultraspiracle) and EcRB1 (ecdysone receptor B1) to regulate gene expression in MB neurons. To identify ecdysone-dependent gene expression changes in MB neurons at the onset of axon pruning, we use laser capture microdissection to isolate wild-type and mutant MB neurons in which EcR (ecdysone receptor) activity is genetically blocked, and analyze expression changes by microarray. We identify several molecular pathways that are regulated in MB neurons by ecdysone. The most striking observation is the upregulation of genes involved in the UPS (ubiquitin–proteasome system), which is cell autonomously required for neuron pruning. In addition, we characterize the function of Boule, an evolutionarily conserved RNA-binding protein previously implicated in spermatogenesis in flies and vertebrates. boule expression is downregulated by ecdysone in MB neurons at the onset of pruning, and forced expression of Boule in MB neurons is sufficient to inhibit axon pruning. This activity is dependent on the RNA-binding domain of Boule and a conserved DAZ (deleted in azoospermia) domain implicated in interactions with other RNA-binding proteins. However, loss of Boule does not result in obvious defects in axon pruning or morphogenesis of MB neurons, suggesting that it acts redundantly with other ecdyonse-regulated genes. We propose a novel function for Boule in the CNS as a negative regulator of developmental axon pruning.

Key words: axon degeneration; mushroom body; neural development; ecdysone; ecdysone receptor; ubiquitin proteasome system; metamorphosis

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Received Feb. 14, 2008; revised April 7, 2008; accepted April 28, 2008.

Correspondence should be addressed to Liqun Luo at the above address. Email: lluo{at}stanford.edu

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