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The Journal of Neuroscience, July 16, 2003, 23(15):6362-6372

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Acute Induction of Conserved Synaptic Signaling Pathways in Drosophila Melanogaster

C. A. Hoeffer,¹ S. Sanyal,¹ and M. Ramaswami^1,2

¹Department of Molecular and Cellular Biology and ²Arizona Research Labs Division of Neurobiology, University of Arizona, Tucson, Arizona 85721

Analyses of early molecular and cellular events associated with long-term plasticity remain hampered in Drosophila by the lack of an acute procedure to activate signal transduction pathways, gene expression patterns, and other early cellular events associated with long-term synaptic change. Here we describe the development and first use of such a technique. Bursts of neural activity induced in Drosophila comatose^ts and CaP60A ^Kumts mutants, with conditional defects in N-ethylmaleimide-sensitive fusion factor 1 and sarco-endoplasmic reticulum Ca²⁺ ATPase, respectively, result in persistent (>4 hr) activation of neuronal extracellular signal-regulated kinase (ERK). ERK activation at the larval neuromuscular junction coincides with rapid reduction of synaptic Fasciclin II; in soma, nuclear translocation of activated ERK occurs together with increased transcription of the immediate-early genes Fos and c/EBP (CCAAT element binding protein). The effect of "seizure-stimulation" on ERK activation requires neural activity and is mediated through activation of MEK (MAPK/erk kinase), the MAPKK (mitogen-activated protein kinase kinase) that functions upstream of ERK. Our results (1) provide direct proof for the conservation of synaptic signaling pathways in arthropods, (2) demonstrate the utility of a new genetic tool for analysis of synaptic plasticity in Drosophila, and (3) potentially enable new proteomic and genomic analyses of activity-regulated molecules in an important model organism.

View larger version (49K): [in this window] [in a new window]   Figure 1. Temperature dependence of paralysis in Drosophila Na + channel (para ts1), NSF (comt tp7), and SERCA (CaP60A Kum170) mutants. Drosophila were exposed to different restrictive temperatures for 2 min and assayed for paralysis. Tight and distinct restrictive temperatures for Drosophila mutants shown in the figure are para ts1 (30°C), comt tp7 (35°C), and Ca60A Kum170 (40°C).

 

Key words: neurogenetics; temperature-sensitive paralysis; presynaptic; extracellular-signal regulated kinase; ERK; MAPK; Ras; sarcoendoplasmic reticulum Ca²⁺ ATPase; SERCA; Fasciclin II; Fas II; Drosophila; larval neuromuscular junction; NMJ

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Received Feb. 24, 2003; revised Apr. 22, 2003; accepted May. 2, 2003.

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