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The Journal of Neuroscience, March 23, 2005, 25(12):3067-3079; doi:10.1523/JNEUROSCI.3738-04.2005

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Development/Plasticity/Repair
Distinct Roles of Calcineurin-Nuclear Factor of Activated T-Cells and Protein Kinase A-cAMP Response Element-Binding Protein Signaling in Presynaptic Differentiation

Tomoyuki Yoshida and Masayoshi Mishina

Department of Molecular Neurobiology and Pharmacology, Graduate School of Medicine, University of Tokyo, and Solution-Oriented Research for Science and Technology, Japan Science and Technology Corporation, Tokyo 113-0033, Japan

Synaptic vesicle accumulation and morphological changes are characteristic features of axon terminal differentiation during synaptogenesis. To investigate the regulatory mechanism that orchestrates synaptic molecules to form mature presynaptic terminals, we visualized a single axon terminal of zebrafish olfactory sensory neurons in vivo and examined the effects of the neuron-specific gene manipulations on the axon terminal differentiation. Synaptic vesicles visualized with vesicle-associated membrane protein 2 (VAMP2)-enhanced green fluorescent protein (EGFP) fusion protein gradually accumulated in axon terminals, whereas the axon terminals visualized with GAP43 fused with EGFP remodeled from complex shapes with filopodia to simple shapes without filopodia from 50 h postfertilization (hpf) to 84 hpf. Expression of dominant-negative protein kinase A (PKA) or cAMP response element-binding protein (CREB) suppressed the VAMP2-EGFP punctum formation in axon terminals during synaptogenesis. Consistently, constitutively active PKA or CREB stimulated VAMP2-EGFP puncta formation. On the other hand, cyclosporine A treatment or suppression of nuclear factor of activated T cells (NFAT) activation prevented the axon terminal remodeling from complex to simple shapes during synaptogenesis. Consistently, expression of constitutively active calcineurin accelerated the axon terminal remodeling. These results suggest that calcineurin-NFAT signaling regulates axon terminal remodeling, and PKA-CREB signaling controls synaptic vesicle accumulation.

Key words: protein kinase A; CREB; calcineurin; NFAT; synapse formation; zebrafish

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Received Sep 9, 2004; revised January 12, 2005; accepted February 10, 2005.

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