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The Journal of Neuroscience, August 10, 2005, 25(32):7299-7308; doi:10.1523/JNEUROSCI.1573-05.2005

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Cellular/Molecular
Phosphorylation of Synapsin I by cAMP-Dependent Protein Kinase Controls Synaptic Vesicle Dynamics in Developing Neurons

Dario Bonanomi,¹ Andrea Menegon,¹ Annarita Miccio,² Giuliana Ferrari,² Anna Corradi,³ Hung-Teh Kao,⁴ Fabio Benfenati,³ and Flavia Valtorta¹

¹Department of Neuroscience, San Raffaele Scientific Institute and Vita-Salute University, 20132 Milan, Italy, ²Telethon Institute for Gene Therapy, San Raffaele Scientific Institute, 20132 Milan, Italy, ³Department of Experimental Medicine, Section of Physiology, University of Genova, 16132 Genova, Italy, and ⁴Nathan Kline Institute for Psychiatric Research, Orangeburg, New York 10962

In developing neurons, synaptic vesicles (SVs) undergo cycles of exo-endocytosis along isolated axons. However, it is currently unknown whether SV exocytosis is regulated before synaptogenesis. Here, we show that cAMP-dependent pathways affect SV distribution and recycling in the axonal growth cone and that these effects are mediated by the SV-associated phosphoprotein synapsin I. The presence of synapsin I on SVs is necessary for the correct localization of the vesicles in the central portion of the growth cone. Phosphorylation of synapsin I by cAMP-dependent protein kinase (protein kinase A) causes the dissociation of the protein from the SV membrane, allowing diffusion of the vesicles to the periphery of the growth cone and enhancing their rate of recycling. These results provide new clues as to the bases of the well known activity of synapsin I in synapse maturation and indicate that molecular mechanisms similar to those operating at mature nerve terminals are active in developing neurons to regulate the SV life cycle before synaptogenesis.

Key words: growth cone; phosphorylation; synapse formation; trafficking; knock-out mice; lentiviruses

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Received Jan 18, 2005; revised June 24, 2005; accepted June 25, 2005.

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