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The Journal of Neuroscience, July 4, 2007, 27(27):7284-7296; doi:10.1523/JNEUROSCI.0731-07.2007

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Cellular/Molecular
Syntabulin–Kinesin-1 Family Member 5B-Mediated Axonal Transport Contributes to Activity-Dependent Presynaptic Assembly

Qian Cai, Ping-Yue Pan, and Zu-Hang Sheng

Synaptic Function Unit, The Porter Neuroscience Research Center, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, Maryland 20892-3701

Correspondence should be addressed to Zu-Hang Sheng, Synaptic Function Unit, The Porter Neuroscience Research Center, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Building 35, Room 3B203, 35 Convent Drive, Bethesda, MD 20892-3701. Email: shengz{at}ninds.nih.gov

The mechanism by which microtubule-based axonal transport regulates activity-dependent presynaptic plasticity in developing neurons remains mostly unknown. Our previous studies established that syntabulin is an adaptor capable of conjoining the kinesin family member 5B (KIF5B) motor and syntaxin-1. We now report that the complex of syntaxin-1–syntabulin–KIF5B mediates axonal transport of the active zone (AZ) components essential for presynaptic assembly. Syntabulin associates with AZ precursor carriers and colocalizes and comigrates with green fluorescent protein (GFP)-Bassoon-labeled AZ transport cargos within developing axons. Knock-down of syntabulin or disruption of the syntaxin-1–syntabulin–KIF5B complex impairs the anterograde transport of GFP-Bassoon out of the soma and reduces the axonal densities of synaptic vesicle (SV) clusters and FM4-64 [N-(3-triethylammoniumpropyl)-4-(p-dibutylaminostyryl)pyridinium, dibromide] loading. Furthermore, syntabulin loss of function results in a reduction in both the amplitude of postsynaptic currents and the frequency of asynchronous quantal events, and abolishes the activity-induced recruitment of new GFP-Bassoon into the axons and subsequent coclustering with SVs. Consequently, syntabulin loss of function blocks the formation of new presynaptic boutons during activity-dependent synaptic plasticity in developing neurons. These studies establish that a kinesin motor–adaptor complex is critical for the anterograde axonal transport of AZ components, thus contributing to activity-dependent presynaptic assembly during neuronal development.

Key words: axonal transport; microtubules; presynaptic assembly; synaptogenesis; presynaptic plasticity; active zone precursor; kinesin-1 motor

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Received Feb. 16, 2007; revised May 30, 2007; accepted May 30, 2007.

Correspondence should be addressed to Zu-Hang Sheng, Synaptic Function Unit, The Porter Neuroscience Research Center, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Building 35, Room 3B203, 35 Convent Drive, Bethesda, MD 20892-3701. Email: shengz{at}ninds.nih.gov

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