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A Drosophila kinesin required for synaptic bouton formation and synaptic vesicle transport

Nature Neuroscience volume 10, pages 980–989 (2007)Cite this article

Abstract

The morphological transition of growth cones to synaptic boutons characterizes synaptogenesis. Here we have isolated mutations in immaculate connections (imac; CG8566), a previously uncharacterized Drosophila gene encoding a member of the Kinesin-3 family. Whereas earlier studies in Drosophila implicated Kinesin-1 in transporting synaptic vesicle precursors, we find that Imac is essential for this transport. An unexpected feature of imac mutants is the failure of synaptic boutons to form. Motor neurons lacking imac properly target to muscles but remain within target fields as thin processes, a structure that is distinct from either growth cones or mature terminals. Few active zones form at these endings. We show that the arrest of synaptogenesis is not a secondary consequence of the absence of transmission. Our data thus indicate that Imac transports components required for synaptic maturation and provide insight into presynaptic maturation as a process that can be differentiated from axon outgrowth and targeting.

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Figure 1: Defective photoreceptor synaptic transmission and motor neuron synapse formation in imac mutants.
Figure 2: imac encodes a kinesin.
Figure 3: Synaptic and dense-core vesicle proteins are absent in imac nerve endings.
Figure 4: Synaptic vesicle proteins are selectively concentrated in cell bodies.
Figure 5: Altered developmental distribution of the active-zone marker nc82 in imac mutants.
Figure 6: Synaptic vesicles are rare and active zones are few in imac nerve profiles.
Figure 7: Postsynaptic differentiation in imac mutants.

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Acknowledgements

We thank W. Saxton, D. Van Vactor and J. Kaplan for comments on the manuscript; A. DiAntonio, R. Palmer, N. Reist, M. Higashi, and the Bloomington Stock Center for reagents and fly strains; A.Y.N. Goldstein and J. Salogiannis for experimental assistance; members of the Schwarz laboratory for discussions; HCNR and DDRC imaging cores for imaging and analysis assistance; A. Prokop and the HMS electron microscopy facility for electron microscopy help. This work was supported by a US National Research Service Award predoctoral fellowship (E.P.-C.), a Howard Hughes Medical Institute predoctoral fellowship (D.K.D.), and a grant from the US National Institutes of Health (RO1-MH075058 to T.L.S.).

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  1. Dion K Dickman

    Present address: Present address: Department of Biochemistry and Biophysics, University of California, San Francisco, 1550 4th St., San Francisco, California 94158, USA.,

Authors and Affiliations

  1. Program in Neurobiology, Children's Hospital, 300 Longwood Avenue, Boston, 02115, Massachusetts, USA

    Eunju Pack-Chung, Peri T Kurshan, Dion K Dickman & Thomas L Schwarz

  2. Department of Neurobiology, Harvard Medical School, 220 Longwood Avenue, Boston, 02115, Massachusetts, USA

    Eunju Pack-Chung, Peri T Kurshan, Dion K Dickman & Thomas L Schwarz

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Correspondence to Thomas L Schwarz.

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Pack-Chung, E., Kurshan, P., Dickman, D. et al. A Drosophila kinesin required for synaptic bouton formation and synaptic vesicle transport. Nat Neurosci 10, 980–989 (2007). https://doi.org/10.1038/nn1936

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