Late Recruitment of Synapsin to Nascent Synapses is Regulated by Cdk5

Overview

Journal Cell Rep

Publisher Cell Press

Specialties Biology
Cell Biology
Molecular Biology

Date 2013 Apr 23

PMID 23602570

Citations 25

Authors

Courtney Easley-Neal

Javier Fierro Jr

JoAnn Buchanan

Philip Washbourne

Affiliations

Soon will be listed here.

Abstract

Synapse formation is a complex process that involves the recruitment and assembly of a myriad of pre- and postsynaptic proteins. Despite being present at every synapse in the vertebrate CNS, little is known about the transport, recruitment, and stabilization of synapsin at nascent synapses during development. We examined the transport and recruitment of synapsin to nascent presynaptic terminals in vivo in the developing zebrafish spinal cord. Synapsin was transported in a transport packet independently of two other presynaptic organelles: synaptic vesicle (SV) protein transport vesicles (STVs) and Piccolo-containing active zone precursor transport vesicles (PTVs). During presynaptic assembly, recruitment of all three transport packets occurred in an ordered sequence: STVs preceded PTVs, which in turn preceded synapsin. Importantly, cyclin-dependent kinase 5 (Cdk5) specifically regulated the late recruitment of synapsin transport packets at synapses. These results point to additional layers of complexity in the established mechanisms of synaptogenesis.

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References

Ando K, Uemura K, Kuzuya A, Maesako M, Asada-Utsugi M, Kubota M . N-cadherin regulates p38 MAPK signaling via association with JNK-associated leucine zipper protein: implications for neurodegeneration in Alzheimer disease. J Biol Chem. 2010; 286(9):7619-28. PMC: 3045016. DOI: 10.1074/jbc.M110.158477. View

Samuels B, Hsueh Y, Shu T, Liang H, Tseng H, Hong C . Cdk5 promotes synaptogenesis by regulating the subcellular distribution of the MAGUK family member CASK. Neuron. 2007; 56(5):823-37. PMC: 2151975. DOI: 10.1016/j.neuron.2007.09.035. View

Valor L, Grant S . Integrating synapse proteomics with transcriptional regulation. Behav Genet. 2006; 37(1):18-30. DOI: 10.1007/s10519-006-9114-3. View

Huttner W, Schiebler W, Greengard P, De Camilli P . Synapsin I (protein I), a nerve terminal-specific phosphoprotein. III. Its association with synaptic vesicles studied in a highly purified synaptic vesicle preparation. J Cell Biol. 1983; 96(5):1374-88. PMC: 2112660. DOI: 10.1083/jcb.96.5.1374. View

Fabry B, Klemm A, Kienle S, Schaffer T, Goldmann W . Focal adhesion kinase stabilizes the cytoskeleton. Biophys J. 2011; 101(9):2131-8. PMC: 3207160. DOI: 10.1016/j.bpj.2011.09.043. View

Jontes J, Buchanan J, Smith S . Growth cone and dendrite dynamics in zebrafish embryos: early events in synaptogenesis imaged in vivo. Nat Neurosci. 2000; 3(3):231-7. DOI: 10.1038/72936. View

Douglass A, Kraves S, Deisseroth K, Schier A, Engert F . Escape behavior elicited by single, channelrhodopsin-2-evoked spikes in zebrafish somatosensory neurons. Curr Biol. 2008; 18(15):1133-7. PMC: 2891506. DOI: 10.1016/j.cub.2008.06.077. View

Pineda R, Heiser R, Ribera A . Developmental, molecular, and genetic dissection of INa in vivo in embryonic zebrafish sensory neurons. J Neurophysiol. 2005; 93(6):3582-93. DOI: 10.1152/jn.01070.2004. View

Lazarevic V, Schone C, Heine M, Gundelfinger E, Fejtova A . Extensive remodeling of the presynaptic cytomatrix upon homeostatic adaptation to network activity silencing. J Neurosci. 2011; 31(28):10189-200. PMC: 6623065. DOI: 10.1523/JNEUROSCI.2088-11.2011. View

10.

Jontes J, Emond M, Smith S . In vivo trafficking and targeting of N-cadherin to nascent presynaptic terminals. J Neurosci. 2004; 24(41):9027-34. PMC: 6730076. DOI: 10.1523/JNEUROSCI.5399-04.2004. View

11.

Bonanomi D, Menegon A, Miccio A, Ferrari G, Corradi A, Kao H . Phosphorylation of synapsin I by cAMP-dependent protein kinase controls synaptic vesicle dynamics in developing neurons. J Neurosci. 2005; 25(32):7299-308. PMC: 6725302. DOI: 10.1523/JNEUROSCI.1573-05.2005. View

12.

Eisen J, Pike S . The spt-1 mutation alters segmental arrangement and axonal development of identified neurons in the spinal cord of the embryonic zebrafish. Neuron. 1991; 6(5):767-76. DOI: 10.1016/0896-6273(91)90173-w. View

13.

Kanungo J, Li B, Goswami M, Zheng Y, Ramchandran R, Pant H . Cloning and characterization of zebrafish (Danio rerio) cyclin-dependent kinase 5. Neurosci Lett. 2006; 412(3):233-8. PMC: 2696171. DOI: 10.1016/j.neulet.2006.11.016. View

14.

Ribera A, Nusslein-Volhard C . Zebrafish touch-insensitive mutants reveal an essential role for the developmental regulation of sodium current. J Neurosci. 1998; 18(22):9181-91. PMC: 6792885. View

15.

Downes G, Granato M . Supraspinal input is dispensable to generate glycine-mediated locomotive behaviors in the zebrafish embryo. J Neurobiol. 2006; 66(5):437-51. DOI: 10.1002/neu.20226. View

16.

Bozdagi O, Valcin M, Poskanzer K, Tanaka H, Benson D . Temporally distinct demands for classic cadherins in synapse formation and maturation. Mol Cell Neurosci. 2004; 27(4):509-21. PMC: 2910522. DOI: 10.1016/j.mcn.2004.08.008. View

17.

Matsubara M, Kusubata M, Ishiguro K, Uchida T, Titani K, Taniguchi H . Site-specific phosphorylation of synapsin I by mitogen-activated protein kinase and Cdk5 and its effects on physiological functions. J Biol Chem. 1996; 271(35):21108-13. DOI: 10.1074/jbc.271.35.21108. View

18.

Scott D, Das U, Tang Y, Roy S . Mechanistic logic underlying the axonal transport of cytosolic proteins. Neuron. 2011; 70(3):441-54. PMC: 3096075. DOI: 10.1016/j.neuron.2011.03.022. View

19.

Kanungo J, Zheng Y, Mishra B, Pant H . Zebrafish Rohon-Beard neuron development: cdk5 in the midst. Neurochem Res. 2008; 34(6):1129-37. PMC: 6007013. DOI: 10.1007/s11064-008-9885-4. View

20.

Bury L, Sabo S . Coordinated trafficking of synaptic vesicle and active zone proteins prior to synapse formation. Neural Dev. 2011; 6:24. PMC: 3103415. DOI: 10.1186/1749-8104-6-24. View