Dynamin Phosphorylation Controls Optimization of Endocytosis for Brief Action Potential Bursts

Overview

Journal Elife

Specialty Biology

Date 2013 Aug 3

PMID 23908769

Citations 41

Authors

Moritz Armbruster

Mirko Messa

Shawn M Ferguson

Pietro De Camilli

Timothy A Ryan

Affiliations

Soon will be listed here.

Abstract

Modulation of synaptic vesicle retrieval is considered to be potentially important in steady-state synaptic performance. Here we show that at physiological temperature endocytosis kinetics at hippocampal and cortical nerve terminals show a bi-phasic dependence on electrical activity. Endocytosis accelerates for the first 15-25 APs during bursts of action potential firing, after which it slows with increasing burst length creating an optimum stimulus for this kinetic parameter. We show that activity-dependent acceleration is only prominent at physiological temperature and that the mechanism of this modulation is based on the dephosphorylation of dynamin 1. Nerve terminals in which dynamin 1 and 3 have been replaced with dynamin 1 harboring dephospho- or phospho-mimetic mutations in the proline-rich domain eliminate the acceleration phase by either setting endocytosis at an accelerated state or a decelerated state, respectively. DOI:http://dx.doi.org/10.7554/eLife.00845.001.

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References

Wu X, McNeil B, Xu J, Fan J, Xue L, Melicoff E . Ca(2+) and calmodulin initiate all forms of endocytosis during depolarization at a nerve terminal. Nat Neurosci. 2009; 12(8):1003-1010. PMC: 4887276. DOI: 10.1038/nn.2355. View

Koch D, Spiwoks-Becker I, Sabanov V, Sinning A, Dugladze T, Stellmacher A . Proper synaptic vesicle formation and neuronal network activity critically rely on syndapin I. EMBO J. 2011; 30(24):4955-69. PMC: 3243622. DOI: 10.1038/emboj.2011.339. View

Yamashita T, Eguchi K, Saitoh N, von Gersdorff H, Takahashi T . Developmental shift to a mechanism of synaptic vesicle endocytosis requiring nanodomain Ca2+. Nat Neurosci. 2010; 13(7):838-44. PMC: 3677945. DOI: 10.1038/nn.2576. View

Larsen M, Graham M, Robinson P, Roepstorff P . Improved detection of hydrophilic phosphopeptides using graphite powder microcolumns and mass spectrometry: evidence for in vivo doubly phosphorylated dynamin I and dynamin III. Mol Cell Proteomics. 2004; 3(5):456-65. DOI: 10.1074/mcp.M300105-MCP200. View

HARATA N, Ryan T, Smith S, Buchanan J, Tsien R . Visualizing recycling synaptic vesicles in hippocampal neurons by FM 1-43 photoconversion. Proc Natl Acad Sci U S A. 2001; 98(22):12748-53. PMC: 60125. DOI: 10.1073/pnas.171442798. View

Graham M, Anggono V, Bache N, Larsen M, Craft G, Robinson P . The in vivo phosphorylation sites of rat brain dynamin I. J Biol Chem. 2007; 282(20):14695-707. DOI: 10.1074/jbc.M609713200. View

Kim S, Ryan T . Synaptic vesicle recycling at CNS snapses without AP-2. J Neurosci. 2009; 29(12):3865-74. PMC: 2713063. DOI: 10.1523/JNEUROSCI.5639-08.2009. View

Denker A, Bethani I, Krohnert K, Korber C, Horstmann H, Wilhelm B . A small pool of vesicles maintains synaptic activity in vivo. Proc Natl Acad Sci U S A. 2011; 108(41):17177-82. PMC: 3193224. DOI: 10.1073/pnas.1112688108. View

Chircop M, Sarcevic B, Larsen M, Malladi C, Chau N, Zavortink M . Phosphorylation of dynamin II at serine-764 is associated with cytokinesis. Biochim Biophys Acta. 2011; 1813(10):1689-99. DOI: 10.1016/j.bbamcr.2010.12.018. View

10.

Ferguson S, Brasnjo G, Hayashi M, Wolfel M, Collesi C, Giovedi S . A selective activity-dependent requirement for dynamin 1 in synaptic vesicle endocytosis. Science. 2007; 316(5824):570-4. DOI: 10.1126/science.1140621. View

11.

Liu J, Powell K, Sudhof T, Robinson P . Dynamin I is a Ca(2+)-sensitive phospholipid-binding protein with very high affinity for protein kinase C. J Biol Chem. 1994; 269(33):21043-50. View

12.

Balaji J, Armbruster M, Ryan T . Calcium control of endocytic capacity at a CNS synapse. J Neurosci. 2008; 28(26):6742-9. PMC: 2671224. DOI: 10.1523/JNEUROSCI.1082-08.2008. View

13.

Granseth B, Odermatt B, Royle S, Lagnado L . Clathrin-mediated endocytosis is the dominant mechanism of vesicle retrieval at hippocampal synapses. Neuron. 2006; 51(6):773-86. DOI: 10.1016/j.neuron.2006.08.029. View

14.

Kim S, Ryan T . Balance of calcineurin Aα and CDK5 activities sets release probability at nerve terminals. J Neurosci. 2013; 33(21):8937-50. PMC: 3808255. DOI: 10.1523/JNEUROSCI.4288-12.2013. View

15.

Tan T, Valova V, Malladi C, Graham M, Berven L, Jupp O . Cdk5 is essential for synaptic vesicle endocytosis. Nat Cell Biol. 2003; 5(8):701-10. DOI: 10.1038/ncb1020. View

16.

Ceccarelli B, HURLBUT W . Ca2+-dependent recycling of synaptic vesicles at the frog neuromuscular junction. J Cell Biol. 1980; 87(1):297-303. PMC: 2110728. DOI: 10.1083/jcb.87.1.297. View

17.

Sankaranarayanan S, De Angelis D, Rothman J, Ryan T . The use of pHluorins for optical measurements of presynaptic activity. Biophys J. 2000; 79(4):2199-208. PMC: 1301110. DOI: 10.1016/S0006-3495(00)76468-X. View

18.

Poskanzer K, Marek K, Sweeney S, Davis G . Synaptotagmin I is necessary for compensatory synaptic vesicle endocytosis in vivo. Nature. 2003; 426(6966):559-63. DOI: 10.1038/nature02184. View

19.

von Gersdorff H, Matthews G . Inhibition of endocytosis by elevated internal calcium in a synaptic terminal. Nature. 1994; 370(6491):652-5. DOI: 10.1038/370652a0. View

20.

Ceccarelli B, Grohovaz F, HURLBUT W . Freeze-fracture studies of frog neuromuscular junctions during intense release of neurotransmitter. I. Effects of black widow spider venom and Ca2+-free solutions on the structure of the active zone. J Cell Biol. 1979; 81(1):163-77. PMC: 2111523. DOI: 10.1083/jcb.81.1.163. View