Calcineurin is universally involved in vesicle endocytosis at neuronal and nonneuronal secretory cells

Cell Reports

Volumn 7, Issue 4, 2014, Pages 982-988

  Wu, Xin Sheng ^a   Zhang, Zhen ^a   Zhao, Wei Dong ^a   Wang, Dongsheng ^a   Luo, Fujun ^a   Wu, Ling Gang ^a  

^a NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCINEURIN; CALCIUM; CALMODULIN; CALCIUM ION;

ANIMAL EXPERIMENT; ARTICLE; CALCIUM TRANSPORT; CELL TYPE; CHROMAFFIN CELL; CONTROLLED STUDY; DEVELOPMENTAL STAGE; ENDOCYTOSIS; FEMALE; MALE; MOUSE; NERVE ENDING; NEUROMUSCULAR SYNAPSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; SECRETORY CELL; ANIMAL CELL; CALCINEURIN GENE; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CELL VACUOLE; CELLULAR DISTRIBUTION; DOWN REGULATION; GLYCOCALYX; KNOCKOUT GENE; NERVE CELL PLASTICITY; NEUROSECRETORY CELL; PROTEIN ANALYSIS; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SYNAPSE; ANIMAL; BRAIN STEM; CYTOLOGY; KNOCKOUT MOUSE; METABOLISM; NERVE CELL; PHYSIOLOGY; SYNAPSE VESICLE;

ANIMALS; BRAIN STEM; CALCINEURIN; CHROMAFFIN CELLS; ENDOCYTOSIS; FEMALE; MALE; MICE; MICE, KNOCKOUT; NEURONS; SYNAPTIC VESICLES;

EID: 84901266719     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2014.04.020     Document Type: Article

References (33)

1. Armbruster M., Messa M., Ferguson S.M., De Camilli P., Ryan T.A. Dynamin phosphorylation controls optimization of endocytosis for brief action potential bursts. Elife 2013, 2:e00845.
2. Artalejo C.R., Elhamdani A., Palfrey H.C. Calmodulin is the divalent cation receptor for rapid endocytosis, but not exocytosis, in adrenal chromaffin cells. Neuron 1996, 16:195-205.
3. Chan S.A., Smith C. Physiological stimuli evoke two forms of endocytosis in bovine chromaffin cells. J. Physiol. 2001, 537:871-885.
4. Cheung G., Cousin M.A. Synaptic vesicle generation from activity-dependent bulk endosomes requires calcium and calcineurin. J. Neurosci. 2013, 33:3370-3379.
5. Chiang H.C., Shin W., Zhao W.D., Hamid E., Sheng J., Baydyuk M., Wen P.J., Jin A., Momboisse F., Wu L.G. Post-fusion structural changes and their roles in exocytosis and endocytosis of dense-core vesicles. Nat Commun. 2014, 5:3356.
6. Clayton E.L., Anggono V., Smillie K.J., Chau N., Robinson P.J., Cousin M.A. The phospho-dependent dynamin-syndapin interaction triggers activity-dependent bulk endocytosis of synaptic vesicles. J. Neurosci. 2009, 29:7706-7717.
7. Cousin M.A., Robinson P.J. The dephosphins: dephosphorylation by calcineurin triggers synaptic vesicle endocytosis. Trends Neurosci. 2001, 24:659-665.
8. Dittman J., Ryan T.A. Molecular circuitry of endocytosis at nerve terminals. Annu. Rev. Cell Dev. Biol. 2009, 25:133-160.
9. Engisch K.L., Nowycky M.C. Compensatory and excess retrieval: two types of endocytosis following single step depolarizations in bovine adrenal chromaffin cells. J. Physiol. 1998, 506:591-608.
10. Fulop T., Radabaugh S., Smith C. Activity-dependent differential transmitter release in mouse adrenal chromaffin cells. J. Neurosci. 2005, 25:7324-7332.
11. Hosoi N., Holt M., Sakaba T. Calcium dependence of exo- and endocytotic coupling at a glutamatergic synapse. Neuron 2009, 63:216-229.
12. Kim S.H., Ryan T.A. Balance of calcineurin Aα and CDK5 activities sets release probability at nerve terminals. J. Neurosci. 2013, 33:8937-8950.
13. Kuromi H., Yoshihara M., Kidokoro Y. An inhibitory role of calcineurin in endocytosis of synaptic vesicles at nerve terminals of Drosophila larvae. Neurosci. Res. 1997, 27:101-113.
14. Marks B., McMahon H.T. Calcium triggers calcineurin-dependent synaptic vesicle recycling in mammalian nerve terminals. Curr. Biol. 1998, 8:740-749.
15. Nicholson-Tomishima K., Ryan T.A. Kinetic efficiency of endocytosis at mammalian CNS synapses requires synaptotagmin I. Proc. Natl. Acad. Sci. USA 2004, 101:16648-16652.
16. Poskanzer K.E., Fetter R.D., Davis G.W. Discrete residues in the c(2)b domain of synaptotagmin I independently specify endocytic rate and synaptic vesicle size. Neuron 2006, 50:49-62.
17. Saheki Y., De Camilli P. Synaptic vesicle endocytosis. Cold Spring Harb. Perspect. Biol. 2012, 4:a005645.
18. Sankaranarayanan S., Ryan T.A. Real-time measurements of vesicle-SNARE recycling in synapses of the central nervous system. Nat. Cell Biol. 2000, 2:197-204.
19. Smillie K.J., Evans G.J., Cousin M.A. Developmental change in the calcium sensor for synaptic vesicle endocytosis in central nerve terminals. J. Neurochem. 2005, 94:452-458.
20. Sun J.Y., Wu L.G. Fast kinetics of exocytosis revealed by simultaneous measurements of presynaptic capacitance and postsynaptic currents at a central synapse. Neuron 2001, 30:171-182.
21. Sun J.Y., Wu X.S., Wu W., Jin S.X., Dondzillo A., Wu L.G. Capacitance measurements at the calyx of Held in the medial nucleus of the trapezoid body. J. Neurosci. Methods 2004, 134:121-131.
22. Sun T., Wu X.S., Xu J., McNeil B.D., Pang Z.P., Yang W., Bai L., Qadri S., Molkentin J.D., Yue D.T., Wu L.G. The role of calcium/calmodulin-activated calcineurin in rapid and slow endocytosis at central synapses. J. Neurosci. 2010, 30:11838-11847.
23. Wang L.Y., Neher E., Taschenberger H. Synaptic vesicles in mature calyx of Held synapses sense higher nanodomain calcium concentrations during action potential-evoked glutamate release. J. Neurosci. 2008, 28:14450-14458.
24. Wu L.G., Betz W.J. Nerve activity but not intracellular calcium determines the time course of endocytosis at the frog neuromuscular junction. Neuron 1996, 17:769-779.
25. Wu X.S., Wu L.G. The yin and yang of calcium effects on synaptic vesicle endocytosis. J. Neurosci. 2014, 34:2652-2659.
26. Wu W., Xu J., Wu X.S., Wu L.G. Activity-dependent acceleration of endocytosis at a central synapse. J. Neurosci. 2005, 25:11676-11683.
27. Wu X.S., McNeil B.D., Xu J., Fan J., Xue L., Melicoff E., Adachi R., Bai L., Wu L.G. Ca(2+) and calmodulin initiate all forms of endocytosis during depolarization at a nerve terminal. Nat. Neurosci. 2009, 12:1003-1010.
28. Wu L.G., Hamid E., Shin W., Chiang H.C. Exocytosis and endocytosis: modes, functions, and coupling mechanisms. Annu. Rev. Physiol. 2014, 76:301-331.
29. Xu J., Wu L.G. The decrease in the presynaptic calcium current is a major cause of short-term depression at a calyx-type synapse. Neuron 2005, 46:633-645.
30. Xu J., McNeil B., Wu W., Nees D., Bai L., Wu L.G. GTP-independent rapid and slow endocytosis at a central synapse. Nat. Neurosci. 2008, 11:45-53.
31. 2+. Nat. Neurosci. 2010, 13:838-844.
32. Yao J., Kwon S.E., Gaffaney J.D., Dunning F.M., Chapman E.R. Uncoupling the roles of synaptotagmin I during endo- and exocytosis of synaptic vesicles. Nat. Neurosci. 2011, 15:243-249.
33. Zhu Y., Xu J., Heinemann S.F. Two pathways of synaptic vesicle retrieval revealed by single-vesicle imaging. Neuron 2009, 61:397-411.