Three modes of synaptic vesicular recycling revealed by single-vesicle imaging (original) (raw)

• Ryan, T. A. & Smith, S. J. Vesicle pool mobilization during action potential firing at hippocampal synapses. Neuron 14, 983–989 (1995)
  Article CAS Google Scholar
• Harata, N. et al. Limited numbers of recycling vesicles in small CNS nerve terminals: implications for neural signaling and vesicular cycling. Trends Neurosci. 24, 637–643 (2001)
  Article CAS Google Scholar
• Ryan, T. A. et al. The kinetics of synaptic vesicle recycling measured at single presynaptic boutons. Neuron 11, 713–724 (1993)
  Article CAS Google Scholar
• von Gersdorff, H. & Matthews, G. Dynamics of synaptic vesicle fusion and membrane retrieval in synaptic terminals. Nature 367, 735–739 (1994)
  Article ADS CAS Google Scholar
• von Gersdorff, H. & Matthews, G. Inhibition of endocytosis by elevated internal calcium in a synaptic terminal. Nature 370, 652–655 (1994)
  Article ADS CAS Google Scholar
• Wu, L. G. & Betz, W. J. Nerve activity but not intracellular calcium determines the time course of endocytosis at the frog neuromuscular junction. Neuron 17, 769–779 (1996)
  Article CAS Google Scholar
• Ryan, T. A., Smith, S. J. & Reuter, H. The timing of synaptic vesicle endocytosis. Proc. Natl Acad. Sci. USA 93, 5567–5571 (1996)
  Article ADS CAS Google Scholar
• Klingauf, J., Kavalali, E. T. & Tsien, R. W. Kinetics and regulation of fast endocytosis at hippocampal synapses. Nature 394, 581–585 (1998)
  Article ADS CAS Google Scholar
• Pyle, J. L., Kavalali, E. T., Piedras-Renteria, E. S. & Tsien, R. W. Rapid reuse of readily releasable pool vesicles at hippocampal synapses. Neuron 28, 221–231 (2000)
  Article CAS Google Scholar
• Stevens, C. F. & Williams, J. H. ‘Kiss and run’ exocytosis at hippocampal synapses. Proc. Natl Acad. Sci. USA 97, 12828–12833 (2000)
  Article ADS CAS Google Scholar
• Sankaranarayanan, S. & Ryan, T. A. Real-time measurements of vesicle-SNARE recycling in synapses of the central nervous system. Nature Cell Biol. 2, 197–204 (2000)
  Article CAS Google Scholar
• Neves, G., Gomis, A. & Lagnado, L. Calcium influx selects the fast mode of endocytosis in the synaptic terminal of retinal bipolar cells. Proc. Natl Acad. Sci. USA 98, 15282–15287 (2001)
  Article ADS CAS Google Scholar
• Sankaranarayanan, S. & Ryan, T. A. Calcium accelerates endocytosis of vSNAREs at hippocampal synapses. Nature Neurosci. 4, 129–136 (2001)
  Article CAS Google Scholar
• Heidelberger, R. ATP is required at an early step in compensatory endocytosis in synaptic terminals. J. Neurosci. 21, 6467–6474 (2001)
  Article CAS Google Scholar
• Sun, J. Y., Wu, X. S. & Wu, L. G. Single and multiple vesicle fusion induce different rates of endocytosis at a central synapse. Nature 417, 555–559 (2002)
  Article ADS CAS Google Scholar
• Zenisek, D., Steyer, J. A., Feldman, M. E. & Almers, W. A membrane marker leaves synaptic vesicles in milliseconds after exocytosis in retinal bipolar cells. Neuron 35, 1085–1097 (2002)
  Article CAS Google Scholar
• Heidelberger, R., Zhou, Z. Y. & Matthews, G. Multiple components of membrane retrieval in synaptic terminals revealed by changes in hydrostatic pressure. J. Neurophysiol. 88, 2509–2517 (2002)
  Article Google Scholar
• Miesenbock, G., De Angelis, D. A. & Rothman, J. E. Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 394, 192–195 (1998)
  Article ADS CAS Google Scholar
• Murthy, V. N., Sejnowski, T. J. & Stevens, C. F. Heterogeneous release properties of visualized individual hippocampal synapses. Neuron 18, 599–612 (1997)
  Article CAS Google Scholar
• Huang, E. P. & Stevens, C. F. Estimating the distribution of synaptic reliabilities. J. Neurophysiol. 78, 2870–2880 (1997)
  Article CAS Google Scholar
• Goda, Y. & Stevens, C. F. Two components of transmitter release at a central synapse. Proc. Natl Acad. Sci. USA 91, 12942–12946 (1994)
  Article ADS CAS Google Scholar
• Smith, C. & Neher, E. Multiple forms of endocytosis in bovine adrenal chromaffin cells. J. Cell Biol. 139, 885–894 (1997)
  Article CAS Google Scholar
• Taraska, J. W., Perrais, D., Ohara-Imaizumi, M., Nagamatsu, S. & Almers, W. Secretory granules are recaptured largely intact after stimulated exocytosis in cultured endocrine cells. Proc. Natl Acad. Sci. USA 100, 2070–2075 (2003)
  Article ADS CAS Google Scholar
• Beutner, D., Voets, T., Neher, E. & Moser, T. Calcium dependence of exocytosis and endocytosis at the cochlear inner hair cell afferent synapse. Neuron 29, 681–690 (2001)
  Article CAS Google Scholar
• 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. 506, 591–608 (1998)
  Article CAS Google Scholar
• Hsu, S. F. & Jackson, M. B. Rapid exocytosis and endocytosis in nerve terminals of the rat posterior pituitary. J. Physiol. 494, 539–553 (1996)
  Article CAS Google Scholar
• Neale, E. A., Bowers, L. M., Jia, M., Bateman, K. E. & Williamson, L. C. Botulinum neurotoxin A blocks synaptic vesicle exocytosis but not endocytosis at the nerve terminal. J. Cell Biol. 147, 1249–1260 (1999)
  Article CAS Google Scholar
• Thomas, P., Lee, A. K., Wong, J. G. & Almers, W. A triggered mechanism retrieves membrane in seconds after Ca(2 + )-stimulated exocytosis in single pituitary cells. J. Cell Biol. 124, 667–675 (1994)
  Article CAS Google Scholar
• Albillos, A. et al. The exocytotic event in chromaffin cells revealed by patch amperometry. Nature 389, 509–512 (1997)
  Article ADS CAS Google Scholar
• Klyachko, V. A. & Jackson, M. B. Capacitance steps and fusion pores of small and large-dense-core vesicles in nerve terminals. Nature 418, 89–92 (2002)
  Article ADS CAS Google Scholar
• Ales, E. et al. High calcium concentrations shift the mode of exocytosis to the kiss- and-run mechanism. Nature Cell Biol. 1, 40–44 (1999)
  Article CAS Google Scholar
• Cousin, M. A. & Robinson, P. J. Two mechanisms of synaptic vesicle recycling in rat brain nerve terminals. J. Neurochem. 75, 1645–1653 (2000)
  Article CAS Google Scholar
• Murthy, V. N. & Stevens, C. F. Reversal of synaptic vesicle docking at central synapses. Nature Neurosci. 2, 503–507 (1999)
  Article CAS Google Scholar
• Sankaranarayanan, S., De Angelis, D., Rothman, J. E. & Ryan, T. A. The use of pHluorins for optical measurements of presynaptic activity. Biophys. J. 79, 2199–2208 (2000)
  Article CAS Google Scholar
• Wu, M. M. et al. Mechanisms of pH regulation in the regulated secretory pathway. J. Biol. Chem. 276, 33027–33035 (2001)
  Article CAS Google Scholar
• Wu, M. M. et al. Organelle pH studies using targeted avidin and fluorescein-biotin. Chem. Biol. 7, 197–209 (2000)
  Article CAS Google Scholar
• Nishi, T. & Forgac, M. The vacuolar (H + )-ATPases—nature's most versatile proton pumps. Nature Rev. Mol. Cell Biol. 3, 94–103 (2002)
  Article CAS Google Scholar