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Rapid kinetics of endocytosis at rod photoreceptor synapses depends upon endocytic load and calcium

Published online by Cambridge University Press:  15 April 2014

KARLENE M. CORK  and
WALLACE B. THORESON
KARLENE M. CORK
Affiliation:
Department of Pharmacology and Experimental Neuroscience, University of Nebraska Medical Center, Omaha, NE Department of Ophthalmology and Visual Sciences, University of Nebraska Medical Center, Omaha, NE
WALLACE B. THORESON*
Affiliation:
Department of Pharmacology and Experimental Neuroscience, University of Nebraska Medical Center, Omaha, NE Department of Ophthalmology and Visual Sciences, University of Nebraska Medical Center, Omaha, NE
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Abstract

Release from rods is triggered by the opening of L-type Ca2+ channels that lie beneath synaptic ribbons. After exocytosis, vesicles are retrieved by compensatory endocytosis. Previous work showed that endocytosis is dynamin-dependent in rods but dynamin-independent in cones. We hypothesized that fast endocytosis in rods may also differ from cones in its dependence upon the amount of Ca2+ influx and/or endocytic load. We measured exocytosis and endocytosis from membrane capacitance (Cm) changes evoked by depolarizing steps in voltage clamped rods from tiger salamander retinal slices. Similar to cones, the time constant for endocytosis in rods was quite fast, averaging <200 ms. We manipulated Ca2+ influx and the amount of vesicle release by altering the duration and voltage of depolarizing steps. Unlike cones, endocytosis kinetics in rods slowed after increasing Ca2+ channel activation with longer step durations or more strongly depolarized voltage steps. Endocytosis kinetics also slowed as Ca2+ buffering was decreased by replacing BAPTA (10 or 1 mM) with the slower Ca2+ buffer EGTA (5 or 0.5 mM) in the pipette solution. These data provide further evidence that endocytosis mechanisms differ in rods and cones and suggest that endocytosis in rods is regulated by both endocytic load and local Ca2+ levels.

Keywords

Rod photoreceptorsRetinaExocytosisEndocytosisRibbon synapse
Type
Research Articles
Information
Visual Neuroscience , Volume 31 , Issue 3 , May 2014 , pp. 227 - 235
Copyright
Copyright © Cambridge University Press 2014 

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References

Alabi, A.A. & Tsien, R.W. (2012). Synaptic vesicle pools and dynamics. Cold Spring Harbor Perspectives in Biology 4, a013680.CrossRefGoogle ScholarPubMed
Artalejo, C.R., Henley, J.R., McNiven, M.A. & Palfrey, H.C. (1995). Rapid endocytosis coupled to exocytosis in adrenal chromaffin cells involves Ca2+, GTP, and dynamin but not clathrin. Proceedings of the National Academy of Sciences of the United States of America 92, 8328–8332.CrossRefGoogle Scholar
Barg, S. & Machado, J.D. (2008). Compensatory endocytosis in chromaffin cells. Acta Physiologica (Oxford) 192, 195–201.CrossRefGoogle ScholarPubMed
Bartoletti, T.M., Babai, N. & Thoreson, W.B. (2010). Vesicle pool size at the salamander cone ribbon synapse. Journal of Neurophysiology 103, 419–423.CrossRefGoogle ScholarPubMed
Berntson, A. & Taylor, W.R. (2003). The unitary event amplitude of mouse retinal on-cone bipolar cells. Visual Neuroscience 20, 621–626.CrossRefGoogle ScholarPubMed
Beutner, D., Voets, T., Neher, E. & Moser, T. (2001). Calcium dependence of exocytosis and endocytosis at the cochlear inner hair cell afferent synapse. Neuron 29, 681–690.CrossRefGoogle ScholarPubMed
Chen, M., Krizaj, D. & Thoreson, W.B. (2014) Intracellular calcium stores drive slow non-ribbon vesicle release from rod photoreceptors. Frontiers in Cellular Neuroscience 8, 20.CrossRefGoogle ScholarPubMed
Chen, M., Van Hook, M.J., Zenisek, D. & Thoreson, W.B. (2013). Properties of ribbon and non-ribbon release from rod photoreceptors revealed by visualizing individual synaptic vesicles. The Journal of Neuroscience 33, 2071–2086.CrossRefGoogle ScholarPubMed
Cho, S., Li, G.L. & von Gersdorff, H. (2011). Recovery from short-term depression and facilitation is ultrafast and Ca2+ dependent at auditory hair cell synapses. The Journal of Neuroscience 31, 5682–5692.CrossRefGoogle ScholarPubMed
Chung, C., Barylko, B., Leitz, J., Liu, X. & Kavalali, E.T. (2010). Acute dynamin inhibition dissects synaptic vesicle recycling pathways that drive spontaneous and evoked neurotransmission. The Journal of Neuroscience 30, 1363–1376.CrossRefGoogle ScholarPubMed
Coggins, M.R., Grabner, C.P., Almers, W. & Zenisek, D. (2007) Stimulated exocytosis of endosomes in goldfish retinal bipolar neurons. The Journal of Physiology 584, 853–865.CrossRefGoogle ScholarPubMed
Dittman, J. & Ryan, T.A. (2009). Molecular circuitry of endocytosis at nerve terminals. Annual Review of Cell and Developmental Biology 25, 133–160.CrossRefGoogle ScholarPubMed
Dowling, J.E. (2012) The Retina: An Approachable Part of the Brain. Cambridge, MA: Belknap Press.CrossRefGoogle Scholar
Fuchs, M., Brandstätter, J.H. & Regus-Leidig, H. (2014). Evidence for a clathrin-independent mode of endocytosis at a continuously active sensory synapse. Frontiers in Cellular Neuroscience 25, 60.Google Scholar
Gandhi, S.P. & Stevens, C.F. (2003). Three modes of synaptic vesicular recycling revealed by single-vesicle imaging. Nature 423, 607–613.CrossRefGoogle ScholarPubMed
Gray, E.G. & Pease, H.L. (1971). On understanding the organisation of the retinal receptor synapses. Brain Research 35, 1–15.CrossRefGoogle ScholarPubMed
Gundelfinger, E.D., Kessels, M.M. & Qualmann, B. (2003). Temporal and spatial coordination of exocytosis and endocytosis. Nature Reviews Molecular Cell Biology 4, 127–139.CrossRefGoogle ScholarPubMed
Haucke, V., Neher, E., Sigrist, S.J. (2011). Protein scaffolds in the coupling of synaptic exocytosis and endocytosis. Nature Reviews Neuroscience 12, 127–138.CrossRefGoogle ScholarPubMed
Heidelberger, R. (2001). ATP is required at an early step in compensatory endocytosis in synaptic terminals. The Journal of Neuroscience 21, 6467–6474.CrossRefGoogle ScholarPubMed
Holt, M., Cooke, A., Wu, M.M. & Lagnado, L. (2003). Bulk membrane retrieval in the synaptic terminal of retinal bipolar cells. The Journal of Neuroscience 23, 1329–1339.CrossRefGoogle ScholarPubMed
Hsu, S.F. & Jackson, M.B. (1996). Rapid exocytosis and endocytosis in nerve terminals of the rat posterior pituitary. The Journal of Physiology 494, 539–553.CrossRefGoogle ScholarPubMed
Innocenti, B. & Heidelberger, R. (2008). Mechanisms contributing to tonic release at the cone photoreceptor ribbon synapse. Journal of Neurophysiology 99, 25–36.CrossRefGoogle ScholarPubMed
Jockusch, W.J., Praefcke, G.J., McMahon, H.T. & Lagnado, L. (2005). Clathrin-dependent and clathrin-independent retrieval of synaptic vesicles in retinal bipolar cells. Neuron 46, 869–878.CrossRefGoogle ScholarPubMed
Johnson, S.L., Thomas, M.V. & Kros, C.J. (2002). Membrane capacitance measurement using patch clamp with integrated self-balancing lock-in amplifier. Pflugers Archiv 443, 653–663.CrossRefGoogle ScholarPubMed
Leitz, J. & Kavalali, E.T. (2011). Ca2+ influx slows single synaptic vesicle endocytosis. The Journal of Neuroscience 31, 16318–16326.CrossRefGoogle ScholarPubMed
Linton, J.D., Holzhausen, L.C., Babai, N., Song, H., Miyagishima, K.J., Stearns, G.W., Lindsay, K., Wei, J., Chertov, A.O., Peters, T.A., Caffe, R., Pluk, H., Seeliger, M.W., Tanimoto, N., Fong, K., Bolton, L., Kuok, D.L., Sweet, I.R., Bartoletti, T.M., Radu, R.A., Travis, G.H., Zagotta, W.N., Townes-Anderson, E., Parker, E., Van der Zee, C.E., Sampath, A.P., Sokolov, M., Thoreson, W.B. & Hurley, J.B. (2010). Flow of energy in the outer retina in darkness and in light. Proceedings of the National Academy of Sciences of the United States of America 107, 8599–8604.CrossRefGoogle ScholarPubMed
Llobet, A., Beaumont, V. & Lagnado, L. (2003). Real-time measurement of exocytosis and endocytosis using interference of light. Neuron 40, 1075–1086.CrossRefGoogle ScholarPubMed
Llobet, A., Gallop, J.L., Burden, J.J., Camdere, G., Chandra, P., Vallis, Y., Hopkins, C.R., Lagnado, L. & McMahon, H.T. (2011). Endophilin drives the fast mode of vesicle retrieval in a ribbon synapse. The Journal of Neuroscience 31, 8512–8519.CrossRefGoogle Scholar
LoGiudice, L. & Matthews, G. (2007). Endocytosis at ribbon synapses. Traffic 8, 1123–1128.CrossRefGoogle ScholarPubMed
LoGiudice, L., Sterling, P. & Matthews, G. (2009). Vesicle recycling at ribbon synapses in the finely branched axon terminals of mouse retinal bipolar neurons. Neuroscience 164, 1546–1556.CrossRefGoogle ScholarPubMed
Miller, T.M. & Heuser, J.E. (1984). Endocytosis of synaptic vesicle membrane at the frog neuromuscular junction. The Journal of Cell Biology 98, 685–698.CrossRefGoogle ScholarPubMed
Neef, J., Jung, S., Wong, A.B., Reuter, K., Pangrsic, T., Chakrabarti, R., Kügler, S., Lenz, C., Nouvian, R., Boumil, R.M., Frankel, W.N., Wichmann, C. & Moser, T. (2014). Modes and regulation of endocytic membrane retrieval in mouse auditory hair cells. The Journal of Neuroscience 34, 705–716.CrossRefGoogle ScholarPubMed
Neher, E. (2010). What is rate-limiting during sustained synaptic activity: Vesicle supply or the availability of release sites. Frontiers in Synaptic Neuroscience 2, 144.CrossRefGoogle ScholarPubMed
Neves, G., Gomis, A. & Lagnado, L. (2001). Calcium influx selects the fast mode of endocytosis in the synaptic terminal of retinal bipolar cells. Proceedings of the National Academy of Sciences of the United States of America 98, 15282–15287.CrossRefGoogle ScholarPubMed
Neves, G. & Lagnado, L. (1999). The kinetics of exocytosis and endocytosis in the synaptic terminal of goldfish retinal bipolar cells. The Journal of Physiology 515, 181–202.CrossRefGoogle ScholarPubMed
Oltedal, L. & Hartveit, E. (2010). Transient release kinetics of rod bipolar cells revealed by capacitance measurement of exocytosis from axon terminals in rat retinal slices. The Journal of Physiology 588, 1469–1487.CrossRefGoogle ScholarPubMed
Pysh, J.J. & Wiley, R.G. (1974). Synaptic vesicle depletion and recovery in cat sympathetic ganglia electrically stimulated in vivo. Evidence for transmitter secretion by exocytosis. The Journal of Cell Biology 60, 365–374.CrossRefGoogle ScholarPubMed
Rabl, K., Cadetti, L. & Thoreson, W.B. (2005). Kinetics of exocytosis is faster in cones than in rods. The Journal of Neuroscience 25, 4633–4640.CrossRefGoogle ScholarPubMed
Rabl, K., Cadetti, L. & Thoreson, W.B. (2006). Paired-pulse depression at photoreceptor synapses. The Journal of Neuroscience 26, 2555–2563.CrossRefGoogle ScholarPubMed
Renden, R. & von Gersdorff, H. (2007). Synaptic vesicle endocytosis at a CNS nerve terminal: Faster kinetics at physiological temperatures and increased endocytic capacity during maturation. Journal of Neurophysiology 98, 3349–3359.CrossRefGoogle Scholar
Rieke, F. & Schwartz, E.A. (1996). Asynchronous transmitter release: Control of exocytosis and endocytosis at the salamander rod synapse. The Journal of Physiology 493, 1–8.CrossRefGoogle ScholarPubMed
Sankaranarayanan, S. & Ryan, T.A. (2000). Real-time measurements of vesicle-SNARE recycling in synapses of the central nervous system. Nature Cell Biology 2, 197–204.CrossRefGoogle ScholarPubMed
Santos-Sacchi, J. (2004). Determination of cell capacitance using the exact empirical solution of partial differential Y/partial differential Cm and its phase angle. Biophysical Journal 87, 714–727.CrossRefGoogle ScholarPubMed
Schaeffer, S.F. & Raviola, E. (1978). Membrane recycling in the cone cell endings of the turtle retina. The Journal of Cell Biology 79, 802–825.CrossRefGoogle ScholarPubMed
Schmitz, F. (2009). The making of synaptic ribbons: how they are built and what they do. Neuroscientist 15, 611–624.CrossRefGoogle Scholar
Sheng, Z., Choi, S.Y., Dharia, A., Li, J., Sterling, P. & Kramer, R.H. (2007). Synaptic Ca2+ in darkness is lower in rods than cones, causing slower tonic release of vesicles. The Journal of Neuroscience 27, 5033–5042.CrossRefGoogle ScholarPubMed
Sherry, D.M. & Heidelberger, R. (2005). Distribution of proteins associated with synaptic vesicle endocytosis in the mouse and goldfish retina. The Journal of Comparative Neurology 484, 440–457.CrossRefGoogle ScholarPubMed
Singer, J.H. & Diamond, J.S. (2006). Vesicle depletion and synaptic depression at a mammalian ribbon synapse. Journal of Neurophysiology 95, 3191–3198.CrossRefGoogle Scholar
Smith, S.M., Renden, R. & von Gersdorff, H. (2008). Synaptic vesicle endocytosis: Fast and slow modes of membrane retrieval. Trends in Neurosciences 31, 559–568.CrossRefGoogle ScholarPubMed
Snellman, J., Mehta, B., Babai, N., Bartoletti, T.M., Akmentin, W., Francis, A., Matthews, G., Thoreson, W. & Zenisek, D. (2011). Acute destruction of the synaptic ribbon reveals a role for the ribbon in vesicle priming. Nature Neuroscience 14, 1135–1141.CrossRefGoogle ScholarPubMed
Sterling, P. & Matthews, G. (2005). Structure and function of ribbon synapses. Trends in Neurosciences 28, 20–29.CrossRefGoogle ScholarPubMed
Sun, J.Y. & Wu, L.G. (2001). Fast kinetics of exocytosis revealed by simultaneous measurements of presynaptic capacitance and postsynaptic currents at a central synapse. Neuron 30, 171–182.CrossRefGoogle Scholar
Sun, J.Y., Wu, X.S. & Wu, L.G. (2002). Single and multiple vesicle fusion induce different rates of endocytosis at a central synapse. Nature 417, 555–559.CrossRefGoogle Scholar
Thomas, P., Lee, A.K., Wong, J.G. & Almers, W. (1994). A triggered mechanism retrieves membrane in seconds after Ca(2+)-stimulated exocytosis in single pituitary cells. The Journal of Cell Biology 124, 667–675.CrossRefGoogle ScholarPubMed
Thoreson, W.B., Rabl, K., Townes-Anderson, E. & Heidelberger, R. (2004). A highly Ca2+-sensitive pool of vesicles contributes to linearity at the rod photoreceptor ribbon synapse. Neuron 42, 595–605.CrossRefGoogle ScholarPubMed
Townes-Anderson, E., MacLeish, P.R. & Raviola, E. (1985). Rod cells dissociated from mature salamander retina: ultrastructure and uptake of horseradish peroxidase. The Journal of Cell Biology 100, 175–188.CrossRefGoogle ScholarPubMed
Ullrich, B. & Südhof, T.C. (1994). Distribution of synaptic markers in the retina: Implications for synaptic vesicle traffic in ribbon synapses. Journal of Physiology, Paris 88, 249–257.CrossRefGoogle ScholarPubMed
Van Hook, M.J. & Thoreson, W.B. (2012). Rapid synaptic vesicle endocytosis in cone photoreceptors of salamander retina. The Journal of Neuroscience 32, 18112–18123.CrossRefGoogle ScholarPubMed
Van Hook, M.J. & Thoreson, W.B. (2013). Simultaneous whole-cell recordings from photoreceptors and second-order neurons in an amphibian retinal slice preparation. Journal of Visualized Experiments 76: e50007.CrossRefGoogle Scholar
von Gersdorff, H. & Matthews, G. (1994 a). Inhibition of endocytosis by elevated internal calcium in a synaptic terminal. Nature 370, 652–655.CrossRefGoogle Scholar
von Gersdorff, H. & Matthews, G. (1994 b). Dynamics of synaptic vesicle fusion and membrane retrieval in synaptic terminals. Nature 367, 735–739.CrossRefGoogle ScholarPubMed
von Gersdorff, H., Sakaba, T., Berglund, K. & Tachibana, M. (1998). Submillisecond kinetics of glutamate release from a sensory synapse. Neuron 21. 1177–1188.CrossRefGoogle ScholarPubMed
Wahl, S., Katiyar, R. & Schmitz, F. (2013). A local, periactive zone endocytic machinery at photoreceptor synapses in close vicinity to synaptic ribbons. The Journal of Neuroscience 33, 10278–10300.CrossRefGoogle ScholarPubMed
Waites, C.L. & Garner, C.C. (2011). Presynaptic function in health and disease. Trends in Neurosciences 34, 326–337.CrossRefGoogle ScholarPubMed
Wan, Q.F. & Heidelberger, R. (2011). Synaptic release at mammalian bipolar cell terminals. Visual Neuroscience 28, 109–119.CrossRefGoogle ScholarPubMed
Wan, Q.F., Vila, A., Zhou, Z.Y. & Heidelberger, R. (2008). Synaptic vesicle dynamics in mouse rod bipolar cells. Visual Neuroscience 25, 523–533.CrossRefGoogle ScholarPubMed
Watanabe, S., Liu, Q., Davis, M.W., Hollopeter, G., Thomas, N., Jorgensen, N.B. & Jorgensen, E.M. (2013 a). Ultrafast endocytosis at Caenorhabditis elegans neuromuscular junctions. Elife 2, e00723.CrossRefGoogle ScholarPubMed
Watanabe, S., Rost, B.R., Camacho-Pérez, M., Davis, M.W., Söhl-Kielczynski, B., Rosenmund, C. & Jorgensen, E.M. (2013 b). Ultrafast endocytosis at mouse hippocampal synapses. Nature 504, 242–247.CrossRefGoogle ScholarPubMed
Wu, L.G. & Betz, W.J. (1996). Nerve activity but not intracellular calcium determines the time course of endocytosis at the frog neuromuscular junction. Neuron 17, 769–779.CrossRefGoogle Scholar
Wu, L.G., Hamid, E., Shin, W. & Chiang, H.C. (2014). Exocytosis and endocytosis: Modes, function, and coupling mechanisms. Annual Review of Physiology 76, 301–331.CrossRefGoogle ScholarPubMed
Wu, L.G., Ryan, T.A. & Lagnado, L. (2007). Modes of vesicle retrieval at ribbon synapses, calyx-type synapses, and small central synapses. The Journal of Neuroscience 27, 11793–11802.CrossRefGoogle ScholarPubMed
Wu, W., Xu, J., Wu, X.S. & Wu, L.G. (2005). Activity-dependent acceleration of endocytosis at a central synapse. The Journal of Neuroscience 25, 11676–11683.CrossRefGoogle Scholar
Wu, X.S. & Wu, L.G. (2014). The yin and yang of calcium effects of synaptic vesicle endocytosis. The Journal of Neuroscience 34, 2652–2659.CrossRefGoogle ScholarPubMed
Xu, J., McNeil, B., Wu, W., Nees, D., Bai, L. & Wu, LG. (2008). GTP-independent rapid and slow endocytosis at a central synapse. Nature Neuroscience 11, 45–53.CrossRefGoogle Scholar
Xue, L. & Mei, Y.A. (2011). Synaptic vesicle recycling at the calyx of held. Acta Pharmacologica Sinica 32, 280–287.CrossRefGoogle ScholarPubMed
Yamashita, T. (2012). Ca2+-dependent regulation of synaptic vesicle endocytosis. Neuroscience Research 73, 1–7.CrossRefGoogle ScholarPubMed
Yamashita, T., Eguchi, K., Saitoh, N., von Gersdorff, H. & Takahashi, T. (2010) Developmental shift to a mechanism of synaptic vesicle endocytosis requiring nanodomain Ca2+. Nature Neuroscience 13, 838–844.CrossRefGoogle ScholarPubMed
Zampighi, G.A., Schietroma, C., Zampighi, L.M., Woodruff, M., Wright, E.M. & Brecha, N.C. (2011). Conical tomography of a ribbon synapse: Structural evidence for vesicle fusion. PLOS One 6, e16944.CrossRefGoogle ScholarPubMed
Zenisek, D., Steyer, J.A., Feldman, M.E. & Almers, W. (2002). A membrane marker leaves synaptic vesicles in milliseconds after exocytosis in retinal bipolar cells. Neuron 35, 1085–1097.CrossRefGoogle ScholarPubMed