Calcium Extrusion from Mammalian Photoreceptor Terminals

Ribbon synapses of vertebrate photoreceptors constantly release glutamate in darkness. Transmitter release is maintained by a steady influx of calcium through voltage-dependent calcium channels, implying the presence of a mechanism that is able to extrude calcium at an equal rate. The two predominant mechanisms of intracellular calcium extrusion are the plasma membrane calcium ATPase (PMCA) and the Na+/Ca2+-exchanger. Immunohistochemical staining of retina sections revealed strong immunoreactivity for the PMCA in rod and cone terminals, whereas staining for the Na+/Ca2+-exchanger was very weak. The PMCA was localized to the plasma membrane along the sides of the photoreceptor terminals and was excluded from the base of the terminals where the active zones are located. The amplitude of a calcium-activated chloride current was used to monitor the intracellular calcium concentration. An upper limit for the time required to remove intracellular free calcium is obtained from two time constants measured for the calcium-activated chloride current tail currents: one of 50 msec and a second of 190 msec. Calcium extrusion was inhibited in the absence of intracellular ATP or in the presence of the PMCA inhibitor orthovanadate, but was unaffected by replacement of external Na+ with Li+. The data indicate that the PMCA, rather than the Na+/Ca2+-exchanger, is the predominant mechanism for calcium extrusion from photoreceptor synaptic terminals.

[1]  C. Morgans,et al.  Localization and properties of voltage-gated calcium channels in cone photoreceptors of Tupaia belangeri , 1998, Visual Neuroscience.

[2]  P. Witkovsky,et al.  Dependence of photoreceptor glutamate release on a dihydropyridine-sensitive calcium channel , 1997, Neuroscience.

[3]  H. Wässle,et al.  A SNARE Complex Containing Syntaxin 3 Is Present in Ribbon Synapses of the Retina , 1996, The Journal of Neuroscience.

[4]  Leon Lagnado,et al.  Continuous Vesicle Cycling in the Synaptic Terminal of Retinal Bipolar Cells , 1996, Neuron.

[5]  R. Fettiplace,et al.  Monitoring calcium in turtle hair cells with a calcium‐activated potassium channel. , 1996, The Journal of physiology.

[6]  H. Wässle,et al.  Distributions of two homologous synaptic vesicle proteins, synaptoporin and synaptophysin, in the mammalian retina , 1996, The Journal of comparative neurology.

[7]  E. A. Schwartz,et al.  Asynchronous transmitter release: control of exocytosis and endocytosis at the salamander rod synapse. , 1996, The Journal of physiology.

[8]  M. Wilkinson,et al.  The dihydropyridine-sensitive calcium channel subtype in cone photoreceptors , 1996, The Journal of general physiology.

[9]  H. Wässle,et al.  The Plasma Membrane Protein SNAP‐25, but not Syntaxin, is Present at Photoreceptor and Bipolar Cell Synapses in the Rat Retina , 1996, The European journal of neuroscience.

[10]  T. Stauffer,et al.  Tissue Distribution of the Four Gene Products of the Plasma Membrane Ca Pump , 1995, The Journal of Biological Chemistry.

[11]  T. Stauffer,et al.  Tissue distribution of the four gene products of the plasma membrane Ca2+ pump. A study using specific antibodies. , 1995, The Journal of biological chemistry.

[12]  S A Lipton,et al.  Multiple GABA receptor subtypes mediate inhibition of calcium influx at rat retinal bipolar cell terminals , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[13]  Gary Matthews,et al.  Calcium dependence of the rate of exocytosis in a synaptic terminal , 1994, Nature.

[14]  E. A. Schwartz,et al.  A cGMP-gated current can control exocytosis at cone synapses , 1994, Neuron.

[15]  H. V. Gersdorff,et al.  Dynamics of synaptic vesicle fusion and membrane retrieval in synaptic terminals , 1994, Nature.

[16]  T. Yagi,et al.  Ionic conductances of monkey solitary cone inner segments. , 1994, Journal of neurophysiology.

[17]  J. T. Penniston,et al.  Immunocytochemical localization of the plasma membrane calcium pump, calbindin-D28k, and parvalbumin in Purkinje cells of avian and mammalian cerebellum. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[18]  M. Tachibana,et al.  Dihydropyridine-sensitive calcium current mediates neurotransmitter release from bipolar cells of the goldfish retina , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[19]  William M. Roberts,et al.  Spatial calcium buffering in saccular hair cells , 1993, Nature.

[20]  Denis A. Baylor,et al.  Synaptic circuitry of the retina and olfactory bulb , 1993, Cell.

[21]  J. T. Penniston,et al.  Use of expression mutants and monoclonal antibodies to map the erythrocyte Ca2+ pump. , 1992, The Journal of biological chemistry.

[22]  E Carafoli,et al.  The Ca2+ pump of the plasma membrane. , 1992, The Journal of biological chemistry.

[23]  G. Matthews,et al.  Calcium influx and calcium current in single synaptic terminals of goldfish retinal bipolar neurons. , 1992, The Journal of physiology.

[24]  J. T. Penniston,et al.  Oxytocin pretreatment of pregnant rat uterus inhibits Ca2+ uptake in plasma membrane and sarcoplasmic reticulum. , 1991, Biochimica et biophysica acta.

[25]  P. Gazzotti,et al.  Partial purification and characterization of the Ca2(+)-pumping ATPase of the liver plasma membrane. , 1990, The Journal of biological chemistry.

[26]  D. Copenhagen,et al.  Release of endogenous excitatory amino acids from turtle photoreceptors , 1989, Nature.

[27]  B. Hille,et al.  Ionic channels of the inner segment of tiger salamander cone photoreceptors , 1989, The Journal of general physiology.

[28]  David Clark,et al.  From East to West , 1989, Nature.

[29]  M. Blaustein.  Calcium transport and buffering in neurons , 1988, Trends in Neurosciences.

[30]  A. V. Maricq,et al.  Calcium and calcium-dependent chloride currents generate action potentials in solitary cone photoreceptors , 1988, Neuron.

[31]  L. Lagnado,et al.  Ion transport by the Na-Ca exchange in isolated rod outer segments. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[32]  R. Fettiplace,et al.  Variation of membrane properties in hair cells isolated from the turtle cochlea. , 1987, The Journal of physiology.

[33]  C. C. Hale,et al.  The stoichiometry of the cardiac sodium-calcium exchange system. , 1984, The Journal of biological chemistry.

[34]  J. T. Penniston,et al.  Purified (Ca2+-Mg2+)-ATPase of the erythrocyte membrane. Reconstitution and effect of calmodulin and phospholipids. , 1981, The Journal of biological chemistry.

[35]  R. Dipolo,et al.  Physiological role of ATP-driven calcium pump in squid axon , 1979, Nature.

[36]  M. Blaustein,et al.  Effects of internal and external cations and of ATP on sodium-calcium and calcium-calcium exchange in squid axons. , 1977, Biophysical journal.

[37]  U. K. Laemmli,et al.  Cleavage of Structural Proteins during the Assembly of the Head of Bacteriophage T4 , 1970, Nature.

[38]  B. Katz,et al.  The timing of calcium action during neuromuscular transmission , 1967, The Journal of physiology.