Cell‐specific expression of plasma membrane calcium ATPase isoforms in retinal neurons

Ca2+ extrusion by high‐affinity plasma membrane calcium ATPases (PMCAs) is a principal mechanism for the clearance of Ca2+ from the cytosol. The PMCA family consists of four isoforms (PMCA1–4). Little is known about the selective expression of these isoforms in brain tissues or about the physiological function conferred upon neurons by any given isoform. We investigated the cellular and subcellular distribution of PMCA isoforms in a mammalian retina. Mouse photoreceptors, cone bipolar cells and horizontal cells, which respond to light with a graded polarization, express isoform 1 (PMCA1) of the PMCA family. PMCA2 is localized to rod bipolar cells, horizontal cells, amacrine cells, and ganglion cells, and PMCA3 is predominantly expressed in spiking neurons, including both amacrine and ganglion cells but is also found in horizontal cells. PMCA4 was found to be selectively expressed in both synaptic layers. Optical measurements of Ca2+ clearance showed that PMCAs mediate Ca2+ extrusion in both rod and cone bipolar cells. In addition, we found that rod bipolar cells, but not cone bipolar cells possess a prominent Na+/Ca2+ exchange mechanism. We conclude that PMCA isoforms are selectively expressed in retinal neurons and that processes of Ca2+ clearance are different in rod and cone bipolar cells. J. Comp. Neurol. 451:1–21, 2002. © 2002 Wiley‐Liss, Inc.

[1]  Z Bajzer,et al.  The Plasma Membrane Calcium Pump Displays Memory of Past Calcium Spikes , 2001, The Journal of Biological Chemistry.

[2]  Peter G. Gillespie,et al.  Plasma Membrane Ca2+-ATPase Isoform 2a Is the PMCA of Hair Bundles , 2001, The Journal of Neuroscience.

[3]  K. Pászty,et al.  Delayed activation of the plasma membrane calcium pump by a sudden increase in Ca2+: fast pumps reside in fast cells. , 2001, Cell calcium.

[4]  S. DeMarco,et al.  Plasma Membrane Ca2+-ATPase Isoforms 2b and 4b Interact Promiscuously and Selectively with Members of the Membrane-associated Guanylate Kinase Family of PDZ (PSD95/Dlg/ZO-1) Domain-containing Proteins* , 2001, The Journal of Biological Chemistry.

[5]  Y. Usachev,et al.  Differentiation induces up‐regulation of plasma membrane Ca2+‐ATPase and concomitant increase in Ca2+ efflux in human neuroblastoma cell line IMR‐32 , 2001, Journal of neurochemistry.

[6]  B. Tempel,et al.  Effects of PMCA2 mutation on DPOAE amplitudes and latencies in deafwaddler mice , 2001, Hearing Research.

[7]  D. Zacharias,et al.  Role of alternative splicing in generating isoform diversity among plasma membrane calcium pumps. , 2001, Physiological reviews.

[8]  M. Berridge,et al.  The versatility and universality of calcium signalling , 2000, Nature Reviews Molecular Cell Biology.

[9]  H. Wässle,et al.  Immunocytochemical analysis of the mouse retina , 2000, The Journal of comparative neurology.

[10]  E. Carafoli,et al.  Calcineurin Controls the Transcription of Na+/Ca2+ Exchanger Isoforms in Developing Cerebellar Neurons* , 2000, The Journal of Biological Chemistry.

[11]  H. Wässle,et al.  Synaptic localization of NMDA receptor subunits in the rat retina , 2000, The Journal of comparative neurology.

[12]  E. F. Stanley,et al.  Location of calcium transporters at presynaptic terminals , 2000, The European journal of neuroscience.

[13]  D. Copenhagen,et al.  Localization and Developmental Expression Patterns of the Neuronal K–Cl Cotransporter (KCC2) in the Rat Retina , 2000, The Journal of Neuroscience.

[14]  P. Witkovsky,et al.  Somatostatin Modulates Voltage-Gated K+ and Ca2+ Currents in Rod and Cone Photoreceptors of the Salamander Retina , 2000, The Journal of Neuroscience.

[15]  Z. Pan,et al.  Differential expression of high- and two types of low-voltage-activated calcium currents in rod and cone bipolar cells of the rat retina. , 2000, Journal of neurophysiology.

[16]  G. Matthews,et al.  The Role of Mitochondria in Presynaptic Calcium Handling at a Ribbon Synapse , 2000, Neuron.

[17]  R. S. St Jules,et al.  L‐type calcium channels in the photoreceptor ribbon synapse: Localization and role in plasticity , 1999, The Journal of comparative neurology.

[18]  E. Strehler,et al.  Plasma membrane calcium ATPases as critical regulators of calcium homeostasis during neuronal cell function. , 1999, Frontiers in bioscience : a journal and virtual library.

[19]  D. Copenhagen,et al.  Caffeine-Sensitive Calcium Stores Regulate Synaptic Transmission from Retinal Rod Photoreceptors , 1999, The Journal of Neuroscience.

[20]  K. Kitamura,et al.  A point mutation in a plasma membrane Ca(2+)-ATPase gene causes deafness in Wriggle Mouse Sagami. , 1999, Biochemical and biophysical research communications.

[21]  D. Copenhagen,et al.  Sodium action potentials are not required for light-evoked release of GABA or glycine from retinal amacrine cells. , 1999, Journal of neurophysiology.

[22]  M. Leist,et al.  The Expression of Plasma Membrane Ca2+ Pump Isoforms in Cerebellar Granule Neurons Is Modulated by Ca2+ * , 1999, The Journal of Biological Chemistry.

[23]  G Falk,et al.  A rise in intracellular Ca2+ underlies light adaptation in dogfish retinal ‘on’ bipolar cells , 1999, The Journal of physiology.

[24]  G. Falk,et al.  A rise in intracellular Ca 2+ underlies light adaptation in dogfish retinal , 1999 .

[25]  C. Klee,et al.  Calcium as a cellular regulator , 1999 .

[26]  H. Wässle,et al.  Immunocytochemical Localization of the Postsynaptic Density Protein PSD-95 in the Mammalian Retina , 1998, The Journal of Neuroscience.

[27]  V. Pickel,et al.  The Localization of the Brain-Specific Inorganic Phosphate Transporter Suggests a Specific Presynaptic Role in Glutamatergic Transmission , 1998, The Journal of Neuroscience.

[28]  J. T. Penniston,et al.  Modulation of the Plasma Membrane Ca2+ Pump , 1998, The Journal of Membrane Biology.

[29]  B. Tempel,et al.  Mutations in a plasma membrane Ca2+-ATPase gene cause deafness in deafwaddler mice , 1998, Nature Genetics.

[30]  T. Doetschman,et al.  Balance and Hearing Deficits in Mice with a Null Mutation in the Gene Encoding Plasma Membrane Ca2+-ATPase Isoform 2* , 1998, The Journal of Biological Chemistry.

[31]  H. Wässle,et al.  GABAA and GABAC receptors on mammalian rod bipolar cells , 1998, The Journal of comparative neurology.

[32]  D. Copenhagen,et al.  Compartmentalization of Calcium Extrusion Mechanisms in the Outer and Inner Segments of Photoreceptors , 1998, Neuron.

[33]  B. Christensen,et al.  Na+/Ca2+exchange in catfish retina horizontal cells: regulation of intracellular Ca2+ store function. , 1998, American journal of physiology. Cell physiology.

[34]  D. Protti,et al.  Calcium Currents and Calcium Signaling in Rod Bipolar Cells of Rat Retinal Slices , 1998, The Journal of Neuroscience.

[35]  D. Guerini.  The significance of the isoforms of plasma membrane calcium ATPase , 1998, Cell and Tissue Research.

[36]  W. R. Taylor,et al.  Calcium Extrusion from Mammalian Photoreceptor Terminals , 1998, The Journal of Neuroscience.

[37]  M. Kavanaugh,et al.  Excitatory Amino Acid Transporters of the Salamander Retina: Identification, Localization, and Function , 1998, The Journal of Neuroscience.

[38]  Daniel Tranchina,et al.  Gain of Rod to Horizontal Cell Synaptic Transfer: Relation to Glutamate Release and a Dihydropyridine-Sensitive Calcium Current , 1997, The Journal of Neuroscience.

[39]  Htet Htet Aung,et al.  Plasma Membrane Ca2+ Pump in Rat Brain , 1997, The Journal of Biological Chemistry.

[40]  M. Masu,et al.  The mGluR6 5′ Upstream Transgene Sequence Directs a Cell-Specific and Developmentally Regulated Expression in Retinal Rod and ON-Type Cone Bipolar Cells , 1997, The Journal of Neuroscience.

[41]  T. Stauffer,et al.  Immunolocalization of the plasma membrane Ca2+ pump isoforms in the rat brain , 1997, Brain Research.

[42]  H. Aung,et al.  Plasma Membrane Ca Pump in Rat Brain PATTERNS OF ALTERNATIVE SPLICES SEEN BY ISOFORM-SPECIFIC ANTIBODIES* , 1997 .

[43]  Helga Kolb,et al.  Amacrine cells of the mammalian retina: Neurocircuitry and functional roles , 1997, Eye.

[44]  Á. Szél,et al.  Distribution of cone photoreceptors in the mammalian retina , 1996, Microscopy research and technique.

[45]  A. G. Filoteo,et al.  Detection of isoform 4 of the plasma membrane calcium pump in human tissues by using isoform-specific monoclonal antibodies. , 1996, The Biochemical journal.

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

[47]  B. Roufogalis,et al.  The plasma membrane calcium pump--a physiological perspective on its regulation. , 1995, Cell calcium.

[48]  H. Wässle,et al.  Immunocytochemical identification of cone bipolar cells in the rat retina , 1995, The Journal of comparative neurology.

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

[50]  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.

[51]  S. Borges,et al.  Electrogenic Na-Ca exchange clears Ca2+ loads from retinal amacrine cells in culture , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[52]  T. Green,et al.  Expression of Recombinant Homo-oligomeric 5-Hydroxytryptamine Receptors Provides New Insights into Their Maturation and Structure (*) , 1995, The Journal of Biological Chemistry.

[53]  Tomomitsu Miyoshi,et al.  Specific deficit of the ON response in visual transmission by targeted disruption of the mGIuR6 gene , 1995, Cell.

[54]  E. Malchiodi,et al.  Localization of the plasma membrane Ca(2+)-ATPase isoform PMCA3 in rat cerebellum, choroid plexus and hippocampus. , 1995, Brain research. Molecular brain research.

[55]  M. Tachibana,et al.  Ca2+ regulation in the presynaptic terminals of goldfish retinal bipolar cells. , 1995, The Journal of physiology.

[56]  S. Borges,et al.  Control of transmitter release from retinal amacrine cells by Ca2+ influx and efflux , 1994, Neuron.

[57]  E. Carafoli,et al.  Cloning and expression of isoform 2 of the human plasma membrane Ca2+ ATPase. Functional properties of the enzyme and its splicing products. , 1994, The Journal of biological chemistry.

[58]  J. I. Korenbrot,et al.  Differences in transduction between rod and cone photoreceptors: an exploration of the role of calcium homeostasis , 1994, Current Opinion in Neurobiology.

[59]  A. Ishida,et al.  Na(+)-Ca2+ exchanger-like immunoreactivity and regulation of intracellular Ca2+ levels in fish retinal ganglion cells. , 1994, Journal of neurophysiology.

[60]  J. Meldolesi,et al.  Molecular and cellular physiology of intracellular calcium stores. , 1994, Physiological reviews.

[61]  M. Engels,et al.  The Psychological Maltreatment Inventory: Development of a Measure of Psychological Maltreatment in Childhood for Use in Adult Clinical Settings , 1994, Psychological reports.

[62]  R. Heim,et al.  The Ca2+ affinity of the plasma membrane Ca2+ pump is controlled by alternative splicing. , 1994, The Journal of biological chemistry.

[63]  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.

[64]  W L Stahl,et al.  Plasma membrane Ca(2+)-ATPase isoforms: distribution of mRNAs in rat brain by in situ hybridization. , 1992, Brain research. Molecular brain research.

[65]  C. D. Benham,et al.  Ca2+ efflux mechanisms following depolarization evoked calcium transients in cultured rat sensory neurones. , 1992, The Journal of physiology.

[66]  J. Hume,et al.  Role of Reverse‐Mode Na+‐Ca2+ Exchange in Excitation‐Contraction Coupling in the Heart a , 1991, Annals of the New York Academy of Sciences.

[67]  M. Tso,et al.  Amelioration of light-induced retinal degeneration by a calcium overload blocker. Flunarizine. , 1991, Archives of ophthalmology.

[68]  E Carafoli,et al.  The calcium pumping ATPase of the plasma membrane. , 1991, Annual review of physiology.

[69]  Ursula Greferath,et al.  Rod bipolar cells in the mammalian retina show protein kinase C‐like immunoreactivity , 1990, The Journal of comparative neurology.

[70]  F. Blachier,et al.  Calbindin and calretinin localization in retina from different species , 1990, Visual Neuroscience.

[71]  D. Copenhagen,et al.  Signal transmission through the dark-adapted retina of the toad (Bufo marinus). Gain, convergence, and signal/noise , 1990, The Journal of general physiology.

[72]  J. Greeb,et al.  Molecular cloning of a third isoform of the calmodulin-sensitive plasma membrane Ca2+-transporting ATPase that is expressed predominantly in brain and skeletal muscle. , 1989, The Journal of biological chemistry.

[73]  K. Negishi,et al.  Dopamine cells and rod bipolar cells contain protein kinase C-like immunoreactivity in some vertebrate retinas , 1988, Neuroscience Letters.

[74]  A Kaneko,et al.  Neuronal architecture of on and off pathways to ganglion cells in carp retina. , 1977, Science.

[75]  Voltage signal of photoreceptors at visual threshold , 1977, Nature.

[76]  J. Dowling,et al.  Organization of the retina of the mudpuppy, Necturus maculosus. II. Intracellular recording. , 1969, Journal of neurophysiology.