InsP3-induced Ca2+release in permeabilized invertebrate photoreceptors: a link between phototransduction and Ca2+stores

Abstract Using the low-affinity fluorescent Ca 2+ indicators, Mag-Fura-2 and Mag-Fura Red, we studied light- and InsP 3 -induced Ca 2+ release in permeabilized microvillar photoreceptors of the medicinal leech, Hirudo medicinalis . Two major components of the phosphoinositide signaling pathway, phospholipase-C and the InsP 3 receptor, were characterized immunologically and appropriately localized in photoreceptors. Whereas phospholipase-C was abudantly expressed in photoreceptive microvilli, InsP 3 receptors were found mostly in submicrovillar endoplasmic reticulum (SER). Permeabilization of the peripheral plasma membrane with saponin allowed direct measurements of luminal free Ca 2+ concentration (Ca L ) changes. Confocal Ca 2+ imaging using Mag-Fura Red demonstrated that Ins(1,4,5)P 3 mobilizes Ca 2+ from SER. As detected with Mag-Fura-2, a brief 50ms light flash activated rapid Ca 2+ depletion of SER, followed by an effective refilling within 1min of dark adaptation after the light flash. Sensitivity to Ins(1,4,5)P 3 of the Ca 2+ release from SER in leech photoreceptors was accompanied by irreversible uncoupling of phototransduction from Ca 2+ release. Depletion of Ca 2+ stores was induced by Ins(1,4,5)P 3 (EC 50 = 4.75 μM) and the hyper-potent agonist adenophostin A (EC 50 /40nM) while the stereoisomer L -myo Ins(1,4,5)P 3 was totally inactive. Ins(1,4,5)P 3 - or adenophostin A-induced Ca 2+ release was inhibited by 0.1–1mg/ml heparin. The Ca 2+ pump inhibitors, cyclopiazonic acid and thapsigargin, in the presence of Ins(1,4,5)P 3 , completely depleted Ca 2+ stores in leech photoreceptors.

[1]  K. Ukhanov,et al.  The phosphoinositide signaling cascade is involved in photoreception in the leech Hirudo medicinalis , 2001, Journal of Comparative Physiology A.

[2]  K. Ukhanov,et al.  Actions of neomycin on electrical light responses, Ca2+ release, and intracellular Ca2+ changes in photoreceptors of the honeybee drone , 2000, Journal of Comparative Physiology A.

[3]  R. Hardie,et al.  Normal Phototransduction in Drosophila Photoreceptors Lacking an InsP3 Receptor Gene , 2000, Molecular and Cellular Neuroscience.

[4]  A. M. Riley,et al.  Synthesis of adenophostin A and congeners modified at glucose , 2000 .

[5]  K. Mikoshiba,et al.  Inositol 1,4,5-trisphosphate receptors are strongly expressed in the nervous system, pharynx, intestine, gonad and excretory cell of Caenorhabditis elegans and are encoded by a single gene (itr-1). , 1999, Journal of molecular biology.

[6]  K. Nagy,et al.  Photoreceptor cells with unusual functional properties on the ventral nerve of Limulus , 1999, Visual Neuroscience.

[7]  Roger C. Hardie,et al.  Polyunsaturated fatty acids activate the Drosophila light-sensitive channels TRP and TRPL , 1999, Nature.

[8]  T. Miyata,et al.  Phospholipase C cDNAs from sponge and hydra: antiquity of genes involved in the inositol phospholipid signaling pathway 1 , 1998, FEBS letters.

[9]  C. Taylor,et al.  Rapid activation and partial inactivation of inositol trisphosphate receptors by inositol trisphosphate. , 1998, Biochemistry.

[10]  T. Yoshioka,et al.  Evidence for the Involvement of Inositol Trisphosphate but Not Cyclic Nucleotides in Visual Transduction in HermissendaEye* , 1998, The Journal of Biological Chemistry.

[11]  Doekele G. Stavenga,et al.  Light Dependence of Calcium and Membrane Potential Measured in Blowfly Photoreceptors In Vivo , 1998, The Journal of general physiology.

[12]  B. Walz,et al.  Pleated septate junctions in leech photoreceptors: ultrastructure, arrangement of septa, gate and fence functions , 1998, Cell and Tissue Research.

[13]  Maria del Pilar Gomez,et al.  Membrane Current Induced by Protein Kinase C Activators in Rhabdomeric Photoreceptors: Implications for Visual Excitation , 1998, The Journal of Neuroscience.

[14]  K. Mikoshiba,et al.  Apical Vesicles Bearing Inositol 1,4,5-trisphosphate Receptors in the Ca2+Initiation Site of Ductal Epithelium of Submandibular Gland , 1998, The Journal of cell biology.

[15]  A. Tanimura,et al.  Imaging of calcium release in inositol 1,4,5-trisphosphate-sensitive internal stores in permeabilized HSY cells using fluorescent indicators. , 1998, Cell structure and function.

[16]  J. Meldolesi,et al.  The endoplasmic reticulum Ca2+ store: a view from the lumen. , 1998, Trends in biochemical sciences.

[17]  Marlies Dorlöchter,et al.  The Limulus ventral photoreceptor: Light response and the role of calcium in a classic preparation , 1997, Progress in Neurobiology.

[18]  A. M. Riley,et al.  Structural analogues of D-myo-inositol-1,4,5-trisphosphate and adenophostin A: recognition by cerebellar and platelet inositol-1,4,5-trisphosphate receptors. , 1997, Molecular pharmacology.

[19]  Colin W. Taylor,et al.  Cooperative activation of IP3 receptors by sequential binding of IP3 and Ca2+ safeguards against spontaneous activity , 1997, Current Biology.

[20]  B. Potter,et al.  Adenophostin A Can Stimulate Ca2+ Influx without Depleting the Inositol 1,4,5-Trisphosphate-sensitive Ca2+ Stores in the Xenopus Oocyte* , 1997, The Journal of Biological Chemistry.

[21]  R. Payne,et al.  Rapid Coupling of Calcium Release to Depolarization inLimulus polyphemus Ventral Photoreceptors as Revealed by Microphotolysis and Confocal Microscopy , 1997, The Journal of Neuroscience.

[22]  B. Potter,et al.  Synthesis of the enantiomers of myo-inositol 1,2,4,5-tetrakisphosphate, a regioisomer of myo-inositol 1,3,4,5-tetrakisphosphate , 1997 .

[23]  S. Muallem,et al.  Spacial Compartmentalization of Ca2+ Signaling Complexes in Pancreatic Acini* , 1996, The Journal of Biological Chemistry.

[24]  J Bhatia,et al.  Rhodopsin, Gq and phospholipase C activation in cephalopod photoreceptors. , 1996, Journal of photochemistry and photobiology. B, Biology.

[25]  R. Payne,et al.  Light activated calcium release in Limulus ventral photoreceptors as revealed by laser confocal microscopy. , 1995, Cell calcium.

[26]  Tatsuo Suzuki,et al.  Phosphatidyl inositol-phospholipase C in squid photoreceptor membrane is activated by stable metarhodopsin via GTP-binding protein, Gq , 1995, Vision Research.

[27]  B. Walz,et al.  Caffeine- and ryanodine-sensitive Ca(2+)-induced Ca2+ release from the endoplasmic reticulum in honeybee photoreceptors , 1995, The Journal of general physiology.

[28]  T. Takasawa,et al.  Biosynthesis of (+)-cubenene and (+)-epicubenol by cell-free extracts of cultured cells of Heteroscyphus planus and cyclization of [^2H]farnesyl diphosphates , 1995 .

[29]  C. Zuker,et al.  Signal transduction in Drosophila photoreceptors. , 1995, Annual review of neuroscience.

[30]  D L Alkon,et al.  Induction of photoresponse by the hydrolysis of polyphosphoinositides in the Hermissenda type B photoreceptor. , 1994, Biochemical and biophysical research communications.

[31]  J. Lisman,et al.  Ca2+ is an obligatory intermediate in the excitation cascade of limulus photoreceptors , 1993, Neuron.

[32]  P A Ferreira,et al.  Distinctive subtypes of bovine phospholipase C that have preferential expression in the retina and high homology to the norpA gene product of Drosophila. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[33]  J. Brown,et al.  Intracellular injection of heparin and polyamines. Effects on phototransduction in limulus ventral photoreceptors , 1993, The Journal of general physiology.

[34]  K. Mikoshiba,et al.  Molecular cloning and characterization of the inositol 1,4,5-trisphosphate receptor in Drosophila melanogaster. , 1992, The Journal of biological chemistry.

[35]  T. Frank,et al.  The role of the inositol phosphate cascade in visual excitation of invertebrate microvillar photoreceptors , 1991, The Journal of general physiology.

[36]  R. Payne.  Dynamics of the Release of Calcium by Light and Inositol 1,4,5-Trisphosphate in Limulus Ventral Photoreceptors , 1990 .

[37]  E. Z. Szuts,et al.  Inositol trisphosphate production in squid photoreceptors. Activation by light, aluminum fluoride, and guanine nucleotides. , 1989, The Journal of biological chemistry.

[38]  B. T. Bloomquist,et al.  Isolation of a putative phospholipase c gene of drosophila, norpA, and its role in phototransduction , 1988, Cell.

[39]  M. Berridge,et al.  Excitation and adaptation of Limulus ventral photoreceptors by inositol 1,4,5 triphosphate result from a rise in intracellular calcium , 1986, The Journal of general physiology.

[40]  R. Payne,et al.  Pressure injection of calcium both excites and adapts Limulus ventral photoreceptors , 1986, The Journal of general physiology.

[41]  Joel E. Brown,et al.  myo-inositol polyphosphate may be a messenger for visual excitation in Limulus photoreceptors , 1984, Nature.

[42]  B. Walz.  Ca2+-sequestering smooth endoplasmic reticulum in an invertebrate photoreceptor. I. Intracellular topography as revealed by OsFeCN staining and in situ Ca accumulation , 1982, The Journal of cell biology.

[43]  B. Walz.  Ca2+-sequestering smooth endoplasmic reticulum in an invertebrate photoreceptor. II. Its properties as revealed by microphotometric measurements , 1982, The Journal of cell biology.

[44]  B. Walz.  Subcellular calcium localization and AT0-dependent Ca2+-uptake by smooth endoplasmic reticulum in an invertebrate photoreceptor cell. An ultrastrucutral, cytochemical and X-ray microanalytical study. , 1979, European journal of cell biology.