Abstract
The ventral photoreceptors ofLimulushave been one of the main preparations for the study of invertebrate phototransduction. The study of ventral photoreceptors has revealed that they have remarkable performance characteristics, most notably the very large amplification of the transduction process. This amplification is critically dependent upon the coupling of photoactivated rhodopsin to the phosphoinositide cascade, resulting in the release of Ca2+from intracellular stores. The consequent elevation of Ca2+within the photoreceptor’s cytosol is amongst the most rapid and dramatic known to be activated by the phosphoinositide cascade. This review summarizes the evidence that intracellular Ca2+is a key regulator of transduction inLimulusphotoreceptors. The mechanisms that regulate Ca2+as well as the possible targets of the action of Ca2+are reviewed. Ca2+elevation is critical for triggering both excitation and adaptation processes in the photoreceptor. The question of how a single second messenger can produce these two opposing effects is of obvious interest and is a topic dealt with throughout this review.
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References
Millecchia R, Mauro A. The ventral photoreceptor cells ofLimulus.II. The basic photoresponse. J Gen Physiol 1969; 54:310–330.
Scott K et al. Gq alpha protein function in vivo: genetic dissection of its role in photoreceptor cell physiology. Neuron 1995; 15:919–927.
Hardie RC, Raghu P. Visual transduction inDrosophila.Nature 2001; 413(6852):186–193.
Lisman JE, Brown JE. Light induced changes of sensitivity inLimulusventral photoreceptors. J Gen Physiol 1975; 66:473–488.
Brown JE, Coles JA. Saturation of the response to light inLimulusventral photoreceptors. J Physiol 1979; 296:373–392.
Brown JE, Blinks JR. Changes in intracellular free calcium concentration during illumination of invertebrate photoreceptors. Detection with aequorin. J Gen Physiol 1974; 64:643–665.
Lisman JE, Brown JE. The effects of intracellular iontophoretic injection of calcium and sodium ions on the light response ofLimulusventral photoreceptors. J Gen Physiol 1972; 59:701–719.
Lisman JE, Brown JE. Effects of intracellular injection of calcium buffers on light adaptation in Limulus ventral photoreceptors. J Gen Physiol 1975; 66:489–506.
Payne R, Corson DW, Fein A. Pressure injection of calcium both excites and adaptsLimulusventral photoreceptors. J Gen Physiol 1986; 88:107–126.
Bolsover SR, Brown JE. Calcium ion, an intracellular messenger of light adaptation, also participates in excitation ofLimulusphotoreceptors. J Physiol Lond 1985; 364:381–393.
Frank TM, Fein A. The role of the inositol phosphate cascade in visual excitation of invertebrate microvillar photoreceptors. J Gen Physiol 1991; 97:697–723.
Shin J, Richard EA, Lisman JE. Cat+is an obligatory intermediate in the excitation cascade ofLimulusphotoreceptors. Neuron 1993; 11:845–855.
Brown JE et al. myo-inositol polyphosphate may be a messenger for visual excitation inLimulusphotoreceptors. Nature 1984; 311:160–163.
Fein A et al. Photoreceptor excitation and adaptation by inositol 1,4,5-trisphosphate. Nature 1984; 311:157–160.
Payne R et al. Excitation and adaptation ofLimulusventral photoreceptors by inositol 1,4,5 triphosphate result from a rise in intracellular calcium. J Gen Physiol 1986; 88:127–142.
Brown JE, Rubin LJ. A direct demonstration that inositol-trisphosphate induces an increase in intracellular calcium inLimulusphotoreceptors. Biochem Biophys Res Commun 1984; 125:1137–1142.
Richard EA, Sampat P, Lisman JE. Distinguishing between roles for calcium inLimulusphotoreceptor excitation. Cell Calcium 1995; 18:331–341.
Payne R. Dynamics of the release of calcium by light and inositol 1,4,5-trisphosphate inLimulusventral photoreceptors. In: Hidalgo C et al, eds. Transduction in Biological Systems. New York: Plenum, 1990:9–25.
Nasi E, del Pilar Gomez M, Payne R. Phototransduction mechanisms in microvillar and ciliary photoreceptors of invertebrates. In: Stavenga DG, de Grip WJ, Pugh EN Jr, eds. Molecular Mechanisms in Visual Transduction. New York: Elsevier Science, 2000:389–448.
Calman BG, Chamberlain SC. Distinct lobes ofLimulusventral photoreceptors. II. Structure and ultrastructure. J Gen Physiol 1982; 80:839–862.
Ukhanov K, Payne R. Light activated calcium release inLimulusventral photoreceptors as revealed by laser confocal microscopy. Cell Calcium 1995; 18:301–313.
Ukhanov KY et al. Measurement of cytosolic Cat+concentration inLimulusventral photoreceptors using fluorescent dyes. J Gen Physiol 1995; 105:95–116.
Payne R, Demas J. Timing of Cat+release from intracellular stores and the electrical response ofLimulusventral photoreceptors to dim flashes. J Gen Physiol 2000; 115(6):735–748.
Allbritton NL, Meyer T, Stryer L. Range of messenger action of calcium ion and inositol 1,4,5- trisphosphate. Science 1992; 258(5089):1812–1815.
Payne R, Fein A. Localized adaptation within the rhabdomeral lobe ofLimulusventral photoreceptors. J Gen Physiol 1983; 81(5):767–769.
Feng JJ et al. Three-dimensional organization of endoplasmic reticulum in the ventral photoreceptors ofLimulus.J Comp Neurol 1994; 341(2):172–183.
Payne R et al. The localization of calcium release by inositol trisphosphate inLimulusphotoreceptors and its control by negative feedback. Philos Trans R Soc Lond B Biol Sci 1988; 320:359–379.
Ukhanov K et al. Putative inositol 1,4,5-trisphosphate receptor localized to endoplasmic reticulum inLimulusphotoreceptors. Neuroscience 1998; 86(1):23–28.
Ukhanov K, Payne R. Rapid coupling of calcium release to depolarization inLimuluspolyphemus ventral photoreceptors as revealed by microphotolysis and confocal microscopy. J Neurosci 1997; 17:1701–1709.
Dorlochter M, Yuan W, Stieve H. Effects of calcium and cyclopiazonic acid on the photoresponse in theLimulusventral photoreceptor. Zeitschrift fur Naturforschung 1999; 54c:446–455.
Maaz G, Stieve H. The correlation of the receptor potential with the light induced transient increase in intracellular calcium-concentration measured by absorption change of arsenazo III injected intoLimulusventral nerve photoreceptor cell. Biophys Struct Mech 1980; 6:191–208.
Payne R, Flores TM, Fein A. Feedback inhibition by calcium limits the release of calcium by inositol trisphosphate inLimulusventral photoreceptors. Neuron 1990; 4(4):547–55.
Payne R, Potter BV. Injection of inositol trisphosphorothioate intoLimulusventral photoreceptors causes oscillations of free cytosolic calcium. J Gen Physiol 1991; 97:1165–1186.
Levy S, Payne R. A lingering elevation of Ca, accompanies inhibition of inositol 1,4,5 trisphosphate-induced Ca release inLimulusventral photoreceptors. J Gen Physiol 1993; 101:67–84.
Levitan I, Hillman P, Payne R. Fast desensitization of the response to InsP3 inLimulusventral photoreceptors. Biophys J 1993; 64:1354–1360.
Bezprozvanny I, Watras J, Ehrlich BE. Bell-shaped calcium-response curves of Ins(1,4,5)P3and calcium-gated channels from endoplasmic reticulum of cerebellum. Nature 1991; 351:751–754.
Levitan I et al. Facilitation of the responses to injections of inositol 1,4,5-trisphosphate analogs inLimulusventral photoreceptors. Biophysical Journal 1994; 67:1161–1172.
Keizer J et al. InsP3-induced Ca2+excitability of the endoplasmic reticulum. Mol Biol Cell 1995; 6(8):945–951.
Wood SF, Szuts EZ, Fein A. Metabolism of inositol 1,4,5-trisphosphate in squid photoreceptors. J Comp Physiol [B] 1990; 160(3):293–298.
Vallet AM, Fein A. A role for hydrolysis of inositol 1,4,5-trisphosphate in terminating the response to inositol 1,4,5-trisphosphate and to a flash of light inLimulusventral photoreceptors. Brain Res 1997; 768:91–101.
O’Day PM, Gray-Keller MP. Evidence for electrogenic Na+/Ca2+exchange inLimulusventral photoreceptors. J Gen Physiol 1989; 93:473–494.
Battelle BA et al. Immunocytochemical localization of opsin, visual arrestin, myosin III, and calmodulin inLimuluslateral eye retinular cells and ventral photoreceptors. J Comp Neurol 2001; 435(2):211–225.
Fein A, Tsacopoulos M. Activation of mitochondrial oxidative metabolism by calcium ions inLimulusventral photoreceptor. Nature 1988; 331:437–440.
Decked A, Stieve H. Electrogenic Na(+)-Ca2+exchanger, the link between intra-and extra-cellular calcium in theLimulusventral photoreceptor. J Physiol Lond 1991; 433:467–482.
Lisman JE. Effects of removing extracellular Ca2+on excitation and adaptation inLimulusventral photoreceptors. Biophys J 1976; 16:1331–1335.
Lisman JE, Fain GL, O’Day PM. Voltage-dependent conductances inLimulusventral photoreceptors. J Gen Physiol 1982; 79:187–209.
Hsiao HS, Payne R. Light-induced Mn2+influx inLimulusventral photoreceptors. J Comp Physiol [A] 1998; 183(2):193–202.
Brown JE, Mote MI. Ionic dependence of reversal voltage of the light response inLimulusventral photoreceptors. J Gen Physiol 1974; 63(3):337–350.
Hardie RC, Minke B. Thetipgene is essential for a light-activated Ca2+channel inDrosophilaphotoreceptors. Neuron 1992; 8:643–651.
Levy S, Fein A. Relationship between light sensitivity and intracellular free Ca concentration inLimulusventral photoreceptors. A quantitative study using Ca-selective microelectrodes. J Gen Physiol 1985; 85:805–841.
Richard EA et al. Cat+/calmodulin-binding peptides block phototransduction inLimulusventral photoreceptors: Evidence for direct inhibition of phospholipase C. Proc Natl Acad Sci USA 1997; 94:14095–14099.
Payne R, Flores TM. The latency of the response ofLimulusphotoreceptors to inositol trisphosphate lacks the calcium-sensitivity of that to light. J Comp Physiol A 1992; 170:311–316.
Stieve H, Benner S. The light-induced rise in cytosolic calcium starts later than the receptor current of theLimulusventral photoreceptor. Vision Research 1992; 32:403–416.
O’Day PM, Lisman JE, Goldring M. Functional significance of voltage-dependent conductances inLimulusventral photoreceptors. J Gen Physiol 1982; 79:211–232.
Stommel G et al. The light-stimulated cytosolic calcium transient inLimulusventral nerve photoreceptors: two components in the rising phase. Z Naturforsch [C] 1996; 51(1–2):101–112.
Faddis MN, Brown JE. Intracellular injection of heparin and polyamines. Effects on phototransduction inLimulusventral photoreceptors. J Gen Physiol 1993; 101:909–931.
Nagy K, Contzen K. Inhibition of phospholipase C by U-73122 blocks one component of the receptor current inLimulusphotoreceptor. Vis Neurosci 1997; 14:995–998.
Johnson EC, Gray-Keller MP, O’Day PM. Rescue of excitation by inositol following Lit induced block inLimulusventral photoreceptors. Vis Neurosci 1998; 15(1):105–112.
Bacigalupo J, Lisman JE. Single-channel currents activated by light inLimulusventral photoreceptors. Nature 1983; 304:268–270.
Bacigalupo J, Chinn K, Lisman JE. Ion channels activated by light inLimulusventral photoreceptors. J Gen Physiol 1986; 87:73–89.
Bacigalupo J et al. Light-dependent channels from excised patches ofLimulusventral photoreceptors are opened by cGMP. Proc Natl Acad Sci USA 1991; 88:7938–7942.
Nagy K. Inhibition of the first component of the receptor current inLimulusphotoreceptor. Neuroreport 1994; 5:847–849.
Johnson EC, Robinson PR, Lisman JE. Cyclic GMP is involved in the excitation of invertebrate photoreceptors. Nature 1986; 324:468–470.
Feng JJ, Frank TM, Fein A. Excitation ofLimulusphotoreceptors by hydrolysis-resistant analogs of cGMP and cAMP. Brain Res 1991; 552:291–294.
Brown JE, Kaupp UB, Malbon CC. 3’,5’-cyclic adenosine monophosphate and adenylate cyclase in phototransduction byLimulusventral photoreceptors. J Physiol 1984; 353:523–539.
Johnson EC, O’Day PM. Inhibitors of cyclic-GMP phosphodiesterase alter excitation ofLimulusventral photoreceptors in Cat+-dependent fashion. J Neurosci 1995; 15:6586–6591.
Chen FH et al. A cGMP-gated channel subunit inLimulusphotoreceptors. Visual Neuroscience 2001; 18(4):517–526.
Garger A, Richard EA, Lisman JE. Inhibitors of guanylate cyclase inhibit phototransduction inLimulusphotoreceptors. Visual Neuroscience 2001; 18(4):625–632.
Schmidt JA, Farber DB. Light-induced changes in cAMP levels inLimulusphotoreceptors. Biochem Biophys Res Commun 1980; 94(2):438–42.
Brown JE, Faddis M, Combs A. Light does not induce an increase in cyclic-GMP content of squid orLimulusphotoreceptors. Exp Eye Res 1992; 54:403–410.
Dorlochter MdeVente J. Cyclic GMP in lateral eyes of the horseshoe crab Limulus.Vision Res 2000; 40(27):3677–3684.
Gillespie PG, Beavo JA. cGMP is tightly bound to bovine retinal rod phosphodiesterase. Proc Natl Acad Sci USA 1989; 86:4311–4315.
Gorczyca WA et al. Purification and physiological evaluation of a guanylate cyclase activating protein from retinal rods. Proc Nati Acad Sci USA 1994; 91(9):4014–4018.
Palczewski K et al. Molecular cloning and characterization of retinal photoreceptor guanylyl cyclase-activating protein. Neuron 1994; 13(2):395–404.
Dizhoor AM et al. Cloning, sequencing, and expression of a 24-kDa Ca2+-binding protein activating photoreceptor guanylyl cyclase. J Biol Chem 1995; 270(42):25200–25206.
Pozdnyakov N et al. A novel calcium-dependent activator of retinal rod outer segment membrane guanylate cyclase. Biochemistry 1995; 34(44):14279–14283.
Schultz JE, Klumpp S. Lanthanum dissociates calmodulin from the guanylate cyclase of the excitable ciliary membrane fromParamecium.FEMS Microbiol Letts 1982; 13:303–306.
Klumpp S, Schultz JE. Characterization of a Ca2+-dependent guanylate cyclase in the excitable ciliary membrane fromParamecium.Eur J Biochem 1982; 124:317–324.
Estacion M, Sinkins WG, Schilling WP. Regulation ofDrosophilatransient receptor potential-like (TrpL) channels by phospholipase C-dependent mechanisms. J Physiol 2001; 530(Pt 1):1–19.
Chyb S, Raghu P, Hardie RC. Polyunsaturated fatty acids activate theDrosophilalight-sensitive channels TRP and TRPL. Nature 1999; 397:255–259.
Fein A, Cavar S. Divergent mechanisms for phototransduction of invertebrate microvillar photoreceptors. Vis Neurosci 2000; 17(6):911–917.
Brown JE, Lisman JE. An electrogenic sodium pump inLimulusventral photoreceptor cells. J Gen Physiol 1972; 59:720–733.
Fuortes MGF, Hodgkin AL. Changes in time scale and sensitivity in the ommatidia ofLimulus.J Physiol 1964; 172:239–263.
Lisman JE, Bering H. Electrophysiological measurement of the number of rhodopsin molecules in singleLimulusphotoreceptors. J Gen Physiol 1977; 70:621–633.
Lisman JE. An electrophysiological investigation of the ventral eye of the horseshoe crabLimulus polyphemus.[Ph.D.]. Massachusetts Institute of Technology, 1971.
Payne R, Fein A. Inositol 1,4,5 trisphosphate releases calcium from specialized sites withinLimulussphotoreceptors. J Cell Biol 1987; 104:933–937.
Adler EM et al. Alien intracellular calcium chelators attenuate neurotransmitter release at the squid giant synapse. J Neurosci 1991; 11:1496–1507.
Naraghi M, Neher E. Linearizedbu ffered Ca2+diffusion in microdomains and its implications for calculation of [Ca2+] at the mouth of a calcium channel. J Neurosci 1997; 17(18):6961–6973.
Grzywacz NM, Hillman P, Knight BW. Response transfer functions ofLimulusventral photoreceptors: Interpretation in terms of transduction mechanisms. Biol.Cybern. 1992; 66:429–435.
Anion A et al. Calmodulin regulation of light adaptation and store-operated dark current inDrosophilaphotoreceptors. Proc Natl Acad Sci USA 1997; 94:5894–5899.
Scott K et al. Calmodulin regulation ofDrosophilalight-activated channels and receptor function mediates termination of the light response in vivo. Cell 1997; 91:375–383.
Hardie RC et al. Ca2+limits the development of the light response inDrosophilaphotoreceptors. Proc R Soc Lond B Biol Sci 1993; 252:223–229.
Smith DP et al. Photoreceptor deactivation and retinal degeneration mediated by a photoreceptor-specific protein kinase C. Science 1991; 254:1478–1484.
Richard EA, Lisman JE. Rhodopsin inactivation is a modulated process inLimulusphotoreceptors. Nature 1992; 356:336–338.
Calman BG et al. Calcium/calmodulin-dependent protein kinase II and arrestin phosphorylation inLimuluseyes. J Photochem Photobiol B Biol 1996; 35:33–44.
Ellis DZ, Edwards SC. Characterization of a calcium/calmodulin-dependent protein phosphatase in theLimulusnervous tissue and its light regulation in the lateral eye. Vis Neurosci 1994; 11:851–860.
Kass L et al. Inhibition of the calcineurin-like protein phosphatase activity inLimulusventral eye photoreceptor cells alters the characteristics of the spontaneous quantal bumps and the light-mediated inward currents, and enhances arrestin phosphorylation. Vis Neurosci 1998; 15(6):1039–1049.
Kass L, Bray WO. Kinetic model for phototransduction and G-protein enzyme cascade: Understanding quantal bumps during inhibition of CaM-KII or PP2B. J Photochem Photobiol B 1996; 35(1–2):105–113.
Dabdoub A, Payne R. Protein kinase C activators inhibit the visual cascade inLimulusventral photoreceptors at an early stage. J Neurosci 1999; 19:10262–10269.
Herman KG. Light-stimulated rhabdom turnover inLimulusventral photoreceptors maintained in vitro. J Comp Neurol 1991; 303(1):11–21.
Jinks RN, White RH, Chamberlain SC. Dawn, diacylglycerol, calcium, and protein kinase C—The retinal wrecking crew. A signal transduction cascade for rhabdom shedding in theLimulus eye.J Photochem Photobiol B 1996; 35:45–52.
Corson DW, Fein A. Inositol 1,4,5-trisphosphate induces bursts of calcium release insideLimulusventral photoreceptors. Brain Res 1987; 423:343–346.
Hardie RC. Photolysis of caged Cat+facilitates and inactivates but does not directly excite light-sensitive channels inDrosophilaphotoreceptors. J Neurosci 1995; 15:889–902.
Acharya JK et al. InsP3 receptor is essential for growth and differentiation but not for vision inDrosophila.Neuron 1997; 18:881–887.
Ranganathan R et al. ADrosophilamutant defective in extracellular calcium-dependent photoreceptor deactivation and rapid desensitization. Nature 1991; 354:230–232.
Hardie RC. Whole-cell recordings of the light induced current in dissociatedDrosophilaphotoreceptors: evidence for feedback by calcium permeating the light-sensitive channels. Proc R Soc Lond B 1991; 245:203–210.
Matsumoto H et al. Phosrestin I undergoes the earliest light-induced phosphorylation by a calcium/calmodulin-dependent protein kinase inDrosophilaphotoreceptors. Neuron 1994; 12:997–1010.
Dabdoub A, Payne R, Jinks RN. Protein kinase C-induced disorganization and endocytosis of photosensitive membrane inLimulusventral photoreceptors. J Comp Neurol 2002; 442:217–225.
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Lisman, J.E., Richard, E.A., Raghavachari, S., Payne, R. (2002). Simultaneous Roles for Ca2+ in Excitation and Adaptation of Limulus Ventral Photoreceptors. In: Baehr, W., Palczewski, K. (eds) Photoreceptors and Calcium. Advances in Experimental Medicine and Biology, vol 514. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-0121-3_31
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