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Calcium uptake by smooth endoplasmic reticulum of peeled retinal photoreceptors of the crayfish

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Summary

The localization and basic properties of Ca2+-accumulating sites in crayfish photoreceptors were studied with a novel preparation of peeled retinula cells in suspension. Peeled photoreceptors were obtained by gentle mechanical disruption of the retina, and incubated in media based on a Ca2+-EGTA buffer with ATP and oxalate. Electron microscopy of photoreceptors so treated showed the appearance of peculiar dense deposits inside vesicles of smooth endoplasmic reticulum (SER). EGTA-extraction and energy-dispersive X-ray microanalysis identified Ca as a major constituent of such deposits.45Ca2+ uptake experiments with peeled photoreceptors or with the crude particulate fraction of retinal homogenates revealed a rapid binding of radioactivity over the first 8 min, followed by a slower continued accumulation, which did not occur in the absence of ATP.45Ca2+ uptake is stimulated by an increase in the concentration of free Ca over the range 4×10−7 to 5×10−6 M, and becomes inhibited at higher levels.45Ca2+ uptake is depressed when K+ is replaced by Na+ or Li+ as the main monovalent cation in the medium, but it is not affected by illumination nor by the presence of caffeine or ruthenium red. These findings attest that the SER has a Na+-sensitive capacity for regulating the intracellular concentration of Ca2+ in these photoreceptors, and support the hypothesis of its probable role in the control of pigment granule transport and other structural changes involved in light/dark adaptation.

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References

  • Abercrombie RF, Masukawa LM, Sjodin RA, Livengood D (1981) Uptake and release of45Ca byMyxicola axoplasm. J Gen Physiol 78:413–429

    Google Scholar 

  • Ali MA (1971) Les responses rétinomotrices: caractères et méchanismes. Vision Res 11:1225–1288

    Google Scholar 

  • Bader CR, Bauman F, Bertrand D (1976) Role of intracellular calcium and sodium in light-adaptation in the retina of the honey bee drone (Apis mellifera L.). J Gen Physiol 67:475–491

    Google Scholar 

  • Behrens M, Krebs W (1976) The effect of light-dark adaptation on the ultrastructure ofLimulus lateral eye retinular cells. J Comp Physiol 107:77–96

    Google Scholar 

  • Bernhards H (1916) Der Bau des Komplexauges vonAstacus fluviatilis (Potamobius astacus L.). Z Wiss Zool 116:649–707

    Google Scholar 

  • Burnside B, Basinger S (1983) Retinomotor pigment migration in the teleost retinal pigment epithelium. II. Cyclic-3′,5′adenosine monophosphate induction of dark-adaptive movement in vitro. Invest Ophthalmol Visual Sci 24:16–22

    Google Scholar 

  • Burnside B, Smith B, Nagata M, Porrello K (1982) Reactivation of contraction in detergent-lysed teleost retinal cones. J Cell Biol 92:199–206

    Google Scholar 

  • Burton PR, Laveri LA (1985) The distribution, relationships to other organelles, and calcium-sequestering ability of smooth endoplasmic reticulum in frog olfactory axons. J Neurosci 5:3047–3060

    Google Scholar 

  • Chan SY, Ochs S, Worth RM (1980) The requirement for calcium ions and the effect of other ions on axoplasmic transport in mammalian nerve. J Physiol (Lond) 301:477–504

    Google Scholar 

  • Chan SY, Ochs S, Jersild RA (1984) Localization of calcium in nerve fibers. J Neurobiol 15:89–108

    Google Scholar 

  • Coles JA, Rick R (1985) An electron microprobe analysis of photoreceptors and outer pigment cells in the retina of the honeybee drone. J Comp Physiol A 156:213–222

    Google Scholar 

  • Donaldson SKB (1985) Peeled mammalian skeletal muscle fibers. Possible stimulation of Ca2+ release via a transverse tubule-sarcoplasmic reticulum mechanism. J Gen Physiol 86:501–526

    Google Scholar 

  • Duce IR, Keen P (1978) Can neuronal smooth endoplasmic reticulum function as a calcium reservoir? Neuroscience 3:837–848

    Google Scholar 

  • Eguchi E, Waterman T (1967) Changes in retinal fine structure induced in the crabLibinia by light and dark adaptation. Z Zellforsch 79:209–229

    Google Scholar 

  • Eroglu L, Keen P (1977) Active uptake of45Ca by a microsomal fraction prepared from rat dorsal roots. J Neurochem 29:905–909

    Google Scholar 

  • Fahrenbach W (1975) The visual system of the horseshoe crabLimulus polyphemus. Int Rev Cytol 41:285–349

    Google Scholar 

  • Frixione E (1983a) The microtubular system of the crayfish retinula cells and its changes in relation to screening pigment migration. Cell Tissue Res 232:335–348

    Google Scholar 

  • Frixione E (1983b) Firm structural associations of migratory pigment granules with microtubules in crayfish retinula cells. J Cell Biol 96:1258–1265

    Google Scholar 

  • Frixione E, Aréchiga H (1981) Ionic dependence of screening pigment migrations in crayfish retinal photoreceptors. J Comp Physiol 144:35–43

    Google Scholar 

  • Frixione E, Porter RM (1986) Volume and surface changes of smooth endoplasmic reticulum in crayfish retinula cells upon light- and dark-adaptation. J Comp Physiol A 159:667–674

    Google Scholar 

  • Frixione E, Aréchiga H, Tsutsumi V (1979) Photomechanical migrations of pigment granules along the retinula cells of the crayfish. J Neurobiol 10:573–590

    Google Scholar 

  • Henkart MP (1980) Identification and function of intracellular calcium stores in neurons. Fed Proc 39:2776–2814

    Google Scholar 

  • Hitchcock SE (1977) Regulation of motility in non muscle cells. J Cell Biol 74:1–15

    Google Scholar 

  • Horridge GA, Barnard PB (1965) Movement of palisade in locust retinula cells when illuminated. Q J Microsc Sci 106:131–135

    Google Scholar 

  • Kanje M, Edström A, Ekström P (1982) The role of Ca2+ in rapid axonal transport. In: Weiss D (ed) Axoplasmic transport. Springer, Berlin Heidelberg New York, pp 294–300

    Google Scholar 

  • Kirschfeld K, Vogt V (1980) Calcium ions and pigment migration in fly photoreceptors. Naturwissenschaften 67:516–517

    Google Scholar 

  • Krebs W (1972) The fine structure of the retinula of the compound eye ofAstacus fluviatilis. Z Zellforsch 133:399–414

    Google Scholar 

  • Lavoie PA, Bolen F, Hammerschlag R (1979) Divalent cation specificity of the calcium requirement for fast transport of proteins in axons of desheathed nerves. J Neurochem 32:1745–1751

    Google Scholar 

  • Lieberman EM, Palmer RF, Collins GH (1967) Calcium ion uptake by crustacean peripheral nerve subcellular particles. Exp Cell Res 46:412–418

    Google Scholar 

  • Lisman JE, Brown JE (1972) The effects of intracellular iontophoretic injection of calcium and sodium ions on the light response ofLimulus ventral photoreceptors. J Gen Physiol 59:701–719

    Google Scholar 

  • Luby-Phelps K, Porter KR (1982) The control of pigment migration in isolated erythrophores ofHolocentrus ascensionis (Osbeck). II. The role of calcium. Cell 29:441–450

    Google Scholar 

  • Moore CL (1971) Specific inhibition of mitochondrial Ca++ transport by ruthenium red. Biochem Biophys Res Comm 42:298–305

    Google Scholar 

  • Ochs S, Worth RM, Chan SY (1977) Calcium requirement for axoplasmic transport in mammalian nerve. Nature 270:748–750

    Google Scholar 

  • Parker GH (1895) The retina and optic ganglia in Decapods, especially inAstacus. Mitt Zool Stat Neapel 12:1–73

    Google Scholar 

  • Payne R, Fein A (1987) Inositol 1, 4, 5 triphosphate releases calcium from specialized sites withinLimulus photoreceptors. J Cell Biol 104:933–937

    Google Scholar 

  • Perrelet A, Bader CR (1978) Morphological evidence for Ca++ stores in the retina of honeybee drones. J Ultrastruct Res 63:237–243

    Google Scholar 

  • Röhlich P, Török LJ (1962) The effect of light and darkness on the fine structure of the retinal clubs ofDendrocoelum lacteum. Q J Microsc Sci 103:543–548

    Google Scholar 

  • Ruiz L, Frixione E (1985) Compartamentalización intracelular de calcio en fotorreceptores retinales de crustáceo. Res Congr Nac Ciencias Fisiol, México, p 147a

  • Schröder W, Frings D, Stieve H (1980) Measuring calcium uptake and release by invertebrate photoreceptor cells by laser microprobe mass spectroscopy. Scanning Electron Microsc II:647–656

    Google Scholar 

  • Snyder AW, Horridge GA (1972) The optical function of changes in the medium surrounding the cockroach rhabdom. J Comp Physiol 81:1–8

    Google Scholar 

  • Snyder WZ, Zadunaisky JA (1976) A role for calcium in the migration of retinal screening pigment in the frog. Exp Eye Res 22:377–388

    Google Scholar 

  • Somlyo AP (1984) Cellular site of calcium regulation. Nature 309:516–517

    Google Scholar 

  • Somlyo AP, Walz B (1985) Elemental distribution inRana pipiens retinal rods: quantitative electron probe analysis. J Physiol (Lond) 358:183–196

    Google Scholar 

  • Sommer JR, Wallace NR, Junker J (1980) The intermediate cisterna of the sarcoplasmic reticulum of skeletal muscle. J Ultrastruct Res 71:126–142

    Google Scholar 

  • Stearns ME, Ochs RL (1982) A functional in vitro model for studies of intracellular motility in digitonin-permeabilized erythrophores. J Cell Biol 94:727–739

    Google Scholar 

  • Tsutsumi V, Frixione E, Aréchiga H (1981) Transformations in the cytoplasmic structure of crayfish retinula cells during light- und dark-adaptation. J Comp Physiol 145:179–189

    Google Scholar 

  • Ungar F, Piscopo I, Letizia J, Holtzman E (1984) Uptake of calcium by the endoplasmic reticulum of the frog photoreceptor. J Cell Biol 98:1645–1655

    Google Scholar 

  • Walcott B (1975) Anatomical changes during light adaptation in insect compound eyes. In: Horridge GA (ed) The compound eye and vision of insects. Clarendon Press, Oxford, pp 20–33

    Google Scholar 

  • Waloga G, Brown JE, Pinto LH (1975) Detection of changes of Cain fromLimulus ventral photoreceptors using arsenazo III. Biol Bull 149:449–450

    Google Scholar 

  • Walz B (1979) Subcellular calcium localization and ATP-dependent Ca2+-uptake by smooth endoplasmic reticulum in an invertebrate photoreceptor cell. An ultrastructural, cytochemical and X-ray microanalytical study. Eur J Cell Biol 20:83–91

    Google Scholar 

  • Walz B (1982a) Ca2+-sequestering smooth endoplasmic reticulum in an inverbrate photoreceptor. I. Intracellular topography as revealed by OsFeCN staining and in situ accumulation. J Cell Biol 93:839–848

    Google Scholar 

  • Walz B (1982b) Ca2+-sequestering smooth endoplasmic reticulum in an invertebrate photoreceptor. II. Its properties as revealed by microphotometric measurements. J Cell Biol 93:849–859

    Google Scholar 

  • Walz B (1982c) Calcium-sequestering smooth endoplasmic reticulum in retinula cells of the blowfly. J Ultrastruct Res 81:240–248

    Google Scholar 

  • Waterman TH (1961) Light sensitivity and vision. In: Waterman TH (ed) The physiology of Crustacea. Academic Press, New York, pp 1–64

    Google Scholar 

  • White RH, Michaud NA (1980) Calcium is a component of ommochrome pigment granules in insect eyes. Comp Biochem Physiol 65A:239–242

    Google Scholar 

  • Worth RM, Ochs S (1982) Dependence of batrachotoxin block of axoplasmic transport on sodium. J Neurobiol 13:537–549

    Google Scholar 

Download references

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Frixione, E., Ruiz, L. Calcium uptake by smooth endoplasmic reticulum of peeled retinal photoreceptors of the crayfish. J. Comp. Physiol. 162, 91–100 (1988). https://doi.org/10.1007/BF01342706

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