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. 1984 May 1;98(5):1645–1655. doi: 10.1083/jcb.98.5.1645

Uptake of calcium by the endoplasmic reticulum of the frog photoreceptor

PMCID: PMC2113183  PMID: 6609924

Abstract

We studied retinal photoreceptors of Rana pipiens by using techniques designed to investigate calcium localization. Particularly useful were methods in which intracellular sites of calcium uptake were detected by incubation of saponin-treated isolated retinas in calcium-containing media, with oxalate present as a trapping agent. With these procedures, cell compartments accumulate deposits, which can be shown to contain calcium by x-ray microanalysis. Calcium accumulation was prominent in the rough endoplasmic reticulum in the myoid region. In addition, deposits were observed in agranular reticulum and in certain Golgi- associated compartments of the myoid region, in mitochondria, in axonal reticulum, and in agranular reticulum of presynaptic terminals. Calcium was also detected in the endoplasmic reticulum of retinas fixed directly upon isolation, by a freeze-substitution method. The factors influencing accumulation of calcium in the endoplasmic reticulum were evaluated by a semiquantitative approach based on determining the relative frequency of calcium oxalate crystals under varying conditions. Calcium accumulation was markedly enhanced by ATP. Studies with a nonhydrolyzable ATP analogue (adenylyl- imidodiphosphate ) and with inhibitors of the sarcoplasmic reticulum Ca2+-Mg2+ ATPase (mersalyl and tetracaine) indicated that this ATP-dependent calcium uptake reflects an energy-dependent process roughly comparable to that in the sarcoplasmic reticulum.

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Selected References

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  1. Agostini B., Hasselbach W. Electron cytochemistry of calcium uptake in the fragmented sarcoplasmic reticulum. Histochemie. 1971;28(1):55–67. doi: 10.1007/BF00305632. [DOI] [PubMed] [Google Scholar]
  2. Arshad J. H., Holdsworth E. S. Calcium uptake and release by rat liver mitochondria in the presence of rat liver cytosol or the components of cytosol. J Membr Biol. 1980 Dec 30;57(3):195–205. doi: 10.1007/BF01869587. [DOI] [PubMed] [Google Scholar]
  3. Bader C., Baumann F., Bertrand D. Role of intracellular calcium and sodium in light adaptation in the retina of the honey bee drone (Apis mellifera, L). J Gen Physiol. 1976 Apr;67(4):475–491. doi: 10.1085/jgp.67.4.475. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Beil F. U., von Chak D., Hasselbach W., Weber H. H. Competition between oxalate and phosphate during active calcium accumulation by sarcoplasmic vesicles. Z Naturforsch C. 1977 Mar-Apr;32(3-4):281–287. doi: 10.1515/znc-1977-3-421. [DOI] [PubMed] [Google Scholar]
  5. Black B. L., Jarett L., McDonald J. M. Relationship between calcium ion transport and (Ca2+ + Mg2+)-atpase activity in adipocyte endoplasmic reticulum. Biochim Biophys Acta. 1980 Mar 13;596(3):359–371. doi: 10.1016/0005-2736(80)90123-6. [DOI] [PubMed] [Google Scholar]
  6. Blaustein M. P., Ratzlaff R. W., Kendrick N. C., Schweitzer E. S. Calcium buffering in presynaptic nerve terminals. I. Evidence for involvement of a nonmitochondrial ATP-dependent sequestration mechanism. J Gen Physiol. 1978 Jul;72(1):15–41. doi: 10.1085/jgp.72.1.15. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Blaustein M. P., Ratzlaff R. W., Schweitzer E. S. Calcium buffering in presynaptic nerve terminals. II. Kinetic properties of the nonmitochondrial Ca sequestration mechanism. J Gen Physiol. 1978 Jul;72(1):43–66. doi: 10.1085/jgp.72.1.43. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Blaustein M. P., Ratzlaff R. W., Schweitzer E. S. Control of intracellular calcium in presynaptic nerve terminals. Fed Proc. 1980 Aug;39(10):2790–2795. [PubMed] [Google Scholar]
  9. Blitz A. L., Fine R. E., Toselli P. A. Evidence that coated vesicles isolated from brain are calcium-sequestering organelles resembling sarcoplasmic reticulum. J Cell Biol. 1977 Oct;75(1):135–147. doi: 10.1083/jcb.75.1.135. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Brinley F. J., Jr, Tiffert T., Scarpa A. Mitochondria and other calcium buffers of squid axon studied in situ. J Gen Physiol. 1978 Jul;72(1):101–127. doi: 10.1085/jgp.72.1.101. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Brown J. E., Brown P. K., Pinto L. H. Detection of light-induced changes of intracellular ionized calcium concentration in Limulus ventral photoreceptors using arsenazo III. J Physiol. 1977 May;267(2):299–320. doi: 10.1113/jphysiol.1977.sp011814. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Brown J. E., Coles J. A., Pinto L. H. Effects of injections of calcium and EGTA into the outer segments of retinal rods of Bufo marinus. J Physiol. 1977 Aug;269(3):707–722. doi: 10.1113/jphysiol.1977.sp011924. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Carafoli E., Crompton M. The regulation of intracellular calcium by mitochondria. Ann N Y Acad Sci. 1978 Apr 28;307:269–284. doi: 10.1111/j.1749-6632.1978.tb41957.x. [DOI] [PubMed] [Google Scholar]
  14. Carsten M. E., Reedy M. K. Cardiac sarcoplasmic reticulum: chemical and electron microscope studies of calcium accumulation. J Ultrastruct Res. 1971 Jun;35(5):554–574. doi: 10.1016/s0022-5320(71)80011-4. [DOI] [PubMed] [Google Scholar]
  15. Devine C. E., Somlyo A. V., Somlyo A. P. Sarcoplasmic reticulum and mitochondria as cation accumulation sites in smooth muscle. Philos Trans R Soc Lond B Biol Sci. 1973 Mar 15;265(867):17–23. doi: 10.1098/rstb.1973.0005. [DOI] [PubMed] [Google Scholar]
  16. Duce I. R., Keen P. Can neuronal smooth endoplasmic reticulum function as a calcium reservoir? Neuroscience. 1978;3(9):837–848. doi: 10.1016/0306-4522(78)90036-2. [DOI] [PubMed] [Google Scholar]
  17. Dunant Y., Babel-Guéin E., Droz B. Calcium metabolism and acetylcholine release at the nerve-electroplaque junction. J Physiol (Paris) 1980 Sep;76(5):471–478. [PubMed] [Google Scholar]
  18. Ellisman M. H., Lindsey J. D. The axoplasmic reticulum within myelinated axons is not transported rapidly. J Neurocytol. 1983 Jun;12(3):393–411. doi: 10.1007/BF01159382. [DOI] [PubMed] [Google Scholar]
  19. Endo M. Calcium release from the sarcoplasmic reticulum. Physiol Rev. 1977 Jan;57(1):71–108. doi: 10.1152/physrev.1977.57.1.71. [DOI] [PubMed] [Google Scholar]
  20. Evans J. A., Hood D. C., Holtzman E. Differential effects of cobalt ions on rod and cone synaptic activity in the isolated frog retina. Vision Res. 1978;18(2):145–151. doi: 10.1016/0042-6989(78)90179-7. [DOI] [PubMed] [Google Scholar]
  21. FEDER N., SIDMAN R. L. Methods and principles of fixation by freeze-substitution. J Biophys Biochem Cytol. 1958 Sep 25;4(5):593–600. doi: 10.1083/jcb.4.5.593. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Fabiato A., Fabiato F. Calcium and cardiac excitation-contraction coupling. Annu Rev Physiol. 1979;41:473–484. doi: 10.1146/annurev.ph.41.030179.002353. [DOI] [PubMed] [Google Scholar]
  23. Fozzard H. A. Heart: excitation-contraction coupling. Annu Rev Physiol. 1977;39:201–220. doi: 10.1146/annurev.ph.39.030177.001221. [DOI] [PubMed] [Google Scholar]
  24. Fukuda J., Kawa K. Permeation of manganese, cadmium, zinc, and beryllium through calcium channels of an insect muscle membrane. Science. 1977 Apr 15;196(4287):309–311. doi: 10.1126/science.847472. [DOI] [PubMed] [Google Scholar]
  25. George J. S., Hagins W. A. Control of Ca2+ in rod outer segment disks by light and cyclic GMP. Nature. 1983 May 26;303(5915):344–348. doi: 10.1038/303344a0. [DOI] [PubMed] [Google Scholar]
  26. Glickman J., Croen K., Kelly S., Al-Awqati Q. Golgi membranes contain an electrogenic H+ pump in parallel to a chloride conductance. J Cell Biol. 1983 Oct;97(4):1303–1308. doi: 10.1083/jcb.97.4.1303. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. HASSELBACH W., MAKINOSE M. [The calcium pump of the "relaxing granules" of muscle and its dependence on ATP-splitting]. Biochem Z. 1961;333:518–528. [PubMed] [Google Scholar]
  28. Hagins W. A., Yoshikami S. Ionic mechanisms in excitation of photoreceptors. Ann N Y Acad Sci. 1975 Dec 30;264:314–325. doi: 10.1111/j.1749-6632.1975.tb31492.x. [DOI] [PubMed] [Google Scholar]
  29. Harreveld A. V., Fifkova E. Rapid freezing of deep cerebral structures for electron microscopy. Anat Rec. 1975 Jul;182(3):377–385. doi: 10.1002/ar.1091820311. [DOI] [PubMed] [Google Scholar]
  30. Henkart M. P., Reese T. S., Brinley F. J., Jr Endoplasmic reticulum sequesters calcium in the squid giant axon. Science. 1978 Dec 22;202(4374):1300–1303. doi: 10.1126/science.725607. [DOI] [PubMed] [Google Scholar]
  31. Henkart M. Identification and function of intracellular calcium stores in axons and cell bodies of neurons. Fed Proc. 1980 Aug;39(10):2783–2789. [PubMed] [Google Scholar]
  32. Holtzman E., Mercurio A. M. Membrane circulation in neurons and photoreceptors: some unresolved issues. Int Rev Cytol. 1980;67:1–67. doi: 10.1016/s0074-7696(08)62426-2. [DOI] [PubMed] [Google Scholar]
  33. Israël M., Manaranche R., Marsal J., Meunier F. M., Morel N., Frachon P., Lesbats B. ATP-dependent calcium uptake by cholinergic synaptic vesicles isolated from Torpedo electric organ. J Membr Biol. 1980 May 23;54(2):115–126. doi: 10.1007/BF01940565. [DOI] [PubMed] [Google Scholar]
  34. Johnson P. N., Inesi G. The effect of methylxanthines and local anesthetics on fragmented sarcoplasmic reticulum. J Pharmacol Exp Ther. 1969 Oct;169(2):308–314. [PubMed] [Google Scholar]
  35. Jorgensen A. O., Shen A. C., MacLennan D. H., Tokuyasu K. T. Ultrastructural localization of the Ca2+ + Mg2+-dependent ATPase of sarcoplasmic reticulum in rat skeletal muscle by immunoferritin labeling of ultrathin frozen sections. J Cell Biol. 1982 Feb;92(2):409–416. doi: 10.1083/jcb.92.2.409. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Katz B., Miledi R. Ionic requirements of synaptic transmitter release. Nature. 1967 Aug 5;215(5101):651–651. doi: 10.1038/215651a0. [DOI] [PubMed] [Google Scholar]
  37. Korenbrot J. I., Cone R. A. Dark ionic flux and the effects of light in isolated rod outer segments. J Gen Physiol. 1972 Jul;60(1):20–45. doi: 10.1085/jgp.60.1.20. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Leslie B. A., Putney J. W., Jr Ionic mechanisms in secretagogue-induced morphological changes in rat parotid gland. J Cell Biol. 1983 Oct;97(4):1119–1130. doi: 10.1083/jcb.97.4.1119. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Lipton S. A., Ostroy S. E., Dowling J. E. Electrical and adaptive properties of rod photoreceptors in Bufo marinus. I. Effects of altered extracellular Ca2+ levels. J Gen Physiol. 1977 Dec;70(6):747–770. doi: 10.1085/jgp.70.6.747. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Liscum L., Hauptman P. J., Hood D. C., Holtzman E. Effect of barium and tetraethylammonium on membrane circulation in frog retinal photoreceptors. J Cell Biol. 1982 Oct;95(1):296–309. doi: 10.1083/jcb.95.1.296. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. MARTONOSI A., FERETOS R. SARCOPLASMIC RETICULUM. I. THE UPTAKE OF CA++ BY SARCOPLASMIC RETICULUM FRAGMENTS. J Biol Chem. 1964 Feb;239:648–658. [PubMed] [Google Scholar]
  42. Matheke M. L., Kalff M., Holtzman E. Effects of monensin on photoreceptors of isolated frog retinas. Tissue Cell. 1983;15(4):509–513. doi: 10.1016/0040-8166(83)90002-2. [DOI] [PubMed] [Google Scholar]
  43. McGraw C. F., Somlyo A. V., Blaustein M. P. Localization of calcium in presynaptic nerve terminals. An ultrastructural and electron microprobe analysis. J Cell Biol. 1980 May;85(2):228–241. doi: 10.1083/jcb.85.2.228. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. McGraw C. F., Somlyo A. V., Blaustein M. P. Probing for calcium at presynaptic nerve terminals. Fed Proc. 1980 Aug;39(10):2796–2801. [PubMed] [Google Scholar]
  45. Meissner G. Isolation and characterization of two types of sarcoplasmic reticulum vesicles. Biochim Biophys Acta. 1975 Apr 21;389(1):51–68. doi: 10.1016/0005-2736(75)90385-5. [DOI] [PubMed] [Google Scholar]
  46. Mercurio A. M., Holtzman E. Smooth endoplasmic reticulum and other agranular reticulum in frog retinal photoreceptors. J Neurocytol. 1982 Apr;11(2):263–293. doi: 10.1007/BF01258247. [DOI] [PubMed] [Google Scholar]
  47. Mercurio A. M., Holtzman E. Ultrastructural localization of glycerolipid synthesis in rod cells of the isolated frog retina. J Neurocytol. 1982 Apr;11(2):295–322. doi: 10.1007/BF01258248. [DOI] [PubMed] [Google Scholar]
  48. Miledi R. Transmitter release induced by injection of calcium ions into nerve terminals. Proc R Soc Lond B Biol Sci. 1973 Jul 3;183(1073):421–425. doi: 10.1098/rspb.1973.0026. [DOI] [PubMed] [Google Scholar]
  49. Moore L., Chen T., Knapp H. R., Jr, Landon E. J. Energy-dependent calcium sequestration activity in rat liver microsomes. J Biol Chem. 1975 Jun 25;250(12):4562–4568. [PubMed] [Google Scholar]
  50. Moore L., Pastan I. Regulation of intracellular calcium in chick embryo fibroblast: calcium uptake by the microsomal fraction. J Cell Physiol. 1977 May;91(2):289–296. doi: 10.1002/jcp.1040910213. [DOI] [PubMed] [Google Scholar]
  51. Ogawa Y., Ebashi S. Ca-releasing action of beta, gamma-methylene adenosine triphosphate on fragmented sarcoplasmic reticulum. J Biochem. 1976 Nov;80(5):1149–1157. doi: 10.1093/oxfordjournals.jbchem.a131370. [DOI] [PubMed] [Google Scholar]
  52. Ornberg R. L., Reese T. S. A freeze-substitution method for localizing divalent cations: examples from secretory systems. Fed Proc. 1980 Aug;39(10):2802–2808. [PubMed] [Google Scholar]
  53. PODOLSKY R. J., COSTANTIN L. L. REGULATION BY CALCIUM OF THE CONTRACTION AND RELAXATION OF MUSCLE FIBERS. Fed Proc. 1964 Sep-Oct;23:933–939. [PubMed] [Google Scholar]
  54. Page E. Correlations between Electron Microscopic and Physiological Observations in Heart Muscle. J Gen Physiol. 1968 May 1;51(5):211–220. [PMC free article] [PubMed] [Google Scholar]
  55. Papermaster D. S., Converse C. A., Siuss J. Membrane biosynthesis in the frog retina: opsin transport in the photoreceptor cell. Biochemistry. 1975 Apr 8;14(7):1343–1352. doi: 10.1021/bi00678a001. [DOI] [PubMed] [Google Scholar]
  56. Parducz A., Joó F. Visualization of stimulated nerve endings by preferential calcium accumulation of mitochondria. J Cell Biol. 1976 May;69(2):513–517. doi: 10.1083/jcb.69.2.513. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Pease D. C., Jenden D. J., Howell J. N. Calcium uptake in glycerol-extracted rabbit psoas muscle fibers. II. Electron microscopic localization of uptake sites. J Cell Physiol. 1965 Apr;65(2):141–153. doi: 10.1002/jcp.1030650203. [DOI] [PubMed] [Google Scholar]
  58. Perrelet A., Bader C. R. Morphological evidence for calcium stores in photoreceptors of the honeybee drone retina. J Ultrastruct Res. 1978 Jun;63(3):237–243. doi: 10.1016/s0022-5320(78)80048-3. [DOI] [PubMed] [Google Scholar]
  59. Politoff A. L., Rose S., Pappas G. D. The calcium binding sites of synaptic vesicles of the frog sartorius neuromuscular junction. J Cell Biol. 1974 Jun;61(3):818–823. doi: 10.1083/jcb.61.3.818. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Popescu L. M., Diculescu I. Calcium in smooth muscle sarcoplasmic reticulum in situ. Conventional and X-ray analytical electron microscopy. J Cell Biol. 1975 Dec;67(3):911–918. doi: 10.1083/jcb.67.3.911. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Quatacker J. The axonal reticulum in the neurons of the superior cervical ganglion of the rat as a direct extension of the Golgi apparatus. Histochem J. 1981 Jan;13(1):109–124. doi: 10.1007/BF01005844. [DOI] [PubMed] [Google Scholar]
  62. Raeymaekers L., Agostini B., Hasselbach W. Electron cytochemistry of oxalate-stimulated calcium uptake in microsomes from the smooth muscle of the pig stomach. Histochemistry. 1980 Feb;65(2):121–129. doi: 10.1007/BF00493160. [DOI] [PubMed] [Google Scholar]
  63. Rambourg A., Droz B. Smooth endoplasmic reticulum and axonal transport. J Neurochem. 1980 Jul;35(1):16–25. doi: 10.1111/j.1471-4159.1980.tb12484.x. [DOI] [PubMed] [Google Scholar]
  64. Reinecke M., Walther C. Aspects of turnover and biogenesis of synaptic vesicles at locust neuromuscular junctions as revealed by zinc iodide-osmium tetroxide (ZIO) reacting with intravesicular SH-groups. J Cell Biol. 1978 Sep;78(3):839–855. doi: 10.1083/jcb.78.3.839. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Ripps H., Shakib M., Chappell R. L., MacDonald E. D. Ultrastructural localization and x-ray analysis of calcium-induced electron-dense deposits in the skate retina. Neuroscience. 1979;4(11):1689–1703. doi: 10.1016/0306-4522(79)90028-9. [DOI] [PubMed] [Google Scholar]
  66. Schwartz E. A. First events in vision: the generation of responses in vertebrate rods. J Cell Biol. 1981 Aug;90(2):271–278. doi: 10.1083/jcb.90.2.271. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Silver R. B., Cole R. D., Cande W. Z. Isolation of mitotic apparatus containing vesicles with calcium sequestration activity. Cell. 1980 Feb;19(2):505–516. doi: 10.1016/0092-8674(80)90525-5. [DOI] [PubMed] [Google Scholar]
  68. Smith H. G., Jr, Fager R. S., Litman R. J. Light-activated calcium release from sonicated bovine retinal rod outer segment disks. Biochemistry. 1977 Apr 5;16(7):1399–1405. doi: 10.1021/bi00626a025. [DOI] [PubMed] [Google Scholar]
  69. Solaro R. J., Briggs F. N. Estimating the functional capabilities of sarcoplasmic reticulum in cardiac muscle. Calcium binding. Circ Res. 1974 Apr;34(4):531–540. doi: 10.1161/01.res.34.4.531. [DOI] [PubMed] [Google Scholar]
  70. Somlyo A. V., Gonzalez-Serratos H. G., Shuman H., McClellan G., Somlyo A. P. Calcium release and ionic changes in the sarcoplasmic reticulum of tetanized muscle: an electron-probe study. J Cell Biol. 1981 Sep;90(3):577–594. doi: 10.1083/jcb.90.3.577. [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Sorenson M. M., Reuben J. P., Eastwood A. B., Orentlicher M., Katz G. M. Functional heterogeneity of the sarcoplasmic reticulum within sarcomeres of skinned muscle fibers. J Membr Biol. 1980 Mar 31;53(1):1–17. doi: 10.1007/BF01871168. [DOI] [PubMed] [Google Scholar]
  72. Stoeckel M. E., Hindelang-Gertner C., Dellmann H-D, Porte A., Stutinsky F. Subcellular localization of calcium in the mouse hypophysis. I. Calcium distribution in the adeno- and neurohypophysis under normal conditions. Cell Tissue Res. 1975;157(3):307–322. doi: 10.1007/BF00225522. [DOI] [PubMed] [Google Scholar]
  73. Szuts E. Z., Cone R. A. Calcium content of frog rod outer segments and discs. Biochim Biophys Acta. 1977 Jul 14;468(2):194–208. doi: 10.1016/0005-2736(77)90114-6. [DOI] [PubMed] [Google Scholar]
  74. Tada M., Yamamoto T., Tonomura Y. Molecular mechanism of active calcium transport by sarcoplasmic reticulum. Physiol Rev. 1978 Jan;58(1):1–79. doi: 10.1152/physrev.1978.58.1.1. [DOI] [PubMed] [Google Scholar]
  75. Thacher S. M. Light-stimulated, magnesium-dependent ATPase in toad retinal rod outer segments. Biochemistry. 1978 Jul 25;17(15):3005–3011. doi: 10.1021/bi00608a011. [DOI] [PubMed] [Google Scholar]
  76. Torp-Pedersen C., Saermark T., Bundgaard M., Thorn N. A. ATP-dependent Ca2+ accumulation by microvesicles isolated from bovine neurohypophyses. J Neurochem. 1980 Sep;35(3):552–557. doi: 10.1111/j.1471-4159.1980.tb03690.x. [DOI] [PubMed] [Google Scholar]
  77. Ungar F., Piscopo I., Holtzman E. Calcium accumulation in intracellular compartments of frog retinal rod photoreceptors. Brain Res. 1981 Jan 26;205(1):200–206. doi: 10.1016/0006-8993(81)90733-2. [DOI] [PubMed] [Google Scholar]
  78. VENABLE J. H., COGGESHALL R. A SIMPLIFIED LEAD CITRATE STAIN FOR USE IN ELECTRON MICROSCOPY. J Cell Biol. 1965 May;25:407–408. doi: 10.1083/jcb.25.2.407. [DOI] [PMC free article] [PubMed] [Google Scholar]
  79. WATSON M. L. Staining of tissue sections for electron microscopy with heavy metals. J Biophys Biochem Cytol. 1958 Jul 25;4(4):475–478. doi: 10.1083/jcb.4.4.475. [DOI] [PMC free article] [PubMed] [Google Scholar]
  80. Wakasugi H., Kimura T., Haase W., Kribben A., Kaufmann R., Schulz I. Calcium uptake into acini from rat pancreas: evidence for intracellular ATP-dependent calcium sequestration. J Membr Biol. 1982;65(3):205–220. doi: 10.1007/BF01869964. [DOI] [PubMed] [Google Scholar]
  81. Walz B. Ca2+-sequestering smooth endoplasmic reticulum in an invertebrate photoreceptor. I. Intracellular topography as revealed by OsFeCN staining and in situ Ca accumulation. J Cell Biol. 1982 Jun;93(3):839–848. doi: 10.1083/jcb.93.3.839. [DOI] [PMC free article] [PubMed] [Google Scholar]
  82. Walz B. Ca2+-sequestering smooth endoplasmic reticulum in an invertebrate photoreceptor. II. Its properties as revealed by microphotometric measurements. J Cell Biol. 1982 Jun;93(3):849–859. doi: 10.1083/jcb.93.3.849. [DOI] [PMC free article] [PubMed] [Google Scholar]
  83. Walz B. Calcium-sequestering smooth endoplasmic reticulum in retinula cells of the blowfly. J Ultrastruct Res. 1982 Nov;81(2):240–248. doi: 10.1016/s0022-5320(82)90079-x. [DOI] [PubMed] [Google Scholar]
  84. Walz B. 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. Eur J Cell Biol. 1979 Oct;20(1):83–91. [PubMed] [Google Scholar]
  85. Winegrad S. Intracellular calcium binding and release in frog heart. J Gen Physiol. 1973 Dec;62(6):693–706. doi: 10.1085/jgp.62.6.693. [DOI] [PMC free article] [PubMed] [Google Scholar]
  86. Wormington C. M., Cone R. A. Ionic blockage of the light-regulated sodium channels in isolated rod outer segments. J Gen Physiol. 1978 Jun;71(6):657–681. doi: 10.1085/jgp.71.6.657. [DOI] [PMC free article] [PubMed] [Google Scholar]
  87. Young R. W. Visual cells and the concept of renewal. Invest Ophthalmol Vis Sci. 1976 Sep;15(9):700–725. [PubMed] [Google Scholar]

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