Inositol 1,4,5-trisphosphate-induced calcium release is necessary for generating the entire light response of Limulus ventral photoreceptors

Journal of General Physiology

Volumn 121, Issue 5, 2003, Pages 441-449

  Fein, Alan ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

2 aminoethoxydiphenyl borate; Calcium buffers; Inositol 1,4,5 trisphosphate receptor; Microvillar photoreceptors; Phototransduction

Indexed keywords

2 AMINOETHOXYDIPHENYLBORANE; BORIC ACID; CALCIUM; CYCLOPIAZONIC ACID; ETHYLENE GLYCOL 1,2 BIS(2 AMINOPHENYL) ETHER N,N,N',N' TETRAACETIC ACID; INOSITOL 1,4,5 TRISPHOSPHATE; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; CALCIUM MOBILIZATION; CALCIUM TRANSPORT; LIGHT INTENSITY; LIMULUS; MEMBRANE PERMEABILITY; NONHUMAN; PHOTOREACTIVITY; PHOTORECEPTOR; PHOTOTRANSDUCTION; STEADY STATE;

ANIMALS; BORON COMPOUNDS; CALCIUM; CALCIUM CHANNELS; CALCIUM SIGNALING; HORSESHOE CRABS; INOSITOL 1,4,5-TRISPHOSPHATE; LIGHT; PATCH-CLAMP TECHNIQUES; PHOTORECEPTORS, INVERTEBRATE; PHOTOTRANSDUCTION; RECEPTORS, CYTOPLASMIC AND NUCLEAR;

EID: 0038301510     PISSN: 00221295     EISSN: None     Source Type: Journal    
DOI: 10.1085/jgp.200208778     Document Type: Article

References (39)

1. Bolsover, S.R., and J.E. Brown. 1985. Calcium ion, an intracellular messenger of light adaptation, also participates in excitation of Limulus photoreceptors. J. Physiol. 364:381-393.
2. Brown, J.E., and J.R. Blinks. 1974. Changes in intracellular free calcium concentration during illumination of invertebrate photoreceptors. Detection with aequorin. J. Gen. Physiol. 64:643-665.
3. Brown, J.E., P.K. Brown, and L.H. Pinto. 1977. Detection of light-induced changes of intracellular ionized calcium concentration in Limulus ventral photoreceptors using arsenazo III. J. Physiol. 267:299-320.
4. Brown, J.E., and L.J. Rubin. 1984. A direct demonstration that inositol-trisphosphate induces an increase in intracellular calcium in Limulus photoreceptors. Biochem. Biophys. Res. Commun. 125: 1137-1142.
5. Brown, J.E., L.J. Rubin, A.J. Ghalayini, A.P. Tarver, R.F. Irvine, M.J. Berridge, and R.E. Anderson. 1984. myo-Inositol polyphosphate may be a messenger for visual excitation in Limulus photoreceptors. Nature. 311:160-163.
6. Calman, B.G., and S.C. Chamberlain. 1982. Distinct lobes of Limulus ventral photoreceptors. II. Structure and ultrastructure. J. Gen. Physiol. 80:839-862.
7. Chorna-Ornan, I., T. Joel-Almagor, H.C. Ben-Ami, S. Frechter, B. Gillo, Z. Selinger, D.L. Gill, and B. Minke. 2001. A common mechanism underlies vertebrate calcium signaling and Drosophila phototransduction. J. Neurosci. 21:2622-2629.
8. Corson, D.W., and A. Fein. 1983. Quantitative pressure injection of picoliter volumes into Limulus ventral photoreceptors. Biophys. J. 44:299-304.
9. Corson, D.W., and A. Fein. 1987. Inositol 1,4,5-trisphosphate induces bursts of calcium release inside Limulus ventral photoreceptors. Brain Res. 423:343-346.
10. Dabdoub, A., and R. Payne. 1999. Protein kinase C activators inhibit the visual cascade in Limulus ventral photoreceptors at an early stage. J. Neurosci. 19:10262-10269.
11. Dorlochter, M., W. Yuan, and H. Stieve. 1999. Effects of calcium and cyclopiazonic acid on the photoresponse in the Limulus ventral photoreceptor. Verlag der Zeitschrift fur Naturforschung. 54c: 446-455.
12. Faddis, M.N., and J.E. Brown. 1993. Intracellular injection of heparin and polyamines. Effects on phototransduction in limulus ventral photoreceptors. J. Gen. Physiol. 101:909-931.
13. Fein, A., and S. Cavar. 2000. Divergent mechanisms for phototransduction of invertebrate microvillar photoreceptors. Vis. Neurosci. 17:911-917.
14. Fein, A., and J.S. Charlton. 1975. Local adaptation in the ventral photoreceptors of Limulus. J. Gen. Physiol. 66:823-836.
15. Fein, A., and J.S. Charlton. 1977. A quantitative comparison of the effects of intracellular calcium injection and light adaptation on the photoresponse of Limulus ventral photoreceptors. J. Gen. Physiol. 70:591-600.
16. Fein, A., and R.D. DeVoe. 1973. Adaptation in the ventral eye of Limulus is functionally independent of the photochemical cycle, membrane potential, and membrane resistance. J. Gen. Physiol. 61:273-289.
17. Fein, A., R. Payne, D.W. Corson, M.J. Berridge, and R.F. Irvine. 1984. Photoreceptor excitation and adaptation by inositol 1,4,5-trisphosphate. Nature. 311:157-160.
18. Frank, T.M., and A. Fein. 1991. The role of the inositol phosphate cascade in visual excitation of invertebrate microvillar photoreceptors. J. Gen. Physiol. 97:697-723.
19. Hardie, R.C., and P. Raghu. 2001. Visual transduction in Drosophila. Nature. 413:186-193.
20. Koganezawa, M., and I. Shimada. 2002. Inositol 1,4,5-trisphosphate transduction cascade in taste reception of the fleshfly, Boettcherisca peregrina. J. Neurobiol. 51:66-83.
21. Levy, S., and A. Fein. 1985. Relationship between light sensitivity and intracellular free Ca concentration in Limulus ventral photoreceptors. A quantitative study using Ca-selective microelectrodes. J. Gen. Physiol. 85:805-841.
22. Lisman, J.E., and J.E. Brown. 1975. Effects of intracellular injection of calcium buffers on light adaptation in Limulus ventral photoreceptors. J. Gen. Physiol. 66:489-506.
23. Ma, H.T., R.L. Patterson, D.B. van Rossum, L. Birnbaumer, K. Mikoshiba, and D.L. Gill. 2000. Requirement of the inositol trisphosphate receptor for activation of store-operated Ca2+ channels. Science. 287:1647-1651.
24. Maruyama, T., T. Kanaji, S. Nakade, T. Kanno, and K. Mikoshiba. 1997. 2APB, 2-aminoethoxydiphenyl borate, a membrane-penetrable modulator of Ins(1,4,5)P3-induced Ca2+ release. J. Biochem. (Tokyo). 122:498-505.
25. Mason, M.J., C. Garcia-Rodriguez, and S. Grinstein. 1991. Coupling between intracellular Ca2+ stores and the Ca2+ permeability of the plasma membrane. Comparison of the effects of thapsigargin, 2,5-di-(tert-butyl)-1,4-hydroquinone, and cyclopiazonic acid in rat thymic lymphocytes. J. Biol. Chem. 266:20856-20862.
26. Payne, R., D.W. Corson, and A. Fein. 1986a. Pressure injection of calcium both excites and adapts Limulus ventral photoreceptors. J. Gen. Physiol. 88:107-126.
27. Payne, R., D.W. Corson, A. Fein, and M.J. Berridge. 1986b. Excitation and adaptation of Limulus ventral photoreceptors by inositol 1,4,5 triphosphate result from a rise in intracellular calcium. J. Gen. Physiol. 88:127-142.
28. Payne, R., and J. Demas. 2000. Timing of Ca(2+) release from intracellular stores and the electrical response of Limulus ventral photoreceptors to dim flashes. J. Gen. Physiol. 115:735-748.
29. Payne, R., and A. Fein. 1986. The initial response of Limulus ventral photoreceptors to bright flashes. Released calcium as a synergist to excitation. J. Gen. Physiol. 87:243-269.
30. Payne, R., and A. Fein. 1987. Inositol 1,4,5 trisphosphate releases calcium from specialized sites within Limulus photoreceptors. J. Cell Biol. 104:933-937.
31. Payne, R., and B.V. Potter. 1991. Injection of inositol trisphosphorothioate into Limulus ventral photoreceptors causes oscillations of free cytosolic calcium. J. Gen. Physiol. 97:1165-1186.
32. Payne, R., B. Walz, S. Levy, and A. Fein. 1988. The localization of calcium release by inositol trisphosphate in Limulus photoreceptors and its control by negative feedback. Philos. Trans. R. Soc. Lond. B Biol. Sci. 320:359-379.
33. Shin, J., E.A. Richard, and J.E. Lisman. 1993. Ca2+ is an obligatory intermediate in the excitation cascade of limulus photoreceptors. Neuron. 11:845-855.
34. Stern, J.H., and J.E. Lisman. 1982. Internal dialysis of Limulus ventral photoreceptors. Proc. Natl. Acad. Sci. USA. 79:7580-7584.
35. Ukhanov, K., and R. Payne. 1995. Light activated calcium release in Limulus ventral photoreceptors as revealed by laser confocal microscopy. Cell Calcium. 18:301-313.
36. Ukhanov, K., and R. Payne. 1997. Rapid coupling of calcium release to depolarization in Limulus polyphemus ventral photoreceptors as revealed by microphotolysis and confocal microscopy. J. Neurosci. 17:1701-1709.
37. Ukhanov, K.Y., T.M. Flores, H.S. Hsiao, P. Mohapatra, C.H. Pitts, and R. Payne. 1995. Measurement of cytosolic Ca2+ concentration in Limulus ventral photoreceptors using fluorescent dyes. J. Gen. Physiol. 105:95-116.
38. Vallet, A.M., and A. Fein. 1997. 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 in Limulus ventral photoreceptors. Brain Res. 768:91-101.
39. Wang, Y., M. Deshpande, and R. Payne. 2002. 2-Aminoethoxydiphenyl borate inhibits phototransduction and blocks voltage-gated potassium channels in Limulus ventral photoreceptors. Cell Calcium. 32:209.