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 Research

Volumn 768, Issue 1-2, 1997, Pages 91-101

  Vallet, Anne M ^a   Fein, Alan ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

Aequorin luminescence; Calcium release; Endoplasmic reticulum; Pressure injection; Signal transduction

Indexed keywords

ENZYME INHIBITOR; FLUORIDE; INOSITOL 1,4,5 TRISPHOSPHATE; INOSITOL 1,4,5 TRISPHOSPHATE 5 PHOSPHATASE; INOSITOL 2,4,5 TRISPHOSPHATE; VANADIC ACID;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEPOLARIZATION; HYDROLYSIS; LIGHT; LIMULUS; NONHUMAN; PHOTORECEPTOR; PRIORITY JOURNAL;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; CALCIUM; HORSESHOE CRABS; HYDROLYSIS; INOSITOL 1,4,5-TRISPHOSPHATE; LIGHT; MEMBRANE POTENTIALS; PHOTORECEPTORS, INVERTEBRATE; VANADATES;

EID: 0030768113     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-8993(97)00603-3     Document Type: Article

References (58)

1. Auethavekiat V., Abrams C.S., Majerus P.W. Phosphorylation of platelet pleckstrin activates inositol polyphosphate 5-phosphatase. J. Biol. Chem. 272:1997;1786-1790.
2. Bencherif M., Lukas R.J. Vanadate amplifies receptor-mediated accumulation of inositol trisphosphates and inhibits inositol tris- and tetrakis-phosphate activities. Neurosci. Lett. 134:1992;157-160.
3. Berridge M.J. Inositol trisphosphate and diacylglycerol: two interacting second messengers. Annu. Rev. Biochem. 56:1987;159-193.
4. Berridge M.J. Elementary and global aspects of calcium signalling. J. Physiol. 499:1996;291-306.
5. Berridge M.J., Irvine R.F. Inositol phosphates and cell signalling. Nature. 341:1989;197-205.
6. Blinks J.R., Wier W.G., Hess P., Prendergast F.G. Measurement of calcium concentrations in living cells. Prog. Biophys. Mol. Biol. 40:1982;1-114.
7. Bloomquist B.T., Shortridge R.D., Schneuwly S., Perdes M., Montell C., Steller H., Rubin G., Pak W.L. Isolation of a putative phospholipase C gene of Drosophila, norpA, and its role in phototransduction. Cell. 54:1988;723-733.
8. Brown J.E., Blinks J.R. Changes in intracellular free calcium concentration during illumination of invertebrate photoreceptors. Detection with aequorin. J. Gen. Physiol. 64:1974;643-665.
9. Brown J.E., Rubin L.J. A direct demonstration that inositol-trisphosphate induces an increase in intracellular calcium in Limulus photoreceptors. Biochem. Biophys. Res. Commun. 125:1984;1137-1142.
10. Brown J.E., Rubin L.J., Ghalayini A.J., Tarver A.P., Irvine R.F., Berridge M.J., Anderson R.E. Myo-inositol polyphosphate may be a messenger for visual excitation in Limulus photoreceptors. Nature. 311:1984;160-163.
11. Calman B.G., Chamberlain S.C. Distinct lobes of Limulus photoreceptors II. Structure and ultrastructure. J. Gen. Physiol. 80:1982;839-862.
12. Corson D.W., Fein A. Chemical excitation of Limulus photoreceptors. I. Phosphatase inhibitors induce discrete-wave production in the dark. J. Gen. Physiol. 82:1983;639-657.
13. Corson D.W., Fein A. Quantitative pressure injection of picoliter volumes into Limulus ventral photoreceptors. Biophys. J. 44:1983;299-304.
14. Corson D.W., Fein A. Inositol 1,4,5-trisphosphate induces bursts of calcium release inside Limulus ventral photoreceptors. Brain Res. 423:1987;343-346.
15. Corson D.W., Fein A., Walthall W.W. Chemical excitation of Limulus photoreceptors. II Vanadate, GTP-gamma-S, and fluoride prolong excitation evoked by dim flashes of light. J. Gen. Physiol. 82:1983;659-677.
16. De Smedt F., Boom A., Pesesse X., Schivvmann S.N., Erneux C. Post-translational modification of human type I inositol-1,4,5-trisphosphate 5-phosphatase by farensylation. J. Biol. Chem. 271:1996;10419-10424.
17. Devary O., Heichal O., Blumenfeld A., Cassel D., Suss E., Barash S., Rubinstein C.T., Minke B., Selinger Z. Coupling of photoexcited rhodopsin to inositol phospholipid hydrolysis in fly photoreceptors. Proc. Natl. Acad. Sci. USA. 84:1987;6939-6943.
18. Downes C.P., Mussat M.C., Michell R.H. The inositol trisphosphate phosphomonoesterase of the human erythrocyte membrane. Biochem. J. 203:1982;169-177.
19. Fein A., Charlton J.S. Local adaptation in Limulus ventral photoreceptors. J. Gen. Physiol. 66:1975;823-838.
20. Fein A., Corson D.W. Both photons and fluoride ion excite Limulus ventral photoreceptors. Science. 204:1979;77-79.
21. A. Fein, R. Payne, Phototransduction in Limulus photoreceptors: roles of calcium and inositol trisphosphate, in: R.C. Hardie, D.G. Stavenga (Eds.), Facets of Vision, Springer, Berlin, 1989, pp. 173-185.
22. Fein A., Payne R., Corson D.W., Berridge M.J., Irvine R.F. Photoreceptor excitation and adaptation by inositol 1,4,5-trisphosphate. Nature. 311:1984;157-160.
23. Frank T.M., Fein A. The role of the inositol phosphate cascade in visual excitation of invertebrate microvillar photoreceptors. J. Gen. Physiol. 97:1991;697-723.
24. Hardie R.C. Photolysis of caged calcium facilitates and inactivates but does not excite light-sensitive channels in Drosophila photoreceptors. J. Neurosci. 15:1995;889-902.
25. Hardie R.C. INDO-1 measurements of absolute resting and light-induced calcium concentration in Drosophila photoreceptors. J. Neurosci. 16:1996;2924-2933.
26. Hardie R.C., Peretz A., Suss-Toby E., Rom-Glas A., Bishop S.A., Selinger Z., Minke B. Protein kinase C is required for light adaptation in Drosophila photoreceptors. Nature. 363:1993;634-637.
27. Jefferson A.B., Majerus P.W. Properties of type II inositol polyphosphate 5-phosphatase. J. Biol. Chem. 270:1995;9370-9377.
28. Kozikowski A.P., Fauq A.H., Aksoy I.A., Seewald M.J., Powis G. Synthesis of the first optically pure, fluorinated inositol 1,4,5-trisphosphate of myo-inositol stereochemistry and its effect on calcium release in Swiss 3T3 cells. J. Am. Chem. Soc. 112:1990;7403-7406.
29. Levitan I., Hillman P., Payne R Fast desensitization of the response to InsP3 in Limulus ventral photoreceptors. Biophys. J. 64:1993;1354-1360.
30. Levitan I., Payne R., Potter B.V.L., Hillman P. Facilitation of the responses to injections of inositol 1,4,5-trisphosphate analogs in Limulus ventral photoreceptors. Biophys. J. 67:1994;1161-1172.
31. Levy S., Payne R. A lingering elevation of intracellular free calcium accompanies inhibition of inositol 1,4,5 trisphosphate-induced Ca release in Limulus ventral photoreceptors. J. Gen. Physiol. 101:1993;67-84.
32. Levy S., Payne R. Limulus ventral photoreceptors contain two functionally dissimilar inositol triphosphate-induced calcium release mechanisms. J. Photochem. Photobiol. 35:1996;97-103.
33. Lisman J.E., Brown J.E. Effects of intracellular injection of calcium buffers on light adaptation in Limulus ventral photoreceptors. J. Gen. Physiol. 66:1975;489-506.
34. McKay R.R., Chen D., Miller K., Kim S., Stark W.S., Shortridge R.D. Phospholipase C rescues visual defect in norpA mutant of Drosophila melanogaster. J. Biol. Chem. 270:1995;13271-13276.
35. Millecchia R., Mauro A. The ventral photoreceptor cells of Limulus. II. The basic photoresponse. J. Gen. Physiol. 54:1969;310-330.
36. Millecchia R., Mauro A. The ventral photoreceptor cells of Limulus. III. A voltage clamp study. J. Gen. Physiol. 54:1969;331-351.
37. B. Minke, Z. Selinger, The inositol-lipid pathway is necessary for light excitation in fly photoreceptors, in: D.P. Corey, S.D. Roper (Eds.), Sensory Transduction, Rockefeller University Press, New York, 1992, pp. 201-217.
38. Payne R., Corson D.W., Fein A. Pressure injection of calcium both excites and adapts Limulus ventral photoreceptors. J. Gen. Physiol. 88:1986;107-126.
39. Payne R., Corson D.W., Fein A., Berridge M.J. Excitation and adaptation of Limulus ventral photoreceptors by inositol 1,4,5 trisphosphate result from a rise in intracellular calcium. J. Gen. Physiol. 88:1986;127-142.
40. Payne R., Flores T.M. The latency of the response of Limulus photoreceptors to inositol trisphosphate lacks the calcium sensitivity of that of light. J. Comp. Physiol. B. 170:1992;311-316.
41. Payne R., Flores T.M., Fein A. Feedback inhibition by calcium limits the release of calcium by inositol trisphosphate in Limulus ventral photoreceptors. Neuron. 4:1990;547-555.
42. Payne R., Potter B.V.L. Injection of inositol trisphosphorothioate into Limulus ventral photoreceptors causes oscillations of free cytosolic calcium. J. Gen. Physiol. 97:1991;1165-1186.
43. Peretz A., Suss-Toby E., Rom-Glass A., Arnon A., Payne R., Minke B. The light response of Drosophila photoreceptors is accompanied by an increase in cellular calcium: effects of specific mutations. Neuron. 12:1994;1257-1267.
44. Polokoff M.A., Bencen G.H., Vacca J.P., deSolms S.J., Young S.D., Huff J.R. Metabolism of synthetic inositol trisphosphate analogs. J. Biol. Chem. 263:1988;11922-11927.
45. Ranganathan R., Backskai B.J., Tsien R.Y., Zuker C.S. Cytosolic calcium transients: spatial localization and role in Drosophila photoreceptor cell function. Neuron. 13:1994;837-848.
46. Ranganathan R., Harris G.L., Stevens C.F., Zuker C.S. A Drosophila mutant defective in extracellular calcium-dependent photoreceptor deactivation and rapid desensitization. Nature. 354:1991;230-232.
47. Shears S.B. Metabolism of the inositol phosphates produced upon receptor activation. Biochem. J. 260:1989;313-324.
48. Shieh B.-H., Niemeyer B. A novel protein encoded by the inaD gene regulates recovery of visual transduction in Drosophila. Neuron. 14:1995;201-210.
49. Shieh B.-H., Zhu M.-Y. Regulation of the TRP calcium channel by INAD in Drosophila photoreceptors. Neuron. 16:1996;991-998.
50. Shimomura O., Johnson F.H., Saiga Y. Excitation, purification and properties of aequorin, a bioluminescent protein from the luminous hydromedusan Aequorea. J. Cell. Comp. Physiol. 59:1962;223-240.
51. Shin J., Richard E.A., Lisman J.E. Calcium is an obligatory intermediate in the excitation cascade of Limulus photoreceptors. Neuron. 11:1993;845-855.
52. Smith D.P., Ranganathan R., Hardy R.W., Marx J., Tsuchida T., Zuker C.S. Photoreceptor deactivation and retinal degeneration mediated by a photoreceptor-specific protein kinase C. Science. 254:1991;1478-1484.
53. Stern J., Chinn K., Bacigalupo J., Lisman J. Distinct lobes of Limulus ventral photoreceptors. I. Functional and anatomical properties of lobes revealed by removal of glial cells. J. Gen. Physiol. 80:1982;825-837.
54. Stieve H., Bruns M. Bump latency distribution and bump adaptation of Limulus ventral photoreceptor in varied extracellular calcium concentrations. Biophys. Struct. Mech. 9:1983;329-339.
55. Storey D.J., Shears S.B., Kirk C.J., Michell R.H. Stepwise enzymatic dephosphorylation of inositol 1,4,5-trisphosphate to inositol in liver. Nature. 312:1984;374-376.
56. Szuts E.Z., Wood S.F., Reid M.S., Fein A. Light stimulates the rapid formation of inositol trisphosphate in squid retinas. Biochem. J. 240:1986;929-932.
57. Ukhanov K., Payne R. Light activated calcium release in Limulus ventral photoreceptors as revealed by laser confocal microscopy. Cell Calcium. 18:1995;301-313.
58. Wood S.F., Szuts E.Z., Fein A. Metabolism of inositol 1,4,5-trisphosphate in squid photoreceptors. J. Comp. Physiol. B. 160:1990;293-298.