Abstract
Inositol 1,4,5-trisphosphate [InsP3(1,4,5)] is a major second messenger regulating Ca2+ signaling in excitable and nonexcitable cells. InsP3(1,4,5) is extensively metabolized through a network of phosphorylation and dephosphorylation steps to products with potential second messenger function. Inositol 1,3,4,5-tetrakisphosphate [InsP4(1,3,4,5)], the direct metabolite of InsP3(1,4,5), has also been associated with Ca2+ signaling, but whether InsP4(1,3,4,5) acts in combination with InsP3(1,4,5) or whether it regulates Ca2+ signaling directly and independently is unclear, particularly in neurons. We report that olfactory receptor neurons in the lobster (Panulirus argus) express an InsP4(1,3,4,5) receptor in the plasma membrane that is a functional channel. The channel differs in conductance, kinetics, and voltage sensitivity from two plasma membrane InsP3(1,4,5)-gated channels previously reported in these neurons. In close spatial proximity, the InsP4(1,3,4,5)-and InsP3(1,4,5)-gated channels interact reciprocally to alter the channels' open probabilities in what may be a novel mechanism for regulating Ca2+ entry in neurons.
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Selected References
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- Berridge M. J. Inositol trisphosphate and calcium signalling. Nature. 1993 Jan 28;361(6410):315–325. doi: 10.1038/361315a0. [DOI] [PubMed] [Google Scholar]
- Boekhoff I., Michel W. C., Breer H., Ache B. W. Single odors differentially stimulate dual second messenger pathways in lobster olfactory receptor cells. J Neurosci. 1994 May;14(5 Pt 2):3304–3309. doi: 10.1523/JNEUROSCI.14-05-03304.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bradford P. G., Irvine R. F. Specific binding sites for [3H]inositol(1,3,4,5)tetrakisphosphate on membranes of HL-60 cells. Biochem Biophys Res Commun. 1987 Dec 16;149(2):680–685. doi: 10.1016/0006-291x(87)90421-9. [DOI] [PubMed] [Google Scholar]
- Breer H., Boekhoff I., Tareilus E. Rapid kinetics of second messenger formation in olfactory transduction. Nature. 1990 May 3;345(6270):65–68. doi: 10.1038/345065a0. [DOI] [PubMed] [Google Scholar]
- Changya L., Gallacher D. V., Irvine R. F., Petersen O. H. Inositol 1,3,4,5-tetrakisphosphate and inositol 1,4,5-trisphosphate act by different mechanisms when controlling Ca2+ in mouse lacrimal acinar cells. FEBS Lett. 1989 Jul 17;251(1-2):43–48. doi: 10.1016/0014-5793(89)81425-5. [DOI] [PubMed] [Google Scholar]
- Damase-Michel C., Girolami J. P., Bascands J. L., Tran M. A., Moatti J. P., Pecher C., Berthet P., Tarrade T., Montastruc J. L. Effects of cicletanine on vasoactive systems in conscious sinoaortic-denervated dogs. Fundam Clin Pharmacol. 1991;5(8):719–732. doi: 10.1111/j.1472-8206.1991.tb00760.x. [DOI] [PubMed] [Google Scholar]
- De Waard M., Seagar M., Feltz A., Couraud F. Inositol phosphate regulation of voltage-dependent calcium channels in cerebellar granule neurons. Neuron. 1992 Sep;9(3):497–503. doi: 10.1016/0896-6273(92)90187-i. [DOI] [PubMed] [Google Scholar]
- DeLisle S., Pittet D., Potter B. V., Lew P. D., Welsh M. J. InsP3 and Ins(1,3,4,5)P4 act in synergy to stimulate influx of extracellular Ca2+ in Xenopus oocytes. Am J Physiol. 1992 Jun;262(6 Pt 1):C1456–C1463. doi: 10.1152/ajpcell.1992.262.6.C1456. [DOI] [PubMed] [Google Scholar]
- Donié F., Reiser G. A novel, specific binding protein assay for quantitation of intracellular inositol 1,3,4,5-tetrakisphosphate (InsP4) using a high-affinity InsP4 receptor from cerebellum. FEBS Lett. 1989 Aug 28;254(1-2):155–158. doi: 10.1016/0014-5793(89)81029-4. [DOI] [PubMed] [Google Scholar]
- Ely J. A., Hunyady L., Baukal A. J., Catt K. J. Inositol 1,3,4,5-tetrakisphosphate stimulates calcium release from bovine adrenal microsomes by a mechanism independent of the inositol 1,4,5-trisphosphate receptor. Biochem J. 1990 Jun 1;268(2):333–338. doi: 10.1042/bj2680333. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Enyedi P., Williams G. H. Heterogenous inositol tetrakisphosphate binding sites in the adrenal cortex. J Biol Chem. 1988 Jun 15;263(17):7940–7942. [PubMed] [Google Scholar]
- Fadool D. A., Ache B. W. Plasma membrane inositol 1,4,5-trisphosphate-activated channels mediate signal transduction in lobster olfactory receptor neurons. Neuron. 1992 Nov;9(5):907–918. doi: 10.1016/0896-6273(92)90243-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fadool D. A., Michel W. C., Ache B. W. Odor sensitivity of cultured lobster olfactory receptor neurons is not dependent on process formation. J Exp Biol. 1993 Jan;174:215–233. doi: 10.1242/jeb.174.1.215. [DOI] [PubMed] [Google Scholar]
- Ferris C. D., Huganir R. L., Supattapone S., Snyder S. H. Purified inositol 1,4,5-trisphosphate receptor mediates calcium flux in reconstituted lipid vesicles. Nature. 1989 Nov 2;342(6245):87–89. doi: 10.1038/342087a0. [DOI] [PubMed] [Google Scholar]
- Galione A., McDougall A., Busa W. B., Willmott N., Gillot I., Whitaker M. Redundant mechanisms of calcium-induced calcium release underlying calcium waves during fertilization of sea urchin eggs. Science. 1993 Jul 16;261(5119):348–352. doi: 10.1126/science.8392748. [DOI] [PubMed] [Google Scholar]
- Gawler D. J., Potter B. V., Nahorski S. R. Inositol 1,3,4,5-tetrakisphosphate-induced release of intracellular Ca2+ in SH-SY5Y neuroblastoma cells. Biochem J. 1990 Dec 1;272(2):519–524. doi: 10.1042/bj2720519. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Guse A. H., Roth E., Emmrich F. D-myo-inositol 1,3,4,5-tetrakisphosphate releases Ca2+ from crude microsomes and enriched vesicular plasma membranes, but not from intracellular stores of permeabilized T-lymphocytes and monocytes. Biochem J. 1992 Dec 1;288(Pt 2):489–495. doi: 10.1042/bj2880489. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hamill O. P., Marty A., Neher E., Sakmann B., Sigworth F. J. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch. 1981 Aug;391(2):85–100. doi: 10.1007/BF00656997. [DOI] [PubMed] [Google Scholar]
- Hatt H., Ache B. W. Cyclic nucleotide- and inositol phosphate-gated ion channels in lobster olfactory receptor neurons. Proc Natl Acad Sci U S A. 1994 Jul 5;91(14):6264–6268. doi: 10.1073/pnas.91.14.6264. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Higashida H., Brown D. A. Membrane current responses to intracellular injections of inositol 1,3,4,5-tetrakisphosphate and inositol 1,3,4-trisphosphate in NG108-15 hybrid cells. FEBS Lett. 1986 Nov 24;208(2):283–286. doi: 10.1016/0014-5793(86)81033-x. [DOI] [PubMed] [Google Scholar]
- Hill T. D., Dean N. M., Boynton A. L. Inositol 1,3,4,5-tetrakisphosphate induces Ca2+ sequestration in rat liver cells. Science. 1988 Nov 25;242(4882):1176–1178. doi: 10.1126/science.2847317. [DOI] [PubMed] [Google Scholar]
- Huque T., Bruch R. C. Odorant- and guanine nucleotide-stimulated phosphoinositide turnover in olfactory cilia. Biochem Biophys Res Commun. 1986 May 29;137(1):36–42. doi: 10.1016/0006-291x(86)91172-1. [DOI] [PubMed] [Google Scholar]
- Irvine R. F. 'Quantal' Ca2+ release and the control of Ca2+ entry by inositol phosphates--a possible mechanism. FEBS Lett. 1990 Apr 9;263(1):5–9. doi: 10.1016/0014-5793(90)80692-c. [DOI] [PubMed] [Google Scholar]
- Irvine R. F. Inositol tetrakisphosphate as a second messenger: confusions, contradictions, and a potential resolution. Bioessays. 1991 Aug;13(8):419–427. doi: 10.1002/bies.950130810. [DOI] [PubMed] [Google Scholar]
- Irvine R. F., Moor R. M. Inositol(1,3,4,5)tetrakisphosphate-induced activation of sea urchin eggs requires the presence of inositol trisphosphate. Biochem Biophys Res Commun. 1987 Jul 15;146(1):284–290. doi: 10.1016/0006-291x(87)90723-6. [DOI] [PubMed] [Google Scholar]
- Irvine R. F., Moor R. M. Micro-injection of inositol 1,3,4,5-tetrakisphosphate activates sea urchin eggs by a mechanism dependent on external Ca2+. Biochem J. 1986 Dec 15;240(3):917–920. doi: 10.1042/bj2400917. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lee H. C., Aarhus R., Walseth T. F. Calcium mobilization by dual receptors during fertilization of sea urchin eggs. Science. 1993 Jul 16;261(5119):352–355. doi: 10.1126/science.8392749. [DOI] [PubMed] [Google Scholar]
- Lückhoff A., Clapham D. E. Inositol 1,3,4,5-tetrakisphosphate activates an endothelial Ca(2+)-permeable channel. Nature. 1992 Jan 23;355(6358):356–358. doi: 10.1038/355356a0. [DOI] [PubMed] [Google Scholar]
- Mittman S., Flaming D. G., Copenhagen D. R., Belgum J. H. Bubble pressure measurement of micropipet tip outer diameter. J Neurosci Methods. 1987 Dec;22(2):161–166. doi: 10.1016/0165-0270(87)90010-0. [DOI] [PubMed] [Google Scholar]
- Morris A. P., Gallacher D. V., Irvine R. F., Petersen O. H. Synergism of inositol trisphosphate and tetrakisphosphate in activating Ca2+-dependent K+ channels. Nature. 1987 Dec 17;330(6149):653–655. doi: 10.1038/330653a0. [DOI] [PubMed] [Google Scholar]
- Parker I., Ivorra I. Inositol tetrakisphosphate liberates stored Ca2+ in Xenopus oocytes and facilitates responses to inositol trisphosphate. J Physiol. 1991 Feb;433:207–227. doi: 10.1113/jphysiol.1991.sp018422. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Restrepo D., Miyamoto T., Bryant B. P., Teeter J. H. Odor stimuli trigger influx of calcium into olfactory neurons of the channel catfish. Science. 1990 Sep 7;249(4973):1166–1168. doi: 10.1126/science.2168580. [DOI] [PubMed] [Google Scholar]
- Sharp A. H., McPherson P. S., Dawson T. M., Aoki C., Campbell K. P., Snyder S. H. Differential immunohistochemical localization of inositol 1,4,5-trisphosphate- and ryanodine-sensitive Ca2+ release channels in rat brain. J Neurosci. 1993 Jul;13(7):3051–3063. doi: 10.1523/JNEUROSCI.13-07-03051.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Theibert A. B., Estevez V. A., Ferris C. D., Danoff S. K., Barrow R. K., Prestwich G. D., Snyder S. H. Inositol 1,3,4,5-tetrakisphosphate and inositol hexakisphosphate receptor proteins: isolation and characterization from rat brain. Proc Natl Acad Sci U S A. 1991 Apr 15;88(8):3165–3169. doi: 10.1073/pnas.88.8.3165. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Theibert A. B., Estevez V. A., Mourey R. J., Marecek J. F., Barrow R. K., Prestwich G. D., Snyder S. H. Photoaffinity labeling and characterization of isolated inositol 1,3,4,5-tetrakisphosphate- and inositol hexakisphosphate-binding proteins. J Biol Chem. 1992 May 5;267(13):9071–9079. [PubMed] [Google Scholar]
- Theibert A. B., Estevez V. A., Mourey R. J., Marecek J. F., Barrow R. K., Prestwich G. D., Snyder S. H. Photoaffinity labeling and characterization of isolated inositol 1,3,4,5-tetrakisphosphate- and inositol hexakisphosphate-binding proteins. J Biol Chem. 1992 May 5;267(13):9071–9079. [PubMed] [Google Scholar]
- Theibert A. B., Supattapone S., Ferris C. D., Danoff S. K., Evans R. K., Snyder S. H. Solubilization and separation of inositol 1,3,4,5-tetrakisphosphate- and inositol 1,4,5-trisphosphate-binding proteins and metabolizing enzymes in rat brain. Biochem J. 1990 Apr 15;267(2):441–445. doi: 10.1042/bj2670441. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Theibert A. B., Supattapone S., Worley P. F., Baraban J. M., Meek J. L., Snyder S. H. Demonstration of inositol 1,3,4,5-tetrakisphosphate receptor binding. Biochem Biophys Res Commun. 1987 Nov 13;148(3):1283–1289. doi: 10.1016/s0006-291x(87)80272-3. [DOI] [PubMed] [Google Scholar]
- Timerman A. P., Mayrleitner M. M., Lukas T. J., Chadwick C. C., Saito A., Watterson D. M., Schindler H., Fleischer S. Inositol polyphosphate receptor and clathrin assembly protein AP-2 are related proteins that form potassium-selective ion channels in planar lipid bilayers. Proc Natl Acad Sci U S A. 1992 Oct 1;89(19):8976–8980. doi: 10.1073/pnas.89.19.8976. [DOI] [PMC free article] [PubMed] [Google Scholar]