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Effect of Inositol 1,3,4,5-Tetrakisphosphate on Inositol Trisphosphate-activated Ca2⁺ Signaling in Mouse Lacrimal Acinar Cells

1996; Elsevier BV; Volume: 271; Issue: 12 Linguagem: Inglês

10.1074/jbc.271.12.6766

1083-351X

Gary S. Bird, James W. Putney,

Erythrocyte Function and Pathophysiology

In mouse lacrimal acinar cells, microinjection of the metabolically stable analog of inositol 1,4,5-trisphosphate, inositol 2,4,5-trisphosphate ((2,4,5)IP3), stimulated both intracellular Ca2⁺ mobilization and Ca2⁺ entry. Microinjection of inositol 1,3,4,5-tetrakisphosphate ((1,3,4,5)IP4), the inositol 1,4,5-trisphosphate-3-kinase product, was ineffective at mobilizing intracellular Ca2⁺ or activating Ca2⁺ entry. In lacrimal cells previously microinjected with submaximal levels of(2.Shears S.B. Adv. Second Messenger Phosphoprotein Res. 1992; 26: 63-92PubMed Google Scholar, 4.Irvine R.F. Cullen P.J. Current Biol. 1993; 3: 540-543Abstract Full Text PDF PubMed Scopus (34) Google Scholar, 5.Irvine R.F. FASEB J. 1992; 6: 3085-3091Crossref PubMed Scopus (166) Google Scholar) IP3, the subsequent microinjection of low to moderate concentrations of (1.Berridge M.J. Nature. 1993; 361: 315-325Crossref PubMed Scopus (6188) Google Scholar, 3.Putney Jr., J.W. Bird G.S.J. Endocr. Rev. 1993; 14: 610-631Crossref PubMed Scopus (486) Google Scholar, 4.Irvine R.F. Cullen P.J. Current Biol. 1993; 3: 540-543Abstract Full Text PDF PubMed Scopus (34) Google Scholar, 5.Irvine R.F. FASEB J. 1992; 6: 3085-3091Crossref PubMed Scopus (166) Google Scholar) IP4 did not result in additional release of intracellular Ca2⁺, nor did it potentiate the Ca2⁺ entry phase attributable to(2.Shears S.B. Adv. Second Messenger Phosphoprotein Res. 1992; 26: 63-92PubMed Google Scholar, 4.Irvine R.F. Cullen P.J. Current Biol. 1993; 3: 540-543Abstract Full Text PDF PubMed Scopus (34) Google Scholar, 5.Irvine R.F. FASEB J. 1992; 6: 3085-3091Crossref PubMed Scopus (166) Google Scholar) IP3. However, as previously demonstrated (Bird, G. S. J., Rossier, M. F., Hughes, A. R., Shears, S. B., Armstrong, D. L., and Putney, J. W., Jr. (1991) Nature 352, 162-165), additional injections of (2.Shears S.B. Adv. Second Messenger Phosphoprotein Res. 1992; 26: 63-92PubMed Google Scholar, 4.Irvine R.F. Cullen P.J. Current Biol. 1993; 3: 540-543Abstract Full Text PDF PubMed Scopus (34) Google Scholar, 5.Irvine R.F. FASEB J. 1992; 6: 3085-3091Crossref PubMed Scopus (166) Google Scholar) IP3 induced further mobilization of intracellular Ca2⁺ and increased the elevated and sustained Ca2⁺ entry phase. Introduction of high concentrations of (1.Berridge M.J. Nature. 1993; 361: 315-325Crossref PubMed Scopus (6188) Google Scholar, 3.Putney Jr., J.W. Bird G.S.J. Endocr. Rev. 1993; 14: 610-631Crossref PubMed Scopus (486) Google Scholar, 4.Irvine R.F. Cullen P.J. Current Biol. 1993; 3: 540-543Abstract Full Text PDF PubMed Scopus (34) Google Scholar, 5.Irvine R.F. FASEB J. 1992; 6: 3085-3091Crossref PubMed Scopus (166) Google Scholar) IP4 appeared to inhibit or block the (2.Shears S.B. Adv. Second Messenger Phosphoprotein Res. 1992; 26: 63-92PubMed Google Scholar, 4.Irvine R.F. Cullen P.J. Current Biol. 1993; 3: 540-543Abstract Full Text PDF PubMed Scopus (34) Google Scholar, 5.Irvine R.F. FASEB J. 1992; 6: 3085-3091Crossref PubMed Scopus (166) Google Scholar) IP3-induced Ca2⁺ entry phase. These results were consistent with the observed effect of (1.Berridge M.J. Nature. 1993; 361: 315-325Crossref PubMed Scopus (6188) Google Scholar, 3.Putney Jr., J.W. Bird G.S.J. Endocr. Rev. 1993; 14: 610-631Crossref PubMed Scopus (486) Google Scholar, 4.Irvine R.F. Cullen P.J. Current Biol. 1993; 3: 540-543Abstract Full Text PDF PubMed Scopus (34) Google Scholar, 5.Irvine R.F. FASEB J. 1992; 6: 3085-3091Crossref PubMed Scopus (166) Google Scholar) IP4 in permeabilized lacrimal cells, where (1.Berridge M.J. Nature. 1993; 361: 315-325Crossref PubMed Scopus (6188) Google Scholar, 3.Putney Jr., J.W. Bird G.S.J. Endocr. Rev. 1993; 14: 610-631Crossref PubMed Scopus (486) Google Scholar, 4.Irvine R.F. Cullen P.J. Current Biol. 1993; 3: 540-543Abstract Full Text PDF PubMed Scopus (34) Google Scholar, 5.Irvine R.F. FASEB J. 1992; 6: 3085-3091Crossref PubMed Scopus (166) Google Scholar) IP4 did not release cellular 45Ca2⁺ but at high concentrations inhibited the ability of submaximal concentrations of(2.Shears S.B. Adv. Second Messenger Phosphoprotein Res. 1992; 26: 63-92PubMed Google Scholar, 4.Irvine R.F. Cullen P.J. Current Biol. 1993; 3: 540-543Abstract Full Text PDF PubMed Scopus (34) Google Scholar, 5.Irvine R.F. FASEB J. 1992; 6: 3085-3091Crossref PubMed Scopus (166) Google Scholar) IP3 to release 45Ca2⁺. Likewise, injection of a high concentration of(1.Berridge M.J. Nature. 1993; 361: 315-325Crossref PubMed Scopus (6188) Google Scholar, 3.Putney Jr., J.W. Bird G.S.J. Endocr. Rev. 1993; 14: 610-631Crossref PubMed Scopus (486) Google Scholar, 4.Irvine R.F. Cullen P.J. Current Biol. 1993; 3: 540-543Abstract Full Text PDF PubMed Scopus (34) Google Scholar, 5.Irvine R.F. FASEB J. 1992; 6: 3085-3091Crossref PubMed Scopus (166) Google Scholar) IP4 prior to injection of (2.Shears S.B. Adv. Second Messenger Phosphoprotein Res. 1992; 26: 63-92PubMed Google Scholar, 4.Irvine R.F. Cullen P.J. Current Biol. 1993; 3: 540-543Abstract Full Text PDF PubMed Scopus (34) Google Scholar, 5.Irvine R.F. FASEB J. 1992; 6: 3085-3091Crossref PubMed Scopus (166) Google Scholar) IP3 blocked both release and influx of Ca2⁺. The inhibitory action of(1.Berridge M.J. Nature. 1993; 361: 315-325Crossref PubMed Scopus (6188) Google Scholar, 3.Putney Jr., J.W. Bird G.S.J. Endocr. Rev. 1993; 14: 610-631Crossref PubMed Scopus (486) Google Scholar, 4.Irvine R.F. Cullen P.J. Current Biol. 1993; 3: 540-543Abstract Full Text PDF PubMed Scopus (34) Google Scholar, 5.Irvine R.F. FASEB J. 1992; 6: 3085-3091Crossref PubMed Scopus (166) Google Scholar) IP4 on Ca2⁺ signaling observed in intact cells occurred at concentrations that might be obtained in agonist-stimulated cells. However, in permeabilized cells,(1.Berridge M.J. Nature. 1993; 361: 315-325Crossref PubMed Scopus (6188) Google Scholar, 3.Putney Jr., J.W. Bird G.S.J. Endocr. Rev. 1993; 14: 610-631Crossref PubMed Scopus (486) Google Scholar, 4.Irvine R.F. Cullen P.J. Current Biol. 1993; 3: 540-543Abstract Full Text PDF PubMed Scopus (34) Google Scholar, 5.Irvine R.F. FASEB J. 1992; 6: 3085-3091Crossref PubMed Scopus (166) Google Scholar) IP4 inhibited Ca2⁺ mobilization at concentrations exceeding those likely to occur in agonist-stimulated cells. These results suggest that physiologically relevant levels of(1.Berridge M.J. Nature. 1993; 361: 315-325Crossref PubMed Scopus (6188) Google Scholar, 3.Putney Jr., J.W. Bird G.S.J. Endocr. Rev. 1993; 14: 610-631Crossref PubMed Scopus (486) Google Scholar, 4.Irvine R.F. Cullen P.J. Current Biol. 1993; 3: 540-543Abstract Full Text PDF PubMed Scopus (34) Google Scholar, 5.Irvine R.F. FASEB J. 1992; 6: 3085-3091Crossref PubMed Scopus (166) Google Scholar) IP4 in the cell cytoplasm do not release Ca2⁺, nor do they potentiate inositol trisphosphate-induced Ca2⁺ entry across the plasma membrane. Rather, the possibility is raised that (1.Berridge M.J. Nature. 1993; 361: 315-325Crossref PubMed Scopus (6188) Google Scholar, 3.Putney Jr., J.W. Bird G.S.J. Endocr. Rev. 1993; 14: 610-631Crossref PubMed Scopus (486) Google Scholar, 4.Irvine R.F. Cullen P.J. Current Biol. 1993; 3: 540-543Abstract Full Text PDF PubMed Scopus (34) Google Scholar, 5.Irvine R.F. FASEB J. 1992; 6: 3085-3091Crossref PubMed Scopus (166) Google Scholar) IP4 or one of its metabolites could function as a negative feedback on Ca2⁺ mobilization by inhibiting inositol 1,4,5-trisphosphate-induced Ca2⁺ release. In mouse lacrimal acinar cells, microinjection of the metabolically stable analog of inositol 1,4,5-trisphosphate, inositol 2,4,5-trisphosphate ((2,4,5)IP3), stimulated both intracellular Ca2⁺ mobilization and Ca2⁺ entry. Microinjection of inositol 1,3,4,5-tetrakisphosphate ((1,3,4,5)IP4), the inositol 1,4,5-trisphosphate-3-kinase product, was ineffective at mobilizing intracellular Ca2⁺ or activating Ca2⁺ entry. In lacrimal cells previously microinjected with submaximal levels of(2.Shears S.B. Adv. Second Messenger Phosphoprotein Res. 1992; 26: 63-92PubMed Google Scholar, 4.Irvine R.F. Cullen P.J. Current Biol. 1993; 3: 540-543Abstract Full Text PDF PubMed Scopus (34) Google Scholar, 5.Irvine R.F. FASEB J. 1992; 6: 3085-3091Crossref PubMed Scopus (166) Google Scholar) IP3, the subsequent microinjection of low to moderate concentrations of (1.Berridge M.J. Nature. 1993; 361: 315-325Crossref PubMed Scopus (6188) Google Scholar, 3.Putney Jr., J.W. Bird G.S.J. Endocr. Rev. 1993; 14: 610-631Crossref PubMed Scopus (486) Google Scholar, 4.Irvine R.F. Cullen P.J. Current Biol. 1993; 3: 540-543Abstract Full Text PDF PubMed Scopus (34) Google Scholar, 5.Irvine R.F. FASEB J. 1992; 6: 3085-3091Crossref PubMed Scopus (166) Google Scholar) IP4 did not result in additional release of intracellular Ca2⁺, nor did it potentiate the Ca2⁺ entry phase attributable to(2.Shears S.B. Adv. Second Messenger Phosphoprotein Res. 1992; 26: 63-92PubMed Google Scholar, 4.Irvine R.F. Cullen P.J. Current Biol. 1993; 3: 540-543Abstract Full Text PDF PubMed Scopus (34) Google Scholar, 5.Irvine R.F. FASEB J. 1992; 6: 3085-3091Crossref PubMed Scopus (166) Google Scholar) IP3. However, as previously demonstrated (Bird, G. S. J., Rossier, M. F., Hughes, A. R., Shears, S. B., Armstrong, D. L., and Putney, J. W., Jr. (1991) Nature 352, 162-165), additional injections of (2.Shears S.B. Adv. Second Messenger Phosphoprotein Res. 1992; 26: 63-92PubMed Google Scholar, 4.Irvine R.F. Cullen P.J. Current Biol. 1993; 3: 540-543Abstract Full Text PDF PubMed Scopus (34) Google Scholar, 5.Irvine R.F. FASEB J. 1992; 6: 3085-3091Crossref PubMed Scopus (166) Google Scholar) IP3 induced further mobilization of intracellular Ca2⁺ and increased the elevated and sustained Ca2⁺ entry phase. Introduction of high concentrations of (1.Berridge M.J. Nature. 1993; 361: 315-325Crossref PubMed Scopus (6188) Google Scholar, 3.Putney Jr., J.W. Bird G.S.J. Endocr. Rev. 1993; 14: 610-631Crossref PubMed Scopus (486) Google Scholar, 4.Irvine R.F. Cullen P.J. Current Biol. 1993; 3: 540-543Abstract Full Text PDF PubMed Scopus (34) Google Scholar, 5.Irvine R.F. FASEB J. 1992; 6: 3085-3091Crossref PubMed Scopus (166) Google Scholar) IP4 appeared to inhibit or block the (2.Shears S.B. Adv. Second Messenger Phosphoprotein Res. 1992; 26: 63-92PubMed Google Scholar, 4.Irvine R.F. Cullen P.J. Current Biol. 1993; 3: 540-543Abstract Full Text PDF PubMed Scopus (34) Google Scholar, 5.Irvine R.F. FASEB J. 1992; 6: 3085-3091Crossref PubMed Scopus (166) Google Scholar) IP3-induced Ca2⁺ entry phase. These results were consistent with the observed effect of (1.Berridge M.J. Nature. 1993; 361: 315-325Crossref PubMed Scopus (6188) Google Scholar, 3.Putney Jr., J.W. Bird G.S.J. Endocr. Rev. 1993; 14: 610-631Crossref PubMed Scopus (486) Google Scholar, 4.Irvine R.F. Cullen P.J. Current Biol. 1993; 3: 540-543Abstract Full Text PDF PubMed Scopus (34) Google Scholar, 5.Irvine R.F. FASEB J. 1992; 6: 3085-3091Crossref PubMed Scopus (166) Google Scholar) IP4 in permeabilized lacrimal cells, where (1.Berridge M.J. Nature. 1993; 361: 315-325Crossref PubMed Scopus (6188) Google Scholar, 3.Putney Jr., J.W. Bird G.S.J. Endocr. Rev. 1993; 14: 610-631Crossref PubMed Scopus (486) Google Scholar, 4.Irvine R.F. Cullen P.J. Current Biol. 1993; 3: 540-543Abstract Full Text PDF PubMed Scopus (34) Google Scholar, 5.Irvine R.F. FASEB J. 1992; 6: 3085-3091Crossref PubMed Scopus (166) Google Scholar) IP4 did not release cellular 45Ca2⁺ but at high concentrations inhibited the ability of submaximal concentrations of(2.Shears S.B. Adv. Second Messenger Phosphoprotein Res. 1992; 26: 63-92PubMed Google Scholar, 4.Irvine R.F. Cullen P.J. Current Biol. 1993; 3: 540-543Abstract Full Text PDF PubMed Scopus (34) Google Scholar, 5.Irvine R.F. FASEB J. 1992; 6: 3085-3091Crossref PubMed Scopus (166) Google Scholar) IP3 to release 45Ca2⁺. Likewise, injection of a high concentration of(1.Berridge M.J. Nature. 1993; 361: 315-325Crossref PubMed Scopus (6188) Google Scholar, 3.Putney Jr., J.W. Bird G.S.J. Endocr. Rev. 1993; 14: 610-631Crossref PubMed Scopus (486) Google Scholar, 4.Irvine R.F. Cullen P.J. Current Biol. 1993; 3: 540-543Abstract Full Text PDF PubMed Scopus (34) Google Scholar, 5.Irvine R.F. FASEB J. 1992; 6: 3085-3091Crossref PubMed Scopus (166) Google Scholar) IP4 prior to injection of (2.Shears S.B. Adv. Second Messenger Phosphoprotein Res. 1992; 26: 63-92PubMed Google Scholar, 4.Irvine R.F. Cullen P.J. Current Biol. 1993; 3: 540-543Abstract Full Text PDF PubMed Scopus (34) Google Scholar, 5.Irvine R.F. FASEB J. 1992; 6: 3085-3091Crossref PubMed Scopus (166) Google Scholar) IP3 blocked both release and influx of Ca2⁺. The inhibitory action of(1.Berridge M.J. Nature. 1993; 361: 315-325Crossref PubMed Scopus (6188) Google Scholar, 3.Putney Jr., J.W. Bird G.S.J. Endocr. Rev. 1993; 14: 610-631Crossref PubMed Scopus (486) Google Scholar, 4.Irvine R.F. Cullen P.J. Current Biol. 1993; 3: 540-543Abstract Full Text PDF PubMed Scopus (34) Google Scholar, 5.Irvine R.F. FASEB J. 1992; 6: 3085-3091Crossref PubMed Scopus (166) Google Scholar) IP4 on Ca2⁺ signaling observed in intact cells occurred at concentrations that might be obtained in agonist-stimulated cells. However, in permeabilized cells,(1.Berridge M.J. Nature. 1993; 361: 315-325Crossref PubMed Scopus (6188) Google Scholar, 3.Putney Jr., J.W. Bird G.S.J. Endocr. Rev. 1993; 14: 610-631Crossref PubMed Scopus (486) Google Scholar, 4.Irvine R.F. Cullen P.J. Current Biol. 1993; 3: 540-543Abstract Full Text PDF PubMed Scopus (34) Google Scholar, 5.Irvine R.F. FASEB J. 1992; 6: 3085-3091Crossref PubMed Scopus (166) Google Scholar) IP4 inhibited Ca2⁺ mobilization at concentrations exceeding those likely to occur in agonist-stimulated cells. These results suggest that physiologically relevant levels of(1.Berridge M.J. Nature. 1993; 361: 315-325Crossref PubMed Scopus (6188) Google Scholar, 3.Putney Jr., J.W. Bird G.S.J. Endocr. Rev. 1993; 14: 610-631Crossref PubMed Scopus (486) Google Scholar, 4.Irvine R.F. Cullen P.J. Current Biol. 1993; 3: 540-543Abstract Full Text PDF PubMed Scopus (34) Google Scholar, 5.Irvine R.F. FASEB J. 1992; 6: 3085-3091Crossref PubMed Scopus (166) Google Scholar) IP4 in the cell cytoplasm do not release Ca2⁺, nor do they potentiate inositol trisphosphate-induced Ca2⁺ entry across the plasma membrane. Rather, the possibility is raised that (1.Berridge M.J. Nature. 1993; 361: 315-325Crossref PubMed Scopus (6188) Google Scholar, 3.Putney Jr., J.W. Bird G.S.J. Endocr. Rev. 1993; 14: 610-631Crossref PubMed Scopus (486) Google Scholar, 4.Irvine R.F. Cullen P.J. Current Biol. 1993; 3: 540-543Abstract Full Text PDF PubMed Scopus (34) Google Scholar, 5.Irvine R.F. FASEB J. 1992; 6: 3085-3091Crossref PubMed Scopus (166) Google Scholar) IP4 or one of its metabolites could function as a negative feedback on Ca2⁺ mobilization by inhibiting inositol 1,4,5-trisphosphate-induced Ca2⁺ release.