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. 1989 Nov 1;263(3):795–801. doi: 10.1042/bj2630795

Stimulation of generation of inositol phosphates by carbamoylcholine and its inhibition by phorbol esters and iodide in dog thyroid cells.

E Laurent 1, J Mockel 1, K Takazawa 1, C Erneux 1, J E Dumont 1
PMCID: PMC1133501  PMID: 2557011

Abstract

The action of carbamoylcholine (Cchol), NaF and other agonists on the generation of inositol phosphates (IPs) was studied in dog thyroid slices prelabelled with myo-[2-3H]inositol. The stimulation by Cchol (0.1 microM-0.1 mM) of IPs accumulation through activation of a muscarinic receptor [Graff, Mockel, Laurent, Erneux & Dumont (1987) FEBS Lett. 210, 204-210] was pertussis- and cholera-toxin insensitive. Ins(1,4,5)P3, Ins(1,3,4)P3 and InsP4 were generated. NaF (5-20 mM) also increased IPs generation (Graff et al., 1987); this effect was potentiated by AlCl3 (10 microM) and unaffected by pertussis toxin. Although phorbol dibutyrate (5 microM) abolished the cholinergic stimulation of IPs generation (Graff et al., 1987), it did not affect the fluoride-induced response. Cchol and NaF did not require extracellular Ca2+ to exert their effect, and neither KCl-induced membrane depolarization nor ionophore A23187 (10 microM) had any influence on basal IPs levels, or on cholinergic stimulation. However, more stringent Ca2+ depletion with EGTA (0.1 or 1 mM) decreased basal IPs levels as well as the amplitude of the stimulation by Cchol without abolishing it. Dibutyryl cyclic AMP, forskolin, cholera toxin and prostaglandin E1 had no effect on basal IPs levels and did not decrease the response to Cchol. Iodide (4 or 40 microM) also strongly decreased the cholinergic action on IPs, this inhibition being relieved by methimazole (1 mM). Our data suggest that Cchol activates a phospholipase C hydrolysing PtdIns(4,5)P2 in the dog thyroid cell in a cyclic AMP-independent manner. This activation requires no extracellular Ca2+ and depends on a GTP-binding protein insensitive to both cholera toxin and requires no extracellular Ca2+ and depends on a GTP-binding protein insensitive to both cholera toxin and pertussis toxin. The data are consistent with a rapid metabolism of Ins(1,4,5)P3 to Ins(1,3,4)P3 via the Ins(1,4,5)P3 3-kinase pathway, followed by dephosphorylation by a 5-phosphomonoesterase. Indeed, a Ca2+-sensitive InsP3 3-kinase activity was demonstrated in tissue homogenate. Stimulation of protein kinase C and an organified form of iodine inhibit the Cchol-induced IPs generation. The negative feedback of activated protein kinase C could be exerted at the level of the receptor or of the receptor-G-protein interaction.

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Selected References

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  1. Batty I. R., Nahorski S. R., Irvine R. F. Rapid formation of inositol 1,3,4,5-tetrakisphosphate following muscarinic receptor stimulation of rat cerebral cortical slices. Biochem J. 1985 Nov 15;232(1):211–215. doi: 10.1042/bj2320211. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Berridge M. J., Irvine R. F. Inositol trisphosphate, a novel second messenger in cellular signal transduction. Nature. 1984 Nov 22;312(5992):315–321. doi: 10.1038/312315a0. [DOI] [PubMed] [Google Scholar]
  3. Berridge M. J. Phosphatidylinositol hydrolysis: a multifunctional transducing mechanism. Mol Cell Endocrinol. 1981 Nov;24(2):115–140. doi: 10.1016/0303-7207(81)90055-1. [DOI] [PubMed] [Google Scholar]
  4. Bigay J., Deterre P., Pfister C., Chabre M. Fluoroaluminates activate transducin-GDP by mimicking the gamma-phosphate of GTP in its binding site. FEBS Lett. 1985 Oct 28;191(2):181–185. doi: 10.1016/0014-5793(85)80004-1. [DOI] [PubMed] [Google Scholar]
  5. Blackmore P. F., Bocckino S. B., Waynick L. E., Exton J. H. Role of a guanine nucleotide-binding regulatory protein in the hydrolysis of hepatocyte phosphatidylinositol 4,5-bisphosphate by calcium-mobilizing hormones and the control of cell calcium. Studies utilizing aluminum fluoride. J Biol Chem. 1985 Nov 25;260(27):14477–14483. [PubMed] [Google Scholar]
  6. Casey P. J., Gilman A. G. G protein involvement in receptor-effector coupling. J Biol Chem. 1988 Feb 25;263(6):2577–2580. [PubMed] [Google Scholar]
  7. Cochaux P., Van Sande J., Swillens S., Dumont J. E. Iodide-induced inhibition of adenylate cyclase activity in horse and dog thyroid. Eur J Biochem. 1987 Dec 30;170(1-2):435–442. doi: 10.1111/j.1432-1033.1987.tb13718.x. [DOI] [PubMed] [Google Scholar]
  8. Corvilain B., Van Sande J., Dumont J. E. Inhibition by iodide of iodide binding to proteins: the "Wolff-Chaikoff" effect is caused by inhibition of H2O2 generation. Biochem Biophys Res Commun. 1988 Aug 15;154(3):1287–1292. doi: 10.1016/0006-291x(88)90279-3. [DOI] [PubMed] [Google Scholar]
  9. Decoster C., Mockel J., Van Sande J., Unger J., Dumont J. E. The role of calcium and guanosine 3':5'-monophosphate in the action of acetylcholine on thyroid metabolism. Eur J Biochem. 1980 Feb;104(1):199–208. doi: 10.1111/j.1432-1033.1980.tb04416.x. [DOI] [PubMed] [Google Scholar]
  10. Dillon S. B., Murray J. J., Verghese M. W., Snyderman R. Regulation of inositol phosphate metabolism in chemoattractant-stimulated human polymorphonuclear leukocytes. Definition of distinct dephosphorylation pathways for IP3 isomers. J Biol Chem. 1987 Aug 25;262(24):11546–11552. [PubMed] [Google Scholar]
  11. Downes C. P., Michell R. H. The polyphosphoinositide phosphodiesterase of erythrocyte membranes. Biochem J. 1981 Jul 15;198(1):133–140. doi: 10.1042/bj1980133. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Downes C. P., Mussat M. C., Michell R. H. The inositol trisphosphate phosphomonoesterase of the human erythrocyte membrane. Biochem J. 1982 Apr 1;203(1):169–177. doi: 10.1042/bj2030169. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Dumont J. E., Willems C., Van Sande J., Nève P. Regulation of the release of thyroid hormones: role of cyclic AMP. Ann N Y Acad Sci. 1971 Dec 30;185:291–316. doi: 10.1111/j.1749-6632.1971.tb45255.x. [DOI] [PubMed] [Google Scholar]
  14. Erneux C., Delvaux A., Moreau C., Dumont J. E. The dephosphorylation pathway of D-myo-inositol 1,3,4,5-tetrakisphosphate in rat brain. Biochem J. 1987 Nov 1;247(3):635–639. doi: 10.1042/bj2470635. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Erneux C., Van Sande J., Miot F., Cochaux P., Decoster C., Dumont J. E. A mechanism in the control of intracellular cAMP level: the activation of a calmodulin-sensitive phosphodiesterase by a rise of intracellular free calcium. Mol Cell Endocrinol. 1985 Dec;43(2-3):123–134. doi: 10.1016/0303-7207(85)90075-9. [DOI] [PubMed] [Google Scholar]
  16. Graff I., Mockel J., Laurent E., Erneux C., Dumont J. E. Carbachol and sodium fluoride, but not TSH, stimulate the generation of inositol phosphates in the dog thyroid. FEBS Lett. 1987 Jan 5;210(2):204–210. doi: 10.1016/0014-5793(87)81338-8. [DOI] [PubMed] [Google Scholar]
  17. Guillon G., Balestre M. N., Mouillac B., Devilliers G. Activation of membrane phospholipase C by vasopressin. A requirement for guanyl nucleotides. FEBS Lett. 1986 Feb 3;196(1):155–159. doi: 10.1016/0014-5793(86)80232-0. [DOI] [PubMed] [Google Scholar]
  18. Hunter T., Ling N., Cooper J. A. Protein kinase C phosphorylation of the EGF receptor at a threonine residue close to the cytoplasmic face of the plasma membrane. Nature. 1984 Oct 4;311(5985):480–483. doi: 10.1038/311480a0. [DOI] [PubMed] [Google Scholar]
  19. Imai A., Gershengorn M. C. Phosphatidylinositol 4,5-bisphosphate turnover is transient while phosphatidylinositol turnover is persistent in thyrotropin-releasing hormone-stimulated rat pituitary cells. Proc Natl Acad Sci U S A. 1986 Nov;83(22):8540–8544. doi: 10.1073/pnas.83.22.8540. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Irvine R. F., Anggård E. E., Letcher A. J., Downes C. P. Metabolism of inositol 1,4,5-trisphosphate and inositol 1,3,4-trisphosphate in rat parotid glands. Biochem J. 1985 Jul 15;229(2):505–511. doi: 10.1042/bj2290505. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Michell R. H. Inositol phospholipids and cell surface receptor function. Biochim Biophys Acta. 1975 Mar 25;415(1):81–47. doi: 10.1016/0304-4157(75)90017-9. [DOI] [PubMed] [Google Scholar]
  22. Mockel J., Van Sande J., Decoster C., Dumont J. E. Tumor promoters as probes of protein kinase C in dog thyroid cell: inhibition of the primary effects of carbamylocholine and reproduction of some distal effects. Metabolism. 1987 Feb;36(2):137–143. doi: 10.1016/0026-0495(87)90007-2. [DOI] [PubMed] [Google Scholar]
  23. Nishizuka Y. Studies and perspectives of protein kinase C. Science. 1986 Jul 18;233(4761):305–312. doi: 10.1126/science.3014651. [DOI] [PubMed] [Google Scholar]
  24. Nishizuka Y. The role of protein kinase C in cell surface signal transduction and tumour promotion. Nature. 1984 Apr 19;308(5961):693–698. doi: 10.1038/308693a0. [DOI] [PubMed] [Google Scholar]
  25. Paris S., Pouysségur J. Further evidence for a phospholipase C-coupled G protein in hamster fibroblasts. Induction of inositol phosphate formation by fluoroaluminate and vanadate and inhibition by pertussis toxin. J Biol Chem. 1987 Feb 15;262(5):1970–1976. [PubMed] [Google Scholar]
  26. Pirotton S., Raspe E., Demolle D., Erneux C., Boeynaems J. M. Involvement of inositol 1,4,5-trisphosphate and calcium in the action of adenine nucleotides on aortic endothelial cells. J Biol Chem. 1987 Dec 25;262(36):17461–17466. [PubMed] [Google Scholar]
  27. Pisarev M. A. Thyroid autoregulation. J Endocrinol Invest. 1985 Oct;8(5):475–484. doi: 10.1007/BF03348541. [DOI] [PubMed] [Google Scholar]
  28. Raspé E., Roger P. P., Dumont J. E. Carbamylcholine, TRH, PGF2 alpha and fluoride enhance free intracellular Ca++ and Ca++ translocation in dog thyroid cells. Biochem Biophys Res Commun. 1986 Dec 15;141(2):569–577. doi: 10.1016/s0006-291x(86)80211-x. [DOI] [PubMed] [Google Scholar]
  29. Rodesch F., Neve P., Willems C., Dumont J. E. Stimulation of thyroid metabolism by thyrotropin, cyclic 3':5'-AMP, dibutyryl cyclic 3':5'-AMP and prostaglandin E1. Eur J Biochem. 1969 Mar;8(1):26–32. doi: 10.1111/j.1432-1033.1969.tb00491.x. [DOI] [PubMed] [Google Scholar]
  30. Schimmel R. J., Dzierzanowski D., Elliott M. E., Honeyman T. W. Stimulation of phosphoinositide metabolism in hamster brown adipocytes exposed to alpha 1-adrenergic agents and its inhibition with phorbol esters. Biochem J. 1986 Jun 15;236(3):757–764. doi: 10.1042/bj2360757. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Sheela Rani C. S., Boyd A. E., 3rd, Field J. B. Effects of acetylcholine, TSH and other stimulators on intracellular calcium concentration in dog thyroid cells. Biochem Biophys Res Commun. 1985 Sep 30;131(3):1041–1047. doi: 10.1016/0006-291x(85)90195-0. [DOI] [PubMed] [Google Scholar]
  32. Straub R. E., Gershengorn M. C. Thyrotropin-releasing hormone and GTP activate inositol trisphosphate formation in membranes isolated from rat pituitary cells. J Biol Chem. 1986 Feb 25;261(6):2712–2717. [PubMed] [Google Scholar]
  33. Takazawa K., Passareiro H., Dumont J. E., Erneux C. Ca2+/calmodulin-sensitive inositol 1,4,5-trisphosphate 3-kinase in rat and bovine brain tissues. Biochem Biophys Res Commun. 1988 Jun 16;153(2):632–641. doi: 10.1016/s0006-291x(88)81142-2. [DOI] [PubMed] [Google Scholar]
  34. Van Sande J., Dumont J. E. Effects of thyrotropin, prostaglandin E1 and iodide on cyclic 3',5'-AMP concentration in dog thyroid slices. Biochim Biophys Acta. 1973 Jul 28;313(2):320–328. doi: 10.1016/0304-4165(73)90031-7. [DOI] [PubMed] [Google Scholar]
  35. van Sande J., Decoster C., Dumont J. E. Effects of carbamylcholine and ionophore A-23187 on cyclic 3',5'-AMP and cyclic 3',5'-GMP accumulation in dog-thyroid slices. Mol Cell Endocrinol. 1979 Apr;14(1):45–57. doi: 10.1016/0303-7207(79)90057-1. [DOI] [PubMed] [Google Scholar]

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