Bidirectional control of cytosolic free calcium by thyrotropin-releasing hormone in pituitary cells

Abstract

It is now established that a key step in the action of calcium-mobilizing agonists is stimulation of the hydrolysis of phosphatidylinositol 4,5-bisphosphate (PtdIns(4,5)P2) to 1,2-diacylglycerol and inositol 1,4,5-1 ris phosphate (InsP3)1,2. The latter substance acts as a second messenger, controlling the release of calcium from intracellular stores (see ref. 3 for review). The bifurcating nature of the signalling system is exemplified by the fact that the other product of PtdIns(4,5)P2 hydrolysis, 1,2-diacylglycerol, can alter cellular function by activating protein kinase C, the cellular target for several tumour-promoting agents such as the phorbol esters4,5. In various tissues, including GH3 pituitary tumour cells, a synergistic interaction between calcium ions and protein kinase C underlies agonist-induced changes in cell activity4,6–10. The data presented here suggest that when GH3 cells are stimulated by thyrotropin-releasing hormone (TRH), an agonist inducing PtdIns(4,5)P2 hydrolysis11–14, the two limbs of the inositol lipid signalling system interact to control free cytosolic calcium levels ([Ca2+]i). At low levels of TRH receptor occupancy, [Ca2+]i)increases rapidly, then declines relatively slowly. As receptor occupancy increases, the calcium signal becomes more short-lived due to the appearance of a second, inhibitory, component. This latter component, which is enhanced when [Ca2+]i) is elevated by high potassium depolarization, is mimicked by active phorbol esters and by bacterial phospholipase C. It seems likely that protein kinase C subserves a negative feedback role in agonist-induced calcium mobilization.

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References

  1. 1

    Downes, C. P. & Michell, R. H. Cell Calcium 3, 467–502 (1982).

    CAS  Article  Google Scholar 

  2. 2

    Berridge, M. J. Biochem. J. 220, 345–360 (1984).

    CAS  Article  Google Scholar 

  3. 3

    Berridge, M. J. & Irvine, R. F. Nature 312, 315–321 (1984).

    ADS  CAS  Article  Google Scholar 

  4. 4

    Nishizuka, Y. Nature 308, 693–698 (1984).

    ADS  CAS  Article  Google Scholar 

  5. 5

    Castagna, M. et al. J. biol: Chem. 257, 7847–7851 (1982).

    CAS  Google Scholar 

  6. 6

    Kaibuchi, K., Sano, K., Hoshijima, M., Takai, Y. & Nishizuka, Y. Cell Calcium 3, 323–335 (1983).

    Article  Google Scholar 

  7. 7

    Zawalich, W., Brown, C. & Rasmussen, H. Biochem. biophys. Res. Commun. 117, 448–455 (1983).

    CAS  Article  Google Scholar 

  8. 8

    Delbeke, D., Kojima, I., Dannies, P. S. & Rasmussen, H. Biochem. biophys. Res. Commun. 123, 735–741 (1984).

    CAS  Article  Google Scholar 

  9. 9

    Martin, T. F. J. & Kowalchyk, J. A. Endocrinology 115, 1517–1526 (1984).

    CAS  Article  Google Scholar 

  10. 10

    Martin, T. F. J. & Kowalchyk, J. A. Endocrinology 115, 1527–1536 (1984).

    CAS  Article  Google Scholar 

  11. 11

    Rebecchi, M. J. & Gershengorn, M. C. Biochem. J. 216, 299–308 (1983).

    Article  Google Scholar 

  12. 12

    Martin, T. F. J. J. biol. Chem. 258, 14816–14822 (1983).

    CAS  PubMed  Google Scholar 

  13. 13

    Macphee, C. H. & Drummond, A. H. Molec. Pharmac. 25, 193–200 (1984).

    CAS  Google Scholar 

  14. 14

    Drummond, A. H., Bushfield, M. & Macphee, C. H. Molec. Pharmac. 25, 201–208 (1984).

    CAS  Google Scholar 

  15. 15

    Tsien, R. Y., Pozzan, T. & Rink, T. J. J. Cell Biol. 94, 325–334 (1982).

    CAS  Article  Google Scholar 

  16. 16

    Gershengorn, M. C. & Thaw, C. Endocrinology 113, 1522–1524 (1983).

    CAS  Article  Google Scholar 

  17. 17

    Albert, P. R. & Tashjian, A. H. J. biol. Chem. 259, 5827–5832 (1984).

    CAS  PubMed  Google Scholar 

  18. 18

    Schlegel, W. & Wollheim, C. B. J. Cell Biol. 99, 83–87 (1984).

    CAS  Article  Google Scholar 

  19. 19

    Kruskal, B. A., Keith, C. H. & Maxfield, F. R. J. Cell Biol. 99, 1167–1172 (1984).

    CAS  Article  Google Scholar 

  20. 20

    Drummond, A. H., Knox, R. J. & Macphee, C. H. Biochem. Soc. Trans. 13, 58–60 (1985).

    CAS  Article  Google Scholar 

  21. 21

    Gershengorn, M. C., Hoffstein, S. T., Rebecchi, M. J., Geras, E. & Rubin, B. G. J. clin. Invest. 67, 1769–1776 (1981).

    CAS  Article  Google Scholar 

  22. 22

    Tan, K. & Tashjian, A. H. J. biol. Chem. 259, 427–434 (1984).

    CAS  PubMed  Google Scholar 

  23. 23

    Niedel, J. E., Kuhn, L. J. & Vandenbark, G. R. Proc. natn. Acad. Sci. U.S.A. 80, 36–40 (1983).

    ADS  CAS  Article  Google Scholar 

  24. 24

    Sando, J. J. & Young, M. K. Proc. natn. Acad. Sci. U.S.A. 80, 2642–2646 (1983).

    ADS  CAS  Article  Google Scholar 

  25. 25

    Sharkey, N. A., Leach, K. L. & Blumberg, P. M. Proc. natn. Acad. Sci. U.S.A. 81, 607–610 (1984).

    ADS  CAS  Article  Google Scholar 

  26. 26

    Blumberg, P. M. et al. Biochem. Pharmac. 33, 933–940 (1984).

    CAS  Article  Google Scholar 

  27. 27

    White, J. R. et al. J. biol. Chem. 259, 8605–8611 (1984).

    CAS  PubMed  Google Scholar 

  28. 28

    Garrison, J. C., Johnson, D. E. & Campanile, C. P. J. biol. Chem. 259, 3283–3292 (1984).

    CAS  PubMed  Google Scholar 

  29. 29

    Kawahara, Y., Minabuchi, R., Sano, K. & Nishizuka, Y. Biochem. biophys. Res. Commun. 97, 309–317 (1980).

    CAS  Article  Google Scholar 

  30. 30

    Rozengurt, E., Rodriguez-Pena, M. & Smith, K. A. Proc. natn. Acad. Sci. U.S.A. 80, 7244–7248 (1983).

    ADS  CAS  Article  Google Scholar 

  31. 31

    Martin, T. F. J. in Prolactin: Basic & Clinical Correlates (Liviana, Padova, in the press).

  32. 32

    Drust, D. S. & Martin, T. F. J. J. biol. Chem. 259, 14520–14530 (1984).

    CAS  PubMed  Google Scholar 

  33. 33

    Gershengorn, M. C., Geras, E., Purrello, V. S. & Rebecchi, M. J. J. biol. Chem. 259, 10675–10681 (1984).

    CAS  PubMed  Google Scholar 

  34. 34

    Sagi-Eisenberg, R., Lieman, H. & Pecht, I. Nature 313, 59–60 (1985).

    ADS  CAS  Article  Google Scholar 

  35. 35

    Maclntyre, D. E., McNicol, A. & Drummond, A. H. FEBS Lett. 180, 160–164 (1985).

    Article  Google Scholar 

  36. 36

    Drummond, A. H. & Raeburn, C. A. Biochem. J. 224, 129–136 (1984).

    CAS  Article  Google Scholar 

  37. 37

    Limas, C. J. Biochem. Biophys. Res. Commun. 96, 1378–1383 (1980).

    CAS  Article  Google Scholar 

  38. 38

    Lagast, H., Pozzan, T., Waldvogel, F. A. & Lew, P. D. J. clin. Invest. 73, 878–883 (1984).

    CAS  Article  Google Scholar 

Download references

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Drummond, A. Bidirectional control of cytosolic free calcium by thyrotropin-releasing hormone in pituitary cells. Nature 315, 752–755 (1985). https://doi.org/10.1038/315752a0

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