Abstract
The tyrosine phosphatase inhibitor BpV(phen) stimulated a concentration-dependent increase of phospholipase C (PLC) activity in bovine adrenal medullary chromaffin cells. This response was accompanied by an increase in PLCγ1 tyrosine phosphorylation and its cytosketetal translocation. Insulin, at high concentrations, stimulated PLC activity to a similar extent as BpV(phen), a response that was also accompanied by an increase in PLCγ1 translocation but not its tyrosine phosphorylation. BpV(phen) strongly enhanced the insulin-stimulated increase in PLC activity and caused a small rise in PLCγ1 translocation above that seen with insulin alone. Despite the synergistic rise in activity PLCγ1 tyrosine phosphorylation did not increase beyond that seen with BpV(phen) alone. These results indicate that PLCγ1 activation in chromaffin cells may be more closely associated with its cytoskeletal translocation than its tyrosine phosphorylation although other factors may also be important for activation of enzyme activity.
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REFERENCES
Rebecchi, M. J. and Pentyala, S. N. 2000 Structure, function, and control of phosphoinositide-specific phospholipase C. Physiol. Rev. 80:1291-1335.
Irvine, R. F. and Schell, M. J. 2001 Back in the water:the return of the inositol phosphates. Nature Rev. Mol. Cell Biol. 2:327-338.
Song, C., Hu, C. D., Masago, M., Kariyai, K., Yamawaki-Kataoka, Y., Shibatohge, M., Wu, D., Satoh, T., and Kataoka, T. 2001. Regulation of a novel human phospholipase C, PLCepsilon, through membrane targeting by Ras. J. Biol. Chem. 276:2752-2757.
Luttrell, L. M., Daaka, Y., and Lefkowitz, R. J. 1999 Regulation of tyrosine kinase cascades by G-protein-coupled receptors. Current Opinion Cell Biol. 11:177-183.
Plevin, R. and Boarder, M. R. 1988 Stimulation of formation of inositol phosphates in primary cultures of bovine adrenal chromaffin cells by angiotensin II, histamine, bradykinin, and carbachol. J. Neurochem. 51:634-641.
Bunn, S. J., Marley, P. D., and Livett, B. G. 1990 Receptor stimulated formation of inositol phosphates in cultures of bovine adrenal medullary cells:The effects of bradykinin, bombesin and neurotensin. Neuropeptides 15:187-194.
Bunn, S. J. and Dunkley, P. R. 1997 Histamine-stimulated phospholipase C signalling in the adrenal chroma. n cell: effects on inositol phospholipid metabolism and tyrosine hydroxylase phosphorylation. Clin. Exp. Pharmacol. Physiol. 24:624-631.
Bunn, S. J., Saunders, H. I., and Dunkley, P. R. 1995 Histamine-stimulated inositol phospholipid metabolism in bovine adrenal medullary cells:A kinetic analysis. J. Neurochem. 65:626-635.
Roberts-Thomson, E. L., Saunders, H. I., Palmer, S. M., Powis, D. A., Dunkley, P. R., and Bunn, S. J. 2000. Ca(2+) in. ux stimulated phospholipase C activity in bovine adrenal chroma. n cells:Responses to K(+)depolarization and histamine. Eur. J. Pharmacol. 398:199-207.
Sasakawa, N., Nakaki, T., Yamamoto, S., and Kato, R. 1989. Calcium uptake-dependent and-independent mechanisms of inositol trisphosphate formation in adrenal chromaffin cells:comparative studies with high K+, carbamylcholine and angiotensin II. Cellular Signalling 1:75-84.
Choi, A. Y., Cahill, A. L., Perry, B. D., and Perlman, R. L. 1993. Histamine evokes greater increases in phosphatidylinositol metabolism and catecholamine secretion in epinephrine-containing than in norepinephrine-containing chromaffin cells. J. Neurochem. 61:541-549.
Zerbes, M., Bunn, S. J., and Powis, D. A. 1998. Histamine causes Ca2+ entry via both a store-operated and a store-independent pathway in bovine adrenal chromaffin cells. Cell Calcium 23:379-386.
Waymire, J. C., Bennett, W. F., Boehme, R., Hankins, L., Gilmer-Waymire, K., and Haycock, J. W. 1983 Bovine adrenal chromaffin cells:high-yield purification and viability in suspension culture. J. Neurosci. Meth. 7:329-351.
Tomas, F. M., Walton, P. E., Dunshea, F. R., and Ballard, F. J. 1997 IGF-I variants which bind poorly to IGF-binding proteins show more potent and prolonged hypoglycaemic action than native IGF-I in pigs and marmoset monkeys. J. Endocrinol. 155:377-386.
Ballard, F. J., Wallace, J. C., Francis, G. L., Read, L. C., and Tomas, F. M. 1996. Des(1-3)IGF-I:a truncated form of insulin-like growth factor-I. Int. J. Biochem. Cell Biol. 28:1085-1087.
Matsuda, M., Paterson, H. F., Rodriguez, R., Fensome, A. C., Ellis, M. V., Swann, K., and Katan, M. 2001 Real time fluorescence imaging of PLC gamma translocation and its interaction with the epidermal growth factor receptor. J. Cell Biol. 153:599-612.
Wang, X. J., Liao, H. J., Chattopadhyay, A., and Carpenter, G. 2001. EGF-dependent translocation of green. uorescent protein-tagged PLC-gamma1 to the plasma membrane and endosomes. Exp. Cell Res. 267:28-36.
Hiller, G. and Sundler, R. 2002. Regulation of phospholipase C-gamma 2 via phosphatidylinositol 3-kinase in macrophages. Cellular Signalling 14:169-173.
Palmier, B., Vacher, M., Harbon, S., and Leiber, D. 1999. A tyrosine kinase signaling pathway, regulated by calcium entry and dissociated from tyrosine phosphorylation of phospholipase Cgamma-1, is involved in inositol phosphate production by activated G protein-coupled receptors in myometrium. J. Pharmacol. Exp. Therapeutics 289:1022-1030.
Morelli, S., Buitrago, C., Vazquez, G., De Boland, A. R., and Boland, R. 2000. Involvement of tyrosine kinase activity in 1alpha, 25(OH)2-vitamin D3 signal transduction in skeletal muscle cells. J. Biological Chem. 275:36021-36028.
Boulven, I., Robin, P., Desmyter, C., Harbon, S., and Leiber, D. 2002. Differential involvement of Src family kinases in pervanadate-mediated responses in rat myometrial cells. Cellular Signalling 14:341-349.
Danielsen, A., Larsen, E., and Gammeltoft, S. 1990. Chromaffin cells express two types of insulin-like growth factor receptors. Brain Res. 518:95-100.
Chabot, J. G., Walker, P., and Pelletier, G. 1986. Distribution of epidermal growth factor binding sites in the adult rat adrenal gland by light microscope autoradiography. Acta Endocrino. 113:391-395.
Haycock, J. W. 1993. Multiple signaling pathways in bovine chroma. n cells regulate tyrosine hydroxylase phosphorylation at Ser19, Ser31, and Ser40. Neurochem. Res. 18:15-26.
Pandiella-Alonso, A., Malgaroli, A., Vicentini, L. M., and Meldolesi, J. 1986. Early rise of cytosolic Ca 2+ induced by NGF in PC12 and chromaffin cells. FEBS Lett. 208:48-51.
Nishibe, S., Wahl, M. I., Wedegaertner, P. B., Kim, J. W., Rhee, S. G., Carpenter, G., and Kim, J. J. 1990. Selectivity of phospholipase C phosphorylation by the epidermal growth factor receptor, the insulin receptor, and their cytoplasmic domains. Proc. Nat. Acad Sci. USA 87:424-428.
Kayali, A. G., Eichhorn, J., Haruta, T., Morris, A. J., Nelson, J. G., Vollenweider, P., Olefsky, J. M., and Webster, N. J. 1998. Association of the insulin receptor with phospholipase C-gamma (PLCgamma)in 3T3-L1 adipocytes suggests a role for PLCgamma in metabolic signaling by insulin. J. Biol. Chem. 273:13808-13818.
Eichhorn, J., Kayali, A. G., Resor, L., Austin, D. A., Rose, D. W., and Webster, N. J. 2002. PLC-gamma1 enzyme activity is required for insulin-induced DNA synthesis. Endocrinology 143:655-664.
Serck-Hanssen, G. and Sovik, O. 1991. Binding of insulin and insulin-like growth factor I in bovine chromaffin cells in primary culture. Internat. J. Biochem. 23:85-91.
Yamamoto, R., Yanagita, T., Kobayashi, H., Yuhi, T., Yokoo, H., and Wada, A. 1996. Upregulation of functional voltage-dependent sodium channels by insulin in cultured bovine adrenal chromaffin cells. J. Neurochem. 67:1401-1408.
Shiraishi, S., Yamamoto, R., Yanagita, T., Yokoo, H., Kobayashi, H., Uezono, Y., and Wada, A. 2001. Down-regulation of cell surface insulin receptors by sarco(endo)plasmic reticulum Ca2+-ATPase inhibitor in adrenal chromaffin cells. Brain Res. 898:152-157.
Fladeby, C., Bjonness, B., and Serck-Hanssen, G. 1996 GLUT1-mediated glucose transport and its regulation by IGF-I in cultured bovine chromaffin cells. J. Cellular Physiol. 169:242-247.
Posner, B. I., Faure, R., Burgess, J. W., Bevan, A. P., Lachance, D., Zhang-Sun, G., Fantus, I. G., Ng, J. B., Hall, D. A., and Lum, B. S. 1994. Peroxovanadium compounds. A new class of potent phosphotyrosine phosphatase inhibitors which are insulin mimetics. J. Biol. Chem. 269:4596-4604.
Mitchell, C. J., Kelly, M. M., Blewitt, M., Wilson, J. R., and Biden, T. J. 2001. Phospholipase C-gamma mediates the hydrolysis of phosphatidylinositol, but not of phosphatidylinositol 4, 5-bisphoshate, in carbamylcholine-stimulated islets of langerhans. J. Biol. Chem. 276:19072-19077.
Chasserot-Golaz, PS., Hubert, P., Thierse, D., Dirrig, S., Vlahos, C. J., Aunis, D., and Bader, M. F. 1998. Possible involvement of phosphatidylinositol 3-kinase in regulated exocytosis:studies in chromaffin cells with inhibitor LY294002. J. Neurochem. 70:2347-2356.
Warashina, A. 2001 Mechanism by which wortmannin and LY294002 inhibit catecholamine secretion in the rat adrenal medullary cells. Cell Calcium 29:239-247.
Rose, S. D., Lejen, T., Zhang, L., and Trifaro, J. M. 2001. Chroma. n cell F-actin disassembly and potentiation of catecholamine release in response to protein kinase C activation by phorbol esters is mediated through myristoylated alaninerich C kinase substrate phosphorylation. J. Biol. Chem. 276:36757-36763.
O 'Connell, G. C., Douglas, S. A., and Bunn, S. J. 2003. The involvement of specific phospholipase C isozymes in catecholamine release from digitonin permeabilized bovine adrenal medullary chromaffin cells. Neurosci. Lett. 342:1-4.
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Roberts-Thomson, E.L., Herd, L.M., Saunders, H.I. et al. The Tyrosine Phosphorylation and Cytoskeletal Translocation of Phospholipase Cγ1 in Bovine Adrenal Medullary Chromaffin Cells. Neurochem Res 29, 1847–1855 (2004). https://doi.org/10.1023/B:NERE.0000042211.76499.c6
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DOI: https://doi.org/10.1023/B:NERE.0000042211.76499.c6