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Potentiation of Carbachol-Induced Ca2+ Release by Peroxynitrite in Human Neuroblastoma SH-SY5Y Cells

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Abstract

We have investigated the effect of 3-morpholinosydnonimine (SIN-1), a peroxynitrite donor, on carbachol-induced increase in intracellular Ca2+ concentration ([Ca2+]i) in human neuroblastoma SH-SY5Y cells by means of single cell imaging of [Ca2+]i. SIN-1 potentiated carbachol-induced [Ca2+]i rise regardless of external Ca2+, and the potentiation was completely inhibited by superoxide dismutase, indicating that peroxynitrite may enhance Ca2+ release from intracellular stores. On the other hand, SIN-1 reduced carbachol-induced inositol 1,4,5-trisphosphate (IP3) formation. Genistein, a tyrosine kinase inhibitor, potentiated carbachol-induced rise of [Ca2+]i regardless of external Ca2+. These results suggest that peroxynitrite may potentiate the release of Ca2+ from intracellular stores through the perturbation of regulation in tyrosine phosphorylation-dephosphorylation system.

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REFERENCES

  1. Beckman, J. S., Beckman, T. W., Chen, J., Marshall, P. A., and Freeman, B. A. 1990. Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. Proc. Natl. Acad. Sci. USA 87:1620–1624.

    Google Scholar 

  2. Deliconstantinos, G., Villiotou, V. 1996. NO synthase and xanthine oxidase activities of rabbit brain synaptosomes: peroxynitrite formation as a causative factor of neurotoxicity. Neurochem. Res. 21:51–56.

    Google Scholar 

  3. Nicotera, P. and Lipton, S. A. 1999. Excitotoxins in neuronal apoptosis and necrosis. J. Cereb. Blood Flow Metab. 19:583–591.

    Google Scholar 

  4. Bonfoco, E., Krainc, D., Ankarcrona, M., Nicotera, P. and Lipton, S. A. 1995. Apoptosis and necrosis: two distinct events induced, respectively, by mild and intense insults with N-methyl-D-aspartate or nitric oxide / superoxide in cortical cell cultures. Proc. Natl. Acad. Sci. USA 92:7162–7166.

    Google Scholar 

  5. Guo, Q., Fu, W., Holtsberg, F. W., Steiner, S. M., Mattson, M. P. 1999. Superoxide mediates the cell-death-enhancing action of presenilin-1 mutations. J. Neurosci. Res. 56:457–470.

    Google Scholar 

  6. Beckman, J. S., Ye, Y. Z., Anderson, P. G., Chen, J., Accavitti, M. A., Tarpey, M. M., and White, C. R. 1994. Extensive nitration of protein tyrosines in human atherosclerosis detected by immunohistochemistry. Biol. Chem. Hoppe-Seyler 375:81–88.

    Google Scholar 

  7. Lamarque, D. and Whittle, B. J. 1996. Involvement of peroxynitrite in the lipid peroxidation induced by nitric oxide in rat gastric mucosa. Eur. J. Pharmacol. 313:R5–7.

    Google Scholar 

  8. Ischiropoulos, H. 1998. Biological tyrosine nitration: a pathophysiological function of nitric oxide and reactive oxygen apecies. Arch. Biochem. Biophys. 356:1–11.

    Google Scholar 

  9. Eliasson, M. J., Huang, Z., Ferrante, R. J., Sasamata, M., Molliver, M. E., Snyder, S. H., and Moskowitz, M. A. 1999. Neuronal nitric oxide synthase activation and peroxynitrite formation in ischemic stroke linked to neural damage. J. Neurosci. 15:5910–5918.

    Google Scholar 

  10. Choi, D. W. 1995. Calcium: still center-stage in hypoxic-ischemic neuronal death. Trends. Neurosci. 18:58–60.

    Google Scholar 

  11. Mattson, M. P. 1996. Programmed cell life: anti-apoptotic signaling and therapeutic strategies in neurodegenerative disorders. Retorative Neurol. Neurosci. 9:191–205.

    Google Scholar 

  12. Desole, M. S., Kim, W.-K., Rabin, R. A. and Laychock, S. G. 1994. Nitric oxide reduces depolarization-induced calcium influx in PC12 cells by a cyclic GMP-mediated mechanism. Neuropharmacol. 33:193–198.

    Google Scholar 

  13. Brorson, J. R., Sulit, R. A. and Zhang, H. 1997. Nitric oxide disrupts Ca2??homeostasis in hippocampal neurons. J. Neurochem. 68:95–105.

    Google Scholar 

  14. Guihard, G., Combettes, L., and Capiod, T. 1996. 3',5'-cyclic guanosine monophosphate (cGMP) potentiates the inositol 1,4,5-trisphosphate-evoked Ca2+ release in guinea-pig hepatocytes. Biochem. J. 318:849–855.

    Google Scholar 

  15. Elliott, S. J. 1996. Peroxynitrite modulates receptor-activated Ca2+ signaling in vascular endothelial cells. Am. J. Physiol. 270:L954-L961.

    Google Scholar 

  16. Martin, B. L., Danlin, W., Jakes, S. and Graves, D. J. 1990. Chemical influences on the specificity of tyrosine phosphorylation. J. Biol. Chem. 265:7108–7111.

    Google Scholar 

  17. Gow A. J., Duran D., Malcolm S., Ischiropoulos H. 1996. Effects of peroxynitrite-induced protein modifications on tyrosine phosphorylation and degradation. FEBS Lett 385:63–66.

    Google Scholar 

  18. Kong, S. K., Yim, M. B., Stadtman, E. R. and Chock, P. B. 1996. Peroxynitrite disables the tyrosine phosphorylation regulatory mechanism: lymphocyte-specific tyrosine kinase fails to phosphorylate nitrated cdc2 (6–20) NH2 peptide. Proc. Natl. Acad. Sci. USA 93:3377–3382.

    Google Scholar 

  19. Saeki, M. and Maeda, S. 1999. p130cas is a cellular target protein for tyrosine nitration induced by peroxynitrite. Neurosci. Res. 33:325–328.

    Google Scholar 

  20. Saeki, M. Kamisaki, Y. and Maeda, S. 2000. Involvement of mitogen-activated protein kinase in peroxynitrite-induced cell death of human neuroblastoma SH-SY5Y cells. Neurosci. Res. in press.

  21. Ross, R. A. and Biedler, J. L. 1985. Presence and regulation of tyrosinase activity in human neuroblastoma cell variants in vitro. Cancer Res. 45:1628–1632.

    Google Scholar 

  22. Lambert, D. G., Ghataorre, A. S. and Nahorski S. R. 1989. Muscarinic receptor binding characteristics of a human neuroblastoma SK-N-SH and its clones SH-SY5Y and SH-EP1. Eur. J. Pharmacol. 165:71–77.

    Google Scholar 

  23. Vaughan, P. F., Peers, C. and Walker, J. H. 1995. The use of human neuroblastoma SH-SY5Y to study the effect of second messengers on noradrenaline release. Gen. Pharmacol. 26: 1191–1201.

    Google Scholar 

  24. Grynkiewicz, G., Poenie, M. and Tsien, R. Y. 1985. A new generation of Ca2+ indicators with greatly improved fluorescence properties. J. Biol. Chem. 260:3440–3450.

    Google Scholar 

  25. Lowry, O. H., Rosebrough, N. J., Farr, A. L., Randall, R. J. 1951. Protein measurement with Folin phenol reagent. J. Biol. Chem. 193:265–275.

    Google Scholar 

  26. Lambert, D. G., Nahorski, S. R. 1990. Muscarinic-receptor mediated changes in intracellular and inositol 1,4,5-trisphosphate mass in human neuroblastoma cell line, SH-SY5Y. Biochem. J. 273:791–794.

    Google Scholar 

  27. Murphy, N. P., Vaughan, P. F., Ball, S. G. and McCormack, J. G. 1991. The cholinergic regulation of intracellular calcium in the human neuroblastoma, SHS-Y5Y. J. Neurochem. 57:2116–2123.

    Google Scholar 

  28. Wojcikiewicz, R. J., Tobin, A. B. and Nahorski, S. R. 1994. Muscarinic receptor-mediated inositol 1,4,5-trisphosphate formation in SH-SY5Y neuroblastoma cells is regulated acutely by cytosolic Ca2+ and by rapid desensitization. J. Neurochem. 63:177–185.

    Google Scholar 

  29. Hogg, N., Darley-Usmar, V. M., Wilson, M. T. and Moncada, S. 1992. Production of hydroxyl radicals from the simultaneous generation of superoxide and nitric oxide. Biochem. J. 281:419–424.

    Google Scholar 

  30. Casnellie, J. E. 1991. Protein kinase inhibitor: probes for the functions of protein phosphorylation. Adv. Pharmacol. 22:167–205.

    Google Scholar 

  31. Clementi, E. 1998. Role of nitric oxide and its intracellular signalling pathways in the control of Ca2+ homeostasis. Biochem. Pharmacol. 55:713–718.

    Google Scholar 

  32. Garthwaite, J. 1991. Glutamate, nitric oxide and cell-cell signalling in the nervous system. Trends Neurosci. 14:60–67.

    Google Scholar 

  33. Shaw, P. J., Charles, S. L. and Salt, T. E. 1999. Actions of 8-bromo-cyclic-GMP on neurones in the rat thalamus in vivo and in vitro. Brain Res 833:272–277.

    Google Scholar 

  34. Li, X., Sarno, P. D., Song, L., Beckman, J. S. and Jope, R. S. 1998. Peroxynitrite modulates tyrosine phosphorylation and phosphoinositide signalling in human neuroblastoma SH-SY5Y cells: attenuated effects in human 1321N1 astrocytoma cells. Biochem. J. 331:599–606.

    Google Scholar 

  35. Sheehan, J. P., Swerdlow, R. H., Miller, S. W., Davis, R. E., Parks, J. K., Parker, W. D. and Tuttle, J. B. 1997. Calcium homeostasis and reactive oxygen species production in cells transformed by mitochondria from individuals with sporadic Alzheimer's disease. J. Neurosci. 17:4612–4622.

    Google Scholar 

  36. Mattson, M. P., Guo, Q., Furukawa, K. and Pedersen, W. A. 1998. Presenilins, the endoplasmic reticulum, and neuronal apoptosis in Alzheimer's disease. J. Neurochem. 70:1–14.

    Google Scholar 

  37. Leissring, M. A., Paul, B. A., Parker, I., Cotman, C. W. and LaFerla, F. M. 1999. Alzheimer's presenilin-1 mutation potentiates inositol 1,4,5-trisphosphate-mediated calcium signaling in Xenopus oocytes. J. Neurochem. 72:1061–1068.

    Google Scholar 

  38. Guo, G., Sopher, B. L., Pham, D. G., Furukawa, K., Robinson, N., Martin, G. M. and Mattson, M. P. 1997. Alzheimer's presenilin mutation sensitizes neural cells to apoptosis induced by trophic factor withdrawal and amyloid ?-peptide: involvement of calcium and oxyradicals. J. Neurosci. 17:4212–4222.

    Google Scholar 

  39. Ito, E., Oka, K., Etcheberrigaray, R., Nelson, T. J., McPhie, D. L., Tofel-Grehl, B., Gibson, G. E. and Alkon, D. L. 1994. Internal Ca2+ mobilization is altered in fibroblasts from patients with Alzheimer disease. Proc. Natl. Acad. Sci. USA91: 534–538.

    Google Scholar 

  40. Sorrenti, V., Di-Giacomo, C., Campisi, A., Perez-Polo, J. R. and Vanella, A. 1999. Nitric oxide synthetase activity in cerebral postischemic reperfusion and effects of L-N(G)-nitroarginine and 7-nitroindazole on the survival. Neurochem. Res. 24:861–866.

    Google Scholar 

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Authors and Affiliations

  1. Department of Pharmacology, Faculty of Dentistry, Osaka University, Suita, Osaka, 565-0871, Japan

    Makio Saeki, Yoshinori Kamisaki & Sadaaki Maeda

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  1. Makio Saeki
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  2. Yoshinori Kamisaki
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Saeki, M., Kamisaki, Y. & Maeda, S. Potentiation of Carbachol-Induced Ca2+ Release by Peroxynitrite in Human Neuroblastoma SH-SY5Y Cells. Neurochem Res 25, 909–914 (2000). https://doi.org/10.1023/A:1007540005737

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