Hydrogen Peroxide Attenuates Store-operated Calcium Entry and Enhances Calcium Extrusion in Thyroid FRTL-5 Cells

Overview

Journal Biochem J

Specialty Biochemistry

Date 2000 Sep 22

PMID 10998346

Citations 7

Authors

K Tornquist

P J Vainio

S Bjorklund

A Titievsky

B Dugue

R K Tuominen

Affiliations

Soon will be listed here.

Abstract

Redox modulation participates in the regulation of intracellular free calcium concentration ([Ca(2+)](i)) in several cell types. In thyroid cells, including FRTL-5 cells, changes in [Ca(2+)](i) regulate several important functions, including the production of H(2)O(2) (hydrogen peroxide). As H(2)O(2) is of crucial importance for the production of thyroid hormones, we investigated the effects of H(2)O(2) on [Ca(2+)](i) in thyroid FRTL-5 cells. H(2)O(2) itself did not modulate basal [Ca(2+)](i). However, H(2)O(2) attenuated store-operated calcium entry evoked by thapsigargin, both in a sodium-containing buffer and in a sodium-free buffer. The effect of H(2)O(2) was abrogated by the reducing agent beta-mercaptoethanol. H(2)O(2) also attenuated the thapsigargin-evoked entry of barium and manganese. The effect of H(2)O(2) was, at least in part, mediated by activation of protein kinase C (PKC), as H(2)O(2) enhanced the binding of [(3)H]phorbol 12,13-dibutyrate. H(2)O(2) also stimulated the translocation of the isoenzyme PKCepsilon from the cytosolic fraction to the particulate fraction. Furthermore, H(2)O(2) did not attenuate store-operated calcium entry in cells treated with staurosporine or calphostin C, or in cells with down-regulated PKC. H(2)O(2) depolarized the membrane potential in bisoxonol-loaded cells and when patch-clamp in the whole-cell mode was used. The depolarization was attenuated in cells with down-regulated PKC. This depolarization, at least in part, explained the H(2)O(2)-evoked inhibition of calcium entry. In addition, H(2)O(2) enhanced the extrusion of calcium from cells stimulated with thapsigargin and this effect was abolished in cells with down-regulated PKC and after treatment of the cells with the reducing agent beta-mercaptoethanol. In conclusion H(2)O(2) attenuates an increase in [Ca(2+)](i). As H(2)O(2) is produced in thyroid cells in a calcium-dependent manner, our results suggest that H(2)O(2) may participate in the regulation of [Ca(2+)](i) in these cells via a negative-feedback mechanism involving activation of PKC.

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References

Larsson R, Cerutti P . Translocation and enhancement of phosphotransferase activity of protein kinase C following exposure in mouse epidermal cells to oxidants. Cancer Res. 1989; 49(20):5627-32. View

Xu Y, Ware J . Selective inhibition of thrombin receptor-mediated Ca2+ entry by protein kinase C beta. J Biol Chem. 1995; 270(41):23887-90. DOI: 10.1074/jbc.270.41.23887. View

Sugawara M, Yamaguchi D, Lee H, Yanagisawa K, Murakami S, Summer C . Hydrogen peroxide inhibits iodide influx and enhances iodide efflux in cultured FRTL-5 rat thyroid cells. Acta Endocrinol (Copenh). 1990; 122(5):610-6. DOI: 10.1530/acta.0.1220610. View

Takada K, Amino N, Tada H, Miyai K . Relationship between proliferation and cell cycle-dependent Ca2+ influx induced by a combination of thyrotropin and insulin-like growth factor-I in rat thyroid cells. J Clin Invest. 1990; 86(5):1548-55. PMC: 296902. DOI: 10.1172/JCI114874. View

Raspe E, Laurent E, Corvilain B, Verjans B, Erneux C, Dumont J . Control of the intracellular Ca(2+)-concentration and the inositol phosphate accumulation in dog thyrocyte primary culture: evidence for different kinetics of Ca(2+)-phosphatidylinositol cascade activation and for involvement in the regulation of.... J Cell Physiol. 1991; 146(2):242-50. DOI: 10.1002/jcp.1041460208. View

Schmidt K, Traenckner E, Meier B, Baeuerle P . Induction of oxidative stress by okadaic acid is required for activation of transcription factor NF-kappa B. J Biol Chem. 1995; 270(45):27136-42. DOI: 10.1074/jbc.270.45.27136. View

Sakamoto T, Repasky W, Uchida K, Hirata A, Hirata F . Modulation of cell death pathways to apoptosis and necrosis of H2O2-treated rat thymocytes by lipocortin I. Biochem Biophys Res Commun. 1996; 220(3):643-7. DOI: 10.1006/bbrc.1996.0457. View

Liu B, Xu X, Fridman R, Muallem S, Kuo T . Consequences of functional expression of the plasma membrane Ca2+ pump isoform 1a. J Biol Chem. 1996; 271(10):5536-44. DOI: 10.1074/jbc.271.10.5536. View

Parekh A, Penner R . Activation of store-operated calcium influx at resting InsP3 levels by sensitization of the InsP3 receptor in rat basophilic leukaemia cells. J Physiol. 1995; 489 ( Pt 2):377-82. PMC: 1156765. DOI: 10.1113/jphysiol.1995.sp021058. View

10.

Roychoudhury S, Ghosh S, Chakraborti T, Chakraborti S . Role of hydroxyl radical in the oxidant H2O2-mediated Ca2+ release from pulmonary smooth muscle mitochondria. Mol Cell Biochem. 1996; 159(2):95-103. DOI: 10.1007/BF00420911. View

11.

Hoyal C, Thomas A, Forman H . Hydroperoxide-induced increases in intracellular calcium due to annexin VI translocation and inactivation of plasma membrane Ca2+-ATPase. J Biol Chem. 1996; 271(46):29205-10. DOI: 10.1074/jbc.271.46.29205. View

12.

Ward C, Giles W . Ionic mechanism of the effects of hydrogen peroxide in rat ventricular myocytes. J Physiol. 1997; 500 ( Pt 3):631-42. PMC: 1159414. DOI: 10.1113/jphysiol.1997.sp022048. View

13.

Nofer J, Tepel M, Walter M, Seedorf U, Assmann G, Zidek W . Phosphatidylcholine-specific phospholipase C regulates thapsigargin-induced calcium influx in human lymphocytes. J Biol Chem. 1998; 272(52):32861-8. DOI: 10.1074/jbc.272.52.32861. View

14.

Riou C, Remy C, Rabilloud R, Rousset B, Fonlupt P . H2O2 induces apoptosis of pig thyrocytes in culture. J Endocrinol. 1998; 156(2):315-22. DOI: 10.1677/joe.0.1560315. View

15.

Tian L, Philp J, Shipston M . Glucocorticoid block of protein kinase C signalling in mouse pituitary corticotroph AtT20 D16:16 cells. J Physiol. 1999; 516 ( Pt 3):757-68. PMC: 2269291. DOI: 10.1111/j.1469-7793.1999.0757u.x. View

16.

Tornquist K, Vainio P, Titievsky A, Dugue B, Tuominen R . Redox modulation of intracellular free calcium concentration in thyroid FRTL-5 cells: evidence for an enhanced extrusion of calcium. Biochem J. 1999; 339 ( Pt 3):621-8. PMC: 1220198. View

17.

Wartenberg M, Diedershagen H, Hescheler J, Sauer H . Growth stimulation versus induction of cell quiescence by hydrogen peroxide in prostate tumor spheroids is encoded by the duration of the Ca(2+) response. J Biol Chem. 1999; 274(39):27759-67. DOI: 10.1074/jbc.274.39.27759. View

18.

Maechler P, Jornot L, Wollheim C . Hydrogen peroxide alters mitochondrial activation and insulin secretion in pancreatic beta cells. J Biol Chem. 1999; 274(39):27905-13. DOI: 10.1074/jbc.274.39.27905. View

19.

Tuominen R, Hudson P, McMillian M, Ye H, Stachowiak M, Hong J . Long-term activation of protein kinase C by angiotensin II in cultured bovine adrenal medullary cells. J Neurochem. 1991; 56(4):1292-8. DOI: 10.1111/j.1471-4159.1991.tb11424.x. View

20.

Saji M, Ikuyama S, Akamizu T, Kohn L . Increases in cytosolic Ca++ down regulate thyrotropin receptor gene expression by a mechanism different from the cAMP signal. Biochem Biophys Res Commun. 1991; 176(1):94-101. DOI: 10.1016/0006-291x(91)90894-d. View