The Korean Journal of Physiology and Pharmacology

The Korean Society of Pharmacology (대한약리학회)
권호 표지
DOI QR코드

DOI QR Code

Octyl Gallate Inhibits ATP-induced Intracellular Calcium Increase in PC12 Cells by Inhibiting Multiple Pathways

  • Guo, Yujie (Department of Physiology, College of Medicine, The Catholic University of Korea) ;
  • Hong, Yi-Jae (Department of Physiology, College of Medicine, The Catholic University of Korea) ;
  • Jang, Hyun-Jong (Department of Physiology, College of Medicine, The Catholic University of Korea) ;
  • Kim, Myung-Jun (Department of Physiology, College of Medicine, The Catholic University of Korea) ;
  • Rhie, Duck-Joo (Department of Physiology, College of Medicine, The Catholic University of Korea) ;
  • Jo, Yang-Hyeok (Department of Physiology, College of Medicine, The Catholic University of Korea) ;
  • Hahn, Sang-June (Department of Physiology, College of Medicine, The Catholic University of Korea) ;
  • Yoon, Shin-Hee (Department of Physiology, College of Medicine, The Catholic University of Korea)
  • Published : 2010.02.28
Download PDF
⟨ Previous Next ⟩

Abstract

Phenolic compounds affect intracellular free $Ca^{2+}$ concentration ($[Ca^{2+}]_i$) signaling. The study examined whether the simple phenolic compound octyl gallate affects ATP-induced $Ca^{2+}$ signaling in PC12 cells using fura-2-based digital $Ca^{2+}$ imaging and whole-cell patch clamping. Treatment with ATP ($100\;{\mu}M$) for 90 s induced increases in $[Ca^{2+}]_i$ in PC12 cells. Pretreatment with octyl gallate (100 nM to $20\;{\mu}M$) for 10 min inhibited the ATP-induced $[Ca^{2+}]_i$ response in a concentration-dependent manner ($IC_{50}=2.84\;{\mu}M$). Treatment with octyl gallate ($3\;{\mu}M$) for 10 min significantly inhibited the ATP-induced response following the removal of extracellular $Ca^{2+}$ with nominally $Ca^{2+}$-free HEPES HBSS or depletion of intracellular $Ca^{2+}$ stores with thapsigargin ($1\;{\mu}M$). Treatment for 10 min with the L-type $Ca^{2+}$ channel antagonist nimodipine ($1\;{\mu}M$) significantly inhibited the ATP-induced $[Ca^{2+}]_i$ increase, and treatment with octyl gallate further inhibited the ATP-induced response. Treatment with octyl gallate significantly inhibited the $[Ca^{2+}]_i$ increase induced by 50 mM KCI. Pretreatment with protein kinase C inhibitors staurosporin (100 nM) and GF109203X (300 nM), or the tyrosine kinase inhibitor genistein ($50\;{\mu}M$) did not significantly affect the inhibitory effects of octyl gallate on the ATP-induced response. Treatment with octyl gallate markedly inhibited the ATP-induced currents. Therefore, we conclude that octyl gallate inhibits ATP-induced $[Ca^{2+}]_i$ increase in PC12 cells by inhibiting both non-selective P2X receptor-mediated influx of $Ca^{2+}$ from extracellular space and P2Y receptor-induced release of $Ca^{2+}$ from intracellular stores in protein kinase-independent manner. In addition, octyl gallate inhibits the ATP-induced $Ca^{2+}$ responses by inhibiting the secondary activation of voltage-gated $Ca^{2+}$ channels.

Keywords

References

  1. Jahr CE, Jessell TM. ATP excites a subpopulation of rat dorsal horn neurones. Nature. 1983;304:730-733. https://doi.org/10.1038/304730a0
  2. Inoue K. ATP receptors for the protection of hippocampal functions. Jpn J Pharmacol. 1998;78:405-410. https://doi.org/10.1254/jjp.78.405
  3. Fasolato C, Pizzo P, Pozzan T. Receptor-mediated calcium influx in PC12 cells. ATP and bradykinin activate two independent pathways. J Biol Chem. 1990;265:20351-20355.
  4. Murrin RJ, Boarder MR. Neuronal "nucleotide" receptor linked to phospholipase C and phospholipase D: Stimulation of PC12 cells by ATP analogues and UTP. Mol Pharmacol. 1992;41:561-568.
  5. Kim HJ, Choi JS, Lee YM, Shim EY, Hong SH, Kim MJ, Min DS, Rhie DJ, Kim MS, Jo YH, Hahn SJ, Yoon SH. Fluoxetine inhibits ATP-induced $[Ca^{2+}]_{i}$ increase in PC12 cells by inhibiting both extracellular $Ca^{2+}$ influx and $Ca^{2+}$ release from intracellular stores. Neuropharmacology. 2005;49:265-274. https://doi.org/10.1016/j.neuropharm.2005.03.007
  6. Manach C, Mazur A, Scalbert A. Polyphenols and prevention of cardiovascular diseases. Curr Opin Lipidol. 2005;16:77-84. https://doi.org/10.1097/00041433-200502000-00013
  7. Duthie SJ. Berry phytochemicals, genomic stability and cancer: evidence for chemoprotection at several stages in the carcinogenic process. Mol Nutr Food Res. 2007;51:665-674. https://doi.org/10.1002/mnfr.200600257
  8. Levites Y, Amit T, Mandel S, Youdim MB. Neuroprotection and neurorescue against Abeta toxicity and PKC-dependent release of nonamyloidogenic soluble precursor protein by green tea polyphenol (-)-epigallocatechin-3-gallate. FASEB J. 2003;17:952-954. https://doi.org/10.1096/fj.02-0881fje
  9. Ono K, Yoshiike Y, Takashima A, Hasegawa K, Naiki H, Yamada M. Potent anti-amyloidogenic and fibril-destabilizing effects of polyphenols in vitro: implications for the prevention and therapeutics of Alzheimer's disease. J Neurochem. 2003;87:172-181.
  10. Ramassamy C. Emerging role of polyphenolic compounds in the treatment of neurodegenerative diseases: a review of their intracellular targets. Eur J Pharmacol. 2006;545:51-64. https://doi.org/10.1016/j.ejphar.2006.06.025
  11. Silva JP, Proenca F, Coutinho OP. Protective role of new nitrogen compounds on ROS/RNS-mediated damage to PC12 cells. Free Radic Res. 2008;42:57-69. https://doi.org/10.1080/10715760701787719
  12. Zhao B. Natural antioxidants protect neurons in Alzheimer's disease and Parkinson's disease. Neurochem Res. 2009;34:630-638. https://doi.org/10.1007/s11064-008-9900-9
  13. Bastianetto S, Yao ZX, Papadopoulos V, Quirion R. Neuro-protective effects of green and black teas and their catechin gallate esters against beta-amyloid-induced toxicity. Eur J Neurosci. 2006;23:55-64. https://doi.org/10.1111/j.1460-9568.2005.04532.x
  14. Ko FN, Huang TF, Teng CM. Vasodilatory action mechanisms of apigenin isolated from Apium graveolens in rat thoracic aorta. Biochim Biophys Acta. 1991;1115:69-74. https://doi.org/10.1016/0304-4165(91)90013-7
  15. Saponara S, Sgaragli G, Fusi F. Quercetin as a novel activator of L-type $Ca^{2+}$ channels in rat tail artery smooth muscle cells. Br J Pharmacol. 2002;135:1819-1827. https://doi.org/10.1038/sj.bjp.0704631
  16. Losi G, Puia G, Garzon G, de Vuono MC, Baraldi M. Apigenin modulates GABAergic and glutamatergic transmission in cultured cortical neurons. Eur J Pharmacol. 2004;502:41-46. https://doi.org/10.1016/j.ejphar.2004.08.043
  17. Kim HJ, Yum KS, Sung JH, Rhie DJ, Kim MJ, Min do S, Hahn SJ, Kim MS, Jo YH, Yoon SH. Epigallocatechin-3-gallate increases intracellular $[Ca^{2+}]_{i}$ in U87 cells mainly by influx of extracellular $Ca^{2+}$ and partly by release of intracellular stores. Naunyn Schmiedebergs Arch Pharmacol. 2004;369:260-267. https://doi.org/10.1007/s00210-003-0852-y
  18. Formica JV, Regelson W. Review of the biology of quercetin and related bioflavonoids. Food Chem Toxicol. 1995;33:1061-1080. https://doi.org/10.1016/0278-6915(95)00077-1
  19. Han JH, Kim KJ, Jang HJ, Jang JH, Kim MJ, Sung KW, Rhie DJ, Jo YH, Hahn SJ, Lee MY, Yoon SH. Effects of apigenin on glutamate-induced $[Ca^{2+}]_{i}$ Increases in aultured rat hippocampal neurons. Kor J Physiol Pharmacol. 2008;12:43-50. https://doi.org/10.4196/kjpp.2008.12.2.43
  20. Lin F, Xin Y, Wang J, Ma L, Liu J, Liu C, Long L, Wang F, Jin Y, Zhou J, Chen J. Puerarin facilitates $Ca^{2+}$-induced $Ca^{2+}$ release triggered by KCl-depolarization in primary cultured rat hippocampal neurons. Eur J Pharmacol. 2007;570:43-49. https://doi.org/10.1016/j.ejphar.2007.05.023
  21. Ban JY, Jeon SY, Bae K, Song KS, Seong YH. Catechin and epicatechin from Smilacis chinae rhizome protect cultured rat cortical neurons against amyloid beta protein (25-35)-induced neurotoxicity through inhibition of cytosolic calcium elevation. Life Sci. 2006;79:2251-2259. https://doi.org/10.1016/j.lfs.2006.07.021
  22. Shimmyo Y, Kihara T, Akaike A, Niidome T, Sugimoto H. Three distinct neuroprotective functions of myricetin against glutamate-induced neuronal cell death: involvement of direct inhibition of caspase-3. J Neurosci Res. 2008;86:1836-1845. https://doi.org/10.1002/jnr.21629
  23. Summanen J, Vuorela P, Rauha JP, Tammela P, Marjamaki K, Pasternack M, Tornquist K, Vuorela H. Effects of simple aromatic compounds and flavonoids on $Ca^{2+}$ fluxes in rat pituitary $GH_{4}C_{1}$ cells. Eur J Pharmacol. 2001;414:125-133. https://doi.org/10.1016/S0014-2999(01)00774-9
  24. Majid MA, Okajima F, Kondo Y. Characterization of ATP receptor which mediates norepinephrine release in PC12 cells. Biochim Biophys Acta. 1992;1136:283-289. https://doi.org/10.1016/0167-4889(92)90118-U
  25. Nakazawa K, Inoue K. Roles of $Ca^{2+}$ influx through ATP-activated channels in catecholamine release from pheochromocytoma PC12 cells. J Neurophysiol. 1992;68:2026-2032. https://doi.org/10.1152/jn.1992.68.6.2026
  26. Suh BC, Lee CO, Kim KT. Signal flows from two phospholipase C-linked receptors are independent in PC12 cells. J Neurochem. 1995;64:1071-1079.
  27. Sun AY, Chen YM. Extracellular ATP-induced apoptosis in PC12 cells. Adv Exp Med Biol. 1998;446:73-83. https://doi.org/10.1007/978-1-4615-4869-0_5
  28. Rhie DJ, Sung JH, Kim HJ, Ha US, Min DS, Kim MS, Jo YH, Hahn SJ, Yoon SH. Endogenous somatostatin receptors mobilize calcium from inositol 1,4,5-trisphosphate-sensitive stores in NG108-15 cells. Brain Res. 2003;975:120-128. https://doi.org/10.1016/S0006-8993(03)02596-4
  29. Choi JS, Choi BH, Ahn HS, Kim MJ, Rhie DJ, Yoon SH, Min do S, Jo YH, Kim MS, Sung KW, Hahn SJ. Mechanism of block by fluoxetine of 5-$hydroxytryptamine_{3}$ ($5-HT_{3}$)-mediated currents in NCB-20 neuroblastoma cells. Biochem Pharmacol. 2003;66:2125-2132. https://doi.org/10.1016/j.bcp.2003.08.012
  30. Thastrup O, Cullen PJ, Drobak BK, Hanley MR, Dawson AP. Thapsigargin, a tumor promoter, discharges intracellular $Ca^{2+}$ stores by specific inhibition of the endoplasmic reticulum $Ca^{2+}$-ATPase. Proc Natl Acad Sci U S A. 1990;87:2466-2470. https://doi.org/10.1073/pnas.87.7.2466
  31. Agullo G, Gamet-Payrastre L, Manenti S, Viala C, Remesy C, Chap H, Payrastre B. Relationship between flavonoid structure and inhibition of phosphatidylinositol 3-kinase: a comparison with tyrosine kinase and protein kinase C inhibition. Biochem Pharmacol. 1997;53:1649-1657. https://doi.org/10.1016/S0006-2952(97)82453-7
  32. Munaron L, Distasi C, Carabelli V, Baccino FM, Bonelli G, Lovisolo D. Sustained calcium influx activated by basic fibroblast growth factor in Balb-c 3T3 fibroblasts. J Physiol. 1995;484:557-566. https://doi.org/10.1113/jphysiol.1995.sp020686
  33. Nakazawa K, Fujimori K, Takanaka A, Inoue K. An ATP-activated conductance in pheochromocytoma cells and its suppression by extracellular calcium. J Physiol. 1990;428:257-272. https://doi.org/10.1113/jphysiol.1990.sp018211
  34. Gollasch M, Haller H. Multiple pathways for ATP-induced intracellular calcium elevation in pheochromocytoma (PC12) cells. Ren Physiol Biochem. 1995;18:57-65.
  35. Ferriola PC, Cody V, Middleton E Jr. Protein kinase C inhibition by plant flavonoids. Kinetic mechanisms and structure-activity relationships. Biochem Pharmacol. 1989;38:1617-1624. https://doi.org/10.1016/0006-2952(89)90309-2
  36. Duarte J, Perez Vizcaino F, Utrilla P, Jimenez J, Tamargo J, Zarzuelo A. Vasodilatory effects of flavonoids in rat aortic smooth muscle. Structure-activity relationships. Gen Pharmacol. 1993;24:857-862. https://doi.org/10.1016/0306-3623(93)90159-U
  37. Revuelta MP, Cantabrana B, Hidalgo A. Depolarization-dependent effect of flavonoids in rat uterine smooth muscle contraction elicited by CaCl2. Gen Pharmacol. 1997;29:847-857. https://doi.org/10.1016/S0306-3623(97)00002-5
  38. D'Ambrosi N, Murra B, Cavaliere F, Amadio S, Bernardi G, Burnstock G, Volonte C. Interaction between ATP and nerve growth factor signalling in the survival and neuritic outgrowth from PC12 cells. Neuroscience. 2001;108:527-534. https://doi.org/10.1016/S0306-4522(01)00431-6
  39. Avallone R, Zanoli P, Puia G, Kleinschnitz M, Schreier P, Baraldi M. Pharmacological profile of apigenin, a flavonoid isolated from Matricaria chamomilla. Biochem Pharmacol. 2000;59:1387-1394. https://doi.org/10.1016/S0006-2952(00)00264-1
  40. Paillart C, Carlier E, Guedin D, Dargent B, Couraud F. Direct block of voltage-sensitive sodium channels by genistein, a tyrosine kinase inhibitor. J Pharmacol Exp Ther. 1997;280:521-526.
  41. Choi BH, Choi JS, Min DS, Yoon SH, Rhie DJ, Jo YH, Kim MS, Hahn SJ. Effects of (-)-epigallocatechin-3-gallate, the main component of green tea, on the cloned rat brain Kv1.5 potassium channels. Biochem Pharmacol. 2001;62:527-535. https://doi.org/10.1016/S0006-2952(01)00678-5
  42. Hendrich AB, Malon R, Pola A, Shirataki Y, Motohashi N, Michalak K. Differential interaction of Sophora isoflavonoids with lipid bilayers. Eur J Pharm Sci. 2002;16:201-208. https://doi.org/10.1016/S0928-0987(02)00106-9
  43. Hendrich AB. Flavonoid-membrane interactions: possible consequences for biological effects of some polyphenolic compounds. Acta Pharmacol Sin. 2006;27:27-40. https://doi.org/10.1111/j.1745-7254.2006.00238.x
  44. Tillman TS, Cascio M. Effects of membrane lipids on ion channel structure and function. Cell Biochem Biophys. 2003;38:161-190. https://doi.org/10.1385/CBB:38:2:161
  45. Zhang YX, Yamashita H, Ohshita T, Sawamoto N, Nakamura S. ATP increases extracellular dopamine level through stimulation of P2Y purinoceptors in the rat striatum. Brain Res. 1995;691:205-212. https://doi.org/10.1016/0006-8993(95)00676-H
  46. Cunha RA, Ribeiro JA. ATP as a presynaptic modulator. Life Sci. 2000;68:119-137. https://doi.org/10.1016/S0024-3205(00)00923-1
  47. Choi YM, Jang JY, Jang M, Kim SH, Kang YK, Cho H, Chung S, Park MK. Modulation of firing activity by ATP in dopamine neurons of the rat substantia nigra pars compacta. Neuroscience. 2009;160:587-595. https://doi.org/10.1016/j.neuroscience.2009.02.067

Cited by

  1. Inhibitory Effects of Acorn Extract on Glutamate-Induced Calcium Signaling in Cultured Rat Hippocampal Neurons vol.36, pp.3, 2010, https://doi.org/10.1248/bpb.b12-00263
  2. Low-level laser therapy (810 nm) protects primary cortical neurons against excitotoxicity in vitro : LLLT protects cortical neurons against excitotoxicity vol.7, pp.8, 2010, https://doi.org/10.1002/jbio.201300125
  3. Mango Fruit Extracts Differentially Affect Proliferation and Intracellular Calcium Signalling in MCF-7 Human Breast Cancer Cells vol.2015, pp.None, 2010, https://doi.org/10.1155/2015/613268