Abstract
Calcium signaling is probably one of the evolutionary oldest and the most common way by which the signal can be transmitted from the cell environment to the cytoplasmic calcium binding effectors. Calcium signal is fast and due to diversity of calcium binding proteins it may have a very broad effect on cell behavior. Being a crucial player in neuronal transmission it is also very important for glia physiology. It is responsible for the cross-talk between neurons and astrocytes, for microglia activation and motility. Changes in calcium signaling are also crucial for the behavior of transformed glioma cells. The present chapter summarizes molecular mechanisms of calcium signal formation present in glial cells with a strong emphasis on extracellular nucleotide-evoked signaling pathways. Some aspects of glioma C6 signaling such as the cross-talk between P2Y1 and P2Y12 nucleotide receptors in calcium signal generation will be discussed in-depth, to show complexity of machinery engaged in formation of this signal. Moreover, possible mechanisms of modulation of the calcium signal in diverse environments there will be presented herein. Finally, the possible role of calcium signal in glioma motility is also discussed. This is a very important issue, since glioma cells, contrary to the vast majority of neoplastic cells, cannot spread in the body with the bloodstream and, at least in early stages of tumor development, may expand only by means of sheer motility.
Keywords
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- 2MeSADP:
-
2-methylthio ADP
- DAG:
-
Diacylglycerol
- ER:
-
Endoplasmic reticulum
- GPCR:
-
G-protein coupled receptor
- IP3 :
-
Inositol (1,4,5) trisphosphate
- IP3R:
-
IP3 receptor
- MLC:
-
Myosin light chain
- NCX:
-
Sodium/calcium exchanger
- PI3K:
-
Phosphatidylinositol 3-kinase
- PIP2 :
-
Phosphatidylinositol 4,5-biphosphate
- PLC:
-
Phospholipase C
- PM:
-
Plasma membrane
- PMCA:
-
Plasma membrane calcium ATPase
- PSF:
-
Point spread function
- RyR:
-
Ryanodine receptor
- SERCA:
-
Sarco/endoplasmic reticulum calcium ATPase
- SOC:
-
Store-operated channel
- SOCE:
-
Store-operated calcium entry
- STIM1,2:
-
Stromal interaction molecule 1,2
- TRP channel:
-
Transient receptor potential channel
- TRPA:
-
Ankyrin transient receptor potential channel
- TRPC:
-
Canonical transient receptor potential channel
- TRPM:
-
Melastatin transient receptor potential channel
- TRPV:
-
Vanilloid transient receptor potential channel
- VGCC:
-
Voltage-gated calcium channels
References
Adinolfi E, Callegari MG, Cirillo M et al (2009) Expression of the P2X7 receptor increases the Ca2+ content of the endoplasmic reticulum, activates NFATc1, and protects from apoptosis. J Biol Chem 284:10120–10128. https://doi.org/10.1074/jbc.M805805200
Adinolfi E, Cirillo M, Woltersdorf R et al (2010) Trophic activity of a naturally occurring truncated isoform of the P2X7 receptor. FASEB J 24:3393–3404. https://doi.org/10.1096/fj.09-153601
Adinolfi E, Raffaghello L, Giuliani AL et al (2012) Expression of P2X7 receptor increases in vivo tumor growth. Cancer Res 72:2957–2969. https://doi.org/10.1158/0008-5472.CAN-11-1947
Aguado F, Espinosa-Parrilla JF, Carmona MA, Soriano E (2002) Neuronal activity regulates correlated network properties of spontaneous calcium transients in astrocytes in situ. J Neurosci 22:9430–9444. https://doi.org/10.1523/JNEUROSCI.22-21-09430.2002
Ajami B, Bennett JL, Krieger C et al (2007) Local self-renewal can sustain CNS microglia maintenance and function throughout adult life. Nat Neurosci 10:1538–1543. https://doi.org/10.1038/nn2014
Allen NJ, Barres BA (2009) Neuroscience: glia—more than just brain glue. Nature 457:675–677. https://doi.org/10.1038/457675a
Bach G (2005) Mucolipin 1: endocytosis and cation channel—a review. Pflügers Arch Eur J Physiol 451:313–317. https://doi.org/10.1007/s00424-004-1361-7
Bae YS, Cantley LG, Chen CS et al (1998) Activation of phospholipase C-gamma by phosphatidylinositol 3,4,5-trisphosphate. J Biol Chem 273:4465–4469. https://doi.org/10.1074/jbc.273.8.4465
Barańska J, Przybyłek K, Sabała P (1999) Capacitative calcium entry. Glioma C6 as a model of nonexcitable cells. Pol J Pharmacol 51:153–162
Barańska J, Czajkowski R, Sabała P (2004) Cross-talks between nucleotide receptor-induced signaling pathways in serum-deprived and non-starved glioma C6 cells. Adv Enzym Regul 44:219–232. https://doi.org/10.1016/j.advenzreg.2003.11.001
Barańska J, Czajkowski R, Pomorski P (2017) P2Y1 receptors – properties and functional activities. Springer, Singapore, pp 71–89
Benfenati V, Caprini M, Dovizio M et al (2011) An aquaporin-4/transient receptor potential vanilloid 4 (AQP4/TRPV4) complex is essential for cell-volume control in astrocytes. Proc Natl Acad Sci U S A 108:2563–2568. https://doi.org/10.1073/pnas.1012867108
Berridge MJ (1993) Inositol trisphosphate and calcium signalling. Nature 361:315–325. https://doi.org/10.1038/361315a0
Berridge MJ (1995) Capacitative calcium entry. Biochem J 312(Pt 1):1–11. https://doi.org/10.1042/bj3120001
Berridge MJ (2009) Inositol trisphosphate and calcium signalling mechanisms. Biochim Biophys Acta, Mol Cell Res 1793:933–940. https://doi.org/10.1016/J.BBAMCR.2008.10.005
Berridge MJ, Lipp P, Bootman MD (2000) The versatility and universality of calcium signalling. Nat Rev Mol Cell Biol 1:11–21. https://doi.org/10.1038/35036035
Bianco F, Fumagalli M, Pravettoni E et al (2005) Pathophysiological roles of extracellular nucleotides in glial cells: differential expression of purinergic receptors in resting and activated microglia. Brain Res Rev 48:144–156. https://doi.org/10.1016/J.BRAINRESREV.2004.12.004
Bird GS, Hwang S-Y, Smyth JT et al (2009) STIM1 is a calcium sensor specialized for digital signaling. Curr Biol 19:1724–1729. https://doi.org/10.1016/j.cub.2009.08.022
Brandao-Burch A, Key ML, Patel JJ et al (2012) The P2X7 receptor is an important regulator of extracellular ATP levels. Front Endocrinol (Lausanne) 3:41. https://doi.org/10.3389/fendo.2012.00041
Brandman O, Liou J, Park WS, Meyer T (2007) STIM2 is a feedback regulator that stabilizes basal cytosolic and endoplasmic reticulum Ca2+ levels. Cell 131:1327–1339. https://doi.org/10.1016/J.CELL.2007.11.039
Burnstock G (2006) Purinergic signalling–an overview. Novartis Found Symp 276:26–48
Burnstock G, Kennedy C (2011) P2X receptors in health and disease. Adv Pharmacol 61:333–372. https://doi.org/10.1016/B978-0-12-385526-8.00011-4
Calloway N, Vig M, Kinet J-P et al (2009) Molecular clustering of STIM1 with Orai1/CRACM1 at the plasma membrane depends dynamically on depletion of Ca2+ stores and on electrostatic interactions. Mol Biol Cell 20:389–399. https://doi.org/10.1091/mbc.E07-11-1132
Caltabiano R, Torrisi A, Condorelli D et al (2010) High levels of connexin 43 mRNA in high grade astrocytomas. Study of 32 cases with in situ hybridization. Acta Histochem 112:529–535. https://doi.org/10.1016/J.ACTHIS.2009.05.008
Carafoli E, Stauffer T (1994) The plasma membrane calcium pump: functional domains, regulation of the activity, and tissue specificity of isoform expression. J Neurobiol 25:312–324. https://doi.org/10.1002/neu.480250311
Carmignoto G, Pasti L, Pozzan T (1998) On the role of voltage-dependent calcium channels in calcium signaling of astrocytes in situ. J Neurosci 18:4637–4645. https://doi.org/10.1523/JNEUROSCI.18-12-04637.1998
Cavaliere F, Dinkel K, Reymann K (2005) Microglia response and P2 receptor participation in oxygen/glucose deprivation-induced cortical damage. Neuroscience 136:615–623. https://doi.org/10.1016/J.NEUROSCIENCE.2005.04.038
Chan WY, Kohsaka S, Rezaie P (2007) The origin and cell lineage of microglia—new concepts. Brain Res Rev 53:344–354. https://doi.org/10.1016/J.BRAINRESREV.2006.11.002
Cheewatrakoolpong B, Gilchrest H, Anthes JC, Greenfeder S (2005) Identification and characterization of splice variants of the human P2X7 ATP channel. Biochem Biophys Res Commun 332:17–27. https://doi.org/10.1016/J.BBRC.2005.04.087
Cisneros-Mejorado A, Pérez-Samartín A, Gottlieb M, Matute C (2015) ATP signaling in brain: release, excitotoxicity and potential therapeutic targets. Cell Mol Neurobiol 35:1–6. https://doi.org/10.1007/s10571-014-0092-3
Clapham DE (2007) SnapShot: mammalian TRP channels. Cell 129:220.e1–220.e2. https://doi.org/10.1016/J.CELL.2007.03.034
Coco S, Calegari F, Pravettoni E et al (2003) Storage and release of ATP from astrocytes in culture. J Biol Chem 278:1354–1362. https://doi.org/10.1074/jbc.M209454200
Cotrina ML, Kang J, Lin JH et al (1998) Astrocytic gap junctions remain open during ischemic conditions. J Neurosci 18:2520–2537. https://doi.org/10.1523/JNEUROSCI.18-07-02520.1998
Covington ED, Wu MM, Lewis RS (2010) Essential role for the CRAC activation domain in store-dependent oligomerization of STIM1. Mol Biol Cell 21:1897–1907. https://doi.org/10.1091/mbc.e10-02-0145
Czajkowski R, Barańska J (2002) Cross-talk between the ATP and ADP nucleotide receptor signalling pathways in glioma C6 cells. Acta Biochim Pol 49:877–889. 024904877
Czajkowski R, Banachewicz W, Ilnytska O et al (2004) Differential effects of P2Y1 and P2Y12 nucleotide receptors on ERK1/ERK2 and phosphatidylinositol 3-kinase signalling and cell proliferation in serum-deprived and nonstarved glioma C6 cells. Br J Pharmacol 141:497–507. https://doi.org/10.1038/sj.bjp.0705639
Daniel JL, Dangelmaier C, Jin J et al (1998) Molecular basis for ADP-induced platelet activation. I. Evidence for three distinct ADP receptors on human platelets. J Biol Chem 273:2024–2029. https://doi.org/10.1074/jbc.273.4.2024
Davalos D, Grutzendler J, Yang G et al (2005) ATP mediates rapid microglial response to local brain injury in vivo. Nat Neurosci 8:752–758. https://doi.org/10.1038/nn1472
Dean GE, Fishkes H, Nelson PJ, Rudnicks G (1984) The hydrogen ion-pumping adenosine Triphosphatase of platelet dense granule membrane: differences from F1F0-and phosphoenzyme-type ATPases. J Biol Chem 259(15):9569–9574
Dixon DA, Haynes DH (1989) Kinetic characterization of the Ca2+-pumping ATPase of cardiac sarcolemma in four states of activation. J Biol Chem 264(23):13612–13622
Dubyak GR (2012) P2X7 receptor regulation of non-classical secretion from immune effector cells. Cell Microbiol 14:1697–1706. https://doi.org/10.1111/cmi.12001
Fabiato A (1983) Calcium-induced release of calcium from the cardiac sarcoplasmic reticulum. Am J Phys 245:C1-14. https://doi.org/10.1152/ajpcell.1983.245.1.C1
Falasca M, Logan SK, Lehto VP et al (1998) Activation of phospholipase C gamma by PI 3-kinase-induced PH domain-mediated membrane targeting. EMBO J 17:414–422. https://doi.org/10.1093/emboj/17.2.414
Feng Y-H, Li X, Wang L et al (2006) A truncated P2X7 receptor variant (P2X7-j) endogenously expressed in cervical cancer cells antagonizes the full-length P2X7 receptor through hetero-oligomerization. J Biol Chem 281:17228–17237. https://doi.org/10.1074/jbc.M602999200
Findeisen F, Minor DL Jr (2010) Progress in the structural understanding of voltage-gated calcium channel (Ca V) function and modulation. Channels 4:459–474. https://doi.org/10.4161/chan.4.6.12867
Finkbeiner S (1992) Calcium waves in astrocytes-filling in the gaps. Neuron 8:1101–1108. https://doi.org/10.1016/0896-6273(92)90131-V
Fox S, Behan MW, Heptinstall S (2004) Inhibition of ADP-induced intracellular Ca2+ responses and platelet aggregation by the P2Y12 receptor antagonists AR-C69931MX and clopidogrel is enhanced by prostaglandin E1. Cell Calcium 35:39–46. https://doi.org/10.1016/S0143-4160(03)00170-2
Franzini-Armstrong C, Protasi F (1997) Ryanodine receptors of striated muscles: a complex channel capable of multiple interactions. Physiol Rev 77:699–729. https://doi.org/10.1152/physrev.1997.77.3.699
Freichel M, Vennekens R, Olausson J et al (2004) Functional role of TRPC proteins in vivo: lessons from TRPC-deficient mouse models. Biochem Biophys Res Commun 322:1352–1358. https://doi.org/10.1016/J.BBRC.2004.08.041
Freije WA, Castro-Vargas FE, Fang Z et al (2004) Gene expression profiling of gliomas strongly predicts survival. Cancer Res 64:6503–6510. https://doi.org/10.1158/0008-5472.CAN-04-0452
Fry T, Evans JH, Sanderson MJ (2001) Propagation of intercellular calcium waves in C6 glioma cells transfected with connexins 43 or 32. Microsc Res Tech 52:289–300. https://doi.org/10.1002/1097-0029(20010201)52:3<289::AID-JEMT1014>3.0.CO;2-0
Gehrmann J, Matsumoto Y, Kreutzberg GW (1995) Microglia: intrinsic immuneffector cell of the brain. Brain Res Rev 20:269–287. https://doi.org/10.1016/0165-0173(94)00015-H
Giuliani AL, Colognesi D, Ricco T et al (2014) Trophic activity of human P2X7 receptor isoforms A and B in osteosarcoma. PLoS One 9:e107224. https://doi.org/10.1371/journal.pone.0107224
Golovina VA (2005) Visualization of localized store-operated calcium entry in mouse astrocytes. Close proximity to the endoplasmic reticulum. J Physiol 564:737–749. https://doi.org/10.1113/jphysiol.2005.085035
Grimm C, Kraft R, Sauerbruch S et al (2003) Molecular and functional characterization of the melastatin-related cation channel TRPM3. J Biol Chem 278:21493–21501. https://doi.org/10.1074/jbc.M300945200
Grimm C, Kraft R, Schultz G, Harteneck C (2005) Activation of the melastatin-related cation channel TRPM3 by D-erythro-sphingosine [corrected]. Mol Pharmacol 67:798–805. https://doi.org/10.1124/mol.104.006734
Grobben B, Claes P, Van Kolen K et al (2001) Agonists of the P2Y(AC)-receptor activate MAP kinase by a ras-independent pathway in rat C6 glioma. J Neurochem 78:1325–1338
Gruszczynska-Biegala J, Pomorski P, Wisniewska MB, Kuznicki J (2011) Differential roles for STIM1 and STIM2 in store-operated calcium entry in rat neurons. PLoS One 6(4):e19285
Gualix J, Pintor J, Miras-Portugal MT (2001) Characterization of nucleotide transport into rat brain synaptic vesicles. J Neurochem 73:1098–1104. https://doi.org/10.1046/j.1471-4159.1999.0731098.x
Gwack Y, Srikanth S, Oh-Hora M et al (2008) Hair loss and defective T- and B-cell function in mice lacking ORAI1. Mol Cell Biol 28:5209–5222. https://doi.org/10.1128/MCB.00360-08
Gyoneva S, Orr AG, Traynelis SF (2009) Differential regulation of microglial motility by ATP/ADP and adenosine. Parkinsonism Relat Disord 15:S195–S199. https://doi.org/10.1016/S1353-8020(09)70813-2
Hakamata Y, Nakai J, Takeshima H, Imoto K (1992) Primary structure and distribution of a novel ryanodine receptor/calcium release channel from rabbit brain. FEBS Lett 312:229–235. https://doi.org/10.1016/0014-5793(92)80941-9
Hambardzumyan D, Gutmann DH, Kettenmann H (2016) The role of microglia and macrophages in glioma maintenance and progression. Nat Neurosci 19:20–27. https://doi.org/10.1038/nn.4185
Hamilton SL (2005) Ryanodine receptors. Cell Calcium 38:253–260. https://doi.org/10.1016/J.CECA.2005.06.037
Hao L, Rigauds J-L, Inesi G (1994) Ca2+/H+ countertransport and electrogenicity in proteoliposomes containing erythrocyte plasma membrane Ca-ATPase and exogenous lipids. J Biol Chem 269:14268–14275
Hardy AR, Jones ML, Mundell SJ et al (2004) Reciprocal cross-talk between P2Y1 and P2Y12 receptors at the level of calcium signaling in human platelets. Blood 104:1745–1752. https://doi.org/10.1182/blood-2004-02-0534
Hartline DK (2011) The evolutionary origins of glia. Glia 59:1215–1236. https://doi.org/10.1002/glia.21149
Hirose M, Ishizaki T, Watanabe N et al (1998) Molecular dissection of the Rho-associated protein kinase (p160ROCK)-regulated neurite remodeling in neuroblastoma N1E-115 cells. J Cell Biol 141:1625–1636. https://doi.org/10.1083/jcb.141.7.1625
Hogan PG, Lewis RS, Rao A (2010) Molecular basis of calcium signaling in lymphocytes: STIM and ORAI. Annu Rev Immunol 28:491–533. https://doi.org/10.1146/annurev.immunol.021908.132550
Hollopeter G, Jantzen H-M, Vincent D et al (2001) Identification of the platelet ADP receptor targeted by antithrombotic drugs. Nature 409:202–207. https://doi.org/10.1038/35051599
Huang GN, Zeng W, Kim JY et al (2006) STIM1 carboxyl-terminus activates native SOC, Icrac and TRPC1 channels. Nat Cell Biol 8:1003–1010. https://doi.org/10.1038/ncb1454
Huang C, Hu Z, Wu W-N et al (2010) Existence and distinction of acid-evoked currents in rat astrocytes. Glia 58:1415–1424. https://doi.org/10.1002/glia.21017
Illes P, Verkhratsky A, Burnstock G, Franke H (2012) P2X receptors and their roles in astroglia in the central and peripheral nervous system. Neuroscientist 18:422–438. https://doi.org/10.1177/1073858411418524
Imagawa T, Smith JS, Coronado R, Campbell KP (1987) Purified ryanodine receptor from skeletal muscle sarcoplasmic reticulum is the Ca2+-permeable pore of the calcium release channel. J Biol Chem 262:16636–16643
Inui M, Saito A, Fleischer S (1987a) Purification of the ryanodine receptor and identity with feet structures of junctional terminal cisternae of sarcoplasmic reticulum from fast skeletal muscle. J Biol Chem 262:1740–1747
Inui M, Saito A, Fleischer S (1987b) Isolation of the ryanodine receptor from cardiac sarcoplasmic reticulum and identity with the feet structures. J Biol Chem 262:15637–15642
James PH, Pruschy M, Vorherr TE et al (1989) Primary structure of the cAMP-dependent phosphorylation site of the plasma membrane calcium pump. Biochemistry 28:4253–4258
Jiang S, Yuan H, Duan L et al (2011) Glutamate release through connexin 43 by cultured astrocytes in a stimulated hypertonicity model. Brain Res 1392:8–15. https://doi.org/10.1016/J.BRAINRES.2011.03.056
Jin J, Tomlinson W, Kirk IP et al (2001) The C6-2B glioma cell P2Y AC receptor is pharmacologically and molecularly identical to the platelet P2Y 12 receptor. Br J Pharmacol 133:521–528. https://doi.org/10.1038/sj.bjp.0704114
Joseph SM, Buchakjian MR, Dubyak GR (2003) Colocalization of ATP release sites and ecto-ATPase activity at the extracellular surface of human astrocytes. J Biol Chem 278:23331–23342. https://doi.org/10.1074/jbc.M302680200
Kawate T (2017) P2X receptor activation. Springer, Singapore, pp 55–69
Kiedrowski L, Czyż A, Baranauskas G et al (2004) Differential contribution of plasmalemmal Na+/Ca2+ exchange isoforms to sodium-dependent calcium influx and NMDA excitotoxicity in depolarized neurons. J Neurochem 90:117–128. https://doi.org/10.1111/j.1471-4159.2004.02462.x
Kirichok Y, Krapivinsky G, Clapham DE (2004) The mitochondrial calcium uniporter is a highly selective ion channel. Nature 427:360–364. https://doi.org/10.1038/nature02246
Korczyński J, Sobierajska K, Krzemiński P, Wasik A, Wypych D, Pomorski P, Kłopocka W (2011) Is MLC phosphorylation essential for the recovery from ROCK inhibition in glioma C6 cells? Acta Biochim Pol 58(1)
Korzeniowski MK, Manjarrés IM, Varnai P, Balla T (2010) Activation of STIM1-Orai1 involves an intramolecular switching mechanism. Sci Signal 3:ra82–ra82. https://doi.org/10.1126/SCISIGNAL.2001122
Krane SM, Glimcher MJ (1962) Transphosphorylation from nucleoside Di- and triphosphates by apatite crystals. J Biol Chem 237:2991–2998
Krzemiński P, Supłat D, Czajkowski R et al (2007) Expression and functional characterization of P2Y1 and P2Y 12 nucleotide receptors in long-term serum-deprived glioma C6 cells. FEBS J 274:1970–1982. https://doi.org/10.1111/j.1742-4658.2007.05741.x
Läuger P (1991) Kinetic basis of voltage dependence of the Na,K-pump. Soc Gen Physiol Ser 46:303–315
Lazarowski E (2006) Regulated release of nucleotides and UDP sugars from astrocytoma cells. Novartis Found Symp 276:73–84; discussion 84-90, 107–12, 275–81
Lazarowski ER, Shea DA, Boucher RC, Harden TK (2003) Release of cellular UDP-glucose as a potential extracellular signaling molecule. Mol Pharmacol 63:1190–1197. https://doi.org/10.1124/MOL.63.5.1190
Lazarowski ER, Sesma JI, Seminario-Vidal L, Kreda SM (2011) Molecular mechanisms of purine and pyrimidine nucleotide release. Adv Pharmacol 61:221–261. https://doi.org/10.1016/B978-0-12-385526-8.00008-4
Lewis RS (2001) Calcium signaling mechanisms in T lymphocytes. Annu Rev Immunol 19:497–521. https://doi.org/10.1146/annurev.immunol.19.1.497
Liao Z, Seye CI, Weisman GA et al (2007) The P2Y2 nucleotide receptor requires interaction with alpha v integrins to access and activate G12. J Cell Sci 120:1654–1662. https://doi.org/10.1242/jcs.03441
Lin T, Zhang W, Garrido R et al (2003) The role of the cytoskeleton in capacitaftive calcium entry in myenteric glia. Neurogastroenterol Motil 15:277–287. https://doi.org/10.1046/j.1365-2982.2003.00406.x
Linde CI, Baryshnikov SG, Mazzocco-Spezzia A, Golovina VA (2011) Dysregulation of Ca 2+ signaling in astrocytes from mice lacking amyloid precursor protein. Am J Physiol Cell Physiol 300:C1502–C1512. https://doi.org/10.1152/ajpcell.00379.2010
Liou J, Kim ML, Do Heo W et al (2005) STIM is a Ca2+ sensor essential for Ca2+-store-depletion-triggered Ca2+ influx. Curr Biol 15:1235–1241. https://doi.org/10.1016/J.CUB.2005.05.055
McCully KS (2009) Chemical pathology of homocysteine. IV. Excitotoxicity, oxidative stress, endothelial dysfunction, and inflammation. Ann Clin Lab Sci 39:219–232
Meissner G (2017) The structural basis of ryanodine receptor ion channel function. J Gen Physiol 149:1065–1089. https://doi.org/10.1085/JGP.201711878
Mildner A, Schmidt H, Nitsche M et al (2007) Microglia in the adult brain arise from Ly-6ChiCCR2+ monocytes only under defined host conditions. Nat Neurosci 10:1544–1553. https://doi.org/10.1038/nn2015
Möller T, Kann O, Verkhratsky A, Kettenmann H (2000) Activation of mouse microglial cells affects P2 receptor signaling. Brain Res 853:49–59. https://doi.org/10.1016/S0006-8993(99)02244-1
Monteith GR, Roufogalis BD (1995) The plasma membrane calcium pump - a physiological perspective on its regulation. Cell Calcium 18:459–470. https://doi.org/10.1016/0143-4160(95)90009-8
Morigiwa K, Quan M, Murakami M et al (2000) P2 purinoceptor expression and functional changes of hypoxia-activated cultured rat retinal microglia. Neurosci Lett 282:153–156. https://doi.org/10.1016/S0304-3940(00)00887-9
Muik M, Fahrner M, Schindl R et al (2011) STIM1 couples to ORAI1 via an intramolecular transition into an extended conformation. EMBO J 30:1678–1689. https://doi.org/10.1038/EMBOJ.2011.79
Nazıroğlu M (2011) TRPM2 cation channels, oxidative stress and neurological diseases: where are we now? Neurochem Res 36:355–366. https://doi.org/10.1007/s11064-010-0347-4
Nimmerjahn A, Kirchhoff F, Helmchen F (2005) Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 308:1314–1318. https://doi.org/10.1126/science.1110647
Nwokonko RM, Cai X, Loktionova NA et al (2017) The STIM-Orai pathway: conformational coupling between STIM and Orai in the activation of store-operated Ca2+ entry. Springer, Cham, pp 83–98
Oh-Hora M, Lu X (2018) Function of Orai/Stim proteins studied in transgenic animal models. In: Calcium entry channels in non-excitable cells. https://doi.org/10.1201/9781315152592-6
Ohana L, Newell EW, Stanley EF, Schlichter LC (2009) The Ca 2+ release-activated Ca 2+ current (I CRAC) mediates store-operated Ca 2+ entry in rat microglia. Channels 3:129–139. https://doi.org/10.4161/chan.3.2.8609
Panopoulos A, Howell M, Fotedar R, Margolis RL (2011) Glioblastoma motility occurs in the absence of actin polymer. Mol Biol Cell 22:2212–2220. https://doi.org/10.1091/mbc.e10-10-0849
Parpura V, Grubišić V, Verkhratsky A (2011) Ca2+ sources for the exocytotic release of glutamate from astrocytes. Biochim Biophys Acta, Mol Cell Res 1813:984–991. https://doi.org/10.1016/J.BBAMCR.2010.11.006
Parri HR, Gould TM, Crunelli V (2001) Spontaneous astrocytic Ca2+ oscillations in situ drive NMDAR-mediated neuronal excitation. Nat Neurosci 4:803–812. https://doi.org/10.1038/90507
Parys B, Côté A, Gallo V et al (2010) Intercellular calcium signaling between astrocytes and oligodendrocytes via gap junctions in culture. Neuroscience 167:1032–1043. https://doi.org/10.1016/J.NEUROSCIENCE.2010.03.004
Pinton P, Ferrari D, Magalhães P et al (2000) Reduced loading of intracellular Ca(2+) stores and downregulation of capacitative Ca(2+) influx in Bcl-2-overexpressing cells. J Cell Biol 148:857–862. https://doi.org/10.1083/jcb.148.5.857
Pizzo P, Burgo A, Pozzan T, Fasolato C (2008) Role of capacitative calcium entry on glutamate-induced calcium influx in type-I rat cortical astrocytes. J Neurochem 79:98–109. https://doi.org/10.1046/j.1471-4159.2001.00539.x
Potier M, Trebak M (2008) New developments in the signaling mechanisms of the store-operated calcium entry pathway. Pflügers Arch Eur J Physiol 457:405–415. https://doi.org/10.1007/s00424-008-0533-2
Putney JW (1990) Capacitative calcium entry revisited. Cell Calcium 11:611–624
Putney JW (2009) Capacitative calcium entry: from concept to molecules. Immunol Rev 231:10–22. https://doi.org/10.1111/j.1600-065X.2009.00810.x
Putney JW, Bird GSJ (1993) The inositol phosphate-calcium signaling system in nonexcitable cells. Endocr Rev 14:610–631. https://doi.org/10.1210/edrv-14-5-610
Rao JN, Platoshyn O, Golovina VA et al (2006) TRPC1 functions as a store-operated Ca 2+ channel in intestinal epithelial cells and regulates early mucosal restitution after wounding. Am J Physiol Gastrointest Liver Physiol 290:G782–G792. https://doi.org/10.1152/ajpgi.00441.2005
Ribeiro CM, Reece J, Putney JW (1997) Role of the cytoskeleton in calcium signaling in NIH 3T3 cells. An intact cytoskeleton is required for agonist-induced [Ca2+]i signaling, but not for capacitative calcium entry. J Biol Chem 272:26555–26561. https://doi.org/10.1074/jbc.272.42.26555
Roos J, DiGregorio PJ, Yeromin AV et al (2005) STIM1, an essential and conserved component of store-operated Ca2+ channel function. J Cell Biol 169:435–445. https://doi.org/10.1083/jcb.200502019
Rosado JA, Jenner S, Sage SO (2000) A role for the actin cytoskeleton in the initiation and maintenance of store-mediated calcium entry in human platelets. Evidence for conformational coupling. J Biol Chem 275:7527–7533. https://doi.org/10.1074/jbc.275.11.7527
Roy P, Rajfur Z, Pomorski P, Jacobson K (2002) Microscope-based techniques to study cell adhesion and migration. Nat Cell Biol 4:E91–E96. https://doi.org/10.1038/ncb0402-e91
Sabala P, Czajkowski R, Przybyłek K et al (2001) Two subtypes of G protein-coupled nucleotide receptors, P2Y(1) and P2Y(2) are involved in calcium signalling in glioma C6 cells. Br J Pharmacol 132:393–402. https://doi.org/10.1038/sj.bjp.0703843
Sabała P, Targos B, Caravelli A et al (2002) Role of the actin cytoskeleton in store-mediated calcium entry in glioma C6 cells. Biochem Biophys Res Commun 296:484–491. https://doi.org/10.1016/S0006-291X(02)00893-8
Sage SO, Yamoah EH, Heemskerk JWM (2000) The roles of P2X1and P2T ACreceptors in ADP-evoked calcium signalling in human platelets. Cell Calcium 28:119–126. https://doi.org/10.1054/CECA.2000.0139
Sak K, Illes P (2005) Neuronal and glial cell lines as model systems for studying P2Y receptor pharmacology. Neurochem Int 47:401–412. https://doi.org/10.1016/J.NEUINT.2005.05.012
Sappington RM, Calkins DJ (2008) Contribution of TRPV1 to microglia-derived IL-6 and NFκB translocation with elevated hydrostatic pressure. Invest Opthalmol Vis Sci 49:3004. https://doi.org/10.1167/iovs.07-1355
Scemes E, Suadicani SO, Spray DC (2000) Intercellular communication in spinal cord astrocytes: fine tuning between gap junctions and P2 nucleotide receptors in calcium wave propagation. J Neurosci 20:1435–1445. https://doi.org/10.1523/JNEUROSCI.20-04-01435.2000
Shin Y-C, Shin S-Y, So I et al (2011) TRIP database: a manually curated database of protein–protein interactions for mammalian TRP channels. Nucleic Acids Res 39:D356–D361. https://doi.org/10.1093/nar/gkq814
Soboloff J, Spassova MA, Hewavitharana T et al (2006) STIM2 is an inhibitor of STIM1-mediated store-operated Ca2+ entry. Curr Biol 16:1465–1470. https://doi.org/10.1016/J.CUB.2006.05.051
Sontheimer H (1994) Voltage-dependent ion channels in glial cells. Glia 11:156–172. https://doi.org/10.1002/glia.440110210
Stathopulos PB, Zheng L, Ikura M (2009) Stromal interaction molecule (STIM) 1 and STIM2 calcium sensing regions exhibit distinct unfolding and oligomerization kinetics. J Biol Chem 284:728–732. https://doi.org/10.1074/JBC.C800178200
Steinbeck JA, Henke N, Opatz J et al (2011) Store-operated calcium entry modulates neuronal network activity in a model of chronic epilepsy. Exp Neurol 232:185–194. https://doi.org/10.1016/J.EXPNEUROL.2011.08.022
Stiber J, Hawkins A, Zhang Z-S et al (2008) STIM1 signalling controls store-operated calcium entry required for development and contractile function in skeletal muscle. Nat Cell Biol 10:688–697. https://doi.org/10.1038/ncb1731
Striedinger K, Scemes E (2008) Interleukin-1β affects calcium signaling and in vitro cell migration of astrocyte progenitors. J Neuroimmunol 196:116–123. https://doi.org/10.1016/J.JNEUROIM.2008.03.014
Striedinger K, Meda P, Scemes E (2007) Exocytosis of ATP from astrocyte progenitors modulates spontaneous Ca 2+ oscillations and cell migration. Glia 55:652–662. https://doi.org/10.1002/glia.20494
Suadicani SO, Brosnan CF, Scemes E (2006) P2X7 receptors mediate ATP release and amplification of astrocytic intercellular Ca2+ signaling. J Neurosci 26:1378–1385. https://doi.org/10.1523/JNEUROSCI.3902-05.2006
Supłat D, Targos B, Sabała P et al (2004) Differentiation of answer of glioma C6 cells to SERCA pump inhibitors by actin disorganization. Biochem Biophys Res Commun 323(3):870–875. https://doi.org/10.1016/j.bbrc.2004.08.155
Suplat D, Krzemiński P, Pomorski P, Barańska J (2007) P2Y1 and P2Y12 receptor cross-talk in calcium signalling: evidence from nonstarved and long-term serum-deprived glioma C6 cells. Purinergic Signal 3:221–230. https://doi.org/10.1007/s11302-007-9051-5
Supłat-Wypych D, Dygas A, Barańska J (2010) 2′, 3′-O-(4-benzoylbenzoyl)–ATP-mediated calcium signaling in rat glioma C6 cells: role of the P2Y2 nucleotide receptor. Purinergic Signal 6:317–325. https://doi.org/10.1007/s11302-010-9194-7
Surprenant A, Rassendren F, Kawashima E et al (1996) The cytolytic P2Z receptor for extracellular ATP identified as a P2X receptor (P2X7). Science 272:735–738. https://doi.org/10.1126/SCIENCE.272.5262.735
Targos B, Pomorski P, Krzemiński P et al (2006) Effect of Rho-associated kinase inhibition on actin cytoskeleton structure and calcium response in glioma C6 cells. Acta Biochim Pol 53:825–831
Tatenhorst L, Püttmann S, Senner V, Paulus W (2006) Genes associated with fast glioma cell migration in vitro and in vivo. Brain Pathol 15:46–54. https://doi.org/10.1111/j.1750-3639.2005.tb00099.x
Thebault S, Flourakis M, Vanoverberghe K et al (2006) Differential role of transient receptor potential channels in Ca 2+ entry and proliferation of prostate cancer epithelial cells. Cancer Res 66:2038–2047. https://doi.org/10.1158/0008-5472.CAN-05-0376
Theis M, Söhl G, Eiberger J, Willecke K (2005) Emerging complexities in identity and function of glial connexins. Trends Neurosci 28:188–195. https://doi.org/10.1016/J.TINS.2005.02.006
Van Kolen K, Slegers H (2006) Integration of P2Y receptor-activated signal transduction pathways in G protein-dependent signalling networks. Purinergic Signal 2:451–469. https://doi.org/10.1007/s11302-006-9008-0
Van Kolen K, Gilany K, Moens L et al (2006) P2Y12 receptor signalling towards PKB proceeds through IGF-I receptor cross-talk and requires activation of Src, Pyk2 and Rap1. Cell Signal 18:1169–1181. https://doi.org/10.1016/J.CELLSIG.2005.09.005
Vanderheyden V, Devogelaere B, Missiaen L et al (2009) Regulation of inositol 1,4,5-trisphosphate-induced Ca2+ release by reversible phosphorylation and dephosphorylation. Biochim Biophys Acta, Mol Cell Res 1793:959–970. https://doi.org/10.1016/J.BBAMCR.2008.12.003
Vazquez G, Wedel BJ, Aziz O et al (2004) The mammalian TRPC cation channels. Biochim Biophys Acta, Mol Cell Res 1742:21–36. https://doi.org/10.1016/J.BBAMCR.2004.08.015
Venkatachalam K, van Rossum DB, Patterson RL et al (2002) The cellular and molecular basis of store-operated calcium entry. Nat Cell Biol 4:E263–E272. https://doi.org/10.1038/ncb1102-e263
Verkhratsky A (2006) Calcium ions and integration in neural circuits. Acta Physiol 187:357–369. https://doi.org/10.1111/j.1748-1716.2006.01566.x
Vig M, DeHaven WI, Bird GS et al (2008) Defective mast cell effector functions in mice lacking the CRACM1 pore subunit of store-operated calcium release–activated calcium channels. Nat Immunol 9:89–96. https://doi.org/10.1038/ni1550
Wang M, Kong Q, Gonzalez FA et al (2005) P2Y2 nucleotide receptor interaction with alphaV integrin mediates astrocyte migration. J Neurochem 95:630–640. https://doi.org/10.1111/j.1471-4159.2005.03408.x
Wang Y, Deng X, Hewavitharana T et al (2008) STIM, ORAI and TRPC channels in the control of calcium entry signals in smooth muscle. Clin Exp Pharmacol Physiol 35:1127–1133. https://doi.org/10.1111/j.1440-1681.2008.05018.x
Wang D, Yan B, Rajapaksha W, Fisher TE (2009) The expression of voltage-gated Ca 2+ channels in Pituicytes and the up-regulation of L-type Ca2+ channels during water deprivation. J Neuroendocrinol 21:858–866. https://doi.org/10.1111/j.1365-2826.2009.01906.x
Wang Y, Deng X, Gill DL (2010) Calcium signaling by STIM and Orai: intimate coupling details revealed. Sci Signal 3:pe42. https://doi.org/10.1126/scisignal.3148pe42
Wegierski T, Kuznicki J (2018) Neuronal calcium signaling via store-operated channels in health and disease. Cell Calcium 74:102–111. https://doi.org/10.1016/J.CECA.2018.07.001
Wei W, Ryu JK, Choi HB, McLarnon JG (2008) Expression and function of the P2X7 receptor in rat C6 glioma cells. Cancer Lett 260:79–87. https://doi.org/10.1016/J.CANLET.2007.10.025
Worthylake RA, Burridge K (2003) RhoA and ROCK promote migration by limiting membrane protrusions. J Biol Chem 278:13578–13584. https://doi.org/10.1074/jbc.M211584200
Xiao R, Xu XZS (2009) Function and regulation of TRP family channels in C. elegans. Pflügers Arch Eur J Physiol 458:851–860. https://doi.org/10.1007/s00424-009-0678-7
Yaguchi T, Nishizaki T (2010) Extracellular high K+ stimulates vesicular glutamate release from astrocytes by activating voltage-dependent calcium channels. J Cell Physiol 225:512–518. https://doi.org/10.1002/jcp.22231
Yeromin AV, Zhang SL, Jiang W et al (2006) Molecular identification of the CRAC channel by altered ion selectivity in a mutant of Orai. Nature 443:226–229. https://doi.org/10.1038/nature05108
Yoshikawa S, Tanimura T, Miyawaki A et al (1992) Molecular cloning and characterization of the inositol 1,4,5-trisphosphate receptor in Drosophila melanogaster. J Biol Chem 267:16613–16619
Young CNJ, Górecki DC (2018) P2RX7 purinoceptor as a therapeutic target—the second coming? Front Chem 6:248. https://doi.org/10.3389/fchem.2018.00248
Yu X, Carroll S, Rigaud JL, Inesi G (1993) H+ countertransport and electrogenicity of the sarcoplasmic reticulum Ca2+ pump in reconstituted proteoliposomes. Biophys J 64:1232–1242. https://doi.org/10.1016/S0006-3495(93)81489-9
Yu S-C, Xiao H-L, Jiang X-F et al (2012) Connexin 43 reverses malignant phenotypes of glioma stem cells by modulating e-cadherin. Stem Cells 30:108–120. https://doi.org/10.1002/stem.1685
Zamponi GW, Striessnig J, Koschak A, Dolphin AC (2015) The physiology, pathology, and pharmacology of voltage-gated calcium channels and their future therapeutic potential. Pharmacol Rev 67:821–870. https://doi.org/10.1124/PR.114.009654
Zhang SL, Yu Y, Roos J et al (2005) STIM1 is a Ca2+ sensor that activates CRAC channels and migrates from the Ca2+ store to the plasma membrane. Nature 437:902–905. https://doi.org/10.1038/nature04147
Zhang SL, Yeromin AV, Zhang XH-F et al (2006) Genome-wide RNAi screen of Ca(2+) influx identifies genes that regulate Ca(2+) release-activated Ca(2+) channel activity. Proc Natl Acad Sci U S A 103:9357–9362. https://doi.org/10.1073/pnas.0603161103
Zhou Y, Mancarella S, Wang Y et al (2009) The short N-terminal domains of STIM1 and STIM2 control the activation kinetics of Orai1 channels. J Biol Chem 284:19164–19168. https://doi.org/10.1074/JBC.C109.010900
Zhou Y, Meraner P, Kwon HT et al (2010) STIM1 gates the store-operated calcium channel ORAI1 in vitro. Nat Struct Mol Biol 17:112–116. https://doi.org/10.1038/nsmb.1724
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Authors were supported by grant UMO-2015/17/B/NZ3/03771 from Nntional Science Center, Poland.
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Wypych, D., Pomorski, P. (2020). Calcium Signaling in Glioma Cells: The Role of Nucleotide Receptors. In: Barańska, J. (eds) Glioma Signaling. Advances in Experimental Medicine and Biology, vol 1202. Springer, Cham. https://doi.org/10.1007/978-3-030-30651-9_4
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