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Calcium Signaling in Glioma Cells: The Role of Nucleotide Receptors

  • Dorota Wypych
  • Paweł PomorskiEmail author
Chapter
  • 79 Downloads
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1202)

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

Calcium signaling Nucleotide receptors Store-operated calcium entry 

Abbreviations

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

Notes

Acknowledgment

Authors were supported by grant UMO-2015/17/B/NZ3/03771 from Nntional Science Center, Poland.

References

  1. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  2. 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 CrossRefPubMedGoogle Scholar
  3. 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 CrossRefPubMedGoogle Scholar
  4. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  5. 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 CrossRefGoogle Scholar
  6. Allen NJ, Barres BA (2009) Neuroscience: glia—more than just brain glue. Nature 457:675–677.  https://doi.org/10.1038/457675a CrossRefPubMedGoogle Scholar
  7. 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 CrossRefGoogle Scholar
  8. 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 CrossRefPubMedGoogle Scholar
  9. Barańska J, Przybyłek K, Sabała P (1999) Capacitative calcium entry. Glioma C6 as a model of nonexcitable cells. Pol J Pharmacol 51:153–162PubMedGoogle Scholar
  10. 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 CrossRefGoogle Scholar
  11. Barańska J, Czajkowski R, Pomorski P (2017) P2Y1 receptors – properties and functional activities. Springer, Singapore, pp 71–89Google Scholar
  12. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Berridge MJ (1993) Inositol trisphosphate and calcium signalling. Nature 361:315–325.  https://doi.org/10.1038/361315a0 CrossRefPubMedGoogle Scholar
  14. Berridge MJ (1995) Capacitative calcium entry. Biochem J 312(Pt 1):1–11.  https://doi.org/10.1042/bj3120001 CrossRefPubMedPubMedCentralGoogle Scholar
  15. 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 CrossRefPubMedGoogle Scholar
  16. 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 CrossRefPubMedGoogle Scholar
  17. 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 CrossRefPubMedGoogle Scholar
  18. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  19. 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 CrossRefGoogle Scholar
  20. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Burnstock G (2006) Purinergic signalling–an overview. Novartis Found Symp 276:26–48Google Scholar
  22. 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 CrossRefPubMedGoogle Scholar
  23. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  24. 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 CrossRefPubMedGoogle Scholar
  25. 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 CrossRefPubMedGoogle Scholar
  26. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  27. 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 CrossRefPubMedGoogle Scholar
  28. 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 CrossRefPubMedGoogle Scholar
  29. 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 CrossRefPubMedGoogle Scholar
  30. 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 CrossRefPubMedGoogle Scholar
  31. Clapham DE (2007) SnapShot: mammalian TRP channels. Cell 129:220.e1–220.e2.  https://doi.org/10.1016/J.CELL.2007.03.034 CrossRefGoogle Scholar
  32. 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 CrossRefGoogle Scholar
  33. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  34. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  35. 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. 024904877CrossRefGoogle Scholar
  36. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  37. 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 CrossRefPubMedGoogle Scholar
  38. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  39. 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):9569–9574PubMedGoogle Scholar
  40. 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):13612–13622PubMedGoogle Scholar
  41. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  42. 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 CrossRefGoogle Scholar
  43. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  44. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  45. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  46. 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 CrossRefPubMedGoogle Scholar
  47. 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 CrossRefPubMedGoogle Scholar
  48. 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 CrossRefPubMedGoogle Scholar
  49. 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 CrossRefPubMedGoogle Scholar
  50. 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 CrossRefPubMedGoogle Scholar
  51. 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 CrossRefPubMedGoogle Scholar
  52. 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 CrossRefPubMedGoogle Scholar
  53. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  54. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  55. 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 CrossRefPubMedGoogle Scholar
  56. 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 CrossRefPubMedGoogle Scholar
  57. 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 78:1325–1338CrossRefGoogle Scholar
  58. 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):e19285CrossRefGoogle Scholar
  59. 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 CrossRefGoogle Scholar
  60. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  61. 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 CrossRefPubMedGoogle Scholar
  62. 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 CrossRefPubMedGoogle Scholar
  63. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  64. Hamilton SL (2005) Ryanodine receptors. Cell Calcium 38:253–260.  https://doi.org/10.1016/J.CECA.2005.06.037 CrossRefPubMedGoogle Scholar
  65. 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 269:14268–14275PubMedGoogle Scholar
  66. 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 CrossRefPubMedGoogle Scholar
  67. Hartline DK (2011) The evolutionary origins of glia. Glia 59:1215–1236.  https://doi.org/10.1002/glia.21149 CrossRefPubMedGoogle Scholar
  68. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  69. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  70. 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 CrossRefGoogle Scholar
  71. 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 CrossRefPubMedGoogle Scholar
  72. 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 CrossRefPubMedGoogle Scholar
  73. 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 CrossRefPubMedGoogle Scholar
  74. 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 262:16636–16643PubMedGoogle Scholar
  75. 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 262:1740–1747PubMedGoogle Scholar
  76. 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 262:15637–15642PubMedGoogle Scholar
  77. James PH, Pruschy M, Vorherr TE et al (1989) Primary structure of the cAMP-dependent phosphorylation site of the plasma membrane calcium pump. Biochemistry 28:4253–4258CrossRefGoogle Scholar
  78. 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 CrossRefPubMedGoogle Scholar
  79. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  80. 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 CrossRefPubMedGoogle Scholar
  81. Kawate T (2017) P2X receptor activation. Springer, Singapore, pp 55–69Google Scholar
  82. 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 CrossRefPubMedGoogle Scholar
  83. 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 CrossRefPubMedGoogle Scholar
  84. 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)Google Scholar
  85. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  86. Krane SM, Glimcher MJ (1962) Transphosphorylation from nucleoside Di- and triphosphates by apatite crystals. J Biol Chem 237:2991–2998PubMedGoogle Scholar
  87. 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 CrossRefGoogle Scholar
  88. Läuger P (1991) Kinetic basis of voltage dependence of the Na,K-pump. Soc Gen Physiol Ser 46:303–315PubMedGoogle Scholar
  89. Lazarowski E (2006) Regulated release of nucleotides and UDP sugars from astrocytoma cells. Novartis Found Symp 276:73–84; discussion 84-90, 107–12, 275–81Google Scholar
  90. 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 CrossRefPubMedGoogle Scholar
  91. 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 CrossRefGoogle Scholar
  92. 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 CrossRefPubMedGoogle Scholar
  93. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  94. 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 CrossRefPubMedGoogle Scholar
  95. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  96. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  97. McCully KS (2009) Chemical pathology of homocysteine. IV. Excitotoxicity, oxidative stress, endothelial dysfunction, and inflammation. Ann Clin Lab Sci 39:219–232PubMedGoogle Scholar
  98. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  99. 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 CrossRefPubMedGoogle Scholar
  100. 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 CrossRefPubMedGoogle Scholar
  101. 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 CrossRefPubMedGoogle Scholar
  102. 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 CrossRefPubMedGoogle Scholar
  103. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  104. 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 CrossRefPubMedGoogle Scholar
  105. 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 CrossRefPubMedGoogle Scholar
  106. 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 83–98Google Scholar
  107. 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 CrossRefGoogle Scholar
  108. 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 CrossRefPubMedGoogle Scholar
  109. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  110. 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 CrossRefPubMedGoogle Scholar
  111. 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 CrossRefPubMedGoogle Scholar
  112. 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 CrossRefPubMedGoogle Scholar
  113. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  114. 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 CrossRefGoogle Scholar
  115. 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 CrossRefGoogle Scholar
  116. Putney JW (1990) Capacitative calcium entry revisited. Cell Calcium 11:611–624CrossRefGoogle Scholar
  117. 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 CrossRefPubMedGoogle Scholar
  118. 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 CrossRefGoogle Scholar
  119. 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 CrossRefPubMedGoogle Scholar
  120. 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 CrossRefPubMedGoogle Scholar
  121. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  122. 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 CrossRefPubMedGoogle Scholar
  123. 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 CrossRefPubMedGoogle Scholar
  124. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  125. 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 CrossRefPubMedGoogle Scholar
  126. 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 CrossRefPubMedGoogle Scholar
  127. 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 CrossRefGoogle Scholar
  128. 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 CrossRefGoogle Scholar
  129. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  130. 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 CrossRefPubMedGoogle Scholar
  131. 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 CrossRefPubMedGoogle Scholar
  132. Sontheimer H (1994) Voltage-dependent ion channels in glial cells. Glia 11:156–172.  https://doi.org/10.1002/glia.440110210 CrossRefPubMedGoogle Scholar
  133. 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 CrossRefPubMedGoogle Scholar
  134. 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 CrossRefPubMedGoogle Scholar
  135. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  136. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  137. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  138. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  139. 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 CrossRefPubMedGoogle Scholar
  140. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  141. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  142. 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 CrossRefPubMedGoogle Scholar
  143. 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 53:825–831CrossRefGoogle Scholar
  144. 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 CrossRefGoogle Scholar
  145. 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 CrossRefPubMedGoogle Scholar
  146. 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 CrossRefPubMedGoogle Scholar
  147. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  148. 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 CrossRefPubMedGoogle Scholar
  149. 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 CrossRefPubMedGoogle Scholar
  150. 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 CrossRefPubMedGoogle Scholar
  151. 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 CrossRefPubMedGoogle Scholar
  152. 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 CrossRefGoogle Scholar
  153. 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 CrossRefPubMedGoogle Scholar
  154. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  155. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  156. 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 CrossRefPubMedGoogle Scholar
  157. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  158. 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 CrossRefPubMedGoogle Scholar
  159. 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 CrossRefGoogle Scholar
  160. 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 CrossRefPubMedGoogle Scholar
  161. 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 CrossRefGoogle Scholar
  162. 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 CrossRefPubMedGoogle Scholar
  163. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  164. 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 267:16613–16619PubMedGoogle Scholar
  165. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  166. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  167. 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 CrossRefPubMedGoogle Scholar
  168. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  169. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  170. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  171. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  172. 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 CrossRefPubMedGoogle Scholar

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Authors and Affiliations

  1. 1.Nencki Institute of Experimental BiologyPolish Academy of SciencesWarsawPoland

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