Store-operated calcium entry in physiology and pathology of mammalian cells
Languages of publication
One of the numerous calcium-involving processes in mammalian cells is store-operated calcium entry (SOCE) - the process in which depletion of calcium stores in the endoplasmic reticulum (ER) induces calcium influx from the extracellular space. Previously supposed to function only in non-excitable cells, SOCE is now known to play a role also in such excitable cells as neurons, muscles and neuroendocrine cells and is found in many different cell types. SOCE participates not only in processes dependent on ER calcium level but also specifically regulates some important processes such as cAMP production, T lymphocyte activation or induction of long-term potentiation. Impairment of SOCE can be an element of numerous disorders such as acute pancreatitis, primary immunodeficiency and, since it can take part in apoptosis or cell cycle regulation, SOCE may also be partially responsible for such serious disorders as Alzheimer disease and many types of cancer. Even disturbances in the 'servant' role of maintaining ER calcium level may cause serious effects because they can lead to ER homeostasis disturbance, influencing gene expression, protein synthesis and processing, and the cell cycle.
- Akbari Y, Hitt BD, Murphy MP, Dagher NN, Tseng BP, Green KN, Golde TE, LaFerla FM (2004) Presenilin regulates capacitative calcium entry dependently and independently of γ-secretase activity. Biochem Biophys Res Commun 322: 1145-1152.
- Alessandro R, Masiero L, Liotta LA, Kohn EC (1996) The role of calcium in the regulation of invasion and angiogenesis. In Vivo 10: 153-160.
- Baranska J, Chaban V, Czarny M, Sabala P (1995) Changes in Ca2+ concentration in phorbol ester and thapsigargin treated glioma C6 cells. The role of protein kinase C in regulation of Ca2+ entry. Cell Calcium 17: 207-215.
- Baranska J, Przybylek K, Sabala P (1999) Capacitative calcium entry. Glioma C6 as a model of nonexcitable cells. Pol J Pharmacol 51: 153-162.
- Beck L Jr, D’Amore PA (1997) Vascular development: cellular and molecular regulation. FASEB J 11: 365-373.
- Belkacemi L, Bedard I, Simoneau L, Lafond J (2005) Calcium channels, transporters and exchangers in placenta: a review. Cell Calcium 37: 1-8.
- Berridge MJ (1995a) Calcium signalling and cell proliferation. Bioessays 17: 491-500.
- Berridge MJ (1995b) Capacitative calcium entry. Biochem J 312: 1-11.
- Blackshaw S, Sawa A, Sharp AH, Ross CA, Snyder SH, Khan AA (2000) Type 3 inositol 1,4,5-trisphosphate receptor modulates cell death. FASEB J 14: 1375-1379.
- Bouron A (2000) Activation of a capacitative Ca2+ entry pathway by store depletion in cultured hippocampal neurones. FEBS Lett 470: 269-272.
- Broad LM, Powis DA, Taylor CW (1996) Differentiation of BC3H1 smooth muscle cells changes the bivalent cation selectivity of the capacitative Ca2+ entry pathway. Biochem J 316: 759-764.
- Chetham PM, Babal P, Bridges JP, Moore TM, Stevens T (1999) Segmental regulation of pulmonary vascular permeability by store-operated Ca2+ entry. Am J Physiol 276: L41-50.
- Chiono M, Mahey R, Tate G, Cooper DM (1995) Capacitative Ca2+ entry exclusively inhibits cAMP synthesis in C6-2B glioma cells. Evidence that physiologically evoked Ca2+ entry regulates Ca2+-inhibitable adenylyl cyclase in non-excitable cells. J Biol Chem 270: 1149-1155.
- Cooper DM, Yoshimura M, Zhang Y, Chiono M, Mahey R (1994) Capacitative Ca2+ entry regulates Ca2+-sensitive adenylyl cyclases. Biochem J 297: 437-440.
- Delon J, Bercovici N, Raposo G, Liblau R, Trautmann A (1998) Antigen-dependent and -independent Ca2+ responses triggered in T cells by dendritic cells compared with B cells. J Exp Med 188: 1473-1484.
- Distelhorst CW, Dubyak G (1998) Role of calcium in glucocorticosteroid-induced apoptosis of thymocytes and lymphoma cells: resurrection of old theories by new findings. Blood 91: 731-734.
- Dolmetsch RE, Xu K, Lewis RS (1998) Calcium oscillations increase the efficiency and specificity of gene expression. Nature 392: 933-936.
- Donnadieu E, Bismuth G, Trautmann A (1994) Antigen recognition by helper T cells elicits a sequence of distinct changes of their shape and intracellular calcium. Curr Biol 4: 584-595.
- Emptage NJ, Reid CA, Fine A (2001) Calcium stores in hippocampal synaptic boutons mediate short-term plasticity, store-operated Ca2+ entry, and spontaneous transmitter release. Neuron 29: 197-208.
- Enfissi A, Prigent S, Colosetti P, Capiod T (2004) The blocking of capacitative calcium entry by 2-aminoethyl diphenylborate (2-APB) and carboxyamidotriazole (CAI) inhibits proliferation in Hep G2 and Huh-7 human hepatoma cells. Cell Calcium 36: 459-467.
- Fagan KA, Graf RA, Tolman S, Schaack J, Cooper DM (2000) Regulation of a Ca2+-sensitive adenylyl cyclase in an excitable cell. Role of voltage-gated versus capacitative Ca2+ entry. J Biol Chem 275: 40187-40194.
- Fantozzi I, Zhang S, Platoshyn O, Remillard CV, Cowling RT, Yuan JX (2003) Hypoxia increases AP-1 binding activity by enhancing capacitative Ca2+ entry in human pulmonary artery endothelial cells. Am J Physiol Lung Cell Mol Physiol 285: L1233-1245.
- Fasolato C, Nilius B (1998) Store depletion triggers the calcium release-activated calcium current (ICRAC) in macrovascular endothelial cells: a comparison with Jurkat and embryonic kidney cell lines. Pflugers Arch 436: 69-74.
- Fixemer T, Wissenbach U, Flockerzi V, Bonkhoff H (2003) Expression of the Ca2+-selective cation channel TRPV6 in human prostate cancer: a novel prognostic marker for tumor progression. Oncogene 22: 7858-7861.
- Floto RA, Mahaut-Smith MP, Allen JM, Somasundaram B (1996) Differentiation of the human monocytic cell line U937 results in an upregulation of the calcium release-activated current, ICRAC. J Physiol 495: 331-338.
- Freichel M, Vennekens R, Olausson J, Hoffmann M, Muller C, Stolz S, Scheunemann J, Weissgerber P, Flockerzi V (2004) Functional role of TRPC proteins in vivo: lessons from TRPC-deficient mouse models. Biochem Biophys Res Commun 322: 1352-1358.
- Gardner JP, Balasubramanyam M, Studzinski GP (1997) Up-regulation of Ca2+ influx mediated by store-operated channels in HL60 cells induced to differentiate by 1 α,25-dihydroxyvitamin D3. J Cell Physiol 172: 284-295.
- Gill DL, Waldron RT, Rys-Sikora KE, Ufret-Vincenty CA, Graber MN, Favre CJ, Alfonso A (1996) Calcium pools, calcium entry, and cell growth. Biosci Rep 16: 139-157.
- Golovina VA, Platoshyn O, Bailey CL, Wang J, Limsuwan A, Sweeney M, Rubin LJ, Yuan JX (2001) Upregulated TRP and enhanced capacitative Ca2+ entry in human pulmonary artery myocytes during proliferation. Am J Physiol Heart Circ Physiol 280: H746-755.
- Harteneck C (2003) Proteins modulating TRP channel function. Cell Calcium 33: 303-310.
- He H, Lam M, McCormick TS, Distelhorst CW (1997) Maintenance of calcium homeostasis in the endoplasmic reticulum by Bcl-2. J Cell Biol 138: 1219-1228.
- Hopf FW, Reddy P, Hong J, Steinhardt RA (1996) A capacitative calcium current in cultured skeletal muscle cells is mediated by the calcium-specific leak channel and inhibited by dihydropyridine compounds. J Biol Chem 271: 22358-22367.
- Hsu S, O’Connell PJ, Klyachko VA, Badminton MN, Thomson AW, Jackson MB, Clapham DE, Ahern GP (2001) Fundamental Ca2+ signaling mechanisms in mouse dendritic cells: CRAC is the major Ca2+ entry pathway. J Immunol 166: 6126-6133.
- Ito E, Oka K, Etcheberrigaray R, Nelson TJ, McPhie DL, Tofel-Grehl B, Gibson GE, Alkon DL (1994) Internal Ca2+ mobilization is altered in fibroblasts from patients with Alzheimer disease. Proc Natl Acad Sci USA 91: 534-538.
- Jayadev S, Petranka JG, Cheran SK, Biermann JA, Barrett JC, Murphy E (1999) Reduced capacitative calcium entry correlates with vesicle accumulation and apoptosis. J Biol Chem 274: 8261-8268.
- Jayaraman T, Marks AR (2000) Calcineurin is downstream of the inositol 1,4,5-trisphosphate receptor in the apoptotic and cell growth pathways. J Biol Chem 275: 6417-6420.
- Kiselyov K, Mignery GA, Zhu MX, Muallem S (1999) The N-terminal domain of the IP3 receptor gates store-operated hTrp3 channels. Mol Cell 4: 423-429.
- Kohn EC, Reed E, Sarosy G, Christian M, Link CJ, Cole K, Figg WD, Davis PA, Jacob J, Goldspiel B, Liotta LA (1996) Clinical investigation of a cytostatic calcium influx inhibitor in patients with refractory cancers. Cancer Res 56: 569-573.
- Korkiamaki T, Yla-Outinen H, Koivunen J, Karvonen SL, Peltonen J (2002) Altered calcium-mediated cell signaling in keratinocytes cultured from patients with neurofibromatosis type 1. Am J Pathol 160: 1981-1990.
- Koski GK, Schwartz GN, Weng DE, Czerniecki BJ, Carter C, Gress RE, Cohen PA (1999) Calcium mobilization in human myeloid cells results in acquisition of individual dendritic cell-like characteristics through discrete signaling pathways. J Immunol 163: 82-92.
- Kurebayashi N, Ogawa Y (2001) Depletion of Ca2+ in the sarcoplasmic reticulum stimulates Ca2+ entry into mouse skeletal muscle fibres. J Physiol 533: 185-199.
- Lam M, Dubyak G, Chen L, Nunez G, Miesfeld RL, Distelhorst CW (1994) Evidence that BCL-2 represses apoptosis by regulating endoplasmic reticulum-associated Ca2+ fluxes. Proc Natl Acad Sci USA 91: 6569-6573.
- Lewis RS (2001) Calcium signaling mechanisms in T lymphocytes. Annu Rev Immunol 19: 497-521.
- Lockwich TP, Liu X, Singh BB, Jadlowiec J, Weiland S, Ambudkar IS (2000) Assembly of Trp1 in a signaling complex associated with caveolin-scaffolding lipid raft domains. J Biol Chem 275: 11934-11942.
- Luckhoff A, Clapham DE (1994) Calcium channels activated by depletion of internal calcium stores in A431 cells. Biophys J 67: 177-182.
- Mattson MP, LaFerla FM, Chan SL, Leissring MA, Shepel PN, Geiger JD (2000) Calcium signaling in the ER: its role in neuronal plasticity and neurodegenerative disorders. Trends Neurosci 23: 222-229.
- Meldolesi J, Pozzan T (1998) The endoplasmic reticulum Ca2+ store: a view from the lumen. Trends Biochem Sci 23: 10-4.
- Mentaverri R, Kamel S, Brazier M (2003) Involvement of capacitive calcium entry and calcium store refilling in osteoclastic survival and bone resorption process. Cell Calcium 34: 169-175.
- Minke B, Cook B (2002) TRP channel proteins and signal transduction. Physiol Rev 82: 429-472.
- Missiaen L, Robberecht W, van den Bosch L, Callewaert G, Parys JB, Wuytack F, Raeymaekers L, Nilius B, Eggermont J, De Smedt H (2000) Abnormal intracellular Ca2+homeostasis and disease. Cell Calcium 28: 1-21.
- Ng LC, Gurney AM (2001) Store-operated channels mediate Ca2+ influx and contraction in rat pulmonary artery. Circ Res 89: 923-929.
- Nicotera P, Orrenius S (1998) The role of calcium in apoptosis. Cell Calcium 23: 173-180.
- Nilius B (2003) From TRPs to SOCs, CCEs, and CRACs: consensus and controversies. Cell Calcium 33: 293-298.
- Nilius B (2004) Store-operated Ca2+ entry channels: still elusive! Sci STKE 2004: pe36.
- Norwood N, Moore TM, Dean DA, Bhattacharjee R, Li M, Stevens T (2000) Store-operated calcium entry and increased endothelial cell permeability. Am J Physiol Lung Cell Mol Physiol 279: L815-824.
- Parekh AB (2000) Calcium signaling and acute pancreatitis: specific response to a promiscuous messenger. Proc Natl Acad Sci USA 97: 12933-12934.
- Parekh AB, Penner R (1997) Store depletion and calcium influx. Physiol Rev 77: 901-930.
- Parekh AB, Putney JW Jr (2005) Store-operated calcium channels. Physiol Rev 85: 757-810.
- Partiseti M, Le Deist F, Hivroz C, Fischer A, Korn H, Choquet D (1994) The calcium current activated by T cell receptor and store depletion in human lymphocytes is absent in a primary immunodeficiency. J Biol Chem 269: 32327-32335.
- Perez CA, Margolskee RF, Kinnamon SC, Ogura T (2003) Making sense with TRP channels: store-operated calcium entry and the ion channel Trpm5 in taste receptor cells. Cell Calcium 33: 541-549.
- Pigozzi D, Tombal B, Ducret T, Vacher P, Gailly P (2004) Role of store-dependent influx of Ca2+ and efflux of K+ in apoptosis of CHO cells. Cell Calcium 36: 421-430.
- Pinton P, Ferrari D, Magalhaes P, Schulze-Osthoff K, Di Virgilio F, Pozzan T, Rizzuto R (2000) Reduced loading of intracellular Ca2+ stores and downregulation of capacitative Ca2+ influx in Bcl-2-overexpressing cells. J Cell Biol 148: 857-862.
- Pletjushkina OJ, Rajfur Z, Pomorski P, Oliver TN, Vasiliev JM, Jacobson KA (2001) Induction of cortical oscillations in spreading cells by depolymerization of microtubules. Cell Motil Cytoskeleton 48: 235-244.
- Pomorski P, Watson JM, Haskill S, Jacobson KA (2004) How adhesion, migration, and cytoplasmic calcium transients influence interleukin-1β mRNA stabilization in human monocytes. Cell Motil Cytoskeleton 57: 143-157.
- Preston GA, Barrett JC, Biermann JA, Murphy E (1997) Effects of alterations in calcium homeostasis on apoptosis during neoplastic progression. Cancer Res 57: 537-542.
- Prevarskaya N, Skryma R, Shuba Y (2004) Ca2+ homeostasis in apoptotic resistance of prostate cancer cells. Biochem Biophys Res Commun 322: 1326-35.
- Putney JW Jr (1990) Capacitative calcium entry revisited. Cell Calcium 11: 611-624.
- Putney JW Jr (2000) Presenilins, Alzheimer’s disease, and capacitative calcium entry. Neuron 27: 411-412.
- Putney JW Jr (2003) Capacitative calcium entry in the nervous system. Cell Calcium 34: 339-344.
- Randriamampita C, Tsien RY (1993) Emptying of intracellular Ca2+ stores releases a novel small messenger that stimulates Ca2+ influx. Nature 364: 809-814.
- Raraty M, Ward J, Erdemli G, Vaillant C, Neoptolemos JP, Sutton R, Petersen OH (2000) Calcium-dependent enzyme activation and vacuole formation in the apical granular region of pancreatic acinar cells. Proc Natl Acad Sci USA 97: 13126-13131.
- Ris L, Dewachter I, Reverse D, Godaux E, Van Leuven F (2003) Capacitative calcium entry induces hippocampal long term potentiation in the absence of presenilin-1. J Biol Chem 278: 44393-44399.
- Robinson IM, Cheek TR, Burgoyne RD (1992) Ca2+ influx induced by the Ca(2+)-ATPase inhibitors 2,5-di-(t-butyl)-1,4-benzohydroquinone and thapsigargin in bovine adrenal chromaffin cells. Biochem J 288: 457-463.
- Roche E, Prentki M (1994) Calcium regulation of immediate-early response genes. Cell Calcium 16: 331-338.
- Rohacs T, Bago A, Deak F, Hunyady L, Spat A (1994) Capacitative Ca2+ influx in adrenal glomerulosa cells: possible role in angiotensin II response. Am J Physiol 267: C1246-1252.
- Rosado JA, Sage SO (2000) The actin cytoskeleton in store-mediated calcium entry. J Physiol 526: 221-229.
- Saavedra FR, Redondo PC, Hernandez-Cruz JM, Salido GM, Pariente JA, Rosado JA (2004) Store-operated Ca2+ entry and tyrosine kinase pp60(src) hyperactivity are modulated by hyperglycemia in platelets from patients with non insulin-dependent diabetes mellitus. Arch Biochem Biophys 432: 261-268.
- Sabala P, Amler E, Baranska J (1997). Intracellular Ca2+ signals induced by ATP and thapsigargin in glioma C6 cells. Calcium pools sensitive to inositol 1,4,5-trisphosphate and thapsigargin. Neurochem Int 31: 55-64.
- Sabala P, Czajkowski R, Przybylek K, Kalita K, Kaczmarek L, Baranska J (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.
- Savic N, Sciancalepore M (1998) Intracellular calcium stores modulate miniature GABA-mediated synaptic currents in neonatal rat hippocampal neurons. Eur J Neurosci 10: 3379-3386.
- Short AD, Bian J, Ghosh TK, Waldron RT, Rybak SL, Gill DL (1993) Intracellular Ca2+ pool content is linked to control of cell growth. Proc Natl Acad Sci USA 90: 4986-4990.
- Smith IF, Boyle JP, Vaughan PF, Pearson HA, Cowburn RF, Peers CS (2002) Ca(2+) stores and capacitative Ca2+ entry in human neuroblastoma (SH-SY5Y) cells expressing a familial Alzheimer’s disease presenilin-1 mutation. Brain Res 949: 105-111.
- Suplat D, Targos B, Sabala P, Baranska J, Pomorski P (2004) Differentiation of answer of glioma C6 cells to SERCA pump inhibitors by actin disorganization. Biochem Biophys Res Commun 323: 870-875.
- Thastrup O, Dawson AP, Scharff O, Foder B, Cullen PJ, Drobak BK, Bjerrum PJ, Christensen SB, Hanley MR (1989) Thapsigargin, a novel molecular probe for studying intracellular calcium release and storage. Agents Actions 27: 17-23.
- Timmerman LA, Clipstone NA, Ho SN, Northrop JP, Crabtree GR (1996) Rapid shuttling of NF-AT in discrimination of Ca2+ signals and immunosuppression. Nature 383: 837-840.
- Trepakova ES, Gericke M, Hirakawa Y, Weisbrod RM, Cohen RA, Bolotina VM (2001) Properties of a native cation channel activated by Ca2+ store depletion in vascular smooth muscle cells. J Biol Chem 276: 7782-7790.
- Vandebrouck C, Martin D, Colson-Van Schoor M, Debaix H, Gailly P (2002) Involvement of TRPC in the abnormal calcium influx observed in dystrophic (mdx) mouse skeletal muscle fibers. J Cell Biol 158: 1089-1096.
- Vanden Abeele F, Skryma R, Shuba Y, Van Coppenolle F, Slomianny C, Roudbaraki M, Mauroy B, Wuytack F, Prevarskaya N (2002) Bcl-2-dependent modulation of Ca(2+) homeostasis and store-operated channels in prostate cancer cells. Cancer Cell 1: 169-719.
- Vanden Abeele F, Roudbaraki M, Shuba Y, Skryma R, Prevarskaya N (2003) Store-operated Ca2+ current in prostate cancer epithelial cells. Role of endogenous Ca2+ transporter type 1. J Biol Chem 278: 15381-15389.
- Vanoverberghe K, Vanden Abeele F, Mariot P, Lepage G, Roudbaraki M, Bonnal JL, Mauroy B, Shuba Y, Skryma R, Prevarskaya N (2004) Ca2+ homeostasis and apoptotic resistance of neuroendocrine-differentiated prostate cancer cells. Cell Death Differ 11: 321-330.
- Villalobos C, Garcia-Sancho J (1995) Capacitative Ca2+ entry contributes to the Ca2+ influx induced by thyrotropin-releasing hormone (TRH) in GH3 pituitary cells. Pflugers Arch 430: 923-935.
- Waldron RT, Short AD, Gill DL (1997) Store-operated Ca2+ entry and coupling to Ca2+ pool depletion in thapsigargin-resistant cells. J Biol Chem 272: 6440-6447.
- Wang HG, Pathan N, Ethell IM, Krajewski S, Yamaguchi Y, Shibasaki F, McKeon F, Bobo T, Franke TF, Reed JC (1999) Ca2+-induced apoptosis through calcineurin dephosphorylation of BAD. Science 284: 339-343.
- Wei H, Wei W, Bredesen DE, Perry DC (1998) Bcl-2 protects against apoptosis in neuronal cell line caused by thapsigargin-induced depletion of intracellular calcium stores. J Neurochem 70: 2305-2314.
- Whitaker M, Patel R (1990) Calcium and cell cycle control. Development 108: 525-542.
- Wu X, Zagranichnaya TK, Gurda GT, Eves EM, Villereal ML (2004) A TRPC1/TRPC3-mediated increase in store-operated calcium entry is required for differentiation of H19-7 hippocampal neuronal cells. J Biol Chem 279: 43392-43402.
- Wulfing C, Davis MM (1998) A receptor/cytoskeletal movement triggered by costimulation during T cell activation. Science 282: 2266-2269.
- Wyllie AH (1997) Apoptosis: an overview. Br Med Bull 53: 451-465.
- Xu SZ, Beech DJ (2001) TrpC1 is a membrane-spanning subunit of store-operated Ca(2+) channels in native vascular smooth muscle cells. Circ Res 88: 84-87.
- Yoo AS, Cheng I, Chung S, Grenfell TZ, Lee H, Pack-Chung E, Handler M, Shen J, Xia W, Tesco G, Saunders AJ, Ding K, Frosch MP, Tanzi RE, Kim TW (2000) Presenilin-mediated modulation of capacitative calcium entry. Neuron 27: 561-572.
- Yu SP, Canzoniero LM, Choi DW (2001) Ion homeostasis and apoptosis. Curr Opin Cell Biol 13: 405-411.
- Yu Y, Sweeney M, Zhang S, Platoshyn O, Landsberg J, Rothman A, Yuan JX (2003) PDGF stimulates pulmonary vascular smooth muscle cell proliferation by upregulating TRPC6 expression. Am J Physiol Cell Physiol 284: C316-330.
- Zweifach A (2000) Target-cell contact activates a highly selective capacitative calcium entry pathway in cytotoxic T lymphocytes. J Cell Biol 148: 603-614.
Publication order reference