Skip to main content

Cardiovascular System

SOCE and Ca2+ Handling in Platelet Dysfunction

  • Chapter
  • First Online:
Book cover Store-operated Ca2+ entry (SOCE) pathways

Abstract

Store-operated Ca2+ entry (SOCE) is a major mechanism for Ca2+ influx in platelets, where Ca2+ influx through plasma membrane channels is necessary to achieve full activation of platelet functions. In these cell fragments, SOCE has been reported to involve the dynamic association of the ER Ca2+ sensor STIM1 and different plasma membrane Ca2+ permeable channels, including Orai1 and several TRPC members. A number of intracellular elements have been shown to participate in the regulation of SOCE in platelets, including the cytoskeleton or proteins of the SNARE family. Recent studies have revealed a number of abnormalities in SOCE or in its molecular regulators that result in qualitative platelet disorders and, as a consequence, in a reduced or absent platelet responsiveness upon stimulation with multiple physiological agonists. Platelet SOCE abnormalities include ion channel mutations or altered expression, as well as dysfunction of cytoskeleton-associated proteins. This chapter summarizes the recent advances in this field, as well as the disorders associated to platelet SOCE dysfunction.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Albert AP, Large WA (2002) Activation of store-operated channels by noradrenaline via protein kinase C in rabbit portal vein myocytes. J Physiol 544:113–125

    PubMed  CAS  Google Scholar 

  • Bakowski D, Parekh AB (2000) Voltage-dependent conductance changes in the store-operated Ca2+ current ICRAC in rat basophilic leukaemia cells. J Physiol 529:295–306

    PubMed  CAS  Google Scholar 

  • Bandyopadhyay BC, Ong HL, Lockwich TP, Liu X, Paria BC, Singh BB, Ambudkar IS (2008) TRPC3 controls agonist-stimulated intracellular Ca2+ release by mediating the interaction between inositol 1,4,5-trisphosphate receptor and RACK1. J Biol Chem 283:32821–32830

    PubMed  CAS  Google Scholar 

  • Ben-Amor N, Redondo PC, Bartegi A, Pariente JA, Salido GM, Rosado JA (2006) A role for 5,6-epoxyeicosatrienoic acid in calcium entry by de novo conformational coupling in human platelets. J Physiol 570:309–323

    PubMed  CAS  Google Scholar 

  • Ben Amor NB, Zbidi H, Bouaziz A, Isaac J, Hernandez-Cruz JM, Salido GM, Rosado JA, Bartegi A (2009) Acidic-store depletion is required for human platelet aggregation. Blood Coagul Fibrinolysis 20:511–516

    CAS  Google Scholar 

  • Berg LP, Shamsher MK, El-Daher SS, Kakkar VV, Authi KS (1997) Expression of human TRPC genes in the megakaryocytic cell lines MEG01, DAMI and HEL. FEBS Lett 403:83–86

    PubMed  CAS  Google Scholar 

  • Bergmeier W, Oh-Hora M, McCarl CA, Roden RC, Bray PF, Feske S (2009) R93W mutation in Orai1 causes impaired calcium influx in platelets. Blood 113:675–678

    PubMed  CAS  Google Scholar 

  • Berridge MJ, Lipp P, Bootman MD (2000) The versatility and universality of calcium signalling. Nat Rev Mol Cell Biol 1:11–21

    PubMed  CAS  Google Scholar 

  • Bizzonero J (1882) Über einen formbestandtheil des blutes und dessen rolle bei der thrombose und der blutgerinnung. Virchow’s Arch Path Anat Physiol Klin Med 90:261–232

    Google Scholar 

  • Blankenship KA, Dawson CB, Aronoff GR, Dean WL (2000) Tyrosine phosphorylation of human platelet plasma membrane Ca2+-ATPase in hypertension. Hypertension 35:103–107

    PubMed  CAS  Google Scholar 

  • Bobe R, Bredoux R, Wuytack F, Quarck R, Kovacs T, Papp B, Corvazier E, Magnier C, Enouf J (1994) The rat platelet 97-kDa Ca2+ATPase isoform is the sarcoendoplasmic reticulum Ca2+ATPase 3 protein. J Biol Chem 269:1417–1424

    PubMed  CAS  Google Scholar 

  • Bouaziz A, Amor NB, Woodard GE, Zibidi H, Lopez JJ, Bartegi A, Salido GM, Rosado JA (2007) Tyrosine phosphorylation/dephosphorylation balance is involved in thrombin-evoked microtubular reorganisation in human platelets. Thromb Haemost 98:375–384

    PubMed  CAS  Google Scholar 

  • Boulay G, Brown DM, Qin N, Jiang M, Dietrich A, Zhu MX, Chen Z, Birnbaumer M, Mikoshiba K, Birnbaumer L (1999) Modulation of Ca2+ entry by polypeptides of the inositol 1,4, 5-trisphosphate receptor (IP3R) that bind transient receptor potential (TRP): evidence for roles of TRP and IP3R in store depletion-activated Ca2+ entry. Proc Natl Acad Sci USA 96:14955–14960

    PubMed  CAS  Google Scholar 

  • Braun A, Varga-Szabo D, Kleinschnitz C, Pleines I, Bender M, Austinat M, Bosl M, Stoll G, Nieswandt B (2009) Orai1 (CRACM1) is the platelet SOC channel and essential for pathological thrombus formation. Blood 113:2056–2063

    PubMed  CAS  Google Scholar 

  • Brownlow SL, Sage SO (2005) Transient receptor potential protein subunit assembly and membrane distribution in human platelets. Thromb Haemost 94:839–845

    PubMed  Google Scholar 

  • Carter RN, Tolhurst G, Walmsley G, Vizuete-Forster M, Miller N, Mahaut-Smith MP (2006) Molecular and electrophysiological characterization of transient receptor potential ion channels in the primary murine megakaryocyte. J Physiol 576:151–162

    PubMed  CAS  Google Scholar 

  • Cavallini L, Coassin M, Alexandre A (1995) Two classes of agonist-sensitive Ca2+ stores in platelets, as identified by their differential sensitivity to 2,5-di-(tert-butyl)-1,4-benzohydroquinone and thapsigargin. Biochem J 310(Pt 2):449–452

    PubMed  CAS  Google Scholar 

  • Criado M, Gil A, Viniegra S, Gutierrez LM (1999) A single amino acid near the C terminus of the synaptosomeassociated protein of 25 kDa (SNAP-25) is essential for exocytosis in chromaffin cells. Proc Natl Acad Sci USA 96:7256–7261

    PubMed  CAS  Google Scholar 

  • Dean WL, Pope JE, Brier ME, Aronoff GR (1994) Platelet calcium transport in hypertension. Hypertension 23:31–37

    PubMed  CAS  Google Scholar 

  • Dean WL, Chen D, Brandt PC, Vanaman TC (1997) Regulation of platelet plasma membrane Ca2+-ATPase by cAMP-dependent and tyrosine phosphorylation. J Biol Chem 272:15113–15119

    PubMed  CAS  Google Scholar 

  • Dell’ Angelica EC, Mullins C, Caplan S (2000) Lysosome-related organelles. FASEB J 14:1265–1278

    Google Scholar 

  • den Dekker E, Molin DG, Breikers G, van Oerle R, Akkerman JW, van Eys GJ, Heemskerk JW (2001) Expression of transient receptor potential mRNA isoforms and Ca2+ influx in differentiating human stem cells and platelets. Biochim Biophys Acta 1539:243–255

    Google Scholar 

  • El Haouari M, Rosado JA (2008) Platelet signalling abnormalities in patients with type 2 diabetes mellitus: a review. Blood Cells Mol Dis 41:119–123

    PubMed  CAS  Google Scholar 

  • El Haouari M, Rosado JA (2009) Platelet function in hypertension. Blood Cells Mol Dis 42:38–43

    PubMed  CAS  Google Scholar 

  • El Haouari M, Jardín I, Mekhfi H, Rosado JA, Salido GM (2007) Urtica dioica extract reduces platelet hyperaggregability in type 2 diabetes mellitus by inhibition of oxidant production, Ca2+ mobilization and protein tyrosine phosphorylation. J Appl Biomed 5:105–113

    Google Scholar 

  • Feske S, Gwack Y, Prakriya M, Srikanth S, Puppel SH, Tanasa B, Hogan PG, Lewis RS, Daly M, Rao A (2006) A mutation in Orai1 causes immune deficiency by abrogating CRAC channel function. Nature 441:179–185

    PubMed  CAS  Google Scholar 

  • Fox JE (2001) Cytoskeletal proteins and platelet signaling. Thromb Haemost 86:198–213

    PubMed  CAS  Google Scholar 

  • Galan C, Zbidi H, Bartegi A, Salido GM, Rosado JA (2009) STIM1, Orai1 and hTRPC1 are important for thrombin- and ADP-induced aggregation in human platelets. Arch Biochem Biophys 490:137–144

    PubMed  CAS  Google Scholar 

  • 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–H755

    PubMed  CAS  Google Scholar 

  • Grosse J, Braun A, Varga-Szabo D, Beyersdorf N, Schneider B, Zeitlmann L, Hanke P, Schropp P, Muhlstedt S, Zorn C, Huber M, Schmittwolf C, Jagla W, Yu P, Kerkau T, Schulze H, Nehls M, Nieswandt B (2007) An EF hand mutation in Stim1 causes premature platelet activation and bleeding in mice. J Clin Invest 117:3540–3550

    PubMed  CAS  Google Scholar 

  • Guillausseau PJ, Dupuy E, Guillausseau C, Warnet A, Caen J, Lubetzki J (1985) Hemostasis disorders in diabetes mellitus. Horm Metab Res Suppl 15:60–62

    PubMed  CAS  Google Scholar 

  • Harper AG, Sage SO (2007) A key role for reverse Na+/Ca2+ exchange influenced by the actin cytoskeleton in store-operated Ca2+ entry in human platelets: evidence against the de novo conformational coupling hypothesis. Cell Calcium 42:606–617

    PubMed  CAS  Google Scholar 

  • Harper MT, Sage SO (2010) Src family tyrosine kinases activate thrombin-induced non-capacitative cation entry in human platelets. Platelets 21:445–450

    PubMed  CAS  Google Scholar 

  • Harper AG, Mason MJ, Sage SO (2009) A key role for dense granule secretion in potentiation of the Ca2+ signal arising from store-operated calcium entry in human platelets. Cell Calcium 45:413–420

    PubMed  CAS  Google Scholar 

  • Harrison P, Cramer EM (1993) Platelet alpha-granules. Blood Rev 7:52–62

    PubMed  CAS  Google Scholar 

  • Hassock SR, Zhu MX, Trost C, Flockerzi V, Authi KS (2002) Expression and role of TRPC proteins in human platelets: evidence that TRPC6 forms the store-independent calcium entry channel. Blood 100:2801–2811

    PubMed  CAS  Google Scholar 

  • Hayem G (1882) Sur le méchanisme de l’arrêt des hémorrhagies. CR Acad Sci 95:18

    Google Scholar 

  • Heemskerk JW, Feijge MA, Sage SO, Walter U (1994) Indirect regulation of Ca2+ entry by cAMP-dependent and cGMP-dependent protein kinases and phospholipase C in rat platelets. Eur J Biochem 223:543–551

    PubMed  CAS  Google Scholar 

  • Hiraga H, Oshima T, Yoshimura M, Matsuura H, Kajiyama G (1998) Abnormal platelet Ca2+ handling accompanied by increased cytosolic free Mg2+ in essential hypertension. Am J Physiol 275:R574–R579

    PubMed  CAS  Google Scholar 

  • Hoth M, Penner R (1992) Depletion of intracellular calcium stores activates a calcium current in mast cells. Nature 355:353–356

    PubMed  CAS  Google Scholar 

  • Huang GN, Zeng W, Kim JY, Yuan JP, Han L, Muallem S, Worley PF (2006) STIM1 carboxyl-terminus activates native SOC, ICRAC and TRPC1 channels. Nat Cell Biol 8:1003–1010

    PubMed  CAS  Google Scholar 

  • Itagaki K, Kannan KB, Singh BB, Hauser CJ (2004) Cytoskeletal reorganization internalizes multiple transient receptor potential channels and blocks calcium entry into human neutrophils. J Immunol 172:601–607

    PubMed  CAS  Google Scholar 

  • Jardin I, Redondo PC, Salido GM, Pariente JA, Rosado JA (2006) Endogenously generated reactive oxygen species reduce PMCA activity in platelets from patients with non-insulin-dependent diabetes mellitus. Platelets 17:283–288

    PubMed  CAS  Google Scholar 

  • Jardin I, Ben Amor N, Bartegi A, Pariente JA, Salido GM, Rosado JA (2007a) Differential involvement of thrombin receptors in Ca2+ release from two different intracellular stores in human platelets. Biochem J 401:167–174

    PubMed  CAS  Google Scholar 

  • Jardin I, Ben Amor N, Hernandez-Cruz JM, Salido GM, Rosado JA (2007b) Involvement of SNARE proteins in thrombin-induced platelet aggregation: evidence for the relevance of Ca2+ entry. Arch Biochem Biophys 465:16–25

    PubMed  CAS  Google Scholar 

  • Jardin I, Lopez JJ, Salido GM, Rosado JA (2008a) Functional relevance of the de novo coupling between hTRPC1 and type II IP3 receptor in store-operated Ca2+ entry in human platelets. Cell Signal 20:737–747

    PubMed  CAS  Google Scholar 

  • Jardin I, Lopez JJ, Salido GM, Rosado JA (2008b) Orai1 mediates the interaction between STIM1 and hTRPC1 and regulates the mode of activation of hTRPC1-forming Ca2+ channels. J Biol Chem 283:25296–25304

    PubMed  CAS  Google Scholar 

  • Jardin I, Redondo PC, Salido GM, Rosado JA (2008c) Phosphatidylinositol 4,5-bisphosphate enhances store-operated calcium entry through hTRPC6 channel in human platelets. Biochim Biophys Acta 1783:84–97

    PubMed  CAS  Google Scholar 

  • Jardin I, Salido GM, Rosado JA (2008d) Role of lipid rafts in the interaction between hTRPC1, Orai1 and STIM1. Channels (Austin) 2:401–403

    Google Scholar 

  • Jardin I, Gomez LJ, Salido GM, Rosado JA (2009a) Dynamic interaction of hTRPC6 with the Orai1-STIM1 complex or hTRPC3 mediates its role in capacitative or non-capacitative Ca2+ entry pathways. Biochem J 420:267–276

    PubMed  CAS  Google Scholar 

  • Jardin I, Lopez JJ, Redondo PC, Salido GM, Rosado JA (2009b) Store-operated Ca2+ entry is sensitive to the extracellular Ca2+ concentration through plasma membrane STIM1. Biochim Biophys Acta 1793:1614–1622

    PubMed  CAS  Google Scholar 

  • Kawasaki T, Lange I, Feske S (2009) A minimal regulatory domain in the C terminus of STIM1 binds to and activates ORAI1 CRAC channels. Biochem Biophys Res Commun 385:49–54

    PubMed  CAS  Google Scholar 

  • Kim MS, Zeng W, Yuan JP, Shin DM, Worley PF, Muallem S (2009) Native store-operated Ca2+ influx requires the channel function of Orai1 and TRPC1. J Biol Chem 284:9733–9741

    PubMed  CAS  Google Scholar 

  • Kiselyov K, Xu X, Mozhayeva G, Kuo T, Pessah I, Mignery G, Zhu X, Birnbaumer L, Muallem S (1998) Functional interaction between InsP3 receptors and store-operated Htrp3 channels. Nature 396:478–482

    PubMed  CAS  Google Scholar 

  • Krause E, Pfeiffer F, Schmid A, Schulz I (1996) Depletion of intracellular calcium stores activates a calcium conducting nonselective cation current in mouse pancreatic acinar cells. J Biol Chem 271:32523–32528

    PubMed  CAS  Google Scholar 

  • Kunzelmann C, Freyssinet JM, Martinez MC (2004) Rho A participates in the regulation of phosphatidylserine-dependent procoagulant activity at the surface of megakaryocytic cells. J Thromb Haemost 2:644–650

    PubMed  CAS  Google Scholar 

  • Li Y, Woo V, Bose R (2001) Platelet hyperactivity and abnormal Ca2+ homeostasis in diabetes mellitus. Am J Physiol Heart Circ Physiol 280:H1480–H1489

    PubMed  CAS  Google Scholar 

  • Liao Y, Erxleben C, Yildirim E, Abramowitz J, Armstrong DL, Birnbaumer L (2007) Orai proteins interact with TRPC channels and confer responsiveness to store depletion. Proc Natl Acad Sci USA 104:4682–4687

    PubMed  CAS  Google Scholar 

  • Liao Y, Erxleben C, Abramowitz J, Flockerzi V, Zhu MX, Armstrong DL, Birnbaumer L (2008) Functional interactions among Orai1, TRPCs, and STIM1 suggest a STIM-regulated heteromeric Orai/TRPC model for SOCE/Icrac channels. Proc Natl Acad Sci USA 105:2895–2900

    PubMed  CAS  Google Scholar 

  • Liao Y, Plummer NW, George MD, Abramowitz J, Zhu MX, Birnbaumer L (2009) A role for Orai in TRPC-mediated Ca2+ entry suggests that a TRPC:Orai complex may mediate store and receptor operated Ca2+ entry. Proc Natl Acad Sci USA 106:3202–3206

    PubMed  CAS  Google Scholar 

  • Liou J, Kim ML, Heo WD, Jones JT, Myers JW, Ferrell JE Jr, Meyer T (2005) STIM is a Ca2+ sensor essential for Ca2+-store-depletion-triggered Ca2+ influx. Curr Biol 15:1235–1241

    PubMed  CAS  Google Scholar 

  • Liu X, Singh BB, Ambudkar IS (2003) TRPC1 is required for functional store-operated Ca2+ channels. Role of acidic amino acid residues in the S5-S6 region. J Biol Chem 278:11337–11343

    PubMed  CAS  Google Scholar 

  • Liu J, Fitzgerald ME, Berndt MC, Jackson CW, Gartner TK (2006) Bruton tyrosine kinase is essential for botrocetin/VWF-induced signaling and GPIb-dependent thrombus formation in vivo. Blood 108:2596–2603

    PubMed  CAS  Google Scholar 

  • Liu D, Maier A, Scholze A, Rauch U, Boltzen U, Zhao Z, Zhu Z, Tepel M (2008) High glucose enhances transient receptor potential channel canonical type 6-dependent calcium influx in human platelets via phosphatidylinositol 3-kinase-dependent pathway. Arterioscler Thromb Vasc Biol 28:746–751

    PubMed  Google Scholar 

  • Lopez JJ, Camello-Almaraz C, Pariente JA, Salido GM, Rosado JA (2005) Ca2+ accumulation into acidic organelles mediated by Ca2+- and vacuolar H+-ATPases in human platelets. Biochem J 390:243–252

    PubMed  CAS  Google Scholar 

  • Lopez JJ, Salido GM, Pariente JA, Rosado JA (2006) Interaction of STIM1 with endogenously expressed human canonical TRP1 upon depletion of intracellular Ca2+ stores. J Biol Chem 281:28254–28264

    PubMed  CAS  Google Scholar 

  • Lopez JJ, Jardin I, Bobe R, Pariente JA, Enouf J, Salido GM, Rosado JA (2008) STIM1 regulates acidic Ca2+ store refilling by interaction with SERCA3 in human platelets. Biochem Pharmacol 75:2157–2164

    PubMed  CAS  Google Scholar 

  • Lu M, Branstrom R, Berglund E, Hoog A, Bjorklund P, Westin G, Larsson C, Farnebo LO, Forsberg L (2010) Expression and association of TRPC subtypes with Orai1 and STIM1 in human parathyroid. J Mol Endocrinol 44:285–294

    PubMed  CAS  Google Scholar 

  • Lueckhoff A, Clapham DE (1994) Calcium channels activated by depletion of internal calcium stores in A431 cells. Biophys J 67:177–182

    CAS  Google Scholar 

  • Luik RM, Wang B, Prakriya M, Wu MM, Lewis RS (2008) Oligomerization of STIM1 couples ER calcium depletion to CRAC channel activation. Nature 454:538–542

    PubMed  CAS  Google Scholar 

  • MacKenzie AB, Mahaut-Smith MP, Sage SO (1996) Activation of receptor-operated cation channels via P2X1 not P2T purinoceptors in human platelets. J Biol Chem 271:2879–2881

    PubMed  CAS  Google Scholar 

  • Manji SS, Parker NJ, Williams RT, van Stekelenburg L, Pearson RB, Dziadek M, Smith PJ (2000) STIM1: a novel phosphoprotein located at the cell surface. Biochim Biophys Acta 1481:147–255

    PubMed  CAS  Google Scholar 

  • Mignen O, Thompson JL, Shuttleworth TJ (2008) Orai1 subunit stoichiometry of the mammalian CRAC channel pore. J Physiol 586:419–425

    PubMed  CAS  Google Scholar 

  • Muik M, Fahrner M, Derler I, Schindl R, Bergsmann J, Frischauf I, Groschner K, Romanin C (2009) A cytosolic homomerization and a modulatory domain within STIM1 C terminus determine coupling to ORAI1 channels. J Biol Chem 284:8421–8426

    PubMed  CAS  Google Scholar 

  • Ng LC, McCormack MD, Airey JA, Singer CA, Keller PS, Shen XM, Hume JR (2009) TRPC1 and STIM1 mediate capacitative Ca2+ entry in mouse pulmonary arterial smooth muscle cells. J Physiol 587:2429–2442

    PubMed  CAS  Google Scholar 

  • Ong HL, Cheng KT, Liu X, Bandyopadhyay BC, Paria BC, Soboloff J, Pani B, Gwack Y, Srikanth S, Singh BB, Gill DL, Ambudkar IS (2007) Dynamic assembly of TRPC1-STIM1-Orai1 ternary complex is involved in store-operated calcium influx. Evidence for similarities in store-operated and calcium release-activated calcium channel components. J Biol Chem 282:9105–9116

    PubMed  CAS  Google Scholar 

  • Papp B, Enyedi A, Paszty K, Kovacs T, Sarkadi B, Gardos G, Magnier C, Wuytack F, Enouf J (1992) Simultaneous presence of two distinct endoplasmic-reticulum-type calcium-pump isoforms in human cells. Characterization by radio-immunoblotting and inhibition by 2,5-di-(t-butyl)-1,4-benzohydroquinone. Biochem J 288:297–302

    PubMed  CAS  Google Scholar 

  • Parekh AB, Putney JW Jr (2005) Store-operated calcium channels. Physiol Rev 85:757–810

    PubMed  CAS  Google Scholar 

  • Park CY, Hoover PJ, Mullins FM, Bachhawat P, Covington ED, Raunser S, Walz T, Garcia KC, Dolmetsch RE, Lewis RS (2009) STIM1 clusters and activates CRAC channels via direct binding of a cytosolic domain to Orai1. Cell 136:876–890

    PubMed  CAS  Google Scholar 

  • Putney JW Jr (1986) A model for receptor-regulated calcium entry. Cell Calcium 7:1–12

    PubMed  CAS  Google Scholar 

  • Redondo PC, Harper AG, Salido GM, Pariente JA, Sage SO, Rosado JA (2004) A role for SNAP-25 but not VAMPs in store-mediated Ca2+ entry in human platelets. J Physiol 558:99–109

    PubMed  CAS  Google Scholar 

  • Redondo PC, Ben-Amor N, Salido GM, Bartegi A, Pariente JA, Rosado JA (2005a) Ca2+-independent activation of Bruton’s tyrosine kinase is required for store-mediated Ca2+ entry in human platelets. Cell Signal 17:1011–1021

    PubMed  CAS  Google Scholar 

  • Redondo PC, Jardin I, Hernandez-Cruz JM, Pariente JA, Salido GM, Rosado JA (2005b) Hydrogen peroxide and peroxynitrite enhance Ca2+ mobilization and aggregation in platelets from type 2 diabetic patients. Biochem Biophys Res Commun 333:794–802

    PubMed  CAS  Google Scholar 

  • Redondo PC, Harper MT, Rosado JA, Sage SO (2006) A role for cofilin in the activation of store-operated calcium entry by de novo conformational coupling in human platelets. Blood 107:973–979

    PubMed  CAS  Google Scholar 

  • Redondo PC, Harper AG, Sage SO, Rosado JA (2007) Dual role of tubulin-cytoskeleton in store-operated calcium entry in human platelets. Cell Signal 19:2147–2154

    PubMed  CAS  Google Scholar 

  • Redondo PC, Jardin I, Lopez JJ, Salido GM, Rosado JA (2008) Intracellular Ca2+ store depletion induces the formation of macromolecular complexes involving hTRPC1, hTRPC6, the type II IP3 receptor and SERCA3 in human platelets. Biochim Biophys Acta 1783:1163–1176

    PubMed  CAS  Google Scholar 

  • Roos J, DiGregorio PJ, Yeromin AV, Ohlsen K, Lioudyno M, Zhang S, Safrina O, Kozak JA, Wagner SL, Cahalan MD, Velicelebi G, Stauderman KA (2005) STIM1, an essential and conserved component of store-operated Ca2+ channel function. J Cell Biol 169:435–445

    PubMed  CAS  Google Scholar 

  • Rosado JA, Sage SO (2000a) The actin cytoskeleton in store-mediated calcium entry. J Physiol 526(Pt 2):221–229

    PubMed  CAS  Google Scholar 

  • Rosado JA, Sage SO (2000b) Coupling between inositol 1,4,5-trisphosphate receptors and human transient receptor potential channel 1 when intracellular Ca2+ stores are depleted. Biochem J 350(Pt 3):631–635

    PubMed  CAS  Google Scholar 

  • Rosado JA, Sage SO (2000c) Farnesylcysteine analogues inhibit store-regulated Ca2+ entry in human platelets: evidence for involvement of small GTP-binding proteins and actin cytoskeleton. Biochem J 347(Pt 1):183–192

    PubMed  CAS  Google Scholar 

  • Rosado JA, Sage SO (2000d) Protein kinase C activates non-capacitative calcium entry in human platelets. J Physiol 529(Pt 1):159–169

    PubMed  CAS  Google Scholar 

  • Rosado JA, Sage SO (2000e) A role for the actin cytoskeleton in the initiation and maintenance of store-mediated calcium entry in human platelets. Trends Cardiovasc Med 10:327–332

    PubMed  CAS  Google Scholar 

  • Rosado JA, Sage SO (2001) Activation of store-mediated calcium entry by secretion-like coupling between the inositol 1,4,5-trisphosphate receptor type II and human transient receptor potential (hTrp1) channels in human platelets. Biochem J 356:191–198

    PubMed  CAS  Google Scholar 

  • Rosado JA, Graves D, Sage SO (2000) Tyrosine kinases activate store-mediated Ca2+ entry in human platelets through the reorganization of the actin cytoskeleton. Biochem J 351(Pt 2):429–437

    PubMed  CAS  Google Scholar 

  • Rosado JA, Meijer EM, Hamulyak K, Novakova I, Heemskerk JW, Sage SO (2001a) Fibrinogen binding to the integrin alpha(IIb)beta(3) modulates store-mediated calcium entry in human platelets. Blood 97:2648–2656

    PubMed  CAS  Google Scholar 

  • Rosado JA, Porras T, Conde M, Sage SO (2001b) Cyclic nucleotides modulate store-mediated calcium entry through the activation of protein-tyrosine phosphatases and altered actin polymerization in human platelets. J Biol Chem 276:15666–15675

    PubMed  CAS  Google Scholar 

  • Rosado JA, Brownlow SL, Sage SO (2002) Endogenously expressed Trp1 is involved in store-mediated Ca2+ entry by conformational coupling in human platelets. J Biol Chem 277:42157–42163

    PubMed  CAS  Google Scholar 

  • Rosado JA, Lopez JJ, Harper AG, Harper MT, Redondo PC, Pariente JA, Sage SO, Salido GM (2004a) Two pathways for store-mediated calcium entry differentially dependent on the actin cytoskeleton in human platelets. J Biol Chem 279:29231–29235

    PubMed  CAS  Google Scholar 

  • Rosado JA, Saavedra FR, Redondo PC, Hernandez-Cruz JM, Salido GM, Pariente JA (2004b) Reduced plasma membrane Ca2+-ATPase function in platelets from patients with non-insulin-dependent diabetes mellitus. Haematologica 89:1142–1144

    PubMed  CAS  Google Scholar 

  • Saavedra FR, Redondo PC, Hernandez-Cruz JM, Salido GM, Pariente JA, Rosado JA (2004) Store-operated Ca2+ entry and tyrosine kinase pp 60src hyperactivity are modulated by hyperglycemia in platelets from patients with non insulin-dependent diabetes mellitus. Arch Biochem Biophys 432:261–268

    PubMed  CAS  Google Scholar 

  • Sage SO, Merritt JE, Hallam TJ, Rink TJ (1989) Receptor-mediated calcium entry in fura-2-loaded human platelets stimulated with ADP and thrombin. Dual-wavelengths studies with Mn2+. Biochem J 258:923–926

    PubMed  CAS  Google Scholar 

  • Salido GM, Sage SO, Rosado JA (2009a) Biochemical and functional properties of the store-operated Ca2+ channels. Cell Signal 21:457–461

    PubMed  CAS  Google Scholar 

  • Salido GM, Sage SO, Rosado JA (2009b) TRPC channels and store-operated Ca2+ entry. Biochim Biophys Acta 1793:223–230

    PubMed  CAS  Google Scholar 

  • Sampieri A, Angelica Z, Carlos S, Alfonso S, Vaca L (2008a) STIM1 converts TRPC1 from a receptor-operated to a store-operated channel: moving TRPC1 in and out of lipid rafts. Cell Calcium 44:479–491

    Google Scholar 

  • Sampieri A, Zepeda A, Saldaña C, Salgado A, Vaca L (2008b) STIM1 converts TRPC1 from a receptor-operated to a store-operated channel: moving TRPC1 in and out of lipid rafts. Cell Calcium 44:479–491

    Google Scholar 

  • Sargeant P, Farndale RW, Sage SO (1993) ADP- and thapsigargin-evoked Ca2+ entry and protein-tyrosine phosphorylation are inhibited by the tyrosine kinase inhibitors genistein and methyl-2,5-dihydroxycinnamate in fura-2-loaded human platelets. J Biol Chem 268:18151–18156

    PubMed  CAS  Google Scholar 

  • Sargeant P, Farndale RW, Sage SO (1994) Calcium store depletion in dimethyl BAPTA-loaded human platelets increases protein tyrosine phosphorylation in the absence of a rise in cytosolic calcium. Exp Physiol 79:269–272

    PubMed  CAS  Google Scholar 

  • Schaeffer G, Wascher TC, Kostner GM, Graier WF (1999) Alterations in platelet Ca2+ signalling in diabetic patients is due to increased formation of superoxide anions and reduced nitric oxide production. Diabetologia 42:167–176

    PubMed  CAS  Google Scholar 

  • Smyth JT, DeHaven WI, Bird GS, Putney JW Jr (2007) Role of the microtubule cytoskeleton in the function of the store-operated Ca2+ channel activator STIM1. J Cell Sci 120:3762–3771

    PubMed  CAS  Google Scholar 

  • Sobol AB, Watala C (2000) The role of platelets in diabetes-related vascular complications. Diabetes Res Clin Pract 50:1–16

    PubMed  CAS  Google Scholar 

  • Sours-Brothers S, Ding M, Graham S, Ma R (2009) Interaction between TRPC1/TRPC4 assembly and STIM1 contributes to store-operated Ca2+ entry in mesangial cells. Exp Biol Med (Maywood) 234:673–682

    CAS  Google Scholar 

  • Spassova MA, Soboloff J, He LP, Xu W, Dziadek MA, Gill DL (2006) STIM1 has a plasma membrane role in the activation of store-operated Ca2+ channels. Proc Natl Acad Sci USA 103:4040–4045

    PubMed  CAS  Google Scholar 

  • Tang J, Lin Y, Zhang Z, Tikunova S, Birnbaumer L, Zhu MX (2001) Identification of common binding sites for calmodulin and inositol 1,4,5-trisphosphate receptors on the carboxyl termini of trp channels. J Biol Chem 276:21303–21310

    PubMed  CAS  Google Scholar 

  • Tolhurst G, Carter RN, Amisten S, Holdich JP, Erlinge D, Mahaut-Smith MP (2008) Expression profiling and electrophysiological studies suggest a major role for Orai1 in the store-operated Ca2+ influx pathway of platelets and megakaryocytes. Platelets 19:308–313

    PubMed  CAS  Google Scholar 

  • Tomiyama Y, Shiraga M, Kinoshita S, Ambo H, Kurata Y, Matsuzawa Y, Kunicki TJ (1998) A Glanzmann thrombasthenia-like phenotype caused by a defect in inside-out signaling through the integrin alpha(IIb)beta3. Thromb Haemost 80:735–742

    PubMed  CAS  Google Scholar 

  • Vaca L, Kunze DL (1994) Depletion of intracellular Ca2+ stores activates a Ca2+-selective channel in vascular endothelium. Am J Physiol Cell Physiol 267(4):C920–C925

    CAS  Google Scholar 

  • Varga-Szabo D, Authi KS, Braun A, Bender M, Ambily A, Hassock SR, Gudermann T, Dietrich A, Nieswandt B (2008) Store-operated Ca2+ entry in platelets occurs independently of transient receptor potential (TRP) C1. Pflugers Arch 457:377–387

    PubMed  CAS  Google Scholar 

  • Vazquez G, Bird GS, Mori Y, Putney JW Jr (2006) Native TRPC7 channel activation by an inositol trisphosphate receptor-dependent mechanism. J Biol Chem 281:25250–25258

    PubMed  CAS  Google Scholar 

  • Vig M, Peinelt C, Beck A, Koomoa DL, Rabah D, Koblan-Huberson M, Kraft S, Turner H, Fleig A, Penner R, Kinet JP (2006) CRACM1 is a plasma membrane protein essential for store-operated Ca2+ entry. Science 312:1220–1223

    PubMed  CAS  Google Scholar 

  • Woodard GE, Lopez JJ, Jardin I, Salido GM, Rosado JA (2010) TRPC3 regulates agonist-stimulated Ca2+ mobilization by mediating the interaction between type I inositol 1,4,5-trisphosphate receptor, RACK1, and Orai1. J Biol Chem 285:8045–8053

    PubMed  CAS  Google Scholar 

  • Worley PF, Zeng W, Huang GN, Yuan JP, Kim JY, Lee MG, Muallem S (2007) TRPC channels as STIM1-regulated store-operated channels. Cell Calcium 42:205–211

    PubMed  CAS  Google Scholar 

  • Yeromin AV, Zhang SL, Jiang W, Yu Y, Safrina O, Cahalan MD (2006) Molecular identification of the CRAC channel by altered ion selectivity in a mutant of Orai. Nature 443:226–229

    PubMed  CAS  Google Scholar 

  • Yuan JP, Zeng W, Huang GN, Worley PF, Muallem S (2007) STIM1 heteromultimerizes TRPC channels to determine their function as store-operated channels. Nat Cell Biol 9:636–645

    PubMed  CAS  Google Scholar 

  • Yuan JP, Zeng W, Dorwart MR, Choi YJ, Worley PF, Muallem S (2009) SOAR and the polybasic STIM1 domains gate and regulate Orai channels. Nat Cell Biol 11:337–343

    PubMed  CAS  Google Scholar 

  • Zbidi H, Lopez JJ, Amor NB, Bartegi A, Salido GM, Rosado JA (2009) Enhanced expression of STIM1/Orai1 and TRPC3 in platelets from patients with type 2 diabetes mellitus. Blood Cells Mol Dis 43:211–213

    PubMed  CAS  Google Scholar 

  • Zeng W, Yuan JP, Kim MS, Choi YJ, Huang GN, Worley PF, Muallem S (2008) STIM1 gates TRPC channels, but not Orai1, by electrostatic interaction. Mol Cell 32:439–448

    PubMed  CAS  Google Scholar 

  • Zhang SL, Yu Y, Roos J, Kozak JA, Deerinck TJ, Ellisman MH, Stauderman KA, Cahalan MD (2005) STIM1 is a Ca2+ sensor that activates CRAC channels and migrates from the Ca2+ store to the plasma membrane. Nature 437:902–905

    PubMed  CAS  Google Scholar 

  • Zhang ZY, Pan LJ, Zhang ZM (2010) Functional interactions among STIM1, Orai1 and TRPC1 on the activation of SOCs in HL-7702 cells. Amino Acids 39:195–204

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Juan A. Rosado .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2012 Springer-Verlag Wien

About this chapter

Cite this chapter

Lopez, J.J., Salido, G.M., Rosado, J.A. (2012). Cardiovascular System. In: Groschner, K., Graier, W., Romanin, C. (eds) Store-operated Ca2+ entry (SOCE) pathways. Springer, Vienna. https://doi.org/10.1007/978-3-7091-0962-5_24

Download citation

Publish with us

Policies and ethics