Abstract
Calcium plays important role in biological systems where it is involved in diverse mechanisms such as signaling, muscle contraction and neuromodulation. Action potentials are generated by dynamic interaction of ionic channels located on the plasma-membrane and these drive the rhythmic activity of biological systems such as the smooth muscle and the heart. However, ionic channels are not the only pacemakers; an intimate interaction between intracellular Ca2+ stores and ionic channels underlie rhythmic activity. In this review we will focus on the role of Ca2+ stores in regulation of rhythmical behavior.
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- IP3 :
-
Inositol 1,4,5-trisphosphate
- CICR:
-
Ca2+-induced-Ca2+ release
- ER:
-
Endoplasmic reticulum
References
Berridge MJ, Bootman MD, Roderick HL (2003) Calcium signalling: dynamics, homeostasis and remodelling. Nat Rev Mol Cell Biol 4:517–529
Sammels E, Parys JB, Missiaen L, De Smedt H, Bultynck G (2010) Intracellular Ca2+ storage in health and disease: a dynamic equilibrium. Cell Calcium 47:297–314
Wray S, Burdyga T (2010) Sarcoplasmic reticulum function in smooth muscle. Physiol Rev 90:113–178
Berridge MJ (2002) The endoplasmic reticulum: a multifunctional signaling organelle. Cell Calcium 32:235–249
Foskett JK, White C, Cheung K-H, Mak D-OD (2007) Inositol trisphosphate receptor Ca2+ release channels. Physiol Rev 87:593–658
Mikoshiba K (2007) IP3 receptor/Ca2+ channel: from discovery to new signaling concepts. J Neurochem 102:1426–1446
Zalk R, Lehnart SE, Marks AR (2007) Modulation of the ryanodine receptor and intracellular calcium. Annu Rev Biochem 76:367–385
Woods NM, Cuthbertson KS, Cobbold PH (1986) Repetitive transient rises in cytoplasmic free calcium in hormone-stimulated hepatocytes. Nature 319:600–602
Berridge MJ (1993) Inositol trisphosphate and calcium signalling. Nature 361:315–325
Meissner G (2002) Regulation of mammalian ryanodine receptors. Front Biosci 7:2072–2080
Endo M (1977) Calcium release from the sarcoplasmic reticulum. Physiol Rev 57:71–108
Iino M (1990) Biphasic Ca2+ dependence of inositol 1,4,5-trisphosphate-induced Ca2+ release in smooth muscle cells of the guinea pig taenia caeci. J Gen Physiol 95:1103–1122
Parker I, Yao Y (1991) Regenerative release of calcium from functionally discrete subcellular stores by inositol trisphosphate. Proc R Soc Ser B 246:269–274
Cheng H, Lederer WJ, Cannell MB (1993) Calcium sparks: elementary events underlying excitation-contraction coupling in heart muscle. Science 262:740–744
Lechleiter J, Girard S, Peralta E, Clapham D (1991) Spiral calcium wave propagation and annihilation in Xenopus laevis oocytes. Science 252:123–126
Devine CE, Somlyo AV, Somlyo AP (1972) Sarcoplasmic reticulum and excitation-contraction coupling in mammalian smooth muscles. J Cell Biol 52:690–718
Kuo KH, Herrera AM, Seow CY (2003) Ultrastructure of airway smooth muscle. Respir Physiol Neurobiol 137:197–208
van Breemen C, Chen Q, Laher I (1995) Superficial buffer barrier function of smooth muscle sarcoplasmic reticulum. Trends Pharmacol Sci 16:98–105
Yoshikawa A, van Breemen C, Isenberg G (1996) Buffering of plasmalemmal Ca2+ current by sarcoplasmic reticulum of guinea pig urinary bladder myocytes. Am J Physiol 271:C833–C841
White C, McGeown JG (2000) Ca2+ uptake by the sarcoplasmic reticulum decreases the amplitude of depolarization-dependent [Ca2+]i transients in rat gastric myocytes. Pflugers Arch 440:488–495
Young RC, Schumann R, Zhang P (2001) Intracellular calcium gradients in cultured human uterine smooth muscle: a functionally important subplasmalemmal space. Cell Calcium 29:183–189
Shmigol AV, Eisner DA, Wray S (1999) The role of the sarcoplasmic reticulum as a Ca2+ sink in rat uterine smooth muscle cells. J Physiol 520 Pt 1:153–163
ZhuGe R, Tuft RA, Fogarty KE, Bellve K, Fay FS, Walsh JV Jr (1999) The influence of sarcoplasmic reticulum Ca2+ concentration on Ca2+ sparks and spontaneous transient outward currents in single smooth muscle cells. J Gen Physiol 113:215–228
Ganitkevich V, Hasse V, Pfitzer G (2002) Ca2+-Dependent and Ca2+-independent regulation of smooth muscle contraction. J Muscle Res Cell Motil 23:47–52
Benham CD, Bolton TB (1986) Spontaneous transient outward currents in single visceral and vascular smooth muscle cells of the rabbit. J Physiol 381:385–406
van Helden DF (1991) Spontaneous and noradrenaline-induced transient depolarizations in the smooth muscle of guinea-pig mesenteric vein. J Physiol 437:511–541
Wang Q, Hogg RC, Large WA (1992) Properties of spontaneous inward currents recorded in smooth muscle cells isolated from the rabbit portal vein. J Physiol 451:525–537
Brown HF (1982) Electrophysiology of the sinoatrial node. Physiol Rev 62:505–530
Noble D, Noble SJ (1984) A model of sino-atrial node electrical activity based on a modification of the DiFrancesco-Noble (1984) equations. Proc R Soc Lond B Biol Sci 222:295–304
Hodgkin AL, Rushton WAH (1946) The passive electrical properties of nerve axons. Proc R Soc Ser B 133:444–456
Berridge MJ (2008) Smooth muscle cell calcium activation mechanisms. J Physiol 586:5047–5061
Van Helden DF (1993) Pacemaker potentials in lymphatic smooth muscle of the guinea-pig mesentery. J Physiol 471:465–479
Liu LW, Thuneberg L, Huizinga JD (1995) Cyclopiazonic acid, inhibiting the endoplasmic reticulum calcium pump, reduces the canine colonic pacemaker frequency. J Pharmacol Exp Ther 275:1058–1068
Hashitani H, van Helden DF, Suzuki H (1996) Properties of spontaneous depolarizations in circular smooth muscle cells of rabbit urethra. Br J Pharmacol 118:1627–1632
Sergeant GP, Hollywood MA, McCloskey KD, McHale NG, Thornbury KD (2001) Role of IP(3) in modulation of spontaneous activity in pacemaker cells of rabbit urethra. Am J Physiol Cell Physiol 280:C1349–C1356
Lang RJ, Nguyen DT, Matsuyama H, Takewaki T, Exintaris B (2006) Characterization of spontaneous depolarizations in smooth muscle cells of the Guinea pig prostate. J Urol 175:370–380
van Helden DF (1993) Pacemaker potentials in lymphatic smooth muscle of the guinea-pig mesentery. J Physiol (Lond) 471:465–479
van Helden DF, Imtiaz MS, Nurgaliyeva K, von der Weid P-Y, Dosen PJ (2000) Role of calcium stores and membrane voltage in the generation of slow wave action potentials in the guinea-pig gastric pylorus. J Physiol 524.1:245–265
Sanders KM (1996) A case for Interstitial cells of Cajal as pacemakers and mediators of neurotransmission in the gastrointestinal tract. Gastroenterology 111:492–515
Daniel EE, Bardakjian BL, Huizinga JD, Diamant NE (1994) Relaxation oscillator and core conductor models are needed for understanding of GI electrical activities. Am J Physiol 266:G339–G349
Exintaris B, DT TN, Lam M, Lang RJ (2009) Inositol trisphosphate-dependent Ca(2+) stores and mitochondria modulate slow wave activity arising from the smooth muscle cells of the guinea pig prostate gland. Br J Pharmacol 156:1098–1106
Suzuki H, Takano H, Yamamoto Y, Komuro T, Saito M, Kato K, Mikoshiba K (2000) Properties of gastric smooth muscles obtained from mice which lack inositol trisphosphate receptor. J Physiol 525:105–111
Suzuki H, Hirst GD (1999) Regenerative potentials evoked in circular smooth muscle of the antral region of guinea-pig stomach. J Physiol 517(Pt 2):563–573
Hirst GD, Bramich NJ, Teramoto N, Suzuki H, Edwards FR (2002) Regenerative component of slow waves in the guinea-pig gastric antrum involves a delayed increase in [Ca(2+)](i) and Cl(-) channels. J Physiol 540:907–919
von der Weid PY, Rahman M, Imtiaz MS, van Helden DF (2008) Spontaneous transient depolarizations in lymphatic vessels of the guinea pig mesentery: pharmacology and implication for spontaneous contractility. Am J Physiol Heart Circ Physiol 295:H1989–H2000
Peng H, Matchkov V, Ivarsen A, Aalkjaer C, Nilsson H (2001) Hypothesis for the initiation of vasomotion. Circ Res 88:810–815
van Helden DF, Imtiaz MS (2003) Ca2+ phase waves: a basis for cellular pacemaking and long- range synchronicity in the guinea-pig gastric pylorus. J Physiol 548.1:271–296
Allbritton NL, Meyer T, Stryer L (1992) Range of messenger action of calcium ion and inositol 1,4,5-trisphosphate. Science 258:1812–1815
Imtiaz MS, Zhao J, Hosaka K, von der Weid PY, Crowe M, van Helden DF (2007) Pacemaking through Ca2+ stores interacting as coupled oscillators via membrane depolarization. Biophys J 92:3843–3861
Imtiaz MS, Smith DW, van Helden DF (2002) A theoretical model of slow wave regulation using voltage-dependent synthesis of inositol 1,4,5-trisphosphate. Biophys J 83:1877–1890
Imtiaz MS, Zhao J, Hosaka K, Von Der Weid P-Y, Crowe M, van Helden D (2007) Pacemaking through Ca2+ stores interacting as coupled oscillators via membrane depolarization. Biophys 92:3843–3861
Koenigsberger M, Sauser R, Lamboley M, Beny JL, Meister JJ (2004) Ca2+ dynamics in a population of smooth muscle cells: modeling the recruitment and synchronization. Biophys J 87:92–104
Kapela A, Bezerianos A, Tsoukias NM (2008) A mathematical model of Ca2+ dynamics in rat mesenteric smooth muscle cell: agonist and NO stimulation. J Theor Biol 253:238–260
Mangoni ME, Nargeot J (2008) Genesis and regulation of the heart automaticity. Physiol Rev 88:919–982
DiFrancesco D (1985) The cardiac hyperpolarizing-activated current, if. Origins and developments. Prog Biophys Mol Biol 46:163–183
Maltsev VA, Lakatta EG (2009) Synergism of coupled subsarcolemmal Ca2+ clocks and sarcolemmal voltage clocks confers robust and flexible pacemaker function in a novel pacemaker cell model. Am J Physiol Heart Circ Physiol 296:H594–H615
Lakatta EG, Vinogradova T, Lyashkov A, Sirenko S, Zhu W, Ruknudin A, Maltsev VA (2006) The integration of spontaneous intracellular Ca2+ cycling and surface membrane ion channel activation entrains normal automaticity in cells of the Heart’s pacemaker. Ann N Y Acad Sci 1080:178–206
Imtiaz MS, von der Weid PY, van Helden DF (2010) Synchronization of Ca2+ oscillations: a coupled oscillator-based mechanism in smooth muscle. FEBS J 277:278–285
Huser J, Blatter LA, Lipsius SL (2000) Intracellular Ca2+ release contributes to automaticity in cat atrial pacemaker cells. J Physiol 524:415–422
Lipsius SL, Huser J, Blatter LA (2001) Intracellular Ca2+ release sparks atrial pacemaker activity. News Physiol Sci 16:101–106
Rubenstein DS, Lipsius SL (1989) Mechanisms of automaticity in subsidiary pacemakers from cat right atrium. Circ Res 64:648–657
Zhou Z, Lipsius SL (1993) Na(+)-Ca2+ exchange current in latent pacemaker cells isolated from cat right atrium. J Physiol 466:263–285
Rigg L, Heath BM, Cui Y, Terrar DA (2000) Localisation and functional significance of ryanodine receptors during beta-adrenoceptor stimulation in the guinea-pig sino-atrial node. Cardiovasc Res 48:254–264
Rigg L, Terrar DA (1996) Possible role of calcium release from the sarcoplasmic reticulum in pacemaking in guinea-pig sino-atrial node. Exp Physiol 81:877–880
Imtiaz MS, von der Weid PY, Laver DR, van Helden DF (2010) SR Ca2+ store refill–a key factor in cardiac pacemaking. J Mol Cell Cardiol 49:412–426
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
Casteels R, Droogmans G (1981) Exchange characteristics of the noradrenaline-sensitive calcium store in vascular smooth muscle cells or rabbit ear artery. J Physiol 317:263–279
Launikonis BS, Barnes M, Stephenson DG (2003) Identification of the coupling between skeletal muscle store-operated Ca2+ entry and the inositol trisphosphate receptor. Proc Natl Acad Sci USA 100:2941–2944
Huang J, van Breemen C, Kuo KH, Hove-Madsen L, Tibbits GF (2006) Store-operated Ca2+ entry modulates sarcoplasmic reticulum Ca2+ loading in neonatal rabbit cardiac ventricular myocytes. Am J Physiol Cell Physiol 290:C1572–C1582
Ju YK, Huang W, Jiang L, Barden JA, Allen DG (2003) ATP modulates intracellular Ca2+ and firing rate through a P2Y1 purinoceptor in cane toad pacemaker cells. J Physiol 552:777–787
Yamashita M, Sugioka M, Ogawa Y (2006) Voltage- and Ca2+-activated potassium channels in Ca2+ store control Ca2+ release. FEBS J 273:3585–3597
Yamashita M (2008) Synchronous Ca2+ oscillation emerges from voltage fluctuations of Ca2+ stores. FEBS J 275:4022–4032
Eisner DA, Kashimura T, Venetucci LA, Trafford AW (2009) From the ryanodine receptor to cardiac arrhythmias. Circ J 73:1561–1567
Eisner DA, Kashimura T, O’Neill SC, Venetucci LA, Trafford AW (2009) What role does modulation of the ryanodine receptor play in cardiac inotropy and arrhythmogenesis? J Mol Cell Cardiol 46:474–481
MacLennan DH, Chen SR (2009) Store overload-induced Ca2+ release as a triggering mechanism for CPVT and MH episodes caused by mutations in RYR and CASQ genes. J Physiol 587:3113–3115
Imtiaz MS (2003) Distributed pacemaking through coupled oscillator-based mechanisms: a basis for long-range signaling in smooth muscle. Newcastle, Australia, The University of Newcastle
Imtiaz MS, Katnik CP, Smith DW, van Helden DF (2006) Role of voltage-dependent modulation of store Ca2+ release in synchronization of Ca2+ oscillations. Biophys J 90:1–23
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Imtiaz, M.S. (2012). Calcium Oscillations and Pacemaking. In: Islam, M. (eds) Calcium Signaling. Advances in Experimental Medicine and Biology, vol 740. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-2888-2_22
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DOI: https://doi.org/10.1007/978-94-007-2888-2_22
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