Journal of Bioenergetics and Biomembranes

, Volume 46, Issue 5, pp 403–420 | Cite as

Modelling mechanism of calcium oscillations in pancreatic acinar cells

  • Neeraj ManhasEmail author
  • K. R. Pardasani


We present a simple model for calcium oscillations in the pancreatic acinar cells. This model is based on the calcium release from two receptors, inositol trisphosphate receptors (IPR) and ryanodine receptors (RyR) through the process of calcium induced calcium release (CICR). In pancreatic acinar cells, when the Ca2+ concentration increases, the mitochondria uptake it very fast to restrict Ca2+ response in the cell. Afterwards, a much slower release of Ca2+ from the mitochondria serves as a calcium supply in the cytosol which causes calcium oscillations. In this paper we discuss a possible mechanism for calcium oscillations based on the interplay among the three calcium stores in the cell: the endoplasmic reticulum (ER), mitochondria and cytosol. Our model predicts that calcium shuttling between ER and mitochondria is a pacemaker role in the generation of Ca2+oscillations. We also consider the calcium dependent production and degradation of (1,4,5) inositol-trisphosphate (IP3), which is a key source of intracellular calcium oscillations in pancreatic acinar cells. In this study we are able to predict the different patterns of calcium oscillations in the cell from sinusoidal to raised-baseline, high frequency and low-frequency baseline spiking.


Pancreatic acinar cell Calcium oscillations CICR Raised-baseline MMOs 



The first author is highly thankful to Prof. James Sneyd for inviting him in the University of Auckland and giving him a chance to work under his guidance. The first author would like to thank Dr. Ganesh Dixit former faculty in the University of Auckland for providing him moral support during his stay in Auckland, New Zealand. Authors would like to thank Laurence Palk, and Kate Patterson at the University of Auckland, Ivo Siekmann (Now in the University of Melbourne) for the helpful discussion related to nonlinear dynamics.


  1. Albrecht MA, Colegrove SL, Friel DD (2002) Differential regulation of ER Ca2+ uptake and release rates accounts for multiple modes of Ca2+ -induced Ca2+ release. J Gen Physiol 119:211–233Google Scholar
  2. Altschafl BA, Beutner G, Sharma VK (2007) The mitochondrial ryandoine receptor in rat heart. Biophys Acta 1768:1784–1795Google Scholar
  3. Ashby MC, Tepikin AV (2002) Polarized calcium and calmodulin signalling in secretory epithelia. Physiol Rev 82:701–734Google Scholar
  4. Ashby MC, Craske M, Park MK, Gerasimenko OV, Burgoyne RD, Petersen OH et al (2002) Localized Ca2+ uncaging reveals polarized distribution of Ca2+sensitive Ca2+ release sites: mechanism of unidirectional Ca2+ waves. J Cell Biol 158:283–292Google Scholar
  5. Ashby MC, Petersen OH, Tepikin AV (2003) Spatial characterisation of ryanodine-induced calcium release in mouse pancreatic acinar cells. J Bio Chem 369:441–445Google Scholar
  6. Atanasova KT, Shuttleworth TJ, Yule DI, Thomas JI, Sneyd J (2005) Calcium oscillations and membrane transport: the importance of two time scales. Multiscale Model Simul 3:245–264Google Scholar
  7. Atri A, Amundson J, Clapham D, Sneyd J (1993) A single-pool model for intracellular calcium oscillations and waves in the Xenopus laevis oocyte. Biophys J 65:1727–1739Google Scholar
  8. Bazil JN, Dash RK (2011) A minimal model of calcium dynamics in michondria rapid mode of Ca2+ uptake mechanism. PLoS ONE 6:1–13Google Scholar
  9. Berridge MJ (1993) Inositol trisphosphate and calcium signalling. Nature (London) 361:1727–1739Google Scholar
  10. Berridge MJ (1995) Capacitative calcium entry. Biochem J 312:1–11Google Scholar
  11. Berridge MJ (1997) Elementry and global aspects of calcium signalling. J Physiol 499:291–306Google Scholar
  12. Blank JL, Ross AH, Exton JH (1991) Purification and characterization of two G-protien that activates the beta-1 isozyme of phosphoinositede-specific phospholipase C. J Bio Chem 266:18206–18216Google Scholar
  13. Borghans JAM, Dupont G, Goldbeter A (1997) Complex intracellular calcium oscillations: a theoretical exploration of possible mechanism. Biophy Chem 66:25–41Google Scholar
  14. Chen XF, Li C, Wang PY, Li M, Wang W (2009) Dynamic simulation of the effect of calcium-release activated calcium channel on cytoplasmic Ca2+ oscillation. Biophys Chem 136:87–95Google Scholar
  15. Csordas G, Thomas AP, Hajnoczky G (2001) Calcium signal transmission between ryanodine receptors and mitochondria in cardiac muscle. TCM 11:269–275Google Scholar
  16. Dedkova E, Blatter L (2008) Mitochondrial Ca2+ and the heart. Cell Calcium 44:77–91Google Scholar
  17. Domijan M, Murray R, and Sneyd J (2006) Dynamical probing of the mechanisms underlying calcium oscillations. J Nonlinear Sci 1–24Google Scholar
  18. Dufour JF, Arias IM, Turner TJ (1997) Inositol 1,4,5- trisphosphate and calcium regulate the calcium channel function of the hepatic inositol 1,4,5-trisphosphate receptor. J Biol Chem 272:2675–2681Google Scholar
  19. Dupont G, Combettes L, Leybaer L (2007) Calcium dynamics: spatio-temporal organization from the subcellular to the organ level. Int Rev Cytol 261:193–245Google Scholar
  20. Dyzma M, Szopa P, Kazmierczak B (2012) Membrane associated complexes: new approach to calcium dynamics modelling. Math Model Nat Phenom 7:32–50Google Scholar
  21. Dyzma M, Szopa P, Kazmierczak B (2013) Membrane associated Complexex in calcium dynanmics modelling. Phys Biol 10:1–14Google Scholar
  22. Ermentrout B (2002) Simulating, analyzing,and animating dynamical systems: a guid to XP-PAUT for researcher and students. SIAMGoogle Scholar
  23. Fall CP, Keizer JE (2001) Mitochondrial modulation of intracellular Ca 2+ signaling. J Theor Biol 210:151–165Google Scholar
  24. Favre CJ, Schrenzel J, Jacquet J, Lew DP, Krause KH (1996) Highly supralinear feedback inhibition of Ca2+ uptake by the Ca2+ load of intracellular stores. J Bio Chem 271:14925–14930Google Scholar
  25. Filippin L, Magalhaes PJ, Di BG, Colella M, Pozzan T (2003) Stable interaction between mitochondria and endoplasmic reticulum allow rapid accomulation of calcium in subpopulation of mitochondria. J Bio Chem 278:39224Google Scholar
  26. Finch E, Turner T, Goldin S (1991) Calcium as a coagonist of inositol 1,4,5 trisphosphate-induced calcium release. Science 252:443–446Google Scholar
  27. Friel DD, Chiel HJ (2008) Calcium dynamics: analyzing the Ca2+ regulatory network in intact cells. Trends Neurosci 31:8–19Google Scholar
  28. Gin E, Crampin EJ, Brown DA, Shuttleworth TJ, Yule DI, Sneyd J (2007) A mathematical model of fluid secretion from a parotid acinar cell. J Theor Biol 248:64–80Google Scholar
  29. Gin E, Falcke M, Wagner LE, Yule DI, Sneyd J (2009) A kinetic model of the inositol trisphosphate receptor based on single channel data. Biophys J 96:4053–4062Google Scholar
  30. Giovannucci DR, Bruce JI, Straub SV, Arreola J, Sneyd J, Shuttleworth TJ et al. (2002) Cytosolic Ca2+ and Ca2+ activated Cl− current dynamics: insights from two functionally distinct mouse exocrine cells. J Physiol 1–16Google Scholar
  31. Grubelnik V, Larsen AZ, Kummer U, Olsen LF, Marhl M (2001) Mitochondria regulate the amplitude of simple and complex calcium oscillations. Biophys Chem 94:59–74Google Scholar
  32. Gunter TE, Gunter KK (2001) Uptake of calcium by mitochondria: transport and possible function. IUBMB Life 52:197–04Google Scholar
  33. Gunter TE, Yule DI, Gunter KK, Eliseev RA, Salter JD (2004) Calcium and mitochondria. FEBS Lett 567:96–102Google Scholar
  34. Habara Y, Kanno T (1993) Stimulus-secretion coupling and Ca2+ dynamics in pancreatic acinar cells. Pergamon 25:843–850Google Scholar
  35. Hajnoczky G, Csordas G, Yi M (2002) Old players in a new role:mitochondria-associated membranes, VDAC, and ryanodine receptors as contributors to calcium signalpropagation from endoplasmic reticulum to the mitochondria. Cell Calcium 32:363–377Google Scholar
  36. Harootunian AT, Kao JP, Paranjape S, Tsien RY (1991) Generation of calcium oscillation in fibroblasts by postive feedback between calcium and IP3. Science 251:75–78Google Scholar
  37. Harvey E, Kirk V, Osinga HM, Sneyd J (2010) Understanding anomalous delays in a model of intracellular calcium dynamics. Chaos 20:1–20, 045104Google Scholar
  38. Harvey E, Kirk V, Wechselberger M, Sneyd J (2011) Multiple timescales, mixed mode oscillations and canards in models of intracellular calcium dynamics. J Nonlinear Sci 21:639–683Google Scholar
  39. Iino M (2010) Spatiotemporal dynamics of Ca2+ signaling and its physiological roles. Proc Jpn Acad Ser B 86:244–256Google Scholar
  40. Ishii K, Hirose K, Iino M (2006) Ca2+ shuttling between endoplasmic reticulum and mitochondria underlying Ca2+ oscillations. EMBO J 7:390–396Google Scholar
  41. Jacob R (1989) Calcium oscillations in electrically non-excitable cells. Biochim Biophys Acta 1052:427–438Google Scholar
  42. Jaing D, Zhao L, Clapham DE (2009) Genome-wide rnai screen identifies letm1 as a mitochondrial Ca2+/H+ antiporter. Science 326:144–147Google Scholar
  43. Jouaville LS, Ichas F, Holmuhamedov EL, Camacho P, Lechleiter JD (1995) Synchronization of calcium waves by mitochondrial substrates in Xenopus laevis oocyte. Nature 377:438–441Google Scholar
  44. Keener J, Sneyd J (2008) Mathematical physiology: Cellular physiology. In: Antman SS, Marsden JE, Sirovich L (eds) Interdisciplinary applied mathematics, vol 8, 2nd edn. Springer, New York, p 1182Google Scholar
  45. Keizer J, De Young GW (1992) Two roles for calcium in agonist stimulated calcium oscillations. J Biophys 61:649–660Google Scholar
  46. Keizer J, Levine L (1996) Ryanodine receptor adaptation and Ca2+ induced Ca2+ release dependent Ca2+ oscillations. Biophys J 71:3477–3487Google Scholar
  47. Kopach O, Kruglikov I, Pivneva T, Voitenko N, Verkhratsky A, Fedirko N (2011) Mitochondria adjust Ca2+ signaling regime to a pattern of stimulation in salivary acinar cells. Biochim Biophys Acta 1813:1740–1748Google Scholar
  48. LeBeau AP, Yule DI, Groblewski GE, Sneyd J (1999) Agonist-dependent phosphorylation of the Inositol1,4,5-trisphosphate receptor:a possible mechanism for agonist-specific calcium oscillations in pancreatic acinar cells. J Gen Physiol 113:851–871Google Scholar
  49. Lee MG, Xu X, Zeng W, Diaz J, Wojcikiewicz RJH, Kuo TH et al (1997) Polarized expression of Ca2+ channels in pancreatic and salivary gland cells. J Biol Chem 272:15765–15770Google Scholar
  50. Leite MF, Dranoff JA, Gao L, Nathanson MH (1999) Expression and subcellular localization of the ryanodine receptor in rat pancreatic acinar cells. Biochem J 337:305–309Google Scholar
  51. Leite MF, Andrade VA, Nathanson MH (2010) Signaling pathways in biliary epithelial cells 25–39Google Scholar
  52. Leung PS (2010) Physiology of the pancreas. In (ed.), Vol. 690, pp. 13–27, Springer ScienceGoogle Scholar
  53. Low JT, Shukla A, Thorn P (2010) Pancreatic acinar cell: new insight into the control of secreation. Int J Biochem Cell Biol 42:1586–1589Google Scholar
  54. Lu X, Ginsburg KS, Kettlewell S, Bossuyt J, Smith GL, Bers DM (2013) Measuring local gradients of intramitochondrial [Ca(2+)] in cardiac myocytes during sarcoplasmic reticulum Ca(2+) release. Circ Res 112:424–431Google Scholar
  55. Magnus G, Keizer J (1997) Minimal model of beta -cell mitochondria Ca2+ handeling. Am J Physiol Cell 42:C717–C733Google Scholar
  56. Magnus G, Keizer J (1998a) Model of beta-cell mitochondrial calcium handeling and electrical activity:I cytoplasmic variables. Am J Physiol Cell 43:C1158–C1173Google Scholar
  57. Magnus G, Keizer J (1998b) Model of beta-cell mitochondrial calcium handeling and electrical activity:II mitochondrial variables. Am J Physiol Cell 43:C1174–C1184Google Scholar
  58. Marhl M, Schuster S, Brumen M (1997a) Mitochondria as an important factor in the maintenance of constant amplitudes of cyosolic calcium oscillations. Biophys Chem 71:125–132Google Scholar
  59. Marhl M, Schuster S, Brumen M, Heinrich R (1997b) Modelling the interrelations between calcium oscillations and ER membrane potential oscillations. Biophys Chem 63:221–299Google Scholar
  60. Marhl M, Haberichter T, Brumen M, Heinrich R (2000) Complex calcium oscillations and the role of mitochondria and cytosolic proteins. Biosystems 57:75–86Google Scholar
  61. Matveer V, Bertram R, Sherman A (2011) Calcium cooperativity of exocytosis as a measure of Ca2+ channel domain overlap. Brain Res 1398:126–138Google Scholar
  62. Mazel T, Raymond R, Raymond-Stintz M, Jett S, Wilson BS (2009) Stochastic modeling of calcium in 3D geometry. Biophys J 96:1691–1706Google Scholar
  63. McCoy MK, Cookson MR (2012) Mitochondrial quality control and dynamics in Parkinson’s disease. Antioxid Redox Signal 16:869–873Google Scholar
  64. Meyer T, Stryer (1988) Molecular model for receptor-stimulation calcium spiking. Proc Natl Acad Sci U S A 85:5051–5055Google Scholar
  65. Mignen O, Thompson JL, Yule DI, Shuttleworth TJ (2005) Agonist activation of arachidonate-regulated Ca2+ -selective (ARC) channels in murine parotid and pancreatic acinar cells. J Physiol 564:791–801Google Scholar
  66. Nalaskowski MM, Mayr GW (2004) The families of kinase removing the Ca2+ releasing second messenger Ins(1,4,5) P3. curr. Mol Med 4:277–290Google Scholar
  67. Nassar A, Simpson AW (2000) Elevation of mitochondrial calcium by ryanodine-sensitive calcium-induced calcium release. J Biol Chem 275:23661–23665Google Scholar
  68. Nathanson MH, Padfeild PJ, O’Sullivan AJ, Burgstahler AD, Jamieson JD (1992) Mechanism of Ca2+ waves in pancreatic acinar cell. Cell Calcium 267:18118–18121Google Scholar
  69. Nathanson MH, Fallon MB, Padfeild PJ, Maranto AR (1994) Localization of the type 3 inositol 1,4,5 trisphosphate receptor in the Ca2+ waves triger zone of pancreatic acinar cell. J Biol Chem 269:4693–4696Google Scholar
  70. Nicholls DG (1978) Calcium transport and porton electrochemical potential gradient in mitochondria from guinea-pig cerebral cortex and rat heart. Biochem J 170:511–522Google Scholar
  71. Oster AM, Thomas B, Terman D, Fall CP (2011) The low conductance mitochondrial permeability transition pore confers excitability and CICR wave propagation in a computational model. J Theor Biol 273:216–231Google Scholar
  72. Palk L, Sneyd J, Shuttleworth TJ, Yule DI, Crampin EJ (2010) A dynamic model of saliva secreation. J Theor Biol 266:625–640Google Scholar
  73. Pan S, Ryu SY, Sheu SS (2011) Distinctive characteristics and functions of multiple mitochondrial Ca2+ influx mechanisms. Sci China Life Sci 54:763–769Google Scholar
  74. Park MK, Ashby MC, Erdemli G, Petersen OH, Tepikin AV (2001) Perinuclear, perigranular and sub-plasmalemmal mitochondria have distinct functions in the regulation of cellular calcium transport. EMBO J 20:1863–1874Google Scholar
  75. Parkash J, Asotra K (2010) Calcium wave signaling in cancer cells. Life Sci 87:587–595Google Scholar
  76. Perc M, Marhl M (2004) Local dissipation and coupling properties of cellular oscillators: a case study on calcium oscillations. Bioelectrochemistry 62:1–10Google Scholar
  77. Petersen OH (2005) Ca2+ Signalling and Ca2+ activation ion channels in exocrine acinar cells. Cell Calcium 38:171–200Google Scholar
  78. Petersen OH (2009) Ca2+ signalling in pancreatic acinar cells: physiology and pathophysiology. Braz J Med Biol Res 42:9–16Google Scholar
  79. Petersen CC, Petersen OH (1991) Receptor-activated cytoplasmic Ca2+ spikes in communicating clusters of pancreatic acinar cells. FEBS 264:113–116Google Scholar
  80. Petersen OH, Tepikin AV (2008) Polarized calcium signaling in exocrine gland cells. Annu Rev Physiol 70:273–299Google Scholar
  81. Petersen OH, Wakui M, Osipchuk Y, Yule D, Gallacher DV (1990) Electrophysiology of pancreatic acinar cells. Methods Enzymol 192:301–308Google Scholar
  82. Politi A, Gaspers LD, Thomas AP, Hofer T (2006) Models of IP3 and Ca2+ oscillations: frequency encoding and identification of underlying feedbacks. Biophys J 90:3120–3133Google Scholar
  83. Romeo MM, Jones CRT (2003) The stability of traveling calcium pulses in a pancreatic acinar cell. Phys D 177:242–258Google Scholar
  84. Ryu SY, Beutner G, Dirksen RT, Kinnally KW, Sheu SS (2010) Mitochondrial ryanodine receptors and other mitochondrial Ca2+ permeable channels. FEBS Lett 584:1948–1955Google Scholar
  85. Simpson D, Kirk V, Sneyd J (2005) Complex oscillations and waves of calcium in pancreatic acinar cell. Phys D 200:303–324Google Scholar
  86. Sneyd J (1994) Calcium buffering and diffusion: on regulation of an outstanding problem. Biophys 67:4–5Google Scholar
  87. Sneyd J and Falcke M (2004) Models of the inositol trisphosphate receptor. Prog Biophys Mol Biol 1–39Google Scholar
  88. Sneyd J, LeBeau A, Yule D (2000) Traveling waves of calcium in pancreatic acinar cells: model construction and bifurcation analysis. Phys D 145:158–179Google Scholar
  89. Sneyd J and Dufour JF (2002) A dynamic model of the type-2 inositol trisphosphate receptor. Proc Natl Acad Sci U S A 99:2398-403Google Scholar
  90. Sneyd J, Atanasova KT, Bruce JI, Straub SV, Giovannucci DR, Yule DI (2003) A model of calcium waves in pancreatic and parotid acinar cells. Biophys J 85:1392–1405Google Scholar
  91. Sneyd J, Falcke M, Dufour JF, Fox C (2004) A comparison of three models of the inositol trisphosphate receptor. Prog Biophys Mol Biol 85:121–140Google Scholar
  92. Sneyd J, Atanasova KT, Reznikov V, Bai Y, Sanderson MJ, Yule DI (2006) A method for determining the dependence of calcium oscillations on inositol trisphosphate oscillations. PNAS 103:1675–1680Google Scholar
  93. Somogyi R, Stucki JW (1991) Hormone induced calcium oscillations in liver cells can be explained by a simple One pool model. J Biol Chem 266:11068–11077Google Scholar
  94. Soulsby MD, Wojcikiewicz RJ (2006) The type III inositol 1,4,5-trisphosphate receptor is phosphorylated by cAMP-dependent protein kinase at three sites. Biochim J 392:493–497Google Scholar
  95. Spat A, Szanda G, Csordas G, Hajnoczky G (2008) High- and low-calcium-dependent mechanisms of mitochondrial calcium signalling. Cell Calcium 44:51–63Google Scholar
  96. Straub SV, Giovannucci DR, Yule DI (2000) Calcium wave propogation in pancreatic acinar cell: functional interaction of inositol 1,4,5-trisphosphate receptors, ryanodine receptors, and mitochondria. J Gen Physiol 116:547–559Google Scholar
  97. Strizhak P, Magura IS, YatsimirshII KB, Masyuk AI (1995) Return map approach to description of the deterministic chaos in cytosolic calcium oscillation. J Biol Phys 21:233–239Google Scholar
  98. Szanda G, Rajki A, Spat A (2012) Control mechanisms of mitochondrial Ca(2+) uptake - feed-forward modulation of aldosterone secretion. Mol Cell Endocrinol 353:101–108Google Scholar
  99. Tanimura A (2009) Mechanism of calcium waves and oscillations in non-excitable cells. Int J Oral-Med Sci 8:1–11Google Scholar
  100. Tepikin AV, Petersen OH (1992) Mechanisms of cellular calcium oscillations in secretory cells. Biochim Biophys Acta 1137:197–207Google Scholar
  101. Thorn P (1993) Spatial aspects of Ca2+ signalling in pancreatic acinar cell. Jexp Biol 184:129–144Google Scholar
  102. Thorn P (1996) Spatial domains of Ca2+ signalling in secretory epithelial cells. Cell Calcium 20:203–214Google Scholar
  103. Thorn P, Lawrie AM, Smith PM, Gallacher DV, Petersen OH (1993) Local and global cytosolic Ca2+ oscillations in exocrine cells evoked by agonist and inositol trisphosphate. Cell 74:661–668Google Scholar
  104. Tinel H, Cancela JM, Mogami H, Gerasimenko JV, Gerasimenko OV, Tepikin AV et al (1999) Active mitochondria surrounding the pancreatic acinar granule region prevent spreading of inositol trisphosphate-evoked local cytosolic Ca2+ signals. EMBOJ 18:4999–5008Google Scholar
  105. Trenker M, Malli R, Fertschai I (2007) Uncoupling protiens 2 and 3 are fundamental for mitochondrial Ca2+ uniporter. Nat Cell Biol 9:445–452Google Scholar
  106. Tsunoda Y (1991) Oscillatory Ca2+ signalling and its cellular function. New Biol 3:3–17Google Scholar
  107. Uchi JO, Pan S, Sheu SS (2012) Perspectives on: SGP symposium on mitochondrial physiology and medicine: molecular identities of mitochondrial Ca2+ influx mechanism: updated passwords for accessing mitochondrial Ca2+−linked health and disease. J Gen Physiol 139:435–443Google Scholar
  108. Ventura AC and Sneyd J (2006) Calcium Oscillations and Waves Generated by Multiple Release Mechanisms in Pancreatic Acinar Cells. Bull Math Biol 68:2205–2231Google Scholar
  109. Wagner J, Keizer J (1994) Effects of rapid buffers on Ca2+ diffusion and Ca2+ oscillations. Biophys J 67:447–456Google Scholar
  110. Williams JA and Yule DI (2012) Stimulus-secretion coupling in pancreatic acinar cells 1361–98Google Scholar
  111. Wojcikiewicz RJH (1995) Type I, II, III inositol 1,4,5-trisphosphate receptors are unequally susceptible to down-regulation and are expressed in markedly different proportions in different cell type. J Biol Chem 270:11678–11683Google Scholar
  112. Wojcikiewicz RJH, Luo SG (1997) Differences among type I, II, and III inositole-1,4,5 trisphosphate receptors in ligand- binding affinity influence the sensitivity of calcium stores to inositol-1,4,5 trisphosphate. Mol Pharmacol 53:656–662Google Scholar
  113. Woodring PJ, Garrison JC (1997) Expression, purification, and regulation of two isoforms of the inositol 1,4,5 trisphosphate 3-kinase. J Bio Chem 272:30447–30454Google Scholar
  114. Young GWD, Keizer J (1992) A single-pool inositol 1,4,5-trisphosphate-receptor-based model for agonist-stimulated oscillations in Ca2+ concentration. Proc Natl Acad Sci U S A 89:9895–9899Google Scholar
  115. Yule DI, Gallacher DV (1988) Oscillations of cytosolic calcium in single pancreatic acinar cells stimulated by acetylcholine. FEBS 239:358–362Google Scholar
  116. Yule DI, Lawrie AM, Gallacher DV (1991) Acetylcholine and Cholecystokinin induce different patterns of oscillationg calcium signals in pancreatic acinar cell. Cell Calcium 12:145–151Google Scholar
  117. Yule DI, Stuenkel E, Williams JA (1996) Intracellular calcium waves in rat pancreatic acini:mechanism of transmission. Am J Physiol 271:C1285–C1294Google Scholar
  118. Yule DI, Ernst SA, Ohnishi H, Wojcikiewicz RJ (1997) Evidence that zymogen granules are not a physiologically relevent calcium pool; defining the distribution of inositol 1,4,5-trisphosphate receptors in pancreatic acinar cells. J Biol Chem 272:9093–9098Google Scholar

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Authors and Affiliations

  1. 1.Department of Applied MathematicsMaulana Azad National Institute of TechnologyBhopalIndia

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