Advertisement

Coordination of Calcium Signaling by cADPR and NAADP in Pancreatic Acinar Cells

  • Jose Manuel Cancela

Abstract

In mouse pancreatic acinar cells, the hormone cholecystokinin (CCK) and the neurotransmitter acetylcholine (ACh) are the most important secretagogues and both of them elicit specific Ca2+ signatures (Fig. 1) [1– 4]. At low physiological concentration, CCK evokes a mixture of short-lasting local Ca2+ spikes in the secretory pole of the cell and long-lasting global Ca2+ spikes, whereas ACh at low concentration elicits local Ca2+ spikes in the secretory pole of the cell. At higher concentrations, CCK and ACh evoke global Ca2+ transients. Despite intensive research, the mechanisms underlying the complex Ca2+ oscillations remain unclear. It has been shown that heparin, an IP3-receptor antagonist, blocked the Ca2+ response elicited by ACh and CCK [5– 6]. These pharmacological data suggested that the IP3 receptors are involved in the secretagogue-evoked Ca2+ spikes and a two-pool model has been proposed for both ACh and CCK. In this model IP3 induces primary Ca2+ release, which then releases Ca2+ from an IP3-insensitive pool by a Ca2+-induced Ca2+ release (CICR) process [1,5]. However, this two-pool model relies on IP3 generation by CCK and ACh, which is not supported by biochemical data on the entire pancreatic acinar cell population [7]. In contrast to ACh, a physiological concentration of CCK does not generate detectable IP3.

Keywords

Ryanodine Receptor Pancreatic Acinar Cell Inositol Trisphosphate Apical Pole Nicotinic Acid Adenine Dinucleotide Phosphate 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Petersen OH, Petersen CCH and Kasai H. 1994. Ca2+ and hormone action. Annu. Rev. Physiol., 56: 297–319.CrossRefPubMedGoogle Scholar
  2. 2.
    Petersen OH and Cancela JM. 1999. New Ca2+-releasing messengers: are they important in the nervous system? Trends Neurosci. 22: 488–494.CrossRefPubMedGoogle Scholar
  3. 3.
    Cancela JM, Gerasimenko OV, Gerasimenko JV, Tepikin AV and Petersen, O.H. 2000. Two different but converging messenger pathways to intracellular Ca2+ release: the roles of NAADP, cADPR and IP3. EMBO J. 19: 2549–2557.CrossRefPubMedGoogle Scholar
  4. 4.
    Petersen CH, Toescu EC and Petersen OH. 1991. Different patterns of receptor-activated cytoplasmic Ca2+ oscillations in single pancreatic acinar cells: dependence on receptor type, agonist concentration and intracellular Ca2+ buffering. EMBO J. 10: 527–533.PubMedGoogle Scholar
  5. 5.
    Wakui M, Osipchuk YV and Petersen OH. 1990. Receptor-activated cytoplasmic Ca2+ spiking mediated by inositol trisphosphate is due to Ca2+-induced Ca2+ release. Cell 63: 1025–1032.CrossRefPubMedGoogle Scholar
  6. 6.
    Thorn P and Petersen OH. 1993. Ca2+ oscillations in pancreatic acinar cells, evoked by the cholecystokinin analogue JMV-180, depend on functional inositol 1,4,5-trisphosphate receptors. J. Biol. Chem. 268: 23219–23221.PubMedGoogle Scholar
  7. 7.
    Matozaki T, Goke B, Tsunoda Y, Rodriguez M, Martinez J and Williams J A. 1990. Two functionally distinct cholecystokinin receptors show different modes of action on Ca2+ mobilization and phospholipid hydrolysis in isolated rat pancreatic acini. Studies using a new cholecystokinin analog, JMV-180. J. Biol. Chem. 265: 6247–6254.PubMedGoogle Scholar
  8. 8.
    Xu X, Zeng W and Muallem S. 1996. Regulation of the inositol 1,4,5-trisphosphate-activated Ca2+ channel by activation of G-proteins. J. Biol. Chem. 271: 11737–11744.CrossRefPubMedGoogle Scholar
  9. 9.
    Muallem S and Wilkie TM. 1999. G protein-dependent Ca2+ signaling complexes in polarized cells. Cell Calcium. 26: 173–180.CrossRefPubMedGoogle Scholar
  10. 10.
    LeBeau AP, Yule DI, Groblewski GE and Sneyd J. 1999. Agonist-dependent phosphorylation of the inositol 1,4,5-trisphosphate receptor. J. Gen. Physiol. 113: 851–871.CrossRefPubMedGoogle Scholar
  11. 11.
    Thorn P, Gerasimenko O and Petersen OH. 1994. Cyclic ADP-ribose regulation of ryanodine receptors involved in agonist evoked cytosolic Ca2+ oscillations in pancreatic acinar cells. EMBO J. 13: 2038-2043.PubMedGoogle Scholar
  12. 12.
    Schulz I, Krause E, Gonzalez A, Gobel A, Sternfeld L and Schmid A. 1999. Agonist-stimulated pathways of Ca2+ signaling in pancreatic acinar cells. Biol. Chem. 380: 903-908.CrossRefPubMedGoogle Scholar
  13. 13.
    Galione A, Lee HC and Busa WB. 1991. Ca2+-induced Ca2+ release in sea urchin egg homogenates and its modulation by cyclic ADP-ribose. Science. 253: 1143-1146.CrossRefPubMedGoogle Scholar
  14. 14.
    Meszaros LG, Bak J and Chu A. 1993. Cyclic ADP-ribose as an endogeneous regulator of the non-skeletal type ryanodine receptor Ca2+ channel. Nature. 364: 76–79.CrossRefPubMedGoogle Scholar
  15. 15.
    Lee HC. 1997. Mechanisms of Ca2+ signalling by cyclic ADP-ribose and NAADP. Physiol. Rev. 11: 1133–1164.Google Scholar
  16. 16.
    Sonnleitner A, Conti A, Bertocchini F, Schindler H and Sorrentino V. 1998. Functional properties of the ryanodine receptor type 3 (RYR3) Ca2+ release channel.EMBO J. 17: 2790–2798.CrossRefPubMedGoogle Scholar
  17. 17.
    Lee HC.2000. NAADP: an emerging Ca2+ signaling molecule. J. Memb. Biol. 173: 1–8.CrossRefGoogle Scholar
  18. 18.
    Munshi C, Thiel DJ, Mathews II, Aarhus R, Walseth TF and Lee HC. 1999. Characterization of the active site of ADP-ribosyl cyclase. J. Biol. Chem. 274: 30770–30777.CrossRefPubMedGoogle Scholar
  19. 19.
    Hirata Y, Kimura N, Sato K, Ohsugi Y, Takasawa S, et al. 1994. ADP ribosyl cyclase activity of a novel bone marrow stromal cell surface molecule, BST-1. FEBS Lett. 356: 244–248.CrossRefPubMedGoogle Scholar
  20. 20.
    Guse AH. 1999. Cyclic ADP-ribose: A novel Ca2+-mobilising second messenger. Cell. Signal. 11:309–316.CrossRefPubMedGoogle Scholar
  21. 21.
    Lee HC. 2001. Physiological functions of cADP-ribose and NAADP as Ca2+ messengers. Annu. Rev. Pharmacol. Toxicol. 41: 317–345.CrossRefPubMedGoogle Scholar
  22. 22.
    Tinel H, Cancela JM, Mogami H, Gerasimenko JV, Gerasimenko OV, Tepikin AV and Petersen OH. 1999. Active mitochondria surrounding the pancreatic acinar granule region prevent spreading of inositol trisphosphate-evoked local cytosolic Ca2+ signals. EMBO J. 18. 4999–5008.CrossRefPubMedGoogle Scholar
  23. 23.
    Thorn P, Lawrie AM, Smith PM, Gallacher DV and Petersen OH. 1993. Local and global cytosolic Ca2+ oscillations in exocrine cells evoked by agonists and inositol trisphosphate. Cell 74: 661–668.CrossRefPubMedGoogle Scholar
  24. 24.
    Cancela JM. 2001. Specific Ca2+ signaling evoked by cholecystokinin and acetylcholine: the roles of NAADP, cADPR, and IP3. Annu. Rev. Physiol. 63, 99–117.CrossRefPubMedGoogle Scholar
  25. 25.
    Ziegler M, Jorcke D and Schweiger M. 1997. Identification of bovine liver mitochondrial NAD+ glycohydrolase as ADP-ribosyl cyclase. Biochem. J. 326: 401–405.PubMedGoogle Scholar
  26. 26.
    Adebanjo OA, Anandatheerthavarada HK, Koval AP, Moonga BS, Biswast G, et al. 1999. A new function for CD38/ADP-ribosyl cyclase in nuclear Ca2+ homeostasis. Nature Cell Biol. 1:409–414.CrossRefPubMedGoogle Scholar
  27. 27.
    Liang M, Chini ED, Cheng J and Dousa TP. 1999. Synthesis of NAADP and cADPr in mitochondria. Arch. Biochem. Biophys. 15: 317–325.CrossRefGoogle Scholar
  28. 28.
    Takasawa S, Nata S, Yonekura H and Okamoto H. 1993. Cyclic ADP-ribose in insulin secretion from pancreatic P cells. Science. 259: 370–373.CrossRefPubMedGoogle Scholar
  29. 29.
    Kuemmerle JF and Makhlouf GM. 1995. Agonist-stimulated cyclic ADP ribose. Endogenous modulator of Ca2+-induced Ca2+ release in intestinal longitudinal muscle. J. Biol. Chem. 270: 25488–25494.CrossRefPubMedGoogle Scholar
  30. 30.
    Cancela JM and Petersen OH. 1998. The cyclic ADP-ribose antagonist 8-NH2-CADP-ribose blocks cholecystokinin-evoked cytosolic Ca2+ spiking in pancreatic acinar cells. Pflugers Arch. 435: 746–48.CrossRefPubMedGoogle Scholar
  31. 31.
    Cancela JM, Mogami H, Tepikin AV and Petersen OH. 1998. Intracellular glucose switches between cyclic ADP-ribose and inositol trisphosphate triggering of cytosolic Ca2+ spiking. Curr. Biol. 8: 865–68.CrossRefPubMedGoogle Scholar
  32. 32.
    Walseth TF and Lee HC. 1993. Synthesis and characterization of antagonists of cyclic ADP-ribose. Biochim. Biophys. Acta. 1178: 235–242.CrossRefPubMedGoogle Scholar
  33. 33.
    Gilon P, Arredouani A, Gailly, P, Gromada J and Henquin JC. 1999. Uptake and release of Ca2+ by the endoplasmic reticulum contribute to the oscillations of the cytosolic Ca2+ concentration triggered by Ca2+ influx in the excitable pancreatic ß-cell. J. Biol. Chem. 274:20197–20205.CrossRefPubMedGoogle Scholar
  34. 34.
    Tengholm A, Hagman C, Gylfe E and Hellman B. 1998. In situ characterization of nonmitochondrial Ca2+ stores in individual pancreatic beta-cells. Diabetes 47: 1224–1230.CrossRefPubMedGoogle Scholar
  35. 35.
    Korc M, Wiliams J A and Goldfine ID. 1979. Stimulation of the glucose transport system in isolated mouse pancreatic acini by Cholecystokinin and analogues. J. Biol. Chem. 254: 7624–7629.PubMedGoogle Scholar
  36. 36.
    Chini EN and Dousa TP. 1999. Differential effect of glycolytic intermediaries upon cyclic ADP-ribose, inositol 1,4,5-trisphosphate-, and nicotinate adenine dinucleotide phosphate-induced Ca2+ release systems. Arch. Biochem. Biophys. 370: 294–299.CrossRefPubMedGoogle Scholar
  37. 37.
    Chini EN, Beers KW, Dousa TP. 1995. Nicotinate adenine dinucleotide phosphate (NAADP) triggers a specific Ca2+ release system in sea urchin eggs. J. Biol. Chem. 270: 3216–3223.CrossRefPubMedGoogle Scholar
  38. 38.
    Lee HC and Aarhus R. 1995. A derivative of NADP mobilizes Ca2+ stores insensitive to inositol trisphophate and cyclic ADP-ribose. J. Biol. Chem. 270: 2152–2157.CrossRefPubMedGoogle Scholar
  39. 39.
    Genazzani AA and Galione A. 1997. A Ca2+ release mechanism gated by the novel pyridine nucleotide, NAADP. Trends Pharmacol. Sci. 18: 108–110.CrossRefPubMedGoogle Scholar
  40. 40.
    Cancela JM, Churchill GC and Galione A. 1999. Coordination of agonist-induced Ca2+-signalling patterns by NAADP in pancreatic acinar cells. Nature 398: 74–76.CrossRefPubMedGoogle Scholar
  41. 41.
    Patel S, Churchill GC and Galione A. 2001. Coordination of Ca2+ signalling by NAADP. Trends Biol. Sci. 26, 482–489.CrossRefGoogle Scholar
  42. 42.
    Chini EN and Dousa TP. 1996. Nicotinate-adenine dinucleotide phosphate-induced Ca2+ release does not behave as a Ca2+-induced Ca2+ release system. Biochem. J. 316: 709–711.PubMedGoogle Scholar
  43. 43.
    Cancela JM, Coppenolle FV, Galione A, Tepikin AV and Petersen OH. 2002. Transformation of local Ca2+ spikes to global Ca2+ transients: the combinatorial roles of multiple Ca2+ releasing messengers. EMBO J 21:909–19.CrossRefPubMedGoogle Scholar
  44. 44.
    Burdakov D, Galione A. 2000. Two neuropeptides recruit different messenger pathways to evoke Ca2+ signals in the same cell. Curr Biol 10: 993–96.CrossRefPubMedGoogle Scholar
  45. 45.
    Fukushi Y, Kato I, Takasawa S, Sasaki T, Ong BH, Sato M, Ohsaga A., Sato K, Shirato K, Okamoto H, Maruyama Y. 2001. Identification of Cyclic ADP-ribose-dependent Mechanisms inPancreatic Muscarinic Ca 21 Signaling Using CD38 Knockout Mice. J. Biol. Chem. 276: 649–655.CrossRefPubMedGoogle Scholar
  46. 46.
    Ito K., Miyashita Y. and Kasai H. 1999. Kinetic control of multiple forms of Ca2+ spikes by inositol trisphosphate in pancreatic acinar cells. J. Cell Biol. 146: 405–413.CrossRefPubMedGoogle Scholar
  47. 47.
    Kasai H and Augustine GJ. 1990. Cytosolic Ca2+ gradients triggering unidirectional fluid secretion from exocrine pancreas. Nature. 348: 735–738.CrossRefPubMedGoogle Scholar
  48. 48.
    Maruyama Y and Petersen OH. 1994. Delay in granular fusion evoked by repetitive cytosolic Ca2+ spikes in mouse pancreatic acinar cells. Cell Calcium 16: 419–430.CrossRefPubMedGoogle Scholar
  49. 49.
    Park MK, Lomax RB, Tepikin AV and Petersen OH. 2001. Local uncaging of caged Ca2+ reveals distribution of Ca2+-activated Cl- channels in pancreatic acinar cells. Proc. Natl. Acad. Sci USA 98: 10948–10953.CrossRefPubMedGoogle Scholar
  50. 50.
    Boittin FX, Coussin F, Macrez N, Mironneau C and Mironneau J. 1998. Inositol 1,4,5-trisphosphate- and ryanodine-sensitive Ca2+ release channel-dependent Ca2+ signalling in rat portal vein myocytes. Cell Calcium 23: 303–311.CrossRefPubMedGoogle Scholar
  51. 51.
    Koizumi S, Bootman MD, Bobanovic LK, Schell MJ, Berridge MJ and Lipp P. 1999. Characteriztion of elementary Ca2+ release signals in NGF-differentiated PC12 cells and hippocampal neurons. Neuron 22: 125–37.CrossRefPubMedGoogle Scholar
  52. 52.
    Parker I, Choi J and Yao Y. 1996. Elementary events of InsP3-induced Ca2+ liberation in Xenopus oocytes: hot spots, puffs and blips. Cell Calcium 20: 105–121.CrossRefPubMedGoogle Scholar
  53. 53.
    Berridge MJ. 1997. Elementary and global aspects of calcium signalling. J. Physiol. 499: 291–306.PubMedGoogle Scholar
  54. 54.
    Cannell MB and Soeller C. 1999. Mechanisms underlying Ca2+ sparks in cardiac muscle. J. Gen. Physiol. 113: 373–376.CrossRefPubMedGoogle Scholar
  55. 55.
    Nathanson MH, Fallon MB, Padfield PJ and Maranto AR. 1994. Localization of the type 3 inositol 1,4,5-trisphosphate receptor in the Ca2+ wave trigger zone of pancreatic acinar cells. J. Biol. Chem. 269: 4693–4696.PubMedGoogle Scholar
  56. 56.
    Lee MG, Xu X, Zeng W, Diaz J, Wojcikiewicz JH, Kuo TH, Wuytack F, Racymaekers L and Muallem S. 1997. Polarized expression of Ca2+ channels in pancreatic and salivary gland cells. J. Biol. Chem. 272: 15765–15770.CrossRefPubMedGoogle Scholar
  57. 57.
    Kasai H and Petersen OH. 1994. Spatial dynamics of second messengers: IP3 and cAMP as long-range and associative messengers. Trends Neurosci. 17: 95–101.CrossRefPubMedGoogle Scholar
  58. 58.
    Leite MF, Dranoff J A, Gao L and Nathanson MH. 1999. Expression and subcellular localization of the ryanodine receptor in rat pancreatic acinar cells. Biochem. J. 337: 305–309.CrossRefPubMedGoogle Scholar
  59. 59.
    Fitzsimmons TJ, Gukovsky I, McRoberts JA, Rodriguez E, Lai FA and Pandol SJ. 2000 Multiple isoforms of the ryanodine receptor are expressed in rat pancreatic acinar cells. Biochem. J. 351:265–271.CrossRefPubMedGoogle Scholar
  60. 60.
    Straub SV, Giovannucci DR, Yule DI. 2000. Ca2+ wave propagation in pancreatic acinar cells: functional interaction of inositol 1,4,5-trisphosphate receptors, ryanodine receptors, and mitochondria. J. Gen. Physiol. 116: 547–559.CrossRefPubMedGoogle Scholar
  61. 61.
    Park MK, Ashby MC, Erdemli G, Petersen OH and Tepikin AV. 2001. Perinuclear, perigranular and sub-plasmalemmal mitochondria have distinct functions in the regulation of cellular Ca2+ transport. EMBO J. 20: 1863–1874.CrossRefPubMedGoogle Scholar
  62. 62.
    Toescu EC Lawrie AM, Petersen OH and Gallacher, DV. 1992. Spatial and temporal distribution of agonist-evoked cytoplasmic Ca2+ signals in exocrine acinar cells analysed by digital image microscopy. EMBO J. 11: 1623–1629.Google Scholar
  63. 63.
    Toescu EC, Gallacher DV and Petersen OH. 1994. Identical regional mechanisms of intracellular free Ca2+ concentration increase during polarized agonist-evoked Ca2+ response in pancreatic acinar cells. Biochem J. 304: 313–316.PubMedGoogle Scholar
  64. 64.
    Marchant J, Callamaras N and Parker I. 1999. Initiation of IP3-mediated Ca2+ waves in Xenopus oocytes. EMBO J. 18: 5285–5299.CrossRefPubMedGoogle Scholar
  65. 65.
    Berridge MJ, Lipp P and Bootman MD. 2000. The versality and universality of Ca2+ signaling. Nature Rev. 1: 11–21.CrossRefGoogle Scholar
  66. 66.
    Churchill GC and Galione A. 2000. Spatial control of Ca2+ signaling by nicotinic acid adenine dinucleotide phosphate diffusion and gradients. J. Biol. Chem. 275: 38687–38692.CrossRefPubMedGoogle Scholar
  67. 67.
    Churchill GC and Galione A. 2001. NAADP induces Ca2+ oscillations via a two-pool mechanism by priming IP3 and cADPR-sensitive Ca2+ stores. EMBO J. 20: 2666–2671.CrossRefPubMedGoogle Scholar
  68. 68.
    Malgaroli A, Fesce R and Meldolesi J. 1990. Spontaneous [Ca2+]i fluctuations in rat chromaffin cells do not require inositol 1,4,5-trisphosphate elevations but are generated by a caffeine- and ryanodine-sensitive intracellular Ca2+ store. J. Biol. Chem. 265: 3005–3008.PubMedGoogle Scholar
  69. 69.
    Golovina VA and Blaustein MP. 1997. Spatially and functionally distinct Ca2+ stores in sarcoplasmic and endoplasmic reticulum. Science. 275: 1643–1648.CrossRefPubMedGoogle Scholar
  70. 70.
    Hofer AM, Landolfi B, Debellis L, Pozzan, T and Curci S. 1998. Free [Ca2+] dynamics measured in agonist-sensitive stores of single living intact cells: A new look at the refilling process. EMBO J. 17: 1986–1995.CrossRefPubMedGoogle Scholar
  71. 71.
    Mogami H, Nakano K, Tepikin AV and Petersen,O.H. 1997. Ca2+ flow via tunnels in polarized cells: recharging of apical Ca2+ stores by focal Ca2+ entry through basal membrane patch. Cell 88: 49–55.CrossRefPubMedGoogle Scholar
  72. 72.
    Meldolesi J and Pozzan T. 1998. The heterogeneity of ER Ca2+ stores has a key role in non muscle cell signaling and function. J. Cell Biol. 142: 1395–1398.CrossRefPubMedGoogle Scholar
  73. 73.
    Park MK, Petersen OH and Tepikin AV. 2000. The endoplasmic reticulum as one continuous Ca2+ pool: visualization of rapid Ca2+ movement and equilibration. EMBO J. 19.5729–5739.CrossRefPubMedGoogle Scholar
  74. 74.
    Petersen OH, Tepikin AV and Park MK. 2001. The endoplasmic reticulum: one continuous or several separate Ca2+ stores. Trends Neurosci. 24: 271–76.CrossRefPubMedGoogle Scholar
  75. 75.
    Albrieux M, Lee HC and Villaz M. 1998. Ca2+ signaling by cyclic ADP-ribose, NAADP, and inositol trisphosphate are involved in distinct functions in ascidian oocytes. J. Biol. Chem. 273: 14566–14574.CrossRefPubMedGoogle Scholar
  76. 76.
    Guse AH, da Silva CP, Berg I, Skapenko AL, Weber K, et al. 1999. Regulation of Ca2+ signalling in T lymphocytes by the second messenger cyclic ADP-ribose. Nature. 398: 70–73CrossRefPubMedGoogle Scholar
  77. 77.
    Berg I, Potter BVL, Mayr GW and Guse AH. 2000. Nicotinic acid adenine dinuleotide phosphate (NAADP+) is an essential regulator of T-lymphocyte Ca2+ signaling. J. Cell Biol. 150:581–588.CrossRefPubMedGoogle Scholar
  78. 78.
    Santella L, Kyozuka K, Genazzani AA, De Riso L and Carafoli E. 2000. Nicotinic acid adenine dinucleotide phosphate-induced Ca2+ release. J. Biol. Chem. 275: 8301–8306.CrossRefPubMedGoogle Scholar
  79. 79.
    Galione A. 1994. Cyclic ADP-ribose, the ADP-ribosyl cyclase pathway and Ca2+ signalling. Mol. Cell. Endocrinol. 98: 125–131.CrossRefPubMedGoogle Scholar
  80. 80.
    Perez-Tersic CM, Chini EN, Shen SS, Dousa TP and Clapham DE. 1995. Ca2+ release triggered by nicotinate adenine dinucleotide phosphate in intact sea urchin eggs. Biochem. J. 312:955–959.Google Scholar

Copyright information

© Springer Science+Business Media New York 2002

Authors and Affiliations

  • Jose Manuel Cancela
    • 1
  1. 1.Affiliation Laboratoire de Neurobiologie Cellulaire et MoléculaireCNRSGif-sur-Yvette cédexFrance

Personalised recommendations