Both RyRs and TPCs are required for NAADP-induced intracellular Ca2+ release

Cell Calcium

Volumn 58, Issue 3, 2015, Pages 237-245

  Gerasimenko, Julia V ^a   Charlesworth, Richard M ^a   Sherwood, Mark W ^b   Ferdek, Pawel E ^a   Mikoshiba, Katsuhiko ^b,c   Parrington, John ^d   Petersen, Ole H ^a   Gerasimenko, Oleg V ^a  

^a CARDIFF UNIVERSITY   (United Kingdom)

^b RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^d UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Acidic store; CADPR; Pancreatic acinar cells; RyR3 knockouts; TPC2 knockouts

Indexed keywords

MEMBRANE PROTEIN; NICOTINIC ACID ADENINE DINUCLEOTIDE PHOSPHATE; RYANODINE RECEPTOR 2; RYANODINE RECEPTOR 3; TWO PORE CHANNEL; UNCLASSIFIED DRUG; CALCIUM; CALCIUM CHANNEL; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; RYANODINE RECEPTOR; TPCN1 PROTEIN, MOUSE; TPCN2 PROTEIN, MOUSE;

ACINAR CELL; ADULT; ANIMAL CELL; ANIMAL TISSUE; ANTIBODY DETECTION; ARTICLE; CALCIUM TRANSPORT; CELL ISOLATION; CELL MEMBRANE PERMEABILITY; CELL ORGANELLE; CONTROLLED STUDY; ENDOSOME; FEMALE; GRANULE CELL; LYSOSOME; MALE; MEMBRANE PERMEABILITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; ANALOGS AND DERIVATIVES; ANIMAL; CALCIUM SIGNALING; ENDOPLASMIC RETICULUM; EXOCRINE PANCREAS; KNOCKOUT MOUSE; METABOLISM; PHYSIOLOGY; ULTRASTRUCTURE;

ACINAR CELLS; ANIMALS; CALCIUM; CALCIUM CHANNELS; CALCIUM SIGNALING; ENDOPLASMIC RETICULUM; ENDOSOMES; LYSOSOMES; MICE; MICE, KNOCKOUT; NADP; PANCREAS, EXOCRINE; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL;

EID: 84938751053     PISSN: 01434160     EISSN: 15321991     Source Type: Journal    
DOI: 10.1016/j.ceca.2015.05.005     Document Type: Article

References (46)

1. Selinger Z., Naim E., Lasser M. ATP-dependent calcium uptake by microsomal preparations from rat parotid and submaxillary glands. Biochim. Biophys. Acta 1970, 2013:326-334.
2. Nielsen S.P., Petersen O.H. Transport of calcium in the perfused submandibular gland of the cat. J. Physiol. 1972, 223:685-697.
3. 2+ from a non-mitochondrial intracellular store in pancreatic acinar cells by inositol-1,4,5-trisphosphate. Nature 1983, 306:67-69.
4. 2+ oscillations in exocrine cells evoked by agonists and inositol trisphosphate. Cell 1993, 74:661-668.
5. 2+ waves and oscillations in exocrine pancreas. Cell 1993, 74:669-677.
6. 2+] waves. J. Biol. Chem. 1997, 272:15765-15770.
7. 2+ entry through basal membrane patch. Cell 1997, 88:49-55.
8. Streb H., Bayerdorffer E., Haase W., Irvine R.F., Schulz I. Effect of inositol-1,4,5-trisphosphate on isolated subcellular fractions of rat pancreas. J. Membr. Biol. 1984, 81:241-253.
9. 2+ wave trigger zone of pancreatic acinar cells. J. Biol. Chem. 1994, 269:4693-4696.
10. Yule D.I., Ernst S.A., Ohnishi H., Wojcikiewicz R.J. Evidence that zymogen granules are not a physiologically relevant calcium pool. Defining the distribution of inositol 1,4,5-trisphosphate receptors in pancreatic acinar cells. J. Biol. Chem. 1997, 272:9093-9098.
11. 2+ pools. Cell Calcium 1989, 10:325-336.
12. 2+ release from bovine adrenal medullary secretory vesicles. J. Biol. Chem. 1990, 265:13446-13448.
13. 2+ from single isolated pancreatic zymogen granules. Cell 1996, 84:473-480.
14. 2+. Nature 1998, 395:908-912.
15. Gerasimenko J.V., Tepikin A.V., Petersen O.H., Gerasimenko O.V. Calcium uptake via endocytosis with rapid release from acidifying endosomes. Curr. Biol. 1998, 8:1335-1338.
16. 2+ signals in pancreatic acinar and beta cells. J. Biol. Chem. 2004, 279:7234-7240.
17. 2+ spiking in mouse pancreatic acinar cells. Curr. Biol. 2005, 15:874-878.
18. Petersen O.H., Tepikin A.V. Polarized calcium signalling in exocrine gland cells. Annu. Rev. Physiol. 2008, 70:273-299.
19. 2+ movements and equilibration. EMBO J. 2000, 19:5729-5739.
20. 2+ signalling through acidic calcium stores in pancreatic acinar cells. Cell Calcium 2011, 50:193-199.
21. 2+ in the pathophysiology of pancreatitis. J. Physiol. 2014, 592:269-280.
22. 2+ from the endoplasmic reticulum and an acidic store in the secretory granule area. J. Cell Sci. 2006, 119:226-238.
23. 3. EMBO J. 2000, 19:2549-2557.
24. 2+ signal generation and acute pancreatitis. Cell Calcium 2009, 45:634-642.
25. Guse A.H. Linking NAADP to ion channel activity: a unifying hypothesis. Sci. Signal 2012, 5(221):pe18.
26. Calcraft P.J., Ruas M., Pan Z., Cheng X.T., Arredouani A., Hao X.M., Tang J.S., Rietdorf K., Teboul L., Chuang K.T., Lin P.H., Xiao R., Wang C.B., Zhu Y.M., Lin Y.K., Watt C.N., Parrington J., Ma J.J., Evans A.M., Galione A., Zhu M.X. NAADP mobilizes calcium from acidic organelles through two-pore channels. Nature 2009, 459:596-600.
27. Brailoiu E., Churamani D., Cai X.J., Schrlau M.G., Brailoiu G.C., Gao X., Hooper R., Boulware M.J., Dun N.J., Marchant J.S., Patel S. Essential requirement for two-pore channel 1 in NAADP-mediated calcium signaling. J. Cell Biol. 2009, 186:201-209.
28. Sherwood M., Prior I.A., Voronina S.G., Barrow S.L., Woodsmith J.D., Gerasimenko O.V., Petersen O.H., Tepikin A.V. Activation of trypsinogen in large endocytic vacuoles of pancreatic acinar cells. PNAS 2007, 104:5674-5679.
29. Wang X., Zhang X., Dong X.P., Samie M., Li X., Cheng X., Goschka A., Shen D., Zhou Y., Harlow J., Zhu M.X., Clapham D.E., Ren D., Xu H. TPC proteins are phosphoinositide-activated sodium-selective ion channels in endosomes and lysosomes. Cell 2012, 151:372-383.
30. + channels to adapt to metabolic state. Cell 2013, 152:778-790.
31. Galione A., Petersen O.H. The NAADP receptor: new receptors or new regulation?. Mol. Interv. 2005, 5:73-79.
32. Naylor E., Arredouani A., Vasudevan S.R., Lewis A.M., Parkesh R., Mizote A., Rosen D., Thomas J.M., Izumi M., Ganesan A., Galione A., Churchill G.C. Identification of a chemical probe for NAADP by virtual screening. Nat. Chem. Biol. 2009, 5:220-226.
33. Rosen D., Lewis A.M., Mizote A., Thomas J.M., Aley P.K., Vasudevan S.R., Parkesh R., Galione A., Izumi M., Ganesan A., Churchill G.C. Analogues of the nicotinic acid adenine dinucleotide phosphate (NAADP) antagonist Ned-19 indicate two binding sites on the NAADP receptor. J. Biol. Chem. 2009, 284:34930-34934.
34. 2 and multiple protein kinases. EMBO J. 2014, 33:501-511.
35. Singaravelu K., Deitmer J.W. Calcium mobilization by nicotinic acid adenine dinucleotide phosphate (NAADP) in rat astrocytes. Cell Calcium 2006, 39:143-153.
36. Billington R.A., Genazzani A.A. PPADS is a reversible competitive antagonist of the NAADP receptor. Cell Calcium 2007, 41:505-511.
37. Lambrecht G., Friebe T., Grimm U., Windscheif U., Bungardt E., Hildebrandt C., Bäumert H.G., Spatz-Kümbel G., Mutschler E. PPADS, a novel functionally selective antagonist of P2 purinoceptor-mediated responses. Eur. J. Pharm. 1992, 217:217-219.
38. Ziganshin A.U., Hoyle C.H.V., Bo X., Lambrecht G., Mutschler E., Baumert H.G., Burnstock G. PPADS selectively antagonizes P2x-purinoceptor-mediated responses in the rabbit urinary bladder. Br. J. Pharmacol. 1993, 110:1491-1495.
39. Vigne P., Pacaud P., Urbach V., Feolde E., Breittmayer J.P., Frelin C. The effect of PPADS as an antagonist of inositol (1,4,5) trisphosphate induced intracellular calcium mobilization. Br. J. Pharmacol. 1996, 119:360-364.
40. 2+ release. Cell 1990, 63:1025-1032.
41. 2+ signalling: from sea urchin eggs to mammalian cells. Cell Calcium 2014, pii:S0143-4160(14)00155-9.
42. Yan Z., Bai X., Yan C., Wu J., Li Z., Xie T., Peng W., Yin C., Li X., Scheres S.H.W., Shi Y., Yan N. Structure of the rabbit RyR1 at near-atomic resolution. Nature 2015, 517:50-55.
43. Zalk R., Clarke O.B., des Georges A., Grasucci R.A., Reiken S., Mancia F., Hendrickson W.H., Frank J., Marks A.R. Structure of the mammalian ryanodine receptor. Nature 2015, 517:44-49.
44. 2+ signaling in T-lymphocytes. J. Biol. Chem. 2005, 280:21394-21399.
45. 2+ signaling via type 1 ryanodine receptor in T cells revealed by a synthetic NAADP antagonist. PNAS 2009, 106:10678-10683.
46. Futatsugi A., Kato K., Ogura H., Li S.T., Nagata E., Kuwajima G., Tanaka K., Itohara S., Mikoshiba K. Facilitation of NMDAR-independent LTP and spatial learning in mutant mice lacking ryanodine receptor type 3. Neuron 1999, 24:701-713.