Extracellular ATP and zinc are co-secreted with insulin and activate multiple P2X purinergic receptor channels expressed by islet beta-cells to potentiate insulin secretion

Purinergic Signalling

Volumn 4, Issue 4, 2008, Pages 393-405

  Richards Williams, Clintoria ^a   Contreras, Juan L ^b   Berecek, Kathleen H ^a   Schwiebert, Erik M ^a,c  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b Kentucky   (United States)

^c Innovation Depot   (United States)

Author keywords

cells; ATP; Insulinsecretion; Islets; P2X receptor channels; Zinc

Indexed keywords

EID: 56549115233     PISSN: 15739538     EISSN: 15739546     Source Type: Journal    
DOI: 10.1007/s11302-008-9126-y     Document Type: Article

References (60)

1. Foster DW, McGarry JD (2000) Glucose, lipid and protein metabolism. Griffin JE, Ojeda SR (eds) Textbook of endocrine physiology, 4th edn. Oxford University Press, New York, pp 393-420
2. Straub SG, Sharp GW (2002) Glucose-stimulated signaling pathways in biphasic insulin secretion. Diabetes Metab Res Rev 18:451-463
3. Straub SG, Sharp GW (2004) Hypothesis: One rate-limiting step controls the magnitude of both phases of glucose-stimulated insulin secretion. Am J Physiol Cell Physiol 287:C565-C571
4. Newgard CB, McGarry JD (1995) Metabolic coupling factors in pancreatic beta-cell signal transduction. Annu Rev Biochem 64:689-719
5. Bryan J, Crane A, Vila-Carriles WH, Babenko AP, Aguilar-Bryan L (2005) Insulin secretagogues, sulfonylurea receptors, and K(ATP) channels. Curr Pharm Des 11(21):2699-2676
6. Aponte G, Gross D, Yamada T (1985) Capillary orientation of rat pancreatic D-cell processes: Evidence for endocrine release of somatostatin. Am J Physiol 249:G599-G606
7. Ballian N, Brunicardi FC (2007) Islet vasculature as a regulator of endocrine pancreas function. World J Surg 31:705-714
8. Bertrand G, Chapal J, Loubatieres-Mariani MM, Roye M (1987) Evidence for two different P2-purinoceptors on beta cell and pancreatic vascular bed. Br J Pharmacol 91:783-787
9. Bratanova-Tochkova TK, Cheng H, Daniel S, Gunawardana S, Liu YJ, Mulvaney-Musa J, Schermerhorn T, Straub SG, Yajima H, Sharp GW (2002) Triggering and augmentation mechanisms, granule pools, and biphasic insulin secretion. Diabetes 51(Suppl 1):S83-S90
10. Chimienti F, Devergnas S, Favier A, Seve M (2004) Identification and cloning of a beta-cell-specific zinc transporter, ZnT-8, localized into insulin secretory granules. Diabetes 53:2330-2337
11. Chimienti F, Devergnas S, Pattou F, Schuit F, Garcia-Cuenca R, Vandewalle B, Kerr-Conte J, Van LL, Grunwald D, Favier A, Seve M (2006) In vivo expression and functional characterization of the zinc transporter ZnT8 in glucose-induced insulin secretion. J Cell Sci 119:4199-4206
12. Chimienti F, Favier A, Seve M (2005) ZnT-8, a pancreatic beta-cell-specific zinc transporter. Biometals 18:313-317
13. Zalewski PD, Millard SH, Forbes IJ, Kapaniris O, Slavotinek A, Betts WH, Ward AD, Lincoln SF, Mahadevan I (1994) Video image analysis of labile zinc in viable pancreatic islet cells using a specific fluorescent probe for zinc. J Histochem Cytochem 42:877-884
14. Hazama A, Hayashi S, Okada Y (1998) Cell surface measurements of ATP release from single pancreatic beta cells using a novel biosensor technique. Pflugers Arch 437:31-35
15. Obermuller S, Lindqvist A, Karanauskaite J, Galvanovskis J, Rorsman P, Barg S (2005) Selective nucleotide-release from dense-core granules in insulin-secreting cells. J Cell Sci 118:4271-4282
16. Hellman B, Dansk H, Grapengiesser E (2004) Pancreatic beta-cells communicate via intermittent release of ATP. Am J Physiol Endocrinol Metab 286:E759-E765
17. Leitner JW, Sussman KE, Vatter AE, Schneider FH (1975) Adenine nucleotides in the secretory granule fraction of rat islets. Endocrinology 96:662-677
18. Grapengiesser E, Dansk H, Hellman B (2004) Pulses of external ATP aid to the synchronization of pancreatic beta-cells by generating premature Ca(2+) oscillations. Biochem Pharmacol 68:667-674
19. Leitner JW, Sussman KE, Vatter AE, Schneider FH (1975) Adenine nucleotides in the secretory granule fraction of rat islets. Endocrinology 96:662-677
20. Qian WJ, Gee KR, Kennedy RT (2003) Imaging of Zn2+ release from pancreatic beta-cells at the level of single exocytotic events. Anal Chem 75:3468-3475
21. Qian WJ, Peters JL, Dahlgren GM, Gee KR, Kennedy RT (2004) Simultaneous monitoring of Zn2+ secretion and intracellular Ca2+ from islets and islet cells by fluorescence microscopy. Biotechniques 37:922-930
22. Schwiebert EM, Zsembery A (2003) Extracellular ATP as a signaling molecule for epithelial cells. Biochim Biophys Acta 1615:7-32
23. Schwiebert EM, Liang L, Cheng NL, Olteanu D, Richards-Williams C, Welty EA, Zsembery A (2005) Extracellular ATP- and zinc-gated P2X receptor calcium entry channels: Physiological sensors and therapeutic targets. Purinergic Signal 1(4):299-310
24. Novak I (2007) Purinergic receptors in the endocrine and exocrine pancreas. Purinergic Signal. doi: 10.1007/s11302-007-9087-6
25. Burnstock G (2007) Purine and pyrimidine receptors. Cell Mol Life Sci 64:1471-1483
26. North RA (2002) Molecular physiology of P2X receptors. Physiol Rev 82:1013-1067
27. Ralevic V, Burnstock G (1998) Receptors for purines and pyrimidines. Pharmacol Rev 50:413-492
28. Roberts JA, Vial C, Digby HR, Agboh KC, Wen H, Catterbury-Thomas A, Evans RJ (2006) Molecular properties of P2X receptors. Pflugers Arch 452:486-500
29. Khakh BS, North RA (2006) P2X receptors as cell-surface ATP sensors in health and disease. Nature 442:527-532
30. Novak I, Hede SE, Hansen MR (2008) Adenosine receptors in rat and human pancreatic ducts stimulate chloride transport. Pflugers Arch 456:437-447
31. Tuduri E, Filiputti E, Carneiro E, Quesada I (2008) Inhibition of Ca2+ signaling and glucagon secretion in mouse pancreatic {alpha}-cells by extracellular ATP and purinergic receptors. Am J Physiol Endocrinol Metab. doi: 10.1152/ajpendo.00641.2007
32. Bertrand G, Chapal J, Loubatieres-Mariani MM, Roye M (1987) Evidence for two different P2-purinoceptors on beta cell and pancreatic vascular bed. Br J Pharmacol 91:783-787
33. Verspohl EJ, Johannwille B, Waheed A, Neye H (2002) Effect of purinergic agonists and antagonists on insulin secretion from INS-1 cells (insulinoma cell line) and rat pancreatic islets. Can J Physiol Pharmacol 80:562-568
34. Petit P, Hillaire-Buys D, Manteghetti M, Debrus S, Chapal J, Loubatieres-Mariani MM (1998) Evidence for two different types of P2 receptors stimulating insulin secretion from pancreatic B cell. Br J Pharmacol 125:1368-1374
35. Petit P, Manteghetti M, Puech R, Loubatieres-Mariani MM (1987) ATP and phosphate-modified adenine nucleotide analogues. Effects on insulin secretion and calcium uptake. Biochem Pharmacol 36:377-380
36. Chapal J, Loubatieres-Mariani MM, Roye M (1981) Effect of adenosine and phosphated derivatives on insulin release from the newborn dog pancreas. J Physiol (Paris) 77:873-875
37. Fernandez-Alvarez L, Hillaire-Buys D, Loubatieres-Mariani MM, Gomis R, Petit P (2001) P2 receptor agonists stimulate insulin release from human pancreatic islets. Pancreas 22:69-71
38. Farret A, Vignaud M, Dietz S, Vignon J, Petit P, Gross R (2004) P2Y purinergic potentiation of glucose-induced insulin secretion and pancreatic beta-cell metabolism. Diabetes 53(Suppl 3):S63-S66
39. Coutinho-Silva R, Parsons M, Robson T, Burnstock G (2001) Changes in expression of P2 receptors in rat and mouse pancreas during development and ageing. Cell Tissue Res 306:373-383
40. Coutinho-Silva R, Parsons M, Robson T, Lincoln J, Burnstock G (2003) P2X and P2Y purinoceptor expression in pancreas from streptozotocin-diabetic rats. Mol Cell Endocrinol 204:141-154
41. Liang L, Schwiebert EM (2005) Large pore formation uniquely associated with P2X7 purinergic receptor channels. Am J Physiol Cell Physiol 288(2):C240-C242
42. Coddou C, Morales B, Huidobro-Toro JP (2003) Neuromodulator role of zinc and copper during prolonged ATP applications to P2X4 purinoceptors. Eur J Pharmacol 472:49-56
43. Cuna-Castillo C, Morales B, Huidobro-Toro JP (2000) Zinc and copper modulate differentially the P2X4 receptor. J Neurochem 74:1529-1537
44. Xiong K, Peoples RW, Montgomery JP, Chiang Y, Stewart RR, Weight FF, Li C (1999) Differential modulation by copper and zinc of P2X2 and P2X4 receptor function. J Neurophysiol 81:2088-2094
45. Hohmeier HE, Mulder H, Chen G, Henkel-Rieger R, Prentki M, Newgard CB (2000) Isolation of INS-1-derived cell lines with robust ATP-sensitive K+ channel-dependent and -independent glucose-stimulated insulin secretion. Diabetes 49:424-430
46. D'Ambra R, Surana M, Efrat S, Starr RG, Fleischer N (1990) Regulation of insulin secretion from beta-cell lines derived from transgenic mice insulinomas resembles that of normal beta-cells. Endocrinology 126:2815-2822
47. Eckhoff DE, Eckstein C, Smyth CA, Vilatoba M, Bilbao G, Rahemtulla FG, Young CJ, Thompson J, Chaudry IH, Contreras JL (2004) Enhanced isolated pancreatic islet recovery and functionality in rats by 17beta-estradiol treatment of brain death donors. Surgery 136:336-345
48. Taylor AL, Kudlow BA, Marrs KL, Gruenert DC, Guggino WB, Schwiebert EM (1998) Bioluminescence detection of ATP release mechanisms in epithelia. Am J Physiol 275:C1391-C1406
49. Taylor AL, Schwiebert LM, Smith JJ, King C, Jones JR, Sorscher EJ, Schwiebert EM (1999) Epithelial P2X purinergic receptor channel expression and function. J Clin Invest 104:875-884
50. Liang L, Zsembery A, Schwiebert EM (2005) RNA interference targeted to multiple P2X receptor subtypes attenuates zinc-induced calcium entry. Am J Physiol Cell Physiol 289:C388-C396
51. Schwiebert EM, Wallace DP, Braunstein GM, King SR, Peti-Peterdi J, Hanaoka K, Guggino WB, Guay-Woodford LM, Bell PD, Sullivan LP, Grantham JJ, Taylor AL (2002) Autocrine extracellular purinergic signaling in epithelial cells derived from polycystic kidneys. Am J Physiol Renal Physiol 282:F763-F775
52. Schwiebert LM, Rice WC, Kudlow BA, Taylor AL, Schwiebert EM (2002) Extracellular ATP signaling and P2X nucleotide receptors in monolayers of primary human vascular endothelial cells. Am J Physiol Cell Physiol 282:C289-C301
53. Burnstock G (2007) Physiology and pathophysiology of purinergic neurotransmission. Physiol Rev 87(2):659-797
54. da Silva RL, Resende RR, Ulrich H (2007) Alternative splicing of P2X6 receptors in developing mouse brain and during in vitro neuronal differentiation. Exp Physiol 92:139-145
55. Dhulipala PD, Wang YX, Kotlikoff MI (1998) The human P2X4 receptor gene is alternatively spliced. Gene 207:259-266
56. Le KT, Paquet M, Nouel D, Babinski K, Seguela P (1997) Primary structure and expression of a naturally truncated human P2X ATP receptor subunit from brain and immune system. FEBS Lett 418:195-199
57. Ohkubo T, Yamazaki J, Nakashima Y, Kitamura K (2000) Presence and possible role of the spliced isoform of the P2X1 receptor in rat vascular smooth muscle cells. Pflugers Arch 441:57-64
58. Simon J, Kidd EJ, Smith FM, Chessell IP, Murrell-Lagnado R, Humphrey PP, Barnard EA (1997) Localization and functional expression of splice variants of the P2X2 receptor. Mol Pharmacol 52:237-248
59. Worthington RA, Dutton JL, Poronnik P, Bennett MR, Barden JA (1999) Localisation of P2X receptors in human salivary gland epithelial cells and human embryonic kidney cells by sodium dodecyl sulfate-polyacrylamide gel electrophoresis/Western blotting and immunofluorescence. Electrophoresis 20:2065-2070
60. Stojilkovic SS, Tomic M, He ML, Yan Z, Koshimizu TA, Zemkova H (2005) Molecular dissection of purinergic P2X receptor channels. Ann NY Acad Sci 1048:116-130