Intracellular and extracellular adenosine triphosphate in regulation of insulin secretion from pancreatic β cells

Journal of Diabetes

Volumn 6, Issue 2, 2014, Pages 113-119

  Wang, Chunjiong ^a   Geng, Bin ^b,c   Cui, Qinghua ^b,c   Guan, Youfei ^b,c   Yang, Jichun ^b,c  

^a TIANJIN MEDICAL UNIVERSITY   (China)

^b PEKING UNIVERSITY   (China)

^c PEKING UNIVERSITY HEALTH SCIENCE CENTER   (China)

Author keywords

Adenosine triphosphate; Insulin secretion; Mitochondria; Pancreatic cells

Indexed keywords

ADENOSINE TRIPHOSPHATE; MITOCHONDRIA; PANCREATIC Β CELLS;

ADENOSINE TRIPHOSPHATE; CALCIUM; CALCIUM CHANNELS, L-TYPE; EXTRACELLULAR SPACE; HUMANS; INSULIN; INSULIN-SECRETING CELLS; INTRACELLULAR SPACE; KATP CHANNELS; RECEPTORS, PURINERGIC P2;

EID: 84895070554     PISSN: 17530393     EISSN: 17530407     Source Type: Journal    
DOI: 10.1111/1753-0407.12098     Document Type: Review

References (61)

1. Abdul-Ghani MA, Muller FL, Liu Y etal. Deleterious action of FA metabolites on ATP synthesis: Possible link between lipotoxicity, mitochondrial dysfunction, and insulin resistance. Am J Physiol Endocrinol Metab. 2008; 295: E678-685.
2. Wu L, Nicholson W, Knobel SM etal. Oxidative stress is a mediator of glucose toxicity in insulin-secreting pancreatic islet cell lines. J Biol Chem. 2004; 279: 12126-12134.
3. Chen M, Yang Z, Wu R, Nadler JL. Lisofylline, a novel antiinflammatory agent, protects pancreatic beta-cells from proinflammatory cytokine damage by promoting mitochondrial metabolism. Endocrinology. 2002; 143: 2341-2348.
4. Chapal J, Bertrand G, Hillaire-Buys D, Gross R, Loubatieres-Mariani MM. Prior glucose deprivation increases the first phase of glucose-induced insulin response: Possible involvement of endogenous ATP and (or) ADP. Can J Physiol Pharmacol. 1993; 71: 611-614.
5. Nakamura S, Takamura T, Matsuzawa-Nagata N etal. Palmitate induces insulin resistance in H4IIEC3 hepatocytes through reactive oxygen species produced by mitochondria. J Biol Chem. 2009; 284: 14809-14818.
6. Remedi MS, Koster JC. K(ATP) channelopathies in the pancreas. Pflugers Arch. 2010; 460: 307-320.
7. Smith AJ, Taneja TK, Mankouri J, Sivaprasadarao A. Molecular cell biology of KATP channels: Implications for neonatal diabetes. Expert Rev Mol Med. 2007; 9: 1-17.
8. Stoy J, Steiner DF, Park SY, Ye H, Philipson LH, Bell GI. Clinical and molecular genetics of neonatal diabetes due to mutations in the insulin gene. Rev Endocr Metab Disord. 2010; 11: 205-215.
9. Edghill EL, Gloyn AL, Gillespie KM etal. Activating mutations in the KCNJ11 gene encoding the ATP-sensitive K+ channel subunit Kir6.2 are rare in clinically defined type 1 diabetes diagnosed before 2 years. Diabetes. 2004; 53: 2998-3001.
10. Li J, Shuai HY, Gylfe E, Tengholm A. Oscillations of sub-membrane ATP in glucose-stimulated beta cells depend on negative feedback from Ca(2+). Diabetologia. 2013; 56: 1577-1586.
11. Peyot ML, Pepin E, Lamontagne J etal. Beta-cell failure in diet-induced obese mice stratified according to body weight gain: Secretory dysfunction and altered islet lipid metabolism without steatosis or reduced beta-cell mass. Diabetes. 2010; 59: 2178-2187.
12. Zhang Y, Liu D. Flavonol kaempferol improves chronic hyperglycemia-impaired pancreatic beta-cell viability and insulin secretory function. Eur J Pharmacol. 2011; 670: 325-332.
13. Zhang CY, Parton LE, Ye CP etal. Genipin inhibits UCP2-mediated proton leak and acutely reverses obesity- and high glucose-induced beta cell dysfunction in isolated pancreatic islets. Cell Metab. 2006; 3: 417-427.
14. Doliba NM, Qin W, Najafi H etal. Glucokinase activation repairs defective bioenergetics of islets of langerhans isolated from type-2-diabetics. Am J Physiol Endocrinol Metab. 2012; 302: E87-102.
15. Soty M, Visa M, Soriano S, Carmona MD, Nadal A, Novials A. Involvement of katp channels in the loss of beta-cell function induced by human islet amyloid polypeptide. J Biol Chem. 2011; 286: 40857-40866.
16. Yang J, Wong RK, Wang X etal. Leucine culture reveals that ATP synthase functions as a fuel sensor in pancreatic beta-cells. J Biol Chem. 2004; 279: 53915-53923.
17. Yang J, Wong RK, Park M etal. Leucine regulation of glucokinase and ATP synthase sensitizes glucose-induced insulin secretion in pancreatic beta-cells. Diabetes. 2006; 55: 193-201.
18. Yang J, Chi Y, Burkhardt BR, Guan Y, Wolf BA. Leucine metabolism in regulation of insulin secretion from pancreatic beta cells. Nutr Rev. 2010; 68: 270-279.
19. Brennan L, Shine A, Hewage C etal. A nuclear magnetic resonance-based demonstration of substantial oxidative L-alanine metabolism and L-alanine-enhanced glucose metabolism in a clonal pancreatic beta-cell line: Metabolism of L-alanine is important to the regulation of insulin secretion. Diabetes. 2002; 51: 1714-1721.
20. Kyriazis GA, Soundarapandian MM, Tyrberg B. Sweet taste receptor signaling in beta cells mediates fructose-induced potentiation of glucose-stimulated insulin secretion. Proc Natl Acad Sci U S A. 2012; 109: E524-532.
21. Kang Y, Zhang Y, Liang T etal. ATP modulates interaction of syntaxin-1A with sulfonylurea receptor 1 to regulate pancreatic beta-cell KATP channels. J Biol Chem. 2011; 286: 5876-5883.
22. Pasyk EA, Kang Y, Huang X, Cui N, Sheu L, Gaisano HY. Syntaxin-1A binds the nucleotide-binding folds of sulphonylurea receptor 1 to regulate the KATP channel. J Biol Chem. 2004; 279: 4234-4240.
23. Lee JW, Kim WH, Lim JH etal. Mitochondrial dysfunction: Glucokinase downregulation lowers interaction of glucokinase with mitochondria, resulting in apoptosis of pancreatic beta-cells. Cell Signal. 2009; 21: 69-78.
24. Kim WH, Lee JW, Suh YH etal. Exposure to chronic high glucose induces beta-cell apoptosis through decreased interaction of glucokinase with mitochondria: Downregulation of glucokinase in pancreatic beta-cells. Diabetes. 2005; 54: 2602-2611.
25. Kim WH, Lee JW, Suh YH etal. AICAR potentiates ROS production induced by chronic high glucose: Roles of AMPK in pancreatic beta-cell apoptosis. Cell Signal. 2007; 19: 791-805.
26. Koshkin V, Wang X, Scherer PE, Chan CB, Wheeler MB. Mitochondrial functional state in clonal pancreatic beta-cells exposed to free fatty acids. J Biol Chem. 2003; 278: 19709-19715.
27. Rachek LI, Thornley NP, Grishko VI, LeDoux SP, Wilson GL. Protection of INS-1 cells from free fatty acid-induced apoptosis by targeting hOGG1 to mitochondria. Diabetes. 2006; 55: 1022-1028.
28. Joseph JW, Koshkin V, Saleh MC etal. Free fatty acid-induced beta-cell defects are dependent on uncoupling protein 2 expression. J Biol Chem. 2004; 279: 51049-51056.
29. Kebede M, Favaloro J, Gunton JE etal. Fructose-1, 6-bisphosphatase overexpression in pancreatic beta-cells results in reduced insulin secretion: A new mechanism for fat-induced impairment of beta-cell function. Diabetes. 2008; 57: 1887-1895.
30. Winzell MS, Svensson H, Enerback S etal. Pancreatic beta-cell lipotoxicity induced by overexpression of hormone-sensitive lipase. Diabetes. 2003; 52: 2057-2065.
31. Piro S, Rabuazzo AM, Renis M, Purrello F. Effects of Metformin on oxidative stress, adenine nucleotides balance and glucose-induced insulin release impaired by chronic FFA exposure in rat pancreatic islets. J Endocrinol Invest. 2012; 35: 504-510.
32. Kohnke R, Mei J, Park M, York DA, Erlanson-Albertsson C. Fatty acids and glucose in high concentration down-regulates ATP synthase beta-subunit protein expression in INS-1 cells. Nutr Neurosci. 2007; 10: 273-278.
33. Kiely A, McClenaghan NH, Flatt PR, Newsholme P. Pro-inflammatory cytokines increase glucose, alanine and triacylglycerol utilization but inhibit insulin secretion in a clonal pancreatic beta-cell line. J Endocrinol. 2007; 195: 113-123.
34. Collier JJ, Fueger PT, Hohmeier HE, Newgard CB. Pro- and antiapoptotic proteins regulate apoptosis but do not protect against cytokine-mediated cytotoxicity in rat islets and beta-cell lines. Diabetes. 2006; 55: 1398-1406.
35. Giannoukakis N, Rudert WA, Ghivizzani SC etal. Adenoviral gene transfer of the interleukin-1 receptor antagonist protein to human islets prevents IL-1beta-induced beta-cell impairment and activation of islet cell apoptosis in vitro. Diabetes. 1999; 48: 1730-1736.
36. Zhang Z, Ding Y, Dai X, Wang J, Li Y. Epigallocatechin-3-gallate protects pro-inflammatory cytokine induced injuries in insulin-producing cells through the mitochondrial pathway. Eur J Pharmacol. 2011; 670: 311-316.
37. Azevedo-Martins AK, Lortz S, Lenzen S, Curi R, Eizirik DL, Tiedge M. Improvement of the mitochondrial antioxidant defense status prevents cytokine-induced nuclear factor-kappaB activation in insulin-producing cells. Diabetes. 2003; 52: 93-101.
38. Kim MJ, Ryu GR, Kang JH etal. Inhibitory effects of epicatechin on interleukin-1beta-induced inducible nitric oxide synthase expression in RINm5F cells and rat pancreatic islets by down-regulation of NF-kappaB activation. Biochem Pharmacol. 2004; 68: 1775-1785.
39. Li N, Brun T, Cnop M, Cunha DA, Eizirik DL, Maechler P. Transient oxidative stress damages mitochondrial machinery inducing persistent beta-cell dysfunction. J Biol Chem. 2009; 284: 23602-23612.
40. Saksida T, Stosic-Grujicic S, Timotijevic G, Sandler S, Stojanovic I. Macrophage migration inhibitory factor deficiency protects pancreatic islets from palmitic acid-induced apoptosis. Immunol Cell Biol. 2012; 90: 688-698.
41. Yano M, Watanabe K, Yamamoto T etal. Mitochondrial dysfunction and increased reactive oxygen species impair insulin secretion in sphingomyelin synthase 1-null mice. J Biol Chem. 2011; 286: 3992-4002.
42. Li XL, Chen T, Wong YS etal. Involvement of mitochondrial dysfunction in human islet amyloid polypeptide-induced apoptosis in INS-1E pancreatic beta cells: An effect attenuated by phycocyanin. Int J Biochem Cell Biol. 2011; 43: 525-534.
43. Coughlan MT, Yap FY, Tong DC etal. Advanced Glycation end products are direct modulators of {beta}-cell function. Diabetes. 2011; 60: 2523-2532.
44. Kennedy C. The discovery and development of P2 receptor subtypes. J Auton Nerv Syst. 2000; 81: 158-163.
45. Franke H, Illes P. Involvement of P2 receptors in the growth and survival of neurons in the CNS. Pharmacol Ther. 2006; 109: 297-324.
46. Richards-Williams C, Contreras JL, Berecek KH, Schwiebert EM. 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 Signal. 2008; 4: 393-405.
47. Coutinho-Silva R, Parsons M, Robson T, Burnstock G. Changes in expression of P2 receptors in rat and mouse pancreas during development and ageing. Cell Tissue Res. 2001; 306: 373-383.
48. Lynch KJ, Touma E, Niforatos W etal. Molecular and functional characterization of human P2X(2) receptors. Mol Pharmacol. 1999; 56: 1171-1181.
49. Hazama A, Hayashi S, Okada Y. Cell surface measurements of ATP release from single pancreatic beta cells using a novel biosensor technique. Pflugers Arch. 1998; 437: 31-35.
50. Obermuller S, Lindqvist A, Karanauskaite J, Galvanovskis J, Rorsman P, Barg S. Selective nucleotide-release from dense-core granules in insulin-secreting cells. J Cell Sci. 2005; 118: 4271-4282.
51. Geschwind JF, Hiriart M, Glennon MC etal. Selective activation of Ca2+ influx by extracellular ATP in a pancreatic beta-cell line (HIT). Biochim Biophys Acta. 1989; 1012: 107-115.
52. Ohtani M, Suzuki J, Jacobson KA, Oka T. Evidence for the possible involvement of the P2Y(6) receptor in Ca (2+) mobilization and insulin secretion in mouse pancreatic islets. Purinergic Signal. 2008; 4: 365-375.
53. Balasubramanian R, Maruoka H, Jayasekara PS, Gao ZG, Jacobson KA. AMP-activated protein kinase as regulator of P2Y(6) receptor-induced insulin secretion in mouse pancreatic beta-cells. Biochem Pharmacol. 2013; 85: 991-998.
54. Hellman B, Dansk H, Grapengiesser E. Pancreatic beta-cells communicate via intermittent release of ATP. Am J Physiol Endocrinol Metab. 2004; 286: E759-765.
55. Ohtani M, Ohura K, Oka T. Involvement of P2X Receptors in the regulation of insulin secretion, proliferation and survival in mouse pancreatic beta-cells. Cell Physiol Biochem. 2011; 28: 355-366.
56. Fischer B, Shahar L, Chulkin A etal. 2-Thioether-5′-O-(1-thiotriphosphate)-adenosine derivatives: New insulin secretagogues acting through P2Y-receptors. Isr Med Assoc J. 2000; 2 (Suppl): 92-98.
57. Jacques-Silva MC, Correa-Medina M, Cabrera O etal. ATP-gated P2X3 receptors constitute a positive autocrine signal for insulin release in the human pancreatic beta cell. Proc Natl Acad Sci U S A. 2010; 107: 6465-6470.
58. Amisten S, Meidute-Abaraviciene S, Tan C etal. ADP mediates inhibition of insulin secretion by activation of P2Y13 receptors in mice. Diabetologia. 2010; 53: 1927-1934.
59. Bertrand G, Chapal J, Loubatieres-Mariani MM. Potentiating synergism between adenosine diphosphate or triphosphate and acetylcholine on insulin secretion. Am J Physiol. 1986; 251: E416-421.
60. Pacheco PA, Ferreira LG, Alves LA, Faria RX. Modulation of P2 receptors on pancreatic beta-cells by agonists and antagonists: A molecular target for type 2 diabetes treatment. Curr Diab Rev. 2013; 9: 228-236.
61. Lavoie EG, Fausther M, Kauffenstein G etal. Identification of the ectonucleotidases expressed in mouse, rat, and human Langerhans islets: Potential role of NTPDase3 in insulin secretion. Am J Physiol Endocrinol Metab. 2010; 299: E647-656.