Bile acid effects are mediated by ATP release and purinergic signalling in exocrine pancreatic cells

Cell Communication and Signaling

Volumn 13, Issue 1, 2015, Pages

  Kowal, Justyna M ^a   Haanes, Kristian A ^a,b   Christensen, Nynne M ^a   Novak, Ivana ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b Mental Health Center Glostrup   (Denmark)

Author keywords

AT1.03YEMK; ATP release; ATP sensor; Bile acids; Ca2+; CDCA; FLIM FRET; FXR; P2 receptors; Pancreas; TGR5

Indexed keywords

ADENOSINE RECEPTOR; ADENOSINE TRIPHOSPHATE; BILE ACID; CALCIUM ION; CHENODEOXYCHOLIC ACID; GLYCINE; MEMBRANE RECEPTOR; PROTEIN TGR5 RECEPTOR; PURINERGIC RECEPTOR BLOCKING AGENT; SODIUM CALCIUM EXCHANGE PROTEIN; TAURINE; UNCLASSIFIED DRUG; CALCIUM; G PROTEIN COUPLED RECEPTOR; GLYCOCHENODEOXYCHOLIC ACID; GPBAR1 PROTEIN, HUMAN; PURINERGIC P2 RECEPTOR; TAUROCHENODEOXYCHOLIC ACID;

ACINAR CELL; ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EXOCRINE PANCREAS; HUMAN; HUMAN CELL; INTESTINE; NONHUMAN; PANCREAS CELL; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN LOCALIZATION; PROTEIN MODIFICATION; PROTEIN SECRETION; RAT; SIGNAL TRANSDUCTION; ANIMAL; CELL LINE; CYTOLOGY; METABOLISM; PANCREAS;

ADENOSINE TRIPHOSPHATE; ANIMALS; BILE ACIDS AND SALTS; CALCIUM; CELL LINE; CHENODEOXYCHOLIC ACID; GLYCOCHENODEOXYCHOLIC ACID; HUMANS; PANCREAS; RATS; RECEPTORS, G-PROTEIN-COUPLED; RECEPTORS, PURINERGIC P2; SIGNAL TRANSDUCTION; TAUROCHENODEOXYCHOLIC ACID;

EID: 84931067481     PISSN: None     EISSN: 1478811X     Source Type: Journal    
DOI: 10.1186/s12964-015-0107-9     Document Type: Article

References (72)

1. Kawamata Y, Fujii R, Hosoya M, Harada M, Yoshida H, Miwa M, et al. A G protein-coupled receptor responsive to bile acids. J Biol Chem. 2003;278:9435-40.
2. Makishima M, Okamoto AY, Repa JJ, Tu H, Learned RM, Luk A, et al. Identification of a nuclear receptor for bile acids. Science. 1999;284:1362-5.
3. Maruyama T, Miyamoto Y, Nakamura T, Tamai Y, Okada H, Sugiyama E, et al. Identification of membrane-type receptor for bile acids (M-BAR). Biochem Biophys Res Commun. 2002;298:714-9.
4. Schaap FG, Trauner M, Jansen PL. Bile acid receptors as targets for drug development. Nat Rev Gastroenterol Hepatol. 2014;11:55-67.
5. Maruyama T, Tanaka K, Suzuki J, Miyoshi H, Harada N, Nakamura T, et al. Targeted disruption of G protein-coupled bile acid receptor 1 (Gpbar1/M-Bar) in mice. J Endocrinol. 2006;191:197-205.
6. Watanabe M, Houten SM, Mataki C, Christoffolete MA, Kim BW, Sato H, et al. Bile acids induce energy expenditure by promoting intracellular thyroid hormone activation. Nature. 2006;439:484-9.
7. Pols TW, Noriega LG, Nomura M, Auwerx J, Schoonjans K. The bile acid membrane receptor TGR5 as an emerging target in metabolism and inflammation. J Hepatol. 2011;54:1263-72.
8. Keely SJ, Scharl MM, Bertelsen LS, Hagey LR, Barrett KE, Hofmann AF. Bile acid-induced secretion in polarized monolayers of T84 colonic epithelial cells: Structure-activity relationships. Am J Physiol Gastrointest Liver Physiol. 2007;292:G290-7.
9. Mroz MS, Keating N, Ward JB, Sarker R, Amu S, Aviello G, et al. Farnesoid X receptor agonists attenuate colonic epithelial secretory function and prevent experimental diarrhoea in vivo. Gut. 2014;63:808-17.
10. - channels in Calu-3 airway epithelial cells. Am J Physiol Lung Cell Mol Physiol. 2014;307:L407-18.
11. Keitel V, Gorg B, Bidmon HJ, Zemtsova I, Spomer L, Zilles K, et al. The bile acid receptor TGR5 (Gpbar-1) acts as a neurosteroid receptor in brain. Glia. 2010;58:1794-805.
12. Masyuk AI, Huang BQ, Radtke BN, Gajdos GB, Splinter PL, Masyuk TV, et al. Ciliary subcellular localization of TGR5 determines the cholangiocyte functional response to bile acid signaling. Am J Physiol Gastrointest Liver Physiol. 2013;304:G1013-24.
13. - umbrella: a unifying hypothesis on pathogenetic and therapeutic aspects of fibrosing cholangiopathies. Hepatology. 2010;52:1489-96.
14. Keitel V, Haussinger D. TGR5 in cholangiocytes. Curr Opin Gastroenterol. 2013;29:299-304.
15. Lee YY, Hong SH, Lee YJ, Chung SS, Jung HS, Park SG, et al. Tauroursodeoxycholate (TUDCA), chemical chaperone, enhances function of islets by reducing ER stress. Biochem Biophys Res Commun. 2010;397:735-9.
16. ATP channel inhibition. Diabetes. 2012;61:1479-89.
17. Kumar DP, Rajagopal S, Mahavadi S, Mirshahi F, Grider JR, Murthy KS, et al. Activation of transmembrane bile acid receptor TGR5 stimulates insulin secretion in pancreatic beta cells. Biochem Biophys Res Commun. 2012;427:600-5.
18. Thomas C, Gioiello A, Noriega L, Strehle A, Oury J, Rizzo G, et al. TGR5-mediated bile acid sensing controls glucose homeostasis. Cell Metab. 2009;10:167-77.
19. Meloni AR, DeYoung MB, Lowe C, Parkes DG. GLP-1 receptor activated insulin secretion from pancreatic beta-cells: mechanism and glucose dependence. Diabetes Obes Metab. 2013;15:15-27.
20. Kim JY, Kim KH, Lee JA, Namkung W, Sun AQ, Ananthanarayanan M, et al. Transporter-mediated bile acid uptake causes Ca2 + -dependent cell death in rat pancreatic acinar cells. Gastroenterology. 2002;122:1941-53.
21. + concentration. J Biol Chem. 2005;280:1764-70.
22. 2+ signalling and pancreatitis: effects of alcohol, bile and coffee. Trends Pharmacol Sci. 2006;27:113-20.
23. 2+ release from both the endoplasmic reticulum and acidic intracellular calcium stores through activation of inositol trisphosphate receptors and ryanodine receptors. J Biol Chem. 2006;281:40154-63.
24. Wan MH, Huang W, Latawiec D, Jiang K, Booth DM, Elliott V, et al. Review of experimental animal models of biliary acute pancreatitis and recent advances in basic research. HPB (Oxford). 2012;14:73-81.
25. Perides G, Laukkarinen JM, Vassileva G, Steer ML. Biliary acute pancreatitis in mice is mediated by the G-protein-coupled cell surface bile acid receptor Gpbar1. Gastroenterology. 2010;138:715-25.
26. Okolo C, Wong T, Moody MW, Nguyen TD. Effects of bile acids on dog pancreatic duct epithelial cell secretion and monolayer resistance. Am J Physiol Gastrointest Liver Physiol. 2002;283:G1042-50.
27. Venglovecz V, Rakonczay Jr Z, Ozsvari B, Takacs T, Lonovics J, Varro A, et al. Effects of bile acids on pancreatic ductal bicarbonate secretion in guinea pig. Gut. 2008;57:1102-12.
28. Hegyi P, Petersen OH. The exocrine pancreas: the acinar-ductal tango in physiology and pathophysiology. Rev Physiol Biochem Pharmacol. 2013;165:1-30.
29. 2+-activated potassium channels in pancreatic duct epithelial cells. Gut. 2011;60:361-9.
30. -. Pancreas. 2009;38:921-9.
31. Burnstock G, Novak I. Purinergic signalling in the pancreas in health and disease. J Endocrinol. 2012;213:123-41.
32. Novak I, Haanes KA, Wang J. Acid-base transport in pancreas-new challenges. Front Physiol. 2013;4:380.
33. Haanes KA, Novak I. ATP storage and uptake by isolated pancreatic zymogen granules. Biochem J. 2010;429:303-11.
34. Haanes KA, Kowal JM, Arpino G, Lange SC, Moriyama Y, Pedersen PA, Novak I. Role of vesicular nucleotide transporter VNUT (SLC17A9) in release of ATP from AR42J cells and mouse pancreatic acinar cells. Purinergic Signal. 2014
35. Sorensen CE, Novak I. Visualization of ATP release in pancreatic acini in response to cholinergic stimulus. Use of fluorescent probes and confocal microscopy. J Biol Chem. 2001;276:32925-32.
36. Lazarowski ER. Vesicular and conductive mechanisms of nucleotide release. Purinergic Signal. 2012;8:359-73.
37. Lohman AW, Isakson BE. Differentiating connexin hemichannels and pannexin channels in cellular ATP release. FEBS Lett. 2014;588:1379-88.
38. Yegutkin GG, Samburski SS, Jalkanen S, Novak I. ATP-consuming and ATP-generating enzymes secreted by pancreas. J Biol Chem. 2006;281:29441-7.
39. Okada SF, Nicholas RA, Kreda SM, Lazarowski ER, Boucher RC. Physiological regulation of ATP release at the apical surface of human airway epithelia. J Biol Chem. 2006;281:22992-3002.
40. Yegutkin GG, Mikhailov A, Samburski SS, Jalkanen S. The detection of micromolar pericellular ATP pool on lymphocyte surface by using lymphoid ecto-adenylate kinase as intrinsic ATP sensor. Mol Biol Cell. 2006;17:3378-85.
41. Imamura H, Nhat KP, Togawa H, Saito K, Iino R, Kato-Yamada Y, et al. Visualization of ATP levels inside single living cells with fluorescence resonance energy transfer-based genetically encoded indicators. Proc Natl Acad Sci U S A. 2009;106:15651-6.
42. Becker W, Bergmann A, Hink MA, Konig K, Benndorf K, Biskup C. Fluorescence lifetime imaging by time-correlated single-photon counting. Microsc Res Tech. 2004;63:58-66.
43. Fiorotto R, Spirli C, Fabris L, Cadamuro M, Okolicsanyi L, Strazzabosco M. Ursodeoxycholic acid stimulates cholangiocyte fluid secretion in mice via CFTR-dependent ATP secretion. Gastroenterology. 2007;133:1603-13.
44. 2+-ATPase. Proc Natl Acad Sci U S A. 1990;87:2466-70.
45. Parker HE, Wallis K, le Roux CW, Wong KY, Reimann F, Gribble FM. Molecular mechanisms underlying bile acid-stimulated glucagon-like peptide-1 secretion. Br J Pharmacol. 2012;165:414-23.
46. 2+. Cell Physiol Biochem. 2009;23:387-96.
47. 2+ exchanger in rat pancreatic ducts. J Membr Biol. 2002;186:43-53.
48. Neale G, Lewis B, Weaver V, Panveliwalla D. Serum bile acids in liver disease. Gut. 1971;12:145-52.
49. Brufau G, Bahr MJ, Staels B, Claudel T, Ockenga J, Boker KH, et al. Plasma bile acids are not associated with energy metabolism in humans. Nutr Metab (Lond). 2010;7:73.
50. Fisher MM, Yousef IM. Sex differences in the bile acid composition of human bile: studies in patients with and without gallstones. Can Med Assoc J. 1973;109:190-3.
51. Liu HT, Toychiev AH, Takahashi N, Sabirov RZ, Okada Y. Maxi-anion channel as a candidate pathway for osmosensitive ATP release from mouse astrocytes in primary culture. Cell Res. 2008;18:558-65.
52. Sabirov RZ, Dutta AK, Okada Y. Volume-dependent ATP-conductive large-conductance anion channel as a pathway for swelling-induced ATP release. J Gen Physiol. 2001;118:251-66.
53. Gutierrez-Martin Y, Bustillo D, Gomez-Villafuertes R, Sanchez-Nogueiro J, Torregrosa-Hetland C, Binz T, et al. P2X7 receptors trigger ATP exocytosis and modify secretory vesicle dynamics in neuroblastoma cells. J Biol Chem. 2011;286:11370-81.
54. Pelegrin P, Surprenant A. The P2X7 receptor-pannexin connection to dye uptake and IL-1beta release. Purinergic Signal. 2009;5:129-37.
55. Wiemuth D, Sahin H, Falkenburger BH, Lefevre CM, Wasmuth HE, Grunder S. BASIC-a bile acid-sensitive ion channel highly expressed in bile ducts. FASEB J. 2012;26:4122-30.
56. Schroder O, Rathner W, Caspary WF, Stein J. Bile acid-induced increase of rat colonic apical membrane fluidity and proton permeability. Z Gastroenterol. 1996;34:365-70.
57. 2+-dependent signaling pathways. J Biol Chem. 2009;284:20638-48.
58. Wilson PD, Hovater JS, Casey CC, Fortenberry JA, Schwiebert EM. ATP release mechanisms in primary cultures of epithelia derived from the cysts of polycystic kidneys. J Am Soc Nephrol. 1999;10:218-29.
59. Bjaelde RG, Arnadottir SS, Overgaard MT, Leipziger J, Praetorius HA. Renal epithelial cells can release ATP by vesicular fusion. Front Physiol. 2013;4:238.
60. Praetorius HA, Leipziger J. Released nucleotides amplify the cilium-dependent, flow-induced [Ca2+]i response in MDCK cells. Acta Physiol (Oxf). 2009;197:241-51.
61. + channels in human pancreatic duct epithelium. Am J Physiol Cell Physiol. 2013;304:C673-84.
62. Kelly OB, Mroz MS, Ward JB, Colliva C, Scharl M, Pellicciari R, et al. Ursodeoxycholic acid attenuates colonic epithelial secretory function. J Physiol. 2013;591:2307-18.
63. Voronina SG, Barrow SL, Simpson AW, Gerasimenko OV, da Silva X, Rutter GA, et al. Dynamic changes in cytosolic and mitochondrial ATP levels in pancreatic acinar cells. Gastroenterology. 2010;138:1976-87.
64. Ignacio BJ, Olmo N, Perez-Ramos P, Santiago-Gomez A, Lecona E, Turnay J, et al. Deoxycholic and chenodeoxycholic bile acids induce apoptosis via oxidative stress in human colon adenocarcinoma cells. Apoptosis. 2011;16:1054-67.
65. Duan RD, Erlanson-Albertsson C. Effect of bile salt on amylase release from rat pancreatic acini. Scand J Gastroenterol. 1985;20:1239-45.
66. Nguyen A, Bouscarel B. Bile acids and signal transduction: role in glucose homeostasis. Cell Signal. 2008;20:2180-97.
67. Keitel V, Reinehr R, Gatsios P, Rupprecht C, Gorg B, Selbach O, et al. The G-protein coupled bile salt receptor TGR5 is expressed in liver sinusoidal endothelial cells. Hepatology. 2007;45:695-704.
68. Xie Q, Khaoustov VI, Chung CC, Sohn J, Krishnan B, Lewis DE, et al. Effect of tauroursodeoxycholic acid on endoplasmic reticulum stress-induced caspase-12 activation. Hepatology. 2002;36:592-601.
69. Cummings BP, Bettaieb A, Graham JL, Kim J, Ma F, Shibata N, et al. Bile-acid-mediated decrease in endoplasmic reticulum stress: a potential contributor to the metabolic benefits of ileal interposition surgery in UCD-T2DM rats. Dis Model Mech. 2013;6:443-56.
70. Logsdon CD, Moessner J, Williams JA, Goldfine ID. Glucocorticoids increase amylase mRNA levels, secretory organelles, and secretion in pancreatic acinar AR42J cells. J Cell Biol. 1985;100:1200-8.
71. Hansen MR, Krabbe S, Novak I. Purinergic receptors and calcium signalling in human pancreatic duct cell lines. Cell Physiol Biochem. 2008;22:157-68.
72. 2+ indicators with greatly improved fluorescence properties. J Biol Chem. 1985;260:3440-50.