Calcium Signaling in the Islets

Islets of Langerhans, Second Edition

Volumn , Issue , 2015, Pages 605-632

  Islam, Md Shahidul ^a,b  

^a STOCKHOLM SÖDER HOSPITAL   (Sweden)

^b UPPSALA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

Basal calcium; Calcium oscillation; Calcium Induced calcium release; Cicr; Depolarization; KATP< inf> channel; Membrane potential; Ryanodine receptor; Ryr1; Ryr2; Ryr3; Transient receptor potential channels; Trp channels; Trpm2; Trpm3; Trpv1; Trpv2; Trpv4

Indexed keywords

EID: 84943311680     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-94-007-6686-0_9     Document Type: Chapter

References (143)

1. Ainscow EK, Rutter GA (2002) Glucose-stimulated oscillations in free cytosolic ATP concentration imaged in single islet β-cells: evidence for a Ca2+-dependent mechanism. Diabetes 51(Suppl 1):S162–S170
2. Akiba Y, Kato S, Katsube KI, Nakamura M, Takeuchi K, Ishii H, Hibi T (2004) Transient receptor potential vanilloid subfamily 1 expressed in pancreatic islet β cells modulates insulin secretion in rats. Biochem Biophys Res Commun 321:219–225
3. Babes A, Fischer MJ, Filipovic M, Engel MA, Flonta ML, Reeh PW (2013) The anti-diabetic drug glibenclamide is an agonist of the transient receptor potential Ankyrin 1 (TRPA1) ion channel. Eur J Pharmacol 704:15–22
4. Bari MR, Akbar S, Eweida M, Kuhn FJ, Gustafsson AJ, Luckhoff A, Islam MS (2009) H2O2-induced Ca2+ influx and its inhibition by N-(p-amylcinnamoyl) anthranilic acid in the β-cells: involvement of TRPM2 channels. J Cell Mol Med 13:3260–3267
5. Barnett DW, Pressel DM, Misler S (1995) Voltage-dependent Na+ and Ca2+ currents in human pancreatic islet β-cells: evidence for roles in the generation of action potentials and insulin secretion. Pflugers Arch 431:272–282
6. Beauvois MC, Merezak C, Jonas JC, Ravier MA, Henquin JC, Gilon P (2006) Glucose-induced mixed [Ca2+]c oscillations in mouse β-cells are controlled by the membrane potential and the SERCA3 Ca2+-ATPase of the endoplasmic reticulum. Am J Physiol Cell Physiol 290:C1503–C1511
7. Bergsten P, Hellman B (1993) Glucose-induced amplitude regulation of pulsatile insulin secretion from individual pancreatic islets. Diabetes 42:670–674
8. Bezprozvanny I, Watras J, Ehrlich BE (1991) Bell-shaped calcium-response curves of Ins(1,4,5) P3- and calcium gated channels from endoplasmic reticulum of cerebellum. Nature 351:751–754
9. Bokvist K, Eliasson L, Ämmälä C, Renström E, Rorsman P (1995) Co-localization of L-type Ca2+ channels and insulin-containing secretory granules and its significance for the initiation of exocytosis in mouse pancreatic β-cells. EMBO J 14:50–57
10. Braun M, Ramracheya R, Bengtsson M, Zhang Q, Karanauskaite J, Partridge C, Johnson PR, Rorsman P (2008) Voltage-gated ion channels in human pancreatic β-cells: electrophysiological characterization and role in insulin secretion. Diabetes 57:1618–1628
11. Brixel LR, Monteilh-Zoller MK, Ingenbrandt CS, Fleig A, Penner R, Enklaar T, Zabel BU, Prawitt D (2010) TRPM5 regulates glucose-stimulated insulin secretion. Pflugers Arch 460:69–76
12. Bruton JD, Lemmens R, Shi CL, Persson-Sjögren S, Westerblad H, Ahmed M, Pyne NJ, Frame M, Furman BL, Islam MS (2003) Ryanodine receptors of pancreatic β-cells mediate a distinct context-dependent signal for insulin secretion. FASEB J 17:301–303
13. Bruzzone S, Bodrato N, Usai C, Guida L, Moreschi I, Nano R, Antonioli B, Fruscione F, Magnone M, Scarfi S, De Flora A, Zocchi E (2008) Abscisic acid is an endogenous stimulator of insulin release from human pancreatic islets with cyclic ADP ribose as second messenger. J Biol Chem 283:32188–32197
14. Cabrera O, Berman DM, Kenyon NS, Ricordi C, Berggren PO, Caicedo A (2006) The unique cytoarchitecture of human pancreatic islets has implications for islet cell function. Proc Natl Acad Sci USA 103:2334–2339
15. Calcraft PJ, Ruas M, Pan Z, Cheng X, Arredouani A, Hao X, Tang J, Rietdorf K, Teboul L, Chuang KT, Lin P, Xiao R, Wang C, Zhu Y, Lin Y, Wyatt CN, Parrington J, Ma J, Evans AM, Galione A, Zhu MX (2009) NAADP mobilizes calcium from acidic organelles through two-pore channels. Nature 459:596–600
16. Cao DS, Zhong L, Hsieh TH, Abooj M, Bishnoi M, Hughes L, Premkumar LS (2012) Expression of Transient Receptor Potential Ankyrin 1 (TRPA1) and its role in insulin release from rat pancreatic β cells. PLoS One 7:e38005
17. Casas S, Novials A, Reimann F, Gomis R, Gribble FM (2008) Calcium elevation in mouse pancreatic β cells evoked by extracellular human islet amyloid polypeptide involves activation of the mechanosensitive ion channel TRPV4. Diabetologia 51:2252–2262
18. Cheng H, Beck A, Launay P, Gross SA, Stokes AJ, Kinet JP, Fleig A, Penner R (2007) TRPM4 controls insulin secretion in pancreatic β-cells. Cell Calcium 41:51–61
19. Cheng KT, Ong HL, Liu X, Ambudkar IS (2013) Contribution and regulation of TRPC channels in store-operated Ca2+ entry. Curr Top Membr 71:149–179
20. Colsoul B, Schraenen A, Lemaire K, Quintens R, Van Lommel L, Segal A, Owsianik G, Talavera K, Voets T, Margolskee RF, Kokrashvili Z, Gilon P, Nilius B, Schuit FC, Vennekens R (2010) Loss of high-frequency glucose-induced Ca2+ oscillations in pancreatic islets correlates with impaired glucose tolerance in Trpm5-/- mice. Proc Natl Acad Sci USA 107:5208–5213
21. Cuesta-Munoz AL, Huopio H, Otonkoski T, Gomez-Zumaquero JM, Nanto-Salonen K, Rahier J, Lopez-Enriquez S, Garcia-Gimeno MA, Sanz P, Soriguer FC, Laakso M (2004) Severe persistent hyperinsulinemic hypoglycemia due to a de novo glucokinase mutation. Diabetes 53:2164–2168
22. Davalli AM, Biancardi E, Pollo A, Socci C, Pontiroli AE, Pozza G, Clementi F, Sher E, Carbone E (1996) Dihydropyridine-sensitive and -insensitive voltage-operated calcium channels participate in the control of glucose-induced insulin release from human pancreatic β cells. J Endocrinol 150:195–203
23. Dehaven WI, Jones BF, Petranka JG, Smyth JT, Tomita T, Bird GS, Putney JW Jr (2009) TRPC channels function independently of STIM1 and Orai1. J Physiol 587:2275–2298
24. Demion M, Bois P, Launay P, Guinamard R (2007) TRPM4, a Ca2+-activated nonselective cation channel in mouse sino-atrial node cells. Cardiovasc Res 73:531–538
25. Dixit SS, Wang T, Manzano EJ, Yoo S, Lee J, Chiang DY, Ryan N, Respress JL, Yechoor VK, Wehrens XH (2013) Effects of CaMKII-mediated phosphorylation of ryanodine receptor type 2 on islet calcium handling, insulin secretion, and glucose tolerance. PLoS One 8:e58655
26. Dror V, Kalynyak TB, Bychkivska Y, Frey MH, Tee M, Jeffrey KD, Nguyen V, Luciani DS, Johnson JD (2008) Glucose and endoplasmic reticulum calcium channels regulate HIF-1β via presenilin in pancreatic β-cells. J Biol Chem 283:9909–9916
27. Du J, Xie J, Yue L (2009) Intracellular calcium activates TRPM2 and its alternative spliced isoforms. Proc Natl Acad Sci USA 106:7239–7244
28. Dyachok O, Gylfe E (2001) Store-operated influx of Ca2+ in pancreatic β-cells exhibits graded dependence on the filling of the endoplasmic reticulum. J Cell Sci 114:2179–2186
29. Dyachok O, Gylfe E (2004) Ca2+-induced Ca2+ release via inositol 1,4,5-trisphosphate receptors is amplified by protein kinase A and triggers exocytosis in pancreatic β-cells. J Biol Chem 279:45455–45461
30. Dyachok O, Tufveson G, Gylfe E (2004) Ca2+-induced Ca2+ release by activation of inositol 1,4,5-trisphosphate receptors in primary pancreatic β-cells. Cell Calcium 36:1–9
31. Dyachok O, Idevall-Hagren O, Sagetorp J, Tian G, Wuttke A, Arrieumerlou C, Akusjarvi G, Gylfe E, Tengholm A (2008) Glucose-induced cyclic AMP oscillations regulate pulsatile insulin secretion. Cell Metab 8:26–37
32. Eisfeld J, Luckhoff A (2007) TRPM2. Handb Exp Pharmacol 179:237–252
33. Fabiato A (1985) Time and calcium dependence of activation and inactivation of calcium-induced release of calcium from the sarcoplasmic reticulum of a skinned canine cardiac Purkinje cell. J Gen Physiol 85:247–289
34. Fruhwald J, Camacho LJ, Dembla S, Mannebach S, Lis A, Drews A, Wissenbach U, Oberwinkler J, Philipp SE (2012) Alternative splicing of a protein domain indispensable for function of transient receptor potential melastatin 3 (TRPM3) ion channels. J Biol Chem 287:36663–36672
35. Gembal M, Detimary P, Gilon P, Gao ZY, Henquin JC (1993) Mechanisms by which glucose can control insulin release independently from its action on adenosine triphosphate-sensitive K+ channels in mouse B cells. J Clin Invest 91:871–880
36. Gilon P, Henquin JC (1992) Influence of membrane potential changes on cytoplasmic Ca2+ concentration in an electrically excitable cell, the insulin-secreting pancreatic β-cell. J Biol Chem 267:20713–20720
37. Gilon P, Henquin JC (2001) Mechanisms and physiological significance of the cholinergic control of pancreatic β-cell function. Endocr Rev 22:565–604
38. Goodner CJ, Hom FG, Koerker DJ (1982) Hepatic glucose production oscillates in synchrony with the islet secretory cycle in fasting rhesus monkeys. Science 215:1257–1260
39. Gram DX, Ahren B, Nagy I, Olsen UB, Brand CL, Sundler F, Tabanera R, Svendsen O, Carr RD, Santha P, Wierup N, Hansen AJ (2007) Capsaicin-sensitive sensory fibers in the islets of Langerhans contribute to defective insulin secretion in Zucker diabetic rat, an animal model for some aspects of human type 2 diabetes. Eur J Neurosci 25:213–223
40. Grimberg A, Ferry RJ Jr, Kelly A, Koo-McCoy S, Polonsky K, Glaser B, Permutt MA, Aguilar-Bryan L, Stafford D, Thornton PS, Baker L, Stanley CA (2001) Dysregulation of insulin secretion in children with congenital hyperinsulinism due to sulfonylurea receptor mutations. Diabetes 50:322–328
41. Gustafsson AJ, Ingelman-Sundberg H, Dzabic M, Awasum J, Nguyen KH, Östenson CG, Pierro C, Tedeschi P, Woolcott O, Chiounan S, Lund PE, Larsson O, Islam MS (2005) Ryanodine receptor-operated activation of TRP-like channels can trigger critical Ca2+ signaling events in pancreatic β-cells. FASEB J 19:301–303
42. Hara Y, Wakamori M, Ishii M, Maeno E, Nishida M, Yoshida T, Yamada H, Shimizu S, Mori E, Kudoh J, Shimizu N, Kurose H, Okada Y, Imoto K, Mori Y (2002) LTRPC2 Ca2+-permeable channel activated by changes in redox status confers susceptibility to cell death. Mol Cell 9:163–173
43. Haspel D, Krippeit-Drews P, Aguilar-Bryan L, Bryan J, Drews G, Dufer M (2005) Crosstalk between membrane potential and cytosolic Ca2+ concentration in β cells from Sur1-/- mice. Diabetologia 48:913–921
44. Heiner I, Eisfeld J, Warnstedt M, Radukina N, Jungling E, Lückhoff A (2006) Endogenous ADP-ribose enables calcium-regulated cation currents through TRPM2 channels in neutrophil granulocytes. Biochem J 398:225–232
45. Hellman B, Gylfe E, Bergsten P, Grapengiesser E, Lund PE, Berts A, Tengholm A, Pipeleers DG, Ling Z (1994) Glucose induces oscillatory Ca2+ signalling and insulin release in human pancreatic β cells. Diabetologia 37(Suppl 2):S11–S20
46. Hellman B, Gylfe E, Bergsten P, Grapengiesser E, Berts A, Liu YJ, Tengholm A, Westerlund J (1997) Oscillatory signaling and insulin release in human pancreatic β-cells exposed to strontium. Endocrinology 138:3161–3165
47. Henquin JC, Meissner HP, Schmeer W (1982) Cyclic variations of glucose-induced electrical activity in pancreatic B cells. Pflugers Arch 393:322–327
48. Henquin JC, Dufrane D, Nenquin M (2006) Nutrient control of insulin secretion in isolated normal human islets. Diabetes 55:3470–3477
49. Herson PS, Ashford ML (1997) Activation of a novel non-selective cation channel by alloxan and H2O2 in the rat insulin-secreting cell line CRI-G1. J Physiol 501(Pt 1):59–66
50. Hisanaga E, Nagasawa M, Ueki K, Kulkarni RN, Mori M, Kojima I (2009) Regulation of calcium permeable TRPV2 channel by insulin in pancreatic β-cells. Diabetes 58:174–184
51. Holmkvist J, Tojjar D, Almgren P, Lyssenko V, Lindgren CM, Isomaa B, Tuomi T, Berglund G, Renstrom E, Groop L (2007) Polymorphisms in the gene encoding the voltage-dependent Ca2+ channel Ca (V)2.3 (CACNA1E) are associated with type 2 diabetes and impaired insulin secretion. Diabetologia 50:2467–2475
52. Holz GG, Leech CA, Habener JF (1995) Activation of a cAMP-regulated Ca2+-signaling pathway in pancreatic β-cells by the insulinotropic hormone glucagon-like peptide-1. J Biol Chem 270:17749–17757
53. Holz GG, Leech CA, Heller RS, Castonguay M, Habener JF (1999) cAMP-dependent mobilization of intracellular Ca2+ stores by activation of ryanodine receptors in pancreatic β-cells. A Ca2+ signalling system stimulated by the insulinotropic hormone glucagon-like peptide-1-(7-37). J Biol Chem 274:14147–14156
54. Idevall-Hagren O, Jakobsson I, Xu Y, Tengholm A (2013) Spatial control of Epac2 activity by cAMP and Ca2+-mediated activation of Ras in pancreatic β cells. Sci Signal 6:ra29-6
55. Islam MS (2002) The ryanodine receptor calcium channel of β-cells: molecular regulation and physiological significance. Diabetes 51:1299–1309
56. Islam MS (2011) TRP channels of islets. Adv Exp Med Biol 704:811–830
57. Islam MS, Leibiger I, Leibiger B, Rossi D, Sorrentino V, Ekström TJ, Westerblad H, Andrade FH, Berggren PO (1998) In situ activation of the type 2 ryanodine receptor in pancreatic β cells requires cAMP-dependent phosphorylation. Proc Natl Acad Sci USA 95:6145–6150
58. Jabin FA, Kannisto K, Bostrom A, Hadrovic B, Farre C, Eweida M, Wester K, Islam MS (2012) Insulin-secreting INS-1E cells express functional TRPV1 channels. Islets 4:56–63
59. Johnson JD, Misler S (2002) Nicotinic acid-adenine dinucleotide phosphate-sensitive calcium stores initiate insulin signaling in human β cells. Proc Natl Acad Sci USA 99:14566–14571
60. Johnson JD, Han Z, Otani K, Ye H, Zhang Y, Wu H, Horikawa Y, Misler S, Bell GI, Polonsky KS (2004a) RyR2 and calpain-10 delineate a novel apoptosis pathway in pancreatic islets. J Biol Chem 279:24794–24802
61. Johnson JD, Kuang S, Misler S, Polonsky KS (2004b) Ryanodine receptors in human pancreatic β cells: localization and effects on insulin secretion. FASEB J 18:878–880
62. Johnson JD, Ford EL, Bernal-Mizrachi E, Kusser KL, Luciani DS, Han Z, Tran H, Randall TD, Lund FE, Polonsky KS (2006) Suppressed insulin signaling and increased apoptosis in CD38-null islets. Diabetes 55:2737–2746
63. Jones PM, Persaud SJ (1993) Arachidonic acid as a second messenger in glucose-induced insulin secretion from pancreatic β-cells. J Endocrinol 137:7–14
64. Jung SR, Reed BJ, Sweet IR (2009) A highly energetic process couples calcium influx through L-type calcium channels to insulin secretion in pancreatic β-cells. Am J Physiol Endocrinol Metab 297:E717–E727
65. Kaddis JS, Olack BJ, Sowinski J, Cravens J, Contreras JL, Niland JC (2009) Human pancreatic islets and diabetes research. JAMA 301:1580–1587
66. Kahl S, Malfertheiner P (2004) Exocrine and endocrine pancreatic insufficiency after pancreatic surgery. Best Pract Res Clin Gastroenterol 18:947–955
67. Kang G, Holz GG (2003) Amplification of exocytosis by Ca2+-induced Ca2+ release in INS-1 pancreatic β cells. J Physiol 546:175–189
68. Kang G, Joseph JW, Chepurny OG, Monaco M, Wheeler MB, Bos JL, Schwede F, Genieser HG, Holz GG (2003) Epac-selective cAMP analog 8-pCPT-2′-O-Me-cAMP as a stimulus for Ca2+-induced Ca2+ release and exocytosis in pancreatic β-cells. J Biol Chem 278:8279–8285
69. Kang G, Chepurny OG, Rindler MJ, Collis L, Chepurny Z, Li WH, Harbeck M, Roe MW, Holz GG (2005) A cAMP and Ca2+ coincidence detector in support of Ca2+-induced Ca2+ release in mouse pancreatic β cells. J Physiol 566:173–188
70. Kermode H, Chan WM, Williams AJ, Sitsapesan R (1998) Glycolytic pathway intermediates activate cardiac ryanodine receptors. FEBS Lett 431:59–62
71. Kim BJ, Park KH, Yim CY, Takasawa S, Okamoto H, Im MJ, Kim UH (2008) Generation of nicotinic acid adenine dinucleotide phosphate and cyclic ADP-ribose by glucagon-like peptide-1 evokes Ca2+ signal that is essential for insulin secretion in mouse pancreatic islets. Diabetes 57:868–878
72. Kim MS, Zeng W, Yuan JP, Shin DM, Worley PF, Muallem S (2009) Native store-operated Ca2+ influx requires the channel function of Orai1 and TRPC1. J Biol Chem 284:9733–9741
73. Kindmark H, Köhler M, Nilsson T, Arkhammar P, Wiechel K-L, Rorsman P, Efendic S (1991) Measurements of cytoplasmic free Ca2+ concentration in human pancreatic islets and insulinoma cells. FEBS Lett 291:310–314
74. Kindmark H, Kohler M, Arkhammar P, Efendic S, Larsson O, Linder S, Nilsson T, Berggren PO (1994) Oscillations in cytoplasmic free calcium concentration in human pancreatic islets from subjects with normal and impaired glucose tolerance. Diabetologia 37:1121–1131
75. Kjems LL, Ravier MA, Jonas JC, Henquin JC (2002) Do oscillations of insulin secretion occur in the absence of cytoplasmic Ca2+ oscillations in β-cells? Diabetes 51(Suppl 1):S177–S182
76. Klose C, Straub I, Riehle M, Ranta F, Krautwurst D, Ullrich S, Meyerhof W, Harteneck C (2011) Fenamates as TRP channel blockers: mefenamic acid selectively blocks TRPM3. Br J Pharmacol 162:1757–1769
77. Krishnan K, Ma Z, Björklund A, Islam MS (2014) Role of Transient Receptor Potential Melastatin-like Subtype 5 Channel in Insulin Secretion From Rat β-Cells. Pancreas 43:597–604
78. Kyriazis GA, Soundarapandian MM, Tyrberg B (2012) Sweet taste receptor signaling in β cells mediates fructose-induced potentiation of glucose-stimulated insulin secretion. Proc Natl Acad Sci USA 109:E524–E532
79. Lange I, Yamamoto S, Partida-Sanchez S, Mori Y, Fleig A, Penner R (2009) TRPM2 functions as a lysosomal Ca2+-release channel in β cells. Sci Signal 2:ra23
80. Launay P, Fleig A, Perraud AL, Scharenberg AM, Penner R, Kinet JP (2002) TRPM4 is a Ca2+-activated nonselective cation channel mediating cell membrane depolarization. Cell 109:397–407
81. Lee HC (2012) Cyclic ADP-ribose and nicotinic acid adenine dinucleotide phosphate (NAADP) as messengers for calcium mobilization. J Biol Chem 287:31633–31640
82. Lemmens R, Larsson O, Berggren PO, Islam MS (2001) Ca2+-induced Ca2+ release from the endoplasmic reticulum amplifies the Ca2+ signal mediated by activation of voltage-gated L-type Ca2+ channels in pancreatic β-cells. J Biol Chem 276:9971–9977
83. Lheureux PE, Zahir S, Penaloza A, Gris M (2005) Bench-to-bedside review: antidotal treatment of sulfonylurea-induced hypoglycaemia with octreotide. Crit Care 9:543–549
84. Li F, Zhang ZM (2009) Comparative identification of Ca2+ channel expression in INS-1 and rat pancreatic β cells. World J Gastroenterol 15:3046–3050
85. Lin Y, Sun Z (2012) Antiaging gene Klotho enhances glucose-induced insulin secretion by up-regulating plasma membrane levels of TRPV2 in MIN6 β-cells. Endocrinology 153:3029–3039
86. Lopez-Lopez JR, Shacklock PS, Balke CW, Wier WG (1995) Local calcium transients triggered by single L-type calcium channel currents in cardiac cells. Science 268:1042–1045
87. Maechler P, Kennedy ED, Sebo E, Valeva A, Pozzan T, Wollheim CB (1999) Secretagogues modulate the calcium concentration in the endoplasmic reticulum of insulin-secreting cells. Studies in aequorin-expressing intact and permeabilized INS-1 cells. J Biol Chem 274:12583–12592
88. Majeed Y, Tumova S, Green BL, Seymour VA, Woods DM, Agarwal AK, Naylor J, Jiang S, Picton HM, Porter KE, O’Regan DJ, Muraki K, Fishwick CW, Beech DJ (2012) Pregnenolone sulphate-independent inhibition of TRPM3 channels by progesterone. Cell Calcium 51:1–11
89. Manning Fox JE, Gyulkhandanyan AV, Satin LS, Wheeler MB (2006) Oscillatory membrane potential response to glucose in islet β-cells: a comparison of islet-cell electrical activity in mouse and rat. Endocrinology 147:4655–4663
90. Marigo V, Courville K, Hsu WH, Feng JM, Cheng H (2009) TRPM4 impacts on Ca2+ signals during agonist-induced insulin secretion in pancreatic β-cells. Mol Cell Endocrinol 299:194–203
91. Martin F, Soria B (1996) Glucose-induced [Ca2+]i oscillations in single human pancreatic islets. Cell Calcium 20:409–414
92. Masgrau R, Churchill GC, Morgan AJ, Ashcroft SJ, Galione A (2003) NAADP. A new second messenger for glucose-induced Ca2+ responses in clonal pancreatic β cells. Curr Biol 13:247–251
93. Mears D, Zimliki CL (2004) Muscarinic agonists activate Ca2+ store-operated and -independent ionic currents in insulin-secreting HIT-T15 cells and mouse pancreatic β-cells. J Membr Biol 197:59–70
94. Michael DJ, Xiong W, Geng X, Drain P, Chow RH (2007) Human insulin vesicle dynamics during pulsatile secretion. Diabetes 56:1277–1288
95. Misler S, Barnett DW, Pressel DM, Gillis KD, Scharp DW, Falke LC (1992) Stimulus-secretion coupling in β-cells of transplantable human islets of Langerhans. Evidence for a critical role for Ca2+ entry. Diabetes 41:662–670
96. Misler S, Dickey A, Barnett DW (2005) Maintenance of stimulus-secretion coupling and single β-cell function in cryopreserved-thawed human islets of Langerhans. Pflugers Arch 450:395–404
97. Misler S, Zhou Z, Dickey AS, Silva AM, Pressel DM, Barnett DW (2009) Electrical activity and exocytotic correlates of biphasic insulin secretion from β-cells of canine islets of Langerhans: contribution of tuning two modes of Ca2+ entry-dependent exocytosis to two modes of glucose induced electrical activity. Channels (Austin) 3:181–193
98. Mitchell KJ, Lai FA, Rutter GA (2003) Ryanodine receptor type I and nicotinic acid adenine dinucleotide phosphate receptors mediate Ca2+ release from insulin-containing vesicles in living pancreatic β-cells (MIN6). J Biol Chem 278:11057–11064
99. Nagamatsu S, Ohara-Imaizumi M, Nakamichi Y, Kikuta T, Nishiwaki C (2006) Imaging docking and fusion of insulin granules induced by antidiabetes agents: sulfonylurea and glinide drugs preferentially mediate the fusion of newcomer, but not previously docked, insulin granules. Diabetes 55:2819–2825
100. Neher E (1995) The use of fura-2 for estimating Ca buffers and Ca fluxes. Neuropharmacology 34:1423–1442
101. Nelson PL, Zolochevska O, Figueiredo ML, Soliman A, Hsu WH, Feng JM, Zhang H, Cheng H (2011) Regulation of Ca2+-entry in pancreatic α-cell line by transient receptor potential melastatin 4 plays a vital role in glucagon release. Mol Cell Endocrinol 335:126–134
102. Nilius B, Prenen J, Tang J, Wang C, Owsianik G, Janssens A, Voets T, Zhu MX (2005) Regulation of the Ca2+ sensitivity of the nonselective cation channel TRPM4. J Biol Chem 280:6423–6433
103. Nilius B, Mahieu F, Prenen J, Janssens A, Owsianik G, Vennekens R, Voets T (2006) The Ca2+-activated cation channel TRPM4 is regulated by phosphatidylinositol 4,5-biphosphate. EMBO J 25:467–478
104. Noguchi N, Yoshikawa T, Ikeda T, Takahashi I, Shervani NJ, Uruno A, Yamauchi A, Nata K, Takasawa S, Okamoto H, Sugawara A (2008) FKBP12.6 disruption impairs glucose-induced insulin secretion. Biochem Biophys Res Commun 371:735–740
105. Oberwinkler J, Lis A, Giehl KM, Flockerzi V, Philipp SE (2005) Alternative splicing switches the divalent cation selectivity of TRPM3 channels. J Biol Chem 280:22540–22548
106. Otsuguro K, Tang J, Tang Y, Xiao R, Freichel M, Tsvilovskyy V, Ito S, Flockerzi V, Zhu MX, Zholos AV (2008) Isoform-specific inhibition of TRPC4 channel by phosphatidylinositol 4,5-bisphosphate. J Biol Chem 283:10026–10036
107. Palmer RK, Atwal K, Bakaj I, Carlucci-Derbyshire S, Buber MT, Cerne R, Cortes RY, Devantier HR, Jorgensen V, Pawlyk A, Lee SP, Sprous DG, Zhang Z, Bryant R (2010) Triphenylphosphine oxide is a potent and selective inhibitor of the transient receptor potential melastatin-5 ion channel. Assay Drug Dev Technol 8:703–713
108. Pinton P, Tsuboi T, Ainscow EK, Pozzan T, Rizzuto R, Rutter GA (2002) Dynamics of glucose induced membrane recruitment of protein kinase C β II in living pancreatic islet β-cells. J Biol Chem 277:37702–37710
109. Prawitt D, Monteilh-Zoller MK, Brixel L, Spangenberg C, Zabel B, Fleig A, Penner R (2003) TRPM5 is a transient Ca2+-activated cation channel responding to rapid changes in [Ca2+]i. Proc Natl Acad Sci USA 100:15166–15171
110. Ravier MA, Guldenagel M, Charollais A, Gjinovci A, Caille D, Sohl G, Wollheim CB, Willecke K, Henquin JC, Meda P (2005) Loss of connexin36 channels alters β-cell coupling, islet synchronization of glucose-induced Ca2+ and insulin oscillations, and basal insulin release. Diabetes 54:1798–1807
111. Ravier MA, Nenquin M, Miki T, Seino S, Henquin JC (2009) Glucose controls cytosolic Ca2+ and insulin secretion in mouse islets lacking adenosine triphosphate-sensitive K+ channels owing to a knockout of the pore-forming subunit Kir6.2. Endocrinology 150:33–45
112. Reinbothe TM, Alkayyali S, Ahlqvist E, Tuomi T, Isomaa B, Lyssenko V, Renstrom E (2013) The human L-type calcium channel Cav1.3 regulates insulin release and polymorphisms in CACNA1D associate with type 2 diabetes. Diabetologia 56:340–349
113. Roe MW, Worley JF III, Qian F, Tamarina N, Mittal AA, Dralyuk F, Blair NT, Mertz RJ, Philipson LH, Dukes ID (1998) Characterization of a Ca2+ release-activated nonselective cation current regulating membrane potential and [Ca2+]i oscillations in transgenically derived β-cells. J Biol Chem 273:10402–10410
114. Rorsman P, Eliasson L, Renstrom E, Gromada J, Barg S, Gopel S (2000) The cell physiology of biphasic insulin secretion. News Physiol Sci 15:72–77
115. Rosker C, Meur G, Taylor EJ, Taylor CW (2009) Functional ryanodine receptors in the plasma membrane of RINm5F pancreatic β-cells. J Biol Chem 284:5186–5194
116. Sakura H, Ashcroft FM (1997) Identification of four trp1 gene variants murine pancreatic β-cells. Diabetologia 40:528–532
117. Schulla V, Renstrom E, Feil R, Feil S, Franklin I, Gjinovci A, Jing XJ, Laux D, Lundquist I, Magnuson MA, Obermuller S, Olofsson CS, Salehi A, Wendt A, Klugbauer N, Wollheim CB, Rorsman P, Hofmann F (2003) Impaired insulin secretion and glucose tolerance in β cell selective Cav1.2 Ca2+ channel null mice. EMBO J 22:3844–3854
118. Schwaller B (2012) The regulation of a cell’s Ca2+ signaling toolkit: the Ca2+ homeostasome. Adv Exp Med Biol 740:1–25
119. Serre-Beinier V, Bosco D, Zulianello L, Charollais A, Caille D, Charpantier E, Gauthier BR, Diaferia GR, Giepmans BN, Lupi R, Marchetti P, Deng S, Buhler L, Berney T, Cirulli V, Meda P (2009) Cx36 makes channels coupling human pancreatic β-cells, and correlates with insulin expression. Hum Mol Genet 18:428–439
120. Shigeto M, Katsura M, Matsuda M, Ohkuma S, Kaku K (2007) Nateglinide and mitiglinide, but not sulfonylureas, induce insulin secretion through a mechanism mediated by calcium release from endoplasmic reticulum. J Pharmacol Exp Ther 322:1–7
121. Song SH, McIntyre SS, Shah H, Veldhuis JD, Hayes PC, Butler PC (2000) Direct measurement of pulsatile insulin secretion from the portal vein in human subjects. J Clin Endocrinol Metab 85:4491–4499
122. Splawski I, Timothy KW, Sharpe LM, Decher N, Kumar P, Bloise R, Napolitano C, Schwartz PJ, Joseph RM, Condouris K, Tager-Flusberg H, Priori SG, Sanguinetti MC, Keating MT (2004) Cav1.2 calcium channel dysfunction causes a multisystem disorder including arrhythmia and autism. Cell 119:19–31
123. Stozer A, Dolensek J, Rupnik MS (2013) Glucose-stimulated calcium dynamics in islets of Langerhans in acute mouse pancreas tissue slices. PLoS One 8:e54638
124. Swatton JE, Morris SA, Cardy TJ, Taylor CW (1999) Type 3 inositol trisphosphate receptors in RINm5F cells are biphasically regulated by cytosolic Ca2+ and mediate quantal Ca2+ mobilization. Biochem J 344(Pt 1):55–60
125. Szollosi A, Nenquin M, Aguilar-Bryan L, Bryan J, Henquin JC (2007) Glucose stimulates Ca2+ influx and insulin secretion in 2-week-old β-cells lacking ATP-sensitive K+ channels. J Biol Chem 282:1747–1756
126. Takahashi N, Mizuno Y, Kozai D, Yamamoto S, Kiyonaka S, Shibata T, Uchida K, Mori Y (2008) Molecular characterization of TRPA1 channel activation by cysteine-reactive inflammatory mediators. Channels (Austin) 2:287–298
127. Takasawa S, Kuroki M, Nata K, Noguchi N, Ikeda T, Yamauchi A, Ota H, Itaya-Hironaka A, Sakuramoto-Tsuchida S, Takahashi I, Yoshikawa T, Shimosegawa T, Okamoto H (2010) A novel ryanodine receptor expressed in pancreatic islets by alternative splicing from type 2 ryanodine receptor gene. Biochem Biophys Res Commun 397:140–145
128. Tarasov AI, Girard CA, Ashcroft FM (2006) ATP sensitivity of the ATP-sensitive K+ channel in intact and permeabilized pancreatic β-cells. Diabetes 55:2446–2454
129. Thore S, Wuttke A, Tengholm A (2007) Rapid turnover of phosphatidylinositol-4,5-bisphosphate in insulin-secreting cells mediated by Ca2+ and the ATP-to-ADP ratio. Diabetes 56:818–826
130. Tian G, Tepikin AV, Tengholm A, Gylfe E (2012) cAMP induces stromal interaction molecule 1 (STIM1) puncta but neither Orai1 protein clustering nor store-operated Ca2+ entry (SOCE) in islet cells. J Biol Chem 287:9862–9872
131. Togashi K, Hara Y, Tominaga T, Higashi T, Konishi Y, Mori Y, Tominaga M (2006) TRPM2 activation by cyclic ADP-ribose at body temperature is involved in insulin secretion. EMBO J 25:1804–1815
132. Trombetta M, Bonetti S, Boselli M, Turrini F, Malerba G, Trabetti E, Pignatti P, Bonora E, Bonadonna RC (2012) CACNA1E variants affect β cell function in patients with newly diagnosed type 2 diabetes. The Verona newly diagnosed type 2 diabetes study (VNDS) 3. PLoS One 7:e32755
133. Uchida K, Dezaki K, Damdindorj B, Inada H, Shiuchi T, Mori Y, Yada T, Minokoshi Y, Tominaga M (2011) Lack of TRPM2 impaired insulin secretion and glucose metabolisms in mice. Diabetes 60:119–126
134. Ullrich ND, Voets T, Prenen J, Vennekens R, Talavera K, Droogmans G, Nilius B (2005) Comparison of functional properties of the Ca2+-activated cation channels TRPM4 and TRPM5 from mice. Cell Calcium 37:267–278
135. Wagner TF, Loch S, Lambert S, Straub I, Mannebach S, Mathar I, Dufer M, Lis A, Flockerzi V, Philipp SE, Oberwinkler J (2008) Transient receptor potential M3 channels are ionotropic steroid receptors in pancreatic β cells. Nat Cell Biol 10:1421–1430
136. Wang X, Zhang X, Dong XP, Samie M, Li X, Cheng X, Goschka A, Shen D, Zhou Y, Harlow J, Zhu MX, Clapham DE, Ren D, Xu H (2012) TPC proteins are phosphoinositide- activated sodium-selective ion channels in endosomes and lysosomes. Cell 151:372–383
137. Woolcott OO, Gustafsson AJ, Dzabic M, Pierro C, Tedeschi P, Sandgren J, Bari MR, Hoa NK, Bianchi M, Rakonjac M, Radmark O, Ostenson CG, Islam MS (2006) Arachidonic acid is a physiological activator of the ryanodine receptor in pancreatic β-cells. Cell Calcium 39:529–537
138. Worley JF III, McIntyre MS, Spencer B, Mertz RJ, Roe MW, Dukes ID (1994) Endoplasmic reticulum calcium store regulates membrane potential in mouse islet β-cells. J Biol Chem 269:14359–14362
139. Xu W, Lipscombe D (2001) Neuronal CaV.3α1 L-type channels activate at relatively hyperpolarized membrane potentials and are incompletely inhibited by dihydropyridines. J Neurosci 21:5944–5951
140. Yue DT, Wier WG (1985) Estimation of intracellular [Ca2+] by nonlinear indicators. A quantitative analysis. Biophys J 48:533–537
141. Zhan X, Yang L, Yi M, Jia Y (2008) RyR channels and glucose-regulated pancreatic β-cells. Eur Biophys J 37:773–782
142. Zhang W, Chu X, Tong Q, Cheung JY, Conrad K, Masker K, Miller BA (2003) A novel TRPM2 isoform inhibits calcium influx and susceptibility to cell death. J Biol Chem 278:16222–16229
143. Zhang Z, Zhang W, Jung DY, Ko HJ, Lee Y, Friedline RH, Lee E, Jun J, Ma Z, Kim F, Tsitsilianos N, Chapman K, Morrison A, Cooper MP, Miller BA, Kim JK (2012) TRPM2 Ca2+ channel regulates energy balance and glucose metabolism. Am J Physiol Endocrinol Metab 302:E807–E816