Calcium influx activates adenylyl cyclase 8 for sustained insulin secretion in rat pancreatic beta cells

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• 作者：Haiqiang Dou (1) (2) (3) (4) (5)
  Changhe Wang (1) (2) (3) (4) (5)
  Xi Wu (1) (2) (3) (4) (5)
  Lijun Yao (1) (2) (3) (4) (5)
  Xiaoyu Zhang (1) (2) (3) (4) (5)
  Sasa Teng (1) (2) (3) (4) (5)
  Huadong Xu (1) (2) (3) (4) (5)
  Bin Liu (1) (2) (3) (4) (5)
  Qihui Wu (1) (2) (3) (4) (5)
  Quanfeng Zhang (1) (2) (3) (4) (5)
  Meiqin Hu (1) (2) (3) (4) (5)
  Yeshi Wang (1) (2) (3) (4) (5)
  Li Wang (1) (2) (3) (4) (5)
  Yi Wu (1) (3)
  Shujiang Shang (1) (2) (3) (4) (5)
  Xinjiang Kang (1) (2) (3) (4) (5)
  Lianghong Zheng (1) (2) (3) (4) (5)
  Jin Zhang (6)
  Matthieu Raoux (7)
  Jochen Lang (7)
  Qing Li (8)
  Jing Su (8)
  Xiao Yu (8)
  Liangyi Chen (1) (3)
  Zhuan Zhou (1) (2) (3) (4) (5)
  
  1. Institute of Molecular Medicine ; Peking University ; 5 Yiheyuan Road ; Beijing ; 100871 ; China
  2. State Key Laboratory of Biomembrane and Membrane Biotechnology ; Peking University ; Beijing ; People鈥檚 Republic of China
  3. Beijing Key Laboratory of Cardiometabolic Molecular Medicine ; Peking University ; Beijing ; People鈥檚 Republic of China
  4. PKU-IDG/McGovern Institute for Brain Research ; Peking University ; Beijing ; People鈥檚 Republic of China
  5. Peking-Tsinghua Centre for Life Sciences ; Peking University ; Beijing ; People鈥檚 Republic of China
  6. Department of Pharmacology and Molecular Sciences ; The Johns Hopkins University School of Medicine ; Baltimore ; MD ; USA
  7. Universit茅 de Bordeaux I Institut Europ茅en de Chimie et Biologie UMR CNRS 5248 ; Bordeaux ; France
  8. Department of Physiology ; Shandong University School of Medicine ; 44 Wenhua Xi Road ; Jinan ; 250012 ; People鈥檚 Republic of China
  
• 关键词：Adenylyl cyclase 8 ; Ca2+ ; Pancreatic beta cell ; Protein kinase A ; Vesicle pool
• 刊名：Diabetologia
• 出版年：2015
• 出版时间：February 2015
• 年：2015
• 卷：58
• 期：2
• 页码：324-333
• 全文大小：1,309 KB
• 参考文献：1. Tarasov AI, Semplici F, Ravier MA et al (2012) The mitochondrial Ca2+ uniporter MCU is essential for glucose-induced ATP increases in pancreatic beta-cells. Plos One 7:e39722
  2. Ashcroft FM, Rorsman P (2012) Diabetes mellitus and the beta cell: the last ten years. Cell 148:1160鈥?171 CrossRef
  3. Zhou Z, Misler S (1996) Amperometric detection of quantal secretion from patch-clamped rat pancreatic beta-cells. J Biol Chem 271:270鈥?77 CrossRef
  4. Renstrom E, Eliasson L, Rorsman P (1997) Protein kinase A-dependent and -independent stimulation of exocytosis by cAMP in mouse pancreatic B cells. J Physiol 502(Pt 1):105鈥?18 CrossRef
  5. Eliasson L, Ma X, Renstrom E et al (2003) SUR1 regulates PKA-independent cAMP-induced granule priming in mouse pancreatic B cells. J Gen Physiol 121:181鈥?97 CrossRef
  6. Shibasaki T, Takahashi H, Miki T et al (2007) Essential role of Epac2/Rap1 signaling in regulation of insulin granule dynamics by cAMP. Proc Natl Acad Sci U S A 104:19333鈥?9338 CrossRef
  7. Gremlich S, Porret A, Hani EH et al (1995) Cloning, functional expression, and chromosomal localization of the human pancreatic islet glucose-dependent insulinotropic polypeptide receptor. Diabetes 44:1202鈥?208 44.10.1202" target="_blank" title="It opens in new window">CrossRef
  8. Thorens B (1992) Expression cloning of the pancreatic beta cell receptor for the gluco-incretin hormone glucagon-like peptide 1. Proc Natl Acad Sci U S A 89:8641鈥?645 CrossRef
  9. Grill V, Cerasi E (1973) Activation by glucose of adenyl cyclase in pancreatic islets of the rat. FEBS Lett 33:311鈥?14 CrossRef
  10. Ramos LS, Zippin JH, Kamenetsky M, Buck J, Levin LR (2008) Glucose and GLP-1 stimulate cAMP production via distinct adenylyl cyclases in INS-1E insulinoma cells. J Gen Physiol 132:329鈥?38 44" target="_blank" title="It opens in new window">CrossRef
  11. Dyachok O, Idevall-Hagren O, Sagetorp J et al (2008) Glucose-induced cyclic AMP oscillations regulate pulsatile insulin secretion. Cell Metab 8:26鈥?7 CrossRef
  12. Hodson DJ, Mitchell RK, Marselli L et al (2014) ADCY5 couples glucose to insulin secretion in human islets. Diabetes 63:3009鈥?021 CrossRef
  13. Delmeire D, Flamez D, Hinke SA, Cali JJ, Pipeleers D, Schuit F (2003) Type VIII adenylyl cyclase in rat beta cells: coincidence signal detector/generator for glucose and GLP-1. Diabetologia 46:1383鈥?393 CrossRef
  14. Landa LR Jr, Harbeck M, Kaihara K et al (2005) Interplay of Ca2+ and cAMP signaling in the insulin-secreting MIN6 beta-cell line. J Biol Chem 280:31294鈥?1302 CrossRef
  15. Ni Q, Ganesan A, Aye-Han NN et al (2011) Signaling diversity of PKA achieved via a Ca2+-cAMP-PKA oscillatory circuit. Nat Chem Biol 7:34鈥?0 CrossRef
  16. De Marinis YZ, Salehi A, Ward CE et al (2010) GLP-1 inhibits and adrenaline stimulates glucagon release by differential modulation of N- and L-type Ca2+ channel-dependent exocytosis. Cell Metab 11:543鈥?53 CrossRef
  17. Kamp TJ, Hell JW (2000) Regulation of cardiac L-type calcium channels by protein kinase A and protein kinase C. Circ Res 87:1095鈥?102 CrossRef
  18. Kang G, Chepurny OG, Rindler MJ et al (2005) A cAMP and Ca2+ coincidence detector in support of Ca2+-induced Ca2+ release in mouse pancreatic beta cells. J Physiol 566:173鈥?88 CrossRef
  19. Dyachok O, Gylfe E (2004) Ca(2+)-induced Ca(2+) release via inositol 1,4,5-trisphosphate receptors is amplified by protein kinase A and triggers exocytosis in pancreatic beta-cells. J Biol Chem 279:45455鈥?5461 CrossRef
  20. Idevall-Hagren O, Barg S, Gylfe E, Tengholm A (2010) cAMP mediators of pulsatile insulin secretion from glucose-stimulated single beta-cells. J Biol Chem 285:23007鈥?3018 CrossRef
  21. Kim JW, Roberts CD, Berg SA, Caicedo A, Roper SD, Chaudhari N (2008) Imaging cyclic AMP changes in pancreatic islets of transgenic reporter mice. PLoS One 3:e2127 CrossRef
  22. Zhang J, Ma Y, Taylor SS, Tsien RY (2001) Genetically encoded reporters of protein kinase A activity reveal impact of substrate tethering. Proc Natl Acad Sci U S A 98:14997鈥?5002 CrossRef
  23. Lou XL, Yu X, Chen XK et al (2003) Na+ channel inactivation: a comparative study between pancreatic islet beta-cells and adrenal chromaffin cells in rat. J Physiol 548:191鈥?02 4405" target="_blank" title="It opens in new window">CrossRef
  24. Zhang C, Zhou Z (2002) Ca(2+)-independent but voltage-dependent secretion in mammalian dorsal root ganglion neurons. Nat Neurosci 5:425鈥?30
  25. Dou HQ, Xu YF, Sun JP et al (2012) Thiopental-induced insulin secretion via activation of IP3-sensitive calcium stores in rat pancreatic beta-cells. Am J Physiol Cell Physiol 302:C796鈥揅803 CrossRef
  26. Rorsman P (1997) The pancreatic beta-cell as a fuel sensor: an electrophysiologist鈥檚 viewpoint. Diabetologia 40:487鈥?95 CrossRef
  27. Willoughby D, Cooper DM (2007) Organization and Ca2+ regulation of adenylyl cyclases in cAMP microdomains. Physiol Rev 87:965鈥?010 CrossRef
  28. Roger B, Papin J, Vacher P et al (2011) Adenylyl cyclase 8 is central to glucagon-like peptide 1 signalling and effects of chronically elevated glucose in rat and human pancreatic beta cells. Diabetologia 54:390鈥?02 CrossRef
  29. Merrins MJ, Stuenkel EL (2008) Kinetics of Rab27a-dependent actions on vesicle docking and priming in pancreatic beta-cells. J Physiol 586:5367鈥?381 CrossRef
  30. Zhang X, Candas M, Griko NB, Taussig R, Bulla LA Jr (2006) A mechanism of cell death involving an adenylyl cyclase/PKA signaling pathway is induced by the Cry1Ab toxin of Bacillus thuringiensis. Proc Natl Acad Sci U S A 103:9897鈥?902 CrossRef
  31. Katz B (1969) The release of neural transmitter substances. Liverpool University Press, Liverpool
  32. Neher E, Sakaba T (2008) Multiple roles of calcium ions in the regulation of neurotransmitter release. Neuron 59:861鈥?72 CrossRef
  33. Sudhof TC (2004) The synaptic vesicle cycle. Annu Rev Neurosci 27:509鈥?47 CrossRef
  34. Ammala C, Ashcroft FM, Rorsman P (1993) Calcium-independent potentiation of insulin release by cyclic AMP in single beta-cells. Nature 363:356鈥?58 CrossRef
  35. Gustavsson N, Lao Y, Maximov A et al (2008) Impaired insulin secretion and glucose intolerance in synaptotagmin-7 null mutant mice. Proc Natl Acad Sci U S A 105:3992鈥?997 CrossRef
  36. Michael DJ, Ritzel RA, Haataja L, Chow RH (2006) Pancreatic beta-cells secrete insulin in fast- and slow-release forms. Diabetes 55:600鈥?07 CrossRef
  37. von Ruden L, Neher E (1993) A Ca-dependent early step in the release of catecholamines from adrenal chromaffin cells. Science 262:1061鈥?065 CrossRef
  38. Zhang B, Sun L, Yang YM et al (2011) Action potential bursts enhance transmitter release at a giant central synapse. J Physiol 589:2213鈥?227 CrossRef
  39. Everett KL, Cooper DM (2013) An improved targeted cAMP sensor to study the regulation of adenylyl cyclase 8 by Ca2+ entry through voltage-gated channels. PLoS One 8:e75942 CrossRef
  40. Tian G, Sandler S, Gylfe E, Tengholm A (2011) Glucose- and hormone-induced cAMP oscillations in alpha- and beta-cells within intact pancreatic islets. Diabetes 60:1535鈥?543 CrossRef
  41. Willoughby D, Masada N, Wachten S et al (2010) AKAP79/150 interacts with AC8 and regulates Ca2+-dependent cAMP synthesis in pancreatic and neuronal systems. J Biol Chem 285:20328鈥?0342 CrossRef
  42. Leech CA, Castonguay MA, Habener JF (1999) Expression of adenylyl cyclase subtypes in pancreatic beta-cells. Biochem Biophys Res Commun 254:703鈥?06 CrossRef
  43. Fonseca SG, Urano F, Weir GC, Gromada J, Burcin M (2012) Wolfram syndrome 1 and adenylyl cyclase 8 interact at the plasma membrane to regulate insulin production and secretion. Nat Cell Biol 14:1105鈥?112 CrossRef
  44. Takahashi N, Kishimoto T, Nemoto T, Kadowaki T, Kasai H (2002) Fusion pore dynamics and insulin granule exocytosis in the pancreatic islet. Science 297:1349鈥?352 CrossRef
  
• 刊物类别：Medicine
• 刊物主题：Medicine & Public Health
  Internal Medicine
  Metabolic Diseases
  Human Physiology
  
• 出版者：Springer Berlin / Heidelberg
• ISSN：1432-0428

文摘

Aims/hypothesis Insulin is a key metabolic regulator in health and diabetes. In pancreatic beta cells, insulin release is regulated by the major second messengers Ca2+ and cAMP: exocytosis is triggered by Ca2+ and mediated by the cAMP/protein kinase A (PKA) signalling pathway. However, the causal link between these two processes in primary beta cells remains undefined. Methods Time-resolved confocal imaging of fluorescence resonance energy transfer signals was performed to visualise PKA activity, and combined membrane capacitance recordings were used to monitor insulin secretion from patch-clamped rat beta cells. Results Membrane depolarisation-induced Ca2+ influx caused an increase in cytosolic PKA activity via activating a Ca2+-sensitive adenylyl cyclase 8 (ADCY8) subpool. Glucose stimulation triggered coupled Ca2+ oscillations and PKA activation. ADCY8 knockdown significantly reduced the level of depolarisation-evoked PKA activation and impaired replenishment of the readily releasable vesicle pool. Pharmacological inhibition of PKA by two inhibitors reduced depolarisation-induced PKA activation to a similar extent and reduced the capacity for sustained vesicle exocytosis and insulin release. Conclusions/interpretation Our findings suggest that depolarisation-induced Ca2+ influx plays dual roles in regulating exocytosis in rat pancreatic beta cells by triggering vesicle fusion and replenishing the vesicle pool to support sustained insulin release. Therefore, Ca2+ influx may be important for glucose-stimulated insulin secretion.