Pancreatic β-cell signaling: Toward better understanding of diabetes and its treatment

Proceedings of the Japan Academy Series B: Physical and Biological Sciences

Volumn 86, Issue 6, 2010, Pages 563-577

  Seino, Susumu ^a,b   Shibasaki, Tadao ^a   Minami, Kohtaro ^a  

^a KOBE UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

cAMP; Cell signaling; Epac2; Insulin; Pancreatic acinar cell; Transdifferentiation

Indexed keywords

CYCLIC AMP; INSULIN;

ANIMAL; DIABETES MELLITUS; HUMAN; METABOLISM; PANCREAS; PANCREAS ISLET BETA CELL; PATHOLOGY; REVIEW; SECRETION; SIGNAL TRANSDUCTION;

ANIMALS; CYCLIC AMP; DIABETES MELLITUS; HUMANS; INSULIN; INSULIN-SECRETING CELLS; PANCREAS, EXOCRINE; SIGNAL TRANSDUCTION;

EID: 77955120393     PISSN: 03862208     EISSN: 13492896     Source Type: Journal    
DOI: 10.2183/pjab.86.563     Document Type: Review

References (88)

1. International Diabetes Atlas, http://www.diabetesatlas.org/
2. 2+, cAMP, and phospholipid-derived messengers in coupling mechanisms of insulin secretion. Physiol. Rev. 67, 1185-1248.
3. Wollheim, C.B. and Sharp, G.W. (1981) Regulation of insulin release by calcium. Physiol. Rev. 61, 914-973.
4. Ashcroft, F.M. (1988) Adenosine 5'-triphosphatesensitive potassium channels. Annu. Rev. Neurosci. 11, 97-118.
5. Ohara-Imaizumi, M., Nakamichi, Y., Tanaka, T., Ishida, H. and Nagamatsu, S. (2002) Imaging exocytosis of single insulin secretory granules with evanescent wave microscopy: distinct behavior of granule motion in biphasic insulin release. J. Biol. Chem. 277, 3805-3808.
6. Shibasaki, T., Takahashi, H., Miki, T., Sunaga, Y., Matsumura, K., Yamanaka, M. et al. (2007) Essential role of Epac2/Rap1 signaling in regulation of insulin granule dynamics by cAMP. Proc. Natl. Acad. Sci. USA 104, 19333-19338.
7. Kasai, K., Fujita, T., Gomi, H. and Izumi, T. (2008) Docking is not a prerequisite but a temporal constraint for fusion of secretory granules. Traffic 9, 1191-1203.
8. Rorsman, P. and Renstrom, E. (2003) Insulin granule dynamics in pancreatic β cells. Diabetologia 46, 1029-1045.
9. Eliasson, L., Abdulkader, F., Braun, M., Galvanovskis, J., Hoppa, M.B. and Rorsman, P. (2008) Novel aspects of the molecular mechanisms controlling insulin secretion. J. Physiol. 586, 3313-3324.
10. Seino, S., Takahashi, H., Fujimoto, W. and Shibasaki, T. (2009) Roles of cAMP signalling in insulin granule exocytosis. Diabetes Obes. Metab. 11, 180-188.
11. McIntyre, N., Holdsworth, C.D. and Turner, D.S. (1964) New interpretation of oral glucose tolerance. Lancet 2, 20-21.
12. Elrick, H., Stimmler, L., Hlad, C.J. Jr. and Arai, Y. (1964) Plasma insulin response to oral and intravenous glucose administration. J. Clin. Endocrinol. Metab. 24, 1076-1082.
13. Bell, G.I., Santerre, R.F. and Mullenbach, G.T. (1983) Hamster preproglucagon contains the sequence of glucagon and two related peptides. Nature 302, 716-718.
14. Brown, J.C., Mutt, V. and Pederson, R.A. (1970) Further purification of a polypeptide demonstrating enterogastrone activity. J. Physiol. 209, 57-64.
15. Elliott, R.M., Morgan, L.M., Tredger, J.A., Deacon, S., Wright, J. and Marks, V. (1993) Glucagon-like peptide-1 (7-36)amide and glucose-dependent insulinotropic polypeptide secretion in response to nutrient ingestion in man: acute post-prandial and 24-h secretion patterns. J. Endocrinol. 138, 159-166.
16. Dupre, J., Ross, S.A., Watson, D. and Brown, J.C. (1973) Stimulation of insulin secretion by gastric inhibitory polypeptide in man. J. Clin. Endocrinol. Metab. 37, 826-828.
17. Thorens, B. (1992) Expression cloning of the pancreatic β cell receptor for the gluco-incretin hormone glucagon-like peptide 1. Proc. Natl. Acad. Sci. USA 89, 8641-8645.
18. Usdin, T.B., Mezey, E., Button, D.C., Brownstein, M.J. and Bonner, T.I. (1993) Gastric inhibitory polypeptide receptor, a member of the secretin-vasoactive intestinal peptide receptor family, is widely distributed in peripheral organs and the brain. Endocrinology 133, 2861-2870.
19. Yasuda, K., Inagaki, N., Yamada, Y., Kubota, A., Seino, S. and Seino, Y. (1994) Hamster gastric inhibitory polypeptide receptor expressed in pancreatic islets and clonal insulin-secreting cells: its structure and functional properties. Biochem. Biophys. Res. Commun. 205, 1556-1562.
20. Holst, J.J. and Gromada, J. (2004) Role of incretin hormones in the regulation of insulin secretion in diabetic and nondiabetic humans. Am. J. Physiol. Endocrinol. Metab. 287, E199-E206.
21. Miki, T., Minami, K., Shinozaki, H., Matsumura, K., Saraya, A., Ikeda, H. et al. (2005) Distinct effects of glucose-dependent insulinotropic polypeptide and glucagon-like peptide-1 on insulin secretion and gut motility. Diabetes 54, 1056-1063.
22. Fujimoto, W., Miki, T., Ogura, T., Zhang, M., Seino, Y., Satin, L.S. et al. (2009) Niflumic acid-sensitive ion channels play an important role in the induction of glucose-stimulated insulin secretion by cyclic AMP in mice. Diabetologia 52, 863-872.
23. + channels in mouse B cells. J. Clin. Invest. 91, 871-880.
24. Vilsboll, T., Krarup, T., Madsbad, S. and Holst, J.J. (2003) Both GLP-1 and GIP are insulinotropic at basal and postprandial glucose levels and contribute nearly equally to the incretin effect of a meal in healthy subjects. Regul. Pept. 114, 115-121.
25. Holz, G.G.t., Kuhtreiber, W.M. and Habener, J.F. (1993) Pancreatic β-cells are rendered glucose-competent by the insulinotropic hormone glucagon-like peptide-1(7-37). Nature 361, 362-365.
26. Suzuki, H., Fukushima, M., Okamoto, S., Takahashi, O., Shimbo, T., Kurose, T. et al. (2005) Effects of thorough mastication on postprandial plasma glucose concentrations in nonobese Japanese subjects. Metabolism 54, 1593-1599.
27. Seino, S. and Shibasaki, T. (2005) PKA-dependent and PKA-independent pathways for cAMP-regulated exocytosis. Physiol. Rev. 85, 1303-1342.
28. Malaisse, W.J. and Malaisse-Lagae, F. (1984) The role of cyclic AMP in insulin release. Experientia 40, 1068-1074.
29. Jones, P.M. and Persaud, S.J. (1998) Protein kinases, protein phosphorylation, and the regulation of insulin secretion from pancreatic β-cells. Endocr. Rev. 19, 429-461.
30. Eliasson, L., Ma, X., Renstrom, E., Barg, S., Berggren, P.O., Galvanovskis, J. et al. (2003) SUR1 regulates PKA-independent cAMP-induced granule priming in mouse pancreatic B-cells. J. Gen. Physiol. 121, 181-197.
31. Ozaki, N., Shibasaki, T., Kashima, Y., Miki, T., Takahashi, K., Ueno, H. et al. (2000) cAMP-GEFII is a direct target of cAMP in regulated exocytosis. Nat. Cell Biol. 2, 805-811.
32. Bos, J.L. (2006) Epac proteins: multi-purpose cAMP targets. Trends Biochem. Sci. 31, 680-686.
33. de Rooij, J., Zwartkruis, F.J., Verheijen, M.H., Cool, R.H., Nijman, S.M., Wittinghofer, A. et al. (1998) Epac is a Rap1 guanine-nucleotide-exchange factor directly activated by cyclic AMP. Nature 396, 474-477.
34. Kawasaki, H., Springett, G.M., Mochizuki, N., Toki, S., Nakaya, M., Matsuda, M. et al. (1998) A family of cAMP-binding proteins that directly activate Rap1. Science 282, 2275-2279.
35. de Rooij, J., Rehmann, H., van Triest, M., Cool, R.H., Wittinghofer, A. and Bos, J.L. (2000) Mechanism of regulation of the Epac family of cAMP-dependent RapGEFs. J. Biol. Chem. 275, 20829-20836.
36. Niimura, M., Miki, T., Shibasaki, T., Fujimoto, W., Iwanaga, T. and Seino, S. (2009) Critical role of the N-terminal cyclic AMP-binding domain of Epac2 in its subcellular localization and function. J. Cell. Physiol. 219, 652-658.
37. Ueno, H., Shibasaki, T., Iwanaga, T., Takahashi, K., Yokoyama, Y., Liu, L.M. et al. (2001) Characterization of the gene EPAC2: structure, chromosomal localization, tissue expression, and identification of the liver-specific isoform. Genomics 78, 91-98.
38. Rehmann, H., Das, J., Knipscheer, P., Wittinghofer, A. and Bos, J.L. (2006) Structure of the cyclic-AMP-responsive exchange factor Epac2 in its auto-inhibited state. Nature 439, 625-628.
39. Kashima, Y., Miki, T., Shibasaki, T., Ozaki, N., Miyazaki, M., Yano, H. et al. (2001) Critical role of cAMP-GEFII-Rim2 complex in incretin-potentiated insulin secretion. J. Biol. Chem. 276, 46046-46053.
40. + channels in cardiac muscle. Nature 305, 147-148.
41. Sturgess, N.C., Ashford, M.L., Cook, D.L. and Hales, C.N. (1985) The sulphonylurea receptor may be an ATP-sensitive potassium channel. Lancet 2, 474-475.
42. Aguilar-Bryan, L., Nichols, C.G., Wechsler, S.W., Clement, J.P.t., Boyd, A.E. 3rd, Gonzalez, G. et al. (1995) Cloning of the β cell high-affinity sulfonylurea receptor: a regulator of insulin secretion. Science 268, 423-426.
43. ATP: an inward rectifier subunit plus the sulfonylurea receptor. Science 270, 1166-1170.
44. Inagaki, N., Tsuura, Y., Namba, N., Masuda, K., Gonoi, T., Horie, M. et al. (1995) Cloning and functional characterization of a novel ATP-sensitive potassium channel ubiquitously expressed in rat tissues, including pancreatic islets, pituitary, skeletal muscle, and heart. J. Biol. Chem. 270, 5691-5694.
45. Aguilar-Bryan, L. and Bryan, J. (1999) Molecular biology of adenosine triphosphate-sensitive potassium channels. Endocr. Rev. 20, 101-135.
46. Seino, S. (1999) ATP-sensitive potassium channels: a model of heteromultimeric potassium channel/receptor assemblies. Annu. Rev. Physiol. 61, 337-362.
47. + channels. Prog. Biophys. Mol. Biol. 81, 133-176.
48. Ashcroft, F.M. (2005) ATP-sensitive potassium channelopathies: focus on insulin secretion. J. Clin. Invest. 115, 2047-2058.
49. + channels in the hypothalamus are essential for the maintenance of glucose homeostasis. Nat. Neurosci. 4, 507-512.
50. Yamada, K., Ji, J.J., Yuan, H., Miki, T., Sato, S., Horimoto, N. et al. (2001) Protective role of ATP-sensitive potassium channels in hypoxia-induced generalized seizure. Science 292, 1543-1546.
51. ATP channels in cardioprotection against ischemia/reperfusion injury in mice. J. Clin. Invest. 109, 509-516.
52. ATP channel-deficient mice. Proc. Natl. Acad. Sci. USA 95, 10402-10406.
53. ATP channel-independent regulation of insulin secretion. J. Biol. Chem. 275, 9270-9277.
54. Zhang, C.L., Katoh, M., Shibasaki, T., Minami, K., Sunaga, Y., Takahashi, H. et al. (2009) The cAMP sensor Epac2 is a direct target of antidiabetic sulfonylurea drugs. Science 325, 607-610.
55. Soria, B., Roche, E., Berná, G., León-Quinto, T., Reig, J.A. and Martín, F. (2000) Insulin-secreting cells derived from embryonic stem cells normalize glycemia in streptozotocin-induced diabetic mice. Diabetes 49, 157-162.
56. Lumelsky, N., Blondel, O., Laeng, P., Velasco, I., Ravin, R. and McKay, R. (2001) Differentiation of embryonic stem cells to insulin-secreting structures similar to pancreatic islets. Science 292, 1389-1394.
57. Assady, S., Maor, G., Amit, M., Itskovitz-Eldor, J., Skorecki, K.L. and Tzukerman, M. (2001) Insulin production by human embryonic stem cells. Diabetes 50, 1691-1697.
58. D'Amour, K.A., Bang, A.G., Eliazer, S., Kelly, O.G., Agulnick, A.D., Smart, N.G. et al. (2006) Production of pancreatic hormone-expressing endocrine cells from human embryonic stem cells. Nat. Biotechnol. 24, 1392-1401.
59. Odorico, J.S., Kaufman, D.S. and Thomson, J.A. (2001) Multilineage differentiation from human embryonic stem cell lines. Stem Cells 19, 193-204.
60. McLaren, A. (2001) Ethical and social considerations of stem cell research. Nature 414, 129-131.
61. Rajagopal, J., Anderson, W.J., Kume, S., Martinez, O.I. and Melton, D.A. (2003) Insulin staining of ES cell progeny from insulin uptake. Science 299, 363.
62. Hansson, M., Tonning, A., Frandsen, U., Petri, A., Rajagopal, J., Englund, M.C. et al. (2004) Arti-factual insulin release from differentiated embryonic stem cells. Diabetes 53, 2603-2609.
63. Ramiya, V.K., Maraist, M., Arfors, K.E., Schatz, D.A., Peck, A.B. and Cornelius, J.G. (2000) Reversal of insulin-dependent diabetes using islets generated in vitro from pancreatic stem cells. Nat. Med. 6, 278-282.
64. Bonner-Weir, S., Taneja, M., Weir, G.C., Tatarkiewicz, K., Song, K.H., Sharma, A. et al. (2000) In vitro cultivation of human islets from expanded ductal tissue. Proc. Natl. Acad. Sci. USA 97, 7999-8004.
65. Yang, L., Li, S., Hatch, H., Ahrens, K., Cornelius, J.G., Petersen, B.E. et al. (2002) In vitro trans-differentiation of adult hepatic stem cells into pancreatic endocrine hormone-producing cells. Proc. Natl. Acad. Sci. USA 99, 8078-8083.
66. Gao, R., Ustinov, J., Pulkkinen, M.A., Lundin, K., Korsgren, O. and Otonkoski, T. (2003) Characterization of endocrine progenitor cells and critical factors for their differentiation in human adult pancreatic cell culture. Diabetes 52, 2007-2015.
67. Tang, D.Q., Cao, L.Z., Burkhardt, B.R., Xia, C.Q., Litherland, S.A., Atkinson, M.A. et al. (2004) In vivo and in vitro characterization of insulin-producing cells obtained from murine bone marrow. Diabetes 53, 1721-1732.
68. Takahashi, K. and Yamanaka, S. (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126, 663-676.
69. Tateishi, K., He, J., Taranova, O., Liang, G., D'Alessio, A.C. and Zhang, Y. (2008) Generation of insulin-secreting islet-like clusters from human skin fibroblasts. J. Biol. Chem. 283, 31601-31607.
70. Shen, C.N., Slack, J.M. and Tosh, D. (2000) Molecular basis of transdifferentiation of pancreas to liver. Nat. Cell Biol. 2, 879-887.
71. Slack, J.M. and Tosh, D. (2001) Transdifferentiation and metaplasia-switching cell types. Curr. Opin. Genet. Dev. 11, 581-586.
72. Tosh, D. and Slack, J.M. (2002) How cells change their phenotype. Nat. Rev. Mol. Cell Biol. 3, 187-194.
73. Yeung, R.S., Weese, J.L., Hoffman, J.P., Solin, L.J., Paul, A.R., Engstrom, P.F. et al. (1993) Neo-adjuvant chemoradiation in pancreatic and duodenal carcinoma. A phase II study. Cancer 72, 2124-2133.
74. Rao, M.S., Dwivedi, R.S., Subbarao, V., Usman, M.I., Scarpelli, D.G., Nemali, M.R. et al. (1988) Almost total conversion of pancreas to liver in the adult rat: a reliable model to study transdifferentiation. Biochem. Biophys. Res. Commun. 156, 131-136.
75. Dabeva, M.D., Hwang, S.G., Vasa, S.R., Hurston, E., Novikoff, P.M., Hixson, D.C. et al. (1997) Differentiation of pancreatic epithelial progenitor cells into hepatocytes following transplantation into rat liver. Proc. Natl. Acad. Sci. USA 94, 7356-7361.
76. Song, K.H., Ko, S.H., Ahn, Y.B., Yoo, S.J., Chin, H.M., Kaneto, H. et al. (2004) In vitro trans-differentiation of adult pancreatic acinar cells into insulin-expressing cells. Biochem. Biophys. Res. Commun. 316, 1094-1100.
77. Baeyens, L., De Breuck, S., Lardon, J., Mfopou, J.K., Rooman, I. and Bouwens, L. (2005) In vitro generation of insulin-producing beta cells from adult exocrine pancreatic cells. Diabetologia 48, 49-57.
78. Minami, K., Okuno, M., Miyawaki, K., Okumachi, A., Ishizaki, K., Oyama, K. et al. (2005) Lineage tracing and characterization of insulin-secreting cells generated from adult pancreatic acinar cells. Proc. Natl. Acad. Sci. USA 102, 15116-15121.
79. Srinivas, S., Watanabe, T., Lin, C.S., William, C.M., Tanabe, Y., Jessell, T.M. et al. (2001) Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev. Biol. 1, 4.
80. Okuno, M., Minami, K., Okumachi, A., Miyawaki, K., Yokoi, N., Toyokuni, S. et al. (2007) Generation of insulin-secreting cells from pancreatic acinar cells of animal models of type 1 diabetes. Am. J. Physiol. Endocrinol. Metab. 292, E158-E165.
81. Edlund, H. (2002) Pancreatic organogenesis-developmental mechanisms and implications for therapy. Nat. Rev. Genet. 3, 524-532.
82. Sund, N.J., Vatamaniuk, M.Z., Casey, M., Ang, S.L., Magnuson, M.A., Stoffers, D.A. et al. (2001) Tissue-specific deletion of Foxa2 in pancreatic beta cells results in hyperinsulinemic hypoglycemia. Genes Dev. 15, 1706-1715.
83. Rausa, F., Samadani, U., Ye, H., Lim, L., Fletcher, C.F., Jenkins, N.A. et al. (1997) The cut-homeodomain transcriptional activator HNF-6 is coexpressed with its target gene HNF-3 beta in the developing murine liver and pancreas. Dev. Biol. 192, 228-246.
84. Krapp, A., Knöfler, M., Ledermann, B., Bürki, K., Berney, C., Zoerkler, N. et al. (1998) The bHLH protein PTF1-p48 is essential for the formation of the exocrine and the correct spatial organization of the endocrine pancreas. Genes Dev. 12, 3752-3763.
85. Kawaguchi, Y., Cooper, B., Gannon, M., Ray, M., MacDonald, R.J. and Wright, C.V. (2002) The role of the transcriptional regulator Ptf1a in converting intestinal to pancreatic progenitors. Nat. Genet. 32, 128-134.
86. Cras-Méneur, C., Elghazi, L., Czernichow, P. and Scharfmann, R. (2001) Epidermal growth factor increases undifferentiated pancreatic embryonic cells in vitro: a balance between proliferation and differentiation. Diabetes 50, 1571-1579.
87. Minami, K., Okano, H., Okumachi, A. and Seino, S. (2008) Role of cadherin-mediated cell-cell adhesion in pancreatic exocrine-to-endocrine transdifferentiation. J. Biol. Chem. 283, 13753-13761.
88. Desai, B.M., Oliver-Krasinski, J., De Leon, D.D., Farzad, C., Hong, N., Leach, S.D. et al. (2007) Preexisting pancreatic acinar cells contribute to acinar cell, but not islet beta cell, regeneration. J. Clin. Invest. 117, 971-977.