Generating Mature β-Cells From Embryonic Stem Cells. Strategies for Late-Stage Differentiation.

Vitamins and Hormones

Volumn 87, Issue , 2011, Pages 79-92

  Champeris Tsaniras, Spyridon ^a  

^a Bionetwork Ltd   (Greece)

Author keywords

BMP; Calcineurin; Diabetes; Differentiation; Epac; Hedgehog; Insulin; PI3K; Stem cell; Cell

Indexed keywords

EID: 84857126128     PISSN: 00836729     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-386015-6.00025-1     Document Type: Chapter

References (88)

1. Al-Masri M., Krishnamurthy M., Li J., Fellows G.F., Dong H.H., Goodyer C.G., Wang R. Effect of forkhead box O1 (FOXO1) on beta cell development in the human fetal pancreas. Diabetologia 2010, 53:699-711.
2. Backer J.M., Myers M.G., Sun X.J., Chin D.J., Shoelson S.E., Miralpeix M., White M.F. Association of IRS-1 with the insulin receptor and the phosphatidylinositol 3'-kinase. Formation of binary and ternary signaling complexes in intact cells. J. Biol. Chem. 1993, 268:8204-8212.
3. Barker C.J., Leibiger I.B., Leibiger B., Berggren P.O. Phosphorylated inositol compounds in beta-cell stimulus-response coupling. Am. J. Physiol. Endocrinol. Metab. 2002, 283:E1113-E1122.
4. Beals C.R., Clipstone N.A., Ho S.N., Crabtree G.R. Nuclear localization of NF-ATc by a calcineurin-dependent, cyclosporin-sensitive intramolecular interaction. Genes Dev. 1997, 11:824-834.
5. Biggs W.H., Meisenhelder J., Hunter T., Cavenee W.K., Arden K.C. Protein kinase B/Akt-mediated phosphorylation promotes nuclear exclusion of the winged helix transcription factor FKHR1. Proc. Natl. Acad. Sci. USA 1999, 96:7421-7426.
6. Bluestone J.A., Herold K., Eisenbarth G. Genetics, pathogenesis and clinical interventions in type 1 diabetes. Nature 2010, 464:1293-1300.
7. Blyszczuk P., Wobus A.M. In vitro differentiation of embryonic stem cells into the pancreatic lineage. Methods Mol. Biol. 2007, 330:373-385.
8. Bruno G., Landi A. Epidemiology and costs of diabetes. Transplant. Proc. 2011, 43:327-329.
9. Butler A.A., Yakar S., Gewolb I.H., Karas M., Okubo Y., LeRoith D. Insulin-like growth factor-I receptor signal transduction: At the interface between physiology and cell biology. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 1998, 121:19-26.
10. Centers for Disease Control and Prevention National Diabetes Fact Sheet: National estimates and general information on diabetes and prediabetes in the United States, 2011 2011, [Fact sheet], U.S. Department of Health and Human Services, Centers for Disease Control and Prevention, Atlanta, GA.
11. Champeris Tsaniras S., Jones P.M. Generating pancreatic beta-cells from embryonic stem cells by manipulating signaling pathways. J. Endocrinol. 2010, 206:13-26.
12. Cho Y.M., Lim J.M., Yoo D.H., Kim J.H., Chung S.S., Park S.G., Kim T.H., Oh S.K., Choi Y.M., Moon S.Y., Park K.S., Lee H.K. Betacellulin and nicotinamide sustain PDX1 expression and induce pancreatic beta-cell differentiation in human embryonic stem cells. Biochem. Biophys. Res. Commun. 2008, 366:129-134.
13. Chung W.S., Shin C.H., Stainier D.Y. Bmp2 signaling regulates the hepatic versus pancreatic fate decision. Dev. Cell 2008, 15:738-748.
14. Chung W.S., Andersson O., Row R., Kimelman D., Stainier D.Y. Suppression of Alk8-mediated Bmp signaling cell-autonomously induces pancreatic beta-cells in zebrafish. Proc. Natl. Acad. Sci. USA 2010, 107:1142-1147.
15. Clipstone N.A., Crabtree G.R. Identification of calcineurin as a key signalling enzyme in T-lymphocyte activation. Nature 1992, 357:695-697.
16. Crabtree G.R., Olson E.N. NFAT signaling: Choreographing the social lives of cells. Cell 2002, 109:S67-S79.
17. D'Amour K.A., Bang A.G., Eliazer S., Kelly O.G., Agulnick A.D., Smart N.G., Moorman M.A., Kroon E., Carpenter M.K., Baetge E.E. Production of pancreatic hormone-expressing endocrine cells from human embryonic stem cells. Nat. Biotechnol. 2006, 24:1392-1401.
18. de Rooij J., Zwartkruis F.J., Verheijen M.H., Cool R.H., Nijman S.M., Wittinghofer A., Bos J.L. Epac is a Rap1 guanine-nucleotide-exchange factor directly activated by cyclic AMP. Nature 1998, 396:474-477.
19. Echelard Y., Epstein D.J., St-Jacques B., Shen L., Mohler J., McMahon J.A., McMahon A.P. Sonic Hedgehog, a member of a family of putative signaling molecules, is implicated in the regulation of CNS polarity. Cell 1993, 75:1417-1430.
20. Eiselein L., Schwartz H.J., Rutledge J.C. The challenge of type 1 diabetes mellitus. ILAR J. 2004, 45:231-236.
21. Eliasson L., Ma X., Renström E., Barg S., Berggren P.O., Galvanovskis J., Gromada J., Jing X., Lundquist I., Salehi A., Sewing S., Rorsman P. SUR1 regulates PKA-independent cAMP-induced granule priming in mouse pancreatic B-cells. J. Gen. Physiol. 2003, 121:181-197.
22. Fujimoto K., Shibasaki T., Yokoi N., Kashima Y., Matsumoto M., Sasaki T., Tajima N., Iwanaga T., Seino S. Piccolo, a Ca2+ sensor in pancreatic beta-cells. Involvement of cAMP-GEFII.Rim2. Piccolo complex in cAMP-dependent exocytosis. J. Biol. Chem. 2002, 277:50497-50502.
23. Goulley J., Dahl U., Baeza N., Mishina Y., Edlund H. BMP4-BMPR1A signaling in beta cells is required for and augments glucose-stimulated insulin secretion. Cell Metab. 2007, 5:207-219.
24. Goumans M.J., Mummery C. Functional analysis of the TGFbeta receptor/Smad pathway through gene ablation in mice. Int. J. Dev. Biol. 2000, 44:253-265.
25. Hashiguchi H., Nakazaki M., Koriyama N., Fukudome M., Aso K., Tei C. Cyclic AMP/cAMP-GEF pathway amplifies insulin exocytosis induced by Ca2+ and ATP in rat islet beta-cells. Diabetes Metab. Res. Rev. 2006, 22:64-71.
26. Hebrok M., Kim S.K., Melton D.A. Notochord repression of endodermal Sonic Hedgehog permits pancreas development. Genes Dev. 1998, 12:1705-1713.
27. Hebrok M., Kim S.K., St Jacques B., McMahon A.P., Melton D.A. Regulation of pancreas development by hedgehog signaling. Development 2000, 127:4905-4913.
28. Heit J.J., Apelqvist A.A., Gu X., Winslow M.M., Neilson J.R., Crabtree G.R., Kim S.K. Calcineurin/NFAT signalling regulates pancreatic beta-cell growth and function. Nature 2006, 443:345-349.
29. Holz G.G., Kang G., Harbeck M., Roe M.W., Chepurny O.G. Cell physiology of cAMP sensor Epac. J. Physiol. 2006, 577:5-15.
30. Honegger K.J., Capuano P., Winter C., Bacic D., Stange G., Wagner C.A., Biber J., Murer H., Hernando N. Regulation of sodium-proton exchanger isoform 3 (NHE3) by PKA and exchange protein directly activated by cAMP (EPAC). Proc. Natl. Acad. Sci. USA 2006, 103:803-808.
31. Hori Y., Rulifson I.C., Tsai B.C., Heit J.J., Cahoy J.D., Kim S.K. Growth inhibitors promote differentiation of insulin-producing tissue from embryonic stem cells. Proc. Natl. Acad. Sci. USA 2002, 99:16105-16110.
32. Hua H., Zhang Y.Q., Dabernat S., Kritzik M., Dietz D., Sterling L., Sarvetnick N. BMP4 regulates pancreatic progenitor cell expansion through Id2. J. Biol. Chem. 2006, 281:13574-13580.
33. Hui H., Tang Y., Zhu L., Khoury N., Hui Z., Wang K., Perfetti R., Go V. Glucagon like peptide-1-directed human embryonic stem cells differentiation into insulin-producing cells via Hedgehog, cAMP, and PI3K pathways. Pancreas 2009, 39:315-322.
34. Idevall-Hagren O., Barg S., Gylfe E., Tengholm A. cAMP mediators of pulsatile insulin secretion from glucose-stimulated single beta-cells. J. Biol. Chem. 2010, 285:23007-23018.
35. Ingham P.W., McMahon A.P. Hedgehog signaling in animal development: Paradigms and principles. Genes Dev. 2001, 15:3059-3087.
36. Jacquemin P., Durviaux S.M., Jensen J., Godfraind C., Gradwohl G., Guillemot F., Madsen O.D., Carmeliet P., Dewerchin M., Collen D., Rousseau G.G., Lemaigre F.P. Transcription factor hepatocyte nuclear factor 6 regulates pancreatic endocrine cell differentiation and controls expression of the proendocrine gene ngn3. Mol. Cell. Biol. 2000, 20:4445-4454.
37. Jiang F.X., Stanley E.G., Gonez L.J., Harrison L.C. Bone morphogenetic proteins promote development of fetal pancreas epithelial colonies containing insulin-positive cells. J. Cell Sci. 2002, 115:753-760.
38. Jiang J., Au M., Lu K., Eshpeter A., Korbutt G., Fisk G., Majumdar A.S. Generation of insulin-producing islet-like clusters from human embryonic stem cells. Stem Cells 2007, 25:1940-1953.
39. Jiang W., Shi Y., Zhao D., Chen S., Yong J., Zhang J., Qing T., Sun X., Zhang P., Ding M., Li D., Deng H. In vitro derivation of functional insulin-producing cells from human embryonic stem cells. Cell Res. 2007, 17:333-344.
40. Kaburagi Y., Yamauchi T., Yamamoto-Honda R., Ueki K., Tobe K., Akanuma Y., Yazaki Y., Kadowaki T. The mechanism of insulin-induced signal transduction mediated by the insulin receptor substrate family. Endocr. J. 1999, 46:S25-S34.
41. 2+ release in INS-1 pancreatic beta-cells. J. Physiol. 2001, 536:375-385.
42. Kang G., Joseph J.W., Chepurny O.G., Monaco M., Wheeler M.B., Bos J.L., Schwede F., Genieser H.G., Holz G.G. Epac-selective cAMP analog 8-pCPT-2'-O-Me-cAMP as a stimulus for Ca2+-induced Ca2+ release and exocytosis in pancreatic beta-cells. J. Biol. Chem. 2003, 278(10):8279-8285.
43. Kang G., Chepurny O.G., Malester B., Rindler M.J., Rehmann H., Bos J.L., Schwede F., Coetzee W.A., Holz G.G. cAMP sensor Epac as a determinant of ATP-sensitive potassium channel activity in human pancreatic beta cells and rat INS-1 cells. J. Physiol. 2006, 573:595-609.
44. Kashima Y., Miki T., Shibasaki T., Ozaki N., Miyazaki M., Yano H., Seino S. Critical role of cAMP-GEFII-Rim2 complex in incretin-potentiated insulin secretion. J. Biol. Chem. 2001, 276:46046-46053.
45. Kawahira H., Ma N.H., Tzanakakis E.S., McMahon A.P., Chuang P.T., Hebrok M. Combined activities of hedgehog signaling inhibitors regulate pancreas development. Development 2003, 130:4871-4879.
46. Kawasaki H., Springett G.M., Mochizuki N., Toki S., Nakaya M., Matsuda M., Housman D.E., Graybiel A.M. A family of cAMP-binding proteins that directly activate Rap1. Science 1998, 282:2275-2279.
47. Kiermayer S., Biondi R.M., Imig J., Plotz G., Haupenthal J., Zeuzem S., Piiper A. Epac activation converts cAMP from a proliferative into a differentiation signal in PC12 cells. Mol. Biol. Cell 2005, 16:5639-5648.
48. Kitamura T., Nakae J., Kitamura Y., Kido Y., Biggs W.H., Wright C.V., White M.F., Arden K.C., Accili D. The forkhead transcription factor Foxo1 links insulin signaling to Pdx1 regulation of pancreatic beta cell growth. J. Clin. Invest. 2002, 110:1839-1847.
49. Koblas T., Zacharovova K., Berkova Z., Girman P., Saudek F. An acidic pH and activation of phosphoinositide 3-kinase stimulate differentiation of pancreatic progenitors into insulin-producing cells. Transplant. Proc. 2010, 42:2075-2080.
50. Kops G.J., de Ruiter N.D., De Vries-Smits A.M., Powell D.R., Bos J.L., Burgering B.M. Direct control of the Forkhead transcription factor AFX by protein kinase B. Nature 1999, 398:630-634.
51. Kroon E., Martinson L.A., Kadoya K., Bang A.G., Kelly O.G., Eliazer S., Young H., Richardson M., Smart N.G., Cunningham J., Agulnick A.D., D'Amour K.A., et al. Pancreatic endoderm derived from human embryonic stem cells generates glucose-responsive insulin-secreting cells in vivo. Nat. Biotechnol. 2008, 26:443-452.
52. Ku H.T., Zhang N., Kubo A., O'Connor R., Mao M., Keller G., Bromberg J.S. Committing embryonic stem cells to early endocrine pancreas in vitro. Stem Cells 2004, 22:1205-1217.
53. Kumar M., Jordan N., Melton D., Grapin-Botton A. Signals from lateral plate mesoderm instruct endoderm toward a pancreatic fate. Dev. Biol. 2003, 259:109-122.
54. Lau J., Hebrok M. Hedgehog signaling in pancreas epithelium regulates embryonic organ formation and adult beta-cell function. Diabetes 2010, 59:1211-1221.
55. Lawrence M.C., Bhatt H.S., Watterson J.M., Easom R.A. Regulation of insulin gene transcription by a Ca(2+)-responsive pathway involving calcineurin and nuclear factor of activated T cells. Mol. Endocrinol. 2001, 15:1758-1767.
56. Li H., Lam A., Xu A.M., Lam K.S., Chung S.K. High dosage of Exendin-4 increased early insulin secretion in differentiated beta cells from mouse embryonic stem cells. Acta Pharmacol. Sin. 2010, 31:570-577.
57. Lumelsky N., Blondel O., Laeng P., Velasco I., Ravin R., McKay R. Differentiation of embryonic stem cells to insulin-secreting structures similar to pancreatic islets. Science 2001, 292:1389-1394.
58. Mfopou J.K., Chen B., Mateizel I., Sermon K., Bouwens L. Noggin, retinoids, and fibroblast growth factor regulate hepatic or pancreatic fate of human embryonic stem cells. Gastroenterology 2010, 138:2233-2245.
59. Montrose-Rafizadeh C., Avdonin P., Garant M.J., Rodgers B.D., Kole S., Yang H., Levine M.A., Schwindinger W., Bernier M. Pancreatic glucagon-like peptide-1 receptor couples to multiple G proteins and activates mitogen-activated protein kinase pathways in Chinese hamster ovary cells. Endocrinology 1999, 140:1132-1140.
60. Nohe A., Keating E., Knaus P., Petersen N.O. Signal transduction of bone morphogenetic protein receptors. Cell. Signal. 2004, 16:291-299.
61. Nostro M.C., Sarangi F., Ogawa S., Holtzinger A., Corneo B., Li X., Micallef S.J., Park I.H., Basford C., Wheeler M.B., Daley G.Q., Elefanty A.G., et al. Stage-specific signaling through TGFβ family members and WNT regulates patterning and pancreatic specification of human pluripotent stem cells. Development 2011, 138:861-871.
62. Ohsugi M., Cras-Méneur C., Zhou Y., Warren W., Bernal-Mizrachi E., Permutt M.A. Glucose and insulin treatment of insulinoma cells results in transcriptional regulation of a common set of genes. Diabetes 2004, 53:1496-1508.
63. Onkamo P., Väänänen S., Karvonen M., Tuomilehto J. Worldwide increase in incidence of type I diabetes-The analysis of the data on published incidence trends. Diabetologia 1999, 42:1395-1403.
64. Ozaki N., Shibasaki T., Kashima Y., Miki T., Takahashi K., Ueno H., Sunaga Y., Yano H., Matsuura Y., Iwanaga T., Takai Y., Seino S. cAMP-GEFII is a direct target of cAMP in regulated exocytosis. Nat. Cell Biol. 2000, 2:805-811.
65. Ptasznik A., Beattie G.M., Mally M.I., Cirulli V., Lopez A., Hayek A. Phosphatidylinositol 3-kinase is a negative regulator of cellular differentiation. J. Cell Biol. 1997, 137:1127-1136.
66. Qiu Y., Kung H.J. Signaling network of the Btk family kinases. Oncogene 2000, 19:5651-5661.
67. Redmon J.B., Olson L.K., Armstrong M.B., Greene M.J., Robertson R.P. Effects of tacrolimus (FK506) on human insulin gene expression, insulin mRNA levels, and insulin secretion in HIT-T15 cells. J. Clin. Invest. 1996, 98:2786-2793.
68. Rossi J.M., Dunn N.R., Hogan B.L., Zaret K.S. Distinct mesodermal signals, including BMPs from the septum transversum mesenchyme, are required in combination for hepatogenesis from the endoderm. Genes Dev. 2001, 15:1998-2009.
69. Ryan E.A., Paty B.W., Senior P.A., Bigam D., Alfadhli E., Kneteman N.M., Lakey J.R., Shapiro A.M. Five-year follow-up after clinical islet transplantation. Diabetes 2005, 54:2060-2069.
70. Sabri A., Ziaee A.A., Ostad S.N., Alimoghadam K., Ghahremani M.H. Crosstalk of EGF-directed MAPK signalling pathways and its potential role on EGF-induced cell proliferation and COX-2 expression in human mesenchymal stem cells. Cell Biochem. Funct. 2011, 29:64-70.
71. Schroeder I.S., Rolletschek A., Blyszczuk P., Kania G., Wobus A.M. Differentiation of mouse embryonic stem cells to insulin-producing cells. Nat. Protoc. 2006, 1:495-507.
72. Shapiro A.M., Lakey J.R., Ryan E.A., Korbutt G.S., Toth E., Warnock G.L., Kneteman N.M., Rajotte R.V. Islet transplantation in seven patients with type 1 diabetes mellitus using a glucocorticoid-free immunosuppressive regimen. N. Engl. J. Med. 2000, 343:230-238.
73. Soos M.A., Jensen J., Brown R.A., O'Rahilly S., Shepherd P.R., Whitehead J.P. Class II phosphoinositide 3-kinase is activated by insulin but not by contraction in skeletal muscle. Arch. Biochem. Biophys. 2001, 396:244-248.
74. Soria B., Roche E., Berná G., León-Quinto T., Reig J.A., Martín F. Insulin-secreting cells derived from embryonic stem cells normalize glycemia in streptozotocin-induced diabetic mice. Diabetes 2000, 49:157-162.
75. Spagnoli F.M., Brivanlou A.H. The Gata5 target, TGIF2, defines the pancreatic region by modulating BMP signals within the endoderm. Development 2008, 135:451-461.
76. Stemmer P.M., Klee C.B. Dual calcium ion regulation of calcineurin by calmodulin and calcineurin B. Biochemistry 1994, 33:6859-6866.
77. Talavera-Adame D., Wu G., He Y., Ng T.T., Gupta A., Kurtovic S., Hwang J.Y., Farkas D.L., Dafoe D.C. Endothelial cells in co-culture enhance embryonic stem cell differentiation to pancreatic progenitors and insulin-producing cells through BMP signaling. Stem Cell Rev. 2011, 7:532-543.
78. Thomas M.K., Rastalsky N., Lee J.H., Habener J.F. Hedgehog signaling regulation of insulin production by pancreatic beta-cells. Diabetes 2000, 49:2039-2047.
79. Thomas M.K., Lee J.H., Rastalsky N., Habener J.F. Hedgehog signaling regulation of homeodomain protein islet duodenum homeobox-1 expression in pancreatic beta-cells. Endocrinology 2001, 142:1033-1040.
80. Tsuboi T., da Silva Xavier G., Holz G.G., Jouaville L.S., Thomas A.P., Rutter G.A. Glucagon-like peptide-1 mobilizes intracellular Ca2+ and stimulates mitochondrial ATP synthesis in pancreatic MIN6 beta-cells. Biochem. J. 2003, 369:287-299.
81. Urist M.R. Bone: Formation by autoinduction. Science 1965, 150:893-899.
82. Vanhaesebroeck B., Leevers S.J., Ahmadi K., Timms J., Katso R., Driscoll P.C., Woscholski R., Parker P.J., Waterfield M.D. Synthesis and function of 3-phosphorylated inositol lipids. Annu. Rev. Biochem. 2001, 70:535-602.
83. Varjosalo M., Taipale J. Hedgehog: Functions and mechanisms. Genes Dev. 2008, 22:2454-2472.
84. Wandzioch E., Zaret K.S. Dynamic signaling network for the specification of embryonic pancreas and liver progenitors. Science 2009, 324:1707-1710.
85. Watanabe H., Saito H., Ueda J., Evers B.M. Regulation of pancreatic duct cell differentiation by phosphatidylinositol-3 kinase. Biochem. Biophys. Res. Commun. 2008, 370:33-37.
86. Wozney J.M., Rosen V., Celeste A.J., Mitsock L.M., Whitters M.J., Kriz R.W., Hewick R.M., Wang E.A. Novel regulators of bone formation: Molecular clones and activities. Science 1998, 242:1528-1534.
87. Yew K.H., Hembree M., Prasadan K., Preuett B., McFall C., Benjes C., Crowley A., Sharp S., Tulachan S., Mehta S., Tei E., Gittes G. Cross-talk between bone morphogenetic protein and transforming growth factor-beta signaling is essential for exendin-4-induced insulin-positive differentiation of AR42J cells. J. Biol. Chem. 2005, 280:32209-32217.
88. Zhang D., Jiang W., Liu M., Sui X., Yin X., Chen S., Shi Y., Deng H. Highly efficient differentiation of human ES cells and iPS cells into mature pancreatic insulin-producing cells. Cell Res. 2009, 19:429-438.