Differentiation of stem cells into insulin-producing cells: Current status and challenges

Archivum Immunologiae et Therapiae Experimentalis

Volumn 61, Issue 2, 2013, Pages 149-158

  Pokrywczynska, Marta ^a   Krzyzanowska, Sandra ^a   Jundzill, Arkadiusz ^a   Adamowicz, Jan ^a   Drewa, Tomasz ^a,b  

^a NICOLAUS COPERNICUS UNIVERSITY   (Poland)

^b Nicolaus Copernicus Hospital   (Poland)

Author keywords

Diabetes mellitus; Differentiation; Insulin producing cells; Stem cells

Indexed keywords

ADIPOSE DERIVED STEM CELL; CELL DIFFERENTIATION; CELL TYPE; DIABETES MELLITUS; EMBRYONIC STEM CELL; HEMATOPOIETIC STEM CELL; HUMAN; INSULIN PRODUCING CELL; INSULIN SYNTHESIS; MESENCHYMAL STEM CELL; NONHUMAN; ORGANOGENESIS; PANCREAS CELL; PANCREAS DEVELOPMENT; PLURIPOTENT STEM CELL; REVIEW; STEM CELL;

ANIMALS; CELL DIFFERENTIATION; DIABETES MELLITUS, TYPE 1; HUMANS; INSULIN; INSULIN-SECRETING CELLS; ISLETS OF LANGERHANS TRANSPLANTATION; STEM CELLS;

EID: 84879459888     PISSN: 0004069X     EISSN: 16614917     Source Type: Journal    
DOI: 10.1007/s00005-012-0213-y     Document Type: Review

References (102)

1. Aasen T, Raya A, Barrero MJ et al (2008) Efficient and rapid generation of induced pluripotent stem cells from human keratinocytes. Nat Biotechnol 26:1276-1284
2. American Diabetes Association (2011) Diagnosis and classification of diabetes mellitus. Diabetes Care 34:S62-S69
3. Artner I, Le Lay J, Hang Y et al (2006) MafB: an activator of the glucagon gene expressed in developing islet alpha- and beta-cells. Diabetes 55:297-304 (Pubitemid 43343256)
4. Artner I, Hang Y, Mazur M et al (2010) MafA and MafB regulate genes critical to beta-cells in a unique temporal manner. Diabetes 59:2530-2539
5. Baeyens L, De Breuck S, Lardon J et al (2005) In vitro generation of insulin producing beta cells from adult exocrine pancreatic cells. Diabetologia 48:49-57 (Pubitemid 40174656)
6. Bai L, Meredith G, Tuch BE (2005) Glucagon-like peptide-1 enhances production of insulin in insulin-producing cells derived from mouse embryonic stem cells. J Endocrinol 186:343-352 (Pubitemid 41167403)
7. Bernardo AS, Cho CH, Mason S et al (2009) Biphasic induction of Pdx1 in mouse and human embryonic stem cells can mimic development of pancreatic beta-cells. Stem Cells 27:341-351
8. Blyszczuk P, Czyz J, Kania G et al (2003) Expression of Pax4 in embryonic stem cells promotes differentiation of nestin-positive progenitor and insulin-producing cells. Proc Natl Acad Sci USA 100:998-1003 (Pubitemid 36183944)
9. Blyszczuk P, Asbrand C, Rozzo A (2004) Embryonic stem cells differentiate into insulin-producing cells without selection of nestin-expressing cells. Int J Dev Biol 48:1095-1104 (Pubitemid 40179576)
10. Borowiak M, Maehr R, Chen S (2009) Small molecules efficiently direct endodermal differentiation of mouse and human embryonic stem cells. Cell Stem Cell 4:348-358
11. Boyd AS, Wu DC, Higashi Y et al (2008) A comparison of protocols used to generate insulin-producing cell clusters from mouse embryonic stem cells. Stem Cells 26:1128-1137
12. Cai W, Zhang Y, Kamp TJ (2011) Imaging of induced pluripotent stem cells: from cellular reprogramming to transplantation. Am J Nucl Med Mol Imaging 1:18-28
13. Carlotti F, Zaldumbide A, Loomans CJ et al (2010) Isolated human islets contain a distinct population of mesenchymal stem cells. Islets 2:164-173
14. Chandra V, S G, Phadnis S, Nair PD et al (2009) Generation of pancreatic hormone-expressing islet-like cell aggregates from murine adipose tissue-derived stem cells. Stem Cells 27:1941-1953
15. Chandra V, Swetha G, Muthyala S et al (2011) Islet-like cell aggregates generated from human adipose tissue derived stem cells ameliorate experimental diabetes in mice. PLoS One 6:e20615
16. Chang CM, Kao CL, Chang YL et al (2007) Placenta-derived multipotent stem cells induced to differentiate into insulin-positive cells. Biochem Biophys Res Commun 357:414-420 (Pubitemid 46603147)
17. Chang CF, Hsu KH, Chiou SH et al (2008) Fibronectin and pellet suspension culture promote differentiation of human mesenchymal stem cells into insulin producing cells. J Biomed Mater Res A 86:1097-1105
18. Chao KC, Chao KF, Fu YS et al (2008) Islet-like clusters derived from mesenchymal stem cells in Wharton's Jelly of the human umbilical cord for transplantation to control type 1 diabetes. PLoS One 3:e1451 (Pubitemid 351248247)
19. Chen LB, Jiang XB, Yang L (2004) Differentiation of rat marrow mesenchymal stem cells into pancreatic islet beta-cells. World J Gastroenterol 10:3016-3020 (Pubitemid 39303055)
20. Cho YM, Lim JM, Yoo DH et al (2008) Betacellulin and nicotinamide sustain PDX1 expression and induce pancreatic beta-cell differentiation in human embryonic stem cells. Biochem Biophys Res Commun 366:129-134 (Pubitemid 350297223)
21. Collombat P, Hecksher-Sørensen J, Broccoli V et al (2005) The simultaneous loss of Arx and Pax4 genes promotes a somatostatin- producing cell fate specification at the expense of the alpha- and beta-cell lineages in the mouse endocrine pancreas. Development 132:2969-2980 (Pubitemid 41086732)
22. D'Amour KA, Bang AG, Eliazer S et al (2006) Production of pancreatic hormone-expressing endocrine cells from human embryonic stem cells. Nat Biotechnol 24:1392-1401 (Pubitemid 44722103)
23. Degn KB, Brock B, Juhl CB et al (2004) Effect of intravenous infusion of exenatide (synthetic exendin-4) on glucosedependent insulin secretion and counterregulation during hypoglycemia. Diabetes 53:2397-2403 (Pubitemid 39145595)
24. Ding DC, Shy WC, Lin SZ (2011) Mesenchymal stem cells. Cell Transplant 20:5-14
25. Dor Y, Brown J, Martinez OI et al (2004) Adult pancreatic beta-cells are formed by self-duplication rather than stem-cell differentiation. Nature 429:41-46 (Pubitemid 38620543)
26. Eberhardt M, Salmon P, von Mach MA et al (2006) Multipotential nestin and Isl-1 positive mesenchymal stem cells isolated from human pancreatic islets. Biochem Biophys Res Commun 345:1167-1176 (Pubitemid 43776504)
27. Elghazi L, Cras-Meneur C, Czernichow P et al (2002) Role for FGFR2IIIb-mediated signals in controlling pancreatic endocrine progenitor cell proliferation. Proc Natl Acad Sci USA 99:3884-3889 (Pubitemid 34252200)
28. Feng RQ, Du LY, Guo ZQ (2005) In vitro cultivation and differentiation of fetal liver stem cells from mice. Cell Res 15:401-405 (Pubitemid 41653935)
29. Gao R, Ustinov J, Pulkkinen MA et al (2003) Characterization of endocrine progenitor cells and critical factors for their differentiation in human adult pancreatic cell culture. Diabetes 52:2007-2015 (Pubitemid 36919793)
30. Gao F, Wu DQ, Hu YH et al (2008) Extracellular matrix gel is necessary for in vitro cultivation of insulin producing cells from human umbilical cord blood derived mesenchymal stem cells. Chin Med J 121:811-818
31. Gittes GK (2009) Developmental biology of the pancreas: a comprehensive review. Dev Biol 326:4-35
32. Gu G, Dubauskaite J, Melton DA (2002) Direct evidence for the pancreatic lineage: NGN3ţ cells are islet progenitors and are distinct from duct progenitors. Development 129:2447-2457 (Pubitemid 34863851)
33. Guo T, Hebrok M (2009) Stem cells to pancreatic beta-cells: new sources for diabetes cell therapy. Endocr Rev 30:214-227
34. Habener JF, Kemp DM, Thomas MK (2005) Minireview: transcriptional regulation in pancreatic development. Endocrinology 146:1025-1034 (Pubitemid 40289291)
35. Hardikar AA, Wang XY, Williams L et al (2002) Functional maturation of fetal porcine beta cells by glucagon-like peptide 1 and cholecystokinin. Endocrinology 143:3505-3514 (Pubitemid 34925725)
36. Henseleit KD, Nelson SB, Kuhlbrodt K et al (2005) NKX6 transcription factor activity is required for alpha- and beta-cell development in the pancreas. Development 132:3139-3149 (Pubitemid 41086746)
37. Hisanaga E, Park KY, Yamada S et al (2008) A simple method to induce differentiation of murine bone marrow mesenchymal cells to insulin-producing cells using conophylline and betacellulin-delta 4. Endocr J 55:535-543 (Pubitemid 351949749)
38. Hori Y, Rulifson IC, Tsai BC et al (2002) Growth inhibitors promote differentiation of insulin-producing tissue from embryonic stem cells. Proc Natl Acad Sci USA 99:16105-16110 (Pubitemid 35462756)
39. Hori Y, Gu X, Xie X et al (2005) Differentiation of insulin-producing cells from human neural progenitor cells. PLoS Med 2:e103 (Pubitemid 40721080)
40. Huangfu D, Maehr R, Guo W et al (2008) Induction of pluripotent stem cells by defined factors is greatly improved by small-molecule compounds. Nat Biotechnol 26:795-797 (Pubitemid 351961456)
41. Hui H, Perfetti R (2002) Pancreas duodenum homeobox-1 regulates pancreas development during embryogenesis and islet cell function in adulthood. Eur J Endocrinol 146:129-141 (Pubitemid 34162905)
42. Jiang W, Shi Y, Zhao D et al (2007a) In vitro derivation of functional insulin-producing cells from human embryonic stem cells. Cell Res 17:333-344 (Pubitemid 46639938)
43. Jiang J, Au M, Lu K et al (2007b) Generation of insulin-producing islet-like clusters from human embryonic stem cells. Stem Cells 25:1940-1953 (Pubitemid 47258172)
44. Johansson KA, Dursun U, Jordan N et al (2007) Temporal control of neurogenin3 activity in pancreas progenitors reveals competence windows for the generation of different endocrine cell types. Dev Cell 12:457-465
45. Kaji K, Norrby K, Paca A et al (2009) Virus-free induction of pluripotency and subsequent excision of reprogramming factors. Nature 458:771-775
46. Kajiyama H, Hamazaki TS, Tokuhara M et al (2010) Pdx1-transfected adipose tissue-derived stem cells differentiate into insulin-producing cells in vivo and reduce hyperglycemia in diabetic mice. Int J Dev Biol 54:699-705
47. Karnieli O, Izhar-Prato Y, Bulvik S et al (2007) Generation of insulin-producing cells from human bone marrow mesenchymal stem cells by genetic manipulation. Stem Cells 25:2837-2844 (Pubitemid 350127868)
48. Kataoka K, Han SI, Shioda S et al (2002) MafA is a glucose-regulated and pancreatic beta-cell-specific transcriptional activator for the insulin gene. J Biol Chem 277:49903-49910 (Pubitemid 36014439)
49. Kelly CM, Tyers P, Borg MT et al (2005) EGF and FGF-2 responsiveness of rat and mouse neural precursors derived from the embryonic CNS. Brain Res Bull 68:83-94 (Pubitemid 41698880)
50. Kim JB, Greber B, Arauzo-Bravo MJ et al (2009) Direct reprogramming of human neural stem cells by OCT4. Nature 461:649-653
51. Kim SJ, Choi YS, Ko ES et al (2012) Glucose-stimulated insulin secretion of various mesenchymal stem cells after insulin-producing cell differentiation. J Biosci Bioeng 113:771-777
52. Kroon E, Martinson LA, Kadoya K et al (2008) Pancreatic endoderm derived from human embryonic stem cells generates glucose-responsive insulin-secreting cells in vivo. Nat Biotechnol 26:443-452 (Pubitemid 351501814)
53. Kubo A, Stull R, Takeuchi M et al (2011) Pdx1 and Ngn3 overexpression enhances pancreatic differentiation of mouse ES cell-derived endoderm population. PLoS One 6:e24058
54. Kumar M, Jordan N, Melton D et al (2003) Signals from lateral plate mesoderm instruct endoderm toward a pancreatic fate. Dev Biol 259:109-122 (Pubitemid 36703147)
55. Kunisada Y, Tsubooka-Yamazoe N, Shoji M et al (2012) Small molecules induce efficient differentiation into insulin-producing cells from human induced pluripotent stem cells. Stem Cell Res 8:274-284
56. Lau J, Kawahira H, Hebrok M (2006) Hedgehog signaling in pancreas development and disease. Cell Mol Life Sci 63:642-652
57. Li L, Yi Z, Seno M et al (2004) Activin A and betacellulin: effect on regeneration of pancreatic beta-cells in neonatal streptozotocin-treated rats. Diabetes 53:608-615 (Pubitemid 38270629)
58. Li HY, Chen YJ, Chen SJ et al (2010) Induction of insulin-producing cells derived from endometrial mesenchymal stem-like cells. J Pharmacol Exp Ther 335:817-829
59. Liang XD, Guo YY, Sun M et al (2011) Streptozotocin-induced expression of Ngn3 and Pax4 in neonatal rat pancreatic α-cells. World J Gastroenterol 17:2812-2820
60. Lin HT, Kao CL, Lee KH et al (2007) Enhancement of insulin-producing cell differentiation from embryonic stem cells using pax4-nucleofection method. World J Gastroenterol 13:1672-1679
61. Lin HY, Tsai CC, Chen LL et al (2010) Fibronectin and laminin promote differentiation of human mesenchymal stem cells into insulin producing cells through activating Akt and ERK. J Biomed Sci 17:1-10
62. Loh YH, Agarwal S, Park IH et al (2009) Generation of induced pluripotent stem cells from human blood. Blood 113:5476-5479
63. Lorenzo PI, Jimenez Moreno CM, Delgado I et al (2011) Immunohistochemical assessment of Pax8 expression during pancreatic islet development and in human neuroendocrine tumors. Histochem Cell Biol 136:595-607
64. Lowry WE, Richter L, Yachechko R et al (2008) Generation of human induced pluripotent stem cells from dermal fibroblasts. Proc Natl Acad Sci USA 105:2883-2888 (Pubitemid 351723638)
65. Lumelsky N, Blondel O, Laeng P et al (2001) Differentiation of embryonic stem cells to insulin-secreting structures similar to pancreatic islets. Science 292:1389-1394 (Pubitemid 32476228)
66. May CL (2010) The role of Islet-1 in the endocrine pancreas: lessons from pancreas specific Islet-1 deficient mice. Islets 2:121-123
67. Noguchi H (2009) Pancreatic islet transplantation. World J Gastrointest Surg 1:16-20
68. Oh SH, Muzzonigro TM, Bae SH et al (2004) Adult bone marrow-derived cells trans-differentiating into insulin-producing cells for the treatment of type I diabetes. Lab Invest 84:607-617 (Pubitemid 38858470)
69. Oh YS, Shin S, Lee YJ et al (2011) Betacellulin-induced beta cell proliferation and regeneration is mediated by activation of ErbB-1 and ErbB-2 receptors. PLoS ONE 6:e23894
70. Okita K, Ichisaka T, Yamanaka S (2007) Generation of germline-competent induced pluripotent stem cells. Nature 448:313-317 (Pubitemid 47080336)
71. Okita K, Nakagawa M, Hyenjong H et al (2008) Generation of mouse induced pluripotent stem cells without viral vectors. Science 322:949-953
72. Park IH, Zhao R, West JA et al (2008) Reprogramming of human somatic cells to pluripotency with defined factors. Nature 451:141-146
73. Raslova K (2010) An update on the treatment of type 1 and type 2 diabetes mellitus: focus on insulin detemir, a long-acting human insulin analog. Vasc Health Risk Manag 6:399-410
74. Rodriguez AM, Elabd C, Amri EZ et al (2005) The human adipose tissue is a source of multipotent stem cells. Biochimie 87:125-128 (Pubitemid 40298775)
75. Schwindt TT, Motta FL, Gabriela BF et al (2009) Effects of FGF-2 and EGF removal on the differentiation of mouse neural precursor cells. An Acad Bras Cienc 81:443-452
76. Shi Y, Hou L, Tang F et al (2005) Inducing embryonic stem cells to differentiate into pancreatic β-cells by a novel three-step approach with activin A and all-trans retinoic acid. Stem Cells 23:656-662 (Pubitemid 40647262)
77. Shiroi A, Ueda S, Ouji Y et al (2005) Differentiation of embryonic stem cells into insulin-producing cells promoted by Nkx2.2 gene transfer. World J Gastroenterol 11:4161-4166 (Pubitemid 41086865)
78. Soria B, Bedoya FJ, Martin F (2005) Gastrointestinal stem cells: I. Pancreatic stem cells. Am J Physiol Gastrointest Liver Physiol 289:G177-G180 (Pubitemid 41022741)
79. Stadtfeld M, Nagaya M, Utikal J et al (2008) Induced pluripotent stem cells generated without viral integration. Science 322:945-949
80. Stafford D, Prince VE (2002) Retinoic acid signaling is required for a critical early step in Zebrafish pancreatic development. Curr Biol 12:1215-1220 (Pubitemid 34801169)
81. Stafford D, Hornbruch A, Mueller PR et al (2004) A conserved role for retinoid signaling in vertebrate pancreas development. Dev Genes Evol 214:432-441 (Pubitemid 39378351)
82. Sun Y, Chen L, Hou XG et al (2007) Differentiation of bone marrow-derived mesenchymal stem cells from diabetic patients into insulin-producing cells in vitro. Chin Med J 120:771-776 (Pubitemid 46767823)
83. Suzuki A, Zheng YW, Kaneko S et al (2002) Clonal identification and characterization of self-renewing pluripotent stem cells in the developing liver. J Cell Biol 156:173-184 (Pubitemid 34846945)
84. Takahashi K, Tanabe K, Ohnuki M et al (2007) Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131:861-872 (Pubitemid 350138099)
85. Takenaga M, Fukumoto M, Hori Y (2007) Regulated Nodal signaling promotes differentiation of the definitive endoderm and mesoderm from ES cells. J Cell Sci 120:2078-2090 (Pubitemid 47010003)
86. Tang DQ, Cao LZ, Burkhardt BR et al (2004) In vivo and in vitro characterization of insulin-producing cells obtained from murine bone marrow. Diabetes 53:1721-1732 (Pubitemid 38857030)
87. Tateishi K, He J, Taranova O et al (2008) Generation of insulin-secreting islet-like clusters from human skin fibroblasts. J Biol Chem 283:31601-31607
88. Timper K, Seboek D, Eberhardt M et al (2006) Human adipose tissue-derived mesenchymal stem cells differentiate into insulin, somatostatin, and glucagon expressing cells. Biochem Biophys Res Commun 341:1135-1140 (Pubitemid 43221783)
89. Tureyen K, Vemuganti R, Bowen KK et al (2005) EGF and FGF-2 infusion increases post-ischemic neural progenitor cell proliferation in the adult rat brain. Neurosurgery 57:1254-1263 (Pubitemid 41827421)
90. Wang R, Yashpal N, Bacchus F et al (2004) Hepatocyte growth factor regulates proliferation and differentiation of epithelial monolayers derived from islets of postnatal rat pancreas. J Endocrinol 183:163-171 (Pubitemid 40124653)
91. Wang PX, Yu ZW, Wong S et al (2011) Nkx6.2 synergizes with Cdx-2 in stimulating proglucagon gene expression. World J Diabetes 2:66-74
92. Wilson ME, Scheel D, German MS (2003) Gene expression cascades in pancreatic development. Mech Dev 120:65-80 (Pubitemid 35469131)
93. Wobus AM, Boheler KR (2005) Embryonic stem cells: prospects for developmental biology and cell therapy. Physiol Rev 85:635-678 (Pubitemid 40404638)
94. Woltjen K, Michael IP, Mohseni P et al (2009) PiggyBac transposition reprograms fibroblasts to induced pluripotent stem cells. Nature 458:766-770
95. Yu J, Vodyanik MA, Smuga-Otto K et al (2007) Induced pluripotent stem cell lines derived from human somatic cells. Science 318:1917-1920
96. Yu J, Hu K, Smuga-Otto K et al (2009) Human induced pluripotent stem cells free of vector and transgene sequences. Science 324:797-801
97. Zanini C, Bruno S, Mandili G et al (2011) Differentiation of mesenchymal stem cells derived from pancreatic islets and bone marrow into islet-like cell phenotype. PLoS One 6:e28175
98. Zhang D, Jiang W, Liu M et al (2009a) Highly efficient differentiation of human ES cells and iPS cells into mature pancreatic insulin-producing cells. Cell Res 19:29-438
99. Zhang YH, Wang HF, Liu W (2009b) Insulin-producing cells derived from rat bone marrow and their autologous transplantation in the duodenal wall for treating diabetes. Anat Rec (Hoboken) 292:728-735
100. Zhang Y, Shen W, Hua J et al (2010) Pancreatic islet-like clusters from bone marrow mesenchymal stem cells of human first-trimester abortus can cure streptozocin-induced mouse diabetes. Rejuvenation Res 13:695-706
101. Zhou H, Wu S, Joo JY et al (2009) Generation of induced pluripotent stem cells using recombinant proteins. Cell Stem Cell 4:381-384
102. Zuk PA, Zhu M, Ashjian P et al (2002) Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell 13:4279-4295 (Pubitemid 35471185)