Insulin-Producing Cells Derived from Human Embryonic Stem Cells: Comparison of Definitive Endoderm- and Nestin-Positive Progenitor-Based Differentiation Strategies

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Wei, Rui ^a   Yang, Jin ^a   Hou, Wenfang ^a   Liu, Guoqiang ^a   Gao, Meijuan ^a   Zhang, Lin ^a   Wang, Haining ^a   Mao, Genhong ^a   Gao, Hongwei ^a   Chen, Guian ^a   Hong, Tianpei ^a  

^a PEKING UNIVERSITY THIRD HOSPITAL   (China)

Author keywords

[No Author keywords available]

Indexed keywords

NESTIN;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL LINE; CELL STRUCTURE; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; ENDOCRINE CELL; ENDODERM; HUMAN; HUMAN CELL; IN VITRO STUDY; INSULIN PRODUCING CELL; INTERMETHOD COMPARISON; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PANCREAS ISLET CELL; STEM CELL;

BIOLOGICAL MARKERS; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL LINE; EMBRYONIC STEM CELLS; ENDODERM; HUMANS; INSULIN-SECRETING CELLS; NESTIN;

EID: 84881527255     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0072513     Document Type: Article

References (38)

1. Shapiro AM, Lakey JR, Ryan EA, Korbutt GS, Toth E, et al. (2000) Islet transplantation in seven patients with type 1 diabetes mellitus using a glucocorticoid-free immunosuppressive regimen. N Engl J Med 343: 230-238. doi:10.1056/NEJM200007273430401. PubMed: 10911004.
2. Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, et al. (1998) Embryonic stem cell lines derived from human blastocysts. Science 282: 1145-1147. doi:10.1126/science.282.5391.1145. PubMed: 9804556.
3. Assady S, Maor G, Amit M, Itskovitz-Eldor J, Skorecki KL, et al. (2001) Insulin production by human embryonic stem cells. Diabetes 50: 1691-1697. doi:10.2337/diabetes.50.8.1691. PubMed: 11473026.
4. Lumelsky N, Blondel O, Laeng P, Velasco I, Ravin R, et al. (2001) Differentiation of embryonic stem cells to insulin-secreting structures similar to pancreatic islets. Science 292: 1389-1394. doi:10.1126/science.1058866. PubMed: 11326082.
5. Mao GH, Chen GA, Bai HY, Song TR, Wang YX, (2009) The reversal of hyperglycaemia in diabetic mice using PLGA scaffolds seeded with islet-like cells derived from human embryonic stem cells. Biomaterials 30: 1706-1714. doi:10.1016/j.biomaterials.2008.12.030. PubMed: 19135250.
6. Jiang W, Shi Y, Zhao D, Chen S, Yong J, et al. (2007) In vitro derivation of functional insulin-producing cells from human embryonic stem cells. Cell Res 17: 333-344. doi:10.1038/cr.2007.28. PubMed: 17426693.
7. Wei R, Yang J, Liu GQ, Gao MJ, Hou WF, et al. (2013) Dynamic expression of microRNAs during the differentiation of human embryonic stem cells into insulin-producing cells. Gene 518: 246-255. doi:10.1016/j.gene.2013.01.038. PubMed: 23370336.
8. D'Amour KA, Bang AG, Eliazer S, Kelly OG, Agulnick AD, et al. (2006) Production of pancreatic hormone-expressing endocrine cells from human embryonic stem cells. Nat Biotechnol 24: 1392-1401. doi:10.1038/nbt1259. PubMed: 17053790.
9. Blyszczuk P, Czyz J, Kania G, Wagner M, Roll U, et al. (2003) Expression of Pax4 in embryonic stem cells promotes differentiation of nestin-positive progenitor and insulin-producing cells. Proc Natl Acad Sci U S A 100: 998-1003. doi:10.1073/pnas.0237371100. PubMed: 12525695.
10. Kwon YD, Oh SK, Kim HS, Ku SY, Kim SH, et al. (2005) Cellular manipulation of human embryonic stem cells by TAT-PDX1 protein transduction. Mol Ther 12: 28-32. doi:10.1016/j.ymthe.2005.03.010. PubMed: 15963917.
11. Soria B, Roche E, Berná G, León-Quinto T, Reig JA, et al. (2000) Insulin-secreting cells derived from embryonic stem cells normalize glycemia in streptozotocin-induced diabetic mice. Diabetes 49: 157-162. doi:10.2337/diabetes.49.2.157. PubMed: 10868930.
12. Rojas A, Khoo A, Tejedo JR, Bedoya FJ, Soria B, et al. (2010) Islet cell development. Adv Exp Med Biol 654: 59-75. doi:10.1007/978-90-481-3271-3_4. PubMed: 20217494.
13. Deltour L, Leduque P, Paldi A, Ripoche MA, Dubois P, et al. (1991) Polyclonal origin of pancreatic islets in aggregation mouse chimaeras. Development 112: 1115-1121. PubMed: 1682130.
14. Edlund H, (2001) Developmental biology of the pancreas. Diabetes 50: S5-S9. doi:10.2337/diabetes.50.2007.S5. PubMed: 11272202.
15. Seaberg RM, Smukler SR, Kieffer TJ, Enikolopov G, Asghar Z, et al. (2004) Clonal identification of multipotent precursors from adult mouse pancreas that generate neural and pancreatic lineages. Nat Biotechnol 22: 1115-1124. doi:10.1038/nbt1004. PubMed: 15322557.
16. Rolletschek A, Kania G, Wobus AM, (2006) Generation of pancreatic insulin-producing cells from embryonic stem cells- 'proof of principle', but questions still unanswered. Diabetologia 49: 2541-2545. doi:10.1007/s00125-006-0441-y. PubMed: 17047917.
17. Zulewski H, Abraham EJ, Gerlach MJ, Daniel PB, Moritz W, et al. (2001) Multipotential nestin-positive stem cells isolated from adult pancreatic islets differentiate ex vivo into pancreatic endocrine, exocrine, and hepatic phenotypes. Diabetes 50: 521-533. doi:10.2337/diabetes.50.3.521. PubMed: 11246871.
18. Hori Y, Rulifson IC, Tsai BC, Heit JJ, Cahoy JD, et al. (2002) Growth inhibitors promote differentiation of insulin-producing tissue from embryonic stem cells. Proc Natl Acad Sci U S A 99: 16105-16110. doi:10.1073/pnas.252618999. PubMed: 12441403.
19. Osafune K, Caron L, Borowiak M, Martinez RJ, Fitz-Gerald CS, et al. (2008) Marked differences in differentiation propensity among human embryonic stem cell lines. Nat Biotechnol 26: 313-315. doi:10.1038/nbt1383. PubMed: 18278034.
20. Hong-mei P, Gui-an C (2006) Serum-free medium cultivation to improve efficacy in establishment of human embryonic stem cell lines. Hum Reprod 21: 217-222.
21. Hohmeier HE, Newgard CB, (2004) Cell lines derived from pancreatic islets. Mol Cell Endocrinol 228: 121-128. doi:10.1016/j.mce.2004.04.017. PubMed: 15541576.
22. Cai HQ, Xu SQ, Men XL, Sui WG, Zhang WJ, et al. (2009) Isolation, purification, and functional evaluation of human pancreatic islet. Zhonghua Yi Xue Za Zhi 89: 836-840. PubMed: 19595125.
23. Wang H, Zhang W, Cai H, Xu S, Sui W, et al. (2011) alpha-Cell loss from islet impairs its insulin secretion in vitro and in vivo. Islets 3: 58-65. doi:10.4161/isl.3.2.15036. PubMed: 21372634.
24. Benes V, Castoldi M, (2010) Expression profiling of microRNA using real-time quantitative PCR, how to use it and what is available. Methods 50: 244-249. doi:10.1016/j.ymeth.2010.01.026. PubMed: 20109550.
25. Joglekar MV, Joglekar VM, Hardikar AA, (2009) Expression of islet-specific microRNAs during human pancreatic development. Gene Expr Patterns 9: 109-113. doi:10.1016/j.gep.2008.10.001. PubMed: 18977315.
26. Correa-Medina M, Bravo-Egana V, Rosero S, Ricordi C, Edlund H, et al. (2009) MicroRNA miR-7 is preferentially expressed in endocrine cells of the developing and adult human pancreas. Gene Expr Patterns 9: 193-199. doi:10.1016/j.gep.2008.12.003. PubMed: 19135553.
27. Lynn FC, Skewes-Cox P, Kosaka Y, McManus MT, Harfe BD, et al. (2007) MicroRNA expression is required for pancreatic islet cell genesis in the mouse. Diabetes 56: 2938-2945. doi:10.2337/db07-0175. PubMed: 17804764.
28. Kloosterman WP, Lagendijk AK, Ketting RF, Moulton JD, Plasterk RH, (2007) Targeted inhibition of miRNA maturation with morpholinos reveals a role for miR-375 in pancreatic islet development. PLOS Biol 5: e203. doi:10.1371/journal.pbio.0050203. PubMed: 17676975.
29. Poy MN, Hausser J, Trajkovski M, Braun M, Collins S, et al. (2009) miR-375 maintains normal pancreatic alpha- and beta-cell mass. Proc Natl Acad Sci U S A 106: 5813-5818. doi:10.1073/pnas.0810550106. PubMed: 19289822.
30. Krichevsky AM, Sonntag KC, Isacson O, Kosik KS, (2006) Specific microRNAs modulate embryonic stem cell-derived neurogenesis. Stem Cells 24: 857-864. doi:10.1634/stemcells.2005-0441. PubMed: 16357340.
31. Ivey KN, Muth A, Arnold J, King FW, Yeh RF, et al. (2008) MicroRNA regulation of cell lineages in mouse and human embryonic stem cells. Cell Stem Cell 2: 219-229. doi:10.1016/j.stem.2008.01.016. PubMed: 18371447.
32. Bramblett DE, Huang HP, Tsai MJ, (2000) Pancreatic islet development. Adv Pharmacol 47: 255-315. PubMed: 10582089.
33. Scharfmann R, Xiao X, Heimberg H, Mallet J, Ravassard P, (2008) Beta cells within single human islets originate from multiple progenitors. PLOS ONE 3: e3559. doi:10.1371/journal.pone.0003559. PubMed: 18958289.
34. Guo T, Hebrok M, (2009) Stem cells to pancreatic beta-cells: new sources for diabetes cell therapy. Endocr Rev 30: 214-227. doi:10.1210/er.2009-0004. PubMed: 19389995.
35. Meivar-Levy I, Sapir T, Gefen-Halevi S, Aviv V, Barshack I, et al. (2007) Pancreatic and duodenal homeobox gene 1 induces hepatic dedifferentiation by suppressing the expression of CCAAT/enhancer-binding protein beta. Hepatology 46: 898-905. doi:10.1002/hep.21766. PubMed: 17705277.
36. Zhou Q, Brown J, Kanarek A, Rajagopal J, Melton DA, (2008) In vivo reprogramming of adult pancreatic exocrine cells to beta-cells. Nature 455: 627-632. doi:10.1038/nature07314. PubMed: 18754011.
37. Thorel F, Népote V, Avril I, Kohno K, Desgraz R, et al. (2010) Conversion of adult pancreatic alpha-cells to beta-cells after extreme beta-cell loss. Nature 464: 1149-1154. doi:10.1038/nature08894. PubMed: 20364121.
38. Wells JM, Melton DA, (1999) Vertebrate endoderm development. Annu Rev Cell Dev Biol 15: 393-410. doi:10.1146/annurev.cellbio.15.1.393. PubMed: 10611967.