Systematically labeling developmental stage-specific genes for the study of pancreatic β-cell differentiation from human embryonic stem cells

Cell Research

Volumn 24, Issue 10, 2014, Pages 1181-1200

  Liu, Haisong ^a   Yang, Huan ^a   Zhu, Dicong ^a   Sui, Xin ^a   Li, Juan ^a   Liang, Zhen ^a   Xu, Lei ^b   Chen, Zeyu ^c   Yao, Anzhi ^c   Zhang, Long ^d   Zhang, Xi ^d   Yi, Xing ^c   Liu, Meng ^a   Xu, Shiqing ^e   Zhang, Wenjian ^e   Lin, Hua ^e   Xie, Lan ^f   Lou, Jinning ^e   Zhang, Yong ^d   Xi, Jianzhong ^a   Deng, Hongkui ^a,c,g   more..

^a PEKING UNIVERSITY   (China)

^b BEIJING INSTITUTE OF MICROBIOLOGY AND EPIDEMIOLOGY   (China)

^c Peking University   (China)

^d BGI SHENZHEN   (China)

^e CHINA JAPAN FRIENDSHIP HOSPITAL   (China)

^f Beijing Renhe Hospital   (China)

^g PEKING UNIVERSITY HEALTH SCIENCE CENTER   (China)

Author keywords

directed differentiation; embryonic stem cell; gene labeling; pancreatic cell; SUSD2

Indexed keywords

BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; FOXA2 PROTEIN, HUMAN; HEPATOCYTE NUCLEAR FACTOR 3BETA; MEMBRANE PROTEIN; NERVE PROTEIN; NEUROG3 PROTEIN, HUMAN; SOX17 PROTEIN, HUMAN; SUSD2 PROTEIN, HUMAN; TRANSCRIPTION FACTOR SOX;

CELL DIFFERENTIATION; CYTOLOGY; EMBRYONIC STEM CELL; GENE EXPRESSION PROFILING; GENETICS; HUMAN; METABOLISM; PANCREAS ISLET BETA CELL; REPORTER GENE; SEQUENCE ANALYSIS;

BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL DIFFERENTIATION; CYTOLOGY; EMBRYONIC STEM CELLS; GENE EXPRESSION PROFILING; GENES, REPORTER; GENETICS; HEPATOCYTE NUCLEAR FACTOR 3-BETA; HUMANS; INSULIN-SECRETING CELLS; MEMBRANE GLYCOPROTEINS; METABOLISM; NERVE TISSUE PROTEINS; SEQUENCE ANALYSIS, RNA; SOXF TRANSCRIPTION FACTORS;

EID: 84964247564     PISSN: 10010602     EISSN: 17487838     Source Type: Journal    
DOI: 10.1038/cr.2014.118     Document Type: Article

References (46)

1. Cohen DE, Melton D. Turning straw into gold: directing cell fate for regenerative medicine. Nat Rev Genet 2011; 12:243-252.
2. Murry CE, Keller G. Differentiation of embryonic stem cells to clinically relevant populations: lessons from embryonic development. Cell 2008; 132:661-680.
3. Nostro MC, Keller G. Generation of ? cells from human pluripotent stem cells: potential for regenerative medicine. Semin Cell Dev Biol 2012; 23:701-710.
4. Nostro MC, Sarangi F, Ogawa S, et al. Stage-specific signaling through TGF? family members and WNT regulates patterning and pancreatic specification of human pluripotent stem cells. Development 2011; 138:861-871.
5. Nazareth EJ, Ostblom JE, Lucker PB, et al. High-throughput fingerprinting of human pluripotent stem cell fate responses and lineage bias. Nat Methods 2013; 10:1225-1231.
6. Rodriguez-Segui S, Akerman I, Ferrer J. GATA believe it: new essential regulators of pancreas development. J Clin Invest 2012; 122:3469-3471.
7. Pan FC, Wright C. Pancreas organogenesis: from bud to plexus to gland. Dev Dyn 2011; 240:530-565.
8. McKnight KD, Wang P, Kim SK. Deconstructing pancreas development to reconstruct human islets from pluripotent stem cells. Cell Stem Cell 2010; 6:300-308.
9. Bu L, Jiang X, Martin-Puig S, et al. Human ISL1 heart progenitors generate diverse multipotent cardiovascular cell lineages. Nature 2009; 460:113-117.
10. Wang P, Rodriguez RT, Wang J, Ghodasara A, Kim SK. Targeting SOX17 in human embryonic stem cells creates unique strategies for isolating and analyzing developing endoderm. Cell Stem Cell 2011; 8:335-346.
11. Micallef SJ, Li X, Schiesser JV, et al. INS(GFP/w) human embryonic stem cells facilitate isolation of in vitro derived insulin-producing cells. Diabetologia 2012; 55:694-706.
12. Giudice A, Trounson A. Genetic modification of human embryonic stem cells for derivation of target cells. Cell Stem Cell 2008; 2:422-433.
13. Kim Y, Kweon J, Kim A, et al. A library of TAL effector nucleases spanning the human genome. Nat Biotechnol 2013; 31:251-258.
14. Wang H, Hu YC, Markoulaki S, et al. TALEN-mediated editing of the mouse Y chromosome. Nat Biotechnol 2013; 31:530-532.
15. Shalem O, Sanjana NE, Hartenian E, et al. Genome-scale CRISPR-Cas9 knockout screening in human cells. Science 2014; 343:84-87.
16. Wang T, Wei JJ, Sabatini DM, Lander ES. Genetic screens in human cells using the CRISPR-Cas9 system. Science 2014; 343:80-84.
17. Pagliuca FW, Melton DA. How to make a functional ?-cell. Development 2013; 140:2472-2483.
18. Shi Y, Hou L, Tang F, et al. Inducing embryonic stem cells to differentiate into pancreatic ? cells by a novel three-step approach with activin A and all-trans retinoic acid. Stem Cells 2005; 23:656-662.
19. D'Amour KA, Bang AG, Eliazer S, et al. Production of pancreatic hormone-expressing endocrine cells from human embryonic stem cells. Nat Biotechnol 2006; 24:1392-1401.
20. Jiang J, Au M, Lu K, et al. Generation of insulin-producing islet-like clusters from human embryonic stem cells. Stem Cells 2007; 25:1940-1953.
21. Jiang W, Shi Y, Zhao D, et al. In vitro derivation of functional insulin-producing cells from human embryonic stem cells. Cell Res 2007; 17:333-344.
22. Chen S, Borowiak M, Fox JL, et al. A small molecule that directs differentiation of human ESCs into the pancreatic lineage. Nat Chem Biol 2009; 5:258-265.
23. Zhang D, Jiang W, Liu M, et al. Highly efficient differentiation of human ES cells and iPS cells into mature pancreatic insulin-producing cells. Cell Res 2009; 19:429-438.
24. Kelly OG, Chan MY, Martinson LA, et al. Cell-surface markers for the isolation of pancreatic cell types derived from human embryonic stem cells. Nat Biotechnol 2011; 29:750-756.
25. Rezania A, Bruin JE, Riedel MJ, et al. Maturation of human embryonic stem cell-derived pancreatic progenitors into functional islets capable of treating pre-existing diabetes in mice. Diabetes 2012; 61:2016-2029.
26. Zhu FF, Zhang PB, Zhang DH, et al. Generation of pancreatic insulin-producing cells from rhesus monkey induced pluripotent stem cells. Diabetologia 2011; 54:2325-2336.
27. Rukstalis JM, Habener JF. Neurogenin3: a master regulator of pancreatic islet differentiation and regeneration. Islets 2009; 1:177-184.
28. Oliver-Krasinski JM, Stoffers DA. On the origin of the ? cell. Genes Dev 2008; 22:1998-2021.
29. Kroon E, Martinson LA, Kadoya K, et al. Pancreatic endoderm derived from human embryonic stem cells generates glucose-responsive insulin-secreting cells in vivo. Nat Biotechnol 2008; 26:443-452.
30. Bruin JE, Erener S, Vela J, et al. Characterization of polyhormonal insulin-producing cells derived in vitro from human embryonic stem cells. Stem Cell Res 2014; 12:194-208.
31. Hasegawa K, Cowan AB, Nakatsuji N, Suemori H. Efficient multicistronic expression of a transgene in human embryonic stem cells. Stem Cells 2007; 25:1707-1712.
32. Wang Z, Li J, Huang H, et al. An integrated chip for the high-throughput synthesis of transcription activator-like effectors. Angew Chem Int Ed Engl 2012; 51:8505-8508.
33. Gittes GK. Developmental biology of the pancreas: a comprehensive review. Dev Biol 2009; 326:4-35.
34. Zorn AM, Wells JM. Vertebrate endoderm development and organ formation. Annu Rev Cell Dev Biol 2009; 25:221-251.
35. Sander M, Sussel L, Conners J, et al. Homeobox gene Nkx6.1 lies downstream of Nkx2.2 in the major pathway of ?-cell formation in the pancreas. Development 2000; 127:5533-5540.
36. Ejarque M, Cervantes S, Pujadas G, et al. Neurogenin3 cooperates with Foxa2 to autoactivate its own expression. J Biol Chem 2013; 288:11705-11717.
37. Schwitzgebel VM, Scheel DW, Conners JR, et al. Expression of neurogenin3 reveals an islet cell precursor population in the pancreas. Development 2000; 127:3533-3542.
38. Wilson ME, Scheel D, German MS. Gene expression cascades in pancreatic development. Mech Dev 2003; 120:65-80.
39. Collombat P, Mansouri A, Hecksher-Sorensen J, et al. Opposing actions of Arx and Pax4 in endocrine pancreas development. Genes Dev 2003; 17:2591-2603.
40. Rezania A, Riedel MJ, Wideman RD, et al. Production of functional glucagon-secreting ?-cells from human embryonic stem cells. Diabetes 2011; 60:239-247.
41. Xie R, Everett LJ, Lim HW, et al. Dynamic chromatin remodeling mediated by polycomb proteins orchestrates pancreatic differentiation of human embryonic stem cells. Cell Stem Cell 2013; 12:224-237.
42. Desgraz R, Herrera PL. Pancreatic neurogenin 3-expressing cells are unipotent islet precursors. Development 2009; 136:3567-3574.
43. Watson AP, Evans RL, Egland KA. Multiple functions of sushi domain containing 2 (SUSD2) in breast tumorigenesis. Mol Cancer Res 2013; 11:74-85.
44. Gouzi M, Kim YH, Katsumoto K, Johansson K, Grapin-Botton A. Neurogenin3 initiates stepwise delamination of differentiating endocrine cells during pancreas development. Dev Dyn 2011; 240:589-604.
45. He S, Kim I, Lim MS, Morrison SJ. Sox17 expression confers self-renewal potential and fetal stem cell characteristics upon adult hematopoietic progenitors. Genes Dev 2011; 25:1613-1627.
46. Arntfield ME, van der Kooy D. ?-Cell evolution: How the pancreas borrowed from the brain: The shared toolbox of genes expressed by neural and pancreatic endocrine cells may reflect their evolutionary relationship. Bioessays 2011; 33:582-587.