Human intestinal tissue with adult stem cell properties derived from pluripotent stem cells

Stem Cell Reports

Volumn 2, Issue 6, 2014, Pages 838-852

  Forster, Ryan ^a   Chiba, Kunitoshi ^a   Schaeffer, Lorian ^a   Regalado, Samuel G ^a   Lai, Christine S ^b   Gao, Qing ^b   Kiani, Samira ^b   Farin, Henner F ^c   Clevers, Hans ^c,d   Cost, Gregory J ^e   Chan, Andy ^e   Rebar, Edward J ^e   Urnov, Fyodor D ^e   Gregory, Philip D ^e   Pachter, Lior ^a   Jaenisch, Rudolf ^b,d,f   Hockemeyer, Dirk ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^c UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^d SKOLKOVO INSTITUTE OF SCIENCE AND TECHNOLOGY   (Russian Federation)

^e SANGAMO BIOSCIENCES INC   (United States)

^f MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

KRUPPEL LIKE FACTOR 4; KRUPPEL LIKE FACTOR 5; TRANSCRIPTION FACTOR SOX9; ZINC FINGER NUCLEASE; G PROTEIN COUPLED RECEPTOR; LGR5 PROTEIN, HUMAN; CHROMOGRANIN A; LYSOZYME; MUCIN 2; TRANSCRIPTION FACTOR PDX 1;

ADULT; ADULT STEM CELL; ARTICLE; CELL DIFFERENTIATION; CELL SUSPENSION; CELL TYPE; CONTROLLED STUDY; CYTOPLASM; EMBRYONIC STEM CELL; ENTEROPATHY; ENZYME ACTIVITY; GOBLET CELL; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; INTESTINE BIOPSY; INTESTINE CELL; INTESTINE EPITHELIUM; ORGANISMS; PANETH CELL; PATHOPHYSIOLOGY; PLURIPOTENT STEM CELL; PRIMARY CULTURE; PRIORITY JOURNAL; RNA SEQUENCE; ROUGH ENDOPLASMIC RETICULUM; SOUTHERN BLOTTING; STEM CELL TRANSPLANTATION; TELOMERIC REPEAT AMPLIFICATION PROTOCOL; CELL CULTURE; CYTOLOGY; GENE EXPRESSION PROFILING; INTESTINE; METABOLISM; PROCEDURES; BASOLATERAL MEMBRANE; CARTILAGE; CELL MATURATION; ENTEROENDOCRINE CELL; GENE LOCUS; GENOME; HUMAN TISSUE; INTESTINAL STEM CELL; MARKER GENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ROSETTE FORMATION; SEQUENCE ANALYSIS; SMOOTH MUSCLE; UPREGULATION;

ADULT STEM CELLS; CELLS, CULTURED; GENE EXPRESSION PROFILING; HUMANS; INTESTINES; PLURIPOTENT STEM CELLS; RECEPTORS, G-PROTEIN-COUPLED;

EID: 84902144564     PISSN: 22136711     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.stemcr.2014.05.001     Document Type: Article

References (47)

1. S. Anders, and W. Huber Differential expression analysis for sequence count data Genome Biol. 11 2010 R106
2. N. Barker, J.H. van Es, J. Kuipers, P. Kujala, M. van den Born, M. Cozijnsen, A. Haegebarth, J. Korving, H. Begthel, P.J. Peters, and H. Clevers Identification of stem cells in small intestine and colon by marker gene Lgr5 Nature 449 2007 1003 1007 (Pubitemid 350014593)
3. L. Cao, J.D. Gibson, S. Miyamoto, V. Sail, R. Verma, D.W. Rosenberg, C.E. Nelson, and C. Giardina Intestinal lineage commitment of embryonic stem cells Differentiation 81 2011 1 10
4. K.S. Carmon, X. Gong, Q. Lin, A. Thomas, and Q. Liu R-spondins function as ligands of the orphan receptors LGR4 and LGR5 to regulate Wnt/beta-catenin signaling Proc. Natl. Acad. Sci. USA 108 2011 11452 11457
5. W. de Lau, N. Barker, T.Y. Low, B.-K. Koo, V.S.W. Li, H. Teunissen, P. Kujala, A. Haegebarth, P.J. Peters, and M. van de Wetering et al. Lgr5 homologues associate with Wnt receptors and mediate R-spondin signalling Nature 476 2011 293 297
6. R.C. DeKelver, V.M. Choi, E.A. Moehle, D.E. Paschon, D. Hockemeyer, S.H. Meijsing, Y. Sancak, X. Cui, E.J. Steine, and J.C. Miller et al. Functional genomics, proteomics, and regulatory DNA analysis in isogenic settings using zinc finger nuclease-driven transgenesis into a safe harbor locus in the human genome Genome Res. 20 2010 1133 1142
7. J.F. Dekkers, C.L. Wiegerinck, H.R. de Jonge, I. Bronsveld, H.M. Janssens, K.M. de Winter-de Groot, A.M. Brandsma, N.W.M. de Jong, M.J.C. Bijvelds, and B.J. Scholte et al. A functional CFTR assay using primary cystic fibrosis intestinal organoids Nat. Med. 19 2013 939 945
8. S.R. Finkbeiner, and J.R. Spence A gutsy task: generating intestinal tissue from human pluripotent stem cells Dig. Dis. Sci. 58 2013 1176 1184
9. P. Flicek, I. Ahmed, M.R. Amode, D. Barrell, K. Beal, S. Brent, D. Carvalho-Silva, P. Clapham, G. Coates, and S. Fairley et al. Ensembl 2013 Nucleic Acids Res. 41 Database issue 2013 D48 D55
10. R.P. Fordham, S. Yui, N.R. Hannan, C. Soendergaard, A. Madgwick, P.J. Schweiger, O.H. Nielsen, L. Vallier, R.A. Pedersen, and T. Nakamura et al. Transplantation of expanded fetal intestinal progenitors contributes to colon regeneration after injury Cell Stem Cell 13 2013 734 744
11. C. Günes, and K.L. Rudolph The role of telomeres in stem cells and cancer Cell 152 2013 390 393
12. D. Hockemeyer, F. Soldner, E.G. Cook, Q. Gao, M. Mitalipova, and R. Jaenisch A drug-inducible system for direct reprogramming of human somatic cells to pluripotency Cell Stem Cell 3 2008 346 353
13. D. Hockemeyer, F. Soldner, C. Beard, Q. Gao, M. Mitalipova, R.C. DeKelver, G.E. Katibah, R. Amora, E.A. Boydston, and B. Zeitler et al. Efficient targeting of expressed and silent genes in human ESCs and iPSCs using zinc-finger nucleases Nat. Biotechnol. 27 2009 851 857
14. D. Hockemeyer, H. Wang, S. Kiani, C.S. Lai, Q. Gao, J.P. Cassady, G.J. Cost, L. Zhang, Y. Santiago, and J.C. Miller et al. Genetic engineering of human pluripotent cells using TALE nucleases Nat. Biotechnol. 29 2011 731 734
15. P. Jung, T. Sato, A. Merlos-Suárez, F.M. Barriga, M. Iglesias, D. Rossell, H. Auer, M. Gallardo, M.A. Blasco, and E. Sancho et al. Isolation and in vitro expansion of human colonic stem cells Nat. Med. 17 2011 1225 1227
16. N.W. Kim, and F. Wu Advances in quantification and characterization of telomerase activity by the telomeric repeat amplification protocol (TRAP) Nucleic Acids Res. 25 1997 2595 2597 (Pubitemid 27298154)
17. K.-A. Kim, M. Kakitani, J. Zhao, T. Oshima, T. Tang, M. Binnerts, Y. Liu, B. Boyle, E. Park, and P. Emtage et al. Mitogenic influence of human R-spondin1 on the intestinal epithelium Science 309 2005 1256 1259 (Pubitemid 41170922)
18. V. Korinek, N. Barker, P. Moerer, E. van Donselaar, G. Huls, P.J. Peters, and H. Clevers Depletion of epithelial stem-cell compartments in the small intestine of mice lacking Tcf-4 Nat. Genet. 19 1998 379 383 (Pubitemid 28357912)
19. B. Langmead, and S.L. Salzberg Fast gapped-read alignment with Bowtie 2 Nat. Methods 9 2012 357 359
20. C.J. Lengner, A.A. Gimelbrant, J.A. Erwin, A.W. Cheng, M.G. Guenther, G.G. Welstead, R. Alagappan, G.M. Frampton, P. Xu, and J. Muffat et al. Derivation of pre-X inactivation human embryonic stem cells under physiological oxygen concentrations Cell 141 2010 872 883
21. K.W. McCracken, J.C. Howell, J.M. Wells, and J.R. Spence Generating human intestinal tissue from pluripotent stem cells in vitro Nat. Protoc. 6 2011 1920 1928
22. T. McDonald, R. Wang, W. Bailey, G. Xie, F. Chen, C.T. Caskey, and Q. Liu Identification and cloning of an orphan G protein-coupled receptor of the glycoprotein hormone receptor subfamily Biochem. Biophys. Res. Commun. 247 1998 266 270 (Pubitemid 28420811)
23. H. Miyoshi, and T.S. Stappenbeck In vitro expansion and genetic modification of gastrointestinal stem cells in spheroid culture Nat. Protoc. 8 2013 2471 2482
24. S. Ogaki, N. Shiraki, K. Kume, and S. Kume Wnt and Notch signals guide embryonic stem cell differentiation into the intestinal lineages Stem Cells 31 2013 1086 1096
25. A. Ootani, X. Li, E. Sangiorgi, Q.T. Ho, H. Ueno, S. Toda, H. Sugihara, K. Fujimoto, I.L. Weissman, M.R. Capecchi, and C.J. Kuo Sustained in vitro intestinal epithelial culture within a Wnt-dependent stem cell niche Nat. Med. 15 2009 701 706
26. L. Pellegrinet, V. Rodilla, Z. Liu, S. Chen, U. Koch, L. Espinosa, K.H. Kaestner, R. Kopan, J. Lewis, and F. Radtke Dll1- and dll4-mediated notch signaling are required for homeostasis of intestinal stem cells Gastroenterology 140 2011 1230 1240 e1-e7
27. A. Roberts, and L. Pachter Streaming fragment assignment for real-time analysis of sequencing experiments Nat. Methods 10 2013 71 73
28. H. Ruffner, J. Sprunger, O. Charlat, J. Leighton-Davies, B. Grosshans, A. Salathe, S. Zietzling, V. Beck, M. Therier, and A. Isken et al. R-Spondin potentiates Wnt/β-catenin signaling through orphan receptors LGR4 and LGR5 PLoS ONE 7 2012 e40976
29. T. Sato, R.G. Vries, H.J. Snippert, M. van de Wetering, N. Barker, D.E. Stange, J.H. van Es, A. Abo, P. Kujala, P.J. Peters, and H. Clevers Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche Nature 459 2009 262 265
30. T. Sato, D.E. Stange, M. Ferrante, R.G.J. Vries, J.H. Van Es, S. Van den Brink, W.J. Van Houdt, A. Pronk, J. Van Gorp, P.D. Siersema, and H. Clevers Long-term expansion of epithelial organoids from human colon, adenoma, adenocarcinoma, and Barrett's epithelium Gastroenterology 141 2011 1762 1772
31. T. Sato, J.H. van Es, H.J. Snippert, D.E. Stange, R.G. Vries, M. van den Born, N. Barker, N.F. Shroyer, M. van de Wetering, and H. Clevers Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts Nature 469 2011 415 418
32. A.G. Schepers, R. Vries, M. van den Born, M. van de Wetering, and H. Clevers Lgr5 intestinal stem cells have high telomerase activity and randomly segregate their chromosomes EMBO J. 30 2011 1104 1109
33. G. Schwank, B.K. Koo, V. Sasselli, J.F. Dekkers, I. Heo, T. Demircan, N. Sasaki, S. Boymans, E. Cuppen, and C.K. van der Ent et al. Functional repair of CFTR by CRISPR/Cas9 in intestinal stem cell organoids of cystic fibrosis patients Cell Stem Cell 13 2013 653 658
34. R.I. Sherwood, T.Y. Chen, and D.A. Melton Transcriptional dynamics of endodermal organ formation Dev. Dyn. 238 2009 29 42
35. H.J. Snippert, L.G. van der Flier, T. Sato, J.H. van Es, M. van den Born, C. Kroon-Veenboer, N. Barker, A.M. Klein, J. van Rheenen, B.D. Simons, and H. Clevers Intestinal crypt homeostasis results from neutral competition between symmetrically dividing Lgr5 stem cells Cell 143 2010 134 144
36. F. Soldner, and R. Jaenisch Medicine. iPSC disease modeling Science 338 2012 1155 1156
37. F. Soldner, J. Laganière, A.W. Cheng, D. Hockemeyer, Q. Gao, R. Alagappan, V. Khurana, L.I. Golbe, R.H. Myers, and S. Lindquist et al. Generation of isogenic pluripotent stem cells differing exclusively at two early onset Parkinson point mutations Cell 146 2011 318 331
38. J.R. Spence, C.N. Mayhew, S.A. Rankin, M.F. Kuhar, J.E. Vallance, K. Tolle, E.E. Hoskins, V.V. Kalinichenko, S.I. Wells, and A.M. Zorn et al. Directed differentiation of human pluripotent stem cells into intestinal tissue in vitro Nature 470 2011 105 109
39. M. Stelzner, M. Helmrath, J.C. Dunn, S.J. Henning, C.W. Houchen, C. Kuo, J. Lynch, L. Li, S.T. Magness, M.G. Martin NIH Intestinal Stem Cell Consortium A nomenclature for intestinal in vitro cultures Am. J. Physiol. Gastrointest. Liver Physiol. 302 2012 G1359 G1363
40. K. Takahashi, K. Tanabe, M. Ohnuki, M. Narita, T. Ichisaka, K. Tomoda, and S. Yamanaka Induction of pluripotent stem cells from adult human fibroblasts by defined factors Cell 131 2007 861 872 (Pubitemid 350138099)
41. J.H. van Es, M.E. van Gijn, O. Riccio, M. van den Born, M. Vooijs, H. Begthel, M. Cozijnsen, S. Robine, D.J. Winton, F. Radtke, and H. Clevers Notch/gamma-secretase inhibition turns proliferative cells in intestinal crypts and adenomas into goblet cells Nature 435 2005 959 963 (Pubitemid 40896322)
42. P. Wang, R.T. Rodriguez, J. Wang, A. Ghodasara, and S.K. Kim Targeting SOX17 in human embryonic stem cells creates unique strategies for isolating and analyzing developing endoderm Cell Stem Cell 8 2011 335 346
43. F. Wang, D. Scoville, X.C. He, M.M. Mahe, A. Box, J.M. Perry, N.R. Smith, N.Y. Lei, P.S. Davies, and M.K. Fuller et al. Isolation and characterization of intestinal stem cells based on surface marker combinations and colony-formation assay Gastroenterology 145 2013 383 395 e1-e21
44. J.M. Wells, and J.R. Spence How to make an intestine Development 141 2014 752 760
45. + stem cell Nat. Med. 18 2012 618 623
46. K. Yusa, S.T. Rashid, H. Strick-Marchand, I. Varela, P.-Q. Liu, D.E. Paschon, E. Miranda, A. Ordóñez, N.R.F. Hannan, and F.J. Rouhani et al. Targeted gene correction of α1-antitrypsin deficiency in induced pluripotent stem cells Nature 478 2011 391 394
47. J. Zou, M.L. Maeder, P. Mali, S.M. Pruett-Miller, S. Thibodeau-Beganny, B.K. Chou, G. Chen, Z. Ye, I.H. Park, and G.Q. Daley et al. Gene targeting of a disease-related gene in human induced pluripotent stem and embryonic stem cells Cell Stem Cell 5 2009 97 110