Niche-independent high-purity cultures of Lgr5 + intestinal stem cells and their progeny

Nature Methods

Volumn 11, Issue 1, 2014, Pages 106-112

  Yin, Xiaolei ^a,b,c,d   Farin, Henner F ^e   Van Es, Johan H ^e   Clevers, Hans ^e   Langer, Robert ^a,f   Karp, Jeffrey M ^a,b,c,d  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d HARVARD STEM CELL INSTITUTE   (United States)

^e UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^f Massachusetts Institute of Technology Cambridge   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN; GLYCOGEN SYNTHASE KINASE 3 INHIBITOR; NOTCH RECEPTOR; VALPROIC ACID; WNT PROTEIN; CHIR 99021; G PROTEIN COUPLED RECEPTOR; GREEN FLUORESCENT PROTEIN; LGR5 PROTEIN, MOUSE; PYRIDINE DERIVATIVE; PYRIMIDINE DERIVATIVE; 6 [[2 [[4 (2,4 DICHLOROPHENYL) 5 (4 METHYL 1H IMIDAZOL 2 YL) 2 PYRIMIDINYL]AMINO]ETHYL]AMINO]NICOTINONITRILE;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL FUNCTION; CELL LINEAGE; CELL MATURATION; CELL RENEWAL; COLONY FORMING UNIT; CONTROLLED STUDY; GOBLET CELL; INTESTINAL STEM CELL; INTESTINE CELL; INTESTINE EPITHELIUM CELL; INTRACELLULAR SIGNALING; MOLECULE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PANETH CELL; PRIORITY JOURNAL; STEM CELL CULTURE; STEM CELL EXPANSION; STEM CELL NICHE; WNT SIGNALING PATHWAY; ANIMAL; CELL CULTURE; CHEMISTRY; CHROMOSOME; COLON; CONFOCAL MICROSCOPY; CULTURE TECHNIQUE; CYTOLOGY; EQUIPMENT; FLOW CYTOMETRY; HETEROZYGOTE; KARYOTYPING; METABOLISM; METHODOLOGY; SIGNAL TRANSDUCTION; SMALL INTESTINE; STEM CELL; STOMACH; ULTRASTRUCTURE; DEVICES; PROCEDURES;

ANIMALS; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELLS, CULTURED; CHROMOSOMES; COLON; FLOW CYTOMETRY; GREEN FLUORESCENT PROTEINS; HETEROZYGOTE; INTESTINE, SMALL; KARYOTYPING; MICE; MICROSCOPY, CONFOCAL; PANETH CELLS; PYRIDINES; PYRIMIDINES; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION; STEM CELLS; STOMACH; VALPROIC ACID;

EID: 84894623720     PISSN: 15487091     EISSN: 15487105     Source Type: Journal    
DOI: 10.1038/nmeth.2737     Document Type: Article

References (39)

1. Barker, N. et al. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 449, 1003-1007 (2007).
2. Sato, T. et al. Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature 459, 262-265 (2009).
3. Sato, T. et al. Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts. Nature 469, 415-418 (2011).
4. Yilmaz, Ö.H. et al. mTORC1 in the Paneth cell niche couples intestinal stem-cell function to calorie intake. Nature 486, 490-495 (2012).
5. Farin, H.F., van Es, J.H. & Clevers, H. Redundant sources of Wnt regulate intestinal stem cells and promote formation of Paneth cells. Gastroenterology 143, 1518-1529 (2012).
6. Snippert, H.J. et al. Intestinal crypt homeostasis results from neutral competition between symmetrically dividing Lgr5 stem cells. Cell 143, 134-144 (2010).
7. Scoville, D.H., Sato, T., He, X.C. & Li, L. Current view: intestinal stem cells and signaling. Gastroenterology 134, 849-864 (2008).
8. van der Flier, L.G. & Clevers, H. Stem cells, self-renewal, and differentiation in the intestinal epithelium. Annu. Rev. Physiol. 71, 241-260 (2009).
9. Crosnier, C., Stamataki, D. & Lewis, J. Organizing cell renewal in the intestine: stem cells, signals and combinatorial control. Nat. Rev. Genet. 7, 349-359 (2006).
10. Stanger, B.Z., Datar, R., Murtaugh, L.C. & Melton, D.A. Direct regulation of intestinal fate by Notch. Proc. Natl. Acad. Sci. USA 102, 12443-12448 (2005).
11. Zecchini, V., Domaschenz, R., Winton, D. & Jones, P. Notch signaling regulates the differentiation of post-mitotic intestinal epithelial cells. Genes Dev. 19, 1686-1691 (2005).
12. Powell, D.W., Pinchuk, I.V., Saada, J.I., Chen, X. & Mifflin, R.C. Mesenchymal cells of the intestinal lamina propria. Annu. Rev. Physiol. 73, 213-237 (2011).
13. Greenblatt, D.Y. et al. Valproic acid activates Notch-1 signaling and regulates the neuroendocrine phenotype in carcinoid cancer cells. Oncologist 12, 942-951 (2007).
14. Stockhausen, M.T., Sjölund, J., Manetopoulos, C. & Axelson, H. Effects of the histone deacetylase inhibitor valproic acid on Notch signalling in human neuroblastoma cells. Br. J. Cancer 92, 751-759 (2005).
15. van der Flier, L.G. et al. Transcription factor achaete scute-like 2 controls intestinal stem cell fate. Cell 136, 903-912 (2009).
16. de Lau, W. et al. Lgr5 homologues associate with Wnt receptors and mediate R-spondin signalling. Nature 476, 293-297 (2011).
17. Wang, F. et al. Isolation and characterization of intestinal stem cells based on surface marker combinations and colony-formation assay. Gastroenterology 145, 383-395 (2013).
18. van Es, J.H. et al. Dll1+ secretory progenitor cells revert to stem cells upon crypt damage. Nat. Cell Biol. 14, 1099-1104 (2012).
19. Sato, T. et al. Long-term expansion of epithelial organoids from human colon, adenoma, adenocarcinoma, and Barrett's epithelium. Gastroenterology 141, 1762-1772 (2011).
20. Jung, P. et al. Isolation and in vitro expansion of human colonic stem cells. Nat. Med. 17, 1225-1227 (2011).
21. Subramanian, A. et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. USA 102, 15545-15550 (2005).
22. Mu?oz, J. et al. The Lgr5 intestinal stem cell signature: robust expression of proposed quiescent '+4' cell markers. EMBO J. 31, 3079-3091 (2012).
23. Yu, D., Cozma, D., Park, A. & Thomas-Tikhonenko, A. Functional validation of genes implicated in lymphomagenesis: an in vivo selection assay using a Myc-induced B-cell tumor. Ann. NY Acad. Sci. 1059, 145-159 (2005).
24. Milano, J. et al. Modulation of notch processing by ?-secretase inhibitors causes intestinal goblet cell metaplasia and induction of genes known to specify gut secretory lineage differentiation. Toxicol. Sci. 82, 341-358 (2004).
25. Wong, G.T. et al. Chronic treatment with the ?-secretase inhibitor LY-411,575 inhibits ?-amyloid peptide production and alters lymphopoiesis and intestinal cell differentiation. J. Biol. Chem. 279, 12876-12882 (2004).
26. van Es, J.H. et al. Notch/gamma-secretase inhibition turns proliferative cells in intestinal crypts and adenomas into goblet cells. Nature 435, 959-963 (2005).
27. Fre, S. et al. Notch signals control the fate of immature progenitor cells in the intestine. Nature 435, 964-968 (2005).
28. Bain, J. et al. The selectivity of protein kinase inhibitors: a further update. Biochem. J. 408, 297-315 (2007).
29. Conti, L. et al. Niche-independent symmetrical self-renewal of a mammalian tissue stem cell. PLoS Biol. 3, e283 (2005).
30. Pellegrinet, L. et al. Dll1-and Dll4-mediated notch signaling are required for homeostasis of intestinal stem cells. Gastroenterology 140, 1230-1240 (2011).
31. Riccio, O. et al. Loss of intestinal crypt progenitor cells owing to inactivation of both Notch1 and Notch2 is accompanied by derepression of CDK inhibitors p27Kip1 and p57Kip2. EMBO Rep. 9, 377-383 (2008).
32. Kazanjian, A., Noah, T., Brown, D., Burkart, J. & Shroyer, N.F. Atonal homolog 1 is required for growth and differentiation effects of notch/gamma-secretase inhibitors on normal and cancerous intestinal epithelial cells. Gastroenterology 139, 918-928 (2010).
33. Kim, T.H. & Shivdasani, R.A. Genetic evidence that intestinal Notch functions vary regionally and operate through a common mechanism of Math1 repression. J. Biol. Chem. 286, 11427-11433 (2011).
34. VanDussen, K.L. et al. Notch signaling modulates proliferation and differentiation of intestinal crypt base columnar stem cells. Development 139, 488-497 (2012).
35. D'Souza, B., Miyamoto, A. & Weinmaster, G. The many facets of Notch ligands. Oncogene 27, 5148-5167 (2008).
36. Shroyer, N.F. et al. Intestine-specific ablation of mouse atonal homolog 1 (Math1) reveals a role in cellular homeostasis. Gastroenterology 132, 2478-2488 (2007).
37. Han, H. et al. Inducible gene knockout of transcription factor recombination signal binding protein-J reveals its essential role in T versus B lineage decision. Int. Immunol. 14, 637-645 (2002).
38. Shibata, H. et al. Rapid colorectal adenoma formation initiated by conditional targeting of the Apc gene. Science 278, 120-123 (1997).
39. Barker, N. et al. Lgr5+ve stem cells drive self-renewal in the stomach and build long-lived gastric units in vitro. Cell Stem Cell 6, 25-36 (2010).