In vitro expansion of single Lgr5 + liver stem cells induced by Wnt-driven regeneration

Nature

Volumn 494, Issue 7436, 2013, Pages 247-250

  Huch, Meritxell ^a   Dorrell, Craig ^b   Boj, Sylvia F ^a   Van Es, Johan H ^a   Li, Vivian S W ^a   Van De Wetering, Marc ^a   Sato, Toshiro ^a,d   Hamer, Karien ^a   Sasaki, Nobuo ^a   Finegold, Milton J ^c   Haft, Annelise ^b   Vries, Robert G ^a   Grompe, Markus ^b   Clevers, Hans ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^c TEXAS CHILDREN S HOSPITAL   (United States)

^d KEIO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GALACTOSIDASE; G PROTEIN COUPLED RECEPTOR; LEUCINE RICH REPEAT CONTAINING G PROTEIN COUPLED RECEPTOR 5; UNCLASSIFIED DRUG; WNT PROTEIN;

ADULT; CYST; DAMAGE; LIGAND; PROTEIN; REGROWTH; RODENT;

3' UNTRANSLATED REGION; ALLELE; ANIMAL CELL; ARTICLE; BILE DUCT; CELL FATE; CELL LINEAGE; CELL PROLIFERATION; CELL RENEWAL; CULTURE MEDIUM; CYTOPLASM; GENE EXPRESSION PROFILING; GENE LOCUS; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LIVER CELL; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEM CELL EXPANSION; WNT SIGNALING PATHWAY;

ALLELES; ANIMALS; BILE DUCTS; CELL LINEAGE; CLONE CELLS; CULTURE MEDIA; DISEASE MODELS, ANIMAL; FEMALE; GENE KNOCK-IN TECHNIQUES; HEPATOCYTES; HYDROLASES; LIVER; LIVER DISEASES; MALE; MICE; MULTIPOTENT STEM CELLS; ORGANOIDS; RECEPTORS, G-PROTEIN-COUPLED; REGENERATION; STEM CELLS; THROMBOSPONDINS; TYROSINEMIAS; WNT SIGNALING PATHWAY;

MUS;

EID: 84873712443     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature11826     Document Type: Article

References (33)

1. Barker, N. et al. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 449, 1003-1007 (2007).
2. Barker, N. et al.Lgr51ve stemcells drive self-renewal in the stomach and build longlived gastric units in vitro. Cell Stem Cell 6, 25-36 (2010).
3. Jaks, V. et al.Lgr5marks cycling, yet long-lived, hair follicle stemcells.NatureGenet. 40, 1291-1299 (2008).
4. Sato, T. et al. Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature 459, 262-265 (2009).
5. Yui, S. et al. Functional engraftment of colon epithelium expanded in vitro from a single adult Lgr51 stem cell. Nature Med. 18, 618-623 (2012).
6. Kim, K. A. et al. Mitogenic influence of human R-spondin1 on the intestinal epithelium. Science 309, 1256-1259 (2005).
7. Carmon, K. S., Gong, X., Lin, Q., Thomas, A. & Liu, Q. R-spondins function as ligands of the orphan receptors LGR4 and LGR5 to regulateWnt/b-catenin signaling. Proc. Natl Acad. Sci. USA 108, 11452-11457 (2011).
8. de Lau, W. et al. Lgr5 homologues associate with Wnt receptors and mediate R-spondin signalling. Nature 476, 293-297 (2011).
9. Duncan, A. W., Dorrell, C. & Grompe, M. Stem cells and liver regeneration. Gastroenterology 137, 466-481 (2009).
10. Dorrell, C. et al. Prospective isolationof a bipotential clonogenic liver progenitor cell in adult mice. Genes Dev. 25, 1193-1203 (2011).
11. Sackett, S. D. et al. Foxl1 is a marker of bipotential hepatic progenitor cells in mice. Hepatology 49, 920-929 (2009).
12. Furuyama, K. et al. Continuous cell supply from a Sox9-expressing progenitor zone in adult liver, exocrine pancreas and intestine. Nature Genet. 43, 34-41 (2011).
13. Shin, S. et al. Foxl1-Cre-marked adult hepatic progenitors have clonogenic and bilineage differentiation potential. Genes Dev. 25, 1185-1192 (2011).
14. Benhamouche, S. et al. Apc tumor suppressor gene is the 'zonation-keeper' of mouse liver. Dev. Cell 10, 759-770 (2006).
15. Hu, M. et al. Wnt/b-catenin signaling in murine hepatic transit amplifying progenitor cells. Gastroenterology 133, 1579-1591 (2007).
16. Lustig, B. et al. Negative feedback loop of Wnt signaling through upregulation of conductin/axin2 in colorectal and liver tumors. Mol. Cell. Biol. 22, 1184-1193 (2002).
17. Stowell, R. E.&Lee, C. S. Histochemical studies ofmouse liver after single feedingof carbon tetrachloride. AMA Arch. Pathol. 50, 519-537 (1950).
18. Muñoz, J. et al. The Lgr5 intestinal stem cell signature: robust expression of proposed quiescent '14' cell markers. EMBO J. 31, 3079-3091 (2012).
19. Soriano, P. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nature Genet. 21, 70-71 (1999).
20. Akhurst, B. et al. A modified choline-deficient, ethionine-supplemented diet protocol effectively induces oval cells in mouse liver. Hepatology 34, 519-522 (2001).
21. Preisegger, K. H. et al. Atypical ductular proliferation and its inhibition by transforming growth factor beta1 in the 3,5-diethoxycarbonyl-1,4- dihydrocollidine mouse model for chronic alcoholic liver disease. Lab. Invest. 79, 103-109 (1999).
22. Michalopoulos, G. K., Bowen, W. C., Mulè, K. & Stolz, D. B. Histological organization in hepatocyte organoid cultures. Am. J. Pathol. 159, 1877-1887 (2001).
23. Schmelzer, E. et al. Human hepatic stem cells from fetal and postnatal donors. J. Exp. Med. 204, 1973-1987 (2007).
24. Kamiya, A., Kakinuma, S., Yamazaki, Y. & Nakauchi, H. Enrichment and clonal culture of progenitor cells during mouse postnatal liver development in mice. Gastroenterology 137, 1114-1126 (2009).
25. Duncan, A. W. et al. The ploidy conveyor of mature hepatocytes as a source of genetic variation. Nature 467, 707-710 (2010).
26. Tanimizu, N.&Miyajima, A. Notch signaling controls hepatoblast differentiation by altering the expression of liver-enriched transcription factors. J. Cell Sci. 117, 3165-3174 (2004).
27. Lemaigre, F. P. Mechanisms of liver development: concepts for understanding liver disorders and design of novel therapies. Gastroenterology 137, 62-79 (2009).
28. Zaret, K. S. Genetic programming of liver and pancreas progenitors: lessons for stem-cell differentiation. Nature Rev. Genet. 9, 329-340 (2008).
29. Si-Tayeb, K., Lemaigre, F. P.&Duncan, S. A. Organogenesisand development of the liver. Dev. Cell 18, 175-189 (2010).
30. Azuma, H. et al. Robust expansion of human hepatocytes in Fah2/2/Rag22/2/Il2rg2/2 mice. Nature Biotechnol. 25, 903-910 (2007).
31. 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).
32. Huch, M., Gros A., José A., González J. R., Alemnay R. & Fillat C. Urokinase-type plasminogen activator receptor transcriptionally controlled adenoviruses eradicate pancreatic tumors and liver metastasis in mouse models. Neoplasia 11, 518-528 (2009).
33. Wang, X. et al. Cell fusion is the principal source of bone-marrow-derived hepatocytes. Nature 422, 897-901 (2003).