The transcriptional co-repressor Grg3/Tle3 promotes pancreatic endocrine progenitor delamination and β-cell differentiation

Development

Volumn 139, Issue 8, 2012, Pages 1447-1456

  Metzger, David E ^a   Gasperowicz, Malgorzata ^b   Otto, Florian ^c   Cross, James C ^b   Gradwohl, Gerard ^d   Zaret, Kenneth S ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF CALGARY   (Canada)

^c Tumor Center ZeTuP   (Switzerland)

^d UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

cell; Delamination; E cadherin; Endocrine; Grg3; Mouse; Pancreas; Tle3

Indexed keywords

CASPASE 3; CRE RECOMBINASE; GROUCHO RELATED GENE 3 PROTEIN; NEUROGENIN 3; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; UVOMORULIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL TYPE; CELL VIABILITY; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; IMMUNOFLUORESCENCE; MOUSE; NONHUMAN; ORGANOGENESIS; PANCREAS ISLET BETA CELL; PLACENTA DISORDER; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; STEM CELL; TRANSCRIPTION REGULATION; TRUNK;

ANIMALS; APOPTOSIS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CADHERINS; CELL DIFFERENTIATION; CELL PROLIFERATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; INSULIN-SECRETING CELLS; ISLETS OF LANGERHANS; MICE; MICE, KNOCKOUT; MODELS, BIOLOGICAL; NERVE TISSUE PROTEINS; PANCREAS; PROTEINS; STEM CELLS; TIME FACTORS;

EID: 84858841326     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.072892     Document Type: Article

References (47)

1. Ahlgren, U., Jonsson, J., Jonsson, L., Simu, K. and Edlund, H. (1998). Betacell-specific inactivation of the mouse Ipf1/Pdx1 gene results in loss of the betacell phenotype and maturity onset diabetes. Genes Dev. 12, 1763-1768.
2. Anderson, K. R., Singer, R. A., Balderes, D. A., Hernandez-Lagunas, L., Johnson, C. W., Artinger, K. B. and Sussel, L. (2011). The L6 domain tetraspanin Tm4sf4 regulates endocrine pancreas differentiation and directed cell migration. Development 138, 3213-3224.
3. Apelqvist, A., Li, H., Sommer, L., Beatus, P., Anderson, D. J., Honjo, T., Hrabe de Angelis, M., Lendahl, U. and Edlund, H. (1999). Notch signalling controls pancreatic cell differentiation. Nature 400, 877-881.
4. Arce, L., Pate, K. T. and Waterman, M. L. (2009). Groucho binds two conserved regions of LEF-1 for HDAC-dependent repression. BMC Cancer 9, 159.
5. Beucher, A., Martin, M., Spenle, C., Poulet, M., Collin, C. and Gradwohl, G. (2011). Competence of failed endocrine progenitors to give rise to acinar but not ductal cells is restricted to early pancreas development. Dev. Biol. 361, 277-285
6. Borowiak, M. and Melton, D. A. (2009). How to make beta cells? Curr. Opin. Cell Biol. 21, 727-732.
7. Brantjes, H., Roose, J., van De Wetering, M. and Clevers, H. (2001). All Tcf HMG box transcription factors interact with Groucho-related co-repressors. Nucleic Acids Res. 29, 1410-1419.
8. Chen, G., Fernandez, J., Mische, S. and Courey, A. J. (1999). A functional interaction between the histone deacetylase Rpd3 and the corepressor groucho in Drosophila development. Genes Dev. 13, 2218-2230.
9. Cinnamon, E. and Paroush, Z. (2008). Context-dependent regulation of Groucho/TLE-mediated repression. Curr. Opin. Genet. Dev. 18, 435-440.
10. Cole, L., Anderson, M., Antin, P. B. and Limesand, S. W. (2009). One process for pancreatic beta-cell coalescence into islets involves an epithelialmesenchymal transition. J. Endocrinol. 203, 19-31.
11. Doyle, M. J., Loomis, Z. L. and Sussel, L. (2007). Nkx2.2-repressor activity is sufficient to specify alpha-cells and a small number of beta-cells in the pancreatic islet. Development 134, 515-523.
12. Gao, N., LeLay, J., Vatamaniuk, M. Z., Rieck, S., Friedman, J. R. and Kaestner, K. H. (2008). Dynamic regulation of Pdx1 enhancers by Foxa1 and Foxa2 is essential for pancreas development. Genes Dev. 22, 3435-3448.
13. Gasperowicz, M. and Otto, F. (2005). Mammalian Groucho homologs: redundancy or specificity? J. Cell. Biochem. 95, 670-687.
14. Gouzi, M., Kim, Y. H., Katsumoto, K., Johansson, K. and Grapin-Botton, A. (2011). Neurogenin3 initiates stepwise delamination of differentiating endocrine cells during pancreas development. Dev. Dyn. 240, 589-604.
15. Gradwohl, G., Dierich, A., LeMeur, M. and Guillemot, F. (2000). Neurogenin3 is required for the development of the four endocrine cell lineages of the pancreas. Proc. Natl. Acad. Sci. USA 97, 1607-1611.
16. Gu, G., Dubauskaite, J. and Melton, D. A. (2002). Direct evidence for the pancreatic lineage: NGN3+ cells are islet progenitors and are distinct from duct progenitors. Development 129, 2447-2457.
17. Hoffman, B. G., Zavaglia, B., Beach, M. and Helgason, C. D. (2008). Expression of Groucho/TLE proteins during pancreas development. BMC Dev. Biol. 8, 81.
18. Jennings, B. H. and Ish-Horowicz, D. (2008). The Groucho/TLE/Grg family of transcriptional co-repressors. Genome Biol. 9, 205.
19. Jennings, B. H., Pickles, L. M., Wainwright, S. M., Roe, S. M., Pearl, L. H. and Ish-Horowicz, D. (2006). Molecular recognition of transcriptional repressor motifs by the WD domain of the Groucho/TLE corepressor. Mol. Cell 22, 645-655.
20. Jensen, J., Pedersen, E. E., Galante, P., Hald, J., Heller, R. S., Ishibashi, M., Kageyama, R., Guillemot, F., Serup, P. and Madsen, O. D. (2000). Control of endodermal endocrine development by Hes-1. Nat. Genet. 24, 36-44.
21. Jimenez, G., Paroush, Z. and Ish-Horowicz, D. (1997). Groucho acts as a corepressor for a subset of negative regulators, including Hairy and Engrailed. Genes Dev. 11, 3072-3082.
22. Johansson, K. A., Dursun, U., Jordan, N., Gu, G., Beermann, F., Gradwohl, G. and Grapin-Botton, A. (2007). Temporal control of neurogenin3 activity in pancreas progenitors reveals competence windows for the generation of different endocrine cell types. Dev. Cell 12, 457-465.
23. Lee, C. S., Perreault, N., Brestelli, J. E. and Kaestner, K. H. (2002). Neurogenin 3 is essential for the proper specification of gastric enteroendocrine cells and the maintenance of gastric epithelial cell identity. Genes Dev. 16, 1488-1497.
24. Lee, C. S., Sund, N. J., Behr, R., Herrera, P. L. and Kaestner, K. H. (2005). Foxa2 is required for the differentiation of pancreatic alpha-cells. Dev. Biol. 278, 484-495.
25. Lee, J. C., Smith, S. B., Watada, H., Lin, J., Scheel, D., Wang, J., Mirmira, R. G. and German, M. S. (2001). Regulation of the pancreatic pro-endocrine gene neurogenin3. Diabetes 50, 928-936.
26. Magenheim, J., Klein, A. M., Stanger, B. Z., Ashery-Padan, R., Sosa-Pineda, B., Gu, G. and Dor, Y. (2011). Ngn3(+) endocrine progenitor cells control the fate and morphogenesis of pancreatic ductal epithelium. Dev. Biol. 359, 26-36.
27. Miyatsuka, T., Li, Z. and German, M. S. (2009). Chronology of islet differentiation revealed by temporal cell labeling. Diabetes 58, 1863-1868.
28. Nagel, A. C., Krejci, A., Tenin, G., Bravo-Patino, A., Bray, S., Maier, D. and Preiss, A. (2005). Hairless-mediated repression of notch target genes requires the combined activity of Groucho and CtBP corepressors. Mol. Cell. Biol. 25, 10433-10441.
29. Papizan, J. B., Singer, R. A., Tschen, S. I., Dhawan, S., Friel, J. M., Hipkens, S. B., Magnuson, M. A., Bhushan, A. and Sussel, L. (2011). Nkx2.2 repressor complex regulates islet beta-cell specification and prevents beta-to-alpha-cell reprogramming. Genes Dev. 25, 2291-2305.
30. Pierreux, C. E., Poll, A. V., Kemp, C. R., Clotman, F., Maestro, M. A., Cordi, S., Ferrer, J., Leyns, L., Rousseau, G. G. and Lemaigre, F. P. (2006). The transcription factor hepatocyte nuclear factor-6 controls the development of pancreatic ducts in the mouse. Gastroenterology 130, 532-541.
31. Prado, C. L., Pugh-Bernard, A. E., Elghazi, L., Sosa-Pineda, B. and Sussel, L. (2004). Ghrelin cells replace insulin-producing beta cells in two mouse models of pancreas development. Proc. Natl. Acad. Sci. USA 101, 2924-2929.
32. Rukstalis, J. M. and Habener, J. F. (2007). Snail2, a mediator of epithelialmesenchymal transitions, expressed in progenitor cells of the developing endocrine pancreas. Gene Expr. Patterns 7, 471-479.
33. Sander, M., Sussel, L., Conners, J., Scheel, D., Kalamaras, J., Dela Cruz, F., Schwitzgebel, V., Hayes-Jordan, A. and German, M. (2000). Homeobox gene Nkx6.1 lies downstream of Nkx2.2 in the major pathway of beta-cell formation in the pancreas. Development 127, 5533-5540.
34. Santisteban, P., Recacha, P., Metzger, D. E. and Zaret, K. S. (2010). Dynamic expression of groucho-related genes Grg1 and Grg3 in foregut endoderm and antagonism of differentiation. Dev. Dyn. 239, 980-986.
35. Sekiya, T. and Zaret, K. S. (2007). Repression by Groucho/TLE/Grg proteins: genomic site recruitment generates compacted chromatin in vitro and impairs activator binding in vivo. Mol. Cell 28, 291-303.
36. Solar, M., Cardalda, C., Houbracken, I., Martin, M., Maestro, M. A., De Medts, N., Xu, X., Grau, V., Heimberg, H., Bouwens, L. et al. (2009). Pancreatic exocrine duct cells give rise to insulin-producing beta cells during embryogenesis but not after birth. Dev. Cell 17, 849-860.
37. Soyer, J., Flasse, L., Raffelsberger, W., Beucher, A., Orvain, C., Peers, B., Ravassard, P., Vermot, J., Voz, M. L., Mellitzer, G. et al. (2010). Rfx6 is an Ngn3-dependent winged helix transcription factor required for pancreatic islet cell development. Development 137, 203-212.
38. Spence, J. R. and Wells, J. M. (2007). Translational embryology: using embryonic principles to generate pancreatic endocrine cells from embryonic stem cells. Dev. Dyn. 236, 3218-3227.
39. Srinivas, S., Watanabe, T., Lin, C. S., William, C. M., Tanabe, Y., Jessell, T. M. and Costantini, F. (2001). Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev. Biol. 1, 4.
40. Sussel, L., Kalamaras, J., Hartigan-O'Connor, D. J., Meneses, J. J., Pedersen, R. A., Rubenstein, J. L. and German, M. S. (1998). Mice lacking the homeodomain transcription factor Nkx2.2 have diabetes due to arrested differentiation of pancreatic beta cells. Development 125, 2213-2221.
41. Villasenor, A., Chong, D. C., Henkemeyer, M. and Cleaver, O. (2010). Epithelial dynamics of pancreatic branching morphogenesis. Development 137, 4295-4305.
42. Wang, S., Yan, J., Anderson, D. A., Xu, Y., Kanal, M. C., Cao, Z., Wright, C. V. and Gu, G. (2010). Neurog3 gene dosage regulates allocation of endocrine and exocrine cell fates in the developing mouse pancreas. Dev. Biol. 339, 26-37.
43. White, P., May, C. L., Lamounier, R. N., Brestelli, J. E. and Kaestner, K. H. (2008). Defining pancreatic endocrine precursors and their descendants. Diabetes 57, 654-668.
44. Zaret, K. S. (2008). Genetic programming of liver and pancreas progenitors: lessons for stem-cell differentiation. Nat. Rev. Genet. 9, 329-340.
45. Zhang, H., Ables, E. T., Pope, C. F., Washington, M. K., Hipkens, S., Means, A. L., Path, G., Seufert, J., Costa, R. H., Leiter, A. B. et al. (2009). Multiple, temporal-specific roles for HNF6 in pancreatic endocrine and ductal differentiation. Mech. Dev. 126, 958-973.
46. Zhou, Q., Law, A. C., Rajagopal, J., Anderson, W. J., Gray, P. A. and Melton, D. A. (2007). A multipotent progenitor domain guides pancreatic organogenesis. Dev. Cell 13, 103-114.
47. Zufferey, R., Nagy, D., Mandel, R. J., Naldini, L. and Trono, D. (1997). Multiply attenuated lentiviral vector achieves efficient gene delivery in vivo. Nat. Biotechnol. 15, 871-875.