Transient expression of Ngn3 in Xenopus endoderm promotes early and ectopic development of pancreatic beta and delta cells

Genesis

Volumn 50, Issue 3, 2012, Pages 271-285

  Oropez, Daniel ^a,b   Horb, Marko ^a,b,c,d  

^a CLIN RESEARCH INSTITUTE OF MONTREAL   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c BROWN UNIVERSITY   (United States)

^d MARINE BIOLOGICAL LABORATORY   (United States)

Author keywords

Diabetes; Endocrine; Endoderm progenitor; Hormone inducible; Microarray; Reprogramming; Transcription factor

Indexed keywords

NEUROGENIN 3;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL FATE; CONTROLLED STUDY; ECTOPIC PANCREAS; EMBRYO; ENDODERM; GASTRULATION; GENE EXPRESSION; NONHUMAN; PANCREAS ISLET ALPHA CELL; PANCREAS ISLET BETA CELL; PANCREAS ISLET DELTA CELL; PRIORITY JOURNAL; XENOPUS; XENOPUS LAEVIS;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL DIFFERENTIATION; ENDODERM; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; INSULIN; INSULIN-SECRETING CELLS; ISLETS OF LANGERHANS; SOMATOSTATIN-SECRETING CELLS; T-BOX DOMAIN PROTEINS; TRANSCRIPTION FACTORS; XENOPUS LAEVIS; XENOPUS PROTEINS;

XENOPUS LAEVIS;

EID: 84857999240     PISSN: 1526954X     EISSN: 1526968X     Source Type: Journal    
DOI: 10.1002/dvg.20828     Document Type: Article

References (50)

1. Aaker JD, Patineau AL, Yang HJ, Ewart DT, Gong W, Li T, Nakagawa Y, McLoon SC, Koyano-Nakagawa N. 2009. Feedback regulation of NEUROG2 activity by MTGR1 is required for progression of neurogenesis. Mol Cell Neurosci 42: 267-277.
2. Aaker JD, Patineau AL, Yang HJ, Ewart DT, Nakagawa Y, McLoon SC, Koyano-Nakagawa N. 2010. Interaction of MTG family proteins with NEUROG2 and ASCL1 in the developing nervous system. Neurosci Lett 474: 46-51.
3. Afelik S, Chen Y, Pieler T. 2006. Combined ectopic expression of Pdx1 and Ptf1a/p48 results in the stable conversion of posterior endoderm into endocrine and exocrine pancreatic tissue. Genes Dev 20: 1441-1446.
4. Amann JM, Chyla BJ, Ellis TC, Martinez A, Moore AC, Franklin JL, McGhee L, Meyers S, Ohm JE, Luce KS, Ouelette AJ, Washington MK, Thompson MA, King D, Gautam S, Coffey RJ, Whitehead RH, Hiebert SW. 2005. Mtgr1 is a transcriptional corepressor that is required for maintenance of the secretory cell lineage in the small intestine. Mol Cell Biol 25: 9576-9585.
5. Apelqvist A, Li H, Sommer L, Beatus P, Anderson DJ, Honjo T, Hrabe D.A, Lendahl U, Edlund H. 1999. Notch signalling controls pancreatic cell differentiation. Nature 400: 877-881.
6. Bennett K, James C, Hussain K. 2010. Pancreatic beta-cell KATP channels: Hypoglycaemia and hyperglycaemia. Rev Endocr Metab Disord 11: 157-163.
7. Borowiak M, Melton DA. 2009. How to make beta cells? Curr Opin Cell Biol 21: 727-732.
8. Calabi F, Pannell R, Pavloska G. 2001. Gene targeting reveals a crucial role for MTG8 in the gut. Mol Cell Biol 21: 5658-5666.
9. Cao Y, Zhao H, Grunz H. 2002. XETOR regulates the size of the proneural domain during primary neurogenesis in Xenopus laevis. Mech Dev 119: 35-44.
10. Chalmers AD, Slack JM. 1998. Development of the gut in Xenopus laevis. Dev Dyn 212: 509-521.
11. Chalmers AD, Slack JM. 2000. The Xenopus tadpole gut: fate maps and morphogenetic movements. Development 127: 381-392.
12. Collombat P, Mansouri A, Hecksher-Sorensen J, Serup P, Krull J, Gradwohl G, Gruss P. 2003. Opposing actions of Arx and Pax4 in endocrine pancreas development. Genes Dev 17: 2591-2603.
13. Collombat P, Xu X, Ravassard P, Sosa-Pineda B, Dussaud S, Billestrup N, Madsen OD, Serup P, Heimberg H, Mansouri A. 2009. The ectopic expression of Pax4 in the mouse pancreas converts progenitor cells into alpha and subsequently beta cells. Cell 138: 449-462.
14. Dhawan S, Georgia S, Tschen SI, Fan G, Bhushan A. 2011. Pancreatic beta cell identity is maintained by DNA methylation-mediated repression of Arx. Dev Cell 20: 419-429.
15. Gasa R, Mrejen C, Leachman N, Otten M, Barnes M, Wang J, Chakrabarti S, Mirmira R, German M. 2004. Proendocrine genes coordinate the pancreatic islet differentiation program in vitro. Proc Natl Acad Sci USA 101: 13245-13250.
16. Gasa R, Mrejen C, Lynn FC, Skewes-Cox P, Sanchez L, Yang KY, Lin CH, Gomis R, German MS. 2008. Induction of pancreatic islet cell differentiation by the neurogenin-neuroD cascade. Differentiation 76: 381-391.
17. Gierl MS, Karoulias N, Wende H, Strehle M, Birchmeier C. 2006. The zinc-finger factor Insm1 (IA-1) is essential for the development of pancreatic beta cells and intestinal endocrine cells. Genes Dev 20: 2465-2478.
18. Gittes GK. 2009. Developmental biology of the pancreas: A comprehensive review. Dev Biol 326: 4-35.
19. Grapin-Botton A, Majithia AR, Melton DA. 2001. Key events of pancreas formation are triggered in gut endoderm by ectopic expression of pancreatic regulatory genes. Genes Dev 15: 444-454.
20. Horb LD, Horb ME. 2010. BrunoL1 regulates endoderm proliferation through translational enhancement of cyclin A2 mRNA. Dev Biol 345: 156-169.
21. Horb LD, Jarkji ZH, Horb ME. 2009. Xenopus Insm1 is essential for gastrointestinal and pancreatic endocrine cell development. Dev Dyn 238: 2505-2510.
22. Horb ME, Shen CN, Tosh D, Slack JM. 2003. Experimental conversion of liver to pancreas. Curr Biol 13: 105-115.
23. Horb ME, Slack JM. 2001. Endoderm specification and differentiation in Xenopus embryos. Dev Biol 236: 330-343.
24. Horb ME, Slack JM. 2002. Expression of amylase and other pancreatic genes in Xenopus. Mech Dev 113: 153-157.
25. Jarikji Z, Horb LD, Shariff F, Mandato CA, Cho KW, Horb ME. 2009. The tetraspanin Tm4sf3 is localized to the ventral pancreas and regulates fusion of the dorsal and ventral pancreatic buds. Development 136: 1791-1800.
26. Jarikji ZH, Vanamala S, Beck CW, Wright CV, Leach SD, Horb ME. 2007. Differential ability of Ptf1a and Ptf1a-VP16 to convert stomach, duodenum and liver to pancreas. Dev Biol 304: 786-799.
27. Johansson KA, Dursun U, Jordan N, Gu G, Beermann F, Gradwohl G, 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.
28. Kelly OG, Melton DA. 2000. Development of the pancreas in Xenopus laevis. Dev Dyn 218: 615-627.
29. Kordowich S, Mansouri A, Collombat P. 2010. Reprogramming into pancreatic endocrine cells based on developmental cues. Mol Cell Endocrinol 323: 62-69.
30. Koyano-Nakagawa N, Kintner C. 2005. The expression and function of MTG/ETO family proteins during neurogenesis. Dev Biol 278: 22-34.
31. Ludtke TH, Christoffels VM, Petry M, Kispert A. 2009. Tbx3 promotes liver bud expansion during mouse development by suppression of cholangiocyte differentiation. Hepatology 49: 969-978.
32. Mellitzer G, Bonne S, Luco RF, Van De CM, Lenne-Samuel N, Collombat P, Mansouri A, Lee J, Lan M, Pipeleers D, Nielsen FC, Ferrer J, Gradwohl G, Heimberg H. 2006. IA1 is NGN3-dependent and essential for differentiation of the endocrine pancreas. EMBO J 25: 1344-1352.
33. Murtaugh LC. 2007. Pancreas and beta-cell development: From the actual to the possible. Development 134: 427-438.
34. Pearl EJ, Bilogan CK, Mukhi S, Brown DD, Horb ME. 2009. Xenopus pancreas development. Dev Dyn 238: 1271-1286.
35. Pearl EJ, Horb ME. 2008. Promoting ectopic pancreatic fates: Pancreas development and future diabetes therapies. Clin Genet 74: 316-324.
36. Pearl EJ, Jarikji Z, Horb ME. 2011. Functional analysis of Rfx6 and mutant variants associated with neonatal diabetes. Dev Biol 351: 135-145.
37. Petri A, Ahnfelt-Ronne J, Frederiksen KS, Edwards DG, Madsen D, Serup P, Fleckner J, Heller RS. 2006. The effect of neurogenin3 deficiency on pancreatic gene expression in embryonic mice. J Mol Endocrinol 37: 301-316.
38. Rossetti S, Hoogeveen AT, Sacchi N. 2004. The MTG proteins: Chromatin repression players with a passion for networking. Genomics 84: 1-9.
39. Rukstalis JM, Habener JF. 2009. Neurogenin3: A master regulator of pancreatic islet differentiation and regeneration. Islets 1: 177-184.
40. Schwitzgebel VM, Scheel DW, Conners JR, Kalamaras J, Lee JE, Anderson DJ, Sussel L, Johnson JD, German MS. 2000. Expression of neurogenin3 reveals an islet cell precursor population in the pancreas. Development 127: 3533-3542.
41. Serafimidis I, Rakatzi I, Episkopou V, Gouti M, Gavalas A. 2008. Novel effectors of directed and Ngn3-mediated differentiation of mouse embryonic stem cells into endocrine pancreas progenitors. Stem Cells 26: 3-16.
42. Smith SB, Qu HQ, Taleb N, Kishimoto NY, Scheel DW, Lu Y, Patch AM, Grabs R, Wang J, Lynn FC, Miyatsuka T, Mitchell J, Seerke R, Desir J, Eijnden SV, Abramowicz M, Kacet N, Weill J, Renard ME, Gentile M, Hansen I, Dewar K, Hattersley AT, Wang R, Wilson ME, Johnson JD, Polychronakos C, German MS. 2010. Rfx6 directs islet formation and insulin production in mice and humans. Nature 463: 775-780.
43. Sosa-Pineda B, Chowdhury K, Torres M, Oliver G, Gruss P. 1997. The Pax4 gene is essential for differentiation of insulin-producing beta cells in the mammalian pancreas. Nature 386: 399-402.
44. Soyer J, Flasse L, Raffelsberger W, Beucher A, Orvain C, Peers B, Ravassard P, Vermot J, Voz ML, Mellitzer G, Gradwohl G. 2010. Rfx6 is an Ngn3-dependent winged helix transcription factor required for pancreatic islet cell development. Development 137: 203-212.
45. Suzuki A, Sekiya S, Buscher D, Izpisua Belmonte JC, Taniguchi H. 2008. Tbx3 controls the fate of hepatic progenitor cells in liver development by suppressing p19ARF expression. Development 135: 1589-1595.
46. Tiso N, Moro E, Argenton F. 2009. Zebrafish pancreas development. Mol Cell Endocrinol 312: 24-30.
47. Treff NR, Vincent RK, Budde ML, Browning VL, Magliocca JF, Kapur V, Odorico JS. 2006. Differentiation of embryonic stem cells conditionally expressing neurogenin 3. Stem Cells 24: 2529-2537.
48. White P, May CL, Lamounier RN, Brestelli JE, Kaestner KH. 2008. Defining pancreatic endocrine precursors and their descendants. Diabetes 57: 654-668.
49. Yechoor V, Chan L. 2010. Minireview: beta-cell replacement therapy for diabetes in the 21st century: Manipulation of cell fate by directed differentiation. Mol Endocrinol 24: 1501-1511.
50. Zhou Q, Brown J, Kanarek A, Rajagopal J, Melton DA. 2008. In vivo reprogramming of adult pancreatic exocrine cells to beta-cells. Nature 455: 627-632.