Gene regulatory networks governing pancreas development

Developmental Cell

Volumn 25, Issue 1, 2013, Pages 5-13

  Arda, H Efsun ^a   Benitez, Cecil M ^a   Kim, Seung K ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NEUROGENIN 3;

ACINAR CELL; CELL DIFFERENTIATION; CELL MATURATION; CHROMATIN IMMUNOPRECIPITATION; DATA MINING; DIABETES MELLITUS; ENHANCER REGION; EPIGENETICS; GENE EXPRESSION; GENE REGULATORY NETWORK; HUMAN; MULTIPOTENT STEM CELL; ORGANOGENESIS; PANCREAS; PANCREAS CANCER; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PURIFICATION; REVIEW;

ACINAR CELLS; ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL DEDIFFERENTIATION; CELL DIFFERENTIATION; COMPUTATIONAL BIOLOGY; DATA MINING; DIABETES MELLITUS; GENE REGULATORY NETWORKS; HUMANS; INSULIN-SECRETING CELLS; NERVE TISSUE PROTEINS; NUCLEOTIDE MOTIFS; PANCREAS; STEM CELLS;

EID: 84876351067     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2013.03.016     Document Type: Review

References (77)

1. Afelik S., Chen Y., Pieler T. Combined ectopic expression of Pdx1 and Ptf1a/p48 results in the stable conversion of posterior endoderm into endocrine and exocrine pancreatic tissue. Genes Dev. 2006, 20:1441-1446.
2. Ahnfelt-Rønne J., Jørgensen M.C., Klinck R., Jensen J.N., Füchtbauer E.-M., Deering T., MacDonald R.J., Wright C.V.E., Madsen O.D., Serup P. Ptf1a-mediated control of Dll1 reveals an alternative to the lateral inhibition mechanism. Development 2012, 139:33-45.
3. Alon U. Network motifs: theory and experimental approaches. Nat. Rev. Genet. 2007, 8:450-461.
4. Apelqvist A., Li H., Sommer L., Beatus P., Anderson D.J., Honjo T., Hrabe de Angelis M., Lendahl U., Edlund H. Notch signalling controls pancreatic cell differentiation. Nature 1999, 400:877-881.
5. Arnes L., Hill J.T., Gross S., Magnuson M.A., Sussel L. Ghrelin expression in the mouse pancreas defines a unique multipotent progenitor population. PLoS ONE 2012, 7:e52026.
6. Artner I., Hang Y., Guo M., Gu G., Stein R. MafA is a dedicated activator of the insulin gene in vivo. J. Endocrinol. 2008, 198:271-279.
7. Artner I., Hang Y., Mazur M., Yamamoto T., Guo M., Lindner J., Magnuson M.A., Stein R. MafA and MafB regulate genes critical to beta-cells in a unique temporal manner. Diabetes 2010, 59:2530-2539.
8. Benitez C.M., Goodyer W.R., Kim S.K. Deconstructing pancreas developmental biology. Cold Spring Harb. Perspect. Biol. 2012, 4:4.
9. Beres T.M., Masui T., Swift G.H., Shi L., Henke R.M., MacDonald R.J. PTF1 is an organ-specific and Notch-independent basic helix-loop-helix complex containing the mammalian Suppressor of Hairless (RBP-J) or its paralogue, RBP-L. Mol. Cell. Biol. 2006, 26:117-130.
10. Bhushan A., Itoh N., Kato S., Thiery J.P., Czernichow P., Bellusci S., Scharfmann R. Fgf10 is essential for maintaining the proliferative capacity of epithelial progenitor cells during early pancreatic organogenesis. Development 2001, 128:5109-5117.
11. Bort R., Martinez-Barbera J.P., Beddington R.S.P., Zaret K.S. Hex homeobox gene-dependent tissue positioning is required for organogenesis of the ventral pancreas. Development 2004, 131:797-806.
12. Briscoe J., Pierani A., Jessell T.M., Ericson J. A homeodomain protein code specifies progenitor cell identity and neuronal fate in the ventral neural tube. Cell 2000, 101:435-445.
13. Chen H., Gu X., Liu Y., Wang J., Wirt S.E., Bottino R., Schorle H., Sage J., Kim S.K. PDGF signalling controls age-dependent proliferation in pancreatic β-cells. Nature 2011, 478:349-355.
14. Collombat P., Mansouri A., Hecksher-Sorensen J., Serup P., Krull J., Gradwohl G., Gruss P. Opposing actions of Arx and Pax4 in endocrine pancreas development. Genes Dev. 2003, 17:2591-2603.
15. Collombat P., Hecksher-Sørensen J., Broccoli V., Krull J., Ponte I., Mundiger T., Smith J., Gruss P., Serup P., Mansouri A. The simultaneous loss of Arx and Pax4 genes promotes a somatostatin-producing cell fate specification at the expense of the alpha- and beta-cell lineages in the mouse endocrine pancreas. Development 2005, 132:2969-2980.
16. Collombat P., Xu X., Ravassard P., Sosa-Pineda B., Dussaud S., Billestrup N., Madsen O.D., Serup P., Heimberg H., Mansouri A. The ectopic expression of Pax4 in the mouse pancreas converts progenitor cells into α and subsequently β cells. Cell 2009, 138:449-462.
17. Davidson E.H. The Regulatory Genome: Gene Regulatory Networks 2006, In Development and Evolution Academic Press, London, UK.
18. Davidson E.H. Emerging properties of animal gene regulatory networks. Nature 2010, 468:911-920.
19. Desgraz R., Herrera P.L. Pancreatic neurogenin 3-expressing cells are unipotent islet precursors. Development 2009, 136:3567-3574.
20. Deutsch G., Jung J., Zheng M., Lóra J., Zaret K.S. A bipotential precursor population for pancreas and liver within the embryonic endoderm. Development 2001, 128:871-881.
21. Dhawan S., Georgia S., Tschen S.I., Fan G., Bhushan A. Pancreatic β cell identity is maintained by DNA methylation-mediated repression of Arx. Dev. Cell 2011, 20:419-429.
22. Dorrell C., Schug J., Lin C.F., Canaday P.S., Fox A.J., Smirnova O., Bonnah R., Streeter P.R., Stoeckert C.J., Kaestner K.H., Grompe M. Transcriptomes of the major human pancreatic cell types. Diabetologia 2011, 54:2832-2844.
23. Ejarque M., Cervantes S., Pujadas G., Tutusaus A., Sanchez L., Gasa R. Neurogenin3 cooperates with Foxa2 to autoactivate its own expression. J. Biol. Chem. 2013.
24. Fujikura J., Hosoda K., Kawaguchi Y., Noguchi M., Iwakura H., Odori S., Mori E., Tomita T., Hirata M., Ebihara K., et al. Rbp-j regulates expansion of pancreatic epithelial cells and their differentiation into exocrine cells during mouse development. Dev. Dyn. 2007, 236:2779-2791.
25. Goodyer W.R., Gu X., Liu Y., Bottino R., Crabtree G.R., Kim S.K. Neonatal β cell development in mice and humans is regulated by calcineurin/NFAT. Dev. Cell 2012, 23:21-34.
26. Gouzi M., Kim Y.H., Katsumoto K., Johansson K., Grapin-Botton A. Neurogenin3 initiates stepwise delamination of differentiating endocrine cells during pancreas development. Dev. Dyn. 2011, 240:589-604.
27. Guo T., Landsman L., Li N., Hebrok M. Factors Expressed by Murine Embryonic Pancreatic Mesenchyme Enhance Generation of Insulin-Producing Cells From hESCs. Diabetes 2013, 3:589-604.
28. Hang Y., Stein R. MafA and MafB activity in pancreatic β cells. Trends Endocrinol. Metab. 2011, 22:364-373.
29. Harrison K.A., Thaler J., Pfaff S.L., Gu H., Kehrl J.H. Pancreas dorsal lobe agenesis and abnormal islets of Langerhans in Hlxb9-deficient mice. Nat. Genet. 1999, 23:71-75.
30. Haumaitre C., Fabre M., Cormier S., Baumann C., Delezoide A.-L., Cereghini S. Severe pancreas hypoplasia and multicystic renal dysplasia in two human fetuses carrying novel HNF1beta/MODY5 mutations. Hum. Mol. Genet. 2006, 15:2363-2375.
31. Heit J.J., Apelqvist å A., Gu X., Winslow M.M., Neilson J.R., Crabtree G.R., Kim S.K. Calcineurin/NFAT signalling regulates pancreatic β-cell growth and function. Nature 2006, 443:345-349.
32. Hunter C.S., Dixit S., Cohen T., Ediger B., Wilcox C., Ferreira M., Westphal H., Stein R., May C.L. Islet α-, β-, and δ-Cell Development Is Controlled by the Ldb1 Coregulator, Acting Primarily With the Islet-1 Transcription Factor. Diabetes 2013, 62:875-886.
33. Iype T., Taylor D.G., Ziesmann S.M., Garmey J.C., Watada H., Mirmira R.G. The transcriptional repressor Nkx6.1 also functions as a deoxyribonucleic acid context-dependent transcriptional activator during pancreatic beta-cell differentiation: evidence for feedback activation of the nkx6.1 gene by Nkx6.1. Mol. Endocrinol. 2004, 18:1363-1375.
34. Jensen J., Pedersen E.E., Galante P., Hald J., Heller R.S., Ishibashi M., Kageyama R., Guillemot F., Serup P., Madsen O.D. Control of endodermal endocrine development by Hes-1. Nat. Genet. 2000, 24:36-44.
35. Jiang J., Levine M. Binding affinities and cooperative interactions with bHLH activators delimit threshold responses to the dorsal gradient morphogen. Cell 1993, 72:741-752.
36. Johansson K.A., Dursun U., Jordan N., Gu G., Beermann F., Gradwohl G., Grapin-Botton A. Temporal control of neurogenin3 activity in pancreas progenitors reveals competence windows for the generation of different endocrine cell types. Dev. Cell 2007, 12:457-465.
37. Johnson D.S., Mortazavi A., Myers R.M., Wold B. Genome-wide mapping of in vivo protein-DNA interactions. Science 2007, 316:1497-1502.
38. Kang H.S., Kim Y.-S., ZeRuth G., Beak J.Y., Gerrish K., Kilic G., Sosa-Pineda B., Jensen J., Pierreux C.E., Lemaigre F.P., et al. Transcription factor Glis3, a novel critical player in the regulation of pancreatic beta-cell development and insulin gene expression. Mol. Cell. Biol. 2009, 29:6366-6379.
39. Klochendler A., Weinberg-Corem N., Moran M., Swisa A., Pochet N., Savova V., Vikeså J., Van de Peer Y., Brandeis M., Regev A., et al. A transgenic mouse marking live replicating cells reveals in vivo transcriptional program of proliferation. Dev. Cell 2012, 23:681-690.
40. Kopp J.L., Dubois C.L., Schaffer A.E., Hao E., Shih H.P., Seymour P.A., Ma J., Sander M. Sox9+ ductal cells are multipotent progenitors throughout development but do not produce new endocrine cells in the normal or injured adult pancreas. Development 2011, 138:653-665.
41. Kordowich S., Collombat P., Mansouri A., Serup P. Arx and Nkx2.2 compound deficiency redirects pancreatic alpha- and beta-cell differentiation to a somatostatin/ghrelin co-expressing cell lineage. BMC Dev. Biol. 2011, 11:52.
42. Lango Allen H., Flanagan S.E., Shaw-Smith C., De Franco E., Akerman I., Caswell R., Ferrer J., Hattersley A.T., Ellard S. GATA6 haploinsufficiency causes pancreatic agenesis in humans. Nat. Genet. 2012, 44:20-22. International Pancreatic Agenesis Consortium.
43. Li H., Arber S., Jessell T.M., Edlund H. Selective agenesis of the dorsal pancreas in mice lacking homeobox gene Hlxb9. Nat. Genet. 1999, 23:67-70.
44. Liu J., Hunter C.S., Du A., Ediger B., Walp E., Murray J., Stein R., May C.L. Islet-1 regulates Arx transcription during pancreatic islet alpha-cell development. J. Biol. Chem. 2011, 286:15352-15360.
45. Lynn F.C., Smith S.B., Wilson M.E., Yang K.Y., Nekrep N., German M.S. Sox9 coordinates a transcriptional network in pancreatic progenitor cells. Proc. Natl. Acad. Sci. USA 2007, 104:10500-10505.
46. Lyttle B.M., Li J., Krishnamurthy M., Fellows F., Wheeler M.B., Goodyer C.G., Wang R. Transcription factor expression in the developing human fetal endocrine pancreas. Diabetologia 2008, 51:1169-1180.
47. Magenheim J., Klein A.M., Stanger B.Z., Ashery-Padan R., Sosa-Pineda B., Gu G., Dor Y. Ngn3(+) endocrine progenitor cells control the fate and morphogenesis of pancreatic ductal epithelium. Dev. Biol. 2011, 359:26-36.
48. Martín M., Gallego-Llamas J., Ribes V., Kedinger M., Niederreither K., Chambon P., Dollé P., Gradwohl G. Dorsal pancreas agenesis in retinoic acid-deficient Raldh2 mutant mice. Dev. Biol. 2005, 284:399-411.
49. Masui T., Swift G.H., Hale M.A., Meredith D.M., Johnson J.E., Macdonald R.J. Transcriptional autoregulation controls pancreatic Ptf1a expression during development and adulthood. Mol. Cell. Biol. 2008, 28:5458-5468.
50. McDonald E., Li J., Krishnamurthy M., Fellows G.F., Goodyer C.G., Wang R. SOX9 regulates endocrine cell differentiation during human fetal pancreas development. Int. J. Biochem. Cell Biol. 2012, 44:72-83.
51. Micallef S.J., Li X., Schiesser J.V., Hirst C.E., Yu Q.C., Lim S.M., Nostro M.C., Elliott D.A., Sarangi F., Harrison L.C., et al. INS(GFP/w) human embryonic stem cells facilitate isolation of in vitro derived insulin-producing cells. Diabetologia 2012, 55:694-706.
52. Miyatsuka T., Kosaka Y., Kim H., German M.S. Neurogenin3 inhibits proliferation in endocrine progenitors by inducing Cdkn1a. Proc. Natl. Acad. Sci. USA 2011, 108:185-190.
53. Papatsenko D., Levine M. Quantitative analysis of binding motifs mediating diverse spatial readouts of the Dorsal gradient in the Drosophila embryo. Proc. Natl. Acad. Sci. USA 2005, 102:4966-4971.
54. Papizan J.B., Singer R.A., Tschen S.-I., Dhawan S., Friel J.M., Hipkens S.B., Magnuson M.A., Bhushan A., Sussel L. Nkx2.2 repressor complex regulates islet β-cell specification and prevents β-to-α-cell reprogramming. Genes Dev. 2011, 25:2291-2305.
55. Puri S., Hebrok M. Cellular plasticity within the pancreas-lessons learned from development. Dev. Cell 2010, 18:342-356.
56. Reece-Hoyes J.S., Barutcu A.R., McCord R.P., Jeong J.S., Jiang L., MacWilliams A., Yang X., Salehi-Ashtiani K., Hill D.E., Blackshaw S., et al. Yeast one-hybrid assays for gene-centered human gene regulatory network mapping. Nat. Methods 2011, 8:1050-1052.
57. Ruder W.C., Lu T., Collins J.J. Synthetic biology moving into the clinic. Science 2011, 333:1248-1252.
58. Schaffer A.E., Freude K.K., Nelson S.B., Sander M. Nkx6 transcription factors and Ptf1a function as antagonistic lineage determinants in multipotent pancreatic progenitors. Dev. Cell 2010, 18:1022-1029.
59. Sellick G.S., Barker K.T., Stolte-Dijkstra I., Fleischmann C., Coleman R.J., Garrett C., Gloyn A.L., Edghill E.L., Hattersley A.T., Wellauer P.K., et al. Mutations in PTF1A cause pancreatic and cerebellar agenesis. Nat. Genet. 2004, 36:1301-1305.
60. Seymour P.A., Sander M. Historical perspective: beginnings of the β-cell: current perspectives in β-cell development. Diabetes 2011, 60:364-376.
61. Seymour P.A., Freude K.K., Tran M.N., Mayes E.E., Jensen J., Kist R., Scherer G., Sander M. SOX9 is required for maintenance of the pancreatic progenitor cell pool. Proc. Natl. Acad. Sci. USA 2007, 104:1865-1870.
62. Shannon P., Markiel A., Ozier O., Baliga N.S., Wang J.T., Ramage D., Amin N., Schwikowski B., Ideker T. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 2003, 13:2498-2504.
63. Smith S.B., Watada H., German M.S. Neurogenin3 activates the islet differentiation program while repressing its own expression. Mol. Endocrinol. 2004, 18:142-149.
64. Solar M., Cardalda C., Houbracken I., Martín M., Maestro M.A., De Medts N., Xu X., Grau V., Heimberg H., Bouwens L., Ferrer J. Pancreatic exocrine duct cells give rise to insulin-producing β cells during embryogenesis but not after birth. Dev. Cell 2009, 17:849-860.
65. Stanger B.Z., Tanaka A.J., Melton D.A. Organ size is limited by the number of embryonic progenitor cells in the pancreas but not the liver. Nature 2007, 445:886-891.
66. Stoffers D.A., Zinkin N.T., Stanojevic V., Clarke W.L., Habener J.F. Pancreatic agenesis attributable to a single nucleotide deletion in the human IPF1 gene coding sequence. Nat. Genet. 1997, 15:106-110.
67. Talchai C., Xuan S., Lin H.V., Sussel L., Accili D. Pancreatic β cell dedifferentiation as a mechanism of diabetic β cell failure. Cell 2012, 150:1223-1234.
68. Thompson N., Gésina E., Scheinert P., Bucher P., Grapin-Botton A. RNA profiling and chromatin immunoprecipitation-sequencing reveal that PTF1a stabilizes pancreas progenitor identity via the control of MNX1/HLXB9 and a network of other transcription factors. Mol. Cell. Biol. 2012, 32:1189-1199.
69. Wang S., Hecksher-Sorensen J., Xu Y., Zhao A., Dor Y., Rosenberg L., Serup P., Gu G. Myt1 and Ngn3 form a feed-forward expression loop to promote endocrine islet cell differentiation. Dev. Biol. 2008, 317:531-540.
70. Wang S., Yan J., Anderson D.A., Xu Y., Kanal M.C., Cao Z., Wright C.V.E., Gu G. Neurog3 gene dosage regulates allocation of endocrine and exocrine cell fates in the developing mouse pancreas. Dev. Biol. 2010, 339:26-37.
71. Wiebe P.O., Kormish J.D., Roper V.T., Fujitani Y., Alston N.I., Zaret K.S., Wright C.V.E., Stein R.W., Gannon M. Ptf1a binds to and activates area III, a highly conserved region of the Pdx1 promoter that mediates early pancreas-wide Pdx1 expression. Mol. Cell. Biol. 2007, 27:4093-4104.
72. Xu C.-R., Cole P.A., Meyers D.J., Kormish J., Dent S., Zaret K.S. Chromatin "prepattern" and histone modifiers in a fate choice for liver and pancreas. Science 2011, 332:963-966.
73. Xuan S., Borok M.J., Decker K.J., Battle M.A., Duncan S.A., Hale M.A., Macdonald R.J., Sussel L. Pancreas-specific deletion of mouse Gata4 and Gata6 causes pancreatic agenesis. J. Clin. Invest. 2012, 122:3516-3528.
74. Yang Y.-P., Thorel F., Boyer D.F., Herrera P.L., Wright C.V.E. Context-specific α- to-β-cell reprogramming by forced Pdx1 expression. Genes Dev. 2011, 25:1680-1685.
75. Zaret K.S. Genetic programming of liver and pancreas progenitors: lessons for stem-cell differentiation. Nat. Rev. Genet. 2008, 9:329-340.
76. Zhou Q., Law A.C., Rajagopal J., Anderson W.J., Gray P.A., Melton D.A. A multipotent progenitor domain guides pancreatic organogenesis. Dev. Cell 2007, 13:103-114.
77. Zhou Q., Brown J., Kanarek A., Rajagopal J., Melton D.A. In vivo reprogramming of adult pancreatic exocrine cells to beta-cells. Nature 2008, 455:627-632.