A Gene Regulatory Network Cooperatively Controlled by Pdx1 and Sox9 Governs Lineage Allocation of Foregut Progenitor Cells

Cell Reports

Volumn 13, Issue 2, 2015, Pages 326-336

  Shih, Hung Ping ^a,e   Seymour, Philip A ^a,d   Patel, Nisha A ^a   Xie, Ruiyu ^a   Wang, Allen ^a,f   Liu, Patrick P ^b   Yeo, Gene W ^b   Magnuson, Mark A ^c   Sander, Maike ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c VANDERBILT UNIVERSITY   (United States)

^d University of Copenhagen   (Denmark)

^e University of Macau ^*  (United States)

^f University of Macau   (Macao)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR PDX 1; TRANSCRIPTION FACTOR SOX9; HOMEODOMAIN PROTEIN; PANCREATIC AND DUODENAL HOMEOBOX 1 PROTEIN; SOX9 PROTEIN, MOUSE; TRANSACTIVATOR PROTEIN;

ANIMAL CELL; ARTICLE; CELL FATE; CELL LINEAGE; CONTROLLED STUDY; EMBRYO; FOREGUT; FOREGUT PROGENITOR CELL; GENE ACTIVATION; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENE REPRESSION; INTESTINE CELL; MOUSE; NONHUMAN; PANCREAS CELL; PRIORITY JOURNAL; REGULATORY SEQUENCE; STEM CELL; ANIMAL; CYTOLOGY; EMBRYONIC STEM CELL; GENETICS; INTESTINE; METABOLISM; PANCREAS; TRANSCRIPTION INITIATION;

ANIMALS; CELL LINEAGE; EMBRYONIC STEM CELLS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE REGULATORY NETWORKS; HOMEODOMAIN PROTEINS; INTESTINES; MICE; PANCREAS; SOX9 TRANSCRIPTION FACTOR; TRANS-ACTIVATORS; TRANSCRIPTIONAL ACTIVATION;

EID: 84944051508     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.08.082     Document Type: Article

References (58)

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., Madsen O.D., Serup P. Ptf1a-mediated control of Dll1 reveals an alternative to the lateral inhibition mechanism. Development 2012, 139:33-45.
3. Akiyama H., Chaboissier M.C., Behringer R.R., Rowitch D.H., Schedl A., Epstein J.A., de Crombrugghe B. Essential role of Sox9 in the pathway that controls formation of cardiac valves and septa. Proc. Natl. Acad. Sci. USA 2004, 101:6502-6507.
4. Burlison J.S., Long Q., Fujitani Y., Wright C.V., Magnuson M.A. Pdx-1 and Ptf1a concurrently determine fate specification of pancreatic multipotent progenitor cells. Dev. Biol. 2008, 316:74-86.
5. Calo E., Wysocka J. Modification of enhancer chromatin: what, how, and why?. Mol. Cell 2013, 49:825-837.
6. Carrasco M., Delgado I., Soria B., Martín F., Rojas A. GATA4 and GATA6 control mouse pancreas organogenesis. J. Clin. Invest. 2012, 122:3504-3515.
7. Chen S.X., Osipovich A.B., Ustione A., Potter L.A., Hipkens S., Gangula R., Yuan W., Piston D.W., Magnuson M.A. Quantification of factors influencing fluorescent protein expression using RMCE to generate an allelic series in the ROSA26 locus in mice. Dis. Model. Mech. 2011, 4:537-547.
8. de Vries W.N., Binns L.T., Fancher K.S., Dean J., Moore R., Kemler R., Knowles B.B. Expression of Cre recombinase in mouse oocytes: a means to study maternal effect genes. Genesis 2000, 26:110-112.
9. Dubois C.L., Shih H.P., Seymour P.A., Patel N.A., Behrmann J.M., Ngo V., Sander M. Sox9-haploinsufficiency causes glucose intolerance in mice. PLoS ONE 2011, 6:e23131.
10. Dusing M.R., Maier E.A., Aronow B.J., Wiginton D.A. Onecut-2 knockout mice fail to thrive during early postnatal period and have altered patterns of gene expression in small intestine. Physiol. Genomics 2010, 42:115-125.
11. Frazer K.A., Pachter L., Poliakov A., Rubin E.M., Dubchak I. VISTA: computational tools for comparative genomics. Nucleic Acids Res. 2004, 32:W273-279.
12. Fukuda A., Kawaguchi Y., Furuyama K., Kodama S., Horiguchi M., Kuhara T., Koizumi M., Boyer D.F., Fujimoto K., Doi R., et al. Ectopic pancreas formation in Hes1 -knockout mice reveals plasticity of endodermal progenitors of the gut, bile duct, and pancreas. J. Clin. Invest. 2006, 116:1484-1493.
13. Gao N., White P., Kaestner K.H. Establishment of intestinal identity and epithelial-mesenchymal signaling by Cdx2. Dev. Cell 2009, 16:588-599.
14. Gu G., Dubauskaite J., Melton D.A. Direct evidence for the pancreatic lineage: NGN3+ cells are islet progenitors and are distinct from duct progenitors. Development 2002, 129:2447-2457.
15. 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.
16. Haumaitre C., Barbacci E., Jenny M., Ott M.O., Gradwohl G., Cereghini S. Lack of TCF2/vHNF1 in mice leads to pancreas agenesis. Proc. Natl. Acad. Sci. USA 2005, 102:1490-1495.
17. Holland A.M., Hale M.A., Kagami H., Hammer R.E., MacDonald R.J. Experimental control of pancreatic development and maintenance. Proc. Natl. Acad. Sci. USA 2002, 99:12236-12241.
18. Holmberg J., Perlmann T. Maintaining differentiated cellular identity. Nat. Rev. Genet. 2012, 13:429-439.
19. Huang W., Sherman B.T., Lempicki R.A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 2009, 4:44-57.
20. Jacquemin P., Durviaux S.M., Jensen J., Godfraind C., Gradwohl G., Guillemot F., Madsen O.D., Carmeliet P., Dewerchin M., Collen D., et al. Transcription factor hepatocyte nuclear factor 6 regulates pancreatic endocrine cell differentiation and controls expression of the proendocrine gene ngn3. Mol. Cell. Biol. 2000, 20:4445-4454.
21. 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.
22. Kawaguchi Y., Cooper B., Gannon M., Ray M., MacDonald R.J., Wright C.V. The role of the transcriptional regulator Ptf1a in converting intestinal to pancreatic progenitors. Nat. Genet. 2002, 32:128-134.
23. Kist R., Schrewe H., Balling R., Scherer G. Conditional inactivation of Sox9: a mouse model for campomelic dysplasia. Genesis 2002, 32:121-123.
24. 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.
25. Lee C.S., Sund N.J., Behr R., Herrera P.L., Kaestner K.H. Foxa2 is required for the differentiation of pancreatic alpha-cells. Dev. Biol. 2005, 278:484-495.
26. Lee P.C., Taylor-Jaffe K.M., Nordin K.M., Prasad M.S., Lander R.M., LaBonne C. SUMOylated SoxE factors recruit Grg4 and function as transcriptional repressors in the neural crest. J. Cell Biol. 2012, 198:799-813.
27. Leung V.Y., Gao B., Leung K.K., Melhado I.G., Wynn S.L., Au T.Y., Dung N.W., Lau J.Y., Mak A.C., Chan D., Cheah K.S. SOX9 governs differentiation stage-specific gene expression in growth plate chondrocytes via direct concomitant transactivation and repression. PLoS Genet. 2011, 7:e1002356.
28. Long Q., Shelton K.D., Lindner J., Jones J.R., Magnuson M.A. Efficient DNA cassette exchange in mouse embryonic stem cells by staggered positive-negative selection. Genesis 2004, 39:256-262.
29. 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.
30. Marshak S., Benshushan E., Shoshkes M., Havin L., Cerasi E., Melloul D. Functional conservation of regulatory elements in the pdx-1 gene: PDX-1 and hepatocyte nuclear factor 3beta transcription factors mediate beta-cell-specific expression. Mol. Cell. Biol. 2000, 20:7583-7590.
31. McCracken K.W., Catá E.M., Crawford C.M., Sinagoga K.L., Schumacher M., Rockich B.E., Tsai Y.H., Mayhew C.N., Spence J.R., Zavros Y., Wells J.M. Modelling human development and disease in pluripotent stem-cell-derived gastric organoids. Nature 2014, 516:400-404.
32. Mead T.J., Wang Q., Bhattaram P., Dy P., Afelik S., Jensen J., Lefebvre V. A far-upstream (-70 kb) enhancer mediates Sox9 auto-regulation in somatic tissues during development and adult regeneration. Nucleic Acids Res. 2013, 41:4459-4469.
33. Muzumdar M.D., Tasic B., Miyamichi K., Li L., Luo L. A global double-fluorescent Cre reporter mouse. Genesis 2007, 45:593-605.
34. Nelson S.B., Janiesch C., Sander M. Expression of Nkx6 genes in the hindbrain and gut of the developing mouse. J. Histochem. Cytochem. 2005, 53:787-790.
35. O'Gorman S., Dagenais N.A., Qian M., Marchuk Y. Protamine-Cre recombinase transgenes efficiently recombine target sequences in the male germ line of mice, but not in embryonic stem cells. Proc. Natl. Acad. Sci. USA 1997, 94:14602-14607.
36. Offield M.F., Jetton T.L., Labosky P.A., Ray M., Stein R.W., Magnuson M.A., Hogan B.L., Wright C.V. PDX-1 is required for pancreatic outgrowth and differentiation of the rostral duodenum. Development 1996, 122:983-995.
37. Pedersen J.K., Nelson S.B., Jorgensen M.C., Henseleit K.D., Fujitani Y., Wright C.V., Sander M., Serup P. Endodermal expression of Nkx6 genes depends differentially on Pdx1. Dev. Biol. 2005, 288:487-501. Beta Cell Biology Consortium.
38. Rajagopal N., Xie W., Li Y., Wagner U., Wang W., Stamatoyannopoulos J., Ernst J., Kellis M., Ren B. RFECS: a random-forest based algorithm for enhancer identification from chromatin state. PLoS Comput. Biol. 2013, 9:e1002968.
39. Reginensi A., Clarkson M., Neirijnck Y., Lu B., Ohyama T., Groves A.K., Sock E., Wegner M., Costantini F., Chaboissier M.C., Schedl A. SOX9 controls epithelial branching by activating RET effector genes during kidney development. Hum. Mol. Genet. 2011, 20:1143-1153.
40. Rockich B.E., Hrycaj S.M., Shih H.P., Nagy M.S., Ferguson M.A., Kopp J.L., Sander M., Wellik D.M., Spence J.R. Sox9 plays multiple roles in the lung epithelium during branching morphogenesis. Proc. Natl. Acad. Sci. USA 2013, 110:E4456-4464.
41. 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.
42. Sekido R., Lovell-Badge R. Sex determination involves synergistic action of SRY and SF1 on a specific Sox9 enhancer. Nature 2008, 453:930-934.
43. Seymour P.A., Sander M. Historical perspective: beginnings of the beta-cell: current perspectives in beta-cell development. Diabetes 2011, 60:364-376.
44. 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.
45. Seymour P.A., Freude K.K., Dubois C.L., Shih H.P., Patel N.A., Sander M. A dosage-dependent requirement for Sox9 in pancreatic endocrine cell formation. Dev. Biol. 2008, 323:19-30.
46. Seymour P.A., Shih H.P., Patel N.A., Freude K.K., Xie R., Lim C.J., Sander M. A Sox9/Fgf feed-forward loop maintains pancreatic organ identity. Development 2012, 139:3363-3372.
47. Sherwood R.I., Chen T.Y., Melton D.A. Transcriptional dynamics of endodermal organ formation. Dev. Dyn. 2009, 238:29-42.
48. Shih H.P., Kopp J.L., Sandhu M., Dubois C.L., Seymour P.A., Grapin-Botton A., Sander M. A Notch-dependent molecular circuitry initiates pancreatic endocrine and ductal cell differentiation. Development 2012, 139:2488-2499.
49. Shih H.P., Wang A., Sander M. Pancreas organogenesis: from lineage determination to morphogenesis. Annu. Rev. Cell Dev. Biol. 2013, 29:81-105.
50. Spitz F., Furlong E.E. Transcription factors: from enhancer binding to developmental control. Nat. Rev. Genet. 2012, 13:613-626.
51. Verzi M.P., Shin H., Ho L.L., Liu X.S., Shivdasani R.A. Essential and redundant functions of caudal family proteins in activating adult intestinal genes. Mol. Cell. Biol. 2011, 31:2026-2039.
52. Wang J., Kilic G., Aydin M., Burke Z., Oliver G., Sosa-Pineda B. Prox1 activity controls pancreas morphogenesis and participates in the production of "secondary transition" pancreatic endocrine cells. Dev. Biol. 2005, 286:182-194.
53. Wang A., Yue F., Li Y., Xie R., Harper T., Patel N.A., Muth K., Palmer J., Qiu Y., Wang J., et al. Epigenetic priming of enhancers predicts developmental competence of hESC-derived endodermal lineage intermediates. Cell Stem Cell 2015, 16:386-399.
54. Weedon M.N., Cebola I., Patch A.M., Flanagan S.E., De Franco E., Caswell R., Rodríguez-Seguí S.A., Shaw-Smith C., Cho C.H., Lango Allen H., et al. Recessive mutations in a distal PTF1A enhancer cause isolated pancreatic agenesis. Nat. Genet. 2014, 46:61-64. International Pancreatic Agenesis Consortium.
55. Willet S.G., Hale M.A., Grapin-Botton A., Magnuson M.A., MacDonald R.J., Wright C.V. Dominant and context-specific control of endodermal organ allocation by Ptf1a. Development 2014, 141:4385-4394.
56. Xie R., Everett L.J., Lim H.W., Patel N.A., Schug J., Kroon E., Kelly O.G., Wang A., D'Amour K.A., Robins A.J., et al. Dynamic chromatin remodeling mediated by polycomb proteins orchestrates pancreatic differentiation of human embryonic stem cells. Cell Stem Cell 2013, 12:224-237.
57. 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.
58. Zaret K.S. Genetic programming of liver and pancreas progenitors: lessons for stem-cell differentiation. Nat. Rev. Genet. 2008, 9:329-340.