Hnf1b controls pancreas morphogenesis and the generation of Ngn3+ endocrine progenitors

Development (Cambridge)

Volumn 142, Issue 5, 2015, Pages 871-882

  De Vas, Matias G ^a,b   Kopp, Janel L ^c   Heliot, Claire ^a,b   Sander, Maike ^c   Cereghini, Silvia ^a,b   Haumaitre, Cécile ^a,b  

^a Sorbonne Universités   (France)

^b INSERM   (France)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cystic ducts; Hnf1b; Human; MODY5; Mouse; Ngn3; Pancreas; Progenitors

Indexed keywords

HEPATOCYTE NUCLEAR FACTOR 1; HEPATOCYTE NUCLEAR FACTOR 1B; NEUROGENIN 3; UNCLASSIFIED DRUG; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; GLIS3 PROTEIN, MOUSE; HEPATOCYTE NUCLEAR FACTOR 1BETA; HNF1B PROTEIN, MOUSE; NERVE PROTEIN; NEUROG3 PROTEIN, MOUSE; REPRESSOR PROTEIN; TRANSACTIVATOR PROTEIN;

ACINAR CELL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; CYSTIC DUCT; DEVELOPMENTAL STAGE; EMBRYO; EMBRYO DEVELOPMENT; ENDOCRINE CELL; ENDOCRINE PROGENITOR; FEMALE; MATURITY-ONSET DIABETES OF THE YOUNG TYPE 5; MORPHOGENESIS; MOUSE; MULTIPOTENT STEM CELL; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PANCREAS DEVELOPMENT; PRECURSOR; PRIORITY JOURNAL; ANIMAL; CHROMATIN IMMUNOPRECIPITATION; CYTOLOGY; GENETICS; IMMUNOHISTOCHEMISTRY; METABOLISM; PANCREAS; PHYSIOLOGY; PREGNANCY; TUNEL ASSAY;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL DIFFERENTIATION; CHROMATIN IMMUNOPRECIPITATION; CYSTIC DUCT; FEMALE; HEPATOCYTE NUCLEAR FACTOR 1-BETA; IMMUNOHISTOCHEMISTRY; IN SITU NICK-END LABELING; MICE; MULTIPOTENT STEM CELLS; NERVE TISSUE PROTEINS; PANCREAS; PREGNANCY; REPRESSOR PROTEINS; TRANS-ACTIVATORS;

EID: 84923311310     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.110759     Document Type: Article

References (85)

1. Afelik, S. and Jensen, J. (2013). Notch signaling in the pancreas: patterning and cell fate specification. Wiley Interdiscip. Rev. Dev. Biol. 2, 531-544.
2. Ahnfelt-Ronne, J., Jorgensen, M. C., Klinck, R., Jensen, J. N., Fuchtbauer, E.-M., Deering, T., MacDonald, R. J., Wright, C. V. E., Madsen, O. D. and Serup, P. (2012). Ptf1a-mediated control of Dll1 reveals an alternative to the lateral inhibition mechanism. Development 139, 33-45.
3. Apelqvist, A., Li, H., Sommer, L., Beatus, P., Anderson, D. J., Honjo, T., Hrabĕde Angelis, M., Lendahl, U. and Edlund, H. (1999). Notch signalling controls pancreatic cell differentiation. Nature 400, 877-881.
4. Barbacci, E., Reber, M., Ott, M. O., Breillat, C., Huetz, F. and Cereghini, S. (1999). Variant hepatocyte nuclear factor 1 is required for visceral endoderm specification. Development 126, 4795-4805.
5. Bellanné-Chantelot, C., Chauveau, D., Gautier, J.-F., Dubois-Laforgue, D., Clauin, S., Beaufils, S., Wilhelm, J.-M., Boitard, C., Noël, L.-H., Velho, G. et al. (2004). Clinical spectrum associated with hepatocyte nuclear factor-1beta mutations. Ann. Intern. Med. 140, 510-517.
6. Bhushan, A., Itoh, N., Kato, S., Thiery, J. P., Czernichow, P., Bellusci, S. and Scharfmann, R. (2001). Fgf10 is essential for maintaining the proliferative capacity of epithelial progenitor cells during early pancreatic organogenesis. Development 128, 5109-5117.
7. Cano, D. A., Sekine, S. and Hebrok, M. (2006). Primary cilia deletion in pancreatic epithelial cells results in cyst formation and pancreatitis. Gastroenterology 131, 1856-1869.
8. Chen, Y. Z., Gao, Q., Zhao, X. Z., Chen, Y. Z., Bennett, C. L., Xiong, X. S., Mei, C. L., Shi, Y. Q. and Chen, X. M. (2010). Systematic review of TCF2 anomalies in renal cysts and diabetes syndrome/maturity onset diabetes of the young type 5. Chin. Med. J. 123, 3326-3333.
9. Cogswell, C., Price, S. J., Hou, X., Guay-Woodford, L. M., Flaherty, L. and Bryda, E. C. (2003). Positional cloning of jcpk/bpk locus of the mouse. Mamm. Genome 14, 242-249.
10. Drafahl, K. A., McAndrew, C. W., Meyer, A. N., Haas, M. and Donoghue, D. J. (2010). The receptor tyrosine kinase FGFR4 negatively regulates NF-kappaB signaling. PLoS ONE 5, e14412.
11. Dubois, C. L., Shih, H. P., Seymour, P. A., Patel, N. A., Behrmann, J. M., Ngo, V. and Sander, M. (2011). Sox9-haploinsufficiency causes glucose intolerance in mice. PLoS ONE 6, e23131.
12. Edghill, E. L., Bingham, C., Slingerland, A. S., Minton, J. A. L., Noordam, C., Ellard, S. and Hattersley, A. T. (2006). Hepatocyte nuclear factor-1 beta mutations cause neonatal diabetes and intrauterine growth retardation: support for a critical role of HNF-1beta in human pancreatic development. Diabet. Med. 23, 1301-1306.
13. Ejarque, M., Cervantes, S., Pujadas, G., Tutusaus, A., Sanchez, L. and Gasa, R. (2013). Neurogenin3 cooperates with Foxa2 to autoactivate its own expression. J. Biol. Chem. 288, 11705-11717.
14. Esni, F., Ghosh, B., Biankin, A. V., Lin, J. W., Albert, M. A., Yu, X., MacDonald, R. J., Civin, C. I., Real, F. X., Pack, M. A. et al. (2004). Notch inhibits Ptf1 function and acinar cell differentiation in developing mouse and zebrafish pancreas. Development 131, 4213-4224.
15. 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.
16. Ghosh, B. and Leach, S. D. (2006). Interactions between hairy/enhancer of splitrelated proteins and the pancreatic transcription factor Ptf1-p48 modulate function of the PTF1 transcriptional complex. Biochem. J. 393, 679-685.
17. Golson, M. L., Loomes, K. M., Oakey, R. and Kaestner, K. H. (2009). Ductal malformation and pancreatitis in mice caused by conditional Jag1 deletion. Gastroenterology 136, 1761-1771.e1.
18. Gong, Y., Ma, Z., Patel, V., Fischer, E., Hiesberger, T., Pontoglio, M. and Igarashi, P. (2009). HNF-1beta regulates transcription of the PKD modifier gene Kif12. J. Am. Soc. Nephrol. 20, 41-47.
19. 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.
20. Gresh, L., Fischer, E., Reimann, A., Tanguy, M., Garbay, S., Shao, X., Hiesberger, T., Fiette, L., Igarashi, P., Yaniv, M. et al. (2004). A transcriptional network in polycystic kidney disease. EMBO J. 23, 1657-1668.
21. Hald, J., Hjorth, J. P., German, M. S., Madsen, O. D., Serup, P. and Jensen, J. (2003). Activated Notch1 prevents differentiation of pancreatic acinar cells and attenuate endocrine development. Dev. Biol. 260, 426-437.
22. Haldorsen, I. S., Vesterhus, M., Raeder, H., Jensen, D. K., Søvik, O., Molven, A. and Njølstad, P. R. (2008). Lack of pancreatic body and tail in HNF1B mutation carriers. Diabet. Med. 25, 782-787.
23. Hale, M. A., Swift, G. H., Hoang, C. Q., Deering, T. G., Masui, T., Lee, Y.-K., Xue, J. and MacDonald, R. J. (2014). The nuclear hormone receptor family member NR5A2 controls aspects of multipotent progenitor cell formation and acinar differentiation during pancreatic organogenesis. Development 141, 3123-3133.
24. Hart, A., Papadopoulou, S. and Edlund, H. (2003). Fgf10 maintains notch activation, stimulates proliferation, and blocks differentiation of pancreatic epithelial cells. Dev. Dyn. 228, 185-193.
25. Haumaitre, C., Barbacci, E., Jenny, M., Ott, M. O., Gradwohl, G. and Cereghini, S. (2005). Lack of TCF2/vHNF1 in mice leads to pancreas agenesis. Proc. Natl. Acad. Sci. USA 102, 1490-1495.
26. Haumaitre, C., Fabre, M., Cormier, S., Baumann, C., Delezoide, A.-L. and Cereghini, S. (2006). Severe pancreas hypoplasia and multicystic renal dysplasia in two human fetuses carrying novel HNF1beta/MODY5 mutations. Hum. Mol. Genet. 15, 2363-2375.
27. Heliot, C. and Cereghini, S. (2012). Analysis of in vivo transcription factor recruitment by chromatin immunoprecipitation of mouse embryonic kidney. Methods Mol. Biol. 886, 275-291.
28. Heliot, C., Desgrange, A., Buisson, I., Prunskaite-Hyyrylainen, R., Shan, J., Vainio, S., Umbhauer, M. and Cereghini, S. (2013). HNF1B controls proximalintermediate nephron segment identity in vertebrates by regulating Notch signalling components and Irx1/2. Development 140, 873-885.
29. Hiesberger, T., Shao, X., Gourley, E., Reimann, A., Pontoglio, M. and Igarashi, P. (2005). Role of the hepatocyte nuclear factor-1beta (HNF-1beta) C-terminal domain in Pkhd1 (ARPKD) gene transcription and renal cystogenesis. J. Biol. Chem. 280, 10578-10586.
30. Ho, H. K., Pok, S., Streit, S., Ruhe, J. E., Hart, S., Lim, K. S., Loo, H. L., Aung, M. O., Lim, S. G. and Ullrich, A. (2009). Fibroblast growth factor receptor 4 regulates proliferation, anti-apoptosis and alpha-fetoprotein secretion during hepatocellular carcinoma progression and represents a potential target for therapeutic intervention. J. Hepatol. 50, 118-127.
31. Hou, X., Mrug, M., Yoder, B. K., Lefkowitz, E. J., Kremmidiotis, G., D’Eustachio, P., Beier, D. R. and Guay-Woodford, L. M. (2002). Cystin, a novel ciliaassociated protein, is disrupted in the cpk mouse model of polycystic kidney disease. J. Clin. Invest. 109, 533-540.
32. Jacquemin, P., Durviaux, S. M., Jensen, J., Godfraind, C., Gradwohl, G., Guillemot, F., Madsen, O. D., Carmeliet, P., Dewerchin, M., Collen, D. et al. (2000). Transcription factor hepatocyte nuclear factor 6 regulates pancreatic endocrine cell differentiation and controls expression of the proendocrine gene ngn3. Mol. Cell. Biol. 20, 4445-4454.
33. 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.
34. Kaestner, K. H., Katz, J., Liu, Y., Drucker, D. J. and Schutz, G. (1999). Inactivation of the winged helix transcription factor HNF3alpha affects glucose homeostasis and islet glucagon gene expression in vivo. Genes Dev. 13, 495-504.
35. Kang, H. S., Beak, J. Y., Kim, Y.-S., Herbert, R. and Jetten, A. M. (2009a). Glis3 is associated with primary cilia and Wwtr1/TAZ and implicated in polycystic kidney disease. Mol. Cell. Biol. 29, 2556-2569.
36. Kang, H. S., Kim, Y.-S., ZeRuth, G., Beak, J. Y., Gerrish, K., Kilic, G., Sosa- Pineda, B., Jensen, J., Foley, J. and Jetten, A. M. (2009b). Transcription factor Glis3, a novel critical player in the regulation of pancreatic beta-cell development and insulin gene expression. Mol. Cell. Biol. 29, 6366-6379.
37. Kim, Y.-S., Kang, H. S., Takeda, Y., Hom, L., Song, H.-Y., Jensen, J. and Jetten, A. M. (2012). Glis3 regulates neurogenin 3 expression in pancreatic beta-cells and interacts with its activator, Hnf6. Mol. Cells 34, 193-200.
38. Kopp, J. L., Dubois, C. L., Schaffer, A. E., Hao, E., Shih, H. P., Seymour, P. A., Ma, J. and Sander, M. (2011). Sox9+ ductal cells are multipotent progenitors throughout development but do not produce new endocrine cells in the normal or injured adult pancreas. Development 138, 653-665.
39. Kornfeld, J.-W., Baitzel, C., Könner, A. C., Nicholls, H. T., Vogt, M. C., Herrmanns, K., Scheja, L., Haumaitre, C., Wolf, A. M., Knippschild, U. et al. (2013). Obesity-induced overexpression of miR-802 impairs glucose metabolism through silencing of Hnf1b. Nature 494, 111-115.
40. 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.
41. Lemaire, L. A., Goulley, J., Kim, Y. H., Carat, S., Jacquemin, P., Rougemont, J., Constam, D. B. and Grapin-Botton, A. (2015). Bicaudal C1 promotes pancreatic NEUROG3+ endocrine progenitor differentiation and ductal morphogenesis. Development 142, 858-870.
42. Livak, K. J. and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25, 402-408.
43. Lokmane, L., Haumaitre, C., Garcia-Villalba, P., Anselme, I., Schneider- Maunoury, S. and Cereghini, S. (2008). Crucial role of vHNF1 in vertebrate hepatic specification. Development 135, 2777-2786.
44. Lynn, F. C., Smith, S. B., Wilson, M. E., Yang, K. Y., Nekrep, N. and German, M. S. (2007). Sox9 coordinates a transcriptional network in pancreatic progenitor cells. Proc. Natl. Acad. Sci. USA 104, 10500-10505.
45. Maestro, M. A., Boj, S. F., Luco, R. F., Pierreux, C. E., Cabedo, J., Servitja, J. M., German, M. S., Rousseau, G. G., Lemaigre, F. P. and Ferrer, J. (2003). Hnf6 and Tcf2 (MODY5) are linked in a gene network operating in a precursor cell domain of the embryonic pancreas. Hum. Mol. Genet. 12, 3307-3314.
46. 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.
47. Massa, F., Garbay, S., Bouvier, R., Sugitani, Y., Noda, T., Gubler, M.-C., Heidet, L., Pontoglio, M. and Fischer, E. (2013). Hepatocyte nuclear factor 1beta controls nephron tubular development. Development 140, 886-896.
48. Miura, S., Mitsuhashi, N., Shimizu, H., Kimura, F., Yoshidome, H., Otsuka, M., Kato, A., Shida, T., Okamura, D. and Miyazaki, M. (2012). Fibroblast growth factor 19 expression correlates with tumor progression and poorer prognosis of hepatocellular carcinoma. BMC Cancer 12, 56.
49. Mrug, M., Li, R., Cui, X., Schoeb, T. R., Churchill, G. A. and Guay-Woodford, L. M. (2005). Kinesin family member 12 is a candidate polycystic kidney disease modifier in the cpk mouse. J. Am. Soc. Nephrol. 16, 905-916.
50. Murtaugh, L. C., Stanger, B. Z., Kwan, K. M. and Melton, D. A. (2003). Notch signaling controls multiple steps of pancreatic differentiation. Proc. Natl. Acad. Sci. USA 100, 14920-14925.
51. Nammo, T., Yamagata, K., Tanaka, T., Kodama, T., Sladek, F. M., Fukui, K., Katsube, F., Sato, Y., Miyagawa, J.-i. and Shimomura, I. (2008). Expression of HNF-4alpha (MODY1), HNF-1beta (MODY5), and HNF-1alpha (MODY3) proteins in the developing mouse pancreas. Gene Expr. Patterns 8, 96-106.
52. Oliver-Krasinski, J. M., Kasner, M. T., Yang, J., Crutchlow, M. F., Rustgi, A. K., Kaestner, K. H. and Stoffers, D. A. (2009). The diabetes gene Pdx1 regulates the transcriptional network of pancreatic endocrine progenitor cells in mice. J. Clin. Invest. 119, 1888-1898.
53. Pan, F. C. and Wright, C. (2011). Pancreas organogenesis: from bud to plexus to gland. Dev. Dyn. 240, 530-565.
54. 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.
55. Pin, C. L., Rukstalis, J. M., Johnson, C. and Konieczny, S. F. (2001). The bHLH transcription factor Mist1 is required to maintain exocrine pancreas cell organization and acinar cell identity. J. Cell Biol. 155, 519-530.
56. Poll, A. V., Pierreux, C. E., Lokmane, L., Haumaitre, C., Achouri, Y., Jacquemin, P., Rousseau, G. G., Cereghini, S. and Lemaigre, F. P. (2006). A vHNF1/TCF2- HNF6 cascade regulates the transcription factor network that controls generation of pancreatic precursor cells. Diabetes 55, 61-69.
57. Prevot, P.-P., Simion, A., Grimont, A., Colletti, M., Khalaileh, A., Van den Steen, G., Sempoux, C., Xu, X., Roelants, V., Hald, J. et al. (2012). Role of the ductal transcription factors HNF6 and Sox9 in pancreatic acinar-to-ductal metaplasia. Gut 61, 1723-1732.
58. Pulkkinen, M.-A., Spencer-Dene, B., Dickson, C. and Otonkoski, T. (2003). The IIIb isoform of fibroblast growth factor receptor 2 is required for proper growth and branching of pancreatic ductal epithelium but not for differentiation of exocrine or endocrine cells. Mech. Dev. 120, 167-175.
59. Raynaud, P., Tate, J., Callens, C., Cordi, S., Vandersmissen, P., Carpentier, R., Sempoux, C., Devuyst, O., Pierreux, C. E., Courtoy, P. et al. (2011). A classification of ductal plate malformations based on distinct pathogenic mechanisms of biliary dysmorphogenesis. Hepatology 53, 1959-1966.
60. Rieck, S., Bankaitis, E. D. and Wright, C. V. E. (2012). Lineage determinants in early endocrine development. Semin. Cell Dev. Biol. 23, 673-684.
61. Rooman, I., De Medts, N., Baeyens, L., Lardon, J., De Breuck, S., Heimberg, H. and Bouwens, L. (2006). Expression of the Notch signaling pathway and effect on exocrine cell proliferation in adult rat pancreas. Am. J. Pathol. 169, 1206-1214.
62. Rovira, M., Scott, S.-G., Liss, A. S., Jensen, J., Thayer, S. P. and Leach, S. D. (2010). Isolation and characterization of centroacinar/terminal ductal progenitor cells in adult mouse pancreas. Proc. Natl. Acad. Sci. USA 107, 75-80.
63. 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.
64. Senkel, S., Lucas, B., Klein-Hitpass, L. and Ryffel, G. U. (2005). Identification of target genes of the transcription factor HNF1beta and HNF1alpha in a human embryonic kidney cell line. Biochim. Biophys. Acta 1731, 179-190.
65. Seymour, P. A. and Sander, M. (2011). Historical perspective: beginnings of the beta-cell: current perspectives in beta-cell development. Diabetes 60, 364-376.
66. Seymour, P. A., Freude, K. K., Tran, M. N., Mayes, E. E., Jensen, J., Kist, R., Scherer, G. and Sander, M. (2007). SOX9 is required for maintenance of the pancreatic progenitor cell pool. Proc. Natl. Acad. Sci. USA 104, 1865-1870.
67. Seymour, P. A., Freude, K. K., Dubois, C. L., Shih, H.-P., Patel, N. A. and Sander, M. (2008). A dosage-dependent requirement for Sox9 in pancreatic endocrine cell formation. Dev. Biol. 323, 19-30.
68. Seymour, P. A., Shih, H. P., Patel, N. A., Freude, K. K., Xie, R., Lim, C. J. and Sander, M. (2012). A Sox9/Fgf feed-forward loop maintains pancreatic organ identity. Development 139, 3363-3372.
69. Shah, R. N. H., Ibbitt, J. C., Alitalo, K. and Hurst, H. C. (2002). FGFR4 overexpression in pancreatic cancer is mediated by an intronic enhancer activated by HNF1alpha. Oncogene 21, 8251-8261.
70. Shi, G., Zhu, L., Sun, Y., Bettencourt, R., Damsz, B., Hruban, R. H. and Konieczny, S. F. (2009). Loss of the acinar-restricted transcription factor Mist1 accelerates Kras-induced pancreatic intraepithelial neoplasia. Gastroenterology 136, 1368-1378.
71. Shih, D. Q., Navas, M. A., Kuwajima, S., Duncan, S. A. and Stoffel, M. (1999). Impaired glucose homeostasis and neonatal mortality in hepatocyte nuclear factor 3alpha-deficient mice. Proc. Natl. Acad. Sci. USA 96, 10152-10157.
72. Shih, H. P., Kopp, J. L., Sandhu, M., Dubois, C. L., Seymour, P. A., Grapin- Botton, A. and Sander, M. (2012). A Notch-dependent molecular circuitry initiates pancreatic endocrine and ductal cell differentiation. Development 139, 2488-2499.
73. Solar, M., Cardalda, C., Houbracken, I., Martín, 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.
74. Stanger, B. Z., Tanaka, A. J. and Melton, D. A. (2007). Organ size is limited by the number of embryonic progenitor cells in the pancreas but not the liver. Nature 445, 886-891.
75. Tao, B., Bu, S., Yang, Z., Siroky, B., Kappes, J. C., Kispert, A. and Guay- Woodford, L. M. (2009). Cystin localizes to primary cilia via membrane microdomains and a targeting motif. J. Am. Soc. Nephrol. 20, 2570-2580.
76. Verdeguer, F., Le Corre, S., Fischer, E., Callens, C., Garbay, S., Doyen, A., Igarashi, P., Terzi, F. and Pontoglio, M. (2010). A mitotic transcriptional switch in polycystic kidney disease. Nat. Med. 16, 106-110.
77. Ward, C. J., Hogan, M. C., Rossetti, S., Walker, D., Sneddon, T., Wang, X., Kubly, V., Cunningham, J. M., Bacallao, R., Ishibashi, M. et al. (2002). The gene mutated in autosomal recessive polycystic kidney disease encodes a large, receptor-like protein. Nat. Genet. 30, 259-269.
78. Ware, S. M., Aygun, M. G. and Hildebrandt, F. (2011). Spectrum of clinical diseases caused by disorders of primary cilia. Proc. Am. Thorac. Soc. 8, 444-450.
79. Weinstein, M., Xu, X., Ohyama, K. and Deng, C. X. (1998). FGFR-3 and FGFR-4 function cooperatively to direct alveogenesis in the murine lung. Development 125, 3615-3623.
80. Wells, J. M., Esni, F., Boivin, G. P., Aronow, B. J., Stuart, W., Combs, C., Sklenka, A., Leach, S. D. and Lowy, A. M. (2007). Wnt/beta-catenin signaling is required for development of the exocrine pancreas. BMC Dev. Biol. 7, 4.
81. Xuan, S., Borok, M. J., Decker, K. J., Battle, M. A., Duncan, S. A., Hale, M. A., Macdonald, R. J. and Sussel, L. (2012). Pancreas-specific deletion of mouse Gata4 and Gata6 causes pancreatic agenesis. J. Clin. Invest. 122, 3516-3528.
82. Yang, Y., Chang, B. H.-J., Yechoor, V., Chen, W., Li, L., Tsai, M.-J. and Chan, L. (2011). The Krüppel-like zinc finger protein GLIS3 transactivates neurogenin 3 for proper fetal pancreatic islet differentiation in mice. Diabetologia 54, 2595-2605.
83. Ye, Y. W., Zhou, Y., Yuan, L., Wang, C. M., Du, C. Y., Zhou, X. Y., Zheng, B. Q., Cao, X., Sun, M. H., Fu, H. et al. (2011). Fibroblast growth factor receptor 4 regulates proliferation and antiapoptosis during gastric cancer progression. Cancer 117, 5304-5313.
84. 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.
85. Zhu, L., Tran, T., Rukstalis, J. M., Sun, P., Damsz, B. and Konieczny, S. F. (2004). Inhibition of Mist1 homodimer formation induces pancreatic acinar-to-ductal metaplasia. Mol. Cell. Biol. 24, 2673-2681.