Specification of hepatopancreas progenitors in zebrafish by hnf1ba and wnt2bb

Development (Cambridge)

Volumn 140, Issue 13, 2013, Pages 2669-2679

  Lancman, Joseph J ^a   Zvenigorodsky, Natasha ^b   Gates, Keith P ^a   Zhang, Danhua ^a   Solomon, Keely ^c   Humphrey, Rohan K ^d   Kuo, Taiyi ^b   Setiawan, Linda ^b   Verkade, Heather ^b,e   Chi, Young In ^f   Jhala, Ulupi S ^d   Wright, Christopher V E ^c   Stainier, Didier Y R ^b,g   Duc Si Dong, P ^a  

^a BURNHAM INSTITUTE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e MONASH UNIVERSITY   (Australia)

^f UNIVERSITY OF MINNESOTA   (United States)

^g MAX PLANCK INSTITUTE FOR HEART AND LUNG RESEARCH   (Germany)

Author keywords

Diabetes; Hnf1b; Liver; MODY; Pancreas; Wnt

Indexed keywords

HEPATOCYTE NUCLEAR FACTOR 1; HEPATOCYTE NUCLEAR FACTOR 1BA; UNCLASSIFIED DRUG; WNT PROTEIN; WNT2BB PROTEIN;

ARTICLE; CONTROLLED STUDY; ENDODERM; HEPATOPANCREAS; IN VIVO STUDY; LOSS OF FUNCTION MUTATION; PRIORITY JOURNAL; WNT SIGNALING PATHWAY; ZEBRA FISH;

DIABETES; HNF1B; LIVER; MODY; PANCREAS; WNT;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CELL DIFFERENTIATION; HEPATOCYTE NUCLEAR FACTOR 1-BETA; HEPATOPANCREAS; SIGNAL TRANSDUCTION; STEM CELLS; WNT PROTEINS; ZEBRAFISH; ZEBRAFISH PROTEINS;

DANIO RERIO;

EID: 84878819258     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.090993     Document Type: Article

References (83)

1. Baranzini, S. E., Mudge, J., van Velkinburgh, J. C., Khankhanian, P., Khrebtukova, I., Miller, N. A., Zhang, L., Farmer, A. D., Bell, C. J., Kim, R. W. et al. (2010). Genome, epigenome and RNA sequences of monozygotic twins discordant for multiple sclerosis. Nature 464, 1351-1356.
2. 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.
3. Barbacci, E., Chalkiadaki, A., Masdeu, C., Haumaitre, C., Lokmane, L., Loirat, C., Cloarec, S., Talianidis, I., Bellanne-Chantelot, C. and Cereghini, S. (2004). HNF1beta/TCF2 mutations impair transactivation potential through altered co-regulator recruitment. Hum. Mol. Genet. 13, 3139-3149.
4. Beckers, D., Bellanné-Chantelot, C. and Maes, M. (2007). Neonatal cholestatic jaundice as the first symptom of a mutation in the hepatocyte nuclear factor-1beta gene (HNF-1beta). J. Pediatr. 150, 313-314.
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. Borowiec, M., Liew, C. W., Thompson, R., Boonyasrisawat, W., Hu, J., Mlynarski, W. M., El Khattabi, I., Kim, S. H., Marselli, L., Rich, S. S. et al. (2009). Mutations at the BLK locus linked to maturity onset diabetes of the young and beta-cell dysfunction. Proc. Natl. Acad. Sci. USA 106, 14460-14465.
7. Bort, R., Martinez-Barbera, J. P., Beddington, R. S. and Zaret, K. S. (2004). Hex homeobox gene-dependent tissue positioning is required for organogenesis of the ventral pancreas. Development 131, 797-806.
8. Bort, R., Signore, M., Tremblay, K., Martinez Barbera, J. P. and Zaret, K. S. (2006). Hex homeobox gene controls the transition of the endoderm to a pseudostratified, cell emergent epithelium for liver bud development. Dev. Biol. 290, 44-56.
9. Brackenridge, A., Pearson, E. R., Shojaee-Moradie, F., Hattersley, A. T., Russell-Jones, D. and Umpleby, A. M. (2006). Contrasting insulin sensitivity of endogenous glucose production rate in subjects with hepatocyte nuclear factor-1beta and -1alpha mutations. Diabetes 55, 405-411.
10. Burlison, J. S., Long, Q., Fujitani, Y., Wright, C. V. and Magnuson, M. A. (2008). Pdx-1 and Ptf1a concurrently determine fate specification of pancreatic multipotent progenitor cells. Dev. Biol. 316, 74-86.
11. Chi, Y. I., Frantz, J. D., Oh, B. C., Hansen, L., Dhe-Paganon, S. and Shoelson, S. E. (2002). Diabetes mutations delineate an atypical POU domain in HNF-1alpha. Mol. Cell 10, 1129-1137.
12. Choe, S. K., Hirsch, N., Zhang, X. and Sagerström, C. G. (2008). hnf1b genes in zebrafish hindbrain development. Zebrafish 5, 179-187.
13. Chung, W. S., Shin, C. H. and Stainier, D. Y. (2008). Bmp2 signaling regulates the hepatic versus pancreatic fate decision. Dev. Cell 15, 738-748.
14. Crosnier, C., Vargesson, N., Gschmeissner, S., Ariza-McNaughton, L., Morrison, A. and Lewis, J. (2005). Delta-Notch signalling controls commitment to a secretory fate in the zebrafish intestine. Development 132, 1093-1104.
15. Deutsch, G., Jung, J., Zheng, M., Lóra, J. and Zaret, K. S. (2001). A bipotential precursor population for pancreas and liver within the embryonic endoderm. Development 128, 871-881.
16. Dong, P. D., Munson, C. A., Norton, W., Crosnier, C., Pan, X., Gong, Z., Neumann, C. J. and Stainier, D. Y. (2007). Fgf10 regulates hepatopancreatic ductal system patterning and differentiation. Nat. Genet. 39, 397-402.
17. Dong, P. D., Provost, E., Leach, S. D. and Stainier, D. Y. (2008). Graded levels of Ptf1a differentially regulate endocrine and exocrine fates in the developing pancreas. Genes Dev. 22, 1445-1450.
18. Dupuis, J., Langenberg, C., Prokopenko, I., Saxena, R., Soranzo, N., Jackson, A. U., Wheeler, E., Glazer, N. L., Bouatia-Naji, N., Gloyn, A. L. et al.; DIAGRAM Consortium; GIANT Consortium; Global BPgen Consortium; Anders Hamsten on behalf of Procardis Consortium; MAGIC investigators (2010). New genetic loci implicated in fasting glucose homeostasis and their impact on type 2 diabetes risk. Nat. Genet. 42, 105-116.
19. Edghill, E. L., Bingham, C., Ellard, S. and Hattersley, A. T. (2006a). Mutations in hepatocyte nuclear factor-1beta and their related phenotypes. J. Med. Genet. 43, 84-90.
20. Edghill, E. L., Bingham, C., Slingerland, A. S., Minton, J. A., Noordam, C., Ellard, S. and Hattersley, A. T. (2006b). 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.
21. Field, H. A., Dong, P. D., Beis, D. and Stainier, D. Y. (2003). Formation of the digestive system in zebrafish. II. Pancreas morphogenesis. Dev. Biol. 261, 197-208.
22. Frayling, T. M. (2007). Genome-wide association studies provide new insights into type 2 diabetes aetiology. Nat. Rev. Genet. 8, 657-662.
23. Fukuda, A., Kawaguchi, Y., Furuyama, K., Kodama, S., Horiguchi, M., Kuhara, T., Koizumi, M., Boyer, D. F., Fujimoto, K., Doi, R. et al. (2006). Ectopic pancreas formation in Hes1 -knockout mice reveals plasticity of endodermal progenitors of the gut, bile duct, and pancreas. J. Clin. Invest. 116, 1484-1493.
24. Gärtner, K. (1990). A third component causing random variability beside environment and genotype. A reason for the limited success of a 30 year long effort to standardize laboratory animals? Lab. Anim. 24, 71-77.
25. Glinka, A., Wu, W., Delius, H., Monaghan, A. P., Blumenstock, C. and Niehrs, C. (1998). Dickkopf-1 is a member of a new family of secreted proteins and functions in head induction. Nature 391, 357-362.
26. Godinho, L., Mumm, J. S., Williams, P. R., Schroeter, E. H., Koerber, A., Park, S. W., Leach, S. D. and Wong, R. O. (2005). Targeting of amacrine cell neurites to appropriate synaptic laminae in the developing zebrafish retina. Development 132, 5069-5079.
27. Goessling, W., North, T. E., Lord, A. M., Ceol, C., Lee, S., Weidinger, G., Bourque, C., Strijbosch, R., Haramis, A. P., Puder, M. et al. (2008). APC mutant zebrafish uncover a changing temporal requirement for wnt signaling in liver development. Dev. Biol. 320, 161-174.
28. Gong, H. Y., Lin, C. J., Chen, M. H., Hu, M. C., Lin, G. H., Zhou, Y., Zon, L. I. and Wu, J. L. (2004). Two distinct teleost hepatocyte nuclear factor 1 genes, hnf1alpha/tcf1 and hnf1beta/tcf2, abundantly expressed in liver, pancreas, gut and kidney of zebrafish. Gene 338, 35-46.
29. 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.
30. 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.
31. He, T. C., Sparks, A. B., Rago, C., Hermeking, H., Zawel, L., da Costa, L. T., Morin, P. J., Vogelstein, B. and Kinzler, K. W. (1998). Identification of c-MYC as a target of the APC pathway. Science 281, 1509-1512.
32. Hebrok, M. (2003). Hedgehog signaling in pancreas development. Mech. Dev. 120, 45-57.
33. Heiser, P. W., Lau, J., Taketo, M. M., Herrera, P. L. and Hebrok, M. (2006). Stabilization of beta-catenin impacts pancreas growth. Development 133, 2023-2032.
34. Heller, R. S., Dichmann, D. S., Jensen, J., Miller, C., Wong, G., Madsen, O. D. and Serup, P. (2002). Expression patterns of Wnts, Frizzleds, sFRPs, and misexpression in transgenic mice suggesting a role for Wnts in pancreas and foregut pattern formation. Dev. Dyn. 225, 260-270.
35. Hesselson, D., Anderson, R. M., Beinat, M. and Stainier, D. Y. (2009). Distinct populations of quiescent and proliferative pancreatic beta-cells identified by HOTcre mediated labeling. Proc. Natl. Acad. Sci. USA 106, 14896-14901.
36. Ho, C. Y., Houart, C., Wilson, S. W. and Stainier, D. Y. (1999). A role for the extraembryonic yolk syncytial layer in patterning the zebrafish embryo suggested by properties of the hex gene. Curr. Biol. 9, 1131-1134.
37. Horikawa, Y., Iwasaki, N., Hara, M., Furuta, H., Hinokio, Y., Cockburn, B. N., Lindner, T., Yamagata, K., Ogata, M., Tomonaga, O. et al. (1997). Mutation in hepatocyte nuclear factor-1 beta gene (TCF2) associated with MODY. Nat. Genet. 17, 384-385.
38. Huang, H., Ruan, H., Aw, M. Y., Hussain, A., Guo, L., Gao, C., Qian, F., Leung, T., Song, H., Kimelman, D. et al. (2008). Mypt1-mediated spatial positioning of Bmp2-producing cells is essential for liver organogenesis. Development 135, 3209-3218.
39. Kaestner, K. H. (2005). The making of the liver: developmental competence in foregut endoderm and induction of the hepatogenic program. Cell Cycle 4, 1146-1148.
40. Kawaguchi, Y., Cooper, B., Gannon, M., Ray, M., MacDonald, R. J. and Wright, C. V. (2002). The role of the transcriptional regulator Ptf1a in converting intestinal to pancreatic progenitors. Nat. Genet. 32, 128-134.
41. 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.
42. Kroon, E., Martinson, L. A., Kadoya, K., Bang, A. G., Kelly, O. G., Eliazer, S., Young, H., Richardson, M., Smart, N. G., Cunningham, J. et al. (2008). Pancreatic endoderm derived from human embryonic stem cells generates glucose-responsive insulin-secreting cells in vivo. Nat. Biotechnol. 26, 443-452.
43. Kumar, M., Jordan, N., Melton, D. and Grapin-Botton, A. (2003). Signals from lateral plate mesoderm instruct endoderm toward a pancreatic fate. Dev. Biol. 259, 109-122.
44. Lee, C. S., Friedman, J. R., Fulmer, J. T. and Kaestner, K. H. (2005). The initiation of liver development is dependent on Foxa transcription factors. Nature 435, 944-947.
45. Lin, J. W., Biankin, A. V., Horb, M. E., Ghosh, B., Prasad, N. B., Yee, N. S., Pack, M. A. and Leach, S. D. (2004). Differential requirement for ptf1a in endocrine and exocrine lineages of developing zebrafish pancreas. Dev. Biol. 274, 491-503.
46. 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.
47. Lu, P., Rha, G. B. and Chi, Y. I. (2007). Structural basis of disease-causing mutations in hepatocyte nuclear factor 1beta. Biochemistry 46, 12071-12080.
48. McLin, V. A., Rankin, S. A. and Zorn, A. M. (2007). Repression of Wnt/betacatenin signaling in the anterior endoderm is essential for liver and pancreas development. Development 134, 2207-2217.
49. Murtaugh, L. C. (2008). The what, where, when and how of Wnt/β-catenin signaling in pancreas development. Organogenesis 4, 81-86.
50. Naylor, R. W., Przepiorski, A., Ren, Q., Yu, J. and Davidson, A. J. (2013). HNF1β is essential for nephron segmentation during nephrogenesis. J. Am. Soc. Nephrol. 24, 77-87.
51. Neff, M. M., Neff, J. D., Chory, J. and Pepper, A. E. (1998). dCAPS, a simple technique for the genetic analysis of single nucleotide polymorphisms: experimental applications in Arabidopsis thaliana genetics. Plant J. 14, 387-392.
52. Noël, E. S., Casal-Sueiro, A., Busch-Nentwich, E., Verkade, H., Dong, P. D., Stemple, D. L. and Ober, E. A. (2008). Organ-specific requirements for Hdac1 in liver and pancreas formation. Dev. Biol. 322, 237-250.
53. Nostro, M. C., Sarangi, F., Ogawa, S., Holtzinger, A., Corneo, B., Li, X., Micallef, S. J., Park, I. H., Basford, C., Wheeler, M. B. et al. (2011). Stagespecific signaling through TGFβ family members and WNT regulates patterning and pancreatic specification of human pluripotent stem cells. Development 138, 861-871.
54. Nyunt, O., Wu, J. Y., McGown, I. N., Harris, M., Huynh, T., Leong, G. M., Cowley, D. M. and Cotterill, A. M. (2009). Investigating maturity onset diabetes of the young. Clin. Biochem. Rev. 30, 67-74.
55. Ober, E. A., Verkade, H., Field, H. A. and Stainier, D. Y. (2006). Mesodermal Wnt2b signalling positively regulates liver specification. Nature 442, 688-691.
56. Offield, M. F., Jetton, T. L., Labosky, P. A., Ray, M., Stein, R. W., Magnuson, M. A., Hogan, B. L. and Wright, C. V. (1996). PDX-1 is required for pancreatic outgrowth and differentiation of the rostral duodenum. Development 122, 983-995.
57. Perry, J. R., McCarthy, M. I., Hattersley, A. T., Zeggini, E., Weedon, M. N., Frayling, T. M.; Wellcome Trust Case Control Consortium (2009). Interrogating type 2 diabetes genome-wide association data using a biological pathway-based approach. Diabetes 58, 1463-1467.
58. 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.
59. Poulain, M. and Ober, E. A. (2011). Interplay between Wnt2 and Wnt2bb controls multiple steps of early foregut-derived organ development. Development 138, 3557-3568.
60. Que, J., Okubo, T., Goldenring, J. R., Nam, K. T., Kurotani, R., Morrisey, E. E., Taranova, O., Pevny, L. H. and Hogan, B. L. (2007). Multiple dose-dependent roles for Sox2 in the patterning and differentiation of anterior foregut endoderm. Development 134, 2521-2531.
61. Raj, A., Rifkin, S. A., Andersen, E. and van Oudenaarden, A. (2010). Variability in gene expression underlies incomplete penetrance. Nature 463, 913-918.
62. 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.
63. Shin, D., Lee, Y., Poss, K. D. and Stainier, D. Y. (2011). Restriction of hepatic competence by Fgf signaling. Development 138, 1339-1348.
64. Sneddon, J. B., Borowiak, M. and Melton, D. A. (2012). Self-renewal of embryonic-stem-cell-derived progenitors by organ-matched mesenchyme. Nature 491, 765-768.
65. 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.
66. Song, J., Kim, H. J., Gong, Z., Liu, N. A. and Lin, S. (2007). Vhnf1 acts downstream of Bmp, Fgf, and RA signals to regulate endocrine beta cell development in zebrafish. Dev. Biol. 303, 561-575.
67. Spence, J. R., Lange, A. W., Lin, S. C., Kaestner, K. H., Lowy, A. M., Kim, I., Whitsett, J. A. and Wells, J. M. (2009). Sox17 regulates organ lineage segregation of ventral foregut progenitor cells. Dev. Cell 17, 62-74.
68. Stoick-Cooper, C. L., Weidinger, G., Riehle, K. J., Hubbert, C., Major, M. B., Fausto, N. and Moon, R. T. (2007). Distinct Wnt signaling pathways have opposing roles in appendage regeneration. Development 134, 479-489.
69. Sumazaki, R., Shiojiri, N., Isoyama, S., Masu, M., Keino-Masu, K., Osawa, M., Nakauchi, H., Kageyama, R. and Matsui, A. (2004). Conversion of biliary system to pancreatic tissue in Hes1-deficient mice. Nat. Genet. 36, 83-87.
70. Sun, Z. and Hopkins, N. (2001). vhnf1, the MODY5 and familial GCKD-associated gene, regulates regional specification of the zebrafish gut, pronephros, and hindbrain. Genes Dev. 15, 3217-3229.
71. 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.
72. Voight, B. F., Scott, L. J., Steinthorsdottir, V., Morris, A. P., Dina, C., Welch, R. P., Zeggini, E., Huth, C., Aulchenko, Y. S., Thorleifsson, G. et al.; MAGIC investigators; GIANT Consortium (2010). Twelve type 2 diabetes susceptibility loci identified through large-scale association analysis. Nat. Genet. 42, 579-589.
73. Wan, H., Korzh, S., Li, Z., Mudumana, S. P., Korzh, V., Jiang, Y. J., Lin, S. and Gong, Z. (2006). Analyses of pancreas development by generation of gfp transgenic zebrafish using an exocrine pancreas-specific elastaseA gene promoter. Exp. Cell Res. 312, 1526-1539.
74. Wandzioch, E. and Zaret, K. S. (2009). Dynamic signaling network for the specification of embryonic pancreas and liver progenitors. Science 324, 1707-1710.
75. Wang, L., Coffinier, C., Thomas, M. K., Gresh, L., Eddu, G., Manor, T., Levitsky, L. L., Yaniv, M. and Rhoads, D. B. (2004). Selective deletion of the Hnf1beta (MODY5) gene in beta-cells leads to altered gene expression and defective insulin release. Endocrinology 145, 3941-3949.
76. Wang, C., Hu, C., Zhang, R., Bao, Y., Ma, X., Lu, J., Qin, W., Shao, X., Xu, J., Lu, H. et al. (2009). Common variants of hepatocyte nuclear factor 1b are associated with type 2 diabetes in a Chinese population. Diabetes [Epub ahead of print] doi: 10.2337/db08-1064.
77. Watt, A. J., Zhao, R., Li, J. and Duncan, S. A. (2007). Development of the mammalian liver and ventral pancreas is dependent on GATA4. BMC Dev. Biol. 7, 37.
78. Weidinger, G., Thorpe, C. J., Wuennenberg-Stapleton, K., Ngai, J. and Moon, R. T. (2005). The Sp1-related transcription factors sp5 and sp5-like act downstream of Wnt/beta-catenin signaling in mesoderm and neuroectoderm patterning. Curr. Biol. 15, 489-500.
79. Wiellette, E. L. and Sive, H. (2003). vhnf1 and Fgf signals synergize to specify rhombomere identity in the zebrafish hindbrain. Development 130, 3821-3829.
80. Wingert, R. A. and Davidson, A. J. (2011). Zebrafish nephrogenesis involves dynamic spatiotemporal expression changes in renal progenitors and essential signals from retinoic acid and irx3b. Dev. Dyn. 240, 2011-2027.
81. Yamaguchi, M., Tonou-Fujimori, N., Komori, A., Maeda, R., Nojima, Y., Li, H., Okamoto, H. and Masai, I. (2005). Histone deacetylase 1 regulates retinal neurogenesis in zebrafish by suppressing Wnt and Notch signaling pathways. Development 132, 3027-3043.
82. Yelon, D., Horne, S. A. and Stainier, D. Y. (1999). Restricted expression of cardiac myosin genes reveals regulated aspects of heart tube assembly in zebrafish. Dev. Biol. 214, 23-37.
83. Zecchin, E., Mavropoulos, A., Devos, N., Filippi, A., Tiso, N., Meyer, D., Peers, B., Bortolussi, M. and Argenton, F. (2004). Evolutionary conserved role of ptf1a in the specification of exocrine pancreatic fates. Dev. Biol. 268, 174-184.