Bicaudal C1 promotes pancreatic NEUROG3+ endocrine progenitor differentiation and ductal morphogenesis

Development (Cambridge)

Volumn 142, Issue 5, 2015, Pages 858-870

  Lemaire, Laurence A ^a,b   Goulley, Joan ^b   Kim, Yung Hae ^a,b   Carat, Solenne ^b   Jacquemin, Patrick ^c   Rougemont, Jacques ^b   Constam, Daniel B ^b   Grapin Botton, Anne ^a,b  

^a University of Copenhagen   (Denmark)

^b EPFL   (Switzerland)

^c UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

Author keywords

Beta cell; Cysts; Diabetes; Differentiation; Embryo; Endocrine; Insulin; MODY5; Pancreas; Progenitors; RNA binding protein

Indexed keywords

BICAUDAL C1 PROTEIN; HEPATOCYTE NUCLEAR FACTOR 1BETA; HEPATOCYTE NUCLEAR FACTOR 3BETA; NEUROGENIN 3; ONECUT1 PROTEIN; POLYCYSTIN 2; RNA BINDING PROTEIN; TRANSCRIPTION FACTOR PDX 1; TRANSCRIPTION FACTOR SOX9; TRANSCRIPTOME; UNCLASSIFIED DRUG; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; BICC1 PROTEIN, MOUSE; HEPATOCYTE NUCLEAR FACTOR 6; NERVE PROTEIN; NEUROG3 PROTEIN, MOUSE; ONECUT1 PROTEIN, MOUSE; POLYCYSTIC KIDNEY DISEASE 2 PROTEIN; POLYCYSTIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL INFILTRATION; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; ENDOCRINE CELL; GENE INACTIVATION; IMMUNOCOMPETENT CELL; MORPHOGENESIS; MOUSE; NONHUMAN; ORGANOGENESIS; PANCREAS DEVELOPMENT; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; STEM CELL; ANIMAL; CYTOLOGY; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; GENOTYPE; METABOLISM; NICK END LABELING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS; WESTERN BLOTTING;

MUS;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BLOTTING, WESTERN; FLUORESCENT ANTIBODY TECHNIQUE; GENOTYPE; HEPATOCYTE NUCLEAR FACTOR 6; IN SITU NICK-END LABELING; MICE; NERVE TISSUE PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA-BINDING PROTEINS; SEQUENCE ANALYSIS, RNA; STEM CELLS; TRPP CATION CHANNELS;

EID: 84923284119     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.114611     Document Type: Article

References (81)

1. Apelqvist, Å., 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.
2. Apte, M. V., Haber, P. S., Darby, S. J., Rodgers, S. C., McCaughan, G. W., Korsten, M. A., Pirola, R. C. and Wilson, J. S. (1999). Pancreatic stellate cells are activated by proinflammatory cytokines: implications for pancreatic fibrogenesis. Gut 44, 534-541.
3. Ashcroft, F. M. and Rorsman, P. (2012). Diabetes mellitus and the β cell: the last ten years. Cell 148, 1160-1171.
4. Barbacci, E., Reber, M., Ott, M., 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., Clauin, S., Chauveau, D., Collin, P., Daumont, M., Douillard, C., Dubois-Laforgue, D., Dusselier, L., Gautier, J.-F., Jadoul, M. et al. (2005). Large genomic rearrangements in the hepatocyte nuclear factor- 1beta (TCF2) gene are the most frequent cause of maturity-onset diabetes of the young type 5. Diabetes 54, 3126-3132.
6. Bergmann, C., Fliegauf, M., Brüchle, N. O., Frank, V., Olbrich, H., Kirschner, J., Schermer, B., Schmedding, I., Kispert, A., Kränzlin, B. et al. (2008). Loss of nephrocystin-3 function can cause embryonic lethality, Meckel-Gruber-like syndrome, situs inversus, and renal-hepatic-pancreatic dysplasia. Am. J. Hum. Genet. 82, 959-970.
7. Bingham, C. and Hattersley, A. T. (2004). Renal cysts and diabetes syndrome resulting from mutations in hepatocyte nuclear factor-1beta. Nephrol. Dial. Transplant. 19, 2703-2708.
8. Cai, Q., Brissova, M., Reinert, R. B., Pan, F. C., Brahmachary, P., Jeansson, M., Shostak, A., Radhika, A., Poffenberger, G., Quaggin, S. E. et al. (2012). Enhanced expression of VEGF-A in β cells increases endothelial cell number but impairs islet morphogenesis and β cell proliferation. Dev. Biol. 367, 40-54.
9. Cano, D. A., Murcia, N. S., Pazour, G. J. and Hebrok, M. (2004). Orpk mouse model of polycystic kidney disease reveals essential role of primary cilia in pancreatic tissue organization. Development 131, 3457-3467.
10. 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.
11. Chang, M. Y., Parker, E., Ibrahim, S., Shortland, J. R., Nahas, M. E., Haylor, J. L. and Ong, A. C. M. (2006). Haploinsufficiency of Pkd2 is associated with increased tubular cell proliferation and interstitial fibrosis in two murine Pkd2 models. Nephrol. Dial. Transplant. 21, 2078-2084.
12. 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.
13. Cortijo, C., Gouzi, M., Tissir, F. and Grapin-Botton, A. (2012). Planar cell polarity controls pancreatic beta cell differentiation and glucose homeostasis. Cell Rep. 2, 1593-1606.
14. Desgraz, R. and Herrera, P. L. (2009). Pancreatic neurogenin 3-expressing cells are unipotent islet precursors. Development 136, 3567-3574.
15. Dessimoz, J., Bonnard, C., Huelsken, J. and Grapin-Botton, A. (2005). Pancreas-specific deletion of beta-catenin reveals Wnt-dependent and Wntindependent functions during development. Curr. Biol. 15, 1677-1683.
16. De Vas, M. G., Kopp, J. L., Heliot, C., Sander, M., Cereghini, S. and Haumaitre, C. (2015). Hnf1b controls pancreas morphogenesis and generation of Ngn3+ endocrine progenitors. Development 142, 871-882.
17. 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.
18. Fiskerstrand, T., Houge, G., Sund, S., Scheie, D., Leh, S., Boman, H. and Knappskog, P. M. (2010). Identification of a gene for renal-hepatic-pancreatic dysplasia by microarray-based homozygosity mapping. J. Mol. Diagn. 12, 125-131.
19. Flaherty, L., Bryda, E. C., Collins, D., Rudofsky, U. and Montogomery, J. C. (1995). New mouse model for polycystic kidney disease with both recessive and dominant gene effects. Kidney Int. 47, 552-558.
20. Fossdal, R., Böðarsson, M., Ásmundsson, P., Ragnarsson, J., Peters, D., Breuning, M. H. and Jensson, O. (1993). Icelandic families with autosomal dominant polycystic kidney disease: families unlinked to chromosome 16p13.3 revealed by linkage analysis. Hum. Genet. 91, 609-613.
21. Gamberi, C. and Lasko, P. (2012). The bic-C family of developmental translational regulators. Comp. Funct. Genomics 2012, 141386.
22. Geutskens, S. B., Otonkoski, T., Pulkkinen, M.-A., Drexhage, H. A. and Leenen, P. J. M. (2005). Macrophages in the murine pancreas and their involvement in fetal endocrine development in vitro. J. Leukoc. Biol. 78, 845-852.
23. 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.
24. Green, J. S., Parfrey, P. S., Harnett, J. D., Farid, N. R., Cramer, B. C., Johnson, G., Heath, O., McManamon, P. J., O’Leary, E. and Pryse-Phillips, W. (1989). The cardinal manifestations of Bardet-Biedl syndrome, a form of Laurence-Moon- Biedl syndrome. N. Engl. J. Med. 321, 1002-1009.
25. 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.
26. Gu, G., Dubauskaite, J. and Melton, D. A. (2002). Direct evidence for the pancreatic lineage: NGN3+ cells are islet progenitors and are distinct from duct progenitors. Development 129, 2447-2457.
27. Haber, P. S., Keogh, G. W., Apte, M. V., Moran, C. S., Stewart, N. L., Crawford, D. H. G., Pirola, R. C., McCaughan, G. W., Ramm, G. A. and Wilson, J. S. (1999). Activation of pancreatic stellate cells in human and experimental pancreatic fibrosis. Am. J. Pathol. 155, 1087-1095.
28. Harris, P. C. and Torres, V. E. (2009). Polycystic kidney disease. Annu. Rev. Med. 60, 321-337.
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. 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.
32. Ivemark, B., Oldfelt, V. and Zetterstrom, R. (1959). Familial dysplasia of kidneys, liver and pancreas: a probably genetically determined syndrome. Acta Paediatr. 48, 1-11.
33. 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.
34. Jensen, J., Pedersen, E. E., Galante, P. 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.
35. Johansson, K. A., Dursun, U., Jordan, N., Gu, G., Beermann, F., Gradwohl, G. and 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.
36. Kang, H. S., Kim, Y.-S., ZeRuth, G., Beak, J. Y., Gerrish, K., Kilic, G., Sosa- Pineda, B., Jensen, J., Foley, J., Jetten, A. M. (2009). 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. Karihaloo, A., Koraishy, F., Huen, S. C., Lee, Y., Merrick, D., Caplan, M. J., Somlo, S. and Cantley, L. G. (2011). Macrophages promote cyst growth in polycystic kidney disease. J. Am. Soc. Nephrol. 22, 1809-1814.
38. Kesavan, G., Sand, F.W., Greiner, T. U., Johansson, J. K., Kobberup, S., Wu, X., Brakebusch, C. and Semb, H. (2009). Cdc42-mediated tubulogenesis controls cell specification. Cell 139, 791-801.
39. Kousta, E., Hadjiathanasiou, C. G., Tolis, G. and Papathanasiou, A. (2009). Pleiotropic genetic syndromes with developmental abnormalities associated with obesity. J. Pediatr. Endocrinol. Metab. 22, 581-592.
40. Kraus, M. R.-C., Clauin, S., Pfister, Y., Di Maïo, M., Ulinski, T., Constam, D., Bellanné-Chantelot, C. and Grapin-Botton, A. (2012). Two mutations in human BICC1 resulting in Wnt pathway hyperactivity associated with cystic renal dysplasia. Hum. Mutat. 33, 86-90.
41. Langmead, B., Trapnell, C., Pop, M. and Salzberg, S. L. (2009). Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10, pR25.
42. 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.
43. Lu, W., Peissel, B., Babakhanlou, H., Pavlova, A., Geng, L., Fan, X., Larson, C., Brent, G. and Zhou, J. (1997). Perinatal lethality with kidney and pancreas defects in mice with a targetted Pkd1 mutation. Nat. Genet. 17, 179-181.
44. Lustig, B., Jerchow, B., Sachs, M., Weiler, S., Pietsch, T., Karsten, U., van de Wetering, M., Clevers, H., Schlag, P. M., Birchmeier, W. et al. (2002). Negative feedback loop of Wnt signaling through upregulation of conductin/axin2 in colorectal and liver tumors. Mol. Cell. Biol. 22, 1184-1193.
45. 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.
46. 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.
47. 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.
48. Mahone, M., Saffman, E. E. and Lasko, P. F. (1995). Localized Bicaudal-C RNA encodes a protein containing a KH domain, the RNA binding motif of FMR1. EMBO J. 14, 2043-2055.
49. Maisonneuve, C., Guilleret, I., Vick, P., Weber, T., Andre, P., Beyer, T., Blum, M. and Constam, D. B. (2009). BicaudalC, a novel regulator of Dvl signaling abutting RNA-processing bodies, controls cilia orientation and leftward flow. Development 136, 3019-3030.
50. Marshall, J. D., Bronson, R. T., Collin, G. B., Nordstrom, A. D., Maffei, P., Paisey, R. B., Carey, C., MacDermott, S., Russell-Eggitt, I., Shea, S. E. et al. (2005). New Alström syndrome phenotypes based on the evaluation of 182 cases. Arch. Intern. Med. 165, 675-683.
51. Masamune, A., Watanabe, T., Kikuta, K. and Shimosegawa, T. (2009). Roles of pancreatic stellate cells in pancreatic inflammation and fibrosis. Clin. Gastroenterol. Hepatol. 7, S48-S54.
52. Mesner, L. D., Ray, B., Hsu, Y.-H., Manichaikul, A., Lum, E., Bryda, E. C., Rich, S. S., Rosen, C. J., Criqui, M. H., Allison, M. et al. (2014). Bicc1 is a genetic determinant of osteoblastogenesis and bone mineral density. J. Clin. Invest. 124, 2736-2749.
53. Nauta, J., Ozawa, Y., Sweeney, W. E., Rutledge, J. C. and Avner, E. D. (1993). Renal and biliary abnormalities in a new murine model of autosomal recessive polycystic kidney disease. Pediatr. Nephrol. 7, 163-172.
54. Pan, F. C. and Wright, C. (2011). Pancreas organogenesis: from bud to plexus to gland. Dev. Dyn. 240, 530-565.
55. Piazzon, N., Maisonneuve, C., Guilleret, I., Rotman, S. and Constam, D. B. (2012). Bicc1 links the regulation of cAMP signaling in polycystic kidneys to microRNA-induced gene silencing. J. Mol. Cell Biol. 4, 398-408.
56. 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.
57. Reeders, S. T., Breuning, M. H., Davies, K. E., Nicholls, R. D., Jarman, A. P., Higgs, D. R., Pearson, P. L. and Weatherall, D. J. (1985). A highly polymorphic DNA marker linked to adult polycystic kidney disease on chromosome 16. Nature 317, 542-544.
58. Rees, S., Kittikulsuth, W., Roos, K., Strait, K. A., Van Hoek, A. and Kohan, D. E (2014). Adenylyl Cyclase 6 deficiency ameliorates polycystic kidney disease. J. Am. Soc. Nephrol. 25, 232-237.
59. Saffman, E., Styhler, S., Rother, K., Li, W., Richard, S. and Lasko, P. (1998). Premature translation of oskar in oocytes lacking the RNA-binding protein bicaudal-C. Mol. Cell. Biol. 18, 4855-4862.
60. Schmid-Kotsas, A., Gross, H.-J., Menke, A., Weidenbach, H., Adler, G., Siech, M., Beger, H., Grünert, A. and Bachem, M. G. (1999). Lipopolysaccharideactivated macrophages stimulate the synthesis of collagen type I and C-fibronectin in cultured pancreatic stellate cells. Am. J. Pathol. 155, 1749-1758.
61. Schonhoff, S. E., Giel-Moloney, M. and Leiter, A. B. (2004). Neurogenin 3- expressing progenitor cells in the gastrointestinal tract differentiate into both endocrine and non-endocrine cell types. Dev. Biol. 270, 443-454.
62. Seneé, V., Chelala, C., Duchatelet, S., Feng, D., Blanc, H., Cossec, J.-C., Charon, C., Nicolino, M., Boileau, P., Cavener, D. R. et al. (2006). Mutations in GLIS3 are responsible for a rare syndrome with neonatal diabetes mellitus and congenital hypothyroidism. Nat. Genet. 38, 682-687.
63. 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.
64. Shi, C., Washington, M. K., Chaturvedi, R., Drosos, Y., Revetta, F. L., Weaver, C. J., Buzhardt, E., Yull, F. E., Blackwell, T. S., Sosa-Pineda, B. et al. (2014). Fibrogenesis in pancreatic cancer is a dynamic process regulated by macrophage-stellate cell interaction. Lab. Invest. 94, 409-421.
65. 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.
66. Srinivas, S., Watanabe, T., Lin, C.-S., William, C. M., Tanabe, Y., Jessell, T. M. and Costantini, F. (2001). Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev. Biol. 1, 4.
67. Swenson-Fields, K. I., Vivian, C. J., Salah, S. M., Peda, J. D., Davis, B. M., van Rooijen, N., Wallace, D. P. and Fields, T. A. (2013). Macrophages promote polycystic kidney disease progression. Kidney Int. 83, 855-864.
68. Ta, M. H. T., Harris, D. C. H. and Rangan, G. K. (2013). Role of interstitial inflammation in the pathogenesis of polycystic kidney disease. Nephrology (Carlton) 18, 317-330.
69. Taha, D., Barbar, M., Kanaan, H. and Williamson Balfe, J. (2003). Neonatal diabetes mellitus, congenital hypothyroidism, hepatic fibrosis, polycystic kidneys, and congenital glaucoma: a new autosomal recessive syndrome? Am. J. Med. Genet. A 122A, 269-273.
70. Thompson, N., Gésina, E., Scheinert, P., Bucher, P. and Grapin-Botton, A. (2012). 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. 32, 1189-1199.
71. Tran, U., Zakin, L., Schweickert, A., Agrawal, R., Doger, R., Blum, M., De Robertis, E. M. and Wessely, O. (2010). The RNA-binding protein bicaudal C regulates polycystin 2 in the kidney by antagonizing miR-17 activity. Development 137, 1107-1116.
72. Ulinski, T., Lescure, S., Beaufils, S., Guigonis, V., Decramer, S., Morin, D., Clauin, S., Deschênes, G., Bouissou, F., Bensman, A. et al. (2006). Renal phenotypes related to hepatocyte nuclear factor-1beta (TCF2) mutations in a pediatric cohort. J. Am. Soc. Nephrol. 17, 497-503.
73. Vanhorenbeeck, V., Jenny, M., Cornut, J.-F., Gradwohl, G., Lemaigre, F. P., Rousseau, G. G. and Jacquemin, P. (2007). Role of the Onecut transcription factors in pancreas morphogenesis and in pancreatic and enteric endocrine differentiation. Dev. Biol. 305, 685-694.
74. Vankalakunti, M., Gupta, K., Kakkar, N. and Das, A. (2007). Renal-hepaticpancreatic dysplasia syndrome (Ivemark’s syndrome). Diagn. Pathol. 2, 24.
75. 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.
76. Villiger, M., Goulley, J., Friedrich, M., Grapin-Botton, A., Meda, P., Lasser, T. and Leitgeb, R. A. (2009). In vivo imaging of murine endocrine islets of Langerhans with extended-focus optical coherence microscopy. Diabetologia 52, 1599-1607.
77. Wang, S., Zhang, J., Zhao, A., Hipkens, S., Magnuson, M. A. and Gu, G. (2007). Loss of Myt1 function partially compromises endocrine islet cell differentiation and pancreatic physiological function in the mouse. Mech. Dev. 124, 898-910.
78. Wang, S., Hecksher-Sorensen, J., Xu, Y., Zhao, A., Dor, Y., Rosenberg, L., Serup, P. and Gu, G. (2008). Myt1 and Ngn3 form a feed-forward expression loop to promote endocrine islet cell differentiation. Dev. Biol. 317, 531-540.
79. Wessely, O., Tran, U., Zakin, L. and De Robertis, E. M. (2001). Identification and expression of the mammalian homologue of Bicaudal-C. Mech. Dev. 101, 267-270.
80. Wu, G., Markowitz, G. S., Li, L., D’Agati, V. D., Factor, S. M., Geng, L., Tibara, S., Tuchman, J., Cai, Y., Park, J. H. et al. (2000). Cardiac defects and renal failure in mice with targeted mutations in Pkd2. Nat. Genet. 24, 75-78.
81. 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.