Human pancreas development

Development (Cambridge)

Volumn 142, Issue 18, 2015, Pages 3126-3137

  Jennings, Rachel E ^a,b   Berry, Andrew A ^a   Strutt, James P ^a   Gerrard, David T ^a   Hanley, Neil A ^a,b  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b MANCHESTER UNIVERSITY NHS FOUNDATION TRUST   (United Kingdom)

Author keywords

Development; Embryo; Endoderm; Fetal; Foregut; Gestation; Human; Liver; Pancreas; Stem cells; Transcription factor; cells

Indexed keywords

HEPATOCYTE NUCLEAR FACTOR 1BETA; NEUROGENIC DIFFERENTIATION FACTOR; NEUROGENIN 3; PANCREAS SPECIFIC TRANSCRIPTION FACTOR 1A; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR GATA 4; TRANSCRIPTION FACTOR GATA 6; TRANSCRIPTION FACTOR MNX1; TRANSCRIPTION FACTOR NEK8; TRANSCRIPTION FACTOR NKX2.2; TRANSCRIPTION FACTOR NPHP3; TRANSCRIPTION FACTOR PAX6; TRANSCRIPTION FACTOR PDX 1; TRANSCRIPTION FACTOR RFX6; TRANSCRIPTION FACTOR SOX9; TRANSCRIPTION FACTOR UBR1; UNCLASSIFIED DRUG;

CELL DIFFERENTIATION; CELL PROLIFERATION; DIABETES MELLITUS; EMBRYO DEVELOPMENT; ENDOCRINE CELL; ENDOCRINE SYSTEM; ENDODERM; FETUS DEVELOPMENT; FOREGUT; GENE MUTATION; HUMAN; HUMAN DEVELOPMENT; HYPOPLASIA; IN VITRO STUDY; PANCREAS; PANCREAS AGENESIS; PANCREAS DUCT; PANCREAS HYPOPLASIA; PANCREAS ISLET ALPHA CELL; PANCREAS ISLET BETA CELL; PANCREAS MALFORMATION; PLURIPOTENT STEM CELL; PREGNANCY; PRIORITY JOURNAL; REVIEW; CYTOLOGY; EMBRYOLOGY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; MORPHOGENESIS; PHYSIOLOGY; SPECIES DIFFERENCE;

CELL DIFFERENTIATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; INSULIN-SECRETING CELLS; MORPHOGENESIS; PANCREAS; PLURIPOTENT STEM CELLS; SPECIES SPECIFICITY;

EID: 84942162894     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.120063     Document Type: Review

References (122)

1. Ashar, H. R., Chouinard, R. A., Jr., Dokur, M. and Chada, K. (2010). In vivo modulation of HMGA2 expression. Biochim. Biophys. Acta 1799, 55-61.
2. Assady, S., Maor, G., Amit, M., Itskovitz-Eldor, J., Skorecki, K. L. and Tzukerman, M. (2001). Insulin production by human embryonic stem cells. Diabetes 50, 1691-1697.
3. Baxter, M., Withey, S., Harrison, S., Segeritz, C.-P., Zhang, F., Atkinson-Dell, R., Rowe, C., Gerrard, D. T., Sison-Young, R., Jenkins, R. et al. (2015). Phenotypic and functional analyses show stem cell-derived hepatocyte-like cells better mimic fetal rather than adult hepatocytes. J. Hepatol. 62, 581-589.
4. 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.
5. 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.
6. Body-Bechou, D., Loget, P., D’Herve, D., Le Fiblec, B., Grebille, A.-G., Le Guern, H., Labarthe, C., Redpath, M., Cabaret-Dufour, A.-S., Sylvie, O. et al. (2014). TCF2/HNF-1beta mutations: 3 cases of fetal severe pancreatic agenesis or hypoplasia and multicystic renal dysplasia. Prenat. Diagn. 34, 90-93.
7. Bonal, C. and Herrera, P. L. (2008). Genes controlling pancreas ontogeny. Int. J. Dev. Biol. 52, 823-835.
8. Bonfanti, P., Nobecourt, E., Oshima, M., Albagli-Curiel, O., Laurysens, V., Stangé, G., Sojoodi, M., Heremans, Y., Heimberg, H. and Scharfmann, R. (2015). Ex vivo expansion and differentiation of human and mouse fetal pancreatic progenitors are modulated by epidermal growth factor. Stem Cells Dev. 24, 1766-1778.
9. Bonnefond, A., Sand, O., Guerin, B., Durand, E., De Graeve, F., Huyvaert, M., Rachdi, L., Kerr-Conte, J., Pattou, F., Vaxillaire, M. et al. (2012). GATA6 inactivating mutations are associated with heart defects and, inconsistently, with pancreatic agenesis and diabetes. Diabetologia 55, 2845-2847.
10. Bonnefond, A., Vaillant, E., Philippe, J., Skrobek, B., Lobbens, S., Yengo, L., Huyvaert, M., Cavé, H., Busiah, K., Scharfmann, R. et al. (2013). Transcription factor gene MNX1 is a novel cause of permanent neonatal diabetes in a consanguineous family. Diabetes Metab. 39, 276-280.
11. Bramswig, N. C., Everett, L. J., Schug, J., Dorrell, C., Liu, C., Luo, Y., Streeter, P. R., Naji, A., Grompe, M. and Kaestner, K. H. (2013). Epigenomic plasticity enables human pancreatic alpha to beta cell reprogramming. J. Clin. Invest. 123, 1275-1284.
12. Capito, C., Simon, M.-T., Aiello, V., Clark, A., Aigrain, Y., Ravassard, P. and Scharfmann, R. (2013). Mouse muscle as an ectopic permissive site for human pancreatic development. Diabetes 62, 3479-3487.
13. Carrasco, M., Delgado, I., Soria, B., Martín, F. and Rojas, A. (2012). GATA4 and GATA6 control mouse pancreas organogenesis. J. Clin. Invest. 122, 3504-3515.
14. Castaing, M., Péault, B., Basmaciogullari, A., Casal, I., Czernichow, P. and Scharfmann, R. (2001). Blood glucose normalization upon transplantation of human embryonic pancreas into beta-cell-deficient SCID mice. Diabetologia 44, 2066-2076.
15. Castaing, M., Duvillié, B., Quemeneur, E., Basmaciogullari, A. and Scharfmann, R. (2005). Ex vivo analysis of acinar and endocrine cell development in the human embryonic pancreas. Dev. Dyn. 234, 339-345.
16. Cebola, I., Rodríguez-Seguí, S., Cho, C. H.-H., Bessa, J., Rovira, M., Luengo, M., Chhatriwala, M., Berry, A., Ponsa-Cobas, J., Maestro, M. A., et al. (2015). TEAD and YAP regulate the enhancer network of human embryonic pancreatic progenitors. Nat. Cell Biol. 17, 615-626.
17. Chandra, V., Albagli-Curiel, O., Hastoy, B., Piccand, J., Randriamampita, C., Vaillant, E., Cavé, H., Busiah, K., Froguel, P., Vaxillaire, M. et al. (2014). RFX6 regulates insulin secretion by modulating Ca2+ homeostasis in human beta cells. Cell Rep. 9, 2206-2218.
18. D’Amour, K. A., Agulnick, A. D., Eliazer, S., Kelly, O. G., Kroon, E. and Baetge, E. E. (2005). Efficient differentiation of human embryonic stem cells to definitive endoderm. Nat. Biotechnol. 23, 1534-1541.
19. D’Amour, K. A., Bang, A. G., Eliazer, S., Kelly, O. G., Agulnick, A. D., Smart, N. G., Moorman, M. A., Kroon, E., Carpenter, M. K. and Baetge, E. E. (2006). Production of pancreatic hormone–expressing endocrine cells from human embryonic stem cells. Nat. Biotechnol. 24, 1392-1401.
20. de Rooij, S. R., Painter, R. C., Phillips, D. I. W., Osmond, C., Michels, R. P. J., Godsland, I. F., Bossuyt, P. M. M., Bleker, O. P. and Roseboom, T. J. (2006). Impaired insulin secretion after prenatal exposure to the Dutch famine. Diabetes Care 29, 1897-1901.
21. De Vas, M. G., Kopp, J. L., Heliot, C., Sander, M., Cereghini, S. and Haumaitre, C. (2015). Hnf1b controls pancreas morphogenesis and the generation of Ngn3+ endocrine progenitors. Development 142, 871-882.
22. Decker, K., Goldman, D. C., Grasch, C. L. and Sussel, L. (2006). Gata6 is an important regulator of mouse pancreas development. Dev. Biol. 298, 415-429.
23. Dimitri, P., Warner, J. T., Minton, J. A. L., Patch, A. M., Ellard, S., Hattersley, A. T., Barr, S., Hawkes, D., Wales, J. K. and Gregory, J.W. (2011). Novel GLIS3 mutations demonstrate an extended multisystem phenotype. Eur. J. Endocrinol. 164, 437-443.
24. Docherty, K., Bernardo, A. S. and Vallier, L. (2007). Embryonic stem cell therapy for diabetes mellitus. Semin. Cell Dev. Biol. 18, 827-838.
25. Elghazi, L., Cras-Meneur, C., Czernichow, P. and Scharfmann, R. (2002). Role for FGFR2IIIb-mediated signals in controlling pancreatic endocrine progenitor cell proliferation. Proc. Natl. Acad. Sci. USA 99, 3884-3889.
26. 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.
27. Flanagan, S. E., De Franco, E., Lango Allen, H., Zerah, M., Abdul-Rasoul, M. M., Edge, J. A., Stewart, H., Alamiri, E., Hussain, K., Wallis, S. et al. (2014). Analysis of transcription factors key for mouse pancreatic development establishes NKX2-2 and MNX1 mutations as causes of neonatal diabetes in man. Cell Metab. 19, 146-154.
28. Flechtner, I., Vaxillaire, M., Cavé, H., Scharfmann, R., Froguel, P. and Polak, M. (2008). Neonatal hyperglycaemia and abnormal development of the pancreas. Best Pract. Res. Clin. Endocrinol. Metab. 22, 17-40.
29. Frank, V., Habbig, S., Bartram, M. P., Eisenberger, T., Veenstra-Knol, H. E., Decker, C., Boorsma, R. A. C., Gobel, H., Nurnberg, G., Griessmann, A. et al. (2013). Mutations in NEK8 link multiple organ dysplasia with altered Hippo signalling and increased c-MYC expression. Hum. Mol. Genetics 22, 2177-2185.
30. 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.
31. 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.
32. Guo, T., Landsman, L., Li, N. and Hebrok, M. (2013). Factors expressed by murine embryonic pancreatic mesenchyme enhance generation of insulin-producing cells from hESCs. Diabetes 62, 1581-1592.
33. Hales, C. N. and Barker, D. J. P. (1992). Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia 35, 595-601.
34. Hanley, N. (2014). Closing in on pancreatic beta cells. Nat. Biotechnol. 32, 1100-1102.
35. Harrison, K. A., Thaler, J., Pfaff, S. L., Gu, H. and Kehrl, J. H. (1999). Pancreas dorsal lobe agenesis and abnormal islets of Langerhans in Hlxb9-deficient mice. Nat. Genet. 23, 71-75.
36. Hattersley, A. T. and Tooke, J. E. (1999). The fetal insulin hypothesis: an alternative explanation of the association of low birthweight with diabetes and vascular disease. Lancet 353, 1789-1792.
37. 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.
38. 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.
39. Herrera, P. L. (2000). Adult insulin- and glucagon-producing cells differentiate from two independent cell lineages. Development 127, 2317-2322.
40. Hrvatin, S., O’Donnell, C.W., Deng, F., Millman, J. R., Pagliuca, F.W., DiIorio, P., Rezania, A., Gifford, D. K. and Melton, D. A. (2014). Differentiated human stem cells resemble fetal, not adult, β cells. Proc. Natl. Acad. Sci. USA 111, 3038-3043.
41. Jennings, R. E., Berry, A. A., Kirkwood-Wilson, R., Roberts, N. A., Hearn, T., Salisbury, R. J., Blaylock, J., Piper Hanley, K. and Hanley, N. A. (2013). Development of the human pancreas from foregut to endocrine commitment. Diabetes 62, 3514-3522.
42. Jensen, J. N., Rosenberg, L. C., Hecksher-Sørensen, J. and Serup, P. (2007). Mutant neurogenin-3 in congenital malabsorptive diarrhea. N. Engl. J. Med. 356, 1781-1782; author reply 1782.
43. Jeon, J., Correa-Medina, M., Ricordi, C., Edlund, H. and Diez, J. A. (2009). Endocrine cell clustering during human pancreas development. J. Histochem. Cytochem. 57, 811-824.
44. Jørgensen, M. C., Ahnfelt-Rønne, J., Hald, J., Madsen, O. D., Serup, P. and Hecksher-Sorensen, J. (2007). An illustrated review of early pancreas development in the mouse. Endocr. Rev. 28, 685-705.
45. Kawaguchi, Y., Cooper, B., Gannon, M., Ray, M., MacDonald, R. J. and Wright, C. V. E. (2002). The role of the transcriptional regulator Ptf1a in converting intestinal to pancreatic progenitors. Nat. Genet. 32, 128-134.
46. Kelly, O. G., Chan, M. Y., Martinson, L. A., Kadoya, K., Ostertag, T. M., Ross, K. G., Richardson, M., Carpenter, M. K., D’Amour, K. A., Kroon, E. et al. (2011). Cell-surface markers for the isolation of pancreatic cell types derived from human embryonic stem cells. Nat. Biotechnol. 29, 750-756.
47. 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.
48. Ketola, I., Otonkoski, T., Pulkkinen, M.-A., Niemi, H., Palgi, J., Jacobsen, C. M., Wilson, D. B. and Heikinheimo, M. (2004). Transcription factor GATA-6 is expressed in the endocrine and GATA-4 in the exocrine pancreas. Mol. Cell. Endocrinol. 226, 51-57.
49. Kong, A., Steinthorsdottir, V., Masson, G., Thorleifsson, G., Sulem, P., Besenbacher, S., Jonasdottir, A., Sigurdsson, A., Kristinsson, K. T., Jonasdottir, A. et al. (2009). Parental origin of sequence variants associated with complex diseases. Nature 462, 868-874.
50. Krantz, I. D., Piccoli, D. A. and Spinner, N. B. (1997). Alagille syndrome. J. Med. Genet. 34, 152-157.
51. Krapp, A., Knofler, M., Frutiger, S., Hughes, G. J., Hagenbuchle, O. and Wellauer, P. K. (1996). The p48 DNA-binding subunit of transcription factor PTF1 is a new exocrine pancreas-specific basic helix-loop-helix protein. EMBO J. 15, 4317-4329.
52. 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.
53. Lammert, E., Cleaver, O. and Melton, D. (2001). Induction of pancreatic differentiation by signals from blood vessels. Science 294, 564-567.
54. Lango Allen, H., Flanagan, S. E., Shaw-Smith, C., De Franco, E., Akerman, I., Caswell, R., Ferrer, J., Hattersley, A. T. and Ellard, S. (2011). GATA6 haploinsufficiency causes pancreatic agenesis in humans. Nat. Genet. 44, 20-22.
55. Li, H., Arber, S., Jessell, T. M. and Edlund, H. (1999). Selective agenesis of the dorsal pancreas in mice lacking homeobox gene Hlxb9. Nat. Genet. 23, 67-70.
56. Lyttle, B. M., Li, J., Krishnamurthy, M., Fellows, F., Wheeler, M. B., Goodyer, C. G. and Wang, R. (2008). Transcription factor expression in the developing human fetal endocrine pancreas. Diabetologia 51, 1169-1180.
57. Mahajan, A., DIAbetes Genetics Replication And Meta-analysis (DIAGRAM) Consortium, Asian Genetic Epidemiology Network Type 2 Diabetes (AGENT2D) Consortium, South Asian Type 2 Diabetes (SAT2D) Consortium, Mexican American Type 2 Diabetes (MAT2D) Consortium, Type 2 Diabetes Genetic Exploration by Next-generation sequencing in multi-Ethnic Samples (T2D-GENES) Consortium et al. (2014). Genome-wide transancestry meta-analysis provides insight into the genetic architecture of type 2 diabetes susceptibility. Nat. Genet. 46, 234-244.
58. McCracken, K. W. and Wells, J. M. (2012). Molecular pathways controlling pancreas induction. Semin. Cell Dev. Biol. 23, 656-662.
59. McGrath, P. S., Watson, C. L., Ingram, C., Helmrath, M. A. and Wells, J. M. (2015). The basic helix-loop-helix transcription factor NEUROG3 is required for development of the human endocrine pancreas. Diabetes 64, 2497-2505.
60. Mitchell, J., Punthakee, Z., Lo, B., Bernard, C., Chong, K., Newman, C., Cartier, L., Desilets, V., Cutz, E., Hansen, I. L. et al. (2004). Neonatal diabetes, with hypoplastic pancreas, intestinal atresia and gall bladder hypoplasia: search for the aetiology of a new autosomal recessive syndrome. Diabetologia 47, 2160-2167.
61. Morán, I., Akerman, I., van de Bunt, M., Xie, R., Benazra, M., Nammo, T., Arnes, L., Nakić, N., García-Hurtado, J., Rodríguez-Seguí, S. et al. (2012). Human β cell transcriptome analysis uncovers lncRNAs that are tissue-specific, dynamically regulated, and abnormally expressed in type 2 diabetes. Cell Metab. 16, 435-448.
62. Murtaugh, L. C. (2007). Pancreas and beta-cell development: from the actual to the possible. Development 134, 427-438.
63. Nicolino, M., Claiborn, K. C., Senée, V., Boland, A., Stoffers, D. A. and Julier, C. (2010). A novel hypomorphic PDX1 mutation responsible for permanent neonatal diabetes with subclinical exocrine deficiency. Diabetes 59, 733-740.
64. O’Rahilly, R. and Müller, F. (2010). Developmental stages in human embryos: revised and new measurements. Cells Tissues Organs 192, 73-84.
65. Otonkoski, T. (1988). Insulin and glucagon secretory responses to arginine, glue agon, and theophylline during perifusion of human fetal islet-like cell clusters. J. Clin. Endocrinol. Metab. 67, 734-740.
66. Otonkoski, T., Andersson, S., Knip, M. and Simell, O. (1988). Maturation of insulin response to glucose during human fetal and neonatal development: studies with perifusion of pancreatic isletlike cell clusters. Diabetes 37, 286-291.
67. Pagliuca, F. W. and Melton, D. A. (2013). How to make a functional β-cell. Development 140, 2472-2483.
68. Pagliuca, F.W., Millman, J. R., Gürtler, M., Segel, M., Van Dervort, A., Ryu, J. H., Peterson, Q. P., Greiner, D. and Melton, D. A. (2014). Generation of functional human pancreatic β cells in vitro. Cell 159, 428-439.
69. Pan, F. C. and Wright, C. (2011). Pancreas organogenesis: from bud to plexus to gland. Dev. Dyn. 240, 530-565.
70. Pasquali, L., Gaulton, K. J., Rodríguez-Seguí, S. A., Mularoni, L., Miguel- Escalada, I., Akerman, I., Tena, J. J., Morán, I., Gómez-Marín, C., van de Bunt, M. et al. (2014). Pancreatic islet enhancer clusters enriched in type 2 diabetes risk-associated variants. Nat. Genet. 46, 136-143.
71. Piccand, J., Strasser, P., Hodson, D. J., Meunier, A., Ye, T., Keime, C., Birling, M.-C., Rutter, G. A. and Gradwohl, G. (2014). Rfx6 maintains the functional identity of adult pancreatic beta cells. Cell Rep. 9, 2219-2232.
72. Pinney, S. E., Oliver-Krasinski, J., Ernst, L., Hughes, N., Patel, P., Stoffers, D. A., Russo, P. and De León, D. D. (2011). Neonatal diabetes and congenital malabsorptive diarrhea attributable to a novel mutation in the human neurogenin-3 gene coding sequence. J. Clin. Endocrinol. Metab. 96, 1960-1965.
73. Piper, K., Ball, S. G., Keeling, J.W., Mansoor, S., Wilson, D. I. and Hanley, N. A. (2002). Novel SOX9 expression during human pancreas development correlates to abnormalities in Campomelic dysplasia. Mech. Dev. 116, 223-226.
74. Piper, K., Brickwood, S., Turnpenny, L. W., Cameron, I. T., Ball, S. G., Wilson, D. I. and Hanley, N. A. (2004). Beta cell differentiation during early human pancreas development. J. Endocrinol. 181, 11-23.
75. Piper Hanley, K., Hearn, T., Berry, A., Carvell, M. J., Patch, A.-M., Williams, L. J., Sugden, S. A., Wilson, D. I., Ellard, S. and Hanley, N. A. (2010). In vitro expression of NGN3 identifies RAB3B as the predominant Ras-associated GTPbinding protein 3 family member in human islets. J. Endocrinol. 207, 151-161.
76. Polak, M., Bouchareb-Banaei, L., Scharfmann, R. and Czernichow, P. (2000). Early pattern of differentiation in the human pancreas. Diabetes 49, 225-232.
77. Pritchett, J., Athwal, V., Roberts, N., Hanley, N. A. and Hanley, K. P. (2011). Understanding the role of SOX9 in acquired diseases: lessons from development. Trends Mol. Med. 17, 166-174.
78. Ravassard, P., Hazhouz, Y., Pechberty, S., Bricout-Neveu, E., Armanet, M., Czernichow, P. and Scharfmann, R. (2011). A genetically engineered human pancreatic beta cell line exhibiting glucose-inducible insulin secretion. J. Clin. Invest. 121, 3589-3597.
79. Rezania, A., Bruin, J. E., Xu, J., Narayan, K., Fox, J. K., O’Neil, J. J. and Kieffer, T. J. (2013). Enrichment of human embryonic stem cell-derived NKX6.1- expressing pancreatic progenitor cells accelerates the maturation of insulinsecreting cells in vivo. Stem Cells 31, 2432-2442.
80. Rezania, A., Bruin, J. E., Arora, P., Rubin, A., Batushansky, I., Asadi, A., O’Dwyer, S., Quiskamp, N., Mojibian, M., Albrecht, T. et al. (2014). Reversal of diabetes with insulin-producing cells derived in vitro from human pluripotent stem cells. Nat. Biotechnol. 32, 1121-1133.
81. Riedel, M. J., Asadi, A., Wang, R., Ao, Z., Warnock, G. L. and Kieffer, T. J. (2012). Immunohistochemical characterisation of cells co-producing insulin and glucagon in the developing human pancreas. Diabetologia 55, 372-381.
82. Riopel, M., Li, J., Fellows, G. F., Goodyer, C. G. and Wang, R. (2014). Ultrastructural and immunohistochemical analysis of the 8-20 week human fetal pancreas. Islets 6, e982949.
83. Rodríguez-Seguel, E., Mah, N., Naumann, H., Pongrac, I. M., Cerdá-Esteban, N., Fontaine, J.-F., Wang, Y., Chen, W., Andrade-Navarro, M. A. and Spagnoli, F. M. (2013). Mutually exclusive signaling signatures define the hepatic and pancreatic progenitor cell lineage divergence. Genes Dev. 27, 1932-1946.
84. Rubio-Cabezas, O. and Ellard, S. (2013). Diabetes mellitus in neonates and infants: genetic heterogeneity, clinical approach to diagnosis, and therapeutic options. Horm. Res. Paediatr. 80, 137-146.
85. Rubio-Cabezas, O., Minton, J. A. L., Kantor, I., Williams, D., Ellard, S. and Hattersley, A. T. (2010). Homozygous mutations in NEUROD1 are responsible for a novel syndrome of permanent neonatal diabetes and neurological abnormalities. Diabetes 59, 2326-2331.
86. Rubio-Cabezas, O., Jensen, J. N., Hodgson, M. I., Codner, E., Ellard, S., Serup, P. and Hattersley, A. T. (2011). Permanent neonatal diabetes and enteric anendocrinosis associated with biallelic mutations in NEUROG3. Diabetes 60, 1349-1353.
87. Rubio-Cabezas, O., Hattersley, A. T., Njølstad, P. R., Mlynarski, W., Ellard, S., White, N., Chi, D. V. and Craig, M. E. (2014). The diagnosis and management of monogenic diabetes in children and adolescents. Pediatr. Diabetes 15 Suppl 20, 47-64.
88. Russ, H. A., Parent, A. V., Ringler, J. J., Hennings, T. G., Nair, G. G., Shveygert, M., Guo, T., Puri, S., Haataja, L., Cirulli, V. et al. (2015). Controlled induction of human pancreatic progenitors produces functional beta-like cells in vitro. EMBO J. 34, 1759-1772.
89. Sadler, T. W. (2000). Langman’s Medical Embryology. Baltimore: Lippincott Williams and Wilkins.
90. Salisbury, R. J., Blaylock, J., Berry, A. A., Jennings, R. E., De Krijger, R., Piper Hanley, K. and Hanley, N. A. (2014). The window period of NEUROGENIN3 during human gestation. Islets 6, e954436.
91. Sarkar, S. A., Kobberup, S., Wong, R., Lopez, A. D., Quayum, N., Still, T., Kutchma, A., Jensen, J. N., Gianani, R., Beattie, G. M. et al. (2008). Global gene expression profiling and histochemical analysis of the developing human fetal pancreas. Diabetologia 51, 285-297.
92. Schaffer, A. E., Freude, K. K., Nelson, S. B. and Sander, M. (2010). Nkx6 transcription factors and Ptf1a function as antagonistic lineage determinants in multipotent pancreatic progenitors. Dev. Cell 18, 1022-1029.
93. Scharfmann, R., Pechberty, S., Hazhouz, Y., von Bülow, M., Bricout-Neveu, E., Grenier-Godard, M., Guez, F., Rachdi, L., Lohmann, M., Czernichow, P. et al. (2014). Development of a conditionally immortalized human pancreatic beta cell line. J. Clin. Invest. 124, 2087-2098.
94. Schwitzgebel, V. M. (2014). Many faces of monogenic diabetes. J. Diabetes Invest. 5, 121-133.
95. Schwitzgebel, V. M., Scheel, D. W., Conners, J. R., Kalamaras, J., Lee, J. E., Anderson, D. J., Sussel, L., Johnson, J. D. and German, M. S. (2000). Expression of neurogenin3 reveals an islet cell precursor population in the pancreas. Development 127, 3533-3542.
96. Schwitzgebel, V. M., Mamin, A., Brun, T., Ritz-Laser, B., Zaiko, M., Maret, A., Jornayvaz, F. R., Theintz, G. E., Michielin, O., Melloul, D. et al. (2003). Agenesis of human pancreas due to decreased half-life of insulin promoter factor 1. J. Clin. Endocrinol. Metab. 88, 4398-4406.
97. 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. (2004). Mutations in PTF1A cause pancreatic and cerebellar agenesis. Nat. Genet. 36, 1301-1305.
98. Senée, 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.
99. 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.
100. Shaw-Smith, C., De Franco, E., Lango Allen, H., Batlle, M., Flanagan, S. E., Borowiec, M., Taplin, C. E., van Alfen van der Velden, J., Cruz-Rojo, J., Perez de Nanclares, G. et al. (2014). GATA4 mutations are a cause of neonatal and childhood-onset diabetes. Diabetes 63, 2888-2894.
101. Singh, I., Mehta, A., Contreras, A., Boettger, T., Carraro, G., Wheeler, M., Cabrera-Fuentes, H. A., Bellusci, S., Seeger, W., Braun, T. et al. (2014). Hmga2 is required for canonical WNT signaling during lung development. BMC Biol. 12, 21.
102. Smith, S. B., Qu, H.-Q., Taleb, N., Kishimoto, N. Y., Scheel, D. W., Lu, Y., Patch, A.-M., Grabs, R., Wang, J., Lynn, F. C. et al. (2010). Rfx6 directs islet formation and insulin production in mice and humans. Nature 463, 775-780.
103. 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.
104. Solomon, B. D., Pineda-Alvarez, D. E., Balog, J. Z., Hadley, D., Gropman, A. L., Nandagopal, R., Han, J. C., Hahn, J. S., Blain, D., Brooks, B. et al. (2009). Compound heterozygosity for mutations in PAX6 in a patient with complex brain anomaly, neonatal diabetes mellitus, and microophthalmia. Am. J. Med. Genet. 149A, 2543-2546.
105. Stafford, D. and Prince, V. E. (2002). Retinoic acid signaling is required for a critical early step in zebrafish pancreatic development. Curr. Biol. 12, 1215-1220.
106. Stoffers, D. A., Zinkin, N. T., Stanojevic, V., Clarke, W. L. and Habener, J. F. (1997). Pancreatic agenesis attributable to a single nucleotide deletion in the human IPF1 gene coding sequence. Nat. Genet. 15, 106-110.
107. Sussel, L., Kalamaras, J., Hartigan-O’Connor, D. J., Meneses, J. J., Pedersen, R. A., Rubenstein, J. L. and German, M. S. (1998). Mice lacking the homeodomain transcription factor Nkx2.2 have diabetes due to arrested differentiation of pancreatic beta cells. Development 125, 2213-2221.
108. Thomas, I. H., Saini, N. K., Adhikari, A., Lee, J. M., Kasa-vubu, J. Z., Vazquez, D. M., Menon, R. K., Chen, M. and Fajans, S. S. (2009). Neonatal diabetes mellitus with pancreatic agenesis in an infant with homozygous IPF-1 Pro63fsX60 mutation. Pediatr. Diabetes 10, 492-496.
109. Travers, M. E., Mackay, D. J. G., Dekker Nitert, M., Morris, A. P., Lindgren, C. M., Berry, A., Johnson, P. R., Hanley, N., Groop, L. C., McCarthy, M. I. et al. (2013). Insights into the molecular mechanism for type 2 diabetes susceptibility at the KCNQ1 locus from temporal changes in imprinting status in human islets. Diabetes 62, 987-992.
110. Turnpenny, P. D. and Ellard, S. (2012). Alagille syndrome: pathogenesis, diagnosis and management. Eur. J. Hum. Genet. 20, 251-257.
111. Vaxillaire, M., Bonnefond, A. and Froguel, P. (2012). The lessons of early-onset monogenic diabetes for the understanding of diabetes pathogenesis. Best Pract. Res. Clin. Endocrinol. Metab. 26, 171-187.
112. Villasenor, A., Chong, D. C. and Cleaver, O. (2008). Biphasic Ngn3 expression in the developing pancreas. Dev. Dyn. 237, 3270-3279.
113. Villasenor, A., Chong, D. C., Henkemeyer, M. and Cleaver, O. (2010). Epithelial dynamics of pancreatic branching morphogenesis. Development 137, 4295-4305.
114. Wandzioch, E. and Zaret, K. S. (2009). Dynamic signaling network for the specification of embryonic pancreas and liver progenitors. Science 324, 1707-1710.
115. Wang, J., Cortina, G., Wu, S. V., Tran, R., Cho, J.-H., Tsai, M.-J., Bailey, T. J., Jamrich, M., Ament, M. E., Treem, W. R. et al. (2006). Mutant neurogenin-3 in congenital malabsorptive diarrhea. N. Engl. J. Med. 355, 270-280.
116. 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.-H., Lango Allen, H. et al. (2014). Recessive mutations in a distal PTF1A enhancer cause isolated pancreatic agenesis. Nat. Genet. 46, 61-64.
117. 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.
118. Ye, F., Duvillié, B. and Scharfmann, R. (2005). Fibroblast growth factors 7 and 10 are expressed in the human embryonic pancreatic mesenchyme and promote the proliferation of embryonic pancreatic epithelial cells. Diabetologia 48, 277-281.
119. Yebra, M., Montgomery, A. M. P., Diaferia, G. R., Kaido, T., Silletti, S., Perez, B., Just, M. L., Hildbrand, S., Hurford, R., Florkiewicz, E. et al. (2003). Recognition of the neural chemoattractant Netrin-1 by integrins alpha6beta4 and alpha3beta1 regulates epithelial cell adhesion and migration. Dev. Cell 5, 695-707.
120. Yebra, M., Diaferia, G. R., Montgomery, A. M. P., Kaido, T., Brunken, W. J., Koch, M., Hardiman, G., Crisa, L. and Cirulli, V. (2011). Endothelium-derived Netrin-4 supports pancreatic epithelial cell adhesion and differentiation through integrins alpha2beta1 and alpha3beta1. PLoS ONE 6, e22750.
121. Zenker, M., Mayerle, J., Lerch, M. M., Tagariello, A., Zerres, K., Durie, P. R., Beier, M., Hülskamp, G., Guzman, C., Rehder, H. et al. (2005). Deficiency of UBR1, a ubiquitin ligase of the N-end rule pathway, causes pancreatic dysfunction, malformations and mental retardation (Johanson-Blizzard syndrome). Nat. Genet. 37, 1345-1350.
122. Zenker, M., Mayerle, J., Reis, A. and Lerch, M. M. (2006). Genetic basis and pancreatic biology of Johanson-Blizzard syndrome. Endocrinol. Metab. Clin. North Am. 35, 243-253, vii-viii.