The simultaneous loss of Arx and Pax4 genes promotes a somatostatin-producing cell fate specification at the expense of the α- and β-cell lineages in the mouse endocrine pancreas

Development

Volumn 132, Issue 13, 2005, Pages 2969-2980

  Collombat, Patrick ^a   Hecksher Sørensen, Jacob ^b   Broccoli, Vania ^c   Krull, Jens ^a   Ponte, Ilaria ^c   Mundiger, Tabea ^a   Smith, Julian ^d   Gruss, Peter ^a   Serup, Palle ^b   Mansouri, Ahmed ^a  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^b HAGEDORN RESEARCH INSTITUTE   (Denmark)

^c SAN RAFFAELE HOSPITAL   (Italy)

^d Centre de Biologie du Developpement Toulouse   (France)

Author keywords

Arx; Endocrine pancreas development; Fate specification; Hyperglycaemia; Mouse; Pax4

Indexed keywords

PANCREAS POLYPEPTIDE; SOMATOSTATIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ARX; TRANSCRIPTION FACTOR PAX4; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL FATE; CELL LABELING; CELL LINEAGE; CELL MATURATION; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; EPIGENETICS; FEEDING; FEMALE; GENE LOSS; HORMONE SYNTHESIS; MALE; MOUSE; MOUSE MUTANT; NONHUMAN; PANCREAS; PANCREAS ISLET ALPHA CELL; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; TRANSCRIPTION REGULATION;

ANIMALS; CELL DIFFERENTIATION; CELL LINE; CERCOPITHECUS AETHIOPS; COS CELLS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLUCAGON; HOMEODOMAIN PROTEINS; HYPERGLYCEMIA; INSULIN; ISLETS OF LANGERHANS; MALE; MICE; PAIRED BOX TRANSCRIPTION FACTORS; SOMATOSTATIN; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

ANIMALIA;

EID: 23144432613     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.01870     Document Type: Article

References (39)

1. Adrian, T. E., Bloom, S. R., Hermansen, K. and Iversen, J. (1978). Pancreatic polypeptide, glucagon and insulin secretion from the isolated perfused canine pancreas. Diabetologia 14, 413-417.
2. Ahlgren, U., Pfaff, S. L., Jessell, T. M., Edlund, T. and Edlund, H. (1997). Independent requirement for ISL1 in formation of pancreatic mesenchyme and islet cells. Nature 385, 257-260.
3. Ahlgren, U., Jonsson, J., Jonsson, L., Simu, K. and Edlund, H. (1998). β-cell-specific inactivation of the mouse Ipfl/Pdxl gene results in loss of the β-cell phenotype and maturity onset diabetes. Genes Dev. 12, 1763-1768.
4. Apelqvist, A., Li, H., Sommer, L., Beatus, P., Anderson, D. J., Honjo, T., Hrabe de Angelis, M., Lendahl, U. and Edlund, H. (1999). Notch signalling controls pancreatic cell differentiation. Nature 400, 877-881.
5. Ashery-Padan, R., Zhou, X., Marquardt, T., Herrera, P., Toube, L., Berry, A. and Gruss, P. (2004). Conditional inactivation of Pax6 in the pancreas causes early onset of diabetes. Dev. Biol. 269, 479-488.
6. Blair, H. J., Reed, V., Gormally, E., Wilson, J. B., Novak, J., McInnes, R. R., Phillips, S. J., Taylor, B. A. and Boyd, Y. (2002). Positioning of five genes (CASK, ARX, SAT, IMAGE cDNAs 248928 and 253949) from the human X chromosome short arm with respect to evolutionary breakpoints on the mouse X chromosome. Mamm. Genome 11, 710-712.
7. Brink, C., Chowdhury, K. and Gruss, P. (2001). Pax4 regulatory elements mediate β-cell specific expression in the pancreas. Mech. Dev. 100, 37-43.
8. Collombat, P., Mansouri, A., Hecksher-Sorensen, J., Serup, P., Krull, J., Gradwohl, G. and Gruss, P. (2003). Opposing actions of Arx and Pax4 in endocrine pancreas development. Genes Dev. 17, 2591-2603.
9. Contreas, G., Jorgensen, J. and Madsen, O. D. (1990). Novel islet, duct, and acinar cell markers defined by monoclonal auto-antibodies from prediabetic BB rats. Pancreas 5, 540-547.
10. Csaba, Z. and Dournaud, P. (2001). Cellular biology of somatostatin receptors. Neuropeptides 35, 1-23.
11. Edlund, H. (2002). Pancreatic organogenesis - developmental mechanisms and implications for therapy. Nat. Rev. Genet. 3, 524-532.
12. Fujitani, Y., Kajimoto, Y., Yasuda, T., Matsuoka, T. A., Kaneto, H., Umayahara, Y., Fujita, N., Watada, H., Miyazaki, J. I., Yamasaki, Y. et al. (1999). Identification of a portable repression domain and an E1A-responsive activation domain in Pax4: a possible role of Pax4 as a transcriptional repressor in the pancreas. Mol. Cell Biol. 19, 8281-8291.
13. 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.
14. 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.
15. Guz, Y., Montminy, M. R., Stein, R., Leonard, J., Gamer, L. W., Wright, C. V. and Teitelman, G. (1995). Expression of murine STF-1, a putative insulin gene transcription factor, in β-cells of pancreas, duodenal epithelium and pancreatic exocrine and endocrine progenitors during ontogeny. Development 121, 11-18.
16. Herrera, P. L., Huarte, J., Sanvito, F., Meda, P., Orci, L. and Vassalli, J. D. (1991). Embryogenesis of the murine endocrine pancreas; early expression of pancreatic polypeptide gene. Development 113, 1257-1265.
17. Jensen, J., Heller, R S., Funder-Nielsen, T., Pedersen, E. E., Lindsell, C., Weinmaster, G., Madsen, O. D. and Serup, P. (2000). Independent development of pancreatic α- and β-cells from neurogenin3-expressing precursors: a role for the notch pathway in repression of premature differentiation. Diabetes 49, 163-176.
18. Jensen, P. B., Kristensen, P., Clausen, J. T., Judge, M. E., Hastrup, S., Thim, L., Wulff, B. S., Foged, C., Jensen, J., Holst, J. J. et al. (1999). The hypothalamic satiety peptide CART is expressed in anorectic and non-anorectic pancreatic islet tumors and in the normal islet of Langerhans. FEBS Lett. 447, 139-143.
19. Jonsson, J., Carlsson, L., Edlund, T. and Edlund, H. (1994). Insulin-promoter-factor 1 is required for pancreas development in mice. Nature 371, 606-609.
20. Mansouri, A., St-Onge, L. and Gruss, P. (1999). Role of Genes in Endoderm-derived Organs. Trends Endocrinol. Metab. 10, 164-167.
21. Naya, F. J., Huang, H. P., Qiu, Y., Mutoh, H., DeMayo, F. J., Leiter, A. B. and Tsai, M. J. (1997). Diabetes, defective pancreatic morphogenesis, and abnormal enteroendocrine differentiation in BETA2/neuroD-deficient mice. Genes Dev. 11, 2323-2334.
22. 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.
23. Pictet, R. L., Clark, W. R., Williams, R. H. and Rutter, W. J. (1972). An ultrastructural analysis of the developing embryonic pancreas. Dev. Biol. 29, 436-467.
24. Prado, C. L., Pugh-Bernard, A. E., Elghazi, L., Sosa-Pineda, B. and Sussel, L. (2004). Ghrelin cells replace insulin-producing β cells in two mouse models of pancreas development. Proc. Natl. Acad. Sci. USA 101, 2924-2929.
25. Roncoroni, L., Violi, V., Montanari, M. and Muri, M. (1983). Effect of somatostatin on exocrine pancreas evaluated on a total external pancreatic fistula of neoplastic origin. Am. J. Gastroenterol. 78, 425-428.
26. Sander, M., Neubuser, A., Kalamaras, J., Ee, H. C., Martin, G. R and German, M. S. (1997). Genetic analysis reveals that PAX6 is required for normal transcription of pancreatic hormone genes and islet development. Genes Dev. 11, 1662-1673.
27. Sander, M., Sussel, L., Conners, J., Scheel, D., Kalamaras, J., Dela Cruz, F., Schwitzgebel, V., Hayes-Jordan, A. and German, M. (2000). Homeobox gene Nkx6. 1 lies downstream of Nkx2. 2 in the major pathway of β-cell formation in the pancreas. Development 127, 5533-5540.
28. 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.
29. Seufert, D. W., Prescott, N. L. and El-Hodiri, H. M. (2004). Xenopus aristaless-related homeobox (xARX) gene product functions as both a transcriptional activator and repressor in forebrain development. Dev. Dyn. 21, 21.
30. Slack, J. M. (1995). Developmental biology of the pancreas. Development 121, 1569-1580.
31. Smith, S. B., Ee, H. C., Conners, J. R. and German, M. S. (1999). Paired-homeodomain transcription factor PAX4 acts as a transcriptional repressor in early pancreatic development. Mol. Cell Biol. 19, 8272-8280.
32. Sommer, L., Ma, Q. and Anderson, D. J. (1996). neurogenins, a novel family of atonal-related bHLH transcription factors, are putative mammalian neuronal determination genes that reveal progenitor cell heterogeneity in the developing CNS and PNS. Mol. Cell. Neurosci. 8, 221-241.
33. Sosa-Pineda, B., Chowdhury, K., Torres, M., Oliver, G. and Gruss, P. (1997). The Pax4 gene is essential for differentiation of insulin-producing β-cells in the mammalian pancreas. Nature 386, 399-402.
34. Spieler, D., Baumer, N., Stebler, J., Koprunner, M., Reichman-Fried, M., Teichmann, U., Raz, E., Kessel, M. and Wittler, L. (2004). Involvement of Pax6 and Otx2 in the forebrain-specific regulation of the vertebrate homeobox gene ANF/Hesx1. Dev. Biol. 269, 567-579.
35. St-Onge, L., Sosa-Pineda, B., Chowdhury, K., Mansouri, A. and Gruss, P. (1997). Pax6 is required for differentiation of glucagon-producing α-cells in mouse pancreas. Nature 387, 406-409.
36. Strowski, M. Z., Parmar, R. M., Blake, A. D. and Schaeffer, J. M. (2000). Somatostatin inhibits insulin and glucagon secretion via two receptors subtypes: an in vitro study of pancreatic islets from somatostatin receptor 2 knockout mice. Endocrinology 141, 111-117.
37. 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 β-cells. Development 125, 2213-2221.
38. Teitelman, G., Alpert, S., Polak, J. M., Martinez, A. and Hanahan, D. (1993). Precursor cells of mouse endocrine pancreas coexpress insulin, glucagon and the neuronal proteins tyrosine hydroxylase and neuropeptide Y, but not pancreatic polypeptide. Development 118, 1031-1039.
39. Upchurch, B. H., Aponte, G. W. and Leiter, A. B. (1994). Expression of peptide YY in all four islet cell types in the developing mouse pancreas suggests a common peptide YY-producing progenitor. Development 120, 245-252.