The nuclear hormone receptor family member NR5A2 controls aspects of multipotent progenitor cell formation and acinar differentiation during pancreatic organogenesis

Development (Cambridge)

Volumn 141, Issue 16, 2014, Pages 3123-3133

  Hale, Michael A ^a   Swift, Galvin H ^a   Hoang, Chinh Q ^a   Deering, Tye G ^a   Masui, Toshi ^a   Lee, Youn Kyoung ^b,c   Xue, Jumin ^a   MacDonald, Raymond J ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c NOVARTIS INSTITUTES FOR BIOMEDICAL RESEARCH   (United States)

Author keywords

Acinar cell; Mouse; Nr5a2; Organogenesis; Pancreas; Transcriptional control

Indexed keywords

ACINAR CELL; MOUSE; NR5A2; ORGANOGENESIS; PANCREAS; TRANSCRIPTIONAL CONTROL;

ACINAR CELLS; ANIMALS; BASE SEQUENCE; CELL DIFFERENTIATION; CELL LINEAGE; CELL PROLIFERATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MALE; MICE; MICE, TRANSGENIC; MUTATION; PANCREAS; PHENOTYPE; RECEPTORS, CYTOPLASMIC AND NUCLEAR; STEM CELLS; TRANSGENES;

EID: 84905483275     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.109405     Document Type: Article

References (73)

1. Annicotte, J.-S., Fayard, E., Swift, G. H., Selander, L., Edlund, H., Tanaka, T., Kodama, T., Schoonjans, K. and Auwerx, J. (2003). Pancreatic-duodenal homeobox 1 regulates expression of liver receptor homolog 1 during pancreas development. Mol. Cell. Biol. 23, 6713-6724.
2. Becker-Andre, M., Andre, E. and Delamarter, J. F. (1993). Identification of nuclear receptor mRNAs by RT-PCR amplification of conserved zinc-finger motif sequences. Biochem. Biophys. Res. Commun. 194, 1371-1379.
3. Beres, T. M., Masui, T., Swift, G. H., Shi, L., Henke, R. M. and MacDonald, R. J. (2006). PTF1 is an organ-specific and Notch-independent basic helix-loop-helix complex containing the mammalian Suppressor of Hairless (RBP-J) or its paralogue, RBP-L. Mol. Cell. Biol. 26, 117-130.
4. Bonal, C., Thorel, F., Ait-Lounis, A., Reith, W., Trumpp, A. andHerrera, P.L. (2009). Pancreatic inactivation of c-Myc decreases acinar mass and transdifferentiates acinar cells into adipocytes in mice. Gastroenterology 136, 309-319. e9.
5. Burlison, J. S., Long, Q., Fujitani, Y., Wright, C. V. E. and Magnuson, M. A. (2008). Pdx-1 and Ptf1a concurrently determine fate specification of pancreatic multipotent progenitor cells. Dev. Biol. 316, 74-86.
6. Busby, S., Nuhhant, P., Cameron, M., Mercer, B. A., Hodder, P., Roush, W. R. and Griffin, P. R. (2010). Discovery of Inverse Agonists for the Liver Receptor Homologue-1 (LRH1; NR5A2) Probe Reports from the NIH Molecular Libraries Program: National Center for Biotechnology Information (US).
7. Chen, X., Xu, H., Yuan, P., Fang, F., Huss, M., Vega, V. B., Wong, E., Orlov, Y. L., Zhang, W., Jiang, J. et al. (2008). Integration of external signaling pathways with the core transcriptional network in embryonic stem cells. Cell 133, 1106-1117.
8. Chong, H. K., Biesinger, J., Seo, Y.-K., Xie, X. and Osborne, T. F. (2012). Genome-wide analysis of hepatic LRH-1 reveals a promoter binding preference and suggests a role in regulating genes of lipid metabolism in concert with FXR. BMC Genomics 13, 51.
9. Cleaver, O. and MacDonald, R. J. (2010). Developmental molecular biology of the pancreas. In Handbook of Pancreatic Cancer (ed. J. Neoptolemos, J. Abbruzzese, M. Buchler and R. Urrutia). pp. 71-117. New York: Springer.
10. Costantini, F. (2010). GDNF/Ret signaling and renal branching morphogenesis: from mesenchymal signals to epithelial cell behaviors. Organogenesis 6, 252-262.
11. Costantini, F. and Shakya, R. (2006). GDNF/Ret signaling and the development of the kidney. Bioessays 28, 117-127.
12. 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.
13. Fernandez-Marcos, P. J., Auwerx, J. and Schoonjans, K. (2011). Emerging actions of the nuclear receptor LRH-1 in the gut. Biochim. Biophys. Acta. 1812, 947-955.
14. Flandez, M., Cendrowski, J., Canamero, M., Salas, A., Del Pozo, N., Schoonjans, K. and Real, F. X. (2014). Nr5a2 heterozygosity sensitises to, and cooperates with, inflammation in KRasG12V-driven pancreatic tumourigenesis. Gut. 63, 647-655.
15. Goodwin, B., Jones, S. A., Price, R. R., Watson, M. A., McKee, D. D., Moore, L. B., Galardi, C., Wilson, J. G., Lewis, M. C., Roth, M. E. et al. (2000). A regulatory cascade of the nuclear receptors FXR, SHP-1, and LRH-1 represses bile acid biosynthesis. Mol. Cell 6, 517-526.
16. 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.
17. Gu, P., Goodwin, B., Chung, A. C.-K., Xu, X., Wheeler, D. A., Price, R. R., Galardi, C., Peng, L., Latour, A. M., Koller, B. H. et al. (2005). Orphan nuclear receptor LRH-1 is required to maintain Oct4 expression at the epiblast stage of embryonic development. Mol. Cell. Biol. 25, 3492-3505.
18. 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.
19. Heiser, P. W., Lau, J., Taketo, M. M., Herrera, P. L. and Hebrok, M. (2006). Stabilization of β-catenin impacts pancreas growth. Development 133, 2023-2032.
20. Heng, J.-C. D., Feng, B., Han, J., Jiang, J., Kraus, P., Ng, J.-H., Orlov, Y.L., Huss, M., Yang, L., Lufkin, T. et al. (2010). The nuclear receptorNr5a2 can replaceOct4 in the reprogramming ofmurine somatic cells to pluripotent cells. CellStemCell 6, 167-174.
21. Holland, A. M., Hale, M. A., Kagami, H., Hammer, R. E. and MacDonald, R. J. (2002). Experimental control of pancreatic development and maintenance. Proc. Natl. Acad. Sci. USA 99, 12236-12241.
22. Holmstrom, S. R., Deering, T., Swift, G. H., Poelwijk, F. J., Mangelsdorf, D. J., Kliewer, S. A. and MacDonald, R. J. (2011). LRH-1 and PTF1-L coregulate an exocrine pancreas-specific transcriptional network for digestive function. Genes Dev. 25, 1674-1679.
23. Hori, K., Cholewa-Waclaw, J., Nakada, Y., Glasgow, S. M., Masui, T., Henke, R. M., Wildner, H., Martarelli, B., Beres, T.M., Epstein, J. A. et al. (2008). Anon-classical bHLH-Rbpj transcription factor complex is required for specification of GABAergic neurons independent of Notch signaling. Genes Dev. 22, 166-178.
24. Jonsson, J., Carlsson, L., Edlund, T. and Edlund, H. (1994). Insulin-promoterfactor 1 is required for pancreas development in mice. Nature 371, 606-609.
25. 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.
26. Kent, W. J. (2002). BLAT-The BLAST-like alignment tool. Genome Res. 12, 656-664.
27. 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.
28. Kobberup, S., Nyeng, P., Juhl, K., Hutton, J. and Jensen, J. (2007). ETS-family genes in pancreatic development. Dev. Dyn. 236, 3100-3110.
29. Kopinke, D., Brailsford, M., Shea, J.E., Leavitt, R., Scaife, C. L. andMurtaugh, L.C. (2011). Lineage tracing reveals the dynamic contribution of Hes1+ cells to the developing and adult pancreas. Development 138, 431-441.
30. 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.
31. Labelle-Dumais, C., Jacob-Wagner, M., Paré, J.-F., Belanger, L. and Dufort, D. (2006). Nuclear receptor NR5A2 is required for proper primitive streak morphogenesis. Dev. Dyn. 235, 3359-3369.
32. Lazarus, K. A., Wijayakumara, D., Chand, A. L., Simpson, E. R. and Clyne, C. D. (2012). Therapeutic potential of Liver Receptor Homolog-1 modulators. J. Steroid Biochem. Mol. Biol. 130, 138-146.
33. Lee, Y.-K. and Moore, D. D. (2008). Liver receptor homolog-1, an emerging metabolic modulator. Front. Biosci. 13, 5928-5949.
34. Lee, Y.-K., Choi, Y.-H., Chua, S., Park, Y. J. and Moore, D. D. (2006). Phosphorylation of the hinge domain of the nuclear hormone receptor LRH-1 stimulates transactivation. J. Biol. Chem. 281, 7850-7855.
35. Lee, Y.-K., Schmidt, D. R., Cummins, C. L., Choi, M., Peng, L., Zhang, Y., Goodwin, B., Hammer, R. E., Mangelsdorf, D. J. and Kliewer, S. A. (2008). Liver receptor homolog-1 regulates bile acid homeostasis but is not essential for feedback regulation of bile acid synthesis. Mol. Endocrinol. 22, 1345-1356.
36. Lee, J. M., Lee, Y. K., Mamrosh, J. L., Busby, S. A., Griffin, P. R., Pathak, M. C., Ortlund, E. A. and Moore, D. D. (2011). A nuclear-receptor-dependent phosphatidylcholine pathway with antidiabetic effects. Nature 474, 506-510.
37. MacDonald, R. J., Swift, G. H. and Real, F. X. (2010). Transcriptional control of exocrine pancreas development and homeostasis. In Development, Differentiation and Disease of the Para-alimentary Tract, Vol. 97 (ed. K. H. Kaestner), pp. 1-40. Burlington: Academic Press.
38. Masui, T., Long, Q., Beres, T. M., Magnuson, M. A. and MacDonald, R. J. (2007). Early pancreatic development requires the vertebrate Suppressor of Hairless (RBPJ) in the PTF1 bHLH complex. Genes Dev. 21, 2629-2643.
39. Masui, M., Swift, G. H., Hale, M. A., Meredith, D., Johnson, J. E. and MacDonald, R. J. (2008). Transcriptional autoregulation controls pancreatic Ptf1a expression during development and adulthood. Mol. Cell. Biol. 28, 5458-5468.
40. Masui, T., Swift, G. H., Deering, T., Shen, C., Coats, W. S., Long, Q., Elsässer, H.-P., Magnuson, M. A. andMacDonald, R. J. (2010). Replacement of Rbpj with Rbpjl in the PTF1 complex controls the final maturation of pancreatic acinar cells. Gastroenterology 139, 270-280.
41. McCarthy, D. J., Chen, Y. and Smyth, G. K. (2012). Differential expression analysis of multifactor RNA-Seq experiments with respect to biological variation. Nucleic Acids Res. 40, 4288-4297.
42. Meredith, D. M., Borromeo, M. D., Deering, T. G., Casey, B. H., Savage, T. K., Mayer, P. R., Hoang, C., Tung, K.-C., Kumar, M., Shen, C. et al. (2013). Program specificity for Ptf1a in Pancreas versus Neural Tube Development correlates with distinct collaborating cofactors and chromatin accessibility. Mol. Cell. Biol. 33, 3166-3179.
43. Murtaugh, L. C., Law, A. C., Dor, Y. and Melton, D. A. (2005). β-catenin is essential for pancreatic acinar but not islet development. Development 132, 4663-4674.
44. Nakhai, H., Siveke, J. T., Mendoza-Torres, L. and Schmid, R. M. (2008). Conditional inactivation of Myc impairs development of the exocrine pancreas. Development 135, 3191-3196.
45. Obata, J., Yano, M., Mimura, H., Goto, T., Nakayama, R., Mibu, Y., Oka, C. and Kawaichi, M. (2001). p48 subunit of mouse PTF1 binds to RBP-Jkappa/CBF-1, the intracellular mediator of Notch signalling, and is expressed in the neural tube of early stage embryos. Genes Cells 6, 345-360.
46. Offield, M. F., Jetton, J. L., Labosky, P. A., Ray, M., Stein, R.W., Magnuson, M. A., Hogan, B. L. M. and Wright, C. V. E. (1996). PDX-1 is required for pancreatic outgrowth and differentiation of the rostral duodenum. Development 122, 983-995.
47. Pan, F. C. and Wright, C. (2011). Pancreas organogenesis: from bud to plexus to gland. Dev. Dyn. 240, 530-565.
48. Pan, F. C., Bankaitis, E.D., Boyer, D., Xu, X., Van deCasteele, M., Magnuson, M.A., Heimberg, H. and Wright, C. V. E. (2013). Spatiotemporal patterns of multipotentiality in Ptf1a-expressing cells during pancreas organogenesis and injury-induced facultative restoration. Development 140, 751-764.
49. Paré, J.-F., Roy, S., Galarneau, L. and Bélanger, L. (2001). The mouse fetoprotein transcription factor (FTF) gene promoter is regulated by three GATA elements with tandem E box and Nkx motifs, and FTF in turn activates the Hnf3beta, Hnf4alpha, and Hnf1alpha gene promoters. J. Biol. Chem. 276, 13136-13144.
50. Paré, J.-F., Malenfant, D., Courtemanche, C., Jacob-Wagner, M., Roy, S., Allard, D. andBélanger, L. (2004). The fetoprotein transcription factor (FTF) gene is essential to embryogenesis and cholesterol homeostasis and is regulated by a DR4 element. J. Biol. Chem. 279, 21206-21216.
51. Pictet, R. and Rutter, W. J. (1972). Development of the embryonic endocrine pancreas. In Handbook of Physiology. Section 7: Endocrinology, vol. I. Endocrine Pancreas (ed. D. F. Steiner and N. Freinkel). pp. 25-66. Baltimore: Williams and Wilkins.
52. 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.
53. 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.
54. Rausa, F. M., Galarneau, L., Bélanger, L. and Costa, R. H. (1999). The nuclear receptor fetoprotein transcription factor is coexpressed with its target gene hnf-3beta in the developing murine liver, intestine and pancreas. Mech. Dev. 89, 185-188.
55. Rieck, S., Bankaitis, E. D. and Wright, C. V. E. (2012). Lineage determinants in early endocrine development. Sem. Cell Dev. Biol. 23, 673-684.
56. Rojas, A., Schachterle, W., Xu, S.-M. and Black, B. L. (2009). An endodermspecific transcriptional enhancer from the mouse Gata4 gene requires GATA and homeodomain protein-binding sites for function in vivo. Dev. Dyn. 238, 2588-2598.
57. Rose, S. D., Swift, G. H., Peyton, M. J., Hammer, R. E. and MacDonald, R. J. (2001). The role of PTF1-P48 in pancreatic acinar gene expression. J. Biol. Chem. 276, 44018-44026.
58. Roux, E., Strubin, M., Hagenbuchle, O. and Wellauer, P. K. (1989). The cellspecific transcription factor PTF1 contains two different subunits that interact with the DNA. Genes Dev. 3, 1613-1624.
59. Sablin, E. P., Krylova, I. N., Fletterick, R. J. and Ingraham, H. A. (2003). Structural basis for ligand-independent activation of the orphan nuclear receptor LRH-1. Mol. Cell 11, 1575-1585.
60. Sakai, D., Suzuki, T., Osumi, N. andWakamatsu, Y. (2006). Cooperative action of Sox9, Snail2 and PKA signaling in early neural crest development. Development 133, 1323-1333.
61. 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.
62. Serup, P. (2012). Signaling pathways regulating murine pancreatic development. Sem. Cell Dev. Biol. 23, 663-672.
63. 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.
64. Suzuki, T., Kasahara, M., Yoshioka, H., Morohashi, K.-i. and Umesono, K. (2003). LXXLL-related motifs in Dax-1 have target specificity for the orphan nuclear receptors Ad4BP/SF-1 and LRH-1. Mol. Cell. Biol. 23, 238-249.
65. Thompson, N., Gesina, 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.
66. Venteclef, N., Jakobsson, T., Ehrlund, A., Damdimopoulos, A., Mikkonen, L., Ellis, E., Nilsson, L.-M., Parini, P., Janne, O. A., Gustafsson, J.-A. et al. (2010). GPS2-dependent corepressor/SUMO pathways govern anti-inflammatory actions of LRH-1 and LXRbeta in the hepatic acute phase response. Genes Dev. 24, 381-395.
67. Villasenor, A., Chong, D. C., Henkemeyer, M. and Cleaver, O. (2010). Epithelial dynamics of pancreatic branching morphogenesis. Development 137, 4295-4305.
68. von Figura, G., Morris, J. P., Wright, C. V. E. and Hebrok, M. (2014). Nr5a2 maintains acinar cell differentiation and constrains oncogenic Kras-mediated pancreatic neoplastic initiation. Gut 63, 656-664.
69. Wagner, R. T., Xu, X., Yi, F., Merrill, B. J. and Cooney, A. J. (2010). Canonical Wnt/ beta-catenin regulation of liver receptor homolog-1 mediates pluripotency gene expression. Stem Cells 28, 1794-1804.
70. 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.
71. Xu, P.-L., Liu, Y.-Q., Shan, S.-F., Kong, Y.-Y., Zhou, Q., Li, M., Ding, J.-P., Xie, Y.-H. and Wang, Y. (2004). Molecular mechanism for the potentiation of the transcriptional activity of human liver receptor homolog 1 by steroid receptor coactivator-1. Mol. Endocrinol. 18
72. 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.
73. Zhou, Q., Law, A. C., Rajagopal, J., Anderson, W. J., Gray, P. A. and Melton, D. A. (2007). A multipotent progenitor domain guides pancreatic organogenesis. Dev. Cell 13, 103-114.