Expansion of adult β-cell mass in response to increased metabolic demand is dependent on HNF-4α

Genes and Development

Volumn 21, Issue 7, 2007, Pages 756-769

  Gupta, Rana K ^a   Gao, Nan ^a   Gorski, Regina K ^a   White, Peter ^a   Hardy, Olga T ^a   Rafiq, Kiran ^a   Brestelli, John E ^a   Chen, Guang ^a   Stoeckert Jr , Christian J ^a   Kaestner, Klaus H ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

cells; Extracellular regulated kinase; Gestational diabetes; HNF 4 ; Mitogen activated protein kinase; Ras; Type 2 diabetes

Indexed keywords

HEPATOCYTE NUCLEAR FACTOR 4ALPHA; MITOGEN ACTIVATED PROTEIN KINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CARCINOGENICITY; CELL DIVISION; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; ENZYME PHOSPHORYLATION; FEMALE; GENE EXPRESSION; MALE; MATURITY ONSET DIABETES MELLITUS; MICROARRAY ANALYSIS; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PANCREAS ISLET BETA CELL; PHENOTYPE; PRIORITY JOURNAL; SUPPRESSION OF TUMORIGENICITY 5 GENE; TUMOR SUPPRESSOR GENE;

ANIMALS; BASE SEQUENCE; CELL PROLIFERATION; DNA-BINDING PROTEINS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMALE; HEPATOCYTE NUCLEAR FACTOR 4; INSULIN-SECRETING CELLS; ISLETS OF LANGERHANS; MICE; MICE, TRANSGENIC; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; PREGNANCY; RAS PROTEINS; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC; TUMOR SUPPRESSOR PROTEINS;

MUS;

EID: 34147173677     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.1535507     Document Type: Article

References (57)

1. Ahlgren, U., Jonsson, J., Jonsson, L., Simu, K., and Edlund, H. 1998. β-Cell-specific inactivation of the mouse Ipf1/Pdx1 gene results in loss of the β-cell phenotype and maturity onset diabetes. Genes & Dev. 12: 1763-1768.
2. Amaral, M.E., Ueno, M., Carvalheira, J.B., Carneiro, E.M., Velloso, L.A., Saad, M.J., and Boschero, A.C. 2003. Prolactin-signal transduction in neonatal rat pancreatic islets and interaction with the insulin-signaling pathway. Horm. Metab. Res. 35: 282-289.
3. Amaral, M.E., Cunha, D.A., Anhe, G.F., Ueno, M., Carneiro, E.M., Velloso, L.A., Bordin, S., and Boschero, A.C. 2004. Participation of prolactin receptors and phosphatidylinositol 3-kinase and MAP kinase pathways in the increase in pancreatic islet mass and sensitivity to glucose during pregnancy. J. Endocrinol. 183: 469-476.
4. Blake, J.A., Richardson, J.E., Bult, C.J., Kadin, J.A., and Eppig, J.T. 2003. MGD: The Mouse Genome Database. Nucleic Acids Res. 31: 193-195.
5. Briancon, N. and Weiss, M.C. 2006. In vivo role of the HNF4α AF-1 activation domain revealed by exon swapping. EMBO J. 25: 1253-1262.
6. Buchanan, T.A. and Xiang, A.H. 2005. Gestational diabetes mellitus. J. Clin. Invest. 115: 485-491.
7. Burns, C.J., Squires, P.E., and Persaud, S.J. 2000. Signaling through the p38 and p42/44 mitogen-activated families of protein kinases in pancreatic β-cell proliferation. Biochem. Biophys. Res. Commun. 268: 541-546.
8. Cirillo, L.A., Lin, F.R., Cuesta, I., Friedman, D., Jarnik, M., and Zaret, K.S. 2002. Opening of compacted chromatin by early developmental transcription factors HNF3 (FoxA) and GATA-4. Mol. Cell 9: 279-289.
9. Dor, Y., Brown, J., Martinez, O.I., and Melton, D.A. 2004. Adult pancreatic β-cells are formed by self-duplication rather than stem-cell differentiation. Nature 429: 41-46.
10. Ellard, S., Beards, F., Allen, L.I., Shepherd, M., Ballantyne, E., Harvey, R., and Hattersley, A.T. 2000. A high prevalence of glucokinase mutations in gestational diabetic subjects selected by clinical criteria. Diabetologia 43: 250-253.
11. Finegood, D.T., Scaglia, L., and Bonner-Weir, S. 1995. Dynamics of β-cell mass in the growing rat pancreas. Estimation with a simple mathematical model. Diabetes 44: 249-256.
12. Font de Mora, J., Esteban, L.M., Burks, D.J., Nunez, A., Garces, C., Garcia-Barrado, M.J., Iglesias-Osma, M.C., Moratinos, J., Ward, J.M., and Santos, E. 2003. Ras-GRF1 signaling is required for normal β-cell development and glucose homeostasis. EMBO J. 22: 3039-3049.
13. Friedman, J.R., Larris, B., Le, P.P., Peiris, T.H., Arsenlis, A., Schug, J., Tobias, J.W., Kaestner, K.H., and Greenbaum, L.E. 2004. Orthogonal analysis of C/EBPβ targets in vivo during liver proliferation. Proc. Natl. Acad. Sci. 101: 12986-12991.
14. Fukui, K., Yang, Q., Cao, Y., Takahashi, N., Hatakeyama, H., Wang, H., Wada, J., Zhang, Y., Marselli, L., Nammo, T., et al. 2005. The HNF-1 target collectrin controls insulin exocytosis by SNARE complex formation. Cell Metab. 2: 373-384.
15. Gupta, R.K., Vatamaniuk, M.Z., Lee, C.S., Flaschen, R.C., Fulmer, J.T., Matschinsky, F.M., Duncan, S.A., and Kaestner, K.H. 2005. The MODY1 gene HNF-4α regulates selected genes involved in insulin secretion. J. Clin. Invest.
16. Hagenfeldt-Johansson, K.A., Herrera, P.L., Wang, H., Gjinovci, A., Ishihara, H., and Wollheim, C.B. 2001. β-Cell-targeted expression of a dominant-negative hepatocyte nuclear factor-1 α induces a maturity-onset diabetes of the young (MODY)3-like phenotype in transgenic mice. Endocrinology 142: 5311-5320.
17. Hayhurst, G.P., Lee, Y.H., Lambert, G., Ward, J.M., and Gonzalez, F.J. 2001. Hepatocyte nuclear factor 4α (nuclear receptor 2A1) is essential for maintenance of hepatic gene expression and lipid homeostasis. Mol. Cell. Biol. 21: 1393-1403.
18. Heit, J.J., Apelqvist, A.A., Gu, X., Winslow, M.M., Neilson, J.R., Crabtree, G.R., and Kim, S.K. 2006. Calcineurin/NFAT signalling regulates pancreatic β-cell growth and function. Nature 443: 345-349.
19. Hosack, D.A., Dennis Jr., G., Sherman, B.T., Lane, H.C., and Lempicki, R.A. 2003. Identifying biological themes within lists of genes with EASE. Genome Biol. 4: R70.
20. Johnson, J.D., Ahmed, N.T., Luciani, D.S., Han, Z., Tran, H., Fujita, J., Misler, S., Edlund, H., and Polonsky, K.S. 2003. Increased islet apoptosis in Pdx1+/? mice. J. Clin. Invest. 111: 1147-1160.
21. 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.
22. Kaestner, K.H., Lee, C.S., Scearce, L.M., Brestelli, J.E., Arsenlis, A., Le, P.P., Lantz, K.A., Crabtree, J., Pizarro, A., Mazzarelli, J., et al. 2003. The transcriptional program of the endocrine pancreas. Diabetes 52: 1604-1610.
23. INK4a induces an age-dependent decline in islet regenerative potential. Nature 443: 453-457.
24. Kulkarni, R.N., Jhala, U.S., Winnay, J.N., Krajewski, S., Montminy, M., and Kahn, C.R. 2004. PDX-1 haploinsufficiency limits the compensatory islet hyperplasia that occurs in response to insulin resistance. J. Clin. Invest. 114: 828-836.
25. Lantz, K.A., Vatamaniuk, M.Z., Brestelli, J.E., Friedman, J.R., Matschinsky, F.M., and Kaestner, K.H. 2004. Foxa2 regulates multiple pathways of insulin secretion. J. Clin. Invest. 114: 512-520.
26. Lee, T.I., Rinaldi, N.J., Robert, F., Odom, D.T., Bar-Joseph, Z., Gerber, G.K., Hannett, N.M., Harbison, C.T., Thompson, C.M., Simon, I., et al. 2002. Transcriptional regulatory networks in Saccharomyces cerevisiae. Science 298: 799-804.
27. Li, Y., Hansotia, T., Yusta, B., Ris, F., Halban, P.A., and Drucker, D.J. 2003. Glucagon-like peptide-1 receptor signaling modulates β cell apoptosis. J. Biol. Chem. 278: 471-478.
28. Lichy, J.H., Majidi, M., Elbaum, J., and Tsai, M.M. 1996. Differential expression of the human ST5 gene in HeLa-fibroblast hybrid cell lines mediated by YY1: Evidence that YY1 plays a part in tumor suppression. Nucleic Acids Res. 24: 4700-4708.
29. Lu, Y., Herrera, P.L., Guo, Y., Sun, D., Tang, Z., LeRoith, D., and Liu, J.L. 2004. Pancreatic-specific inactivation of IGF-I gene causes enlarged pancreatic islets and significant resistance to diabetes. Diabetes 53: 3131-3141.
30. Majidi, M., Hubbs, A.E., and Lichy, J.H. 1998. Activation of extracellular signal-regulated kinase 2 by a novel Abl-binding protein, ST5. J. Biol. Chem. 273: 16608-16614.
31. Manduchi, E., Grant, G.R., He, H., Liu, J., Mailman, M.D., Pizarro, A.D., Whetzel, P.L., and Stoeckert Jr., C.J. 2004. RAD and the RAD Study-Annotator: An approach to collection, organization and exchange of all relevant information for high-throughput gene expression studies. Bioinformatics 20: 452-459.
32. McKenna, N.J. and O'Malley, B.W. 2002. Combinatorial control of gene expression by nuclear receptors and coregulators. Cell 108: 465-474.
33. Miura, A., Yamagata, K., Kakei, M., Hatakeyama, H., Takahashi, N., Fukui, K., Nammo, T., Yoneda, K., Inoue, Y., Sladek, F.M., et al. 2006. Hepatocyte nuclear factor-4α is essential for glucose-stimulated insulin secretion by pancreatic β-cells. J. Biol. Chem. 281: 5246-5257.
34. Odom, D.T., Zizlsperger, N., Gordon, D.B., Bell, G.W., Rinaldi, N.J., Murray, H.L., Volkert, T.L., Schreiber, J., Rolfe, P.A., Gifford, D.K., et al. 2004. Control of pancreas and liver gene expression by HNF transcription factors. Science 303: 1378-1381.
35. Parsons, J.A., Brelje, T.C., and Sorenson, R.L. 1992. Adaptation of islets of Langerhans to pregnancy: Increased islet cell proliferation and insulin secretion correlates with the onset of placental lactogen secretion. Endocrinology 130: 1459-1466.
36. Parviz, F., Matullo, C., Garrison, W.D., Savatski, L., Adamson, J.W., Ning, G., Kaestner, K.H., Rossi, J.M., Zaret, K.S., and Duncan, S.A. 2003. Hepatocyte nuclear factor 4α controls the development of a hepatic epithelium and liver morphogenesis. Nat. Genet. 34: 292-296.
37. Phuc Le, P., Friedman, J.R., Schug, J., Brestelli, J.E., Parker, J.B., Bochkis, I.M., and Kaestner, K.H. 2005. Glucocorticoid receptor-dependent gene regulatory networks. PLoS Genet. 1: e16.
38. Pruitt, K.D. and Maglott, D.R. 2001. RefSeq and LocusLink: NCBI gene-centered resources. Nucleic Acids Res. 29: 137-140.
39. Rachdi, L., Balcazar, N., Elghazi, L., Barker, D.J., Krits, I., Kiyokawa, H., and Bernal-Mizrachi, E. 2006. Differential effects of p27 in regulation of β-cell mass during development, neonatal period, and adult life. Diabetes 55: 3520-3528.
40. Ren, B., Robert, F., Wyrick, J.J., Aparicio, O., Jennings, E.G., Simon, I., Zeitlinger, J., Schreiber, J., Hannett, N., Kanin, E., et al. 2000. Genome-wide location and function of DNA binding proteins. Science 290: 2306-2309.
41. Rubins, N.E., Friedman, J.R., Le, P.P., Zhang, L., Brestelli, J., and Kaestner, K.H. 2005. Transcriptional networks in the liver: Hepatocyte nuclear factor 6 function is largely independent of Foxa2. Mol. Cell. Biol. 25: 7069-7077.
42. Scearce, L.M., Brestelli, J.E., McWeeney, S.K., Lee, C.S., Mazzarelli, J., Pinney, D.F., Pizarro, A., Stoeckert Jr., C.J., Clifton, S.W., Permutt, M.A., et al. 2002. Functional genomics of the endocrine pancreas: The pancreas clone set and PancChip, new resources for diabetes research. Diabetes 51: 1997-2004.
43. Shih, D.Q. and Stoffel, M. 2002. Molecular etiologies of MODY and other early-onset forms of diabetes. Curr. Diab. Rep. 2: 125-134.
44. Subramanian, A., Tamayo, P., Mootha, V.K., Mukherjee, S., Ebert, B.L., Gillette, M.A., Paulovich, A., Pomeroy, S.L., Golub, T.R., Lander, E.S., et al. 2005. Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. 102: 15545-15550.
45. Tusher, V.G., Tibshirani, R., and Chu, G. 2001. Significance analysis of microarrays applied to the ionizing radiation response. Proc. Natl. Acad. Sci. 98: 5116-5121.
46. Wang, H., Maechler, P., Hagenfeldt, K.A., and Wollheim, C.B. 1998. Dominant-negative suppression of HNF-1α function results in defective insulin gene transcription and impaired metabolism-secretion coupling in a pancreatic β-cell line. EMBO J. 17: 6701-6713.
47. Wang, H., Maechler, P., Antinozzi, P.A., Hagenfeldt, K.A., and Wollheim, C.B. 2000. Hepatocyte nuclear factor 4α regulates the expression of pancreatic β-cell genes implicated in glucose metabolism and nutrient-induced insulin secretion. J. Biol. Chem. 275: 35953-35959.
48. 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 HNF1β (MODY5) gene in β-cells leads to altered gene expression and defective insulin release. Endocrinology 145: 3941-3949.
49. Weng, J., Ekelund, M., Lehto, M., Li, H., Ekberg, G., Frid, A., Aberg, A., Groop, L.C., and Berntorp, K. 2002. Screening for MODY mutations, GAD antibodies, and type 1 diabetes-associated HLA genotypes in women with gestational diabetes mellitus. Diabetes Care 25: 68-71.
50. White, P., Brestelli, J.E., Kaestner, K.H., and Greenbaum, L.E. 2005. Identification of transcriptional networks during liver regeneration. J. Biol. Chem. 280: 3715-3722.
51. Wilson, M.E., Scheel, D., and German, M.S. 2003. Gene expression cascades in pancreatic development. Mech. Dev. 120: 65-80.
52. Yang, Y.H., Dudoit, S., Luu, P., Lin, D.M., Peng, V., Ngai, J., and Speed, T.P. 2002. Normalization for cDNA microarray data: A robust composite method addressing single and multiple slide systematic variation. Nucleic Acids Res. 30: e15.
53. Zaret, K. 1999. Developmental competence of the gut endoderm: Genetic potentiation by GATA and HNF3/fork head proteins. Dev. Biol. 209: 1-10.
54. Zaret, K.S. 2002. Regulatory phases of early liver development: Paradigms of organogenesis. Nat. Rev. Genet. 3: 499-512.
55. Zhang, H., Ackermann, A.M., Gusarova, G.A., Lowe, D., Feng, X., Kopsombut, U.G., Costa, R.H., and Gannon, M. 2006. The FoxM1 transcription factor is required to maintain pancreatic β-cell mass. Mol. Endocrinol. 20: 1853-1866.
56. Zhu, Y., King, B.L., Parvizi, B., Brunk, B.P., Stoeckert Jr., C.J., Quackenbush, J., Richardson, J., and Bult, C.J. 2003. Integrating computationally assembled mouse transcript sequences with the Mouse Genome Informatics (MGI) database. Genome Biol. 4: R16.
57. Zimmet, P., Alberti, K.G., and Shaw, J. 2001. Global and societal implications of the diabetes epidemic. Nature 414: 782-787.