Glucocorticoid receptor, C/EBP, HNF3, and protein kinase A coordinately activate the glucocorticoid response unit of the carbamoylphosphate synthetase I gene

Molecular and Cellular Biology

Volumn 18, Issue 11, 1998, Pages 6305-6315

  Christoffels, Vincent M ^a   Grange, Thierry ^b   Kaestner, Klaus H ^c   Cole, Timothy J ^d   Darlington, Gretchen J ^e   Croniger, Colleen M ^f   Lamers, Wouter H ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b INSTITUT JACQUES MONOD   (France)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d BAKER IDI HEART AND DIABETES INSTITUTE   (Australia)

^e BAYLOR COLLEGE OF MEDICINE   (United States)

^f CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBAMOYL PHOSPHATE SYNTHASE; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; GLUCOCORTICOID RECEPTOR; MESSENGER RNA; TRANSCRIPTION FACTOR;

ADOLESCENT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CHO CELL; CYCLIC AMP RESPONSIVE ELEMENT; EMBRYO; ENHANCER REGION; GENE ACTIVATION; GENE STRUCTURE; HEPATOMA CELL; HORMONE DEPENDENCE; HORMONE RESPONSIVE ELEMENT; LIVER; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA INTERACTION; TRANSCRIPTION REGULATION;

EID: 0031741137     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.18.11.6305     Document Type: Article

References (75)

1. Adams, C. C., and J. L. Workman. 1993. Nucleosome displacement in transcription. Cell 72:305-308.
2. Ang, S. L., and J. Rossant. 1994. HNF-3beta is essential for node and notochord formation in mouse development. Cell 78:561-574.
3. Beale, E. G., D. E. Clouthier, and R. E. Hammer. 1992. Cell-specific expression of cytosolic phosphoenolpyruvate carboxykinase in transgenic mice. FASEB J. 6:3330-3337.
4. Beato, M., P. Herrlich, and G. Schütz. 1995. Steroid hormone receptors: many actors in search of a plot. Cell 83:851-857.
5. Boshart, M., F. Weih, M. Nichols, and G. Schütz. 1991. The tissue-specific extinguisher locus TSE1 encodes a regulatory subunit of cAMP-dependent protein kinase. Cell 66:849-859.
6. Christoffels, V., and W. Lamers. Unpublished observations.
7. Christoffels, V. M., M. J. B. van den Hoff, M. C. Lamers, M. A. van Roon, P. A. J. de Boer, A. F. M. Moorman, and W. H. Lamers. 1996. The upstream regulatory region of the carbamoyl-phosphate synthetase I gene controls its tissue-specific, developmental and hormonal regulation in vivo. J. Biol. Chem. 271:31243-31250.
8. Christoffels, V. M., M. J. B. van den Hoff, A. F. M. Moorman, and W. H. Lamers. 1995. The far-upstream enhancer of the carbamoylphosphate synthetase I gene is responsible for the tissue specificity and hormone inducibility of its expression. J. Biol. Chem. 270:24932-24940.
9. Cole, T. J., J. A. Blendy, A. P. Monaghan, K. Krieglstein, W. Schmid, A. Aguzzi, G. Fantuzzi, E. Hummler, K. Unsicker, and G. Schütz. 1995. Targeted disruption of the glucocorticoid receptor gene blocks adrenergic chromaffin cell development and severely retards lung maturation. Genes Dev. 9:1608-1621.
10. Cram, E. J., R. A. Ramos, E. C. Wang, H. H. Cha, Y. Nishio, and G. L. Firestone. 1998. Role of CCAAT/enhancer binding protein alpha transcription factor in the glucocorticoid stimulation of p21 (waf1/cip1) gene promoter activity in growth-arrested rat hepatoma cells. J. Biol. Chem. 273:2008-2014.
11. Crosson, S. M., G. F. Davies, and W. J. Roesler. 1997. Hepatic expression of CCAAT/enhancer binding protein alpha: hormonal and metabolic regulation in rats. Diabetologia 40:1117-1124.
12. de Groot, C. J., D. Zonneveld, R. T. M. de Laaf, M. A. Dingemanse, P. G. Mooren, A. F. M. Moorman, W. H. Lamers, and R. Charles. 1986. Developmental and hormonal regulation of carbamoylphosphate synthetase gene expression in rat liver: evidence for control mechanisms at different levels in the perinatal period. Biochim. Biophys. Acta 866:61-67.
13. Dingemanse, M. A., P. A. J. de Boer, M. Mori, W. H. Lamers, and A. F. M. Moorman. 1996. Development of the ornithine cycle in rat liver: zonation of a metabolic pathway. Hepatology 24:407-411.
14. Ernest, M. J., C. L. Chen, and P. Feigelson. 1977. Induction of tyrosine aminotransferase synthesis in isolated liver cell suspensions. J. Biol. Chem. 252:6783-6791.
15. Espinas, M. L., J. Roux, J. Ghysdael, R. Pictet, and T. Grange. 1994. Participation of Ets transcription factors in the glucocorticoid response of the rat tyrosine aminotransferase gene. Mol. Cell Biol. 14:4116-4125.
16. Espinas, M. L., J. Roux, R. Pictet, and T. Grange. 1995. Glucocorticoids and protein kinase A coordinately modulate transcription factor recruitment at a glucocorticoid-responsive unit. Mol. Cell. Biol. 15:5346-5354.
17. Flodby, P., C. Barlow, H. Kylefjord, L. Ährlund-Richter, and K. G. Xanthopoulos. 1996. Increased hepatic cell proliferation and lung abnormalities in mice deficient in CCAAT/enhancer binding protein α. J. Biol. Chem. 271: 24753-24760.
18. Gebhardt, R., and D. Mecke. 1979. Permissive effect of dexametnasone on glucagon induction of urea-cycle enzymes in perifused primary monolayer cultures of rat hepatocytes. Eur. J. Biochem. 97:29-35.
19. Gebhardt, R., and D. Mecke. 1983. Heterogeneous distribution of glutamine synthetase among rat liver parenchymal cells in situ and in primary cultures. EMBO J. 2:567-570.
20. Girard, J. R., G. S. Cuendet, E. B. Marliss, A. Kervan, M. Rieutort, and R. Assan. 1973. Fuels, hormones and liver metabolism at term and during the early postnatal period. J. Clin. Invest. 52:3190-3200.
21. Gotoh, T., S. Chowdhury, M. Takiguchi, and M. Mori. 1997. The glucocorticoid-responsive gene cascade. J. Biol. Chem. 272:3694-3698.
22. Grange, T., J. Roux, G. Rigaud, and R. Pictet. 1990. Cell-type specific activity of two glucocorticoid responsive units of rat tyrosine aminotransferase gene is associated with multiple binding sites for C/EBP and a novel liver-specific nuclear factor. Nucleic Acids Res. 19:131-139.
23. Granner, D. K., A. Lee, and E. B. Thompson. 1977. Interaction of glucocorticoid hormones and cyclic nucleotides in induction of tyrosine aminotransferase in cultured hepatoma cells. J. Biol. Chem. 252:3891-3897.
24. Greengard, O. 1970. The developmental formation of enzymes in rat liver, p. 53-87. In G. Litwack (ed.), Biochemical actions of hormones. Academic Press, New York, N.Y.
25. Imai, E., J. N. Miner, J. A. Mitchell, K. R. Yamamoto, and D. K. Granner. 1993. Glucocorticoid receptor-cAMP response element-binding protein interaction and the response of the phosphoenolpyruvate carboxykinase gene to glucocorticoids. J. Biol. Chem. 268:5353-5356.
26. Jones, K. W., M. H. Shapero, M. Chevrette, and R. E. K. Fournier. 1991. Subtractive hybridization cloning of a tissue-specific extinguisher: TSE1 encodes a regulatory subunit of protein kinase A. Cell 66:861-872.
27. Jonker, A., P. A. J. de Boer, M. J. B. van den Hoff, W. H. Lamers, and A. F. M. Moorman. 1997. Towards quantitative in situ hybridisation. J. Histochem. Cytochem. 45:413-423.
28. Jungermann, K. 1995. Zonation of metabolism and gene expression in liver. Histochemistry 103:81-91.
29. Jungermann, K., and N. Katz. 1989. Functional specialization of different hepatocyte populations. Physiol. Rev. 69:708-764.
30. Jungermann, K., and T. Kietzmann. 1996. Zonation of parenchymal and nonparenchymal metabolism in liver. Annu. Rev. Nutr. 16:179-203.
31. Kaestner, K. H., H. Hiemisch, and G. Schutz. 1998. Targeted disruption of the gene encoding hepatocyte nuclear factor 3γ results in reduced transcription of hepatocyte-specific genes. Mol. Cell. Biol. 18:4245-4251.
32. Kitagawa, M., and E. Sugimoto. 1985. Interaction between glucocorticoids, 8-bromoadenosine 3′,5′ -monophosphate, and insulin in regulation of synthesis of carbamoyl-phosphate synthetase I in Reuber hepatoma H-35. Eur. J. Biochem. 150:249-254.
33. Lalli, E., and P. Sassone-Corsi. 1994. Signal transduction and gene regulation: the nuclear response to cAMP. J. Biol. Chem. 269:17359-17362.
34. Lamers, W. H., and P. G. Mooren. 1981. Multihormonal control of enzyme clusters in rat liver ontogenesis. II. Role of glucocorticosteroid and thyroid hormone and of glucagon and insulin. Mech. Aging Dev. 15:93-118.
35. Lamers, W. H., D. Zonneveld, and R. Charles. 1984. Inducibility of carbamoylphosphate synthetase (ammonia) in cultures of embryonic hepatocytes: Ontogenesis of the responsiveness to hormones. Dev. Biol. 105:500-508.
36. Lie-Venema, H., W. T. Labruyère, M. A. van Roon, P. A. J. de Boer, A. F. M. Moorman, A. J. M. Berns, and W. H. Lamers. 1995. The spatio-temporal control of the expression of glutamine synthetase in the liver is mediated by its 5′-enhancer. J. Biol. Chem. 270:28251-28256.
37. + cells. Am. J. Physiol. 271: F347-F355.
38. Lucas, P. C., and D. K. Granner. 1992. Hormone response domains in gene transcription. Annu. Rev. Biochem. 61:1131-1173.
39. Luisi, B. F., W. X. Xu, Z. Otwinowski, L. P. Freedman, K. R. Yamamoto, and P. B. Sigler. 1991. Crystallographic analysis of the interaction of the glucocorticoid receptor with DNA. Nature 352:497-505.
40. Matsuno, F., S. Chowdhury, T. Gotoh, K. Iwase, H. Matsuzaki, K. Takatsuki, M. Mori, and M. Takiguchi. 1996. Induction of the C/EBP beta gene by dexamethasone and glucagon in primary-cultured rat hepatocytes. J. Biochem. 119:524-532.
41. McEwan, I. J., A. P. H. Wright, and J. A. Gustafsson. 1997. Mechanism of gene expression by the glucocorticoid receptor: role of protein-protein interactions. Bioessays 19:153-160.
42. McGrane, M. M., J. S. Yun, A. F. M. Moorman, W. H. Lamers, G. Hendrick, B. Arafah, T. E. Wagner, and R. W. Hanson. 1990. Metabolic effects of developmental tissue and cell specific expression of a chimeric phosphoenol-pyruvate carboxykinase (GTP)/bovine growth hormone gene in transgenic mice. J. Biol. Chem. 265:22371-22379.
43. Meijer, A. J., W. H. Lamers, and R. A. F. M. Chamuleau. 1990. Nitrogen metabolism and ornithine cycle function. Physiol. Rev. 70:701-748.
44. Moorman, A. F. M., P. A. J. de Boer, M. Watford, M. A. Dingemanse, and W. H. Lamers. 1994. Hepatic glutaminase mRNA is confined to a part of the urea cycle domain in the adult rodent liver lobule. FEBS Lett. 356:76-80.
45. Morris, S. M. 1992. Regulation of enzymes of urea and arginine synthesis. Annu. Rev. Nutr. 12:81-101.
46. Morris, S. M., C. L. Moncman, K. D. Rand, G. J. Dizikes, D. D. Cederbaum, and W. E. O'Brien. 1987. Regulation of mRNA levels for five urea cycle enzymes in rat liver by diet, cyclic AMP and glucocorticoids. Arch. Biochem. Biophys. 256:343-353.
47. Moyer, M. L., K. C. Borror, B. J. Bona, D. B. DeFranco, and S. K. Nordeen. 1993. Modulation of cell signaling pathways can enhance or impair glucocorticoid-induced gene expression without altering the state of receptor phosohorylation. J. Biol. Chem. 268:22933-22940.
48. Nebes, V. L., and S. M. Morris. 1987. Induction of mRNA for phosphoenol-pyruvate carboxykinase (GTP) by dexamethasone in cultured rat hepatocytes requires on-going protein synthesis. Biochem. J. 246:237-240.
49. Nebes, V. L., and S. M. Morris. 1988. Regulation of messenger ribonucleic acid levels for five urea enzymes in cultured rat hepatocytes. Requirements for cyclic adenosine monophosphate, glucocorticoids and ongoing protein synthesis. Mol. Endocrinol. 2:444-451.
50. Nichols, M., F. Weih, W. Schmid, C. DeVack, E. Kowenz-Leutz, B. Luckow, M. Boshart, and G. Schütz. 1992. Phosphorylation of CREB affects its binding to high and low affinity sites: implications for cAMP induced gene transcription. EMBO J. 11:3337-3346.
51. Nishio, Y., H. Isshiki, T. Kishimoto, and S. Akira. 1993. A nuclear factor for interleukin-6 expression (NF-IL6) and the glucocorticoid receptor synergistically activate transcription of the rat alphal-acid glycoprotein gene via direct protein-protein interaction. Mol. Cell. Biol. 13:1854-1862.
52. Nitsch, D., M. Boshart, and G. Schütz. 1993. Activation of the tyrosine aminotransferase gene is dependent on synergy between liver-specific and hormone-responsive elements. Proc. Natl. Acad. Sci. USA 90:5479-5483.
53. Nordeen, S. K., B. J. Suh, B. Kühnel, and C. A. Hutchison. 1990. Structural determinants of a glucocorticoid receptor recognition element. Mol. Endocrinol. 4:1866-1873.
54. Ramesh, T. M., A. W. Ellis, and B. T. Spear. 1995. Individual mouse α-fetoprotein enhancer elements exhibit different patterns of tissue-specific and hepatic position-dependent activities. Mol. Cell. Biol. 15:4947-4955.
55. Rangarajan, P. N., K. Umesono, and R. M. Evans. 1992. Modulation of glucocorticoid receptor function by protein kinase A. Mol. Endocrinol. 6:1451-1457.
56. Rigaud, G., J. Roux, R. Pictet, and T. Grange. 1991. In vivo footprinting of rat TAT gene: dynamic interplay between the glucocorticoid receptor and a liver-specific factor. Cell 67:977-986.
57. Roesler, W. J., S. M. Crosson, C. Vinson, and P. J. McFie. 1996. The α-isoform of the CCAAT/enhancer-binding protein is required for mediating cAMP responsiveness of the phosphoenolpyruvate carboxykinase promoter in hepatoma cells. J. Biol. Chem. 271:8068-8074.
58. Roux, J., R. Pictet, and T. Grange. 1995. Hepatocyte nuclear factor 3 determines the amplitude of the glucocorticoid response of the rat tyrosine aminotransferase gene. DNA Cell Biol. 14:385-396.
59. Ruppert, S., M. Boshart, F. X. Bosch, W. Schmid, R. E. K. Fournier, and G. Schütz. 1990. Two genetically defined transacting loci coordinately regulate overlapping sets of liver-specific genes. Cell 61:895-905.
60. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
61. Sassi, H., R. Pictet, and T. Grange. 1998. Glucocorticoids are insufficient for neonatal gene induction in the liver. Proc. Natl. Acad. Sci. USA 95:5621-5625.
62. Schmid, W., D. Nitsch, M. Boshart, and G. Schütz. 1993. Role of cyclic AMP in the control of cell-specific gene expression. Trends Endocrinol. Metab. 4:204-209.
63. Schudt, C. 1979. Hormonal regulation of glucokinase in primary cultures of rat hepatocytes. Eur. J. Biochem. 98:77-82.
64. Schüle, R., M. Muller, C. Kaltschmidt, and R. Renkawitz. 1988. Many transcription factors interact synergistically with steroid receptors. Science 242:1418-1420.
65. Seitz, H. J., W. Lüth, and W. Tarnowski. 1979. Regulation of rat liver glucokinase activity in vivo: predominant role of hepatic cyclic AMP and glucocorticoids. Arch. Biochem. Biophys. 195:385-391.
66. Singer, R. H., J. B. Lawrence, and C. Villnave. 1986. Optimization of in situ hybridization using isotopic and non-isotopic detection methods. BioTechniques 4:230-250.
67. Takiguchi, M., and M. Mori. 1995. Transcriptional regulation of genes for ornithine cycle enzymes. Biochem. J. 312:649-659.
68. Tomomura, M., A. Tomomura, D. A. Musa, M. Horiuchi, M. Takiguchi, M. Mori, and T. Saheki. 1997. Suppressed expression of the urea cycle enzyme genes in the liver of carnitine-deficient juvenile visceral steatosis (JVS) mice in infancy and during starvation in adulthood. J. Biochem. 121:172-177.
69. Truss, M., and M. Beato. 1993. Steroid hormone receptors: interaction with deoxyribonucleic acid and transcription factors. Endocrinol. Rev. 14:459-479.
70. van den Hoff, M. J. B., L. P. W. G. M. van de Zande, M. A. Dingemanse, A. T. Das, W. T. Labruyère, A. F. M. Moorman, R. Charles, and W. H. Lamers. 1995. Isolation and characterization of the rat gene for carbamoylphosphate synthetase I. Eur. J. Biochem. 228:351-361.
71. Wang, N., M. J. Finegold, A. Bradley, C. N. OU, S. V. Abdelsayed, M. D. Wilde, D. R. Taylor, D. R. Wilson, and G. J. Darlington. 1995. Impaired energy homeostasis in C/EBPα knockout mice. Science 269:1108-1112.
72. Weinstein, D. C., A. R. I. Altaba, W. S. Chen, P. Hoodless, V. R. Prezioso, T. M. Jessell, and J. E. Darnell, Jr. 1994. The winged-helix transcription factor HNF-3beta is required for notochord development in the mouse embryo. Cell 78:575-588.
73. Wu, K. C., and M. Pfahl. 1988. Variable responsiveness of hormone-inducible hybrid genes in different cell lines. Mol. Endocrinol. 2:1294-1301.
74. Yamamoto, K. K., G. A. Gonzalez, W. H. Biggs III, and M. R. Montminy. 1988. Phosphorylation-induced binding and transcriptional efficacy of nuclear factor CREB. Nature 334:494-498.
75. Zhang, H., Y.-C. Li, and A. P. Young. 1993. Protein kinase A activation of glucocorticoid-mediated signaling in the developing retina. Proc. Natl. Acad. Sci. USA 90:3880-3884.