Abstract
3,3',4,4',5-Pentachlorobiphenyl (PenCB), one of the most toxic co-planar polychlorinated biphenyl congeners, specifically induces class Pi glutathione S-transferase (GSTP1) as well as cytochrome P-450 1A1 in primary cultured rat liver parenchymal cells [Aoki, Matsumoto and Suzuki (1993) FEBS Lett. 333, 114-118]. However, the 5'-flanking sequence of the GSTP1 gene does not contain a xenobiotic responsive element, to which arylhydrocarbon receptor binds. Using a chloramphenicol acetyltransferase assay we demonstrate here that the enhancer termed GSTP1 enhancer I (GPEI) is necessary for the stimulation by PenCB of GSTP1 gene expression in primary cultured rat liver parenchymal cells. GPEI is already known to contain a dyad of PMA responsive element-like elements oriented palindromically. It is suggested that a novel signal transduction pathway activated by PenCB contributes to the stimulation of GSTP1 expression.
Full Text
The Full Text of this article is available as a PDF (149.5 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Abramovitz M., Ishigaki S., Listowsky I. Differential regulation of glutathione S-transferases in cultured hepatocytes. Hepatology. 1989 Feb;9(2):235–239. doi: 10.1002/hep.1840090212. [DOI] [PubMed] [Google Scholar]
- Angel P., Imagawa M., Chiu R., Stein B., Imbra R. J., Rahmsdorf H. J., Jonat C., Herrlich P., Karin M. Phorbol ester-inducible genes contain a common cis element recognized by a TPA-modulated trans-acting factor. Cell. 1987 Jun 19;49(6):729–739. doi: 10.1016/0092-8674(87)90611-8. [DOI] [PubMed] [Google Scholar]
- Aoki Y., Matsumoto M., Suzuki K. T. Expression of glutathione S-transferase P-form in primary cultured rat liver parenchymal cells by coplanar polychlorinated biphenyl congeners is suppressed by protein kinase inhibitors and dexamethasone. FEBS Lett. 1993 Oct 25;333(1-2):114–118. doi: 10.1016/0014-5793(93)80386-9. [DOI] [PubMed] [Google Scholar]
- Aoki Y., Satoh K., Sato K., Suzuki K. T. Induction of glutathione S-transferase P-form in primary cultured rat liver parenchymal cells by co-planar polychlorinated biphenyl congeners. Biochem J. 1992 Jan 15;281(Pt 2):539–543. doi: 10.1042/bj2810539. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Birnbaum L. S. Developmental effects of dioxins and related endocrine disrupting chemicals. Toxicol Lett. 1995 Dec;82-83:743–750. doi: 10.1016/0378-4274(95)03592-3. [DOI] [PubMed] [Google Scholar]
- Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1016/0003-2697(76)90527-3. [DOI] [PubMed] [Google Scholar]
- Bronstein I., Fortin J., Stanley P. E., Stewart G. S., Kricka L. J. Chemiluminescent and bioluminescent reporter gene assays. Anal Biochem. 1994 Jun;219(2):169–181. doi: 10.1006/abio.1994.1254. [DOI] [PubMed] [Google Scholar]
- Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987 Apr;162(1):156–159. doi: 10.1006/abio.1987.9999. [DOI] [PubMed] [Google Scholar]
- Couture L. A., Abbott B. D., Birnbaum L. S. A critical review of the developmental toxicity and teratogenicity of 2,3,7,8-tetrachlorodibenzo-p-dioxin: recent advances toward understanding the mechanism. Teratology. 1990 Dec;42(6):619–627. doi: 10.1002/tera.1420420606. [DOI] [PubMed] [Google Scholar]
- Diccianni M. B., Imagawa M., Muramatsu M. The dyad palindromic glutathione transferase P enhancer binds multiple factors including AP1. Nucleic Acids Res. 1992 Oct 11;20(19):5153–5158. doi: 10.1093/nar/20.19.5153. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Favreau L. V., Pickett C. B. The rat quinone reductase antioxidant response element. Identification of the nucleotide sequence required for basal and inducible activity and detection of antioxidant response element-binding proteins in hepatoma and non-hepatoma cell lines. J Biol Chem. 1995 Oct 13;270(41):24468–24474. doi: 10.1074/jbc.270.41.24468. [DOI] [PubMed] [Google Scholar]
- Felgner P. L., Gadek T. R., Holm M., Roman R., Chan H. W., Wenz M., Northrop J. P., Ringold G. M., Danielsen M. Lipofection: a highly efficient, lipid-mediated DNA-transfection procedure. Proc Natl Acad Sci U S A. 1987 Nov;84(21):7413–7417. doi: 10.1073/pnas.84.21.7413. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ford S. R., Hall M. S., Leach F. R. Enhancement of firefly luciferase activity by cytidine nucleotides. Anal Biochem. 1992 Aug 1;204(2):283–291. doi: 10.1016/0003-2697(92)90239-4. [DOI] [PubMed] [Google Scholar]
- Gorman C. M., Merlino G. T., Willingham M. C., Pastan I., Howard B. H. The Rous sarcoma virus long terminal repeat is a strong promoter when introduced into a variety of eukaryotic cells by DNA-mediated transfection. Proc Natl Acad Sci U S A. 1982 Nov;79(22):6777–6781. doi: 10.1073/pnas.79.22.6777. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gorman C. M., Moffat L. F., Howard B. H. Recombinant genomes which express chloramphenicol acetyltransferase in mammalian cells. Mol Cell Biol. 1982 Sep;2(9):1044–1051. doi: 10.1128/mcb.2.9.1044. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gorman C. M., Moffat L. F., Howard B. H. Recombinant genomes which express chloramphenicol acetyltransferase in mammalian cells. Mol Cell Biol. 1982 Sep;2(9):1044–1051. doi: 10.1128/mcb.2.9.1044. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Halazonetis T. D., Georgopoulos K., Greenberg M. E., Leder P. c-Jun dimerizes with itself and with c-Fos, forming complexes of different DNA binding affinities. Cell. 1988 Dec 2;55(5):917–924. doi: 10.1016/0092-8674(88)90147-x. [DOI] [PubMed] [Google Scholar]
- Hayes J. D., Pulford D. J. The glutathione S-transferase supergene family: regulation of GST and the contribution of the isoenzymes to cancer chemoprotection and drug resistance. Crit Rev Biochem Mol Biol. 1995;30(6):445–600. doi: 10.3109/10409239509083491. [DOI] [PubMed] [Google Scholar]
- Hemming H., Flodström S., Wärngård L., Bergman A., Kronevi T., Nordgren I., Ahlborg U. G. Relative tumour promoting activity of three polychlorinated biphenyls in rat liver. Eur J Pharmacol. 1993 Aug 2;248(2):163–174. doi: 10.1016/0926-6917(93)90039-s. [DOI] [PubMed] [Google Scholar]
- Itoh K., Chiba T., Takahashi S., Ishii T., Igarashi K., Katoh Y., Oyake T., Hayashi N., Satoh K., Hatayama I. An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements. Biochem Biophys Res Commun. 1997 Jul 18;236(2):313–322. doi: 10.1006/bbrc.1997.6943. [DOI] [PubMed] [Google Scholar]
- Jarnagin W. R., Debs R. J., Wang S. S., Bissell D. M. Cationic lipid-mediated transfection of liver cells in primary culture. Nucleic Acids Res. 1992 Aug 25;20(16):4205–4211. doi: 10.1093/nar/20.16.4205. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jonat C., Rahmsdorf H. J., Park K. K., Cato A. C., Gebel S., Ponta H., Herrlich P. Antitumor promotion and antiinflammation: down-modulation of AP-1 (Fos/Jun) activity by glucocorticoid hormone. Cell. 1990 Sep 21;62(6):1189–1204. doi: 10.1016/0092-8674(90)90395-u. [DOI] [PubMed] [Google Scholar]
- Krishnan V., Safe S. Polychlorinated biphenyls (PCBs), dibenzo-p-dioxins (PCDDs), and dibenzofurans (PCDFs) as antiestrogens in MCF-7 human breast cancer cells: quantitative structure-activity relationships. Toxicol Appl Pharmacol. 1993 May;120(1):55–61. doi: 10.1006/taap.1993.1086. [DOI] [PubMed] [Google Scholar]
- Lee S. J., Friedman S. L., Whalen R., Boyer T. D. Cellular sources of glutathione S-transferase P in primary cultured rat hepatocytes: localization by in situ hybridization. Biochem J. 1994 Apr 1;299(Pt 1):79–83. doi: 10.1042/bj2990079. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lee W., Mitchell P., Tjian R. Purified transcription factor AP-1 interacts with TPA-inducible enhancer elements. Cell. 1987 Jun 19;49(6):741–752. doi: 10.1016/0092-8674(87)90612-x. [DOI] [PubMed] [Google Scholar]
- Lusska A., Shen E., Whitlock J. P., Jr Protein-DNA interactions at a dioxin-responsive enhancer. Analysis of six bona fide DNA-binding sites for the liganded Ah receptor. J Biol Chem. 1993 Mar 25;268(9):6575–6580. [PubMed] [Google Scholar]
- Mayura K., Spainhour C. B., Howie L., Safe S., Phillips T. D. Teratogenicity and immunotoxicity of 3,3',4,4',5-pentachlorobiphenyl in C57BL/6 mice. Toxicology. 1993 Jan 29;77(1-2):123–131. doi: 10.1016/0300-483x(93)90143-g. [DOI] [PubMed] [Google Scholar]
- Morimura S., Okuda A., Sakai M., Imagawa M., Muramatsu M. Analysis of glutathione transferase P gene regulation with liver cells in primary culture. Cell Growth Differ. 1992 Oct;3(10):685–691. [PubMed] [Google Scholar]
- Murray I. A., Lewendon A., Williams J. A., Cullis P. M., Lashford A. G., Shaw W. V. A novel substrate for assays of gene expression using chloramphenicol acetyltransferase. Nucleic Acids Res. 1991 Dec 11;19(23):6648–6648. doi: 10.1093/nar/19.23.6648. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nebert D. W., Puga A., Vasiliou V. Role of the Ah receptor and the dioxin-inducible [Ah] gene battery in toxicity, cancer, and signal transduction. Ann N Y Acad Sci. 1993 Jun 23;685:624–640. doi: 10.1111/j.1749-6632.1993.tb35928.x. [DOI] [PubMed] [Google Scholar]
- Okuda A., Imagawa M., Maeda Y., Sakai M., Muramatsu M. Structural and functional analysis of an enhancer GPEI having a phorbol 12-O-tetradecanoate 13-acetate responsive element-like sequence found in the rat glutathione transferase P gene. J Biol Chem. 1989 Oct 5;264(28):16919–16926. [PubMed] [Google Scholar]
- Okuda A., Imagawa M., Sakai M., Muramatsu M. Functional cooperativity between two TPA responsive elements in undifferentiated F9 embryonic stem cells. EMBO J. 1990 Apr;9(4):1131–1135. doi: 10.1002/j.1460-2075.1990.tb08219.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Okuda A., Sakai M., Muramatsu M. The structure of the rat glutathione S-transferase P gene and related pseudogenes. J Biol Chem. 1987 Mar 15;262(8):3858–3863. [PubMed] [Google Scholar]
- Rippe R. A., Brenner D. A., Leffert H. L. DNA-mediated gene transfer into adult rat hepatocytes in primary culture. Mol Cell Biol. 1990 Feb;10(2):689–695. doi: 10.1128/mcb.10.2.689. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Safe S. H. Polychlorinated biphenyls (PCBs): environmental impact, biochemical and toxic responses, and implications for risk assessment. Crit Rev Toxicol. 1994;24(2):87–149. doi: 10.3109/10408449409049308. [DOI] [PubMed] [Google Scholar]
- Sakai M., Okuda A., Muramatsu M. Multiple regulatory elements and phorbol 12-O-tetradecanoate 13-acetate responsiveness of the rat placental glutathione transferase gene. Proc Natl Acad Sci U S A. 1988 Dec;85(24):9456–9460. doi: 10.1073/pnas.85.24.9456. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Satoh K., Kitahara A., Soma Y., Inaba Y., Hatayama I., Sato K. Purification, induction, and distribution of placental glutathione transferase: a new marker enzyme for preneoplastic cells in the rat chemical hepatocarcinogenesis. Proc Natl Acad Sci U S A. 1985 Jun;82(12):3964–3968. doi: 10.1073/pnas.82.12.3964. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schüle R., Rangarajan P., Kliewer S., Ransone L. J., Bolado J., Yang N., Verma I. M., Evans R. M. Functional antagonism between oncoprotein c-Jun and the glucocorticoid receptor. Cell. 1990 Sep 21;62(6):1217–1226. doi: 10.1016/0092-8674(90)90397-w. [DOI] [PubMed] [Google Scholar]
- Smith C. L., Hager G. L. Transcriptional regulation of mammalian genes in vivo. A tale of two templates. J Biol Chem. 1997 Oct 31;272(44):27493–27496. doi: 10.1074/jbc.272.44.27493. [DOI] [PubMed] [Google Scholar]
- Subramani S., Southern P. J. Analysis of gene expression using simian virus 40 vectors. Anal Biochem. 1983 Nov;135(1):1–15. doi: 10.1016/0003-2697(83)90723-6. [DOI] [PubMed] [Google Scholar]
- Suemori H., Kadodawa Y., Goto K., Araki I., Kondoh H., Nakatsuji N. A mouse embryonic stem cell line showing pluripotency of differentiation in early embryos and ubiquitous beta-galactosidase expression. Cell Differ Dev. 1990 Mar;29(3):181–186. doi: 10.1016/0922-3371(90)90120-l. [DOI] [PubMed] [Google Scholar]
- Suguoka Y., Kano T., Okuda A., Sakai M., Kitagawa T., Muramatsu M. Cloning and the nucleotide sequence of rat glutathione S-transferase P cDNA. Nucleic Acids Res. 1985 Sep 11;13(17):6049–6057. doi: 10.1093/nar/13.17.6049. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tanno K., Aoki Y. Phosphorylation of c-Jun stimulated in primary cultured rat liver parenchymal cells by a coplanar polychlorinated biphenyl. Biochem J. 1996 Feb 1;313(Pt 3):863–866. doi: 10.1042/bj3130863. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tsuchida S., Sato K. Glutathione transferases and cancer. Crit Rev Biochem Mol Biol. 1992;27(4-5):337–384. doi: 10.3109/10409239209082566. [DOI] [PubMed] [Google Scholar]
- Xie T., Belinsky M., Xu Y., Jaiswal A. K. ARE- and TRE-mediated regulation of gene expression. Response to xenobiotics and antioxidants. J Biol Chem. 1995 Mar 24;270(12):6894–6900. doi: 10.1074/jbc.270.12.6894. [DOI] [PubMed] [Google Scholar]
- Yang-Yen H. F., Chambard J. C., Sun Y. L., Smeal T., Schmidt T. J., Drouin J., Karin M. Transcriptional interference between c-Jun and the glucocorticoid receptor: mutual inhibition of DNA binding due to direct protein-protein interaction. Cell. 1990 Sep 21;62(6):1205–1215. doi: 10.1016/0092-8674(90)90396-v. [DOI] [PubMed] [Google Scholar]
- Yao E. F., Denison M. S. DNA sequence determinants for binding of transformed Ah receptor to a dioxin-responsive enhancer. Biochemistry. 1992 Jun 2;31(21):5060–5067. doi: 10.1021/bi00136a019. [DOI] [PubMed] [Google Scholar]
- de Wet J. R., Wood K. V., DeLuca M., Helinski D. R., Subramani S. Firefly luciferase gene: structure and expression in mammalian cells. Mol Cell Biol. 1987 Feb;7(2):725–737. doi: 10.1128/mcb.7.2.725. [DOI] [PMC free article] [PubMed] [Google Scholar]