The mechanism of AH receptor protein down-regulation (degradation) and its impact on AH receptor-mediated gene regulation

Chemico-Biological Interactions

Volumn 141, Issue 1-2, 2002, Pages 41-61

  Pollenz, Richard S ^a  

^a UNIVERSITY OF SOUTH FLORIDA   (United States)

Author keywords

26S Proteasome; Aryl hydrocarbon receptor (AHR); Gene regulation; Protein degradation; Transcription factors

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; APROTININ; AROMATIC HYDROCARBON RECEPTOR; BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; CALPASTIN; CHLOROQUINE; LACTACYSIN; LEUPEPTIN; PD 150606; PROTEASOME; PROTEINASE INHIBITOR; TRANSCRIPTION FACTOR; UBIQUITIN; UNCLASSIFIED DRUG;

ARTICLE; CELL CULTURE; CELL NUCLEUS; DRUG EFFECT; GENE CONTROL; HUMAN; IN VITRO STUDY; IN VIVO STUDY; LIGAND BINDING; NONHUMAN; PROTEIN DEGRADATION; PROTEIN TRANSPORT; RECEPTOR DOWN REGULATION; SIGNAL TRANSDUCTION;

ANIMALS; DOWN-REGULATION; GENE EXPRESSION REGULATION; HUMANS; LIGANDS; PEPTIDE HYDROLASES; RECEPTORS, ARYL HYDROCARBON;

RODENTIA;

EID: 0037145007     PISSN: 00092797     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0009-2797(02)00065-0     Document Type: Article

References (76)

1. Whitlock J.P. Induction of cytochrome P4501A1. Annu. Rev. Pharmacol. Toxicol. 39:1999;103-125.
2. Gu Y.Z., Hogenesch J.B., Bradfield C.A. The PAS superfamily: sensors of environmental and developmental signals. Annu. Rev. Pharmacol. Toxicol. 40:2000;519-561.
3. Hahn M.E. The Ah receptor: a comparative perspective. Comp. Biochem. Physiol. 121:1998;23-53.
4. Crews S. Control of cell lineage-specific development and transcription by bHLH-PAS proteins. Genes Dev. 12:1998;607-620.
5. Giannone J.V., Okey A.B., Harper P.A. Charcaterization of polyclonal antibodies to the aromatic hydrocarbon receptor. Can. J. Physiol. Pharmacol. 73:1995;7-17.
6. Pollenz R.S. The Ah-receptor but not the Arnt protein is rapidly depleted in hepatic and non-hepatic culture cells exposed to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Mol. Pharmacol. 49:1996;391-398.
7. Pollenz R.S., Santostefano M.J., Klett E., Richardson V.M., Necela B., Birnbaum L.S. A single oral dose of TCDD results in sustained depletion of AHR protein in female Sprague-Dawley rats. Toxicol. Sci. 42:1998;117-128.
8. Roman B.L., Pollenz R.S., Peterson R.E. AHR and ARNT expression and CYP1A1 induction in the adult male rat reproductive tract. Toxicol. Appl. Pharmacol. 150:1998;228-239.
9. Sommer R.J., Sojka K., Pollenz R.S., Cooke P., Peterson R.E. AHR and ARNT protein and mRNA concentrations in rat prostate: effects of stage of development and TCDD. Toxicol. Appl. Pharmacol. 155:1999;177-189.
10. Giannone J.V., Li W., Probst M., Okey A. Prolonged depletion of AH receptor without alteration of receptor mRNA levels after treatment of cells in culture with for 2,3,7,8-tetrachloro-dibenzo-p-dioxin. Biochem. Pharmacol. 55:1998;489-497.
11. Pahl H.L., Baeuerle P.A. Control of gene expression by proteolysis. Curr. Opin. Cell Biol. 8:1996;340-347.
12. Palombella V.J., Rando O.J., Goldberg A.L., Maniatis T. The ubiquitin-proteasome pathway is required for processing the NF-κB1 precursor protein and the activation of NF-κB. Cell. 78:1994;773-785.
13. Hoeck W., Rusconi S., Groner B. Down regulation and phosphorylation of glucocorticoid receptors in cultured cell. J. Biol. Chem. 264:1989;14396-14402.
14. Haupt Y., Maya R., Kazaz A., Oren M. Mdm2 promotes the rapid degradation of p53. Nature. 387:1997;296-299.
15. Roth J., Dobbelstein M., Freedman D.A., Shenk T., Levine A.J. Nucleo-cytoplasmic shuttling of the hdm2 oncoprotein regulates the levels of p53 protein via a pathway used by the human immunodeficiency virus rev protein. EMBO J. 17:1998;554-564.
16. Huang L.E., Gu J., Schau M., Bunn H.F. Regulation of hypoxia inducible factor 1a is mediated by an oxygen-dependent domain via the ubiquitin-proteasome pathway. Proc. Natl. Acad. Sci. USA. 95:1998;7987-7992.
17. Pugh C.W., O'Rourke J.F., Nagao M., Gleadle J.M., Ratcliffe P.J. Activation of hypoxia inducible factor 1: definition of regulatory domains within the alpha subunit. J. Biol. Chem. 272:1997;11205-11214.
18. Salceda S., Caro J. Hypoxia-inducible factor 1a protein is rapidly degraded via the ubiquitin-proteasome system under normoxic conditions. J. Biol. Chem. 272:1997;22642-22650.
19. Davarinos N.A., Pollenz R.S. Aryl hydrocarbon receptor imported into the nucleus following ligand binding is rapidly degraded via the cytoplasmic proteasome following nuclear export. J. Biol. Chem. 274:1999;28707-28715.
20. Pollenz R.S. Barbour E.R. Analysis of the complex relationship between nuclear export and aryl hydrocarbon-mediated gene regulation Mol. Cell. Biol.
21. R.S. Pollenz, E.R. Barbour, Analysis of the complex relationship between nuclear export and aryl hydrocarbon-mediated gene regulation, Mol. Cell. Biol. 20 (2000) 6095-6104.
22. Ma Q., Renzelli A.J., Baldwin K.T., Antonini J.M. Superinduction of CYP1A1 gene expression. J. Biol. Chem. 275:2000;12676-12683.
23. Roberts B.J., Whitelaw M.L. Degradation of the basic helix-loop-helix/Per-ARNT-Sim homology domain dioxin receptor via the ubiquitin/proteasome pathway. J. Biol. Chem. 274:1999;36351-36356.
24. Harris M., Zacharewski T., Astroff B., Safe S. Partial antagonism by 2,3,7,8-tetrachlorodibenzo-p-dioxin mediated induction of aryl hydrocarbon hydroxylase by 6-methyl-1,3,8-trichlorodibenzofuran: mechanistic studies. Mol. Pharmacol. 35:1989;729-735.
25. Prokipcak R.D., Okey A.B. Down regulation of the Ah receptor in mouse hepatoma cells treated with 2,3,7,8-tetrachlorodibenzo-p-dioxin. Arch. Biochem. Biophys. 69:1991;1204-1210.
26. Swanson H.I., Perdew G.H. Half-life of the aryl hydrocarbon receptor in Hepa-1 cells. Arch. Biochem. Biophys. 302:1993;167-174.
27. Pollenz R.S., Sattler C.A., Poland A. The aryl hydrocarbon receptor and aryl hydrocarbon receptor nuclear translocator protein show distinct subcellular localizations in Hepa 1c1c7 cells by immunofluorescence microscopy. Mol. Pharmacol. 45:1994;428-438.
28. Poland A., Glover E., Bradfield C.A. Characterization of polyclonal antibodies to the Ah receptor prepared by immunization with a synthetic peptide hapten. Mol. Pharmacol. 39:1991;20-26.
29. Holmes J.L., Pollenz R.S. Determination of ARNT protein concentration and subcellular localization in hepatic and non-hepatic cell culture lines. Mol. Pharmacol. 52:1997;202-211.
30. Wormke M., Stoner M., Saville B., Safe S. Crosstalk between estrogen receptor a and the aryl hydrocarbon receptor in breast cancer cells involves unidirectional activation of proteasomes. FEBS Lett. 478:2000;109-112.
31. Okey A.B., Dube A.W., Vella L.M. Binding of benzo(a)pyrene and dibenz(a,h)anthracene to the Ah receptor in mouse and rat hepatic cytosols. Cancer Res. 44:1984;1426-1432.
32. Denomme M.A., Leece B., Li A., Towner R., Safe S. Elevation of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) polychlorinated biphenyls. Biochem. Pharmacol. 35:1986;277-282.
33. Bannister R., Davis D., Zacharewski T., Tizard I., Safe S. Aroclor 1254 as a 2,3,7,8-tetrachlorodibenzo-p-dioxin antagonist: effects on enzyme activity and immunotoxicity. Toxicology. 46:1987;29-42.
34. Sloop T.C., Lucier G.W. Dose-dependent elevation of Ah receptor binding by TCDD in rat liver. Toxicol. Appl. Pharmacol. 88:1987;329-337.
35. Abbott B.D., Perdew G.H., Birnbaum L.S. Ah receptor in mouse embryonic palate and the effects of TCDD on receptor expression. Toxicol. Appl. Pharmacol. 126:1994;16-25.
36. Bryant P.L., Clark G., Probst M.R., Abbott B.D. Effects of TCDD on Ah receptor, ARNT, EGF, and TGF-a expression in embryonic mouse urinary tract. Teratology. 55:1997;326-337.
37. Santiago-Josefat B., Pozo-Guisado E., Mulero-Navarro S., Fernandez-Salguero P.M. Proteasome inhibition induces nuclear translocation and transcriptional activation of the dioxin receptor in mouse primary fibroblasts in the absence of xenobiotics. Mol. Cell. Biol. 21:2001;1700-1709.
38. Tanaka K. Proteasomes: structure and biology. J. Biochem. 123:1998;195-204.
39. Ciechanover A., Orian A., Schwartz A.L. Ubiquitin-mediated proteolysis: biological regulation via destruction. Bioessays. 22:2000;442-451.
40. Kornitzer D., Ciechanover A. Modes of regulation of ubiquitin-mediated protein degradation. J. Cell. Physiol. 182:2000;1-11.
41. Hershko A., Heller H., Elias S., Ciechanover A. Components of ubiquitin-protein ligase system. Resolution, affinity purification, and role in protein breakdown. J. Biol. Chem. 258:1983;8206-8214.
42. Kulka R.G., Raboy B., Schuster R., Parag H.A., Diamond G., Ciechanover A., Marcus M. A Chinese hamster cell cycle mutant arrested at G2 phase has a temperature sensitive ubiquitin-activating enzyme, E1. J. Biol. Chem. 263:1988;15726-15731.
43. Burbach K.M., Poland A., Bradfield C.A. Cloning of the Ah-receptor cDNA reveals a distinctive ligand activated transcription factor. Proc. Natl. Acad. Sci. USA. 89:1992;8185-8189.
44. Kudo N., Wolff B., Sekimoto T., Schreiner E., Yoneda Y., Yanagida M., Horinouchi S., Yoshida M. Leptomycin B inhibition of signal-mediated nuclear export by direct binding to CRM1. Exp. Cell Res. 242:1998;540-547.
45. Kudo N., Khochbin S., Nishi K., Kitano K., Yanagida M., Yoshida M., Horinouchi S. Molecular cloning and cell cycle-dependent expression of mammalian CRM-1, a protein involved in nuclear export of proteins. J. Biol. Chem. 272:1997;29742-29751.
46. Ikuta T., Eguchi H., Tachibana T., Yoneda Y., Kawajiri K. Nuclear localization and export signals of the human aryl hydrocarbon receptor. J. Biol. Chem. 273:1998;2895-2904.
47. Richter C.A., Tillit D.E., Hannink M. Regulation of subcellular localization of the aryl hydrocarbon receptor (AhR). Arch. Biochem. Biophys. 389:2001;207-217.
48. Meyer B.K., Perdew G.H. Characterization of the AHR-hsp90-XAP2 ore complex and the role of the immunophilin-related protein XAP2 in AhR stabilization. Biochemistry. 38:1999;8907-8917.
49. LaPres J.J., Glover E., Dunham E.E., Bunger M.K., Bradfield C.A. ARA9 modifies agonist signaling through an increase in cytosolic aryl hydrocarbon receptor. J. Biol. Chem. 275:2000;6153-6159.
50. Meyer B.K., Pray-Grant M.G., Vanden Heuval J.P., Perdew G.H. Hepatitis B virus X-associated protein 2 is a subunit of the unliganded aryl hydrocarbon receptor core complex and exhibits transcriptional enhancer activity. Mol. Cell. Biol. 18:1998;978-988.
51. Whitesell L., Minmaugh E.G., Costa B.D., Meyers C.E., Neckers L.M. Inhibition of heat shock protein HSP90-pp60v-src heteroprotein complex formation by benzoquinone ansamycins: essential role for stress proteins in oncogenic transformation. Proc. Natl. Acad. Sci. USA. 91:1994;8324-8328.
52. Schulte T.W., Blagosklonny M.V., Ingui C., Neckers L.M. Disruption of the Raf-1-Hsp90 molecular complex results in destabilization of Raf-1 and loss of Raf-1-Ras association. J. Biol. Chem. 261:1995;24585-24588.
53. Chen H.-S., Singh S.S., Perdew G.H. The Ah receptor is a sensitive target of geldanamycin-induced protein turnover. Arch. Biochem. Biophys. 348:1997;190-198.
54. Heid S., Pollenz R.S., Swanson H.I. Role of hsp90 dissociation in mediating agonist induced activation of the Ah receptor. Mol. Pharmacol. 57:1999;82-92.
55. Pollenz R.S., Necela B. Characterization of two continuous cell lines from Oncorhynchus mykiss for models of AHR-mediated signal-transduction. Aquat. Toxicol. 41:1998;31-49.
56. Reick M., Robertson R.W., Pasco D.S., Fagan J.B. Down-regulation of nuclear aryl hydrocarbon receptor DNA-binding and transactivation functions. Mol. Cell. Biol. 14:1994;5653-5660.
57. Thompson J.F., Geoghengan K.F., Lloyd D.B., Lanzetti A.J., Magyar R.A., Anderson S.M., Branchini B.R. Mutation of a protease-sensitive region in firefly luciferase alters light emission properties. J. Biol. Chem. 272:1997;18766-18771.
58. Corey M.J., Kinders R.J., Brown L.G., Vessella R.L. A very sensitive coupled luminescent assay for cytotoxicity and complement-mediated lysis. J. Immunol. Methods. 207:1997;43-51.
59. Israel D.I., Estolano M.G., Galeazzi D.R., Whitlock J.P. Superinduction of cytochrome P1-450 gene transcription by inhibition of protein synthesis in wild type and variant mouse hepatoma cells. J. Biol. Chem. 260:1985;5648-5653.
60. Lusska A., Wu L., Whitlock J.P. Superinduction of CYP1A1 transcription by cycloheximide. Role of the DNA binding site for the liganded Ah receptor. J. Biol. Chem. 267:1992;15146-15151.
61. Bunn H.F., Poyton R.O. Oxygen sensing and molecular adaptation to hypoxia. Physiol. Rev. 76:1996;839-885.
62. Semenza G.L. Hypoxia-inducible factor 1: master regulator of O2 homeostasis. J. Lab. Clin. Med. 131:1998;207-214.
63. Pollenz R.S., Davarinos N.A., Shearer T.P. Analysis of aryl hydrocarbon receptor-mediated signaling during physiological hypoxia reveals lack of competition for the aryl hydrocarbon nuclear translocator transcription factor. Mol. Pharmacol. 56:1999;1127-1137.
64. Moffett P., Reece M., Pelletier J. The murine Sim-2 gene product inhibits transcription by active repression and functional interference. Mol. Cell. Biol. 17:1997;4933-4947.
65. Ema M., Morita M., Ikawa S., Tanaka M., Matsuda Y., Gotoh O., Saijoh Y., Fujii H., Hamada H., Kikuchi Y., Fuji-Kuriyama Y. Two new members of the murine Sim gene family are transcriptional repressors and show different expression patterns during mouse embyrogenesis. Mol. Cell. Biol. 16:1996;5865-5875.
66. Sogawa K., Nakano R., Kobayashi A., Kikuchi Y., Ohe N., Matsushita N., Fuji-Kuriyama Y. Possible function of Ah receptor nuclear translocator (ARNT) homodimer in transcriptional regulation. Proc. Natl. Acad. Sci. USA. 92:1995;1936-1940.
67. Swanson H.I., Chan W.K., Bradfield C.A. DNA binding specificities and pairing rules of the Ah receptor, ARNT, and SIM proteins. J. Biol. Chem. 270:1996;26292-26302.
68. Antonsson C., Arulampalam V., Whitelaw M.A., Petersson S., Poellinger L. Consititive function of the basic-helix-loop-helix/PAS factor ARNT. Regulation of target promoters via the E-box motif. J. Biol. Chem. 270:1995;13968-13972.
69. Long W.P., Chen X., Perdew G.H. Protein kinase C modulates aryl hydrocarbon receptor nuclear translocator protein-mediated transactivation potential in a dimer context. J. Biol. Chem. 274:1999;12391-12400.
70. Kozak K.R., Abbott B., Hankinson O. ARNT-deficient mice and placental differentiation. Dev. Biol. 191:1997;297-305.
71. Maltepe E., Schmidt J.V., Baunoch D., Bradfield C.A., Simon M.C. Abnormal angiogenesis and response to glucose and oxygen deprivation in mice lacking the protein ARNT. Nature. 386:1997;403-406.
72. Fernandez-Salguero P., Pineau T., Hilbert D.M., McPhail T., Lee S.S., Kimura S., Nebert D.W., Rudikoff S., Ward J.M., Gonzalez F.J. Immune system impairment and hepatic fibrosis in mice lacking the dioxin-binding Ah receptor. Science. 268:1995;722-726.
73. Hushka L.J., Williams J.S., Greenlee W.F. Characterization of 2,3,7,8-tetrachlorodibenzofuran-dependent suppression and Ah receptor pathway gene expression in the developing mouse mammary gland. Toxicol. Appl. Pharmacol. 152:1998;200-210.
74. Peters J.M., Narotsky M.G., Elizondo G., Fernandez-Salguero P.M., Gonzalez F.J., Abbott B.D. Amelioration of TCDD-induced teratogenesis in aryl hydrocarbon receptor (AhR)-null mice. Toxicol. Sci. 47:1999;86-92.
75. Abbott B.D., Schmid J.E., Pitt J.A., Buckalew A.R., Wood C.R., Held G.A., Diliberto J.J. Adverse reproductive outcomes in the transgenic Ah receptor-deficient mouse. Toxicol. Appl. Pharmacol. 155:1999;62-70.
76. Robles R., Morita Y., Mann K.K., Perez G.I., Yang S., Matikainen T., Sherr D.H., Tilly J.L. The aryl hydrocarbon receptor, a basic helix-loop-helix transcription factor of the PAS gene family, is required for normal ovarian germ cell dynamics in the mouse. Endocrinology. 141:2000;450-453.