A dynamic role for the Ah receptor in cell signaling? Insights from a diverse group of Ah receptor interacting proteins

Journal of Biochemical and Molecular Toxicology

Volumn 16, Issue 6, 2002, Pages 317-325

  Carlson, David B ^b   Perdew, Gary H ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

Author keywords

Ah receptor; ARNT; bHLH PAS proteins; Coregulators; Cross talk; Estrogen receptor; HSP90; NF B; Protein kinase C; Protein Protein interactions; Rb; Signal transduction

Indexed keywords

AROMATIC HYDROCARBON RECEPTOR; CASEIN KINASE II; CHAPERONE; DIOXIN; ESTROGEN RECEPTOR; HEAT SHOCK PROTEIN 90; HELIX LOOP HELIX PROTEIN; HORMONE RECEPTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; IMMUNOPHILIN; LIGAND; PHOSPHATASE; PROTEIN KINASE; PROTEIN KINASE C; PROTEIN P23; PROTEIN TYROSINE KINASE; RETINOBLASTOMA PROTEIN; TRANSCRIPTION FACTOR;

ANGIOGENESIS; ANIMAL CELL; BINDING AFFINITY; CELL DIFFERENTIATION; CELL GROWTH; COMPLEX FORMATION; CONTROLLED STUDY; CYTOTOXICITY; DIMERIZATION; HOMEOSTASIS; HYPOXIA; LIGAND BINDING; LIVER DEVELOPMENT; MOUSE; NONHUMAN; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN PROTEIN INTERACTION; RAT; RECEPTOR BINDING; REVIEW; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION;

ANIMALS; ANOXIA; BINDING, COMPETITIVE; CELL CYCLE; HUMANS; PHOSPHORYLATION; PROMOTER REGIONS (GENETICS); PROTEIN BINDING; RECEPTORS, ARYL HYDROCARBON; RECEPTORS, STEROID; SIGNAL TRANSDUCTION; TETRACHLORODIBENZODIOXIN; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS;

EID: 12244275029     PISSN: 10956670     EISSN: None     Source Type: Journal    
DOI: 10.1002/jbt.10051     Document Type: Review

References (82)

1. Gu YZ, Hogenesch JB, Bradfield CA. The PAS superfamily: Sensors of environmental and developmental signals. Annu Rev Pharmacol Toxicol 2000;40:519-561.
2. Waliser JA, Bradfield CA. The aryl hydrocarbon receptor: A model of gene-environment interactions. In: Vanden Heuvel JP, Perdew GH, Mattes WB, Greenlee WF, editors. Comprehensive Toxicology: Cellular and Molecular Toxicology. Amsterdam: Elsevier; 2002. pp 119-132.
3. Crews ST, Fan CM. Remembrance of things PAS: Regulation of development by bHLH-PAS proteins. Curr Opin Genet Dev 1999;9(5):580-587.
4. Schmidt JV, Su GH, Reddy JK, Simon MC, Bradfield CA. Characterization of a murine Ahr null allele: Involvement of the Ah receptor in hepatic growth and development. PNAS 1996;93(13):6731-6736.
5. Lahvis GP, Lindell SL, Thomas RS, McCuskey RS, Murphy C, Glover E, Bentz M, Southard J, Bradfield CA. Portosystemic shunting and persistent fetal vascular structures in aryl hydrocarbon receptor-deficient mice. PNAS 2000;97(19):10442-10447.
6. Gonzalez FJ, Fernandez-Salguero P. The aryl hydrocarbon receptor: Studies using the AHR-null mice. Drug Metab Dispos 1998;26(12):1194-1198.
7. Zaher H, Fernandez-Salguero PM, Letterio J, Sheikh MS, Fornace AJ Jr, Roberts AB, Gonzalez FJ. The involvement of aryl hydrocarbon receptor in the activation of transforming growth factor-beta and apoptosis. Mol Pharmacol 1998;54(2):313-321.
8. Safe S, Wang F, Porter W, Duan R, McDougal A. Ah receptor agonists as endocrine disruptors: Antiestrogenic activity and mechanisms. Toxicol Lett 1998;102-103:343-347.
9. Klinge CM, Bowers JL, Kulakosky PC, Kamboj KK, Swanson HI. The aryl hydrocarbon receptor (AHR)/AHR nuclear translocator (ARNT) heterodimer interacts with naturally occurring estrogen response elements. Mol Cell Endocrinol 1999;157(1-2):105-119.
10. Weiss C, Kolluri SK, Kiefer F, Gottlicher M. Complementation of Ah receptor deficiency in hepatoma cells: Negative feedback regulation and cell-cycle control by the Ah receptor. Exp Cell Res 1996;226(1):154-163.
11. Nebert DW, Roe AL, Dieter MZ, Solis WA, Yang Y, Dalton TP. Role of the aromatic hydrocarbon receptor and [Ah] gene battery in the oxidative stress response, cell-cycle control, and apoptosis. Biochem Pharmacol 2000;59(1):65-85.
12. Denison MS, Phelan D, Elferink CJ. The Ah receptor signal transduction pathway. In: Denison MS, Helferich WG, editors. Toxicant-Receptor Interactions: Modulation of Signal Transduction and Gene Expression. Bristol, PA: Taylor and Francis; 1998. pp 3-33.
13. Denison MS, Heath-Pagliuso S. The Ah receptor: A regulator of the biochemical and toxicological actions of structurally diverse chemicals. Bull Environ Contam Toxicol 61(5):557-568.
14. Petrulis JR, Perdew GH. The role of chaperone proteins in the aryl hydrocarbon receptor core complex. Chem Biol Interact 141(1-2):25-40.
15. Richter CA, Tillitt DE, Hannink M. Regulation of subcellular localization of the aryl hydrocarbon receptor (AhR). Arch Biochem Biophys 2001;389(2):207-217.
16. Bombick DW, Jankun J, Tullis K, Matsumura F. 2,3,7,8-Tetrachlorodibenzo-p-dioxin causes increases in expression of c-erb-A and levels of protein-tyrosine kinases in selected tissues of responsive mouse strains. PNAS 1988;85(12):4128-4132.
17. Pongratz I, Stromstedt PE, Mason GG, Poellinger L. Inhibition of the specific DNA binding activity of the dioxin receptor by phosphatase treatment. J Biol Chem 1991;266(25):16813-16817.
18. Gradin K, Whitelaw ML, Toftgard R, Poellinger L, Berghard A. A tyrosine kinase-dependent pathway regulates ligand-dependent activation of the dioxin receptor in human keratinocytes. J Biol Chem 1994;269(38):23800-23807.
19. Buchner J. Hsp90 & Co.- A holding for folding. Trends Biochem Sci 1999;24(4):136-141.
20. Mimura J, Ema M, Sogawa K, Fujii-Kuriyama Y. Identification of a novel mechanism of regulation of Ah (dioxin) receptor function. Genes Dev 1999;13(1):20-25.
21. Gradin K, Toftgard R, Poellinger L, Berghard A. Repression of dioxin signal transduction in fibroblasts. Identification of a putative repressor associated with Arnt. J Biol Chem 1999;274(19):13511-13518.
22. Porterfield SP. Thyroidal dysfunction and environmental chemicals - Potential impact on brain development. Environ Health Perspect 2000;108(S3):433-438.
23. Wong GY, Bradlow L, Sepkovic D, Mehl S, Mailman J, Osborne MP. Dose-ranging study of indole-3-carbinol for breast cancer prevention. J Cell Biochem Suppl 1997;28-29:111-116.
24. Klinge CM, Kaur K, Swanson HI. The aryl hydrocarbon receptor interacts with estrogen receptor alpha and orphan receptors COUP-TFI and ERRalpha1. Arch Biochem Biophys 2000;373(1):163-174.
25. Wormke M, Stoner M, Saville B, Safe S. Cross talk between estrogen receptor alpha and the aryl hydrocarbon receptor in breast cancer cells involves unidirectional activation of proteasomes. FEBS Lett 2000;478(1-2):109-112.
26. Jana NR, Sarkar S, Ishizuka M, Yonemoto J, Tohyama C, Sone H. Comparative effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin on MCF-7, RL95-2, and LNCaP cells: Role of target steroid hormones in cellular responsiveness to CYP1A1 induction. Mol Cell Biol Res Commun 2000;4(3):174-180.
27. Ricci MS, Toscano DG, Mattingly CJ, Toscano WA Jr. Estrogen receptor reduces CYP1A1 induction in cultured human endometrial cells. J Biol Chem 1999;274(6):3430-3438.
28. Rogers JM, Denison MS. Analysis of the antiestrogenic activity of 2,3,7,8-tetrachlorodibenzo-p-dioxin in human ovarian carcinoma BG-1 cells. Mol Pharmacol 2002;61(6):1393-1403.
29. Kharat I, Saatcioglu F. Antiestrogenic effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin are mediated by direct transcriptional interference with the liganded estrogen receptor. Cross talk between aryl hydrocarbon- and estrogen- mediated signaling. J Biol Chem 1996;271(18):10533-10537.
30. Wang W, Smith R, III, Safe S. Aryl hydrocarbon receptor-mediated antiestrogenicity in MCF-7 cells: Modulation of hormone-induced cell-cycle enzymes. Arch Biochem Biophys 1998;356(2):239-248.
31. Hall JM, McDonnell DP, Korach KS. Allosteric regulation of estrogen receptor structure, function, and coactivator recruitment by different estrogen response elements. Mol Endocrinol 2002;16(3):469-486.
32. Gradin K, McGuire J, Wenger RH, Kvietikova I, Fhitelaw ML, Toftgard R, Tora L, Gassmann M, Poellinger L. Functional interference between hypoxia and dioxin signal transduction pathways: Competition for recruitment of the Arnt transcription factor. Mol Cell Biol 1996;16(10):5221-5231.
33. Pollenz RS, Davarinos NA, Shearer TP. Analysis of aryl hydrocarbon receptor-mediated signaling during physiological hypoxia reveals lack of competition for the aryl hydrocarbon nuclear translocator transcription factor. Mol Pharmacol 1999;56(6):1127-1137.
34. Tomita S, Sinal CJ, Yim SH, Gonzalez FJ. Conditional disruption of the aryl hydrocarbon receptor nuclear translocator (Arnt) gene leads to loss of target gene induction by the aryl hydrocarbon receptor and hypoxia-inducible factor 1alpha. Mol Endocrinol 2000;14(10):1674-1681.
35. Chan WK, Yao G, Gu YZ, Bradfield CA. Cross-talk between the aryl hydrocarbon receptor and hypoxia inducible factor signaling pathways. Demonstration of competition and compensation. J Biol Chem 1999;274(17):12115-12123.
36. Nie M, Blankenship AL, Giesey JP. Interactions between aryl hydrocarbon receptor (AhR) and hypoxia signaling pathways. Environ Toxicol Pharmacol 2001;10:17-27.
37. Reisdorph R, Lindahl R. Aldehyde dehydrogenase 3 gene regulation: Studies on constitutive and hypoxia-modulated expression. Chem Biol Interact 2001;130-132(1-3):227-233.
38. McKay LI, Cidlowski JA. Cross talk between nuclear factor-kappa B and the steroid hormone receptors: Mechanisms of mutual antagonism. Mol Endocrinol 1998;12(1):45-56.
39. Kim DW, Gazourian L, Quadri SA, Romieu-Mourez R, Sherr DH, Sonenshein GE. The RelA NF-kappaB subunit and the aryl hydrocarbon receptor (AhR) cooperate to transactivate the c-myc promoter in mammary cells. Oncogene 2000;19(48):5498-5506.
40. Tian Y, Ke S, Denison MS, Rabson AB, Gallo MA. Ah receptor and NF-kappaB interactions, a potential mechanism for dioxin toxicity. J Biol Chem 1999;274(1):510-515.
41. Ke S, Rabson AB, Germino JF, Gallo MA, Tian Y. Mechanism of suppression of cytochrome P-450 1A1 expression by tumor necrosis factor-alpha and lipopolysaccharide. J Biol Chem 2001;276(43):39638-39644.
42. Baba T, Mimura J, Gradin K, Kuroiwa A, Watanabe T, Matsuda Y, Inazawa J, Sogawa K, Fujii-Kuriyama Y. Structure and expression of the Ah receptor repressor gene. J Biol Chem 2001;276(35):33101-33110.
43. Kolluri SK, Weiss C, Koff A, Gottlicher M. p27(Kip1) induction and inhibition of proliferation by the intracellular Ah receptor in developing thymus and hepatoma cells. Genes Dev 1999;13(13):1742-1753.
44. Ge NL, Elferink CJ. A direct interaction between the aryl hydrocarbon receptor and retinoblastoma protein. Linking dioxin signaling to the cell-cycle. J Biol Chem 1998;273(35):22708-22713.
45. Puga A, Barnes SJ, Dalton TP, Chang C, Knudsen ES, Maier MA. Aromatic hydrocarbon receptor interaction with the retinoblastoma protein potentiates repression of E2F-dependent transcription and cell-cycle arrest. J Biol Chem 2000;275(4):2943-2950.
46. Elferink CJ, Ge NL, Levine A. Maximal aryl hydrocarbon receptor activity depends on an interaction with the retinoblastoma protein. Mol Pharmacol 2001;59(4):664-673.
47. Reiners JJ Jr, Clift RE. Aryl hydrocarbon receptor regulation of ceramide-induced apoptosis in murine hepatoma 1c1c7 cells. A function independent of aryl hydrocarbon receptor nuclear translocator. J Biol Chem 1999;274(4):2502-2510.
48. Kumar MB, Perdew GH. Modulation of soluble receptor signaling by coregulators. In: Vanden Heuvel JP, Perdew GH, Mattes WB, Greenlee WF, editors. Comprehensive Toxicology: Cellular and Molecular Toxicology. Amsterdam: Elsevier; 2002. pp 202-220.
49. Nguyen TA, Hoivik D, Lee JE, Safe S. Interactions of nuclear receptor coactivator/corepressor proteins with the aryl hydrocarbon receptor complex. Arch Biochem Biophys 1999;367(2):250-257.
50. Rushing SR, Denison MS. The silencing mediator of retinoic acid and thyroid hormone receptors can interact with the aryl hydrocarbon (Ah) receptor but fails to repress Ah receptor-dependent gene expression. Arch Biochem Biophys 403(2):189-201.
51. Kumar MB, Tarpey RW, Perdew GH. Differential recruitment of coactivator RIP140 by Ah and estrogen receptors. Absence of a role for LXXLL motifs. J Biol Chem 1999;274(32):22155-22164.
52. Kobayashi A, Numayama-Tsuruta K, Sogawa K, Fujii-Kuriyama Y. CBP/p300 functions as a possible transcriptional coactivator of Ah receptor nuclear translocator (Arnt). J Biochem (Tokyo) 1997;122(4):703-710.
53. Tohkin M, Fukuhara M, Elizondo G, Tomita S, Gonzalez FJ. Aryl hydrocarbon receptor is required for p300-mediated induction of DNA synthesis by adenovirus E1A. Mol Pharmacol 2000;58(4):845-851.
54. Beischlag TV, Wang S, Rose DW, Torchia J, Reisz-Porszasz S, Muhammad K, Nelson WE, Probst MR, Rosenfeld MG, Hankinson O. Recruitment of the NCoA/SRC-1/p160 family of transcriptional coactivators by the aryl hydrocarbon receptor/aryl hydrocarbon receptor nuclear translocator complex. Mol Cell Biol 2002;22(12):4319-4333.
55. Ravi R, Mookerjee B, van Hensbergen Y, Bedi GC, Giordano A, El Deiry WS, Fuchs EJ, Bedi A. p53-mediated repression of nuclear factor-kappaB RelA via the transcriptional integrator p300. Cancer Res 1998;58(20):4531-4536.
56. Sheppard KA, Phelps KM, Williams AJ, Thanos D, Glass CK, Rosenfeld MG, Gerritsen ME, Collins T. Nuclear integration of glucocorticoid receptor and nuclear factor-kappaB signaling by CREB-binding protein and steroid receptor coactivator-1. J Biol Chem 1998;273(45):29291-29294.
57. Ariumi Y, Kaida A, Lin JY, Hirota M, Masui O, Yamaoka S, Taya Y, Shimotohno K. HTLV-1 tax oncoprotein represses the p53-mediated trans-activation function through coactivator CBP sequestration. Oncogene 2000;19(12):1491-1499.
58. Harnish DC, Scicchitano MS, Adelman SJ, Lyttle CR, Karathanasis SK. The role of CBP in estrogen receptor cross talk with nuclear factor-kappaB in HepG2 cells. Endocrinology 2000;141(9):3403-3411.
59. Okino ST, Pendurthi UR, Tukey RH. Phorbol esters inhibit the dioxin receptor-mediated transcriptional activation of the mouse Cyp1a-1 and Cyp1a-2 genes by 2,3,7,8-tetrachlorodibenzo-p-dioxin. J Biol Chem 1992;267(10):6991-6998.
60. Carrier F, Owens RA, Nebert DW, Puga A. Dioxin-dependent activation of murine Cyp1a-1 gene transcription requires protein kinase C-dependent phosphorylation. Mol Cell Biol 1992;12(4):1856-1863.
61. Berghard A, Gradin K, Pongratz I, Whitelaw M, Poellinger L. Cross-coupling of signal transduction pathways: The dioxin receptor mediates induction of cytochrome P-45OIA1 expression via a protein kinase C-dependent mechanism. Mol Cell Biol 1993;13(1):677-689.
62. Moore M, Narasimhan TR, Steinberg MA, Wang X, Safe S. Potentiation of CYP1A1 gene expression in MCF-7 human breast cancer cells cotreated with 2,3,7,8-tetrachlorodibenzo-p-dioxin and 12-O-tetradecanoylphorbol-13-acetate. Arch Biochem Biophys 1993;305(2):483-488.
63. Chen YH, Tukey RH. Protein kinase C modulates regulation of the CYP1A1 gene by the aryl hydrocarbon receptor. J Biol Chem 1996;271(42):26261-26266.
64. Long WP, Pray-Grant M, Tsai JC, Perdew GH. Protein kinase C activity is required for aryl hydrocarbon receptor pathway-mediated signal transduction. Mol Pharmacol 1998;53(4):691-700.
65. Schafer MW, Madhukar BV, Swanson HI, Tullis K, Denison MS. Protein kinase C is not involved in Ah receptor transformation and DNA binding. Arch Biochem Biophys 1993;307(2):267-271.
66. Long WP, Perdew GH. Lack of an absolute requirement for the native aryl hydrocarbon receptor (AhR) and AhR nuclear translocator transactivation domains in protein kinase C-mediated modulation of the AhR pathway. Arch Biochem Biophys 1999;371(2):246-259.
67. Ou X, Weber TJ, Chapkin RS, Ramos KS. Interference with protein kinase C-related signal transduction in vascular smooth muscle cells by benzo[a]pyrene. Arch Biochem Biophys 1995;318(1):122-130.
68. Kodavanti PR, Ward TR. Interactive effects of environmentally relevant polychlorinated biphenyls and dioxins on [3H]phorbol ester binding in rat cerebellar granule cells. Environ Health Perspect 1998;106(8):479-486.
69. Park S, Henry EC, Gasiewicz TA. Regulation of DNA binding activity of the ligand-activated aryl hydrocarbon receptor by tyrosine phosphorylation. Arch Biochem Biophys 2000;381(2):302-312.
70. Enan E, Matsumura F. Identification of c-Src as the integral component of the cytosolic Ah receptor complex, transducing the signal of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) through the protein phosphorylation pathway. Biochem Pharmacol 1996;52(10):1599-1612.
71. Blankenship A, Matsumura F. 2,3,7,8-Tetrachlorodibenzo-p-dioxin-induced activation of a protein tyrosine kinase, pp60src, in murine hepatic cytosol using a cell-free system. Mol Pharmacol 1997;52(4):667-675.
72. Ashida H, Nagy S, Matsumura F. 2,3,7,8-Tetrachlorodibenzo-p-dioxin (TCDD)-induced changes in activities of nuclear protein kinases and phosphatases affecting DNA binding activity of c-Myc and AP-1 in the livers of guinea pigs. Biochem Pharmacol 2000;59(7):741-751.
73. Dunlap DY, Ikeda I, Nagashima H, Vogel CF, Matsumura F. Effects of src-deficiency on the expression of in vivo toxicity of TCDD in a strain of c-src knockout mice procured through six generations of backcrossings to C57BL/6 mice. Toxicology 2002;172(2):125-141.
74. Dull AB, Carlson DB, Petrulis JR, Perdew GH. Characterization of the phosphorylation status of the hepatitus B virus X-associated protein 2 (XAP2). Arch Biochem Biophys 406(2):209-221.
75. Kazlauskas A, Sundstrom S, Poellinger L, Pongratz I. The hsp90 chaperone complex regulates intracellular localization of the dioxin receptor. Mol Cell Biol 2001;21(7):2594-2607.
76. Cox MB, Miller CA III. The p23 co-chaperone facilitates dioxin receptor signaling in a yeast model system. Toxicol Lett 2002;129(1-2):13-21.
77. Seidel SD, Winters GM, Rogers WJ, Ziccardi MH, Li V, Keser B, Denison MS. Activation of the Ah receptor signaling pathway by prostaglandins. J Biochem Mol Toxicol 2001;15(4):187-196.
78. Klinge CM, Jernigan SC, Risinger KE, Lee JE, Tyulmenkov VV, Falkner KC, Prough RA. Short heterodimer partner (SHP) orphan nuclear receptor inhibits the transcriptional activity of aryl hydrocarbon receptor (AHR)/AHR nuclear translocator (ARNT). Arch Biochem Biophys 2001;390(1):64-70.
79. Perdew GH. Chemical cross-linking of the cytosolic and nuclear forms of the Ah receptor in hepatoma cell line 1c1c7. Biochem Biophys Res Commun 1992;182(1):55-62.
80. Meyer BK, Pray-Grant MG, Vande Heuvel JP, Perdew GH. 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 1998;18(2):978-988.
81. Ma Q, Whitlock JP Jr. A novel cytoplasmic protein that interacts with the Ah receptor, contains tetratricopeptide repeat motifs, and augments the transcriptional response to 2,3,7,8-tetrachlorodibenzo-p-dioxin. J Biol Chem 1997;272(14):8878-8884.
82. Carver LA, Bradfield CA. Ligand-dependent interaction of the aryl hydrocarbon receptor with a novel immunophilin homolog in vivo. J Biol Chem 1997;272(17):11452-11456.