Evidence supporting the hypothesis that one of the main functions of the aryl hydrocarbon receptor is mediation of cell stress responses
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Fumio Matsumura
and Christoph F.A. Vogel
Abstract
We have previously proposed that one of the major consequences of activation of the aryl hydrocarbon receptor (AhR) by 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) could be elicitation of ‘cell stress response’ reactions [Matsumura, Biochem. Pharmacol. 66 (2003), 527–540]. This hypothesis was based mainly on the similarity between the toxic symptoms, particularly those related to the wasting syndrome, and those induced by bacterial endotoxins, namely lipopolysaccharides (LPS) in vivo, as well as the biochemical and molecular consequences of their toxic actions in vitro. Since the basic action mechanism of LPS as an inducer of cell stress responses (CSR) is known to some extent, including knowledge of their specific receptors (i.e., toll-like receptors) and their signaling process through the inflammatory response messengers, the above comparison offered a good point of reference to this subject. Furthermore, the process of constructing this hypothesis itself has provided us with a good opportunity to give a fresh view on the toxic action patterns of TCDD.
References
Arun, C.P. (2004). Fight or flight, forbearance and fortitude: the spectrum of actions of the catecholamines and their cousins. Ann. N.Y. Acad. Sci.1018, 137–140.10.1196/annals.1296.016Search in Google Scholar
Bock, K.W. and Kohle, C. (2005). Ah receptor- and TCDD-mediated liver tumor promotion: clonal selection and expansion of cells evading growth arrest and apoptosis. Biochem. Pharmacol.69, 1403–1408.10.1016/j.bcp.2005.02.004Search in Google Scholar
Bouloumie, A., Curat, C.A., Sengenes, C., Lolmede, K., Miranville, A., and Busse, R. (2005). Role of macrophage tissue infiltration in metabolic diseases. Curr. Opin. Clin. Nutr. Metab. Care8, 347–354.10.1097/01.mco.0000172571.41149.52Search in Google Scholar
Fujiwara, N. and Kobayashi, K. (2005). Macrophages in inflammation. Curr. Drug Targets Inflamm. Allergy4, 281–286.10.2174/1568010054022024Search in Google Scholar
Gonzalez, F.J. and Fernandez-Salguero, P. (1998). The aryl hydrocarbon receptor: studies using the AHR-null mice. Drug Metab. Dispos.26, 1194–1198.Search in Google Scholar
Haimovitz-Friedman, A. (1998). Radiation-induced signal transduction and stress response. Radiat. Res.150, 102–108.10.2307/3579812Search in Google Scholar
Hayashi, S., Okabe-Kado, J., Honma, Y., and Kawajiri, K. (1995). Expression of Ah receptor (TCDD receptor) during human monocytic differentiation. Carcinogenesis16, 1403–1409.10.1093/carcin/16.6.1403Search in Google Scholar
Kher, N., and Marsh, J.D. (2004). Pathobiology of atherosclerosis – a brief review. Semin. Thromb. Hemost.30, 665–672.10.1055/s-2004-861509Search in Google Scholar
Kolb, H., Burkart, V., Appels, B., Hanenberg, H., Kantwerk-Funke, G., Kiesel, U., Funda, J., Schraermeyer, U., and Kolb-Bachofen, V. (1990). Essential contribution of macrophages to islet cell destruction in vivo and in vitro. J. Autoimmun.1, 117–120.10.1016/S0896-8411(09)90020-8Search in Google Scholar
Komarova, E.A. and Gudkov, A.V. (1998). Could p53 be a target for therapeutic suppression? Semin. Cancer Biol.8, 389–400.10.1006/scbi.1998.0101Search in Google Scholar PubMed
Komura, K., Hayashi, S., Makino, I., et al. (2001). Aryl hydrocarbon receptor/dioxin receptor in human monocytes and macrophages. Mol. Cell. Biochem.226, 107–118.10.1023/A:1012762519424Search in Google Scholar
Kultz, D. (2005). Molecular and evolutionary basis of the cellular stress response. Annu. Rev. Physiol.67, 225–257.10.1146/annurev.physiol.67.040403.103635Search in Google Scholar
Kurl, R.N., Abraham, M., and Olnes, M.J. (1993). Early effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) on rat thymocytes in vitro. Toxicology77, 103–114.10.1016/0300-483X(93)90141-ESearch in Google Scholar
Lin, E.Y. and Pollard, J.W. (2004). Macrophages: modulators of breast cancer progression. Novartis Found. Symp.256, 158–168.10.1002/0470856734.ch12Search in Google Scholar
Lucia, M.S. and Torkko, K.C. (2004). Inflammation as a target for prostate cancer chemoprevention: pathological and laboratory rationale. J. Urol.171, 30–34.Search in Google Scholar
Matsumura, F. (1994). How important is the protein phosphorylation pathway in the toxic expression of dioxin-type chemicals? Biochem. Pharmacol.48, 215–224.Search in Google Scholar
Matsumura, F. (2003). On the significance of the role of cellular stress response reactions in the toxic actions of dioxin. Biochem. Pharmacol.66, 527–540.10.1016/S0006-2952(03)00157-6Search in Google Scholar
Moseley, P. (2000). Stress proteins and the immune response. Immunopharmacology48, 299–302.10.1016/S0162-3109(00)00227-7Search in Google Scholar
Nebert, D.W., Roe, A.L., Dieter, M.Z., Solis, W.A., Yang, Y., and Dalton, T.P. (2000). Role of the aromatic hydrocarbon receptor and [Ah] gene battery in the oxidative stress response, cell cycle control, and apoptosis. Biochem. Pharmacol.59, 65–85.10.1016/S0006-2952(99)00310-XSearch in Google Scholar
Ottaviani, E. and Franceschi, C. (1998). A new theory on the common evolutionary origin of natural immunity, inflammation and stress response: the invertebrate phagocytic immunocyte as an eye-witness. Domest. Anim. Endocrinol.15, 291–296.10.1016/S0739-7240(98)00021-6Search in Google Scholar
Pande, K., Moran, S.M., and Bradfield, C.A. (2005). Aspects of dioxin toxicity are mediated by interleukin 1-like cytokines. Mol. Pharmacol.67, 1393–1398.10.1124/mol.105.010983Search in Google Scholar
Park, S. and Matsumura, F. (2006). Characterization of anti-apoptotic action of TCDD as a defensive cellular stress response reaction against the cell damaging action of ultra-violet irradiation in an immortalized normal human mammary epithelial cell line, MCF10A. Toxicology217, 139–146.10.1016/j.tox.2005.09.002Search in Google Scholar
Schuurman, H.J., van Lovered, H., Rozing, J., and Vox, J.G. (1992). Chemicals trophic for the thymus: risk for immunodeficiency and autoimmunity. Int. J. Immunopharmacol.14, 369–375.10.1016/0192-0561(92)90166-ISearch in Google Scholar
Silverstone, A.E., Frazier Jr., D.R., Fiore, N.C., Soults, J.A., and Gasiewicz, T.A. (1994). Dexamethasone, β-estradiol, and 2,3,7,8-tetrachlorodizenzo-p-dioxin elicit thymic atrophy through different cellular targets. Toxicol. Appl. Pharmacol.126, 248–259.10.1006/taap.1994.1114Search in Google Scholar
Speer, C.P. (2001). New insights into the pathogenesis of pulmonary inflammation in preterm infants. Biol. Neonate79, 205–209.Search in Google Scholar
Thurmond, T.S., Silverstone, A.E., Baggs, R.B., Quimby, F.W., Staples, J.E., and Gasiewicz, T.A. (1999). A chimeric aryl hydrocarbon receptor knockout mouse model indicates that aryl hydrocarbon receptor activation in hematopoietic cells contributes to the hepatic lesions induced by 2,3,7,8-tetrachlorodibenzo-p-dioxin. Toxicol. Appl. Pharmacol.58, 33–40.10.1006/taap.1999.8681Search in Google Scholar
Vogel, C., Boerboom, A.M., Baechle, C., El-Bahay, C., Kahl, R., Degen, G.H., and Abel, J. (2000). Regulation of prostaglandin endoperoxide H synthase-2 induction by dioxin in rat hepatocytes: possible c-Src-mediated pathway. Carcinogenesis21, 2267–2274.10.1093/carcin/21.12.2267Search in Google Scholar
Vogel, C.F., Sciullo, E., and Matsumura, F. (2004a). Activation of inflammatory mediators and potential role of Ah-receptor ligands in foam cell formation. Cardiovasc. Toxicol.4, 363–373.10.1385/CT:4:4:363Search in Google Scholar
Vogel, C.F., Sciullo, E., Park, S., Liedtke, C., Trautwein, C., and Matsumura, F. (2004b). Dioxin increases C/EBPβ transcription by activating cAMP/protein kinase A. J. Biol. Chem.279, 8886–8894.10.1074/jbc.M310190200Search in Google Scholar PubMed
Vogel, C.F., Sciullo, E., Wong, P., Kuzmicky, P., Kado, N., and Matsumura, F. (2005). Induction of proinflammatory cytokines and C-reactive protein in human macrophage cell line U937 exposed to air pollution particulates. Environ. Health Perspect.113, 1536–1541.10.1289/ehp.8094Search in Google Scholar PubMed PubMed Central
©2006 by Walter de Gruyter Berlin New York
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Articles in the same Issue
- The arylhydrocarbon receptor: more than a tox story
- The aryl hydrocarbon receptor and light
- The impact of aryl hydrocarbon receptor signaling on matrix metabolism: implications for development and disease
- A role for the aryl hydrocarbon receptor in mammary gland tumorigenesis
- Evidence supporting the hypothesis that one of the main functions of the aryl hydrocarbon receptor is mediation of cell stress responses
- The arylhydrocarbon receptor repressor (AhRR): structure, expression, and function
- Impact of the arylhydrocarbon receptor on eugenol- and isoeugenol-induced cell cycle arrest in human immortalized keratinocytes (HaCaT)
- Aryl hydrocarbon receptor agonists directly activate estrogen receptor α in MCF-7 breast cancer cells
- Identifying target genes of the aryl hydrocarbon receptor nuclear translocator (Arnt) using DNA microarray analysis
- Transcriptional signatures of immune cells in aryl hydrocarbon receptor (AHR)-proficient and AHR-deficient mice
- 14-3-3 proteins in membrane protein transport
- The K+ channel gene, Kcnb1: genomic structure and characterization of its 5′-regulatory region as part of an overlapping gene group
- Structure-based specificity mapping of secreted aspartic proteases of Candida parapsilosis, Candida albicans, and Candida tropicalis using peptidomimetic inhibitors and homology modeling
- The solution structure of the membrane-proximal cytokine receptor domain of the human interleukin-6 receptor
- Sequence determination of lychnin, a type 1 ribosome-inactivating protein from Lychnis chalcedonica seeds
- Paired helical filaments contain small amounts of cholesterol, phosphatidylcholine and sphingolipids
- Induction of intracellular signalling in human endothelial cells by the hyaluronan-binding protease involves two distinct pathways
- A novel proteolytically processed CDP/Cux isoform of 90 kDa is generated by cathepsin L
- Degradation of apolipoprotein B-100 by lysosomal cysteine cathepsins
- Identification of trypsin I as a candidate for influenza A virus and Sendai virus envelope glycoprotein processing protease in rat brain