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J Biol Chem, Vol. 275, Issue 4, 2943-2950, January 28, 2000

Aromatic Hydrocarbon Receptor Interaction with the Retinoblastoma Protein Potentiates Repression of E2F-dependent Transcription and Cell Cycle Arrest*

Alvaro PugaDagger §, Sonya J. BarnesDagger , Timothy P. DaltonDagger , Ching-yi ChangDagger par , Erik S. Knudsen**Dagger Dagger , and Michael A. MaierDagger §§

From the Dagger  Center for Environmental Genetics and Department of Environmental Health, ** Department of Cell Biology, Neurobiology and Anatomy, University of Cincinnati Medical Center, P.O. Box 670056, Cincinnati, Ohio 45267-0056

Polyhalogenated aromatic hydrocarbons, of which 2,3,7,8-tetrachloro-p-dioxin (TCDD) is the prototype compound, elicit a variety of toxic, teratogenic, and carcinogenic responses in exposed animals and in humans. In cultured cells, TCDD shows marked effects on the regulation of cell cycle progression, including thymocyte apoptosis, induction of keratinocyte proliferation and terminal differentiation, and inhibition of estrogen-dependent proliferation in breast cancer cells. The presence of an LXCXE domain in the dioxin aromatic hydrocarbon receptor (AHR), suggested that the effects of TCDD on cell cycle regulation might be mediated by protein-protein interactions between AHR and the retinoblastoma protein (RB). Using the yeast two-hybrid system, AHR and RB were in fact shown to bind to each other. In vitro pull-down experiments with truncated AHR peptides indicated that at least two separate AHR domains form independent complexes with hypophosphorylated RB. Coimmunoprecipitation of whole cell lysates from human breast carcinoma MCF-7 cells, which express both proteins endogenously, revealed that AHR associates with RB in vivo only after receptor transformation and nuclear translocation. However, the AHR nuclear translocator and transcriptional heterodimerization partner, is not required for (nor is it a part of) the AHR·RB complexes detected in vitro. Ectopic expression of AHR and RB in human osteosarcoma SAOS-2 cells, which lack endogenous expression of both proteins, showed that AHR synergizes with RB to repress E2F-dependent transcription and to induce cell cycle arrest. Furthermore, AHR partly blocked T-antigen-mediated reversal of RB-dependent transcriptional repression. These results uncover a potential function for the AHR in cell cycle regulation and suggest that this function may be that of serving as an environmental sensor that signals cell cycle arrest when cells are exposed to certain environmental toxicants.

* The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

This work was supported by NIEHS, National Institutes of Health (NIH), Grants ES06273 and P30 ES06096.

§ To whom correspondence should be addressed. Tel.: 513-558-0916; Fax: 513-558-0925; E-mail: Alvaro.Puga@UC.EDU.

Supported by a NIEHS, NIH, mutagenesis and carcinogenesis training grant.

par Recipient of a predoctoral fellowship from the Pharmaceutical Research and Manufacturers of America Foundation. Present address: Dept. of Pharmacology, Duke University Medical Center, Durham, NC.

Dagger Dagger A Kimmel Scholar.

§§ Supported by a United States Environmental Protection Agency STAR predoctoral fellowship grant.

Copyright © 2000 by The American Society for Biochemistry and Molecular Biology, Inc.
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