Ligand-dependent inhibition of β-catenin/TCF signaling by androgen receptor

Chesire, Dennis R; Isaacs, William B

doi:10.1038/sj.onc.1206049

Cited by 151Wnt/β-catenin signaling in development and cancerProstate Cancer Treatment and ResearchSignaling Pathways in Disease

Ligand-dependent inhibition of β-catenin/TCF signaling by androgen receptor

Chesire, Dennis R, Isaacs, William B·2002·Oncogene

DOI 10.1038/sj.onc.1206049

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Abstract

Beta-catenin signaling may contribute to prostate cancer (CaP) progression. Although beta-catenin is known to upregulate T cell factor (TCF) target gene expression in CaP cells, recent evidence demonstrates its capacity to enhance ligand-dependent androgen receptor (AR) function. Thus, we wished to further understand the interaction between these two pathways. We find in both CaP cells (CWR22-Rv1, LAPC-4, DU145) and non-CaP cells (HEK-293, TSU, SW480, HCT-116) that beta-catenin/TCF-related transcription (CRT), as measured by activation of a synthetic promoter and that of cyclin D1, is inhibited by androgen treatment. This inhibition is AR-dependent, as it only occurs in cells expressing AR endogenously or transiently, and is abrogated by AR antagonists. Additional analyses convey that the ligand-dependent nature of CRT suppression depends on transactivation-competent AR in the nucleus, but not on indirect effects stemming from AR target gene expression. Given the recent work identifying an AR/beta-catenin interaction, and from our finding that liganded AR does not prompt gross changes in the constitutive nuclear localization of TCF4 or mutant beta-catenin, we hypothesized that transcription factor (i.e. AR and TCF) competition for beta-catenin recruitment may explain, in part, androgen-induced suppression of CRT. To address this idea, we expressed an AR mutant lacking its DNA-binding domain (DBD). This receptor could not orchestrate ligand-dependent CRT repression, thereby providing support for those recent data implicating the AR DBD/LBD as necessary for beta-catenin interaction. Further supporting this hypothesis, TCF/LEF over-expression counteracts androgen-induced suppression of CRT, and requires beta-catenin binding activity to do so. Interestingly, TCF4 over-expression potently antagonizes AR function; however, this inhibition may occur independently of beta-catenin/TCF4 interaction. These results from TCF4 over-expression analyses, taken together, provide further evidence that AR-mediated suppression of CRT is a consequence of limiting amounts of beta-catenin, and not AR target gene expression. Our analyses point to a reciprocal balance between AR and CRT function that may shape critical processes during normal prostate development and tumor progression.

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AR competes with TCF4 for β-catenin binding.
“Since AR competes with TCF4 for β-catenin binding [21], the presence of FKBP52 may be enough to shift β-catenin to favor AR over TCF4.”
From The FKBP52 Cochaperone Acts in Synergy with β-Catenin to Potentiate Androgen Receptor Signaling (2015) · cites this paper as [21]
Ligand-bound AR decreases the transcriptional activity of TCF4 in prostate cancer, colon cancer, and neurons.
“Indeed, ligand-bound AR decreases the transcriptional activity of TCF4 in prostate cancer, colon cancer [21], and neurons [16].”
From The FKBP52 Cochaperone Acts in Synergy with β-Catenin to Potentiate Androgen Receptor Signaling (2015) · cites this paper as [21]

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Untitled work
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A Novel Role for Wnt/Ca2+ Signaling in Actin Cytoskeleton Remodeling and Cell Motility in Prostate Cancer
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Analysis of Wnt Gene Expression in Prostate Cancer
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Membrane Androgen Receptors Unrelated to Nuclear Steroid Receptors
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Keratinocyte Growth Inhibition through the Modification of Wnt Signaling by Androgen in Balding Dermal Papilla Cells
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The Modulatable Stem Cell Niche: Tissue Interactions during Hair and Feather Follicle Regeneration
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Synergistic Effects of Coactivators GRIP1 and β-Catenin on Gene Activation
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Isotretinoin and FoxO1
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Androgen receptor (AR) suppresses normal human prostate epithelial cell proliferation via AR/β‐catenin/TCF‐4 complex inhibition of c‐MYC transcription
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A Mouse Model of Androgenetic Alopecia
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Treatment of Androgenetic Alopecia Using PRP to Target Dysregulated Mechanisms and Pathways
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Androgen Regulation of 5α-Reductase Isoenzymes in Prostate Cancer: Implications for Prostate Cancer Prevention
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The Glucocorticoid Receptor Represses Cyclin D1 by Targeting the Tcf-β-Catenin Complex
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Sex Hormones and Colorectal Cancer: What Have We Learned So Far?
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β-Catenin Is Involved in Insulin-Like Growth Factor 1-Mediated Transactivation of the Androgen Receptor
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Constitutive β-Catenin Activation Induces Male-Specific Tumorigenesis in the Bladder Urothelium
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Stromally Expressed c-Jun Regulates Proliferation of Prostate Epithelial Cells
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Decursin Suppresses Human Androgen-Independent PC3 Prostate Cancer Cell Proliferation by Promoting the Degradation of β-Catenin
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Secreted frizzled‐related protein 4 inhibits proliferation and metastatic potential in prostate cancer
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TNFα-Mediated Loss of β-Catenin/E-Cadherin Association and Subsequent Increase in Cell Migration Is Partially Restored by NKX3.1 Expression in Prostate Cells
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Integrin signaling links protein kinase Cɛ to the protein kinase B/Akt survival pathway in recurrent prostate cancer cells
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ACTR/AIB1/SRC-3 and androgen receptor control prostate cancer cell proliferation and tumor growth through direct control of cell cycle genes
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P-Glycoprotein, Breast Cancer Resistance Protein, Organic Anion Transporter 3, and Transporting Peptide 1a4 during Blood–Brain Barrier Maturation: Involvement of Wnt/β-Catenin and Endothelin-1 Signaling
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Activation of β-Catenin Cooperates with Loss of Pten to Drive AR-Independent Castration-Resistant Prostate Cancer
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Positive Inter-Regulation between β-Catenin/T Cell Factor-4 Signaling and Endothelin-1 Signaling Potentiates Proliferation and Survival of Prostate Cancer Cells
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Direct interaction of β‐catenin with nuclear ESM1 supports stemness of metastatic prostate cancer
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Androgen Receptor Expression and Bicalutamide Antagonize Androgen Receptor Inhibit β-Catenin Transcription Complex in Estrogen Receptor-Negative Breast Cancer
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Authors: Chesire, D. R., & Isaacs, W. B.
Affiliations: Johns Hopkins University (US)
Corresponding author: Isaacs, William B
ORCID: Isaacs, William B
Venue: Oncogene
Publisher: Springer Science and Business Media LLC
Published: 2002-12-04
Volume: 21
Issue: 55
Pages: 8453-8469
ISSN: 0950-9232 (ISSN-L)
1476-5594
DOI: 10.1038/sj.onc.1206049
OpenAlex: W1970833195
Cited by: 151
References: 93
Citations by year: 2026: 3 · 2025: 1 · 2024: 2 · 2023: 3 · 2022: 3 · 2021: 8 · 2020: 4 · 2019: 7 · 2018: 2 · 2017: 9 · 2016: 5 · 2015: 5 · 2014: 8 · 2013: 9 · 2012: 10
FWCI: 3.36
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Oncogene (publishedVersion)
PubMed (publishedVersion)
Funders: National Cancer Institute (CA58236, P50CA058236)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Wnt/β-catenin signaling in development and cancer
Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Prostate Cancer Treatment and Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Signaling Pathways in Disease
Keywords: androgen receptor, β-catenin, TCF/LEF, Wnt signaling, prostate cancer, ligand-dependent transcription, transcription factor competition, TCF4, cyclin D1, DNA-binding domain, transcriptional repression
MeSH terms: Animals, Cell Line, Cell Nucleus, Cytoskeletal Proteins, DNA-Binding Proteins, Humans, Ligands, Male, Prostatic Neoplasms, Receptors, Androgen, Transcription Factors, Transcription, Genetic, Tumor Cells, Cultured, Signal Transduction, Trans-Activators, beta Catenin, TCF Transcription Factors, Transcription Factor 7-Like 2 Protein

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Ligand-dependent inhibition of β-catenin/TCF signaling by androgen receptor

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