Non-Cell-Autonomous Regulation of Prostate Epithelial Homeostasis by Androgen Receptor

Mol Cell. 2016 Sep 15;63(6):976-89. doi: 10.1016/j.molcel.2016.07.025. Epub 2016 Sep 1.

Abstract

Prostate inflammation has been suggested as an etiology for benign prostatic hyperplasia (BPH). We show that decreased expression of the androgen receptor (AR) in luminal cells of human BPH specimens correlates with a higher degree of regional prostatic inflammation. However, the cause-and-effect relationship between the two events remains unclear. We investigated specifically whether attenuating AR activity in prostate luminal cells induces inflammation. Disrupting luminal cell AR signaling in mouse models promotes cytokine production cell-autonomously, impairs epithelial barrier function, and induces immune cell infiltration, which further augments local production of cytokines and chemokines including Il-1 and Ccl2. This inflammatory microenvironment promotes AR-independent prostatic epithelial proliferation, which can be abolished by ablating IL-1 signaling or depleting its major cellular source, the macrophages. This study demonstrates that disrupting luminal AR signaling promotes prostate inflammation, which may serve as a mechanism for resistance to androgen-targeted therapy for prostate-related diseases.

Keywords: androgen receptor; benign prostatic hyperplasia; epithelial homeostasis; inflammation; interleukin-1; macrophage; microenvironment.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Cell Proliferation
  • Chemokine CCL2 / genetics
  • Chemokine CCL2 / immunology
  • Chemokine CXCL10 / genetics
  • Chemokine CXCL10 / immunology
  • Epithelial Cells / immunology
  • Epithelial Cells / metabolism*
  • Epithelial Cells / pathology
  • Gene Expression Regulation
  • Homeostasis / genetics*
  • Homeostasis / immunology
  • Humans
  • Inflammation
  • Interleukin-1alpha / genetics
  • Interleukin-1alpha / immunology
  • Interleukin-1beta / genetics
  • Interleukin-1beta / immunology
  • Leukocyte Common Antigens / genetics
  • Leukocyte Common Antigens / immunology
  • Macrophages / immunology
  • Macrophages / metabolism*
  • Macrophages / pathology
  • Male
  • Mice
  • Neutrophil Infiltration
  • Prostate / immunology
  • Prostate / metabolism*
  • Prostate / pathology
  • Prostatic Hyperplasia / genetics*
  • Prostatic Hyperplasia / immunology
  • Prostatic Hyperplasia / metabolism
  • Prostatic Hyperplasia / pathology
  • Receptors, Androgen / genetics*
  • Receptors, Androgen / immunology
  • Signal Transduction
  • Stromal Cells / immunology
  • Stromal Cells / metabolism
  • Stromal Cells / pathology

Substances

  • AR protein, human
  • CCL2 protein, human
  • CXCL10 protein, human
  • Chemokine CCL2
  • Chemokine CXCL10
  • IL1A protein, human
  • IL1B protein, human
  • Interleukin-1alpha
  • Interleukin-1beta
  • Receptors, Androgen
  • Leukocyte Common Antigens
  • PTPRC protein, human