Quantifying effects of ligands on androgen receptor nuclear translocation, intranuclear dynamics, and solubility

J Cell Biochem. 2006 Jul 1;98(4):770-88. doi: 10.1002/jcb.20593.

Abstract

Using manual and automated high throughput microscopy (HTM), ligand-dependent trafficking of green fluorescent protein-androgen receptor (GFP-AR) was analyzed in fixed and living cells to determine its spatial distribution, solubility, mobility, and co-activator interactions. Within minutes, addition of the agonist R1881 resulted translocation of GFP-AR from the cytoplasm to the nucleus, where it displayed a hyperspeckled pattern and extraction resistance in low expressing cells. AR antagonists (Casodex, hydroxyflutamide) also caused nuclear translocation, however, the antagonist-bound GFP-AR had a more diffuse nuclear distribution, distinct from the agonist-bound GFP-AR, and was completely soluble; overexpressed GFP-AR in treated cells was extraction resistant, independent of ligand type. To more dramatically show the different effects of ligand on AR distribution, we utilized an AR with a mutation in the DNA binding domain (ARC619Y) that forms distinct foci upon exposure to agonists but retains a diffuse nuclear distribution in the presence of antagonists. Live-cell imaging of this mutant demonstrated that cytoplasmic foci formation occurs immediately upon agonist but not antagonist addition. Fluorescence recovery after photobleaching (FRAP) revealed that agonist-bound GFP-AR exhibited reduced mobility relative to unliganded or antagonist-bound GFP-AR. Importantly, agonist-bound GFP-AR mobility was strongly affected by protein expression levels in transiently transfected cells, and displayed reduced mobility even in slightly overexpressing cells. Cyan fluorescent protein-AR (CFP-AR) and yellow fluorescent protein-CREB binding protein (YFP-CBP) in the presence of agonists and antagonists were used to demonstrate that CFP-AR specifically co-localizes with YFP-CBP in an agonist dependent manner. Dual FRAP experiments demonstrated that CBP mobility mirrored AR mobility only in the presence of agonist. HTM enabled simultaneous studies of the sub-cellular distribution of GFP-AR and ARC619Y in response to a range of concentrations of agonists and antagonists (ranging from 10(-12) to 10(-5)) in thousands of cells. These results further support the notion that ligand specific interactions rapidly affect receptor and co-factor organization, solubility, and molecular dynamics, and each can be aberrantly affected by mutation and overexpression.

Publication types

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

MeSH terms

  • Active Transport, Cell Nucleus / drug effects
  • Active Transport, Cell Nucleus / physiology
  • Androgen Antagonists / pharmacology*
  • Androgen Receptor Antagonists*
  • Androgens*
  • Anilides / pharmacology*
  • Cell Nucleus / genetics
  • Cell Nucleus / metabolism*
  • Dose-Response Relationship, Drug
  • HeLa Cells
  • Humans
  • Ligands
  • Metribolone / pharmacology*
  • Microscopy, Fluorescence
  • Nitriles
  • Protein Structure, Tertiary / genetics
  • Receptors, Androgen / genetics
  • Receptors, Androgen / metabolism
  • Tosyl Compounds

Substances

  • AR protein, human
  • Androgen Antagonists
  • Androgen Receptor Antagonists
  • Androgens
  • Anilides
  • Ligands
  • Nitriles
  • Receptors, Androgen
  • Tosyl Compounds
  • Metribolone
  • bicalutamide