Androgen suppresses proliferation of castration-resistant LNCaP 104-R2 prostate cancer cells through androgen receptor, Skp2, and c-Myc

Cancer Sci. 2011 Nov;102(11):2022-8. doi: 10.1111/j.1349-7006.2011.02043.x. Epub 2011 Aug 18.

Abstract

Androgen ablation therapy is the primary treatment for metastatic prostate cancer. However, this therapy is associated with several undesired side-effects, including increased risk of cardiovascular diseases. To study if termination of long-term androgen ablation and restoration of testosterone levels could suppress the growth of relapsed hormone-refractory prostate tumors, we implanted testosterone pellets in castrated nude mice carrying androgen receptor (AR)-positive LNCaP 104-R2 cells, which relapsed from androgen-dependent LNCaP 104-S cells after long-term androgen deprivation. 104-R2 tumor xenografts regressed after testosterone pellets were implanted. Of 33 tumors, 24 adapted to elevation of testosterone level and relapsed as androgen-insensitive tumors. Relapsed tumors (R2Ad) expressed less AR and prostate-specific antigen. We then studied the molecular mechanism underlying the androgenic regulation of prostate cancer cell proliferation. Androgen suppresses proliferation of 104-R2 by inducing G(1) cell cycle arrest through reduction of S-phase kinase-associated protein 2 (Skp2) and c-Myc, and induction of p27(Kip1). 104-R2 cells adapted to androgen treatment and the adapted cells, R2Ad, were androgen-insensitive cells with a slower growth rate and low protein level of AR, high levels of c-Myc and Skp2, and low levels of p27(Kip1). Nuclear AR and prostate-specific antigen expression is present in 104-R2 cells but not R2Ad cells when androgen is absent. Overexpression of AR in R2Ad cells regenerated an androgen-repressed phenotype; knockdown of AR in 104-R2 cells generated an androgen-insensitive phenotype. Overexpression of Skp2 and c-Myc in 104-R2 cells blocked the growth inhibition caused by androgens. We concluded that androgens cause growth inhibition in LNCaP 104-R2 prostate cancer cells through AR, Skp2, and c-Myc.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenocarcinoma / metabolism
  • Adenocarcinoma / pathology*
  • Adenocarcinoma / secondary
  • Androgen Antagonists / pharmacology
  • Androgen Antagonists / therapeutic use
  • Anilides / pharmacology
  • Anilides / therapeutic use
  • Animals
  • Cell Cycle / drug effects
  • Cell Division
  • Cell Line, Tumor / drug effects
  • Cell Line, Tumor / metabolism
  • Cell Line, Tumor / pathology
  • Cyclin-Dependent Kinase Inhibitor p27 / biosynthesis
  • Cyclin-Dependent Kinase Inhibitor p27 / genetics
  • Cyclin-Dependent Kinase Inhibitor p27 / physiology
  • Drug Implants
  • Gene Expression Regulation, Neoplastic / drug effects*
  • Humans
  • Lymphatic Metastasis
  • Male
  • Metribolone / pharmacology
  • Mice
  • Mice, Inbred BALB C
  • Mice, Nude
  • Neoplasm Proteins / biosynthesis
  • Neoplasm Proteins / genetics
  • Neoplasm Proteins / physiology*
  • Nitriles / pharmacology
  • Nitriles / therapeutic use
  • Orchiectomy
  • Prostatic Neoplasms / metabolism
  • Prostatic Neoplasms / pathology*
  • Proto-Oncogene Proteins c-myc / biosynthesis
  • Proto-Oncogene Proteins c-myc / genetics
  • Proto-Oncogene Proteins c-myc / physiology*
  • Receptors, Androgen
  • S-Phase Kinase-Associated Proteins / biosynthesis
  • S-Phase Kinase-Associated Proteins / genetics
  • S-Phase Kinase-Associated Proteins / physiology*
  • Testosterone / administration & dosage
  • Testosterone / pharmacology
  • Tosyl Compounds / pharmacology
  • Tosyl Compounds / therapeutic use
  • Xenograft Model Antitumor Assays

Substances

  • Androgen Antagonists
  • Anilides
  • Drug Implants
  • MYC protein, human
  • Neoplasm Proteins
  • Nitriles
  • Proto-Oncogene Proteins c-myc
  • Receptors, Androgen
  • S-Phase Kinase-Associated Proteins
  • Tosyl Compounds
  • Cyclin-Dependent Kinase Inhibitor p27
  • Metribolone
  • Testosterone
  • bicalutamide