Risk of hormone escape in a human prostate cancer model depends on therapy modalities and can be reduced by tyrosine kinase inhibitors

PLoS One. 2012;7(8):e42252. doi: 10.1371/journal.pone.0042252. Epub 2012 Aug 6.

Abstract

Almost all prostate cancers respond to androgen deprivation treatment but many recur. We postulated that risk of hormone escape--frequency and delay--are influenced by hormone therapy modalities. More, hormone therapies induce crucial biological changes involving androgen receptors; some might be targets for escape prevention. We investigated the relationship between the androgen deprivation treatment and the risk of recurrence using nude mice bearing the high grade, hormone-dependent human prostate cancer xenograft PAC120. Tumor-bearing mice were treated by Luteinizing-Hormone Releasing Hormone (LHRH) antagonist alone, continuous or intermittent regimen, or combined with androgen receptor (AR) antagonists (bicalutamide or flutamide). Tumor growth was monitored. Biological changes were studied as for genomic alterations, AR mutations and protein expression in a large series of recurrent tumors according to hormone therapy modalities. Therapies targeting Her-2 or AKT were tested in combination with castration. All statistical tests were two-sided. Tumor growth was inhibited by continuous administration of the LH-RH antagonist degarelix (castration), but 40% of tumors recurred. Intermittent castration or complete blockade induced by degarelix and antiandrogens combination, inhibited tumor growth but increased the risk of recurrence (RR) as compared to continuous castration (RR(intermittent): 14.5, RR(complete blockade): 6.5 and 1.35). All recurrent tumors displayed new quantitative genetic alterations and AR mutations, whatever the treatment modalities. AR amplification was found after complete blockade. Increased expression of Her-2/neu with frequent ERK/AKT activation was detected in all variants. Combination of castration with a Her-2/neu inhibitor decreased recurrence risk (0.17) and combination with an mTOR inhibitor prevented it. Anti-hormone treatments influence risk of recurrence although tumor growth inhibition was initially similar. Recurrent tumors displayed genetic instability, AR mutations, and alterations of phosphorylation pathways. We postulated that Her-2/AKT pathways allowed salvage of tumor cells under castration and we demonstrated that their inhibition prevented tumor recurrence in our model.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Androgens / deficiency
  • Androgens / therapeutic use*
  • Animals
  • Base Sequence
  • Castration
  • Cluster Analysis
  • Combined Modality Therapy
  • Disease-Free Survival
  • Gene Dosage / genetics
  • Humans
  • Male
  • Mice
  • Mutation / genetics
  • Prostatic Neoplasms / drug therapy*
  • Prostatic Neoplasms / enzymology*
  • Prostatic Neoplasms / genetics
  • Prostatic Neoplasms / pathology
  • Protein Kinase Inhibitors / pharmacology*
  • Protein Kinase Inhibitors / therapeutic use*
  • Protein-Tyrosine Kinases / antagonists & inhibitors*
  • Protein-Tyrosine Kinases / metabolism
  • Receptor, ErbB-2 / genetics
  • Receptors, Androgen / genetics
  • Xenograft Model Antitumor Assays*

Substances

  • Androgens
  • Protein Kinase Inhibitors
  • Receptors, Androgen
  • ERBB2 protein, human
  • Protein-Tyrosine Kinases
  • Receptor, ErbB-2

Grants and funding

This work was supported by the ARC and the Ligue contre le cancer (Paris, France). These funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. ARTIC funded the English editing.