CCL2 is induced by chemotherapy and protects prostate cancer cells from docetaxel-induced cytotoxicity

Prostate. 2010 Mar 1;70(4):433-42. doi: 10.1002/pros.21077.

Abstract

Background: Metastatic prostate cancer is either inherently resistant to chemotherapy or rapidly acquires this phenotype after chemotherapy exposure. In this study, we identified a docetaxel-induced resistance mechanism centered on CCL2.

Methods: We compared the gene expression profiles in individual human prostate cancer specimens before and after exposure to chemotherapy collected from previously untreated patients who participated in a clinical trial of preoperative chemotherapy. Subsequently, we used the gain- and loss-of-function approach in vitro to identify a potential mechanism underlying chemotherapy resistance.

Results: Among the molecular signatures associated with treatment, several genes that regulate the inflammatory response and chemokine activity were upregulated including a significant increase in transcripts encoding the CC chemokine CCL2. Docetaxel increased CCL2 expression in prostate cancer cell lines in vitro. CCL2-specific siRNA inhibited LNCaP and LAPC4 cell proliferation and enhanced the growth inhibitory effect of low-dose docetaxel. In contrast, overexpression of CCL2 or recombinant CCL2 protein stimulated prostate cancer cell proliferation and rescued cells from docetaxel-induced cytotoxicity. This protective effect of CCL2 was associated with activation of the ERK/MAP kinase and PI3K/AKT, inhibition of docetaxel-induced Bcl2 phosphorylation at serine 70, phosphorylation of Bad, and activation of caspase-3. The addition of a PI3K/AKT inhibitor Ly294002 reversed the CCL2 protection and was additive to docetaxel-induced toxicity.

Conclusion: These results support a mechanism of chemotherapy resistance mediated by cellular stress responses involving the induction of CCL2 expression and suggest that inhibiting CCL2 activity could enhance therapeutic responses to taxane-based therapy.

Publication types

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

MeSH terms

  • Antineoplastic Agents / pharmacology*
  • Apoptosis / drug effects
  • Cell Line, Tumor
  • Cell Survival / drug effects
  • Chemokine CCL2 / antagonists & inhibitors
  • Chemokine CCL2 / genetics*
  • Chemokine CCL2 / pharmacology
  • Docetaxel
  • Drug Resistance, Neoplasm / genetics
  • Drug Therapy, Combination
  • Gene Expression / drug effects*
  • Gene Expression Profiling
  • Gene Silencing
  • Humans
  • Male
  • Mitoxantrone / pharmacology
  • Prostatic Neoplasms / drug therapy*
  • Prostatic Neoplasms / genetics
  • Prostatic Neoplasms / metabolism
  • RNA, Messenger / metabolism
  • RNA, Small Interfering / genetics
  • Recombinant Proteins / pharmacology
  • Taxoids / pharmacology*
  • Up-Regulation

Substances

  • Antineoplastic Agents
  • CCL2 protein, human
  • Chemokine CCL2
  • RNA, Messenger
  • RNA, Small Interfering
  • Recombinant Proteins
  • Taxoids
  • Docetaxel
  • Mitoxantrone