RRM2 regulates Bcl-2 in head and neck and lung cancers: a potential target for cancer therapy

Clin Cancer Res. 2013 Jul 1;19(13):3416-28. doi: 10.1158/1078-0432.CCR-13-0073. Epub 2013 May 29.

Abstract

Purpose: Ribonucleotide reductase subunit M2 (RRM2) plays an active role in tumor progression. Recently, we reported that depletion of RRM2 by systemic delivery of a nanoparticle carrying RRM2-specific siRNA suppresses head and neck tumor growth. The aim of this study is to clarify the underlying mechanism by which RRM2 depletion inhibits tumor growth.

Experimental design: siRNA-mediated gene silencing was carried out to downregulate RRM2. Immunoblotting, reverse-transcriptase PCR, confocal microscopy, tissue fractionation, gene overexpression and knockdown were employed to analyze critical apoptosis signaling. Conventional immunohistochemistry and quantum dot-based immunofluorescence were applied to detect RRM2 and Bcl2 expression and localization in tissue samples from patients and mice.

Results: Knockdown of RRM2 led to apoptosis through the intrinsic pathway in head and neck squamous cell carcinoma (HNSCC) and non-small cell lung cancer (NSCLC) cell lines. We showed that Bcl-2 is a key determinant controlling apoptosis, both in vitro and in vivo, and that RRM2 depletion significantly reduces Bcl-2 protein expression. We observed that RRM2 regulates Bcl-2 protein stability, with RRM2 suppression leading to increased Bcl-2 degradation, and identified their colocalization in HNSCC and NSCLC cells. In a total of 50 specimens each from patients with HNSCC and NSCLC, we identified the colocalization of Bcl-2 and RRM2 and found a significant positive correlation between their expression in HNSCC (R = 0.98; P < 0.0001) and NSCLC (R = 0.92; P < 0.0001) tumor tissues.

Conclusions: Our novel findings add to the knowledge of RRM2 in regulating expression of the antiapoptotic protein Bcl-2 and reveal a critical link between RRM2 and Bcl-2 in apoptosis signaling.

Publication types

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

MeSH terms

  • Apoptosis / genetics
  • Carcinoma, Non-Small-Cell Lung / genetics*
  • Carcinoma, Non-Small-Cell Lung / metabolism
  • Carcinoma, Squamous Cell / genetics*
  • Carcinoma, Squamous Cell / metabolism
  • Cell Line, Tumor
  • DNA-Binding Proteins / metabolism
  • Gene Expression Regulation, Neoplastic*
  • Gene Knockdown Techniques
  • Head and Neck Neoplasms / genetics*
  • Head and Neck Neoplasms / metabolism
  • Humans
  • Mitochondria / genetics
  • Mitochondria / metabolism
  • Nuclear Proteins / metabolism
  • Protein Binding
  • Protein Stability
  • Protein Transport
  • Proto-Oncogene Proteins c-akt / metabolism
  • Proto-Oncogene Proteins c-bcl-2 / genetics*
  • Proto-Oncogene Proteins c-bcl-2 / metabolism
  • Ribonucleoside Diphosphate Reductase / genetics*
  • Ribonucleoside Diphosphate Reductase / metabolism
  • Signal Transduction
  • Squamous Cell Carcinoma of Head and Neck
  • Transcription, Genetic
  • Tumor Protein p73
  • Tumor Suppressor Protein p53 / metabolism
  • Tumor Suppressor Proteins / metabolism

Substances

  • DNA-Binding Proteins
  • Nuclear Proteins
  • Proto-Oncogene Proteins c-bcl-2
  • Trp73 protein, mouse
  • Tumor Protein p73
  • Tumor Suppressor Protein p53
  • Tumor Suppressor Proteins
  • ribonucleotide reductase M2
  • Ribonucleoside Diphosphate Reductase
  • Proto-Oncogene Proteins c-akt