RB1 status in triple negative breast cancer cells dictates response to radiation treatment and selective therapeutic drugs

PLoS One. 2013 Nov 12;8(11):e78641. doi: 10.1371/journal.pone.0078641. eCollection 2013.

Abstract

Triple negative breast cancer (TNBC) includes basal-like and claudin-low subtypes for which only chemotherapy and radiation therapy are currently available. The retinoblastoma (RB1) tumor suppressor is frequently lost in human TNBC. Knockdown of RB1 in luminal BC cells was shown to affect response to endocrine, radiation and several antineoplastic drugs. However, the effect of RB1 status on radiation and chemo-sensitivity in TNBC cells and whether RB1 status affects response to divergent or specific treatment are unknown. Using multiple basal-like and claudin-low cell lines, we hereby demonstrate that RB-negative TNBC cell lines are highly sensitive to gamma-irradiation, and moderately more sensitive to doxorubicin and methotrexate compared to RB-positive TNBC cell lines. In contrast, RB1 status did not affect sensitivity of TNBC cells to multiple other drugs including cisplatin (CDDP), 5-fluorouracil, idarubicin, epirubicin, PRIMA-1(met), fludarabine and PD-0332991, some of which are used to treat TNBC patients. Moreover, a non-biased screen of ∼3400 compounds, including FDA-approved drugs, revealed similar sensitivity of RB-proficient and -deficient TNBC cells. Finally, ESA(+)/CD24(-/low)/CD44(+) cancer stem cells from RB-negative TNBC lines were consistently more sensitive to gamma-irradiation than RB-positive lines, whereas the effect of chemotherapy on the cancer stem cell fraction varied irrespective of RB1 expression. Our results suggest that patients carrying RB-deficient TNBCs would benefit from gamma-irradiation as well as doxorubicin and methotrexate therapy, but not necessarily from many other anti-neoplastic drugs.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Antineoplastic Agents / pharmacology*
  • Antineoplastic Agents / therapeutic use
  • Cell Line, Tumor
  • Doxorubicin / pharmacology
  • Doxorubicin / therapeutic use
  • Gamma Rays / therapeutic use
  • Humans
  • Methotrexate / pharmacology
  • Methotrexate / therapeutic use
  • Neoplasm Invasiveness
  • Neoplastic Stem Cells / drug effects
  • Neoplastic Stem Cells / radiation effects
  • Oligonucleotide Array Sequence Analysis
  • Pharmacogenetics
  • Retinoblastoma Protein / deficiency
  • Retinoblastoma Protein / metabolism*
  • Treatment Outcome
  • Triple Negative Breast Neoplasms / drug therapy*
  • Triple Negative Breast Neoplasms / metabolism
  • Triple Negative Breast Neoplasms / pathology
  • Triple Negative Breast Neoplasms / radiotherapy*

Substances

  • Antineoplastic Agents
  • Retinoblastoma Protein
  • Doxorubicin
  • Methotrexate

Grants and funding

This study was conducted with support of the Canadian BC Foundation, Canadian BC Research Alliance, Ontario Institute for Cancer Research through funding provided by the Government of Ontario to E. Zacksenhaus, as well as the Terry-Fox Foundation to S.E. Egan and E. Zacksenhaus. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.