Enrichment for DNA mismatch repair-deficient cells during treatment with cisplatin

Int J Cancer. 1998 Aug 31;77(5):741-6. doi: 10.1002/(sici)1097-0215(19980831)77:5<741::aid-ijc13>3.0.co;2-4.

Abstract

In addition to playing a role in tumorigenesis, loss of DNA mismatch repair results in low-level intrinsic resistance to cisplatin and carboplatin. We used a mismatch repair-deficient (clone B) and -proficient (clone B/rev) pair of Chinese hamster ovary sublines to determine the ability of cisplatin to enrich for repair-deficient cells during growth in vitro and in vivo. Clone B cells were 1.8-fold resistant to cisplatin as measured by a clonogenic assay. These cells were molecularly engineered to express constitutively the green fluorescent protein, and changes in the fraction of these repair-deficient cells were monitored by flow cytometric analysis. A single 1-hr exposure to cisplatin at an IC50 concentration enriched populations initially containing either 5 or 10% clone B cells by 81 and 75%, respectively, when measured at 5 days. Enrichment increased as a function of drug concentration to 158 and 169%, respectively, following an IC90 exposure. When grown as a xenograft, a single LD10 dose of cisplatin enriched the tumors by 48% from 4.6 to 6.8% repair-deficient cells (p = 0.04). To determine whether similar enrichment occurs during the treatment of human ovarian cancer patients, paired tumor samples were obtained from 38 patients before and after treatment with a minimum of 3 cycles of platinum drug-based primary chemotherapy and analyzed immunohistochemically for changes in the fraction of tumor cells expressing hMHL1. Following treatment there was a reduction in hMLH1 staining in 66% of the cases (p = 0.0005). Our results demonstrate that, despite the fact that loss of mismatch repair yields only modest levels of cisplatin resistance, even a single exposure to cisplatin produces quite a marked enrichment for repair-deficient cells in vitro and in vivo. Our results are consistent with the concept that treatment with cisplatin or carboplatin selects for preexisting mismatch repair-deficient cells, and that this contributes to the frequent development of clinical resistance.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing
  • Animals
  • Antineoplastic Agents / pharmacology
  • Antineoplastic Agents / therapeutic use
  • CHO Cells
  • Carrier Proteins
  • Cell Survival / drug effects
  • Cell Transformation, Neoplastic
  • Cisplatin / pharmacology*
  • Cisplatin / therapeutic use*
  • Clone Cells
  • Cricetinae
  • DNA Repair*
  • DNA-Binding Proteins*
  • Female
  • Genetic Engineering
  • Green Fluorescent Proteins
  • Humans
  • Luminescent Proteins / biosynthesis
  • Mice
  • Mice, Nude
  • MutL Protein Homolog 1
  • MutS Homolog 2 Protein
  • Neoplasm Proteins / analysis
  • Neoplasm Proteins / biosynthesis
  • Nuclear Proteins
  • Ovarian Neoplasms / drug therapy*
  • Ovarian Neoplasms / pathology
  • Proto-Oncogene Proteins / analysis
  • Proto-Oncogene Proteins / biosynthesis
  • Recombinant Fusion Proteins / biosynthesis
  • Transfection
  • Transplantation, Heterologous

Substances

  • Adaptor Proteins, Signal Transducing
  • Antineoplastic Agents
  • Carrier Proteins
  • DNA-Binding Proteins
  • Luminescent Proteins
  • MLH1 protein, human
  • Mlh1 protein, mouse
  • Neoplasm Proteins
  • Nuclear Proteins
  • Proto-Oncogene Proteins
  • Recombinant Fusion Proteins
  • Green Fluorescent Proteins
  • MSH2 protein, human
  • Msh2 protein, mouse
  • MutL Protein Homolog 1
  • MutS Homolog 2 Protein
  • Cisplatin