Generation and characterisation of cisplatin-resistant non-small cell lung cancer cell lines displaying a stem-like signature

PLoS One. 2013;8(1):e54193. doi: 10.1371/journal.pone.0054193. Epub 2013 Jan 17.

Abstract

Introduction: Inherent and acquired cisplatin resistance reduces the effectiveness of this agent in the management of non-small cell lung cancer (NSCLC). Understanding the molecular mechanisms underlying this process may result in the development of novel agents to enhance the sensitivity of cisplatin.

Methods: An isogenic model of cisplatin resistance was generated in a panel of NSCLC cell lines (A549, SKMES-1, MOR, H460). Over a period of twelve months, cisplatin resistant (CisR) cell lines were derived from original, age-matched parent cells (PT) and subsequently characterized. Proliferation (MTT) and clonogenic survival assays (crystal violet) were carried out between PT and CisR cells. Cellular response to cisplatin-induced apoptosis and cell cycle distribution were examined by FACS analysis. A panel of cancer stem cell and pluripotent markers was examined in addition to the EMT proteins, c-Met and β-catenin. Cisplatin-DNA adduct formation, DNA damage (γH2AX) and cellular platinum uptake (ICP-MS) was also assessed.

Results: Characterisation studies demonstrated a decreased proliferative capacity of lung tumour cells in response to cisplatin, increased resistance to cisplatin-induced cell death, accumulation of resistant cells in the G0/G1 phase of the cell cycle and enhanced clonogenic survival ability. Moreover, resistant cells displayed a putative stem-like signature with increased expression of CD133+/CD44+cells and increased ALDH activity relative to their corresponding parental cells. The stem cell markers, Nanog, Oct-4 and SOX-2, were significantly upregulated as were the EMT markers, c-Met and β-catenin. While resistant sublines demonstrated decreased uptake of cisplatin in response to treatment, reduced cisplatin-GpG DNA adduct formation and significantly decreased γH2AX foci were observed compared to parental cell lines.

Conclusion: Our results identified cisplatin resistant subpopulations of NSCLC cells with a putative stem-like signature, providing a further understanding of the cellular events associated with the cisplatin resistance phenotype in lung cancer.

MeSH terms

  • AC133 Antigen
  • Aldehyde Dehydrogenase / metabolism
  • Antigens, CD / metabolism
  • Antineoplastic Agents / pharmacology
  • Biomarkers, Tumor / metabolism*
  • Carcinoma, Non-Small-Cell Lung / metabolism
  • Carcinoma, Non-Small-Cell Lung / pathology
  • Cell Cycle / drug effects
  • Cell Line, Tumor
  • Cell Proliferation / drug effects
  • Cell Survival / drug effects
  • Cisplatin / pharmacology*
  • DNA Adducts / drug effects
  • Dose-Response Relationship, Drug
  • Drug Resistance, Neoplasm / drug effects*
  • Flow Cytometry
  • Glycoproteins / metabolism
  • Homeodomain Proteins / metabolism
  • Humans
  • Hyaluronan Receptors / metabolism
  • Lung Neoplasms / metabolism
  • Lung Neoplasms / pathology
  • Nanog Homeobox Protein
  • Neoplastic Stem Cells / metabolism*
  • Octamer Transcription Factor-3 / metabolism
  • Peptides / metabolism
  • Proto-Oncogene Proteins c-met / metabolism
  • SOXB1 Transcription Factors / metabolism
  • beta Catenin / metabolism

Substances

  • AC133 Antigen
  • Antigens, CD
  • Antineoplastic Agents
  • Biomarkers, Tumor
  • DNA Adducts
  • Glycoproteins
  • Homeodomain Proteins
  • Hyaluronan Receptors
  • NANOG protein, human
  • Nanog Homeobox Protein
  • Octamer Transcription Factor-3
  • PROM1 protein, human
  • Peptides
  • SOXB1 Transcription Factors
  • beta Catenin
  • Aldehyde Dehydrogenase
  • Proto-Oncogene Proteins c-met
  • Cisplatin

Grants and funding

The authors have no support or funding to report.