High-throughput 3D screening reveals differences in drug sensitivities between culture models of JIMT1 breast cancer cells

PLoS One. 2013 Oct 23;8(10):e77232. doi: 10.1371/journal.pone.0077232. eCollection 2013.

Abstract

The traditional method for studying cancer in vitro is to grow immortalized cancer cells in two-dimensional monolayers on plastic. However, many cellular features are impaired in these artificial conditions, and large changes in gene expression compared to tumors have been reported. Three-dimensional cell culture models have become increasingly popular and are suggested to be better models than two-dimensional monolayers due to improved cell-to-cell contact and structures that resemble in vivo architecture. The aim of this study was to develop a simple high-throughput three-dimensional drug screening method and to compare drug responses in JIMT1 breast cancer cells when grown in two dimensions, in poly(2-hydroxyethyl methacrylate) induced anchorage-independent three-dimensional models, and in Matrigel three-dimensional cell culture models. We screened 102 compounds with multiple concentrations and biological replicates for their effects on cell proliferation. The cells were either treated immediately upon plating, or they were allowed to grow in three-dimensional cultures for 4 days before the drug treatment. Large variations in drug responses were observed between the models indicating that comparisons of culture model-influenced drug sensitivities cannot be made based on the effects of a single drug. However, we show with the 63 most prominent drugs that, in general, JIMT1 cells grown on Matrigel were significantly more sensitive to drugs than cells grown in two-dimensional cultures, while the responses of cells grown in poly(2-hydroxyethyl methacrylate) resembled those of the two-dimensional cultures. Furthermore, comparing the gene expression profiles of the cell culture models to xenograft tumors indicated that cells cultured in Matrigel and as xenografts most closely resembled each other. In this study, we also suggest that three-dimensional cultures can provide a platform for systematic experimentation of larger compound collections in a high-throughput mode and be used as alternatives to traditional two-dimensional screens for better comparability to the in vivo state.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Antineoplastic Agents / pharmacology*
  • Breast Neoplasms / drug therapy*
  • Cell Culture Techniques / methods*
  • Cell Line, Tumor
  • Cell Proliferation / drug effects
  • Collagen
  • Drug Combinations
  • Drug Screening Assays, Antitumor / methods*
  • Female
  • Gene Expression Profiling
  • Gene Expression Regulation, Neoplastic / drug effects
  • High-Throughput Screening Assays / methods*
  • Humans
  • Laminin
  • Linear Models
  • Polyhydroxyethyl Methacrylate
  • Proteoglycans

Substances

  • Antineoplastic Agents
  • Drug Combinations
  • Laminin
  • Proteoglycans
  • matrigel
  • Polyhydroxyethyl Methacrylate
  • Collagen

Grants and funding

Funding for this work has been provided by Academy Finland postdoctoral grant #253108, Academy of Finland Centre of Excellence in Translational Genome Scale Biology program #129620 and Sigrid Juselius Foundation. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.