Evaluation of toxicogenomics approaches for assessing the risk of nongenotoxic carcinogenicity in rat liver

PLoS One. 2014 May 14;9(5):e97678. doi: 10.1371/journal.pone.0097678. eCollection 2014.

Abstract

The current gold-standard method for cancer safety assessment of drugs is a rodent two-year bioassay, which is associated with significant costs and requires testing a high number of animals over lifetime. Due to the absence of a comprehensive set of short-term assays predicting carcinogenicity, new approaches are currently being evaluated. One promising approach is toxicogenomics, which by virtue of genome-wide molecular profiling after compound treatment can lead to an increased mechanistic understanding, and potentially allow for the prediction of a carcinogenic potential via mathematical modeling. The latter typically involves the extraction of informative genes from omics datasets, which can be used to construct generalizable models allowing for the early classification of compounds with unknown carcinogenic potential. Here we formally describe and compare two novel methodologies for the reproducible extraction of characteristic mRNA signatures, which were employed to capture specific gene expression changes observed for nongenotoxic carcinogens. While the first method integrates multiple gene rankings, generated by diverse algorithms applied to data from different subsamplings of the training compounds, the second approach employs a statistical ratio for the identification of informative genes. Both methods were evaluated on a dataset obtained from the toxicogenomics database TG-GATEs to predict the outcome of a two-year bioassay based on profiles from 14-day treatments. Additionally, we applied our methods to datasets from previous studies and showed that the derived prediction models are on average more accurate than those built from the original signatures. The selected genes were mostly related to p53 signaling and to specific changes in anabolic processes or energy metabolism, which are typically observed in tumor cells. Among the genes most frequently incorporated into prediction models were Phlda3, Cdkn1a, Akr7a3, Ccng1 and Abcb4.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Algorithms*
  • Animals
  • Apoptosis Regulatory Proteins / genetics
  • Apoptosis Regulatory Proteins / metabolism
  • Carcinogenicity Tests / methods
  • Carcinogens / toxicity*
  • Cell Cycle Proteins / genetics
  • Cell Cycle Proteins / metabolism
  • Databases, Factual
  • Drug Evaluation, Preclinical
  • Gene Expression Profiling
  • Liver / drug effects
  • Liver / metabolism
  • Liver / pathology
  • Liver Neoplasms / chemically induced
  • Liver Neoplasms / genetics*
  • Liver Neoplasms / metabolism
  • Liver Neoplasms / pathology
  • Models, Genetic
  • RNA, Messenger / genetics*
  • RNA, Messenger / metabolism
  • Rats
  • Risk
  • Toxicogenetics / methods*
  • Transcriptome*
  • Tumor Suppressor Proteins / genetics
  • Tumor Suppressor Proteins / metabolism

Substances

  • Apoptosis Regulatory Proteins
  • Carcinogens
  • Cell Cycle Proteins
  • RNA, Messenger
  • Tumor Suppressor Proteins

Grants and funding

The research leading to these results has received funding from the Innovative Medicine Initiative Joint Undertaking (IMI JU) under grant agreement nr. 115001 (MARCAR project). The authors acknowledge support by Deutsche Forschungsgemeinschaft and Open Access Publishing Fund of Tuebingen University. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.