Gene Expression Profiling of Gliadin Effects on Intestinal Epithelial Cells Suggests Novel Non-Enzymatic Functions of Pepsin and Trypsin

PLoS One. 2013 Jun 18;8(6):e66307. doi: 10.1371/journal.pone.0066307. Print 2013.

Abstract

Gliadin triggers T-cell mediated immunity in celiac disease, and has cytotoxic effects on enterocytes mediated through obscure mechanisms. In addition, gliadin transport mechanisms, potential cell surface receptors and gliadin-activated downstream signaling pathways are not completely understood. In order to screen for novel downstream gliadin target genes we performed a systematic whole genome expression study on intestinal epithelial cells. Undifferentiated Caco-2 cells were exposed to pepsin- and trypsin- digested gliadin (PT-G), a blank pepsin-trypsin control (PT) and to a synthetic peptide corresponding to gliadin p31-43 peptide for six hours. RNA from four different experiments was used for hybridization on Agilent one color human whole genome DNA microarray chips. The microarray data were analyzed using the Bioconductor package LIMMA. Genes with nominal p<0.01 were considered statistically significant. Compared to the untreated cells 1705, 1755 and 211 probes were affected by PT-G, PT and p31-43 respectively. 46 probes were significantly different between PT and PT-G treated cells. Among the p31-43 peptide affected probes, 10 and 21 probes were affected by PT-G and PT respectively. Only PT-G affected genes could be validated by quantitative real-time polymerase chain reaction. All the genes were, nonetheless, also affected to a comparable level by PT treated negative controls. In conclusion, we could not replicate previously reported direct effects of gliadin peptides on enterocytes. The results rather suggest that certain epitopes derived from pepsin and trypsin may also affect epithelial cell gene transcription. Our study suggests novel non-enzymatic effects of pepsin and trypsin on cells and calls for proper controls in pepsin and trypsin digested gliadin experiments. It is conceivable that gliadin effects on enterocytes are secondary mediated through oxidative stress, NFkB activation and IL-15 up-regulation.

Publication types

  • Validation Study

MeSH terms

  • Caco-2 Cells
  • Gene Expression Profiling*
  • Gliadin / genetics*
  • Humans
  • Intestinal Mucosa / immunology
  • Intestinal Mucosa / metabolism*
  • Oligonucleotide Array Sequence Analysis
  • Pepsin A / metabolism*
  • Real-Time Polymerase Chain Reaction
  • Trypsin / metabolism*

Substances

  • Gliadin
  • Trypsin
  • Pepsin A

Grants and funding

This work was funded by the European Union Commission by a Marie Curie Excellence Grant (FP6 contract MEXT-CT-2005-025270)and by the Academy of Finland. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.