Abstract
Mycoplasma hyopneumoniae is the most costly pathogen for swine production. Although several studies have focused on the host-bacterium association, little is known about the changes in gene expression of swine cells upon infection. To improve our understanding of this interaction, we infected swine epithelial NPTr cells with M. hyopneumoniae strain J to identify differentially expressed mRNAs and miRNAs. The levels of 1,268 genes and 170 miRNAs were significantly modified post-infection. Up-regulated mRNAs were enriched in genes related to redox homeostasis and antioxidant defense, known to be regulated by the transcription factor NRF2 in related species. Down-regulated mRNAs were enriched in genes associated with cytoskeleton and ciliary functions. Bioinformatic analyses suggested a correlation between changes in miRNA and mRNA levels, since we detected down-regulation of miRNAs predicted to target antioxidant genes and up-regulation of miRNAs targeting ciliary and cytoskeleton genes. Interestingly, most down-regulated miRNAs were detected in exosome-like vesicles suggesting that M. hyopneumoniae infection induced a modification of the composition of NPTr-released vesicles. Taken together, our data indicate that M. hyopneumoniae elicits an antioxidant response induced by NRF2 in infected cells. In addition, we propose that ciliostasis caused by this pathogen is partially explained by the down-regulation of ciliary genes.
Highlights
Respiratory diseases are among the major health problems in the pig farming industry
The relationship between cell–cell communication and differentially expressed (DE) miRNAs released by infected cells becomes especially interesting when considering genes related to the nuclear factor erythroid 2-related factor 2 (NRF2) pathway: we identified DE miRNAs predicted to regulate such genes only in extracellular and exosome-like vesicle samples, with no difference of expression in intracellular samples (Table 6)
As far as we know, this is the first study to establish a link between gene expression of the swine cells and the most deleterious pathogenic effects of M. hyopneumoniae, namely its cytotoxic epithelial damage and induced ciliostasis
Summary
Respiratory diseases are among the major health problems in the pig farming industry. Exosomes are small membrane vesicles (50–150 nm) released from eukaryotic cells both constitutively and upon induction, under normal and pathological c onditions[13, 15] These vesicles are involved in several cellular functions and have the potential to selectively interact with specific target cells[16, 17]. Host-pathogen interactions result in signaling and physiological modifications in the host cells that induce differential miRNA expression and miRNA-mediated post-transcriptional regulation of genes involved in immune response and several other cellular pathways[19, 20]. Simultaneous identification of differentially expressed miRNAs and mRNAs provides a comprehensive view on host-pathogen interactions during the infection and the disease establishment process. The simultaneous identification of miRNAs and mRNAs will help us draw a full picture of the changes in gene expression and the possible regulatory mechanisms of host cells during the disease establishment
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