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Differential gene expression profiling of porcine epithelial cells infected with three enterotoxigenic Escherichia coli strains.

Zhou C, Liu Z, Jiang J, Yu Y, Zhang Q - BMC Genomics (2012)

Bottom Line: In ETEC strains, the fimbrial types F4 and F18 are commonly found differently colonized within the small intestine and cause huge economic losses in the swine industry annually worldwide.The gene ontology and pathway analysis showed that the differentially expressed genes in C(F4ab)vs control are significantly involved in cell-cycle progress and amino acid metabolism, while the clustered terms of the differentially expressed genes in C(F4ac)vs control comprise immune, inflammation and wounding response and apoptosis as well as cell cycle progress and proteolysis.The genes induced by ETECs with F4 versus F18 fimbriae suggest why ETEC with F4 may be more virulent compared to F18 which seems to elicit milder effects.

View Article: PubMed Central - HTML - PubMed

Affiliation: Key Laboratory of Animal Genetics, Breeding and Reproduction, Ministry of Agriculture, National Engineering Laboratory for Animal Breeding, College of Animal Science and Technology, China Agricultural University, 100193 Beijing, Peoples Republic of China.

ABSTRACT

Background: Enterotoxigenic Escherichia coli (ETEC) is one of the most important pathogenic bacteria causing severe diarrhoea in human and pigs. In ETEC strains, the fimbrial types F4 and F18 are commonly found differently colonized within the small intestine and cause huge economic losses in the swine industry annually worldwide. To address the underlying mechanism, we performed a transcriptome study of porcine intestinal epithelial cells (IPEC-J2) with and without infection of three representative ETEC strains.

Results: A total 2443, 3493 and 867 differentially expressed genes were found in IPEC-J2 cells infected with F4ab ETEC (C(F4ab)), with F4ac ETEC (C(F4ac)) and with F18ac ETEC (C(F18ac)) compared to the cells without infection (control), respectively. The number of differentially expressed genes between C(F4ab) and C(F4ac), C(F4ab) and C(F18ac), and C(F4ac) and C(F18ac) were 77, 1446 and 1629, respectively. The gene ontology and pathway analysis showed that the differentially expressed genes in C(F4ab)vs control are significantly involved in cell-cycle progress and amino acid metabolism, while the clustered terms of the differentially expressed genes in C(F4ac)vs control comprise immune, inflammation and wounding response and apoptosis as well as cell cycle progress and proteolysis. Differentially expressed genes between C(F18ac)vs control are mainly involved in cell-cycle progression and immune response. Furthermore, fundamental differences were observed in expression levels of immune-related genes among the three ETEC treatments, especially for the important pro-inflammatory molecules, including IL-6, IL-8, TNF-α, CCL20, CXCL2 etc.

Conclusions: The discovery in this study provides insights into the interaction of porcine intestinal epithelial cells with F4 ETECs and F18 ETEC, respectively. The genes induced by ETECs with F4 versus F18 fimbriae suggest why ETEC with F4 may be more virulent compared to F18 which seems to elicit milder effects.

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Gene Ontology and pathway enrichment of differentially expressed genes in all comparisons. CF4ab: IPEC-J2 cells infected with F4ab ETEC; CF4ac: IPEC-J2 cells infected with F4ac ETEC; CF18ac: IPEC-J2 cells infected with F18ac ETEC; Control: the non-infected IPEC-J2 cells. The Unigene ID of the genes constituting every “↑” (up-regulated or more highly expressed after ETEC infection) and “↓” (down-regulated or more lowly expressed after ETEC infection) set in Table1 were subjected to enrichment analysis using DAVID annotation tool. Biological processes and pathways that were significantly enriched (adjusted p-value < 0.05) in at least one cluster were shown in heatmap-like graph. A is the result of “↑” genes while B is the result of “↓” genes. Frequency of each term was color coded ranging from white for scarce terms to deep colors saturating with increasing frequency. Rows indicated the enriched terms and columns the frequency of the respective clusters. There was no significant enrichment found by comparisons of CF4abvs CF4ac and CF18acvs control, thus these two comparisons were not included in the figure.
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Figure 2: Gene Ontology and pathway enrichment of differentially expressed genes in all comparisons. CF4ab: IPEC-J2 cells infected with F4ab ETEC; CF4ac: IPEC-J2 cells infected with F4ac ETEC; CF18ac: IPEC-J2 cells infected with F18ac ETEC; Control: the non-infected IPEC-J2 cells. The Unigene ID of the genes constituting every “↑” (up-regulated or more highly expressed after ETEC infection) and “↓” (down-regulated or more lowly expressed after ETEC infection) set in Table1 were subjected to enrichment analysis using DAVID annotation tool. Biological processes and pathways that were significantly enriched (adjusted p-value < 0.05) in at least one cluster were shown in heatmap-like graph. A is the result of “↑” genes while B is the result of “↓” genes. Frequency of each term was color coded ranging from white for scarce terms to deep colors saturating with increasing frequency. Rows indicated the enriched terms and columns the frequency of the respective clusters. There was no significant enrichment found by comparisons of CF4abvs CF4ac and CF18acvs control, thus these two comparisons were not included in the figure.

Mentions: For the 2443 unique genes observed in the comparison of CF4abvs control, 22 enriched GO terms and six pathways (Figure 2A, Additional file 1) were obtained from the up-regulated genes, while six enriched GO terms and five pathways (Figure 2B, Additional file 2) were obtained from the down-regulated genes. The enriched GO terms of the up-regulated genes could be roughly grouped into two clusters. The first cluster is cell cycle progression [23] (cell cycle, M phase of mitotic cell cycle, cell division, chromatin organization, DNA metabolic process, DNA packaging, mitosis, nuclear division, organelle fission, protein-DNA complex assembly, and regulation of cell growth). The second cluster centers on catabolism processes, such as cellular amino acid catabolic process and amine catabolic process. Among the six pathways, the p53 signaling pathway, which can be induced by a number of stress signals such as pathogen infection, oxidative stress, DNA damage and activated oncogenes, has the ability to eliminate excess, damaged or infected cells by apoptosis [24]. Another pathway, the systemic lupus erythematosus pathway, points to that pathogens gain their foothold in host cells through modulating host defense mechanisms [25]. These two pathways had the lowest P-value of 9.06 × 10-4 and 5.82 × 10-4, respectively. The remaining four pathways are cell cycle, bladder cancer, arachidonic acid metabolism and homologous recombination, and the pathway of cell cycle is related with the p53 signaling pathway.


Differential gene expression profiling of porcine epithelial cells infected with three enterotoxigenic Escherichia coli strains.

Zhou C, Liu Z, Jiang J, Yu Y, Zhang Q - BMC Genomics (2012)

Gene Ontology and pathway enrichment of differentially expressed genes in all comparisons. CF4ab: IPEC-J2 cells infected with F4ab ETEC; CF4ac: IPEC-J2 cells infected with F4ac ETEC; CF18ac: IPEC-J2 cells infected with F18ac ETEC; Control: the non-infected IPEC-J2 cells. The Unigene ID of the genes constituting every “↑” (up-regulated or more highly expressed after ETEC infection) and “↓” (down-regulated or more lowly expressed after ETEC infection) set in Table1 were subjected to enrichment analysis using DAVID annotation tool. Biological processes and pathways that were significantly enriched (adjusted p-value < 0.05) in at least one cluster were shown in heatmap-like graph. A is the result of “↑” genes while B is the result of “↓” genes. Frequency of each term was color coded ranging from white for scarce terms to deep colors saturating with increasing frequency. Rows indicated the enriched terms and columns the frequency of the respective clusters. There was no significant enrichment found by comparisons of CF4abvs CF4ac and CF18acvs control, thus these two comparisons were not included in the figure.
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Figure 2: Gene Ontology and pathway enrichment of differentially expressed genes in all comparisons. CF4ab: IPEC-J2 cells infected with F4ab ETEC; CF4ac: IPEC-J2 cells infected with F4ac ETEC; CF18ac: IPEC-J2 cells infected with F18ac ETEC; Control: the non-infected IPEC-J2 cells. The Unigene ID of the genes constituting every “↑” (up-regulated or more highly expressed after ETEC infection) and “↓” (down-regulated or more lowly expressed after ETEC infection) set in Table1 were subjected to enrichment analysis using DAVID annotation tool. Biological processes and pathways that were significantly enriched (adjusted p-value < 0.05) in at least one cluster were shown in heatmap-like graph. A is the result of “↑” genes while B is the result of “↓” genes. Frequency of each term was color coded ranging from white for scarce terms to deep colors saturating with increasing frequency. Rows indicated the enriched terms and columns the frequency of the respective clusters. There was no significant enrichment found by comparisons of CF4abvs CF4ac and CF18acvs control, thus these two comparisons were not included in the figure.
Mentions: For the 2443 unique genes observed in the comparison of CF4abvs control, 22 enriched GO terms and six pathways (Figure 2A, Additional file 1) were obtained from the up-regulated genes, while six enriched GO terms and five pathways (Figure 2B, Additional file 2) were obtained from the down-regulated genes. The enriched GO terms of the up-regulated genes could be roughly grouped into two clusters. The first cluster is cell cycle progression [23] (cell cycle, M phase of mitotic cell cycle, cell division, chromatin organization, DNA metabolic process, DNA packaging, mitosis, nuclear division, organelle fission, protein-DNA complex assembly, and regulation of cell growth). The second cluster centers on catabolism processes, such as cellular amino acid catabolic process and amine catabolic process. Among the six pathways, the p53 signaling pathway, which can be induced by a number of stress signals such as pathogen infection, oxidative stress, DNA damage and activated oncogenes, has the ability to eliminate excess, damaged or infected cells by apoptosis [24]. Another pathway, the systemic lupus erythematosus pathway, points to that pathogens gain their foothold in host cells through modulating host defense mechanisms [25]. These two pathways had the lowest P-value of 9.06 × 10-4 and 5.82 × 10-4, respectively. The remaining four pathways are cell cycle, bladder cancer, arachidonic acid metabolism and homologous recombination, and the pathway of cell cycle is related with the p53 signaling pathway.

Bottom Line: In ETEC strains, the fimbrial types F4 and F18 are commonly found differently colonized within the small intestine and cause huge economic losses in the swine industry annually worldwide.The gene ontology and pathway analysis showed that the differentially expressed genes in C(F4ab)vs control are significantly involved in cell-cycle progress and amino acid metabolism, while the clustered terms of the differentially expressed genes in C(F4ac)vs control comprise immune, inflammation and wounding response and apoptosis as well as cell cycle progress and proteolysis.The genes induced by ETECs with F4 versus F18 fimbriae suggest why ETEC with F4 may be more virulent compared to F18 which seems to elicit milder effects.

View Article: PubMed Central - HTML - PubMed

Affiliation: Key Laboratory of Animal Genetics, Breeding and Reproduction, Ministry of Agriculture, National Engineering Laboratory for Animal Breeding, College of Animal Science and Technology, China Agricultural University, 100193 Beijing, Peoples Republic of China.

ABSTRACT

Background: Enterotoxigenic Escherichia coli (ETEC) is one of the most important pathogenic bacteria causing severe diarrhoea in human and pigs. In ETEC strains, the fimbrial types F4 and F18 are commonly found differently colonized within the small intestine and cause huge economic losses in the swine industry annually worldwide. To address the underlying mechanism, we performed a transcriptome study of porcine intestinal epithelial cells (IPEC-J2) with and without infection of three representative ETEC strains.

Results: A total 2443, 3493 and 867 differentially expressed genes were found in IPEC-J2 cells infected with F4ab ETEC (C(F4ab)), with F4ac ETEC (C(F4ac)) and with F18ac ETEC (C(F18ac)) compared to the cells without infection (control), respectively. The number of differentially expressed genes between C(F4ab) and C(F4ac), C(F4ab) and C(F18ac), and C(F4ac) and C(F18ac) were 77, 1446 and 1629, respectively. The gene ontology and pathway analysis showed that the differentially expressed genes in C(F4ab)vs control are significantly involved in cell-cycle progress and amino acid metabolism, while the clustered terms of the differentially expressed genes in C(F4ac)vs control comprise immune, inflammation and wounding response and apoptosis as well as cell cycle progress and proteolysis. Differentially expressed genes between C(F18ac)vs control are mainly involved in cell-cycle progression and immune response. Furthermore, fundamental differences were observed in expression levels of immune-related genes among the three ETEC treatments, especially for the important pro-inflammatory molecules, including IL-6, IL-8, TNF-α, CCL20, CXCL2 etc.

Conclusions: The discovery in this study provides insights into the interaction of porcine intestinal epithelial cells with F4 ETECs and F18 ETEC, respectively. The genes induced by ETECs with F4 versus F18 fimbriae suggest why ETEC with F4 may be more virulent compared to F18 which seems to elicit milder effects.

Show MeSH
Related in: MedlinePlus