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Avian pathogenic  Escherichia coli  (APEC) cause severe respiratory and systemic disease in chickens, commonly termed colibacillosis. Early immune responses after initial infection are highly important for the outcome of the infection. In this study, the early interactions between  GFP -expressing APEC strains of serotypes O1:K1:H7 and O2:K1:H5 and phagocytic cells in the lung of  CSF1R -reporter transgenic chickens were investigated.  CSF1R -reporter transgenic chickens express fluorescent protein under the control of elements of the  CSF1R  promoter and enhancer, such that cells of the myeloid lineage can be visualized  in situ  and sorted. Chickens were separately inoculated with APEC strains expressing  GFP  and culled 6 h post-infection. Flow cytometric analysis was performed to phenotype and sort the cells that harbored bacteria in the lung, and the response of the sorted cells was defined by transcriptomic analysis. Both APEC strains were mainly detected in  CSF1R -transgene neg  ( CSF1R -tg neg ) and  CSF1R -tg low  MHC II neg  MRC1L-B neg  cells and low numbers of APEC were detected in  CSF1R -tg high  MHC II pos  MRC1L-B pos  cells. Transcriptomic and flow cytometric analysis identified the APEC pos   CSF1R -tg neg  and  CSF1R -tg low  cells as heterophils and the APEC pos   CSF1R -tg high  cells as macrophages and dendritic cells. Both APEC strains induced strong inflammatory responses, however in both  CSF1R -tg neg/low  and  CSF1R -tg high  cells, many immune related pathways were repressed to a greater extent or less activated in birds inoculated with APEC O2- GFP  compared to APEC O1- GFP  inoculated birds. Comparison of the immune pathways revealed the aryl hydrocarbon receptor ( AhR ) pathway,  IL17  and  STAT3  signaling, heterophil recruitment pathways and the acute phase response, are modulated particularly post-APEC O2- GFP  inoculation. In contrast to  in vivo  data, APEC O2- GFP  was more invasive in  CSF1R -tg high  cells  in vitro  than APEC O1- GFP  and had higher survival rates for up to 6 h post-infection. Our data indicate significant differences in the responses induced by APEC strains of prevalent serotypes, with important implications for the design and interpretation of future studies. Moreover, we show that bacterial invasion and survival in phagocyte populations  in vitro  is not predictive of events in the chicken lung.

frontiers in immunology

Avian Pathogenic Escherichia coli (APEC) Strain-Dependent Immunomodulation of Respiratory Granulocytes and Mononuclear Phagocytes in CSF1R-Reporter Transgenic Chickens