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<i>Mycoplasma gallisepticum</i> (<i>MG</i>), a pathogen that infects chickens and some other birds, triggers chronic respiratory disease (CRD) in chickens, which is characterized by inflammation. The investigation of microbial pathogenesis would contribute to the deep understanding of infection control. Since microribonucleic acids (miRNAs) play a key role in this process, gga-mir-146c, an upregulated miRNA upon <i>MG</i> infection, was selected according to our previous RNA-sequencing data. In this paper, we predicted and validated that <i>MMP16</i> is one of gga-miR-146c target genes. Results show that <i>MMP16</i> is the target of gga-miR-146c and gga-miR-146c can downregulate <i>MMP16</i> expression within limits. gga-miR-146c upregulation significantly increased the expression of TLR6, NF-&#954;B p65, MyD88, and TNF-&#945;, whereas the gga-miR-146c inhibitor led to an opposite result. gga-miR-146c upregulation effectively decreased apoptosis and stimulated DF-1 cells proliferation upon <i>MG</i> infection. On the contrary, gga-miR-146c inhibitor promoted apoptosis and repressed the proliferation. Collectively, our results suggest that gga-miR-146c upregulation upon MG infection represses <i>MMP16</i> expression, activating TLR6/MyD88/NF-&#954;B pathway, promoting cell proliferation by inhibiting cell apoptosis, and, finally, enhancing cell cycle progression to defend against host <i>MG</i> infection.