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Background Staphylococcus aureus  ( S. aureus ) mastitis is one of the most difficult diseases to treat in lactating dairy cows worldwide.  S. aureus  with different lineages leads to different host immune responses. Long non-coding RNAs (lncRNAs) are reported to be widely involved in the progress of inflammation. However, no research has identified stable lncRNAs among different  S. aureus  strain infections. In addition, folic acid (FA) can effectively reduce inflammation, and whether the inflammatory response caused by  S. aureus  can be reduced by FA remains to be explored. Methods lncRNA transcripts were identified from Holstein mammary gland tissues infected with different concentrations of  S. aureus  ( in vivo ) and mammary alveolar cells (Mac-T cells,  in vitro ) challenged with different  S. aureus  strains. Differentially expressed (DE) lncRNAs were evaluated, and stable DE lncRNAs were identified  in vivo  and  in vitro . On the basis of the gene sequence conservation and function conservation across species, key lncRNAs with the function of potentially immune regulation were retained for further analysis. The function of FA on inflammation induced by  S. aureus  challenge was also investigated. Then, the association analysis between these keys lncRNA transcripts and hematological parameters (HPs) was carried out. Lastly, the knockdown and overexpression of the important lncRNA were performed to validate the gene function on the regulation of cell immune response. Results Linear regression analysis showed a significant correlation between the expression levels of lncRNA shared by mammary tissue and Mac-T cells ( P  &lt; 0.001,  R  2  = 0.3517). lncRNAs  PRANCR  and  TNK2–AS1  could be regarded as stable markers associated with bovine  S. aureus  mastitis. Several HPs could be influenced by SNPs around lncRNAs  PRANCR  and  TNK2–AS1 . The results of gene function validation showed  PRANCR  regulates the mRNA expression of  SELPLG  and  ITGB2  within the  S. aureus  infection pathway and the Mac-T cells apoptosis. In addition, FA regulated the expression change of DE lncRNA involved in toxin metabolism and inflammation to fight against  S. aureus  infection. Conclusions The remarkable association between SNPs around these two lncRNAs and partial HP indicates the potentially important role of  PRANCR  and  TNK2–AS1  in immune regulation. Stable DE lncRNAs  PRANCR  and  TNK2–AS1  can be regarded as potential targets for the prevention of bovine  S. aureus  mastitis. FA supplementation can reduce the negative effect of  S. aureus  challenge by regulating the expression of lncRNAs.

Transcriptome sequencing analysis for the identification of stable lncRNAs associated with bovine Staphylococcus aureus mastitis