Abstract
Staphylococcus aureus (S. aureus) is problematic for lactating mammals and public health. Understanding of mechanisms by which the hosts respond to severe invasion of S. aureus remains elusive. In this study, the genome-wide expression of mRNAs and miRNAs in bovine mammary gland cells were interrogated at 24 h after intra-mammary infection (IMI) with high or low concentrations of S. aureus. Compared to the negative control quarters, 194 highly-confident responsive genes were identified in the quarters with high concentration (109 cfu/mL) of S. aureus, which were predominantly implicated in pathways and biological processes pertaining to innate immune system, such as cytokine-cytokine receptor interaction and inflammatory response. In contrast, only 21 highly-confident genes were significantly differentially expressed in face of low concentration (106 cfu/mL) of S. aureus, which slightly perturbed the cell signaling and invoked corresponding responses like vasoconstriction, indicating limited perturbations and immunological evading. Additionally, the significant up-regulations of bta-mir-223 and bta-mir-21-3p were observed in the quarters infected by high concentration of S. aureus. Network analysis suggested that the two miRNAs' pivotal roles in defending hosts against bacterial infection probably through inhibiting CXCL14 and KIT. The significant down-regulation of CXCL14 was also observed in bovine mammary epithelial cells at 24 h post-infection of S. aureus (108 cfu/mL) in vitro. Integrated analysis with QTL database further suggested 28 genes (e.g., CXCL14, KIT, and SLC4A11) as candidates of bovine mastitis. This study first systematically revealed transcriptional and post-transcriptional responses of bovine mammary gland cells to invading S. aureus in a dosage-dependent pattern, and highlighted a complicated responsive mechanism in a network of miRNA-gene-pathway interplay.
Highlights
Mastitis, generally defined as inflammatory changes in the mammary gland with an invading microbial agent, has been considered as one of the most prevalent and economically significant diseases in dairy sector worldwide over the last decades (De Oliveira et al, 2000; Bradley, 2002; Halasa et al, 2007; Middleton et al, 2014), which is a concern for animal welfare and a risk for public health as milk is an essential source of human nutrition
The two goals of this study are: (1) to detect the innate immune responses and the global networks of genes, pathways and miRNAs that were activated in bovine mammary gland at 24 h post intra-mammary infection (IMI) with S. aureus; (2) to identify powerful candidate genes associated with bovine S. aureus mastitis for follow-up functional studies
Of note, compared to udder quarters infected with low concentration of S. aureus, the udder quarters infected with high concentration exhibited much stronger physiological responses including udder swelling and milk coagulation that severely obstructed the detection of somatic cell count (SCC) (Table 2)
Summary
Generally defined as inflammatory changes in the mammary gland with an invading microbial agent, has been considered as one of the most prevalent and economically significant diseases in dairy sector worldwide over the last decades (De Oliveira et al, 2000; Bradley, 2002; Halasa et al, 2007; Middleton et al, 2014), which is a concern for animal welfare and a risk for public health as milk is an essential source of human nutrition. S. aureus often causes subclinical and chronic mastitis affecting all lactating mammals due to its resistance to antibiotic treatments and its capability to evade the host’s innate and adaptive immune responses (Fox and Gay, 1993; Bradley, 2002; Contreras and Rodríguez, 2011; Spaan et al, 2013). Keeping in view of the strong need to decrease the use of antibiotics and further enhance food safety as well as animal welfare, effective genetic improvement of immune response through precise genomic selection for mastitis resistance in dairy animals has been considered as a prophylactic and economical approach (Keirn et al, 2001; Tao and Mallard, 2007; Pighetti and Elliott, 2011; Sordillo, 2011)
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