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The C4b binding protein alpha (C4BPA) chain primarily engages in critical inflammatory and coagulation processes. The previous transcriptomic analysis showed that  C4BPA  is a differentially expressed gene in lower and higher fat content mammary gland cell lines from Chinese Holstein. This study aimed to investigate the effects of  C4BPA  on the inflammation and milk fat synthesis in bMECs by  C4BPA  knockdown and overexpression. The results highlighted that knockdown of  C4BPA  in bMECs could suppress the mRNA and protein expression of  IL-6, IL-8, IL-12 , and the TLR-4/NF-κB pathway-related genes and promote the expression of complement and coagulation cascade pathways related genes as well as  TNF-α . Moreover, knockdown of  C4BPA  expression in bMECs reduced the content of triglyceride (TG) and cholesterol (CHOL) in bMECs, increased NEFA content, reduced mRNA and protein expression of  ACSL1  and  PPARA , and increased the mRNA and protein expression of  ELOVL6 ,  FADS1 , and  LPL . The bMECs, with the overexpression of  C4BPA , showed the enhanced expression of  TLR-4/NF-κB  linked genes,  IL-6 ,  IL-8 ,  IL-12 , and mRNA and protein level while reduced mRNA expression of  TNF-α , compliment, and coagulation cascade related genes was observed. In bMECs, overexpression of  C4BPA  enhanced the content of TG and CHOL while reducing NEFA and stimulated the mRNA and protein expression of  ACSL1 ,  PPARA , and  PPARG  genes while inhibiting the mRNA and protein expression of  FADS1  and  LPL  genes. Our results show that  C4BPA  not only regulates the lipid metabolism through the PPAR signaling pathway in bMECs but also contributes to the inflammatory response through TLR-4/NF-κB and the complement and coagulation cascade pathways. This study, for the first time, provides the primary basis for understanding the role of  C4BPA  in immunity and fat metabolism, which enables the researchers for innovative direction to investigate genes associated with fat metabolism and immunity. This study also advocates that the breeders must pay attention to such type of genes with multiple functions during animal breeding.

C4BPA: A Novel Co-Regulator of Immunity and Fat Metabolism in the Bovine Mammary Epithelial Cells