Abstract / Summary
Whereas the C-C chemokine receptor type 2 (CCR2) and its ligand, C-C motif chemokine ligand 2 (CCL2), are best known for regulating immune cell chemotaxis, their direct contribution to intracellular signaling programs controlling inflammatory activation remains incompletely understood. Here, we investigated the role of the CCL2/CCR2 axis in regulating inflammatory polarization and intracellular signaling using THP-1 cells, primary human monocyte-derived macrophages, murine RAW264.7 macrophages, and Ccr2-deficient mice. Recombinant CCL2 induced a robust pro-inflammatory transcriptional and protein expression program comparable to that elicited by lipopolysaccharide (LPS), whereas pharmacological inhibition or genetic silencing of CCR2 suppressed both basal and CCL2- or LPS-induced inflammatory responses while promoting anti-inflammatory marker expression. Mechanistically, CCL2 stimulated CCR2-dependent phosphorylation of protein kinase B (AKT) and the subsequent phosphorylation and nuclear translocation of nuclear factor kappa-light-chain-enhancer of activated B cells (NFκB) in THP-1 cells. Pharmacological inhibition of AKT or NFκB prevented CCL2-induced inflammatory polarization. Inhibition of TLR4 had minimal effect on CCL2-induced AKT/NFκB signaling, indicating that CCL2 engages this pathway independently of TLR4. Conversely, CCR2 blockade abolished AKT and NFκB activation in response to both CCL2 or LPS, while LPS-induced IKK phosphorylation was preserved. Because this block was complete rather than partial, these experiments establish CCR2 as a requirement for AKT/NFκB activation by both stimuli but do not resolve whether CCR2 provides an input parallel to TLR4 or acts downstream of it through autocrine CCL2. Consistent with these findings, Ccr2-deficient mice exhibited impaired AKT and NFκB activation together with markedly attenuated inflammatory responses following LPS challenge, and the proposed signaling mechanism was independently validated in primary human monocyte-derived macrophages and murine RAW264.7 macrophages. Together, these findings identify a conserved CCR2-dependent AKT/NFκB signaling module that regulates inflammatory polarization beyond the established chemotactic functions of CCR2 and provides a mechanistic framework for understanding how CCR2 contributes to inflammatory activation across human and murine systems.