Division of Orthopaedics and Traumatology, Department of Orthopaedics, Nanfang Hospital, Southern Medical University, No.1838 North of Guangzhou Avenue, Guangzhou, Guangdong Province, China.
Guangdong Provincial Key Laboratory of Bone and Cartilage Regenerative Medicine, Nanfang Hospital, Southern Medical University, Guangzhou, China.
PLoS Pathog. 2024 Aug 5;20(8):e1012437. doi: 10.1371/journal.ppat.1012437. eCollection 2024 Aug.
The ability of Staphylococcus aureus (S. aureus) to survive within macrophages is a critical strategy for immune evasion, contributing to the pathogenesis and progression of osteomyelitis. However, the underlying mechanisms remain poorly characterized. This study discovered that inhibiting the MEK1/2 pathway reduced bacterial load and mitigated bone destruction in a mouse model of S. aureus osteomyelitis. Histological staining revealed increased phosphorylated MEK1/2 levels in bone marrow macrophages surrounding abscess in the mouse model of S. aureus osteomyelitis. Activation of MEK1/2 pathway and its roles in impairing macrophage bactericidal function were confirmed in primary mouse bone marrow-derived macrophages (BMDMs). Transcriptome analysis and in vitro experiments demonstrated that S. aureus activates the MEK1/2 pathway through EGFR signaling. Moreover, we found that excessive activation of EGFR-MEK1/2 cascade downregulates mitochondrial reactive oxygen species (mtROS) levels by suppressing Chek2 expression, thereby impairing macrophage bactericidal function. Furthermore, pharmacological inhibition of EGFR signaling prevented upregulation of phosphorylated MEK1/2 and restored Chek2 expression in macrophages, significantly enhancing S. aureus clearance and improving bone microstructure in vivo. These findings highlight the critical role of the EGFR-MEK1/2 cascade in host immune defense against S. aureus, suggesting that S. aureus may reduce mtROS levels by overactivating the EGFR-MEK1/2 cascade, thereby suppressing macrophage bactericidal function. Therefore, combining EGFR-MEK1/2 pathway blockade with antibiotics could represent an effective therapeutic approach for the treatment of S. aureus osteomyelitis.
金黄色葡萄球菌(S. aureus)在巨噬细胞内生存的能力是其免疫逃避的关键策略,有助于骨髓炎的发病和进展。然而,其潜在机制仍知之甚少。本研究发现,抑制 MEK1/2 通路可降低金黄色葡萄球菌骨髓炎小鼠模型中的细菌负荷并减轻骨质破坏。组织学染色显示,金黄色葡萄球菌骨髓炎小鼠模型中骨髓巨噬细胞围绕脓肿的磷酸化 MEK1/2 水平升高。在原代小鼠骨髓源性巨噬细胞(BMDMs)中证实了 MEK1/2 通路的激活及其损害巨噬细胞杀菌功能的作用。转录组分析和体外实验表明,金黄色葡萄球菌通过 EGFR 信号激活 MEK1/2 通路。此外,我们发现 EGFR-MEK1/2 级联的过度激活通过抑制 Chek2 表达下调线粒体活性氧(mtROS)水平,从而损害巨噬细胞的杀菌功能。此外,EGFR 信号转导的药理学抑制可防止磷酸化 MEK1/2 的上调并恢复巨噬细胞中的 Chek2 表达,从而在体内显著增强金黄色葡萄球菌的清除并改善骨微结构。这些发现强调了 EGFR-MEK1/2 级联在宿主对金黄色葡萄球菌免疫防御中的关键作用,表明金黄色葡萄球菌可能通过过度激活 EGFR-MEK1/2 级联来降低 mtROS 水平,从而抑制巨噬细胞的杀菌功能。因此,结合 EGFR-MEK1/2 通路阻断与抗生素可能是治疗金黄色葡萄球菌骨髓炎的有效治疗方法。