Sipprell Sophie E, Krueger Quinton A, Mills Erin L, Marriott Ian, Johnson M Brittany
Department of Biological Sciences, University of North Carolina at Charlotte, Charlotte, NC, 28223, USA.
Computational Intelligence for Predicting Health and Environmental Risks (CIPHER), University of North Carolina at Charlotte, Charlotte, NC, 28223, USA.
Inflammation. 2025 Mar 8. doi: 10.1007/s10753-025-02280-x.
Staphylococcal osteomyelitis is a serious infection of the bone and joints characterized by progressive inflammatory tissue damage and leukocyte recruitment leading to net bone loss. Resident bone cells are capable of recognizing Staphylococcus aureus and initiating an inflammatory immune response that recruits leukocytes and alters bone homeostasis. Importantly, bone tissue is richly innervated with substance P containing nerve fibers and we have previously shown that this neuropeptide can augment the inflammatory responses of both osteoblasts and osteoclasts to S. aureus infection via neurokinin-1 receptors (NK-1R). Here, we have extended these studies by demonstrating that pharmacological inhibition of NK-1R ameliorates disease severity in a mouse model of staphylococcal osteomyelitis. This effect was associated with a significant reduction in leukocyte-attracting chemokine production following infection and reduced local levels of osteoclast and neutrophil activity. We then assessed the effect of S. aureus infection on bone-marrow derived osteoclast gene expression in the absence or presence of substance P. We determined that infection upregulates osteoclast expression of mRNAs encoding inflammatory mediators that include the neutrophil-attracting chemokines identified in vivo. Importantly, we found that, while substance P has no effect on chemokine mRNA expression in infected cells, this neuropeptide significantly increases the release of these chemokines by S. aureus challenged osteoclasts but not osteoblasts. Together, these data further support the ability of substance P to exacerbate inflammatory damage in staphylococcal osteomyelitis and indicate that this effect may be due, in part, to an augmentation of osteoclast immune responses that promote leukocyte recruitment.
金黄色葡萄球菌骨髓炎是一种严重的骨与关节感染,其特征是进行性炎症组织损伤和白细胞募集,导致净骨丢失。驻留骨细胞能够识别金黄色葡萄球菌并启动炎症免疫反应,募集白细胞并改变骨稳态。重要的是,骨组织富含含P物质的神经纤维,我们之前已经表明,这种神经肽可以通过神经激肽-1受体(NK-1R)增强成骨细胞和破骨细胞对金黄色葡萄球菌感染的炎症反应。在这里,我们通过证明NK-1R的药理学抑制可改善金黄色葡萄球菌骨髓炎小鼠模型中的疾病严重程度,扩展了这些研究。这种作用与感染后白细胞吸引趋化因子产生的显著减少以及破骨细胞和中性粒细胞活性的局部水平降低有关。然后,我们评估了在有无P物质的情况下金黄色葡萄球菌感染对骨髓来源的破骨细胞基因表达的影响。我们确定感染会上调编码炎症介质的破骨细胞mRNA表达,这些炎症介质包括在体内鉴定出的中性粒细胞吸引趋化因子。重要的是,我们发现,虽然P物质对感染细胞中的趋化因子mRNA表达没有影响,但这种神经肽显著增加了受金黄色葡萄球菌攻击的破骨细胞而非成骨细胞释放这些趋化因子的量。总之,这些数据进一步支持了P物质加剧金黄色葡萄球菌骨髓炎炎症损伤的能力,并表明这种作用可能部分归因于促进白细胞募集的破骨细胞免疫反应增强。