Liu Shunan, Song Yanyan, Zhang Ian Y, Zhang Leying, Gao Hang, Su Yanping, Yang Yihang, Yin Shi, Zheng Yawen, Ren Lyuzhi, Yin Hongwei Holly, Pillai Raju, Nath Aritro, Medina Eric F, Cosgrove Patrick A, Bild Andrea H, Badie Behnam
Institute of Translational Medicine, the First Hospital of Jilin University, Changchun, Jilin Province, People's Republic of China.
Department of Nephrology, The Second Hospital of Jilin University, Changchun, Jilin Province, People's Republic of China.
Neurotherapeutics. 2022 Mar;19(2):635-648. doi: 10.1007/s13311-022-01207-w. Epub 2022 Feb 28.
Resection of brain tumors frequently causes injury to the surrounding brain tissue that exacerbates cerebral edema by activating an inflammatory cascade. Although corticosteroids are often utilized peri-operatively to alleviate the symptoms associated with brain edema, they increase operative morbidities and suppress the efficacy of immunotherapy. Thus, novel approaches to minimize cerebral edema caused by neurosurgical procedures will have significant utility in the management of patients with brain tumors. We have studied the role of the receptor for advanced glycation end products (RAGE) and its ligands on inflammatory responses to neurosurgical injury in mice and humans. Blood-brain barrier (BBB) integrity and neuroinflammation were characterized by Nanostring, flow cytometry, qPCR, and immunoblotting of WT and RAGE knockout mice brains subjected to surgical brain injury (SBI). Human tumor tissue and fluid collected from the resection cavity of patients undergoing craniotomy were also analyzed by single-cell RNA sequencing and ELISA. Genetic ablation of RAGE significantly abrogated neuroinflammation and BBB disruption in the murine SBI model. The inflammatory responses to SBI were associated with infiltration of S100A9-expressing myeloid-derived cells into the brain. Local release of pro-inflammatory S100A9 was confirmed in patients following tumor resection. RAGE and S100A9 inhibitors were as effective as dexamethasone in attenuating neuroinflammation. However, unlike dexamethasone and S100A9 inhibitor, RAGE inhibition did not diminish the efficacy of anti-PD-1 immunotherapy in glioma-bearing mice. These observations confirm the role of the RAGE axis in surgically induced neuroinflammation and provide an alternative therapeutic option to dexamethasone in managing post-operative cerebral edema.
脑肿瘤切除术经常会损伤周围脑组织,通过激活炎症级联反应加剧脑水肿。尽管皮质类固醇经常在围手术期用于缓解与脑水肿相关的症状,但它们会增加手术并发症并抑制免疫治疗的疗效。因此,尽量减少神经外科手术引起的脑水肿的新方法在脑肿瘤患者的管理中将具有重要作用。我们研究了晚期糖基化终末产物受体(RAGE)及其配体在小鼠和人类对神经外科损伤的炎症反应中的作用。通过对遭受手术性脑损伤(SBI)的野生型和RAGE基因敲除小鼠的大脑进行纳米串分析、流式细胞术、qPCR和免疫印迹,来表征血脑屏障(BBB)的完整性和神经炎症。还通过单细胞RNA测序和ELISA分析了从接受开颅手术的患者切除腔中收集的人类肿瘤组织和液体。在小鼠SBI模型中,RAGE的基因消融显著消除了神经炎症和血脑屏障破坏。对SBI的炎症反应与表达S100A9的髓系来源细胞浸润到大脑有关。肿瘤切除术后患者体内证实了促炎因子S100A9的局部释放。RAGE和S100A9抑制剂在减轻神经炎症方面与地塞米松一样有效。然而,与地塞米松和S100A9抑制剂不同,抑制RAGE并没有降低抗PD-1免疫疗法在荷胶质瘤小鼠中的疗效。这些观察结果证实了RAGE轴在手术诱导的神经炎症中的作用,并为地塞米松在治疗术后脑水肿方面提供了一种替代治疗选择。