Department of Physical Medicine and Rehabilitation, School of Medicine, University of Pittsburgh, 3471 Fifth Avenue, Suite 910, Pittsburgh, PA, 15213, USA.
Safar Center for Resuscitation Research, John G. Rangos Research Center, Pittsburgh, PA, USA.
J Neuroinflammation. 2024 Jun 5;21(1):149. doi: 10.1186/s12974-024-03129-0.
Uncontrolled neuroinflammation mediates traumatic brain injury (TBI) pathology and impairs recovery. Interleukin-6 (IL-6), a pleiotropic inflammatory regulator, is associated with poor clinical TBI outcomes. IL-6 operates via classical-signaling through membrane-bound IL-6 receptor (IL-6R) and trans-signaling through soluble IL-6 receptor (s)IL-6R. IL-6 trans-signaling specifically contributes to neuropathology, making it a potential precision therapeutic TBI target. Soluble glycoprotein 130 (sgp130) prevents IL-6 trans-signaling, sparing classical signaling, thus is a possible treatment. Mice received either controlled cortical impact (CCI) (6.0 ± 0.2 m/s; 2 mm; 50-60ms) or sham procedures. Vehicle (VEH) or sgp130-Fc was subcutaneously administered to sham (VEH or 1 µg) and CCI (VEH, 0.25 µg or 1 µg) mice on days 1, 4, 7, 10 and 13 post-surgery to assess effects on cognition [Morris Water Maze (MWM)] and ipsilateral hemisphere IL-6 related biomarkers (day 21 post-surgery). CCI + sgp130-Fc groups (0.25 µg and 1 µg) were combined for analysis given similar behavior/biomarker outcomes. CCI + VEH mice had longer latencies and path lengths to the platform and increased peripheral zone time versus Sham + VEH and Sham + sgp130-Fc mice, suggesting injury-induced impairments in learning and anxiety. CCI + sgp130-Fc mice had shorter platform latencies and path lengths and had decreased peripheral zone time, indicating a therapeutic benefit of sgp130-Fc after injury on learning and anxiety. Interestingly, Sham + sgp130-Fc mice had shorter platform latencies, path lengths and peripheral zone times than Sham + VEH mice, suggesting a beneficial effect of sgp130-Fc, independent of injury. CCI + VEH mice had increased brain IL-6 and decreased sgp130 levels versus Sham + VEH and Sham + sgp130-Fc mice. There was no treatment effect on IL-6, sIL6-R or sgp130 in Sham + VEH versus Sham + sgp130-Fc mice. There was also no treatment effect on IL-6 in CCI + VEH versus CCI + sgp130-Fc mice. However, CCI + sgp130-Fc mice had increased sIL-6R and sgp130 versus CCI + VEH mice, demonstrating sgp130-Fc treatment effects on brain biomarkers. Inflammatory chemokines (MIP-1β, IP-10, MIG) were increased in CCI + VEH mice versus Sham + VEH and Sham + sgp130-Fc mice. However, CCI + sgp130-Fc mice had decreased chemokine levels versus CCI + VEH mice. IL-6 positively correlated, while sgp130 negatively correlated, with chemokine levels. Overall, we found that systemic sgp130-Fc treatment after CCI improved learning, decreased anxiety and reduced CCI-induced brain chemokines. Future studies will explore sex-specific dosing and treatment mechanisms for sgp130-Fc therapy.
未受控制的神经炎症介导创伤性脑损伤(TBI)病理,并损害恢复。白细胞介素-6(IL-6)是一种多效性炎症调节剂,与不良的临床 TBI 结果相关。IL-6 通过膜结合的 IL-6 受体(IL-6R)的经典信号转导和可溶性 IL-6 受体(s)IL-6R 的转信号转导发挥作用。IL-6 转信号转导特异性导致神经病理学,使其成为潜在的精准治疗 TBI 靶点。可溶性糖蛋白 130(sgp130)可防止 IL-6 转信号转导,保留经典信号转导,因此可能是一种治疗方法。小鼠接受了控制性皮质撞击(CCI)(6.0±0.2 m/s;2mm;50-60ms)或假手术。在手术后第 1、4、7、10 和 13 天,用载体(VEH)或 sgp130-Fc 对假手术(VEH 或 1μg)和 CCI(VEH、0.25μg 或 1μg)小鼠进行皮下给药,以评估对认知的影响[莫里斯水迷宫(MWM)]和同侧半球 IL-6 相关生物标志物(手术后第 21 天)。CCI+sgp130-Fc 组(0.25μg 和 1μg)因类似的行为/生物标志物结果而合并分析。与 Sham+VEH 和 Sham+sgp130-Fc 小鼠相比,CCI+VEH 小鼠的平台潜伏期和路径长度更长,外周区时间增加,表明损伤引起的学习和焦虑障碍。CCI+sgp130-Fc 小鼠的平台潜伏期和路径长度较短,外周区时间减少,表明 sgp130-Fc 在损伤后对学习和焦虑具有治疗益处。有趣的是,与 Sham+VEH 小鼠相比,Sham+sgp130-Fc 小鼠的平台潜伏期、路径长度和外周区时间更短,表明 sgp130-Fc 具有独立于损伤的有益作用。与 Sham+VEH 和 Sham+sgp130-Fc 小鼠相比,CCI+VEH 小鼠的脑内 IL-6 增加,sgp130 减少。Sham+VEH 与 Sham+sgp130-Fc 小鼠相比,IL-6、sIL6-R 或 sgp130 无治疗作用。CCI+VEH 与 CCI+sgp130-Fc 小鼠的 IL-6 也无治疗作用。然而,与 CCI+VEH 小鼠相比,CCI+sgp130-Fc 小鼠的 sIL-6R 和 sgp130 增加,表明 sgp130-Fc 对脑生物标志物有治疗作用。CCI+VEH 小鼠的炎症趋化因子(MIP-1β、IP-10、MIG)比 Sham+VEH 和 Sham+sgp130-Fc 小鼠增加。然而,与 CCI+VEH 小鼠相比,CCI+sgp130-Fc 小鼠的趋化因子水平降低。IL-6 与趋化因子水平呈正相关,而 sgp130 与趋化因子水平呈负相关。总体而言,我们发现 CCI 后系统性 sgp130-Fc 治疗可改善学习,减少焦虑并降低 CCI 引起的脑趋化因子。未来的研究将探索 sgp130-Fc 治疗的性别特异性剂量和治疗机制。