Rosas-Ballina Mauricio, Valdés-Ferrer Sergio I, Dancho Meghan E, Ochani Mahendar, Katz David, Cheng Kai Fan, Olofsson Peder S, Chavan Sangeeta S, Al-Abed Yousef, Tracey Kevin J, Pavlov Valentin A
Laboratory of Biomedical Science, Center for Biomedical Science, The Feinstein Institute for Medical Research, Manhasset, NY, United States.
Laboratory of Medicinal Chemistry, Center for Molecular Innovation, The Feinstein Institute for Medical Research, Manhasset, NY, United States.
Brain Behav Immun. 2015 Feb;44:19-27. doi: 10.1016/j.bbi.2014.07.010. Epub 2014 Jul 23.
Inflammatory conditions characterized by excessive immune cell activation and cytokine release, are associated with bidirectional immune system-brain communication, underlying sickness behavior and other physiological responses. The vagus nerve has an important role in this communication by conveying sensory information to the brain, and brain-derived immunoregulatory signals that suppress peripheral cytokine levels and inflammation. Brain muscarinic acetylcholine receptor (mAChR)-mediated cholinergic signaling has been implicated in this regulation. However, the possibility of controlling inflammation by peripheral administration of centrally-acting mAChR agonists is unexplored. To provide insight we used the centrally-acting M1 mAChR agonist xanomeline, previously developed in the context of Alzheimer's disease and schizophrenia. Intraperitoneal administration of xanomeline significantly suppressed serum and splenic TNF levels, alleviated sickness behavior, and increased survival during lethal murine endotoxemia. The anti-inflammatory effects of xanomeline were brain mAChR-mediated and required intact vagus nerve and splenic nerve signaling. The anti-inflammatory efficacy of xanomeline was retained for at least 20h, associated with alterations in splenic lymphocyte, and dendritic cell proportions, and decreased splenocyte responsiveness to endotoxin. These results highlight an important role of the M1 mAChR in a neural circuitry to spleen in which brain cholinergic activation lowers peripheral pro-inflammatory cytokines to levels favoring survival. The therapeutic efficacy of xanomeline was also manifested by significantly improved survival in preclinical settings of severe sepsis. These findings are of interest for strategizing novel therapeutic approaches in inflammatory diseases.
以免疫细胞过度激活和细胞因子释放为特征的炎症性疾病,与免疫系统和大脑之间的双向通讯有关,是疾病行为和其他生理反应的基础。迷走神经在这种通讯中起着重要作用,它将感觉信息传递到大脑,并传递大脑衍生的免疫调节信号,从而抑制外周细胞因子水平和炎症。大脑毒蕈碱型乙酰胆碱受体(mAChR)介导的胆碱能信号传导与这种调节有关。然而,通过外周给予中枢作用的mAChR激动剂来控制炎症的可能性尚未得到探索。为了深入了解这一情况,我们使用了中枢作用的M1 mAChR激动剂占诺美林,该激动剂先前是在阿尔茨海默病和精神分裂症的背景下开发的。腹腔注射占诺美林可显著抑制血清和脾脏中的肿瘤坏死因子水平,减轻疾病行为,并提高致死性小鼠内毒素血症期间的存活率。占诺美林的抗炎作用是由大脑mAChR介导的,并且需要完整的迷走神经和脾神经信号传导。占诺美林的抗炎功效至少持续20小时,这与脾脏淋巴细胞和树突状细胞比例的改变以及脾细胞对内毒素的反应性降低有关。这些结果突出了M1 mAChR在从大脑到脾脏的神经回路中的重要作用,其中大脑胆碱能激活将外周促炎细胞因子降低到有利于生存的水平。在严重脓毒症的临床前环境中,占诺美林的治疗效果还表现为存活率显著提高。这些发现对于制定炎症性疾病的新型治疗策略具有重要意义。