Vecchiarelli Haley A, Morena Maria, Keenan Catherine M, Chiang Vincent, Tan Kaitlyn, Qiao Min, Leitl Kira, Santori Alessia, Pittman Quentin J, Sharkey Keith A, Hill Matthew N
Neuroscience Graduate Program, University of Calgary, Calgary, AB, T2N4N1, Canada.
Hotchkiss Brain Institute, University of Calgary, Calgary, AB, T2N4N1, Canada.
Neuropsychopharmacology. 2021 Apr;46(5):992-1003. doi: 10.1038/s41386-020-00939-7. Epub 2021 Jan 15.
Peripheral inflammatory conditions, including those localized to the gastrointestinal tract, are highly comorbid with psychiatric disorders such as anxiety and depression. These behavioral symptoms are poorly managed by conventional treatments for inflammatory diseases and contribute to quality of life impairments. Peripheral inflammation is associated with sustained elevations in circulating glucocorticoid hormones, which can modulate central processes, including those involved in the regulation of emotional behavior. The endocannabinoid (eCB) system is exquisitely sensitive to these hormonal changes and is a significant regulator of emotional behavior. The impact of peripheral inflammation on central eCB function, and whether this is related to the development of these behavioral comorbidities remains to be determined. To examine this, we employed the trinitrobenzene sulfonic acid-induced model of colonic inflammation (colitis) in adult, male, Sprague Dawley rats to produce sustained peripheral inflammation. Colitis produced increases in behavioral measures of anxiety and elevations in circulating corticosterone. These alterations were accompanied by elevated hydrolytic activity of the enzyme fatty acid amide hydrolase (FAAH), which hydrolyzes the eCB anandamide (AEA), throughout multiple corticolimbic brain regions. This elevation of FAAH activity was associated with broad reductions in the content of AEA, whose decline was driven by central corticotropin releasing factor type 1 receptor signaling. Colitis-induced anxiety was reversed following acute central inhibition of FAAH, suggesting that the reductions in AEA produced by colitis contributed to the generation of anxiety. These data provide a novel perspective for the pharmacological management of psychiatric comorbidities of chronic inflammatory conditions through modulation of eCB signaling.
外周炎症性疾病,包括局限于胃肠道的疾病,与焦虑和抑郁等精神疾病高度共病。这些行为症状在炎症性疾病的传统治疗中难以得到有效控制,并会导致生活质量受损。外周炎症与循环糖皮质激素持续升高有关,而糖皮质激素可调节中枢过程,包括参与情绪行为调节的过程。内源性大麻素(eCB)系统对这些激素变化极为敏感,是情绪行为的重要调节因子。外周炎症对中枢eCB功能的影响,以及这是否与这些行为共病的发生有关,仍有待确定。为了研究这一问题,我们在成年雄性Sprague Dawley大鼠中采用三硝基苯磺酸诱导的结肠炎症(结肠炎)模型来产生持续的外周炎症。结肠炎导致焦虑行为指标增加以及循环皮质酮升高。这些改变伴随着脂肪酸酰胺水解酶(FAAH)水解活性的升高,FAAH可水解eCB花生四烯乙醇胺(AEA),在多个皮质边缘脑区均有这种情况。FAAH活性的升高与AEA含量的广泛降低有关,AEA含量的下降是由中枢促肾上腺皮质激素释放因子1型受体信号传导驱动的。急性中枢抑制FAAH后,结肠炎诱导的焦虑得到逆转,这表明结肠炎导致的AEA减少促成了焦虑的产生。这些数据为通过调节eCB信号传导对慢性炎症性疾病的精神共病进行药物管理提供了新的视角。