Koh Yeojung, Vázquez-Rosa Edwin, Gao Farrah, Li Hongyun, Chakraborty Suwarna, Tripathi Sunil Jamuna, Barker Sarah, Bud Zea, Bangalore Anusha, Kandjoze Uapingena P, León-Alvarado Rose A, Sridharan Preethy S, Cordova Brittany A, Yu Youngmin, Hyung Jiwon, Fang Hua, Singh Salendra, Katabathula Ramachandra, LaFramboise Thomas, Kasturi Lakshmi, Lutterbaugh James, Beard Lydia, Cordova Erika, Cintrón-Pérez Coral J, Franke Kathryn, Fragoso Mariana Franco, Miller Emiko, Indrakumar Vidya, Noel Kamryn L, Dhar Matasha, Ajroud Kaouther, Zamudio Carlos, Lopes Filipa Blasco Tavares Pereira, Bambakidis Evangeline, Zhu Xiongwei, Wilson Brigid, Flanagan Margaret E, Gefen Tamar, Fujioka Hisashi, Fink Stephen P, Desai Amar B, Dawson Dawn, Williams Noelle S, Kim Young-Kwang, Ready Joseph M, Paul Bindu D, Shin Min-Kyoo, Markowitz Sanford D, Pieper Andrew A
Department of Psychiatry, School of Medicine, Case Western Reserve University, Cleveland, OH 44106.
Brain Health Medicines Center, Harrington Discovery Institute, University Hospitals, Cleveland Medical Center, Cleveland, OH 44106.
Proc Natl Acad Sci U S A. 2025 May 27;122(21):e2417224122. doi: 10.1073/pnas.2417224122. Epub 2025 May 21.
Alzheimer's disease (AD) and traumatic brain injury (TBI) are currently untreatable neurodegenerative disorders afflicting millions of people worldwide. These conditions are pathologically related, and TBI is one of the greatest risk factors for AD. Although blood-brain barrier (BBB) disruption drives progression of both AD and TBI, strategies to preserve BBB integrity have been hindered by lack of actionable targets. Here, we identify 15-hydroxyprostaglandin dehydrogenase (15-PGDH), an enzyme that catabolizes eicosanoids and other anti-inflammatory mediators, as a therapeutic candidate that protects the BBB. We demonstrate that 15-PGDH is enriched in BBB-associated myeloid cells and becomes markedly elevated in human and mouse models of AD and TBI, as well as aging, another major risk factor for AD. Pathological increase in 15-PGDH correlates with pronounced oxidative stress, neuroinflammation, and neurodegeneration, alongside profound BBB structural degeneration characterized by astrocytic endfeet swelling and functional impairment. Pharmacologic inhibition or genetic reduction of 15-PGDH in AD and TBI models strikingly mitigates oxidative damage, suppresses neuroinflammation, and restores BBB integrity. Most notably, inhibiting 15-PGDH not only halts neurodegeneration but also preserves cognitive function at levels indistinguishable from healthy controls. Remarkably, these neuroprotective effects in AD are achieved without affecting amyloid pathology, underscoring a noncanonical mechanism for treating AD. In a murine microglia cell line exposed to amyloid beta oligomer, major protection was demonstrated by multiple anti-inflammatory substrates that 15-PGDH degrades. Thus, our findings position 15-PGDH inhibition as a broad-spectrum strategy to protect the BBB and thereby preserve brain health and cognition in AD and TBI.
阿尔茨海默病(AD)和创伤性脑损伤(TBI)是目前无法治愈的神经退行性疾病,全球数以百万计的人深受其害。这些病症在病理上相关,而TBI是AD最大的风险因素之一。尽管血脑屏障(BBB)破坏推动了AD和TBI的进展,但由于缺乏可操作的靶点,保护BBB完整性的策略受到了阻碍。在这里,我们确定15-羟基前列腺素脱氢酶(15-PGDH),一种分解类花生酸和其他抗炎介质的酶,作为保护BBB的治疗候选物。我们证明15-PGDH在与BBB相关的髓样细胞中富集,并且在AD和TBI的人类和小鼠模型以及衰老(AD的另一个主要风险因素)中显著升高。15-PGDH的病理性增加与明显的氧化应激、神经炎症和神经退行性变相关,同时伴有以星形胶质细胞终足肿胀和功能障碍为特征的严重BBB结构退化。在AD和TBI模型中对15-PGDH进行药理抑制或基因敲低可显著减轻氧化损伤、抑制神经炎症并恢复BBB完整性。最值得注意的是,抑制15-PGDH不仅能阻止神经退行性变,还能将认知功能维持在与健康对照难以区分的水平。值得注意的是,在AD中实现这些神经保护作用时不会影响淀粉样蛋白病理学,这突出了一种治疗AD的非经典机制。在暴露于淀粉样β寡聚体的小鼠小胶质细胞系中,15-PGDH降解的多种抗炎底物显示出主要的保护作用。因此,我们的研究结果将抑制15-PGDH定位为一种广谱策略,以保护BBB,从而在AD和TBI中维持脑健康和认知。