Matera Alessandro, Compagnion Anne-Claire, Pedicone Chiara, Kotah Janssen M, Ivanov Andranik, Monsorno Katia, Labouèbe Gwenaël, Leggio Loredana, Pereira-Iglesias Marta, Beule Dieter, Mansuy-Aubert Virginie, Williams Tim L, Iraci Nunzio, Sierra Amanda, Marro Samuele G, Goate Alison M, Eggen Bart J L, Kerr William G, Paolicelli Rosa C
Department of Biomedical Sciences, University of Lausanne, Lausanne, Switzerland.
Department of Genetics and Genomics Sciences, Icahn School of Medicine at Mt. Sinai, New York, NY, USA; Ronald M. Loeb Center for Alzheimer's Disease, Icahn School of Medicine at Mount Sinai, New York, NY, USA.
Immunity. 2025 Jan 14;58(1):197-217.e13. doi: 10.1016/j.immuni.2024.11.003. Epub 2024 Dec 9.
The gene inositol polyphosphate-5-phosphatase D (INPP5D), which encodes the lipid phosphatase SH2-containing inositol polyphosphate 5-phosphatase 1 (SHIP1), is associated with the risk of Alzheimer's disease (AD). How it influences microglial function and brain physiology is unclear. Here, we showed that SHIP1 was enriched in early stages of healthy brain development. By combining in vivo loss-of-function approaches and proteomics, we discovered that mice conditionally lacking microglial SHIP1 displayed increased complement and synapse loss in the early postnatal brain. SHIP1-deficient microglia showed altered transcriptional signatures and abnormal synaptic pruning that was dependent on the complement system. Mice exhibited cognitive defects in adulthood only when microglial SHIP1 was depleted early postnatally but not at later stages. Induced pluripotent stem cell (iPSC)-derived microglia lacking SHIP1 also showed increased engulfment of synaptic structures. These findings suggest that SHIP1 is essential for proper microglia-mediated synapse remodeling in the healthy developing brain. Disrupting this process has lasting behavioral effects and may be linked to vulnerability to neurodegeneration.
编码含SH2结构域的肌醇多磷酸5-磷酸酶1(SHIP1)的肌醇多磷酸-5-磷酸酶D(INPP5D)基因与阿尔茨海默病(AD)风险相关。其如何影响小胶质细胞功能和脑生理学尚不清楚。在此,我们表明SHIP1在健康脑发育的早期阶段富集。通过结合体内功能丧失方法和蛋白质组学,我们发现条件性缺乏小胶质细胞SHIP1的小鼠在出生后早期脑内补体增加且突触丢失。SHIP1缺陷的小胶质细胞表现出转录特征改变和依赖于补体系统的异常突触修剪。仅在出生后早期而非后期耗尽小胶质细胞SHIP1时,小鼠在成年期才表现出认知缺陷。缺乏SHIP1的诱导多能干细胞(iPSC)衍生的小胶质细胞也表现出对突触结构吞噬增加。这些发现表明SHIP1对于健康发育脑中小胶质细胞介导的适当突触重塑至关重要。破坏这一过程具有持久的行为影响,并且可能与神经退行性变易感性相关。