Cardiolipin Remodeling in Alzheimer’s Disease

NIH RePORTER · NIH · R01 · $339,063 · view on reporter.nih.gov ↗

Abstract

Aging causes bioenergetic dysfunction in the brain, which is implicated in the pathogenesis of Alzheimer’s disease (AD). Cardiolipin (CL) is a mitochondrial signature phospholipid that is essential for membrane structure, bioenergetics, and signaling pathways. Alterations in brain CL content and acyl compositions are implicated in the pathogenesis of neurodegenerative diseases, including AD and Parkinson’s disease (PD), but the underlying causes of these defects remain elusive. Here, we propose to investigate a novel metabolic pathway by which pathological remodeling of CL promotes the development of AD. This pathway is mediated by the ALCAT1 enzyme, the first acyl-CoA dependent lysocardiolipin acyltransferase previously identified by us. Our pioneering work in the field has identified ALCAT1 as a key mediator of mitochondrial dysfunction in age-related metabolic diseases. We show that upregulation of ALCAT1 expression by reactive oxygen species (ROS) generated by aging promotes mitochondrial dysfunction by catalyzing pathological remodeling of CL with long chain polyunsaturated fatty acids, such as docosahexaenoic acid (DHA). Enrichment of DHA renders CL highly sensitive to oxidative damage by ROS, leading to CL peroxidation and mitochondrial dysfunction. We further show that ablation or pharmacological inhibition of ALCAT1 successfully mitigates various age-related metabolic diseases. Remarkably, our preliminary studies also identified a critical role of ALCAT1 in linking aging to the development of AD, which is supported by our findings that: 1) ALCAT1 deficiency significantly extends lifespan in mice; 2) Ablation of ALCAT1 restores cognitive function and mitigates Aβ plague formation in a mouse model of AD; and 3) ALCAT1 deficiency attenuates neuroinflammation in response to Aβ protein aggregation. These exciting findings lead us to test the hypothesis that CL remodeling by ALCAT1 links aging to the development of AD by promoting mitochondrial dysfunction (Fig.1), which will be tested by three Specific Aims: AIM 1 will determine whether CL remodeling by ALCAT1 links mitochondrial dysfunction to AD; AIM 2 will identify mechanisms by which ALCAT1 promotes neuroinflammation in AD, and AIM 3 will provide proof-of-concept studies in targeting ALCAT1 for the treatment of AD.

Key facts

NIH application ID
10839908
Project number
5R01AG081422-02
Recipient
UNIVERSITY OF TEXAS HLTH SCIENCE CENTER
Principal Investigator
YUGUANG SHI
Activity code
R01
Funding institute
NIH
Fiscal year
2024
Award amount
$339,063
Award type
5
Project period
2023-05-15 → 2028-04-30