The Multiple Roles of α-Synuclein in the Pathology and Dopaminergic Neurodegeneration of Parkinson’s Disease
Tejaswi Veerati, MS, MPH
Introduction: Parkinson’s Disease (PD) is a movement disorder characterized by resting tremor, bradykinesia, and rigidity1. There is currently no diagnostic test for PD1. The neuropathology includes selective loss of dopaminergic neurons in the substantia nigra pars compacta and the deposition of misfolded α-synuclein (α-syn) aggregates in the midbrain1. Understanding mechanisms for abnormal aggregation of α-syn and the cell death mechanisms mediated by α-syn could lead to a neuroprotective therapy for PD. Methods: C57BL/6 WT and PARP-1 KO mice were used for in vivo intrastriatal injections of α-syn pre-formed fibrils (α-syn-PFF) and NO levels were measured. Lund human mesencephalic (LUHMES) neurons were differentiated to a dopaminergic phenotype and infected with recombinant AAV2 viruses to mediate expression of WT α-syn and mitochondria-tagged α-syn. Mitochondrial ROS quantification and caspase staining was performed. Thioflavin T Fluorescence Assay was performed on human dopaminergic neuroblastoma cells. Western blot analysis was performed on NLRP3 knockout mice. Plasma and CSF were collected from 75 PD patients receiving either 150, 200, 300, or 400 mg of Nilotinib or a placebo. Results: α-syn-PFF induces the activation of PARP-1 and causes PARP-1 mediated cell death of dopaminergic neurons via NO-induced DNA damage2. PAR causes a more misfolded, toxic form of α-syn-PFF2. Dopaminergic neurons expressing WT α-syn and mitochondria-targeted α-syn had an increase in mitochondrial ROS formation and caspase activation3. Neuronal cells treated with inflammasome activators had truncated α-syn which was reversed with a caspase-1 inhibitor4. Further, truncated α-syn generated by caspase-1 is more aggregation-prone4. Fibrillar α-syn mediated a delayed activation of the inflammasome pathway in microglia and the presence of caspase-1, IL-1B and ASC5. In NLRP3 knockout mice, α-syn could not stimulate release of caspase-1, IL-1B, or ASC from microglia5. Soluble TREM2 was increased in CSF of patients treated with 150 mg and 200 mg of Nilotinib6. Plasma total α-syn was significantly reduced in the 150 mg group6. Conclusions: α-syn-PFF kills dopaminergic neurons via a PARP-1 mediated pathway. Dopaminergic neurons expressing α-syn caused damage to mitochondrial structural/functional and caspase activation. Caspase-1 plays a direct role in the truncation of α-syn, causing aggregation and neuronal cell toxicity. Fibrillar α-syn induces NLRP3 inflammasome pathways driving the neurodegeneration seen in PD through caspase-1 and ASC release. Nilotinib decreases total plasma α-syn and provides an anti-inflammatory effect by triggering TREM2 receptors on myeloid cells. Thus, α-syn is capable of mediating dopaminergic neuron loss via multiple mechanisms, including inflammation and mitochondrial dysfunction.
- Cacabelos R. Parkinson’s Disease: From Pathogenesis to Pharmacogenomics. Int J Mol Sci. 2017;18(3):551. Published 2017 Mar 4. doi:10.3390/ijms18030551
- Kam TI, Mao X, Park H, et al. Poly(ADP-ribose) drives pathologic α-synuclein neurodegeneration in Parkinson’s disease. Science. 2018;362(6414):eaat8407. doi:10.1126/science.aat8407
- Ganjam GK, Bolte K, Matschke LA, et al. Mitochondrial damage by α-synuclein causes cell death in human dopaminergic neurons. Cell Death Dis. 2019;10(11):865. Published 2019 Nov 14. doi:10.1038/s41419-019-2091-2
- Wang W, Nguyen LT, Burlak C, et al. Caspase-1 causes truncation and aggregation of the Parkinson’s disease-associated protein α-synuclein. Proc Natl Acad Sci U S A. 2016;113(34):9587-9592. doi:10.1073/pnas.1610099113
- Gordon R, Albornoz EA, Christie DC, et al. Inflammasome inhibition prevents α-synuclein pathology and dopaminergic neurodegeneration in mice. Sci Transl Med. 2018;10(465):eaah4066. doi:10.1126/scitranslmed.aah4066
- Pagan FL, Hebron ML, Wilmarth B, et al. Pharmacokinetics and pharmacodynamics of a single dose Nilotinib in individuals with Parkinson’s disease. Pharmacol Res Perspect. 2019;7(2):e00470. Published 2019 Mar 12. doi:10.1002/prp2.470