Loss of cannabinoid receptor 2 promotes α-Synuclein-induced microglial synaptic pruning in nucleus accumbens by modulating the pCREB-c-Fos signaling pathway and complement system

Experimental Neurology - Tập 359 - Trang 114230 - 2023
Linjuan Feng1,2,3,4, Hsuan Lo5, Hanlin You1,2,3,4, Wei Wu6, Xiaojuan Cheng1,2,3,4, Jiawei Xin1,2,3, Zucheng Ye6, Xiaochun Chen1,3,4, Xiaodong Pan1,2,3,4,6
1Department of Neurology, Center for Cognitive Neurology, Fujian Medical University Union Hospital, 29 Xinquan Road, Fuzhou 350001, China
2Fujian Institute of Geriatrics, Fujian Medical University Union Hospital, 29 Xinquan Road, Fuzhou 350001, China
3Institute of Clinical Neurology, Fujian Medical University, 29 Xinquan Road, Fuzhou 350001, China
4Fujian Key Laboratory of Molecular Neurology, Fujian Medical University, 88 Jiaotong Road, Fuzhou 350001, China
5Guangdong Cardiovascular Institute, Guangdong Provincial People's Hospital,Guangdong Academy of Medical Sciences, Guangzhou, Guangdong, China
6Key Laboratory of Brain Aging and Neurodegenerative Diseases, Fujian Medical University, 1 Xueyuan Road, Fuzhou 350001, China

Tài liệu tham khảo

Al-Hasani, 2021, Ventral tegmental area GABAergic inhibition of cholinergic interneurons in the ventral nucleus accumbens shell promotes reward reinforcement, Nat. Neurosci., 24, 1414, 10.1038/s41593-021-00898-2 Arcuri, 2017, The pathophysiological role of microglia in dynamic surveillance, phagocytosis and structural remodeling of the developing CNS, Front. Mol. Neurosci., 10, 191, 10.3389/fnmol.2017.00191 Bousset, 2013, Structural and functional characterization of two alpha-synuclein strains, Nat. Commun., 4, 2575, 10.1038/ncomms3575 Bridi, 2018, Mechanisms of α-Synuclein induced synaptopathy in Parkinson’s disease, Front. Neurosci., 12, 80, 10.3389/fnins.2018.00080 Bridi, 2021, Presynaptic accumulation of α-synuclein causes synaptopathy and progressive neurodegeneration in Drosophila, Brain Commun., 3, 1, 10.1093/braincomms/fcab049 Britt, 2012, Synaptic and behavioral profile of multiple glutamatergic inputs to the nucleus accumbens, Neuron, 76, 790, 10.1016/j.neuron.2012.09.040 Cachope, 2012, Selective activation of cholinergic interneurons enhances accumbal phasic dopamine release: setting the tone for reward processing, Cell Rep., 2, 33, 10.1016/j.celrep.2012.05.011 Carriere, 2014, Apathy in Parkinson’s disease is associated with nucleus accumbens atrophy: a magnetic resonance imaging shape analysis, Mov. Disord., 29, 897, 10.1002/mds.25904 Cassano, 2017, Cannabinoid receptor 2 signaling in neurodegenerative disorders: from pathogenesis to a promising therapeutic target, Front. Neurosci., 11, 30, 10.3389/fnins.2017.00030 Castro, 2019, A motivational and Neuropeptidergic hub: anatomical and functional diversity within the nucleus Accumbens Shell, Neuron, 102, 529, 10.1016/j.neuron.2019.03.003 Chaudhuri, 2006, Non-motor symptoms of Parkinson’s disease: diagnosis and management, Lancet Neurol., 5, 235, 10.1016/S1474-4422(06)70373-8 Cheng, 2019, HCN2 channels in cholinergic interneurons of nucleus accumbens shell regulate depressive behaviors, Neuron, 101, 662, 10.1016/j.neuron.2018.12.018 Choi, 2019, Amyloid β-induced elevation of O-GlcNAcylated c-Fos promotes neuronal cell death, Aging Cell, 18, 10.1111/acel.12872 Dhopeshwarkar, 2014, CB2 cannabinoid receptors as a therapeutic target-what does the future hold?, Mol. Pharmacol., 86, 430, 10.1124/mol.114.094649 Doorn, 2014, Microglial phenotypes and toll-like receptor 2 in the substantia nigra and hippocampus of incidental Lewy body disease cases and Parkinson’s disease patients, Acta Neuropathol. Commun., 2, 90 Du, 2017, Role of microglia in neurological disorders and their potentials as a therapeutic target, Mol. Neurobiol., 54, 7567, 10.1007/s12035-016-0245-0 Eun, 2004, Glutamate receptor-mediated regulation of c-fos expression in cultured microglia, Biochem. Biophys. Res. Commun., 325, 320, 10.1016/j.bbrc.2004.10.035 Fatoba, 2021, Complement cascade functions during brain development and neurodegeneration, FEBS J. Ferrer, 2012, Neurochemistry and the non-motor aspects of PD, Neurobiol. Dis., 46, 508, 10.1016/j.nbd.2011.10.019 Gandolfi, 2017, Activation of the CREB/c-Fos pathway during long-term synaptic plasticity in the cerebellum granular layer, Front. Cell. Neurosci., 11, 184, 10.3389/fncel.2017.00184 Gómez-Gálvez, 2016, Potential of the cannabinoid CB(2) receptor as a pharmacological target against inflammation in Parkinson’s disease, Prog. Neuro-Psychopharmacol. Biol. Psychiatry, 64, 200, 10.1016/j.pnpbp.2015.03.017 Guo, 2022, Microglia polarization from M1 to M2 in neurodegenerative diseases, Front. Aging Neurosci., 14, 10.3389/fnagi.2022.815347 Hanganu, 2014, Mild cognitive impairment is linked with faster rate of cortical thinning in patients with Parkinson’s disease longitudinally, Brain, 137, 1120, 10.1093/brain/awu036 Hong, 2016, Complement and microglia mediate early synapse loss in Alzheimer mouse models, Science, 352, 712, 10.1126/science.aad8373 Javed, 2016, Cannabinoid type 2 (CB2) receptors activation protects against oxidative stress and Neuroinflammation associated dopaminergic neurodegeneration in rotenone model of Parkinson’s disease, Front. Neurosci., 10, 321, 10.3389/fnins.2016.00321 Kim, 2013, Neuron-released oligomeric α-synuclein is an endogenous agonist of TLR2 for paracrine activation of microglia, Nat. Commun., 4, 1562, 10.1038/ncomms2534 Lee, 2008, Assembly-dependent endocytosis and clearance of extracellular alpha-synuclein, Int. J. Biochem. Cell Biol., 40, 1835, 10.1016/j.biocel.2008.01.017 Lee, 2019, MPTP-driven NLRP3 inflammasome activation in microglia plays a central role in dopaminergic neurodegeneration, Cell Death Differ., 26, 213, 10.1038/s41418-018-0124-5 Lee, 2020, Dopaminergic regulation of nucleus accumbens cholinergic interneurons demarcates susceptibility to cocaine addiction, Biol. Psychiatry, 88, 746, 10.1016/j.biopsych.2020.05.003 Li, 2018, Dexmedetomidine inhibits inflammation in microglia cells under stimulation of LPS and ATP by c-Fos/NLRP3/caspase-1 cascades, EXCLI J., 17, 302 Maresz, 2005, Modulation of the cannabinoid CB2 receptor in microglial cells in response to inflammatory stimuli, J. Neurochem., 95, 437, 10.1111/j.1471-4159.2005.03380.x Mohebi, 2019, Dissociable dopamine dynamics for learning and motivation, Nature, 570, 65, 10.1038/s41586-019-1235-y Pan, 2011, Microglial phagocytosis induced by fibrillar β-amyloid is attenuated by oligomeric β-amyloid: implications for Alzheimer’s disease, Mol. Neurodegener., 6, 45, 10.1186/1750-1326-6-45 Patterson, 2019, Degeneration of dopaminergic circuitry influences depressive symptoms in Lewy body disorders, Brain Pathol., 29, 544, 10.1111/bpa.12697 Sanchez-Guajardo, 2010, Microglia acquire distinct activation profiles depending on the degree of alpha-synuclein neuropathology in a rAAV based model of Parkinson's disease, PLoS One, 5, 10.1371/journal.pone.0008784 Sato, 2012, Interleukin-1 participates in the classical and alternative activation of microglia/macrophages after spinal cord injury, J. Neuroinflammation, 9, 65, 10.1186/1742-2094-9-65 Schaefer, 2005, The transcription factors AP-1 and Ets are regulators of C3a receptor expression, J. Biol. Chem., 280, 42113, 10.1074/jbc.M508146200 Schafer, 2012, Microglia sculpt postnatal neural circuits in an activity and complement-dependent manner, Neuron, 74, 691, 10.1016/j.neuron.2012.03.026 Scheiblich, 2021, Microglia jointly degrade fibrillar alpha-synuclein cargo by distribution through tunneling nanotubes, Cell, 184, 5089, 10.1016/j.cell.2021.09.007 Song, 2015, Brain-derived neurotrophic factor in Alzheimer’s disease: risk, mechanisms, and therapy, Mol. Neurobiol., 52, 1477, 10.1007/s12035-014-8958-4 Thomsen, 2021, PET imaging reveals early and progressive dopaminergic deficits after intra-striatal injection of preformed alpha-synuclein fibrils in rats, Neurobiol. Dis., 149, 10.1016/j.nbd.2020.105229 Volkow, 2017, The dopamine motive system: implications for drug and food addiction, Nat. Rev. Neurosci., 18, 741, 10.1038/nrn.2017.130 Weinhard, 2018, Microglia remodel synapses by presynaptic trogocytosis and spine head filopodia induction, Nat. Commun., 9, 1228, 10.1038/s41467-018-03566-5 Williams-Gray, 2013, The CamPaIGN study of Parkinson’s disease: 10-year outlook in an incident population-based cohort, J. Neurol. Neurosurg. Psychiatry, 84, 1258, 10.1136/jnnp-2013-305277 Witten, 2010, Cholinergic interneurons control local circuit activity and cocaine conditioning, Science, 330, 1677, 10.1126/science.1193771 Xiao, 2021, A new GABAergic somatostatin projection from the BNST onto accumbal parvalbumin neurons controls anxiety, Mol. Psychiatry, 26, 4719, 10.1038/s41380-020-0816-3 Xue, 2019, Aquaporin-4 deficiency reduces TGF-β1 in mouse midbrains and exacerbates pathology in experimental Parkinson’s disease, J. Cell. Mol. Med., 23, 2568, 10.1111/jcmm.14147 Yang, 2017, Resveratrol regulates microglia M1/M2 polarization via PGC-1α in conditions of neuroinflammatory injury, Brain Behav. Immun., 64, 162, 10.1016/j.bbi.2017.03.003 Zanier, 2014, Bone marrow mesenchymal stromal cells drive protective M2 microglia polarization after brain trauma, Neurotherapeutics, 11, 679, 10.1007/s13311-014-0277-y Zhang, 2005, Aggregated alpha-synuclein activates microglia: a process leading to disease progression in Parkinson’s disease, FASEB J., 19, 533, 10.1096/fj.04-2751com Zhang, 2020, MeCP2 in cholinergic interneurons of nucleus accumbens regulates fear learning, Elife, 9, 10.7554/eLife.55342 Zhang, 2020, MeCP2 in cholinergic interneurons of nucleus accumbens regulates fear learning, Elife, 9, 10.7554/eLife.55342 Zhang, 2021, Age-related LRRK2 G2019S mutation impacts microglial dopaminergic Fiber refinement and synaptic pruning involved in abnormal behaviors, J. Mol. Neurosci.