Prions induce an early Arc response and a subsequent reduction in mGluR5 in the hippocampus

Neurobiology of Disease - Tập 172 - Trang 105834 - 2022
Daniel Ojeda-Juárez1, Jessica A. Lawrence1, Katrin Soldau1, Donald P. Pizzo1, Emily Wheeler2, Patricia Aguilar-Calvo1, Helen Khuu1, Joy Chen1, Adela Malik1, Gail Funk1, Percival Nam3, Henry Sanchez4, Michael D. Geschwind5, Chengbiao Wu6, Gene W. Yeo2, Xu Chen7, Gentry N. Patrick8, Christina J. Sigurdson1,9,10
1Department of Pathology; University of California San Diego; La Jolla, CA USA.
2Department of Cellular and Molecular Medicine, University of California, San Diego, La Jolla, CA, USA
3Department of Pathology, University of California San Diego, La Jolla, CA, USA
4Department of Pathology, Division of Neuropathology, University of California San Francisco, San Francisco, CA, USA
5Department of Neurology, Weill Institute for Neurosciences, Memory and Aging Center, University of California San Francisco, San Francisco, CA, USA
6Department of Neurosciences, University of California–San Diego, La Jolla, CA, USA;
7Department of Neurosciences, University of California, San Diego, La Jolla, CA, USA
8Division of Biological Sciences, Section of Neurobiology, University of California San Diego, La Jolla, CA, USA
9Department of Medicine, University of California San Diego, La Jolla, CA, USA
10Department of Pathology, Microbiology and Immunology, University of California Davis, Davis, CA, USA

Tài liệu tham khảo

Banke, 2000, Control of GluR1 AMPA receptor function by cAMP-dependent protein kinase, J. Neurosci., 20, 89, 10.1523/JNEUROSCI.20-01-00089.2000 Belichenko, 2000, Dendritic and synaptic alterations of hippocampal pyramidal neurones in scrapie-infected mice, Neuropathol. Appl. Neurobiol., 26, 143, 10.1046/j.1365-2990.2000.026002143.x Bounhar, 2001, Prion protein protects human neurons against Bax-mediated apoptosis, J. Biol. Chem., 276, 39145, 10.1074/jbc.C100443200 Bourgognon, 2021, Inhibition of neuroinflammatory nitric oxide signaling suppresses glycation and prevents neuronal dysfunction in mouse prion disease, Proc. Natl. Acad. Sci. U. S. A., 118, 10.1073/pnas.2009579118 Bremer, 2010, Axonal prion protein is required for peripheral myelin maintenance, Nat. Neurosci., 13, 310, 10.1038/nn.2483 Brown, 2001, Early loss of dendritic spines in murine scrapie revealed by confocal analysis, Neuroreport., 12, 179, 10.1097/00001756-200101220-00043 Carroll, 2020, RNA-seq and network analysis reveal unique glial gene expression signatures during prion infection, Mol. Brain., 13, 71, 10.1186/s13041-020-00610-8 Caughey, 1991, The scrapie-associated form of Prp is made from a cell-surface precursor that is both protease-sensitive and phospholipase-sensitive, J. Biol. Chem., 266, 18217, 10.1016/S0021-9258(18)55257-1 Chowdhury, 2006, Arc/Arg3.1 interacts with the endocytic machinery to regulate AMPA receptor trafficking, Neuron., 52, 445, 10.1016/j.neuron.2006.08.033 Collinge, 2016, Mammalian prions and their wider relevance in neurodegenerative diseases, Nature., 539, 217, 10.1038/nature20415 Cunningham, 2003, Synaptic changes characterize early behavioural signs in the ME7 model of murine prion disease, Eur. J. Neurosci., 17, 2147, 10.1046/j.1460-9568.2003.02662.x Cunningham, 2005, Neuropathologically distinct prion strains give rise to similar temporal profiles of behavioral deficits, Neurobiol. Dis., 18, 258, 10.1016/j.nbd.2004.08.015 Diering, 2014, PKA-GluA1 coupling via AKAP5 controls AMPA receptor phosphorylation and cell-surface targeting during bidirectional homeostatic plasticity, Neuron., 84, 790, 10.1016/j.neuron.2014.09.024 Ehlers, 2000, Reinsertion or degradation of AMPA receptors determined by activity-dependent endocytic sorting, Neuron., 28, 511, 10.1016/S0896-6273(00)00129-X Esteban, 2003, PKA phosphorylation of AMPA receptor subunits controls synaptic trafficking underlying plasticity, Nat. Neurosci., 6, 136, 10.1038/nn997 Fang, 2016, A neuronal culture system to detect prion Synaptotoxicity, PLoS Pathog., 12, 10.1371/journal.ppat.1005623 Fang, 2018, Prions activate a p38 MAPK synaptotoxic signaling pathway, PLoS Pathog., 14, 10.1371/journal.ppat.1007283 Ferrer, 2002, Synaptic pathology and cell death in the cerebellum in Creutzfeldt-Jakob disease, Cerebellum., 1, 213, 10.1080/14734220260418448 Fu, 2011, Experience-dependent structural plasticity in the cortex, Trends Neurosci., 34, 177, 10.1016/j.tins.2011.02.001 Godsave, 2008, Cryo-immunogold electron microscopy for prions: toward identification of a conversion site, J. Neurosci., 28, 12489, 10.1523/JNEUROSCI.4474-08.2008 Goniotaki, 2017, Inhibition of group-I metabotropic glutamate receptors protects against prion toxicity, PLoS Pathog., 13, 10.1371/journal.ppat.1006733 Gray, 2009, Selective presynaptic degeneration in the synaptopathy associated with ME7-induced hippocampal pathology, Neurobiol. Dis., 35, 63, 10.1016/j.nbd.2009.04.001 Haas, 2014, Therapeutic molecules and endogenous ligands regulate the interaction between brain cellular prion protein (PrPC) and metabotropic glutamate receptor 5 (mGluR5), J. Biol. Chem., 289, 28460, 10.1074/jbc.M114.584342 Haas, 2016, Metabotropic glutamate receptor 5 couples cellular prion protein to intracellular signalling in Alzheimer’s disease, Brain., 139, 526, 10.1093/brain/awv356 Herms, 1999, Evidence of presynaptic location and function of the prion protein, J. Neurosci., 19, 8866, 10.1523/JNEUROSCI.19-20-08866.1999 Herrmann, 2015, Prion infections and anti-PrP antibodies trigger converging neurotoxic pathways, PLoS Pathog., 11 Hilton, 2013, Early hippocampal synaptic loss precedes neuronal loss and associates with early behavioural deficits in three distinct strains of prion disease, PLoS One, 8, 10.1371/journal.pone.0068062 Huang, 2021, Mutation of copper binding sites on cellular prion protein abolishes its inhibitory action on NMDA receptors in mouse hippocampal neurons, Mol. Brain., 14, 117, 10.1186/s13041-021-00828-0 Hwang, 2009, A systems approach to prion disease, Mol. Syst. Biol., 5, 252, 10.1038/msb.2009.10 Jeffrey, 2000, Synapse loss associated with abnormal PrP precedes neuronal degeneration in the scrapie-infected murine hippocampus, Neuropathol. Appl. Neurobiol., 26, 41, 10.1046/j.1365-2990.2000.00216.x Khosravani, 2008, Prion protein attenuates excitotoxicity by inhibiting NMDA receptors, J. Cell Biol., 181, 551, 10.1083/jcb.200711002 Kim, 2014, Calcineurin mediates synaptic scaling via synaptic trafficking of Ca2+−permeable AMPA receptors, PLoS Biol., 12, 10.1371/journal.pbio.1001900 Ko, 2012, PKC phosphorylation regulates mGluR5 trafficking by enhancing binding of Siah-1A, J. Neurosci., 32, 16391, 10.1523/JNEUROSCI.1964-12.2012 Korb, 2011, Arc in synaptic plasticity: from gene to behavior, Trends Neurosci., 34, 591, 10.1016/j.tins.2011.08.007 Kuffer, 2016, The prion protein is an agonistic ligand of the G protein-coupled receptor Adgrg6, Nature., 536, 464, 10.1038/nature19312 Lee, 2000, Regulation of distinct AMPA receptor phosphorylation sites during bidirectional synaptic plasticity, Nature., 405, 955, 10.1038/35016089 Lee, 2003, Phosphorylation of the AMPA receptor GluR1 subunit is required for synaptic plasticity and retention of spatial memory, Cell., 112, 631, 10.1016/S0092-8674(03)00122-3 Majer, 2012, Early mechanisms of pathobiology are revealed by transcriptional temporal dynamics in hippocampal CA1 neurons of prion infected mice, PLoS Pathog., 8, 10.1371/journal.ppat.1003002 Man, 2007, Regulation of {alpha}-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor trafficking through PKA phosphorylation of the Glu receptor 1 subunit, Proc. Natl. Acad. Sci. U. S. A., 104, 3579, 10.1073/pnas.0611698104 Mantuano, 2020, A soluble derivative of PrP(C) activates cell-signaling and regulates cell physiology through LRP1 and the NMDA receptor, J. Biol. Chem., 295, 14178, 10.1074/jbc.RA120.013779 Mecca, 2021, Effect of age on brain metabotropic glutamate receptor subtype 5 measured with [(18)F]FPEB PET, Neuroimage., 238, 10.1016/j.neuroimage.2021.118217 Moreno, 2012, Sustained translational repression by eIF2alpha-P mediates prion neurodegeneration, Nature., 485, 507, 10.1038/nature11058 Moriyoshi, 2004, Seven in absentia homolog 1A mediates ubiquitination and degradation of group 1 metabotropic glutamate receptors, Proc. Natl. Acad. Sci. U. S. A., 101, 8614, 10.1073/pnas.0403042101 Moya, 2000, Immunolocalization of the cellular prion protein in normal brain, Microsc. Res. Tech., 50, 58, 10.1002/1097-0029(20000701)50:1<58::AID-JEMT9>3.0.CO;2-5 Oh, 2006, Extrasynaptic membrane trafficking regulated by GluR1 serine 845 phosphorylation primes AMPA receptors for long-term potentiation, J. Biol. Chem., 281, 752, 10.1074/jbc.M509677200 Ojeda-Juarez, 2020, Lipocalin-2 mediates HIV-1 induced neuronal injury and behavioral deficits by overriding CCR5-dependent protection, Brain Behav. Immun., 89, 184, 10.1016/j.bbi.2020.06.016 Okuno, 2018, Inverse synaptic tagging: an inactive synapse-specific mechanism to capture activity-induced Arc/arg3.1 and to locally regulate spatial distribution of synaptic weights, Semin. Cell Dev. Biol., 77, 43, 10.1016/j.semcdb.2017.09.025 Orru, 2018, Prion seeds distribute throughout the eyes of sporadic creutzfeldt-jakob disease patients, mBio, 9, 10.1128/mBio.02095-18 Pan, 1993, Conversion of alpha-helices into beta-sheets features in the formation of the scrapie prion proteins, Proc. Natl. Acad. Sci. U. S. A., 90, 10962, 10.1073/pnas.90.23.10962 Park, 2008, Elongation factor 2 and fragile X mental retardation protein control the dynamic translation of arc/Arg3.1 essential for mGluR-LTD, Neuron., 59, 70, 10.1016/j.neuron.2008.05.023 Peebles, 2010, Arc regulates spine morphology and maintains network stability in vivo, Proc. Natl. Acad. Sci. U. S. A., 107, 18173, 10.1073/pnas.1006546107 Polymenidou, 2008, The POM monoclonals: a comprehensive set of antibodies to non-overlapping prion protein epitopes, PLoS One, 3, 10.1371/journal.pone.0003872 Prusiner, 1982, Novel proteinaceous infectious particles cause scrapie, Science., 216, 136, 10.1126/science.6801762 Prusiner, 1991, Molecular biology of prion diseases, Science., 252, 1515, 10.1126/science.1675487 Roucou, 2005, Cellular prion protein inhibits proapoptotic Bax conformational change in human neurons and in breast carcinoma MCF-7 cells, Cell Death Differ., 12, 783, 10.1038/sj.cdd.4401629 Santuccione, 2005, Prion protein recruits its neuronal receptor NCAM to lipid rafts to activate p59fyn and to enhance neurite outgrowth, J. Cell Biol., 169, 341, 10.1083/jcb.200409127 Schmitt-Ulms, 2001, Binding of neural cell adhesion molecules (N-CAMs) to the cellular prion protein, J. Mol. Biol., 314, 1209, 10.1006/jmbi.2000.5183 Shepherd, 2011, New views of Arc, a master regulator of synaptic plasticity, Nat. Neurosci., 14, 279, 10.1038/nn.2708 Shepherd, 2006, Arc/Arg3.1 mediates homeostatic synaptic scaling of AMPA receptors, Neuron., 52, 475, 10.1016/j.neuron.2006.08.034 Siskova, 2013, Brain region specific pre-synaptic and post-synaptic degeneration are early components of neuropathology in prion disease, PLoS One, 8, 10.1371/journal.pone.0055004 Sorce, 2020, Genome-wide transcriptomics identifies an early preclinical signature of prion infection, PLoS Pathog., 16, 10.1371/journal.ppat.1008653 Steward, 2001, Selective targeting of newly synthesized Arc mRNA to active synapses requires NMDA receptor activation, Neuron., 30, 227, 10.1016/S0896-6273(01)00275-6 Tee, 2018, Prion diseases, Neurol. Clin., 36, 865, 10.1016/j.ncl.2018.07.005 Um, 2012, Alzheimer amyloid-beta oligomer bound to postsynaptic prion protein activates Fyn to impair neurons, Nat. Neurosci., 15, 1227, 10.1038/nn.3178 Um, 2013, Metabotropic glutamate receptor 5 is a coreceptor for Alzheimer abeta oligomer bound to cellular prion protein, Neuron., 79, 887, 10.1016/j.neuron.2013.06.036 Vincenti, 2015, Defining the microglia response during the time course of chronic neurodegeneration, J. Virol., 90, 3003, 10.1128/JVI.02613-15 Wadsworth, 2001, Tissue distribution of protease resistant prion protein in variant CJD using a highly sensitive immuno-blotting assay, Lancet., 358, 171, 10.1016/S0140-6736(01)05403-4 Waung, 2008, Rapid translation of Arc/Arg3.1 selectively mediates mGluR-dependent LTD through persistent increases in AMPAR endocytosis rate, Neuron., 59, 84, 10.1016/j.neuron.2008.05.014 Wilkerson, 2014, A role for dendritic mGluR5-mediated local translation of Arc/Arg3.1 in MEF2-dependent synapse elimination, Cell Rep., 7, 1589, 10.1016/j.celrep.2014.04.035 Wilkerson, 2018, Roles for arc in metabotropic glutamate receptor-dependent LTD and synapse elimination: implications in health and disease, Semin. Cell Dev. Biol., 77, 51, 10.1016/j.semcdb.2017.09.035 You, 2012, Abeta neurotoxicity depends on interactions between copper ions, prion protein, and N-methyl-D-aspartate receptors, Proc. Natl. Acad. Sci. U. S. A., 109, 1737, 10.1073/pnas.1110789109 Zhang, 2015, Structural basis of arc binding to synaptic proteins: implications for cognitive disease, Neuron., 86, 490, 10.1016/j.neuron.2015.03.030 Zhang, 2019, Arc oligomerization is regulated by CaMKII phosphorylation of the GAG domain: an essential mechanism for plasticity and memory formation, Mol. Cell, 75