Formation of memory assemblies through the DNA-sensing TLR9 pathway.
Journal
Nature
ISSN: 1476-4687
Titre abrégé: Nature
Pays: England
ID NLM: 0410462
Informations de publication
Date de publication:
27 Mar 2024
27 Mar 2024
Historique:
received:
29
11
2022
accepted:
21
02
2024
medline:
28
3
2024
pubmed:
28
3
2024
entrez:
28
3
2024
Statut:
aheadofprint
Résumé
As hippocampal neurons respond to diverse types of information
Identifiants
pubmed: 38538785
doi: 10.1038/s41586-024-07220-7
pii: 10.1038/s41586-024-07220-7
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2024. The Author(s).
Références
McKenzie, S. et al. Hippocampal representation of related and opposing memories develop within distinct, hierarchically organized neural schemas. Neuron 83, 202–215 (2014).
pubmed: 24910078
pmcid: 4082468
doi: 10.1016/j.neuron.2014.05.019
Terada, S. et al. Adaptive stimulus selection for consolidation in the hippocampus. Nature 601, 240–244 (2022).
pubmed: 34880499
doi: 10.1038/s41586-021-04118-6
Crowe, S. L., Movsesyan, V. A., Jorgensen, T. J. & Kondratyev, A. Rapid phosphorylation of histone H2A.X following ionotropic glutamate receptor activation. Eur. J. Neurosci. 23, 2351–2361 (2006).
pubmed: 16706843
pmcid: 1534119
doi: 10.1111/j.1460-9568.2006.04768.x
Suberbielle, E. et al. Physiologic brain activity causes DNA double-strand breaks in neurons, with exacerbation by amyloid-beta. Nat. Neurosci. 16, 613–621 (2013).
pubmed: 23525040
pmcid: 3637871
doi: 10.1038/nn.3356
Madabhushi, R. et al. Activity-induced DNA breaks govern the expression of neuronal early-response genes. Cell 161, 1592–1605 (2015).
pubmed: 26052046
pmcid: 4886855
doi: 10.1016/j.cell.2015.05.032
Mullee, L. I. & Morrison, C. G. Centrosomes in the DNA damage response—the hub outside the centre. Chromosome Res. 24, 35–51 (2016).
pubmed: 26614090
doi: 10.1007/s10577-015-9503-7
Nicoll, R. A. A brief history of long-term potentiation. Neuron 93, 281–290 (2017).
pubmed: 28103477
doi: 10.1016/j.neuron.2016.12.015
Santini, E., Huynh, T. N. & Klann, E. Mechanisms of translation control underlying long-lasting synaptic plasticity and the consolidation of long-term memory. Prog. Mol. Biol. Transl. Sci. 122, 131–167 (2014).
pubmed: 24484700
pmcid: 6019682
doi: 10.1016/B978-0-12-420170-5.00005-2
Bailey, C. H., Kandel, E. R. & Harris, K. M. Structural components of synaptic plasticity and memory consolidation. Cold Spring Harb. Perspect. Biol. 7, a021758 (2015).
pubmed: 26134321
pmcid: 4484970
doi: 10.1101/cshperspect.a021758
Farooq, U. & Dragoi, G. Emergence of preconfigured and plastic time-compressed sequences in early postnatal development. Science 363, 168–173 (2019).
pubmed: 30630930
pmcid: 6794005
doi: 10.1126/science.aav0502
Han, J. H. et al. Neuronal competition and selection during memory formation. Science 316, 457–460 (2007).
pubmed: 17446403
doi: 10.1126/science.1139438
Deguchi, Y., Donato, F., Galimberti, I., Cabuy, E. & Caroni, P. Temporally matched subpopulations of selectively interconnected principal neurons in the hippocampus. Nat. Neurosci. 14, 495–504 (2011).
pubmed: 21358645
doi: 10.1038/nn.2768
Huszar, R., Zhang, Y., Blockus, H. & Buzsaki, G. Preconfigured dynamics in the hippocampus are guided by embryonic birthdate and rate of neurogenesis. Nat. Neurosci. 25, 1201–1212 (2022).
pubmed: 35995878
pmcid: 10807234
doi: 10.1038/s41593-022-01138-x
Gogolla, N., Caroni, P., Luthi, A. & Herry, C. Perineuronal nets protect fear memories from erasure. Science 325, 1258–1261 (2009).
pubmed: 19729657
doi: 10.1126/science.1174146
Yu, H. et al. Tet3 regulates synaptic transmission and homeostatic plasticity via DNA oxidation and repair. Nat. Neurosci. 18, 836–843 (2015).
pubmed: 25915473
pmcid: 4446239
doi: 10.1038/nn.4008
Rao-Ruiz, P. et al. Engram-specific transcriptome profiling of contextual memory consolidation. Nat. Commun. 10, 2232 (2019).
pubmed: 31110186
pmcid: 6527697
doi: 10.1038/s41467-019-09960-x
Jovasevic, V. et al. Primary cilia are required for the persistence of memory and stabilization of perineuronal nets. iScience 24, 102617 (2021).
pubmed: 34142063
pmcid: 8185192
doi: 10.1016/j.isci.2021.102617
Kawai, T. & Akira, S. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat. Immunol. 11, 373–384 (2010).
pubmed: 20404851
doi: 10.1038/ni.1863
Dong, Y. et al. Stress-induced NLRP3 inflammasome activation negatively regulates fear memory in mice. J. Neuroinflammation 17, 205 (2020).
pubmed: 32635937
pmcid: 7341659
doi: 10.1186/s12974-020-01842-0
Combes, A. et al. BAD–LAMP controls TLR9 trafficking and signalling in human plasmacytoid dendritic cells. Nat. Commun. 8, 913 (2017).
pubmed: 29030552
pmcid: 5640662
doi: 10.1038/s41467-017-00695-1
Maatouk, L. et al. TLR9 activation via microglial glucocorticoid receptors contributes to degeneration of midbrain dopamine neurons. Nat. Commun. 9, 2450 (2018).
pubmed: 29934589
pmcid: 6015079
doi: 10.1038/s41467-018-04569-y
Matsuo, N., Reijmers, L. & Mayford, M. Spine-type-specific recruitment of newly synthesized AMPA receptors with learning. Science 319, 1104–1107 (2008).
pubmed: 18292343
pmcid: 2692967
doi: 10.1126/science.1149967
Reindl, J. et al. Chromatin organization revealed by nanostructure of irradiation induced γH2AX, 53BP1 and Rad51 foci. Sci Rep. 7, 40616 (2017).
pubmed: 28094292
pmcid: 5240115
doi: 10.1038/srep40616
Ferreira da Silva, J., Meyenberg, M. & Loizou, J. I. Tissue specificity of DNA repair: the CRISPR compass. Trends Genet. 37, 958–962 (2021).
pubmed: 34392967
doi: 10.1016/j.tig.2021.07.010
D’Amelio, M., Cavallucci, V. & Cecconi, F. Neuronal caspase-3 signaling: not only cell death. Cell Death Differ. 17, 1104–1114 (2010).
pubmed: 19960023
doi: 10.1038/cdd.2009.180
Yim, H., Shin, S. B., Woo, S. U., Lee, P. C. & Erikson, R. L. Plk1-mediated stabilization of 53BP1 through USP7 regulates centrosome positioning to maintain bipolarity. Oncogene 36, 966–978 (2017).
pubmed: 27477698
doi: 10.1038/onc.2016.263
Messina, G., Prozzillo, Y., Monache, F. D., Santopietro, M. V. & Dimitri, P. Evolutionary conserved relocation of chromatin remodeling complexes to the mitotic apparatus. BMC Biol. 20, 172 (2022).
pubmed: 35922843
pmcid: 9351137
doi: 10.1186/s12915-022-01365-5
Loffler, H., Lukas, J., Bartek, J. & Kramer, A. Structure meets function—centrosomes, genome maintenance and the DNA damage response. Exp. Cell. Res. 312, 2633–2640 (2006).
pubmed: 16854412
doi: 10.1016/j.yexcr.2006.06.008
Radulovic, J., Kammermeier, J. & Spiess, J. Relationship between Fos production and classical fear conditioning: effects of novelty, latent inhibition, and unconditioned stimulus preexposure. J. Neurosci. 18, 7452–7461 (1998).
pubmed: 9736664
pmcid: 6793227
doi: 10.1523/JNEUROSCI.18-18-07452.1998
Jones, M. W. et al. A requirement for the immediate early gene Zif268 in the expression of late LTP and long-term memories. Nat. Neurosci. 4, 289–296 (2001).
pubmed: 11224546
doi: 10.1038/85138
Sun, X. et al. Functionally distinct neuronal ensembles within the memory engram. Cell 181, 410–423.e417 (2020).
pubmed: 32187527
pmcid: 7166195
doi: 10.1016/j.cell.2020.02.055
Elmore, M. R. et al. Colony-stimulating factor 1 receptor signaling is necessary for microglia viability, unmasking a microglia progenitor cell in the adult brain. Neuron 82, 380–397 (2014).
pubmed: 24742461
pmcid: 4161285
doi: 10.1016/j.neuron.2014.02.040
Stetson, D. B., Ko, J. S., Heidmann, T. & Medzhitov, R. Trex1 prevents cell-intrinsic initiation of autoimmunity. Cell 134, 587–598 (2008).
pubmed: 18724932
pmcid: 2626626
doi: 10.1016/j.cell.2008.06.032
Zhou, Y. et al. Molecular landscapes of human hippocampal immature neurons across lifespan. Nature 607, 527–533 (2022).
pubmed: 35794479
pmcid: 9316413
doi: 10.1038/s41586-022-04912-w
Fox-Fisher, I. et al. Remote immune processes revealed by immune-derived circulating cell-free DNA. eLife 10, e70520 (2021).
pubmed: 34842142
pmcid: 8651286
doi: 10.7554/eLife.70520
Dundr, M. & Misteli, T. Biogenesis of nuclear bodies. Cold Spring Harb. Perspect. Biol. 2, a000711 (2010).
pubmed: 21068152
pmcid: 2982170
doi: 10.1101/cshperspect.a000711
Roers, A., Hiller, B. & Hornung, V. Recognition of endogenous nucleic acids by the innate immune system. Immunity 44, 739–754 (2016).
pubmed: 27096317
doi: 10.1016/j.immuni.2016.04.002
Hemmi, H. et al. A Toll-like receptor recognizes bacterial DNA. Nature 408, 740–745 (2000).
pubmed: 11130078
doi: 10.1038/35047123
Haas, T. et al. The DNA sugar backbone 2′ deoxyribose determines toll-like receptor 9 activation. Immunity 28, 315–323 (2008).
pubmed: 18342006
doi: 10.1016/j.immuni.2008.01.013
Fawcett, J. W., Oohashi, T. & Pizzorusso, T. The roles of perineuronal nets and the perinodal extracellular matrix in neuronal function. Nat. Rev. Neurosci. 20, 451–465 (2019).
pubmed: 31263252
doi: 10.1038/s41583-019-0196-3
Huang, H. et al. Endogenous histones function as alarmins in sterile inflammatory liver injury through Toll-like receptor 9 in mice. Hepatology 54, 999–1008 (2011).
pubmed: 21721026
doi: 10.1002/hep.24501
Welch, G. & Tsai, L. H. Mechanisms of DNA damage-mediated neurotoxicity in neurodegenerative disease. EMBO Rep. 23, e54217 (2022).
pubmed: 35499251
pmcid: 9171412
doi: 10.15252/embr.202154217
Soltesz, I. & Losonczy, A. CA1 pyramidal cell diversity enabling parallel information processing in the hippocampus. Nat. Neurosci. 21, 484–493 (2018).
pubmed: 29593317
pmcid: 5909691
doi: 10.1038/s41593-018-0118-0
Kaeser, G. & Chun, J. Brain cell somatic gene recombination and its phylogenetic foundations. J. Biol. Chem. 295, 12786–12795 (2020).
pubmed: 32699111
pmcid: 7476723
doi: 10.1074/jbc.REV120.009192
Ren, L. Y. et al. Stress-induced changes of the cholinergic circuitry promote retrieval-based generalization of aversive memories. Mol. Psychiatry 27, 3795–3805 (2022).
pubmed: 35551246
pmcid: 9846583
doi: 10.1038/s41380-022-01610-x
Wingett, S. W. & Andrews, S. FastQ Screen: a tool for multi-genome mapping and quality control. F1000Res 7, 1338 (2018).
pubmed: 30254741
pmcid: 6124377
doi: 10.12688/f1000research.15931.1
Kitamura, T. et al. Engrams and circuits crucial for systems consolidation of a memory. Science 356, 73–78 (2017).
pubmed: 28386011
pmcid: 5493329
doi: 10.1126/science.aam6808
La Rosa, C. et al. Phylogenetic variation in cortical layer II immature neuron reservoir of mammals. eLife 9, e55456 (2020).
pubmed: 32690132
pmcid: 7373429
doi: 10.7554/eLife.55456
Hagihara, H. et al. Expression of progenitor cell/immature neuron markers does not present definitive evidence for adult neurogenesis. Mol. Brain 12, 108 (2019).
pubmed: 31823803
pmcid: 6902531
doi: 10.1186/s13041-019-0522-8
Tanaka, T. et al. Lis1 and doublecortin function with dynein to mediate coupling of the nucleus to the centrosome in neuronal migration. J. Cell Biol. 165, 709–721 (2004).
pubmed: 15173193
pmcid: 2172383
doi: 10.1083/jcb.200309025
Cryan, J. F. & Mazmanian, S. K. Microbiota–brain axis: context and causality. Science 376, 938–939 (2022).
pubmed: 35617385
doi: 10.1126/science.abo4442
Crack, P. J. & Bray, P. J. Toll-like receptors in the brain and their potential roles in neuropathology. Immunol. Cell Biol. 85, 476–480 (2007).
pubmed: 17667932
doi: 10.1038/sj.icb.7100103
Schumacher, B., Pothof, J., Vijg, J. & Hoeijmakers, J. H. J. The central role of DNA damage in the ageing process. Nature 592, 695–703 (2021).
pubmed: 33911272
pmcid: 9844150
doi: 10.1038/s41586-021-03307-7
Zimmerman, G. et al. Post-traumatic anxiety associates with failure of the innate immune receptor TLR9 to evade the pro-inflammatory NFκB pathway. Transl. Psychiatry 2, e78 (2012).
pubmed: 22832815
pmcid: 3309554
doi: 10.1038/tp.2012.4
Halder, R. et al. DNA methylation changes in plasticity genes accompany the formation and maintenance of memory. Nat. Neurosci. 19, 102–110 (2016).
Lienhard, M., Grimm, C., Morkel, M., Herwig, R. & Chavez, L. MEDIPS: genome-wide differential coverage analysis of sequencing data derived from DNA enrichment experiments. Bioinformatics 30, 284–286 (2014).
pubmed: 24227674
doi: 10.1093/bioinformatics/btt650
Corces, M. R. et al. An improved ATAC-seq protocol reduces background and enables interrogation of frozen tissues. Nat. Methods 14, 959–962 (2017).
pubmed: 28846090
pmcid: 5623106
doi: 10.1038/nmeth.4396
Gillespie, M. et al. The reactome pathway knowledgebase 2022. Nucleic Acids Res. 50, D687–D692 (2022).
pubmed: 34788843
doi: 10.1093/nar/gkab1028
Teo, Y. V., Hinthorn, S. J., Webb, A. E. & Neretti, N. Single-cell transcriptomics of peripheral blood in the aging mouse. Aging 15, 6–20 (2023).
pubmed: 36622281
pmcid: 9876630
doi: 10.18632/aging.204471
Butovsky, O. & Weiner, H. L. Microglial signatures and their role in health and disease. Nat. Rev. Neurosci. 19, 622–635 (2018).
pubmed: 30206328
pmcid: 7255106
doi: 10.1038/s41583-018-0057-5
Szklarczyk, D. et al. STRING v11: protein–protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucleic Acids Res. 47, D607–D613 (2019).
pubmed: 30476243
doi: 10.1093/nar/gky1131
Shen, Y. J. et al. Genome-derived cytosolic DNA contributes to type I interferon expression and immunogenicity of B-cell lymphoma cells. Cytokine 76, 581–582 (2015).
pubmed: 26070935
doi: 10.1016/j.cyto.2015.05.024
Gao, C. et al. Hippocampal NMDA receptor subunits differentially regulate fear memory formation and neuronal signal propagation. Hippocampus 20, 1072–1082 (2010).
pubmed: 19806658
pmcid: 2891656
doi: 10.1002/hipo.20705
Tripathi, A., Bartosh, A., Whitehead, C. & Pillai, A. Activation of cell-free mtDNA–TLR9 signaling mediates chronic stress-induced social behavior deficits. Mol. Psychiatry 28, 3806–3815 (2023).
pubmed: 37528226
pmcid: 10730412
doi: 10.1038/s41380-023-02189-7