Epigenetic maintenance of adult neural stem cell quiescence in the mouse hippocampus via Setd1a – Nature Communications

  • Ming, G. L. & Song, H. Adult neurogenesis in the mammalian brain: significant answers and significant questions. Neuron 70, 687–702 (2011).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Sahay, A., Wilson, D. A. & Hen, R. Pattern separation: a common function for new neurons in hippocampus and olfactory bulb. Neuron 70, 582–588 (2011).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Denoth-Lippuner, A. & Jessberger, S. Formation and integration of new neurons in the adult hippocampus. Nat Rev Neurosci 22, 223–236 (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Toda, T., Parylak, S. L., Linker, S. B. & Gage, F. H. The role of adult hippocampal neurogenesis in brain health and disease. Mol Psychiatry 24, 67–87 (2019).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Kempermann, G. et al. Human adult neurogenesis: evidence and remaining questions. Cell Stem Cell 23, 25–30 (2018).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Terreros-Roncal, J. et al. Impact of neurodegenerative diseases on human adult hippocampal neurogenesis. Science 374, 1106–1113 (2021).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Zhou, Y. et al. Molecular landscapes of human hippocampal immature neurons across lifespan. Nature 607, 527–533 (2022).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Ming, G. L. & Song, H. Adult neurogenesis in the mammalian central nervous system. Annu Rev Neurosci 28, 223–250 (2005).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Christian, K. M., Song, H. & Ming, G. L. Functions and dysfunctions of adult hippocampal neurogenesis. Annu Rev Neurosci 37, 243–262 (2014).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Bonaguidi, M. A. et al. In vivo clonal analysis reveals self-renewing and multipotent adult neural stem cell characteristics. Cell 145, 1142–1155 (2011).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Sun, G. J. et al. Latent tri-lineage potential of adult hippocampal neural stem cells revealed by Nf1 inactivation. Nat Neurosci 18, 1722–1724 (2015).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Urban, N., Blomfield, I. M. & Guillemot, F. Quiescence of adult mammalian neural stem cells: a highly regulated rest. Neuron 104, 834–848 (2019).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Encinas, J. M. et al. Division-coupled astrocytic differentiation and age-related depletion of neural stem cells in the adult hippocampus. Cell Stem Cell 8, 566–579 (2011).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Pilz, G. A. et al. Live imaging of neurogenesis in the adult mouse hippocampus. Science 359, 658–662 (2018).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Bottes, S. et al. Long-term self-renewing stem cells in the adult mouse hippocampus identified by intravital imaging. Nat Neurosci 24, 225–233 (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Kuhn, H. G., Dickinson-Anson, H. & Gage, F. H. Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J Neurosci 16, 2027–2033 (1996).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Ibrayeva, A. et al. Early stem cell aging in the mature brain. Cell Stem Cell 28, 955–966.e957 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Audesse, A. J. & Webb, A. E. Mechanisms of enhanced quiescence in neural stem cell aging. Mech Ageing Dev 191, 111323 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Wu, Y. et al. Chronic in vivo imaging defines age-dependent alterations of neurogenesis in the mouse hippocampus. Nat Aging 3, 380–390 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Paik, J. H. et al. FoxOs cooperatively regulate diverse pathways governing neural stem cell homeostasis. Cell Stem Cell 5, 540–553 (2009).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Renault, V. M. et al. FoxO3 regulates neural stem cell homeostasis. Cell Stem Cell 5, 527–539 (2009).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Zhou, Y. et al. Autocrine Mfge8 signaling prevents developmental exhaustion of the adult neural stem cell pool. Cell Stem Cell 23, 444–452.e444 (2018).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Urban, N. Could a different view of quiescence help us understand how neurogenesis is regulated? Front Neurosci 16, 878875 (2022).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Shin, J. et al. Single-cell RNA-seq with waterfall reveals molecular cascades underlying adult neurogenesis. Cell Stem Cell 17, 360–372 (2015).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Ding, W. Y., Huang, J. & Wang, H. Waking up quiescent neural stem cells: molecular mechanisms and implications in neurodevelopmental disorders. PLoS Genet 16, e1008653 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Blasco-Chamarro, L. & Farinas, I. Fine-tuned rest: unveiling the regulatory landscape of adult quiescent neural stem cells. Neuroscience 525, 26–37 (2023).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Lampada, A. & Taylor, V. Notch signaling as a master regulator of adult neurogenesis. Front Neurosci 17, 1179011 (2023).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Zhang, F., Yoon, K., Kim, N. S., Ming, G. L. & Song, H. Cell-autonomous and non-cell-autonomous roles of NKCC1 in regulating neural stem cell quiescence in the hippocampal dentate gyrus. Stem Cell Reports 18, 1468–1481 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Jang, M. H. et al. Secreted frizzled-related protein 3 regulates activity-dependent adult hippocampal neurogenesis. Cell Stem Cell 12, 215–223 (2013).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Song, J. et al. Neuronal circuitry mechanism regulating adult quiescent neural stem-cell fate decision. Nature 489, 150–154 (2012).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Mira, H. et al. Signaling through BMPR-IA regulates quiescence and long-term activity of neural stem cells in the adult hippocampus. Cell Stem Cell 7, 78–89 (2010).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Song, J., Sun, J., Olsen, R. H. J., Ming, G.-l & Song, H. Neuronal circuitry mechanisms regulating adult mammalian neurogenesis. Cold Spring Harbor Perspective in Biology 8, a018937 (2016).

    Article 

    Google Scholar
     

  • Knobloch, M. et al. Metabolic control of adult neural stem cell activity by Fasn-dependent lipogenesis. Nature 493, 226–230 (2013).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar
     

  • Knobloch, M. et al. A fatty acid oxidation-dependent metabolic shift regulates adult neural stem cell activity. Cell Rep 20, 2144–2155 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Petrelli, F. et al. Mitochondrial pyruvate metabolism regulates the activation of quiescent adult neural stem cells. Sci Adv 9, eadd5220 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kobayashi, T. et al. Enhanced lysosomal degradation maintains the quiescent state of neural stem cells. Nat Commun 10, 5446 (2019).

    Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Gengatharan, A. et al. Adult neural stem cell activation in mice is regulated by the day/night cycle and intracellular calcium dynamics. Cell 184, 709–722 e713 (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Fong, B. C. et al. The Rb/E2F axis is a key regulator of the molecular signatures instructing the quiescent and activated adult neural stem cell state. Cell Rep 41, 111578 (2022).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Andersen, J. et al. A transcriptional mechanism integrating inputs from extracellular signals to activate hippocampal stem cells. Neuron 83, 1085–1097 (2014).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Fan, W. et al. The transcriptional co-activator Yap1 promotes adult hippocampal neural stem cell activation. EMBO J 42, e110384 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Urban, N. et al. Return to quiescence of mouse neural stem cells by degradation of a proactivation protein. Science 353, 292–295 (2016).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Blomfield, I. M. et al. Id4 promotes the elimination of the pro-activation factor Ascl1 to maintain quiescence of adult hippocampal stem cells. Elife 8, e48561 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Sun, J. et al. A septo-temporal molecular gradient of sfrp3 in the dentate gyrus differentially regulates quiescent adult hippocampal neural stem cell activation. Mol Brain 8, 52 (2015).

    Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Berg, D. A. et al. A common embryonic origin of stem cells drives developmental and adult neurogenesis. Cell 177, 654–668.e615 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Yao, B. et al. Epigenetic mechanisms in neurogenesis. Nat Rev Neurosci 17, 537–549 (2016).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Lim, D. A. et al. Chromatin remodelling factor Mll1 is essential for neurogenesis from postnatal neural stem cells. Nature 458, 529–533 (2009).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Delgado, R. N. et al. Maintenance of neural stem cell positional identity by mixed-lineage leukemia 1. Science 368, 48–53 (2020).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Toda, T. et al. Nup153 interacts with Sox2 to enable bimodal gene regulation and maintenance of neural progenitor cells. Cell Stem Cell 21, 618–634.e617 (2017).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Li, X. et al. Ten-eleven translocation 2 interacts with forkhead box O3 and regulates adult neurogenesis. Nat Commun 8, 15903 (2017).

    Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Guerra, M. V. et al. H3K9 methyltransferases Suv39h1 and Suv39h2 control the differentiation of neural progenitor cells in the adult hippocampus. Front Cell Dev Biol 9, 778345 (2021).

    Article 
    PubMed 

    Google Scholar
     

  • Zocher, S. et al. De novo DNA methylation controls neuronal maturation during adult hippocampal neurogenesis. EMBO J 40, e107100 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Jobe, E. M. & Zhao, X. DNA methylation and adult neurogenesis. Brain Plast 3, 5–26 (2017).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Zocher, S. & Toda, T. Epigenetic aging in adult neurogenesis. Hippocampus 33, 347–359 (2023).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Jessberger, S. et al. Epigenetic modulation of seizure-induced neurogenesis and cognitive decline. J Neurosci 27, 5967–5975 (2007).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Ma, D. K. et al. Neuronal activity-induced Gadd45b promotes epigenetic DNA demethylation and adult neurogenesis. Science 323, 1074–1077 (2009).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Wang, S. et al. SETD1A Mediated H3K4 Methylation and Its Role in Neurodevelopmental and Neuropsychiatric Disorders. Front Mol Neurosci 14, 772000 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Singh, T. et al. Rare coding variants in ten genes confer substantial risk for schizophrenia. Nature 604, 509–516 (2022).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Singh, T. et al. Rare loss-of-function variants in SETD1A are associated with schizophrenia and developmental disorders. Nat Neurosci 19, 571–577 (2016).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Takata, A. et al. Loss-of-function variants in schizophrenia risk and SETD1A as a candidate susceptibility gene. Neuron 82, 773–780 (2014).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Mukai, J. et al. Recapitulation and reversal of schizophrenia-related phenotypes in Setd1a-deficient mice. Neuron 104, 471–487.e412 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Nagahama, K. et al. Setd1a insufficiency in mice attenuates excitatory synaptic function and recapitulates schizophrenia-related behavioral abnormalities. Cell Rep 32, 108126 (2020).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Chen, R. et al. Cell type-specific mechanism of Setd1a heterozygosity in schizophrenia pathogenesis. Sci Adv 8, eabm1077 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Shi, Y. et al. Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 119, 941–953 (2004).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Tusi, B. K. et al. Setd1a regulates progenitor B-cell-to-precursor B-cell development through histone H3 lysine 4 trimethylation and Ig heavy-chain rearrangement. FASEB J 29, 1505–1515 (2015).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Tronche, F. et al. Disruption of the glucocorticoid receptor gene in the nervous system results in reduced anxiety. Nat Genet 23, 99–103 (1999).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Bond, A. M., Ming, G. L. & Song, H. Adult mammalian neural stem cells and neurogenesis: five decades later. Cell Stem Cell 17, 385–395 (2015).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Wong, S. Z. H. et al. In vivo clonal analysis reveals spatiotemporal regulation of thalamic nucleogenesis. PLoS Biol 16, e2005211 (2018).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Hoshii, T. et al. A non-catalytic function of SETD1A regulates cyclin K and the dna damage response. Cell 172, 1007–1021.e1017 (2018).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Lee, M. G., Wynder, C., Schmidt, D. M., McCafferty, D. G. & Shiekhattar, R. Histone H3 lysine 4 demethylation is a target of nonselective antidepressive medications. Chem Biol 13, 563–567 (2006).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Maes, T., Carceller, E., Salas, J., Ortega, A. & Buesa, C. Advances in the development of histone lysine demethylase inhibitors. Curr Opin Pharmacol 23, 52–60 (2015).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Maes, T. et al. ORY-1001, a Potent and Selective Covalent KDM1A Inhibitor, for the Treatment of Acute Leukemia. Cancer Cell 33, 495–511.e412 (2018).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Ma, D. K., Chiang, C. H., Ponnusamy, K., Ming, G. L. & Song, H. G9a and Jhdm2a regulate embryonic stem cell fusion-induced reprogramming of adult neural stem cells. Stem Cells 26, 2131–2141 (2008).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Martynoga, B. et al. Epigenomic enhancer annotation reveals a key role for NFIX in neural stem cell quiescence. Genes Dev 27, 1769–1786 (2013).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Marques-Torrejon, M. A. et al. LRIG1 is a gatekeeper to exit from quiescence in adult neural stem cells. Nat Commun 12, 2594 (2021).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Santos-Rosa, H. et al. Active genes are tri-methylated at K4 of histone H3. Nature 419, 407–411 (2002).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar
     

  • Sun, H. et al. Stra13 regulates satellite cell activation by antagonizing Notch signaling. J Cell Biol 177, 647–657 (2007).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Salvi, J. S. et al. ATR activity controls stem cell quiescence via the cyclin F-SCF complex. Proc Natl Acad Sci USA 119, e2115638119 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Lukas, J. et al. Dazap2 modulates transcription driven by the Wnt effector TCF-4. Nucleic Acids Res 37, 3007–3020 (2009).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Qian, X. et al. PTEN suppresses glycolysis by dephosphorylating and inhibiting autophosphorylated PGK1. Mol Cell 76, 516–527.e517 (2019).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Yamauchi, T., Nishiyama, M., Moroishi, T., Kawamura, A. & Nakayama, K. I. FBXL5 inactivation in mouse brain induces aberrant proliferation of neural stem progenitor cells. Mol Cell Biol 37, e00470–16 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Asanoma, K. et al. Regulation of the mechanism of TWIST1 transcription by BHLHE40 and BHLHE41 in cancer cells. Mol Cell Biol 35, 4096–4109 (2015).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • de Morree, A. & Rando, T. A. Regulation of adult stem cell quiescence and its functions in the maintenance of tissue integrity. Nat Rev. Mol. Cell Biol. 24, 334–354 (2023).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Radak, M. & Fallahi, H. The epigenetic regulation of quiescent in stem cells. Glob Med Genet 10, 339–344 (2023).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Cho, I. J. et al. Mechanisms, hallmarks, and implications of stem cell quiescence. Stem Cell Reports 12, 1190–1200 (2019).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Nicetto, D. & Zaret, K. S. Role of H3K9me3 heterochromatin in cell identity establishment and maintenance. Curr Opin Genet Dev 55, 1–10 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kim, M. & Costello, J. DNA methylation: an epigenetic mark of cellular memory. Exp Mol Med 49, e322 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Jiang, Y. & Hsieh, J. HDAC3 controls gap 2/mitosis progression in adult neural stem/progenitor cells by regulating CDK1 levels. Proc Natl Acad Sci USA 111, 13541–13546 (2014).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Imayoshi, I., Sakamoto, M., Yamaguchi, M., Mori, K. & Kageyama, R. Essential roles of notch signaling in maintenance of neural stem cells in developing and adult brains. J Neurosci 30, 3489–3498 (2010).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Sueda, R., Imayoshi, I., Harima, Y. & Kageyama, R. High Hes1 expression and resultant Ascl1 suppression regulate quiescent vs. active neural stem cells in the adult mouse brain. Genes Dev 33, 511–523 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Arndt, K. et al. SETD1A protects HSCs from activation-induced functional decline in vivo. Blood 131, 1311–1324 (2018).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Hyun, K., Jeon, J., Park, K. & Kim, J. Writing, erasing and reading histone lysine methylations. Exp Mol Med 49, e324 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Gates, L. A. et al. Acetylation on histone H3 lysine 9 mediates a switch from transcription initiation to elongation. J Biol Chem 292, 14456–14472 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Karmodiya, K., Krebs, A. R., Oulad-Abdelghani, M., Kimura, H. & Tora, L. H3K9 and H3K14 acetylation co-occur at many gene regulatory elements, while H3K14ac marks a subset of inactive inducible promoters in mouse embryonic stem cells. BMC Genomics 13, 424 (2012).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Huang, Y. et al. Inhibition of lysine-specific demethylase 1 by polyamine analogues results in reexpression of aberrantly silenced genes. Proc Natl Acad Sci USA 104, 8023–8028 (2007).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Wang, S. et al. Loss-of-function variants in the schizophrenia risk gene SETD1A alter neuronal network activity in human neurons through the cAMP/PKA pathway. Cell Rep 39, 110790 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kang, E., Wen, Z., Song, H., Christian, K. M. & Ming, G. L. Adult neurogenesis and psychiatric disorders. Cold Spring Harb Perspect Biol 8, a019026 (2016).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Allen, K. M., Fung, S. J. & Weickert, C. S. Cell proliferation is reduced in the hippocampus in schizophrenia. Aust N Z J Psychiatry 50, 473–480 (2016).

    Article 
    PubMed 

    Google Scholar
     

  • Reif, A. et al. Neural stem cell proliferation is decreased in schizophrenia, but not in depression. Mol Psychiatry 11, 514–522 (2006).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Duan, X. et al. Disrupted-in-schizophrenia 1 regulates integration of newly generated neurons in the adult brain. Cell 130, 1146–1158 (2007).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Weng, Y. L. et al. An intrinsic epigenetic barrier for functional axon regeneration. Neuron 94, 337–346.e336 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Zhang, F. et al. Epitranscriptomic regulation of cortical neurogenesis via Mettl8-dependent mitochondrial tRNA m(3)C modification. Cell Stem Cell 30, 300–311.e311 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Dobin, A. et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15–21 (2013).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Robinson, M. D., McCarthy, D. J. & Smyth, G. K. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139–140 (2010).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Zhou, Y. et al. Metascape provides a biologist-oriented resource for the analysis of systems-level datasets. Nat Commun 10, 1523 (2019).

    Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Gu, Z., Eils, R. & Schlesner, M. Complex heatmaps reveal patterns and correlations in multidimensional genomic data. Bioinformatics 32, 2847–2849 (2016).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat Methods 9, 357–359 (2012).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Li, H. et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078–2079 (2009).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Zhang, Y. et al. Model-based analysis of ChIP-Seq (MACS). Genome Biol 9, R137 (2008).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Ramirez, F. et al. deepTools2: a next generation web server for deep-sequencing data analysis. Nucleic Acids Res 44, W160–W165 (2016).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Yu, G., Wang, L. G. & He, Q. Y. ChIPseeker: an R/Bioconductor package for ChIP peak annotation, comparison and visualization. Bioinformatics 31, 2382–2383 (2015).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Enomoto, M., Bunge, M. B. & Tsoulfas, P. A multifunctional neurotrophin with reduced affinity to p75NTR enhances transplanted Schwann cell survival and axon growth after spinal cord injury. Exp Neurol 248, 170–182 (2013).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Truitt J. M., et al. Inhibition of IKKbeta Reduces Ethanol Consumption in C57BL/6J Mice. eNeuro 3, (2016).

  • Kim, Y. S. et al. Characterizing the conductance underlying depolarization-induced slow current in cerebellar Purkinje cells. J Neurophysiol 109, 1174–1181 (2013).

    Article 
    CAS 
    PubMed 

    Google Scholar