Post-transcriptional mechanisms controlling neurogenesis and direct neuronal reprogramming.
Journal
Neural regeneration research
ISSN: 1673-5374
Titre abrégé: Neural Regen Res
Pays: India
ID NLM: 101316351
Informations de publication
Date de publication:
01 Sep 2024
01 Sep 2024
Historique:
received:
31
07
2023
accepted:
08
11
2023
medline:
16
1
2024
pubmed:
16
1
2024
entrez:
16
1
2024
Statut:
ppublish
Résumé
Neurogenesis is a tightly regulated process in time and space both in the developing embryo and in adult neurogenic niches. A drastic change in the transcriptome and proteome of radial glial cells or neural stem cells towards the neuronal state is achieved due to sophisticated mechanisms of epigenetic, transcriptional, and post-transcriptional regulation. Understanding these neurogenic mechanisms is of major importance, not only for shedding light on very complex and crucial developmental processes, but also for the identification of putative reprogramming factors, that harbor hierarchically central regulatory roles in the course of neurogenesis and bare thus the capacity to drive direct reprogramming towards the neuronal fate. The major transcriptional programs that orchestrate the neurogenic process have been the focus of research for many years and key neurogenic transcription factors, as well as repressor complexes, have been identified and employed in direct reprogramming protocols to convert non-neuronal cells, into functional neurons. The post-transcriptional regulation of gene expression during nervous system development has emerged as another important and intricate regulatory layer, strongly contributing to the complexity of the mechanisms controlling neurogenesis and neuronal function. In particular, recent advances are highlighting the importance of specific RNA binding proteins that control major steps of mRNA life cycle during neurogenesis, such as alternative splicing, polyadenylation, stability, and translation. Apart from the RNA binding proteins, microRNAs, a class of small non-coding RNAs that block the translation of their target mRNAs, have also been shown to play crucial roles in all the stages of the neurogenic process, from neural stem/progenitor cell proliferation, neuronal differentiation and migration, to functional maturation. Here, we provide an overview of the most prominent post-transcriptional mechanisms mediated by RNA binding proteins and microRNAs during the neurogenic process, giving particular emphasis on the interplay of specific RNA binding proteins with neurogenic microRNAs. Taking under consideration that the molecular mechanisms of neurogenesis exert high similarity to the ones driving direct neuronal reprogramming, we also discuss the current advances in in vitro and in vivo direct neuronal reprogramming approaches that have employed microRNAs or RNA binding proteins as reprogramming factors, highlighting the so far known mechanisms of their reprogramming action.
Identifiants
pubmed: 38227517
doi: 10.4103/1673-5374.390976
pii: 01300535-202409000-00020
doi:
Types de publication
Journal Article
Langues
eng
Pagination
1929-1939Informations de copyright
Copyright © 2024 Copyright: © 2024 Neural Regeneration Research.
Références
Abdelmohsen K, Hutchison ER, Lee EK, Kuwano Y, Kim MM, Masuda K, Srikantan S, Subaran SS, Marasa BS, Mattson MP, Gorospe M (2010) miR-375 inhibits differentiation of neurites by lowering HuD levels. Mol Cell Biol 30:4197.
Abernathy DG, Kim WK, McCoy MJ, Lake AM, Ouwenga R, Lee SW, Xing X, Li D, Lee HJ, Heuckeroth RO, Dougherty JD, Wang T, Yoo AS (2017) MicroRNAs induce a permissive chromatin environment that enables neuronal subtype-specific reprogramming of adult human fibroblasts. Cell Stem Cell 21:332–348.
Akamatsu W, Fujihara H, Mitsuhashi T, Yano M, Shibata S, Hayakawa Y, Okano HJ, Sakakibara SI, Takano H, Takano T, Takahashi T, Noda T, Okano H (2005) The RNA-binding protein HuD regulates neuronal cell identity and maturation. Proc Natl Acad Sci U S A 102:4625–4630.
Akten B, Kye MJ, Hao LT, Wertz MH, Singh S, Nie D, Huang J, Merianda TT, Twiss JL, Beattie CE, Steen JAJ, Sahin M (2011) Interaction of survival of motor neuron (SMN) and HuD proteins with mRNA cpg15 rescues motor neuron axonal deficits. Proc Natl Acad Sci U S A 108:10337–10342.
Alarcón CR, Goodarzi H, Lee H, Liu X, Tavazoie S, Tavazoie SF (2015a) HNRNPA2B1 is a mediator of m6A-dependent nuclear RNA processing events. Cell 162:1299–1308.
Alarcón CR, Lee H, Goodarzi H, Halberg N, Tavazoie SF (2015b) N6-methyladenosine marks primary microRNAs for processing. Nature 519:482–485.
Alkallas R, Fish L, Goodarzi H, Najafabadi HS (2017) Inference of RNA decay rate from transcriptional profiling highlights the regulatory programs of Alzheimer's disease. Nat Commun 8:909.
Alrahbeni T, Sartor F, Anderson J, Miedzybrodzka Z, McCaig C, Müller B (2015) Full UPF3B function is critical for neuronal differentiation of neural stem cells. Mol Brain 8:33.
Anderson KD, Sengupta J, Morin M, Neve RL, Valenzuela CF, Perrone-Bizzozero NI (2001) Overexpression of HuD accelerates neurite outgrowth and increases GAP-43 mRNA expression in cortical neurons and retinoic acid-induced embryonic stem cells in vitro. Exp Neurol 168:250–258.
Aranda-Abreu GE, Behar L, Chung S, Furneaux H, Ginzburg I (1999) Embryonic lethal abnormal vision-like RNA-binding proteins regulate neurite outgrowth and tau expression in PC12 cells. J Neurosci 19:6907–6917.
Aravantinou-Fatorou K, Ortega F, Chroni-Tzartou D, Antoniou N, Poulopoulou C, Politis PK, Berninger B, Matsas R, Thomaidou D (2015) CEND1 and NEUROGENIN2 reprogram mouse astrocytes and embryonic fibroblasts to induced neural precursors and differentiated neurons. Stem Cell Reports 5:405–418.
Bakheet T, Williams BRG, Khabar KSA (2006) ARED 3.0: the large and diverse AU-rich transcriptome. Nucleic Acids Res 34:111–114.
Bakheet T, Hitti E, Al-Saif M, Moghrabi WN, Khabar KSA (2018) The AU-rich element landscape across human transcriptome reveals a large proportion in introns and regulation by ELAVL1/HuR. Biochim Biophys Acta Gene Regul Mech 1861:167–177.
Bellavia D, Mecarozzi M, Campese AF, Grazioli P, Talora C, Frati L, Gulino A, Screpanti I (2007) Notch3 and the Notch3-upregulated RNA-binding protein HuD regulate Ikaros alternative splicing. EMBO J 26:1670–1680.
Berto S, Usui N, Konopka G, Fogel BL (2016) ELAVL2-regulated transcriptional and splicing networks in human neurons link neurodevelopment and autism. Hum Mol Genet 25:2451–2464.
Bhat VD, Jayaraj J, Babu K (2022) RNA and neuronal function: the importance of post-transcriptional regulation. Oxford Open Neurosci doi:10.1093/oons/kvac011
Birtele M, Sharma Y, Kidnapillai S, Lau S, Stoker TB, Barker RA, Rylander Ottosson D, Drouin-Ouellet J, Parmar M (2019) Dual modulation of neuron-specific microRNAs and the REST complex promotes functional maturation of human adult induced neurons. FEBS Lett 593:3370–3380.
Black JB, McCutcheon SR, Dube S, Barrera A, Klann TS, Rice GA, Adkar SS, Soderling SH, Reddy TE, Gersbach CA (2020) Master regulators and cofactors of human neuronal cell fate specification identified by CRISPR gene activation screens. Cell Rep 33:108460.
Bolognani F, Contente-Cuomo T, Perrone-Bizzozero NI (2009) Novel recognition motifs and biological functions of the RNA-binding protein HuD revealed by genome-wide identification of its targets. Nucleic Acids Res 38:117–130.
Boudreau RL, Jiang P, Gilmore BL, Spengler RM, Tirabassi R, Nelson JA, Ross CA, Xing Y, Davidson BL (2014) Transcriptome-wide discovery of microRNA binding sites in human brain. Neuron 81:294–305.
Boutz PL, Stoilov P, Li Q, Lin CH, Chawla G, Ostrow K, Shiue L, Ares M, Black DL (2007) A post-transcriptional regulatory switch in polypyrimidine tract-binding proteins reprograms alternative splicing in developing neurons. Genes Dev 21:1636–1652.
Bruno IG, Karam R, Huang L, Bhardwaj A, Lou CH, Shum EY, Song HW, Corbett MA, Gifford WD, Gecz J, Pfaff SL, Wilkinson MF (2011) Identification of a microRNA that activates gene expression by repressing nonsense-mediated RNA decay. Mol Cell 42:500–510.
Capano LS, Sato C, Ficulle E, Yu A, Horie K, Kwon JS, Burbach KF, Barthélemy NR, Fox SG, Karch CM, Bateman RJ, Houlden H, Morimoto RI, Holtzman DM, Duff KE, Yoo AS (2022) Recapitulation of endogenous 4R tau expression and formation of insoluble tau in directly reprogrammed human neurons. Cell Stem Cell 29:918–932.
Chen CYA, Xu N, Shyu AB (2002) Highly selective actions of HuR in antagonizing AU-Rich element-mediated mRNA destabilization. Mol Cell Biol 22:7268–7278.
Chen J, Zhang YC, Huang C, Shen H, Sun B, Cheng X, Zhang YJ, Yang YG, Shu Q, Yang Y, Li X (2019) m6A regulates neurogenesis and neuronal development by modulating histone methyltransferase Ezh2. Genomics Proteomics Bioinformatics 17:154–168.
Chen W, Zhen Q, Huang Q, Ma S, Li M (2022) Repressing PTBP1 fails to convert reactive astrocytes to dopaminergic neurons in a 6-hydroxydopamine mouse model of Parkinson's disease. Elife 11:e75636.
Chen X, Sokirniy I, Wang X, Jiang M, Mseis-Jackson N, Williams C, Mayes K, Jiang N, Puls B, Du Q, Shi Y, Li H (2023) MicroRNA-375 is induced during astrocyte-to-neuron reprogramming and promotes survival of reprogrammed neurons when overexpressed. Cells 12:2202.
Chen Y, Zubovic L, Yang F, Godin K, Pavelitz T, Castellanos J, MacChi P, Varani G (2016) Rbfox proteins regulate microRNA biogenesis by sequence-specific binding to their precursors and target downstream Dicer. Nucleic Acids Res 44:4381–4395.
Chi SW, Zang JB, Mele A, Darnell RB (2009) Argonaute HITS-CLIP decodes microRNA-mRNA interaction maps. Nature 460:479–486.
Colak D, Ji SJ, Porse BT, Jaffrey SR (2013) Regulation of axon guidance by compartmentalized nonsense-mediated mRNA decay. Cell 153:1252.
Conaco C, Otto S, Han JJ, Mandel G (2006) Reciprocal actions of REST and a microRNA promote neuronal identity. Proc Natl Acad Sci U S A 103:2422–2427.
Dai W, Li W, Hoque M, Li Z, Tian B, Makeyev EV (2015) A post-transcriptional mechanism pacing expression of neural genes with precursor cell differentiation status. Nat Commun 6:7576.
De Gregorio R, Pulcrano S, De Sanctis C, Volpicelli F, Guatteo E, von Oerthel L, Latagliata EC, Esposito R, Piscitelli RM, Perrone-Capano C, Costa V, Greco D, Puglisi-Allegra S, Smidt MP, di Porzio U, Caiazzo M, Mercuri NB, Li M, Bellenchi GC (2018) miR-34b/c regulates Wnt1 and enhances mesencephalic dopaminergic neuron differentiation. Stem Cell Reports 10:1237–1250.
DeBoer EM, Azevedo R, Vega TA, Brodkin J, Akamatsu W, Okano H, Wagner GC, Rasin MR (2014) Prenatal deletion of the RNA-binding protein HuD disrupts postnatal cortical circuit maturation and behavior. J Neurosci 34:3674–3686.
Dell'Orco M, Oliver RJ, Perrone-Bizzozero N (2020) HuD binds to and regulates circular RNAs derived from neuronal development- and synaptic plasticity-associated genes. Front Genet 11:790.
Dell'Orco M, Elyaderani A, Vannan A, Sekar S, Powell G, Liang WS, Neisewander JL, Perrone-Bizzozero NI (2021) HuD regulates mRNA-circRNA-miRNA networks in the mouse striatum linked to neuronal development and drug addiction. Biology (Basel) 10:939.
Deschênes-Furry J, Bélanger G, Perrone-Bizzozero N, Jasmin BJ (2003) Post-transcriptional regulation of acetylcholinesterase mRNAs in nerve growth factor-treated PC12 cells by the RNA-binding protein HuD. J Biol Chem 278:5710–5717.
Doeppner TR, Doehring M, Bretschneider E, Zechariah A, Kaltwasser B, Müller B, Koch JC, Bähr M, Hermann DM, Michel U (2013) MicroRNA-124 protects against focal cerebral ischemia via mechanisms involving Usp14-dependent REST degradation. Acta Neuropathol 126:251–265.
Du H, Zhao Y, He J, Zhang Y, Xi H, Liu M, Ma J, Wu L (2016) YTHDF2 destabilizes m6A-containing RNA through direct recruitment of the CCR4–NOT deadenylase complex. Nat Commun 7:12626.
Fabra-Beser J, de Araujo JAM, Marques-Coelho D, Goff LA, Costa MR, Müller U, Gil-Sanz C (2021) Differential expression levels of Sox9 in early neocortical radial glial cells regulate the decision between stem cell maintenance and differentiation. J Neurosci 41:6969.
Fan XC, Steitz JA (1998) Overexpression of HuR, a nuclear-cytoplasmic shuttling protein, increases the in vivo stability of ARE-containing mRNAs. EMBO J 17:3448–3460.
Fogel BL, Wexler E, Wahnich A, Friedrich T, Vijayendran C, Gao F, Parikshak N, Konopka G, Geschwind DH (2012) RBFOX1 regulates both splicing and transcriptional networks in human neuronal development. Hum Mol Genet 21:4171–4186.
Franzoni E, Booker SA, Parthasarathy S, Rehfeld F, Grosser S, Srivatsa S, Fuchs H, Tarabykin V, Vida I, Wulczyn FG (2015) miR-128 regulates neuronal migration, outgrowth and intrinsic excitability via the intellectual disability gene Phf6. Elife 4:e04263.
Galloway A, Saveliev A, Łukasiak S, Hodson DJ, Bolland D, Balmanno K, Ahlfors H, Monzón-Casanova E, Mannurita SC, Bell LS, Andrews S, Díaz-Muñoz MD, Cook SJ, Corcoran A, Turner M (2016) RNA-binding proteins ZFP36L1 and ZFP36L2 promote cell quiescence. Science 352:453–459.
Gao L, Guan W, Wang M, Wang H, Yu J, Liu Q, Qiu B, Yu Y, Ping Y, Bian X, Shen L, Pei G (2017) Direct generation of human neuronal cells from adult astrocytes by small molecules. Stem Cell Reports 8:538–547.
García-Domínguez DJ, Morello D, Cisneros E, Kontoyiannis DL, Frade JM (2011) Stabilization of Dll1 mRNA by Elavl1/HuR in neuroepithelial cells undergoing mitosis. Mol Biol Cell 22:1227–1239.
Gehman LT, Stoilov P, Maguire J, Damianov A, Lin CH, Shiue L, Ares M, Mody I, Black DL (2011) The splicing regulator Rbfox1 (A2BP1) controls neuronal excitation in the mammalian brain. Nat Genet 43:706–711.
Giorgi C, Yeo GW, Stone ME, Katz DB, Burge C, Turrigiano G, Moore MJ (2007) The EJC factor eIF4AIII modulates synaptic strength and neuronal protein expression. Cell 130:179–191.
Gomes C, Lee SJ, Gardiner AS, Smith T, Sahoo PK, Patel P, Thames E, Rodriguez R, Taylor R, Yoo S, Heise T, Kar AN, Perrone-Bizzozero N, Twiss JL (2017) Axonal localization of neuritin/CPG15 mRNA is limited by competition for HuD binding. J Cell Sci 130:3650.
Guajardo L, Aguilar R, Bustos FJ, Nardocci G, Gutiérrez RA, van Zundert B, Montecino M (2020) Downregulation of the polycomb-associated methyltransferase ezh2 during maturation of hippocampal neurons is mediated by microRNAs let-7 and miR-124. Int J Mol Sci 21:8472.
Guo T, Pan X, Jiang G, Zhang D, Qi J, Shao L, Wang Z, Xu H, Zhao Y (2022) Downregulating PTBP1 fails to convert astrocytes into hippocampal neurons and to alleviate symptoms in Alzheimer's mouse models. J Neurosci 42:7309–7317.
Hambardzumyan D, Sergent-Tanguy S, Thinard R, Bonnamain V, Masip M, Fabre A, Boudin H, Neveu I, Naveilhan P (2009) AUF1 and Hu proteins in the developing rat brain: implication in the proliferation and differentiation of neural progenitors. J Neurosci Res 87:1296–1309.
Hao Y, Hu J, Xue Y, Dowdy SF, Mobley WC, Qian H, Fu XD (2023) Reply to: Ptbp1 deletion does not induce astrocyte-to-neuron conversion. Nature 618:E8–13.
Heinrich C, Blum R, Gascón S, Masserdotti G, Tripathi P, Sánchez R, Tiedt S, Schroeder T, Götz M, Berninger B (2010) Directing astroglia from the cerebral cortex into subtype specific functional neurons. PLoS Biol 8:e1000373.
Heinrich C, Bergami M, Gascón S, Lepier A, Viganò F, Dimou L, Sutor B, Berninger B, Götz M (2014) Sox2-mediated conversion of NG2 glia into induced neurons in the injured adult cerebral cortex. Stem Cell Reports 3:1000–1014.
Hinman MN, Lou H (2008) Diverse molecular functions of Hu proteins. Cell Mol Life Sci 65:3168–3181.
Hoang T, Kim DW, Appel H, Pannullo NA, Leavey P, Ozawa M, Zheng S, Yu M, Peachey NS, Blackshaw S (2022) Genetic loss of function of Ptbp1 does not induce glia-to-neuron conversion in retina. Cell Rep 39:110849.
Hoang T, Won Kim D, Appel H, Ozawa M, Zheng S, Kim J, Blackshaw S (2023) Matters arising Ptbp1 deletion does not induce astrocyte-to-neuron conversion. Nature 618:E1–7.
Huang T, Liu Y, Huang M, Zhao X, Cheng L (2010) Wnt1-cre-mediated conditional loss of Dicer results in malformation of the midbrain and cerebellum and failure of neural crest and dopaminergic differentiation in mice. J Mol Cell Biol 2:152–163.
Imai T, Tokunaga A, Yoshida T, Hashimoto M, Mikoshiba K, Weinmaster G, Nakafuku M, Okano H (2001) The neural RNA-binding protein Musashi1 translationally regulates mammalian numb gene expression by interacting with its mRNA. Mol Cell Biol 21:3888.
Ince-Dunn G, Okano HJ, Jensen KB, Park WY, Zhong R, Ule J, Mele A, Fak JJ, Yang CW, Zhang C, Yoo J, Herre M, Okano H, Noebels JL, Darnell RB (2012) Neuronal Elav-like (Hu) proteins regulate RNA splicing and abundance to control glutamate levels and neuronal excitability. Neuron 75:1067–1080.
Jacko M, Weyn-Vanhentenryck SM, Smerdon JW, Yan R, Feng H, Williams DJ, Pai J, Xu K, Wichterle H, Zhang C (2018) Rbfox splicing factors promote neuronal maturation and axon initial segment assembly. Neuron 97:853–868.
Jaffrey SR, Wilkinson MF (2018) Nonsense-mediated RNA decay in the brain: emerging modulator of neural development and disease. Nat Rev Neurosci 19:715–728.
Jolly LA, Homan CC, Jacob R, Barry S, Gecz J (2013) The UPF3B gene, implicated in intellectual disability, autism, ADHD and childhood onset schizophrenia regulates neural progenitor cell behaviour and neuronal outgrowth. Hum Mol Genet 22:4673–4687.
Karow M, Gray Camp J, Falk S, Gerber T, Pataskar A, Gac-Santel M, Kageyama J, Brazovskaja A, Garding A, Fan W, Riedemann T, Casamassa A, Smiyakin A, Schichor C, Götz M, Tiwari VK, Treutlein B, Berninger B (2018) Direct pericyte-to-neuron reprogramming via unfolding of a neural stem cell-like program. Nat Neurosci 21:932–940.
Kim KK, Nam J, Mukouyama YS, Kawamoto S (2013) Rbfox3-regulated alternative splicing of Numb promotes neuronal differentiation during development. J Cell Biol 200:443–458.
Kim KK, Yang Y, Zhu J, Adelstein RS, Kawamoto S (2014) Rbfox3 controls the biogenesis of a subset of microRNAs. Nat Struct Mol Biol 21:901–910.
Kohn DT, Tsai KC, Cansino VV, Neve RL, Perrone-Bizzozero NI (1996) Role of highly conserved pyrimidine-rich sequences in the 3′ untranslated region of the GAP-43 mRNA in mRNA stability and RNA-protein interactions. Mol Brain Res 36:240–250.
Kraushar ML, Thompson K, Wijeratne HRS, Viljetic B, Sakers K, Marson JW, Kontoyiannis DL, Buyske S, Hart RP, Rasin MR (2014) Temporally defined neocortical translation and polysome assembly are determined by the RNA-binding protein Hu antigen R. Proc Natl Acad Sci U S A 111:E3815–3824.
Laneve P, Gioia U, Andriotto A, Moretti F, Bozzoni I, Caffarelli E (2010) A minicircuitry involving REST and CREB controls miR-9-2 expression during human neuronal differentiation. Nucleic Acids Res 38:6895.
Laumonnier F, Shoubridge C, Antar C, Nguyen LS, Van Esch H, Kleefstra T, Briault S, Fryns JP, Hamel B, Chelly J, Ropers HH, Ronce N, Blesson S, Moraine C, Gécz J, Raynaud M (2010) Mutations of the UPF3B gene, which encodes a protein widely expressed in neurons, are associated with nonspecific mental retardation with or without autism. Mol Psychiatry 15:767–776.
Lee JA, Tang ZZ, Black DL (2009) An inducible change in Fox-1/A2BP1 splicing modulates the alternative splicing of downstream neuronal target exons. Genes Dev 23:2284–2293.
Lee JA, Damianov A, Lin CH, Fontes M, Parikshak NN, Anderson ES, Geschwind DH, Black DL, Martin KC (2016) Cytoplasmic Rbfox1 regulates the expression of synaptic and Autism-related genes. Neuron 89:113–128.
Lee SW, Oh YM, Lu YL, Kim WK, Yoo AS (2018) MicroRNAs overcome cell fate barrier by reducing EZH2-controlled REST stability during neuronal conversion of human adult fibroblasts. Dev Cell 46:73–84.
Li A, Chen YS, Ping XL, Yang X, Xiao W, Yang Y, Sun HY, Zhu Q, Baidya P, Wang X, Bhattarai DP, Zhao YL, Sun BF, Yang YG (2017a) Cytoplasmic m6A reader YTHDF3 promotes mRNA translation. Cell Res 27:444–447.
Li L, Zang L, Zhang F, Chen J, Shen H, Shu L, Liang F, Feng C, Chen D, Tao H, Xu T, Li Z, Kang Y, Wu H, Tang L, Zhang P, Jin P, Shu Q, Li X (2017b) Fat mass and obesity-associated (FTO) protein regulates adult neurogenesis. Hum Mol Genet 26:2398.
Li M, Zhao X, Wang W, Shi H, Pan Q, Lu Z, Perez SP, Suganthan R, He C, Bjørås M, Klungland A (2018) Ythdf2-mediated m6A mRNA clearance modulates neural development in mice. Genome Biol 19:69.
Li Q, Zheng S, Han A, Lin CH, Stoilov P, Fu XD, Black DL (2014) The splicing regulator PTBP2 controls a program of embryonic splicing required for neuronal maturation. Elife 3:e01201.
Li X, Zuo X, Jing J, Ma Y, Wang J, Liu D, Zhu J, Du X, Xiong L, Du Y, Xu J, Xiao X, Wang J, Chai Z, Zhao Y, Deng H (2015a) Small-molecule-driven direct reprogramming of mouse fibroblasts into functional neurons. Cell Stem Cell 17:195–203.
Li YI, Sanchez-Pulido L, Haerty W, Ponting CP (2015b) RBFOX and PTBP1 proteins regulate the alternative splicing of micro-exons in human brain transcripts. Genome Res 25:1–13.
Licatalosi DD, Mele A, Fak JJ, Ule J, Kayikci M, Chi SW, Clark TA, Schweitzer AC, Blume JE, Wang X, Darnell JC, Darnell RB (2008) HITS-CLIP yields genome-wide insights into brain alternative RNA processing. Nature 456:464–469.
Licatalosi DD, Yano M, Fak JJ, Mele A, Grabinski SE, Zhang C, Darnell RB (2012) Ptbp2 represses adult-specific splicing to regulate the generation of neuronal precursors in the embryonic brain. Genes Dev 26:1626–1642.
Lin L, Zhang M, Stoilov P, Chen L, Zheng S (2020) Developmental attenuation of neuronal apoptosis by neural-specific splicing of Bak1 microexon. Neuron 107:1180–1196.
Lin YS, Wang HY, Huang DF, Hsieh PF, Lin MY, Chou CH, Wu IJ, Huang GJ, Gau SSF, Huang HS (2016) Neuronal splicing regulator RBFOX3 (NeuN) regulates adult hippocampal neurogenesis and synaptogenesis. PLoS One 11:e0164164.
Linares AJ, Lin CH, Damianov A, Adams KL, Novitch BG, Black DL (2015) The splicing regulator PTBP1 controls the activity of the transcription factor Pbx1 during neuronal differentiation. Elife 4:e09268.
Livneh I, Moshitch-Moshkovitz S, Amariglio N, Rechavi G, Dominissini D (2019) The m6A epitranscriptome: transcriptome plasticity in brain development and function. Nat Rev Neurosci 21:36–51.
Llorian M, Schwartz S, Clark TA, Hollander D, Tan LY, Spellman R, Gordon A, Schweitzer AC, De La Grange P, Ast G, Smith CWJ (2010) Position-dependent alternative splicing activity revealed by global profiling of alternative splicing events regulated by PTB. Nat Struct Mol Biol 17:1114–1123.
Loffreda A, Rigamonti A, Barabino SML, Lenzken SC (2015) RNA-binding proteins in the regulation of miRNA activity: a focus on neuronal functions. Biomolecules 5:2363–2387.
Lou CH, Shao A, Shum EY, Espinoza JL, Huang L, Karam R, Wilkinson MF (2014) Posttranscriptional control of the stem cell and neurogenic programs by the nonsense-mediated RNA decay pathway. Cell Rep 6:748–764.
Lu YL, Liu Y, McCoy MJ, Yoo AS (2021) MiR-124 synergism with ELAVL3 enhances target gene expression to promote neuronal maturity. Proc Natl Acad Sci U S A 118:e2015454118.
Luo Z, Mu L, Zheng Y, Shen W, Li J, Xu L, Zhong B, Liu Y, Zhou Y (2020) NUMB enhances Notch signaling by repressing ubiquitination of NOTCH1 intracellular domain. J Mol Cell Biol 12:345–358.
Lykke-Andersen S, Jensen TH (2015) Nonsense-mediated mRNA decay: an intricate machinery that shapes transcriptomes. Nat Rev Mol Cell Biol 16:665–677.
Maimon R, Chillon-Marinas C, Snethlage CE, Singhal SM, McAlonis-Downes M, Ling K, Rigo F, Bennett CF, Da Cruz S, Hnasko TS, Muotri AR, Cleveland DW (2021) Therapeutically viable generation of neurons with antisense oligonucleotide suppression of PTB. Nat Neurosci 24:1089–1099.
Makeyev EV, Zhang J, Carrasco MA, Maniatis T (2007) The microRNA miR-124 promotes neuronal differentiation by triggering brain-specific alternative pre-mRNA splicing. Mol Cell 27:435–448.
Makita S, Takatori H, Nakajima H (2021) Post-transcriptional regulation of immune responses and inflammatory diseases by RNA-binding ZFP36 family proteins. Front Immunol 12:711633.
Matsuda T, Irie T, Katsurabayashi S, Hayashi Y, Nagai T, Hamazaki N, Adefuin AMD, Miura F, Ito T, Kimura H, Shirahige K, Takeda T, Iwasaki K, Imamura T, Nakashima K (2019) Pioneer factor NeuroD1 rearranges transcriptional and epigenetic profiles to execute microglia-neuron conversion. Neuron 101:472–485.
Merkurjev D, Hong WT, Iida K, Oomoto I, Goldie BJ, Yamaguti H, Ohara T, Kawaguchi SY, Hirano T, Martin KC, Pellegrini M, Wang DO (2018) Synaptic N6-methyladenosine (m6A) epitranscriptome reveals functional partitioning of localized transcripts. Nat Neurosci 21:1004–1014.
Neo WH, Yap K, Lee SH, Looi LS, Khandelia P, Neo SX, Makeyev EV, Su IH (2014) MicroRNA miR-124 controls the choice between neuronal and astrocyte differentiation by fine-tuning Ezh2 expression. J Biol Chem 289:20788–20801.
Nguyen LS, Kim HG, Rosenfeld JA, Shen Y, Gusella JF, Lacassie Y, Layman LC, Shaffer LG, Gécz J (2013) Contribution of copy number variants involving nonsense-mediated mRNA decay pathway genes to neuro-developmental disorders. Hum Mol Genet 22:1816–1825.
Ogawa Y, Yamaguchi J, Yano M, Uchiyama Y, Okano HJ (2018) Elavl3 regulates neuronal polarity through the alternative splicing of an embryo-specific exon in AnkyrinG. Neurosci Res 135:13–20.
Oh YM, Lee SW, Kim WK, Chen S, Church VA, Cates K, Li T, Zhang B, Dolle RE, Dahiya S, Pak SC, Silverman GA, Perlmutter DH, Yoo AS (2022) Age-related Huntington's disease progression modeled in directly reprogrammed patient-derived striatal neurons highlights impaired autophagy. Nat Neurosci 25:1420–1433.
Oh YM, Lee SW, Yoo AS (2023) Modeling Huntington disease through microRNA-mediated neuronal reprogramming identifies age-associated autophagy dysfunction driving the onset of neurodegeneration. Autophagy 19:2613–2615.
Otsuka H, Fukao A, Funakami Y, Duncan KE, Fujiwara T (2019) Emerging evidence of translational control by AU-rich element-binding proteins. Front Genet 10:438938.
Packer AN, Xing Y, Harper SQ, Jones L, Davidson BL (2008) The bifunctional microRNA miR-9/miR-9* regulates REST and CoREST and is downregulated in Huntington's disease. J Neurosci 28:14341–14346.
Pang ZP, Yang N, Vierbuchen T, Ostermeier A, Fuentes DR, Yang TQ, Citri A, Sebastiano V, Marro S, Südhof TC, Wernig M (2011) Induction of human neuronal cells by defined transcription factors. Nature 476:220–223.
Papadimitriou E, Koutsoudaki PN, Thanou I, Karagkouni D, Karamitros T, Chroni-Tzartou D, Gaitanou M, Gkemisis C, Margariti M, Xingi E, Tzartos SJ, Hatzigeorgiou AG, Thomaidou D (2023) A miR-124-mediated post-transcriptional mechanism controlling the cell fate switch of astrocytes to induced neurons. Stem Cell Reports 18:915–935.
Pascale A, Gusev PA, Amadio M, Dottorini T, Govoni S, Alkon DL, Quattrone A (2004) Increase of the RNA-binding protein HuD and posttranscriptional up-regulation of the GAP-43 gene during spatial memory. Proc Natl Acad Sci U S A 101:1217–1222.
Pataskar A, Jung J, Smialowski P, Noack F, Calegari F, Straub T, Tiwari VK (2016) NeuroD1 reprograms chromatin and transcription factor landscapes to induce the neuronal program. EMBO J 35:24–45.
Păun O, Tan YX, Patel H, Strohbuecker S, Ghanate A, Cobolli-Gigli C, Sopena ML, Gerontogianni L, Goldstone R, Ang SL, Guillemot F, Dias C (2023) Pioneer factor ASCL1 cooperates with the mSWI/SNF complex at distal regulatory elements to regulate human neural differentiation. Genes Dev 37:218–242.
Pereira M, Birtele M, Shrigley S, Benitez JA, Hedlund E, Parmar M, Ottosson DR (2017) Direct reprogramming of resident NG2 glia into neurons with properties of fast-spiking parvalbumin-containing interneurons. Stem Cell Reports 9:742–751.
Petersen PH, Tang H, Zou K, Zhong W (2006) The enigma of the numb-Notch relationship during mammalian embryogenesis. Dev Neurosci 28:156–168.
Pilaz LJ, Silver DL (2015) Post-transcriptional regulation in corticogenesis: how RNA-binding proteins help build the brain. Wiley Interdiscip Rev RNA 6:501.
Popovitchenko T, Park Y, Page NF, Luo X, Krsnik Z, Liu Y, Salamon I, Stephenson JD, Kraushar ML, Volk NL, Patel SM, Wijeratne HRS, Li D, Suthar KS, Wach A, Sun M, Arnold SJ, Akamatsu W, Okano H, Paillard L, et al. (2020) Translational derepression of Elavl4 isoforms at their alternative 5′ UTRs determines neuronal development. Nat Commun 11:1674.
Qian H, Kang X, Hu J, Zhang D, Liang Z, Meng F, Zhang X, Xue Y, Maimon R, Dowdy SF, Devaraj NK, Zhou Z, Mobley WC, Cleveland DW, Fu XD (2020) Reversing a model of Parkinson's disease with in situ converted nigral neurons. Nature 582:550–556.
Racca C, Gardiol A, Eom T, Ule J, Triller A, Darnel RB (2010) The neuronal splicing factor nova co-localizes with target RNAs in the dendrite. Front Neural Circuits 4:5.
Rajman M, Schratt G (2017) MicroRNAs in neural development: from master regulators to fine-tuners. Development 144:2310–2322.
Ratti A, Fallini C, Cova L, Fantozzi R, Calzarossa C, Zennaro E, Pascale A, Quattrone A, Silani V (2006) A role for the ELAV RNA-binding proteins in neural stem cells: stabilization of Msi1 mRNA. J Cell Sci 119:1442–1452.
Ray D, Kazan H, Cook KB, Weirauch MT, Najafabadi HS, Li X, Gueroussov S, Albu M, Zheng H, Yang A, Na H, Irimia M, Matzat LH, Dale RK, Smith SA, Yarosh CA, Kelly SM, Nabet B, Mecenas D, Li W, et al. (2013) A compendium of RNA-binding motifs for decoding gene regulation. Nature 499:172–177.
Rivetti Di Val Cervo P, Romanov RA, Spigolon G, Masini D, Martín-Montañez E, Toledo EM, La Manno G, Feyder M, Pifl C, Ng YH, Sánchez SP, Linnarsson S, Wernig M, Harkany T, Fisone G, Arenas E (2017) Induction of functional dopamine neurons from human astrocytes in vitro and mouse astrocytes in a Parkinson's disease model. Nat Biotechnol 35:444–452.
Saito Y, Miranda-Rottmann S, Ruggiu M, Park CY, Fak JJ, Zhong R, Duncan JS, Fabella BA, Junge HJ, Chen Z, Araya R, Fritzsch B, Hudspeth AJ, Darnell RB (2016) NOVA2-mediated RNA regulation is required for axonal pathfinding during development. Elife 5:e14371.
Saito Y, Yuan Y, Zucker-Scharff I, Fak JJ, Jereb S, Tajima Y, Licatalosi DD, Darnell RB (2019) Differential NOVA2-mediated splicing in excitatory and inhibitory neurons regulates cortical development and cerebellar function. Neuron 101:707–720.
Sakakibara SI, Imai T, Hamaguchi K, Okabe M, Aruga J, Nakajima K, Yasutomi D, Nagata T, Kurihara Y, Uesugi S, Miyata T, Ogawa M, Mikoshiba K, Okano H (1996) Mouse-Musashi-1, a neural RNA-binding protein highly enriched in the mammalian CNS stem cell. Dev Biol 176:230–242.
Santos MCT, Tegge AN, Correa BR, Mahesula S, Kohnke LQ, Qiao M, Ferreira MAR, Kokovay E, Penalva LOF (2016) MiR-124, -128, and -137 orchestrate neural differentiation by acting on overlapping gene sets containing a highly connected transcription factor network. Stem Cells 34:220–232.
Scheckel C, Drapeau E, Frias MA, Park CY, Fak J, Zucker-Scharff I, Kou Y, Haroutunian V, Ma'ayan A, Buxbaum JD, Darnell RB (2016) Regulatory consequences of neuronal ELAV-like protein binding to coding and non-coding RNAs in human brain. Elife 5:e10421.
Sena RM, Twiss JL, Gardiner AS, Dell'orco M, Linsenbardt DN, Perrone-Bizzozero NI (2021) The RNA-binding protein HuD regulates alternative splicing and alternative polyadenylation in the mouse neocortex. Molecules 26:2836.
Slobodin B, Han R, Calderone V, Vrielink JAFO, Loayza-Puch F, Elkon R, Agami R (2017) Transcription impacts the efficiency of mRNA translation via co-transcriptional N6-adenosine methylation. Cell 169:326–337.
Smith DK, Yang J, Liu ML, Zhang CL (2016) Small molecules modulate chromatin accessibility to promote NEUROG2-mediated fibroblast-to-neuron reprogramming. Stem Cell Reports 7:955–969.
Sokpor G, Xie Y, Nguyen HP, Tuoc T (2021) Emerging role of m6 A methylome in brain development: implications for neurological disorders and potential treatment. Front Cell Dev Biol 9:656849.
Spellman R, Llorian M, Smith CWJ (2007) Crossregulation and functional redundancy between the splicing regulator PTB and its paralogs nPTB and ROD1. Mol Cell 27:420–434.
Störchel PH, Thümmler J, Siegel G, Aksoy‐Aksel A, Zampa F, Sumer S, Schratt G (2015) A large‐scale functional screen identifies N ova1 and N coa3 as regulators of neuronal mi RNA function. EMBO J 34:2237–2254.
Suzuki F, Okuno M, Tanaka T, Sanuki R (2020) Overexpression of neural miRNAs miR-9/9* and miR-124 suppresses differentiation to Müller glia and promotes differentiation to neurons in mouse retina in vivo. Genes Cells 25:741–752.
Tomassoni-Ardori F, Fulgenzi G, Becker J, Barrick C, Palko ME, Kuhn S, Koparde V, Cam M, Yanpallewar S, Oberdoerffer S, Tessarollo L (2019) Rbfox1 up-regulation impairs bdnf dependent hippocampal LTP by dysregulating TrkB isoform expression levels. Elife 8:e49673.
Tsai KC, Cansino VV, Kohn DT, Neve RL, Perrone-Bizzozero NI (1997) Post-transcriptional regulation of the GAP-43 gene by specific sequences in the 3' untranslated region of the mRNA. J Neurosci 17:1950–1958.
Ule J, Ule A, Spencer J, Williams A, Hu JS, Cline M, Wang H, Clark T, Fraser C, Ruggiu M, Zeeberg BR, Kane D, Weinstein JN, Blume J, Darnell RB (2005) Nova regulates brain-specific splicing to shape the synapse. Nat Genet 37:844–852.
Velasco MX, Kosti A, Guardia GDA, Santos MC, Tegge A, Qiao M, Correa BRS, Hernández G, Kokovay E, Galante PAF, Penalva LOF (2019) Antagonism between the RNA-binding protein Musashi1 and miR-137 and its potential impact on neurogenesis and glioblastoma development. RNA 27:768–782.
Victor MB, Richner M, Hermanstyne TO, Ransdell JL, Sobieski C, Deng PY, Klyachko VA, Nerbonne JM, Yoo AS (2014) Generation of human striatal neurons by microRNA-dependent direct conversion of fibroblasts. Neuron 84:311–323.
Victor MB, Richner M, Olsen HE, Lee SW, Monteys AM, Ma C, Huh CJ, Zhang B, Davidson BL, Yang XW, Yoo AS (2018) Striatal neurons directly converted from Huntington's disease patient fibroblasts recapitulate age-associated disease phenotypes. Nat Neurosci 21:341–352.
Vierbuchen T, Ostermeier A, Pang ZP, Kokubu Y, Südhof TC, Wernig M (2010) Direct conversion of fibroblasts to functional neurons by defined factors. Nature 463:1035–1041.
Visvanathan J, Lee S, Lee B, Lee JW, Lee SK (2007) The microRNA miR-124 antagonizes the anti-neural REST/SCP1 pathway during embryonic CNS development. Genes Dev 21:744–749.
Vo DT, Qiao M, Smith AD, Burns SC, Brenner AJ, Penalva LOF (2011) The oncogenic RNA-binding protein Musashi1 is regulated by tumor suppressor miRNAs. RNA Biol 8:817–828.
Vogel KU, Bell LS, Galloway A, Ahlfors H, Turner M (2016) The RNA-binding proteins Zfp36l1 and Zfp36l2 enforce the thymic β-selection checkpoint by limiting DNA damage response signaling and cell cycle progression. J Immunol 197:2673–2685.
Vuong CK, Wei W, Lee JA, Lin CH, Damianov A, de la Torre-Ubieta L, Halabi R, Otis KO, Martin KC, O'Dell TJ, Black DL (2018) Rbfox1 regulates synaptic transmission through the inhibitory neuron-specific vSNARE Vamp1. Neuron 98:127–141.
Vuong JK, Lin CH, Zhang M, Chen L, Black DL, Zheng S (2016) PTBP1 and PTBP2 serve both specific and redundant functions in neuronal pre-mRNA splicing. Cell Rep 17:2766–2775.
Wang F, Tidei JJ, Polich ED, Gao Y, Zhao H, Perrone-Bizzozero NI, Guo W, Zhao X (2015a) Positive feedback between RNA-binding protein HuD and transcription factor SATB1 promotes neurogenesis. Proc Natl Acad Sci U S A 112:E4995–5004.
Wang G, Jiang B, Jia C, Chai B, Liang A (2013) MicroRNA 125 represses nonsense-mediated mRNA decay by regulating SMG1 expression. Biochem Biophys Res Commun 435:16–20.
Wang HY, Hsieh PF, Huang DF, Chin PS, Chou CH, Tung CC, Chen SY, Lee LJ, Gau SSF, Huang HS (2015b) RBFOX3/NeuN is required for hippocampal circuit balance and function. Sci Rep 5:17383.
Wang LL, Serrano C, Zhong X, Ma S, Zou Y, Zhang CL (2021) Revisiting astrocyte to neuron conversion with lineage tracing in vivo. Cell 184:5465–5481.
Wang LL, Zhang CL (2023) Therapeutic potential of PTBP1 inhibition, if any, is not attributed to glia-to-neuron conversion. Annu Rev Neurosci 46:1–15.
Wang Y, Guo Y, Tang C, Han X, Xu M, Sun J, Zhao Y, Zhang Y, Wang M, Cao X, Zhu X, Guo W (2019) Developmental cytoplasmic-to-nuclear translocation of RNA-binding protein HuR is required for adult neurogenesis. Cell Rep 29:3101–3117.
Wapinski OL, Vierbuchen T, Qu K, Lee QY, Chanda S, Fuentes DR, Giresi PG, Ng YH, Marro S, Neff NF, Drechsel D, Martynoga B, Castro DS, Webb AE, Südhof TC, Brunet A, Guillemot F, Chang HY, Wernig M (2013) Hierarchical mechanisms for direct reprogramming of fibroblasts to neurons. Cell 155:621–635.
Wei-Lin Popp M, Maquat LE (2013) Organizing principles of mammalian nonsense-mediated mRNA decay. Annu Rev Genet 47:139–165.
Weinberg MS, Criswell HE, Powell SK, Bhatt AP, McCown TJ (2017) Viral vector reprogramming of adult resident striatal oligodendrocytes into functional neurons. Mol Ther 25:928–934.
Weyn-Vanhentenryck SM, Mele A, Yan Q, Sun S, Farny N, Zhang Z, Xue C, Herre M, Silver PA, Zhang MQ, Krainer AR, Darnell RB, Zhang C (2014) HITS-CLIP and integrative modeling define the Rbfox splicing-regulatory network linked to brain development and autism. Cell Rep 6:1139–1152.
Widagdo J, Zhao QY, Kempen MJ, Tan MC, Ratnu VS, Wei W, Leighton L, Spadaro PA, Edson J, Anggono V, Bredy TW (2016) Experience-dependent accumulation of N6-methyladenosine in the prefrontal cortex is associated with memory processes in mice. J Neurosci 36:6771–6777.
Widagdo J, Anggono V (2018) The m6A-epitranscriptomic signature in neurobiology: from neurodevelopment to brain plasticity. J Neurochem 147:137–152.
Wohl SG, Reh TA (2016) miR-124-9-9* potentiates Ascl1-induced reprogramming of cultured Müller glia. Glia 64:743–762.
Wohl SG, Hooper MJ, Reh TA (2019) MicroRNAs miR-25, let-7 and miR-124 regulate the neurogenic potential of Müller glia in mice. Development 146:dev179556.
Xiao W, Adhikari S, Dahal U, Chen YS, Hao YJ, Sun BF, Sun HY, Li A, Ping XL, Lai WY, Wang X, Ma HL, Huang CM, Yang Y, Huang N, Jiang GB, Wang HL, Zhou Q, Wang XJ, Zhao YL, et al. (2016) Nuclear m6A reader YTHDC1 regulates mRNA splicing. Mol Cell 61:507–519.
Xie Y, Zhou J, Chen B (2022) Critical examination of Ptbp1-mediated glia-to-neuron conversion in the mouse retina. Cell Rep 39:110960.
Xue Y, Zhou Y, Wu T, Zhu T, Ji X, Kwon YS, Zhang C, Yeo G, Black DL, Sun H, Fu XD, Zhang Y (2009) Genome-wide analysis of PTB-RNA interactions reveals a strategy used by the general splicing repressor to modulate exon inclusion or skipping. Mol Cell 36:996–1006.
Xue Y, Ouyang K, Huang J, Zhou Y, Ouyang H, Li H, Wang G, Wu Q, Wei C, Bi Y, Jiang L, Cai Z, Sun H, Zhang K, Zhang Y, Chen J, Fu XD (2013) Direct conversion of fibroblasts to neurons by reprogramming PTB-regulated MicroRNA circuits. Cell 152:82–96.
Xue Y, Qian H, Hu J, Zhou B, Zhou Y, Hu X, Karakhanyan A, Pang Z, Fu XD (2016) Sequential regulatory loops as key gatekeepers for neuronal reprogramming in human cells. Nat Neurosci 19:807–815.
Yang RY, Chai R, Pan JY, Bao JY, Xia PH, Wang YK, Chen Y, Li Y, Wu J, Chen G (2023) Knockdown of polypyrimidine tract binding protein facilitates motor function recovery after spinal cord injury. Neural Regen Res 18:396.
Yang Y, Hsu PJ, Chen YS, Yang YG (2018) Dynamic transcriptomic m6A decoration: writers, erasers, readers and functions in RNA metabolism. Cell Res 2018 286 28:616–624.
Yano M, Hayakawa-Yano Y, Mele A, Darnell RB (2010) Nova2 regulates neuronal migration through an RNA switch in disabled-1 signaling. Neuron 66:848–858.
Yeom KH, Mitchell S, Linares AJ, Zheng S, Lin CH, Wang XJ, Hoffmann A, Black DL (2018) Polypyrimidine tract-binding protein blocks miRNA-124 biogenesis to enforce its neuronal-specific expression in the mouse. Proc Natl Acad Sci U S A 115:E11061–11070.
Yoo AS, Staahl BT, Chen L, Crabtree GR (2009) MicroRNA-mediated switching of chromatin-remodelling complexes in neural development. Nature 460:642–646.
Yoo AS, Sun AX, Li L, Shcheglovitov A, Portmann T, Li Y, Lee-Messer C, Dolmetsch RE, Tsien RW, Crabtree GR (2011) MicroRNA-mediated conversion of human fibroblasts to neurons. Nature 476:228–231.
Yoon KJ, Ringeling FR, Vissers C, Jacob F, Pokrass M, Jimenez-Cyrus D, Su Y, Kim NS, Zhu Y, Zheng L, Kim S, Wang X, Doré LC, Jin P, Regot S, Zhuang X, Canzar S, He C, Ming GL, Song H (2017) Temporal control of mammalian cortical neurogenesis by m6A methylation. Cell 171:877.
Yuzwa SA, Borrett MJ, Innes BT, Voronova A, Ketela T, Kaplan DR, Bader GD, Miller FD (2017) Developmental emergence of adult neural stem cells as revealed by single-cell transcriptional profiling. Cell Rep 21:3970–3986.
Zhang C, Frias MA, Mele A, Ruggiu M, Eom T, Marney CB, Wang H, Licatalosi DD, Fak JJ, Darnell RB (2010) Integrative modeling defines the Nova splicing-regulatory network and its combinatorial controls. Science 329:439–443.
Zhang W, Kim PJ, Chen Z, Lokman H, Qiu L, Zhang K, Rozen SG, Tan EK, Je HS, Zeng L (2016) MiRNA-128 regulates the proliferation and neurogenesis of neural precursors by targeting PCM1 in the developing cortex. Elife 5:e11324.
Zheng S, Gray EE, Chawla G, Porse BT, O'Dell TJ, Black DL (2012) PSD-95 is post-transcriptionally repressed during early neural development by PTBP1 and PTBP2. Nat Neurosci 15:381–388.
Zhou H, Su J, Hu X, Zhou C, Li H, Chen Z, Xiao Q, Wang B, Wu W, Sun Y, Zhou Y, Tang C, Liu F, Wang L, Feng C, Liu M, Li S, Zhang Y, Xu H, Yao H, et al. (2020) Glia-to-neuron conversion by CRISPR-CasRx alleviates symptoms of neurological disease in mice. Cell 181:590–603.
Zhu H, Hasman RA, Barron VA, Luo G, Lou H (2006) A nuclear function of Hu proteins as neuron-specific alternative RNA processing regulators. Mol Biol Cell 17:5105–5114.
Zimmerman AJ, Hafez AK, Amoah SK, Rodriguez BA, Dell'Orco M, Lozano E, Hartley BJ, Alural B, Lalonde J, Chander P, Webster MJ, Perlis RH, Brennand KJ, Haggarty SJ, Weick J, Perrone-Bizzozero N, Brigman JL, Mellios N (2020) A psychiatric disease-related circular RNA controls synaptic gene expression and cognition. Mol Psychiatry 25:2712–2727.