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Spatial enhancer activation influences inhibitory neuron identity during mouse embryonic development.

التفاصيل البيبلوغرافية
العنوان: Spatial enhancer activation influences inhibitory neuron identity during mouse embryonic development.
المؤلفون: Dvoretskova E; Max Planck Institute for Biological Intelligence, Martinsried, Germany.; Max Planck Institute of Neurobiology, Martinsried, Germany., Ho MC; Max Planck Institute for Biological Intelligence, Martinsried, Germany.; Max Planck Institute of Neurobiology, Martinsried, Germany., Kittke V; Institute of Neurogenomics, Helmholtz Zentrum München GmbH, German Research Center for Environmental Health, Neuhererg, Germany.; TUM School of Medicine and Health, Institute of Human Genetics, Technical University of Munich, Munich, Germany.; DZPG (German Center for Mental Health), Munich, Germany., Neuhaus F; Max Planck Institute for Biological Intelligence, Martinsried, Germany.; Max Planck Institute of Neurobiology, Martinsried, Germany., Vitali I; Max Planck Institute for Biological Intelligence, Martinsried, Germany.; Max Planck Institute of Neurobiology, Martinsried, Germany., Lam DD; Institute of Neurogenomics, Helmholtz Zentrum München GmbH, German Research Center for Environmental Health, Neuhererg, Germany.; TUM School of Medicine and Health, Institute of Human Genetics, Technical University of Munich, Munich, Germany., Delgado I; Cardiovascular Development Program, Centro Nacional de Investigaciones Cardiovasculares (CNIC), Madrid, Spain.; Centro de Investigación Biomédica en Red de Enfermedades Cardiovasculares (CIBERCV), Madrid, Spain.; Departamento de Genética, Fisiología y Microbiología, Facultad de Biología, Universidad Complutense de Madrid, Madrid, Spain., Feng C; Max Planck Institute for Biological Intelligence, Martinsried, Germany.; Max Planck Institute of Neurobiology, Martinsried, Germany., Torres M; Cardiovascular Development Program, Centro Nacional de Investigaciones Cardiovasculares (CNIC), Madrid, Spain.; Centro de Investigación Biomédica en Red de Enfermedades Cardiovasculares (CIBERCV), Madrid, Spain., Winkelmann J; Institute of Neurogenomics, Helmholtz Zentrum München GmbH, German Research Center for Environmental Health, Neuhererg, Germany.; TUM School of Medicine and Health, Institute of Human Genetics, Technical University of Munich, Munich, Germany.; DZPG (German Center for Mental Health), Munich, Germany.; Munich Cluster for Systems Neurology (SyNergy), Munich, Germany., Mayer C; Max Planck Institute for Biological Intelligence, Martinsried, Germany. christian.mayer@bi.mpg.de.; Max Planck Institute of Neurobiology, Martinsried, Germany. christian.mayer@bi.mpg.de.
المصدر: Nature neuroscience [Nat Neurosci] 2024 May; Vol. 27 (5), pp. 862-872. Date of Electronic Publication: 2024 Mar 25.
نوع المنشور: Journal Article; Research Support, Non-U.S. Gov't
اللغة: English
بيانات الدورية: Publisher: Nature Publishing Group Country of Publication: United States NLM ID: 9809671 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1546-1726 (Electronic) Linking ISSN: 10976256 NLM ISO Abbreviation: Nat Neurosci Subsets: MEDLINE
أسماء مطبوعة: Publication: <2002->: New York, NY : Nature Publishing Group
Original Publication: New York, NY : Nature America Inc., c1998-
مواضيع طبية MeSH: Homeodomain Proteins*/metabolism , Homeodomain Proteins*/genetics , Transcription Factors*/metabolism , Transcription Factors*/genetics , Gene Expression Regulation, Developmental* , Embryonic Development*/physiology , Enhancer Elements, Genetic*/genetics, Animals ; Mice ; GABAergic Neurons/metabolism ; GABAergic Neurons/physiology ; Cell Differentiation/physiology ; Interneurons/metabolism ; Interneurons/physiology ; LIM-Homeodomain Proteins/metabolism ; LIM-Homeodomain Proteins/genetics ; Neurogenesis/physiology ; Nerve Tissue Proteins
مستخلص: The mammalian telencephalon contains distinct GABAergic projection neuron and interneuron types, originating in the germinal zone of the embryonic basal ganglia. How genetic information in the germinal zone determines cell types is unclear. Here we use a combination of in vivo CRISPR perturbation, lineage tracing and ChIP-sequencing analyses and show that the transcription factor MEIS2 favors the development of projection neurons by binding enhancer regions in projection-neuron-specific genes during mouse embryonic development. MEIS2 requires the presence of the homeodomain transcription factor DLX5 to direct its functional activity toward the appropriate binding sites. In interneuron precursors, the transcription factor LHX6 represses the MEIS2-DLX5-dependent activation of projection-neuron-specific enhancers. Mutations of Meis2 result in decreased activation of regulatory enhancers, affecting GABAergic differentiation. We propose a differential binding model where the binding of transcription factors at cis-regulatory elements determines differential gene expression programs regulating cell fate specification in the mouse ganglionic eminence.
(© 2024. The Author(s).)
References: Bandler, R. C. & Mayer, C. Deciphering inhibitory neuron development: the paths to diversity. Curr. Opin. Neurobiol. 79, 102691 (2023). (PMID: 36805715)
Leung, R. F. et al. Genetic regulation of vertebrate forebrain development by homeobox genes. Front. Neurosci. 16, 843794 (2022). (PMID: 355468729081933)
Zug, R. Developmental disorders caused by haploinsufficiency of transcriptional regulators: a perspective based on cell fate determination. Biol. Open 11, bio058896 (2022). (PMID: 350893358801891)
Lindtner, S. et al. Genomic resolution of Dlx-orchestrated transcriptional circuits driving development of forebrain GABAergic neurons. Cell Rep. 28, 2048–2063 (2019).
Su, Z. et al. Dlx1/2-dependent expression of Meis2 promotes neuronal fate determination in the mammalian striatum. Development 149, dev200035 (2022). (PMID: 351566808918808)
Giliberti, A. et al. Meis2 gene is responsible for intellectual disability, cardiac defects and a distinct facial phenotype. Eur. J. Med. Genet. 63, 103627 (2020). (PMID: 30735726)
Verheije, R. et al. Heterozygous loss-of-function variants of Meis2 cause a triad of palatal defects, congenital heart defects and intellectual disability. Eur. J. Hum. Genet. 27, 278–290 (2019). (PMID: 30291340)
Bandler, R. C. et al. Single-cell delineation of lineage and genetic identity in the mouse brain. Nature 601, 404–409 (2022). (PMID: 34912118)
Datlinger, P. et al. Pooled CRISPR screening with single-cell transcriptome readout. Nat. Methods 14, 297–301 (2017). (PMID: 280994305334791)
Platt, R. J. et al. CRISPR–Cas9 knockin mice for genome editing and cancer modeling. Cell 159, 440–455 (2014). (PMID: 252633304265475)
Anderson, S. A., Marín, O., Horn, C., Jennings, K. & Rubenstein, J. L. Distinct cortical migrations from the medial and lateral ganglionic eminences. Development 128, 353–363 (2001). (PMID: 11152634)
Korsunsky, I. et al. Fast, sensitive and accurate integration of single-cell data with harmony. Nat. Methods 16, 1289–1296 (2019). (PMID: 317408196884693)
Hao, Y. et al. Integrated analysis of multimodal single-cell data. Cell 184, 3573–3587 (2021).
Song, X. et al. Homeobox gene Six3 is required for the differentiation of D2-type medium spiny neurons. Neurosci. Bull. 37, 985–998 (2021). (PMID: 340145548275777)
Knowles, R., Dehorter, N. & Ellender, T. From progenitors to progeny: shaping striatal circuit development and function. J. Neurosci. 41, 9483–9502 (2021). (PMID: 347895608612473)
Lim, L., Mi, D., Llorca, A. & Marín, O. Development and functional diversification of cortical interneurons. Neuron 100, 294–313 (2018). (PMID: 303595986290988)
Miyoshi, G. et al. Prox1 regulates the subtype-specific development of caudal ganglionic eminence-derived GABAergic cortical interneurons. J. Neurosci. 35, 12869–12889 (2015). (PMID: 263774734571608)
Batista-Brito, R., Machold, R., Klein, C. & Fishell, G. Gene expression in cortical interneuron precursors is prescient of their mature function. Cereb. Cortex 18, 2306–2317 (2008). (PMID: 182500822536702)
Subashini, C. et al. Wnt5a is a crucial regulator of neurogenesis during cerebellum development. Sci. Rep. 7, 42523 (2017). (PMID: 282055315311982)
Gorkin, D. U. et al. An atlas of dynamic chromatin landscapes in mouse fetal development. Nature 583, 744–751 (2020). (PMID: 327282407398618)
Chang, C. P. et al. MEIS proteins are major in vivo DNA binding partners for wild-type but not chimeric Pbx proteins. Mol. Cell Biol. 17, 5679–5687 (1997). (PMID: 9315626232416)
Shen, W. F. et al. AbdB-like Hox proteins stabilize DNA binding by the Meis1 homeodomain proteins. Mol. Cell Biol. 17, 6448–6458 (1997). (PMID: 9343407232497)
Mayer, C. et al. Developmental diversification of cortical inhibitory interneurons. Nature 555, 457–462 (2018). (PMID: 295136536052457)
Flames, N. et al. Delineation of multiple subpallial progenitor domains by the combinatorial expression of transcriptional codes. J. Neurosci.27, 9682–9695 (2007). (PMID: 178046294916652)
Jolma, A. et al. DNA-dependent formation of transcription factor pairs alters their binding specificity. Nature 527, 384–388 (2015). (PMID: 26550823)
Visel, A., Minovitsky, S., Dubchak, I. & Pennacchio, L. A. VISTA enhancer browser—a database of tissue-specific human enhancers. Nucleic Acids Res. 35, D88–D92 (2007). (PMID: 17130149)
Rhodes, C. T. et al. An epigenome atlas of neural progenitors within the embryonic mouse forebrain. Nat. Commun. 13, 4196 (2022). (PMID: 358589159300614)
den Hoed, J., Devaraju, K. & Fisher, S. E. Molecular networks of the FOXP2 transcription factor in the brain. EMBO Rep. 22, e52803 (2021).
Molotkova, N., Molotkov, A. & Duester, G. Role of retinoic acid during forebrain development begins late when Raldh3 generates retinoic acid in the ventral subventricular zone. Dev. Biol. 303, 601–610 (2007). (PMID: 17207476)
Toresson, H., Mata de Urquiza, A., Fagerström, C., Perlmann, T. & Campbell, K. Retinoids are produced by glia in the lateral ganglionic eminence and regulate striatal neuron differentiation. Development 126, 1317–1326 (1999). (PMID: 10021349)
Chatzi, C., Brade, T. & Duester, G. Retinoic acid functions as a key GABAergic differentiation signal in the basal ganglia. PLoS Biol. 9, e1000609 (2011). (PMID: 215327333075211)
Bandler, R. C., Mayer, C. & Fishell, G. Cortical interneuron specification: the juncture of genes, time and geometry. Curr. Opin. Neurobiol. 42, 17–24 (2017). (PMID: 27889625)
Zhao, Y. et al. Distinct molecular pathways for development of telencephalic interneuron subtypes revealed through analysis of lhx6 mutants. J. Comp. Neurol. 510, 79–99 (2008). (PMID: 186131212547494)
Vogt, D. et al. Lhx6 directly regulates Arx and CXCR7 to determine cortical interneuron fate and laminar position. Neuron 82, 350–364 (2014). (PMID: 247424604261952)
Sandberg, M. et al. Transcriptional networks controlled by NKX2-1 in the development of forebrain GABAergic neurons. Neuron 91, 1260–1275 (2016). (PMID: 276574505319854)
Shang, Z. et al. The transcription factor Zfp503 promotes the D1 MSN identity and represses the D2 MSN identity. Front. Cell Dev. Biol. 10, 948331 (2022). (PMID: 360819089445169)
Su-Feher, L. et al. Single cell enhancer activity distinguishes GABAergic and cholinergic lineages in embryonic mouse basal ganglia. Proc. Natl Acad. Sci. USA 119, e2108760119 (2022). (PMID: 353777979169651)
Asgarian, Z. et al. MTG8 interacts with IHX6 to specify cortical interneuron subtype identity. Nat. Commun. 13, 5217 (2022). (PMID: 360645479445035)
Kim, H., Berens, N. C., Ochandarena, N. E. & Philpot, B. D. Region and cell type distribution of TCFf4 in the postnatal mouse brain. Front. Neuroanat. 14, 42 (2020). (PMID: 327652287379912)
Jin, X. et al. In vivo perturb-seq reveals neuronal and glial abnormalities associated with autism risk genes. Science 370, eaaz6063 (2020). (PMID: 332438617985844)
DeTomaso, D. & Yosef, N. Hotspot identifies informative gene modules across modalities of single-cell genomics. Cell Syst. 12, 446–456 (2021).
Berenguer, M. & Duester, G. Retinoic acid, RARs and early development. J. Mol. Endocrinol. 69, T59–T67 (2022). (PMID: 355933899561040)
Mesman, S., Bakker, R. & Smidt, M. P. TCF4 is required for correct brain development during embryogenesis. Mol. Cell. Neurosci. 106, 103502 (2020). (PMID: 32474139)
Marklund, M. et al. Retinoic acid signalling specifies intermediate character in the developing telencephalon. Development 131, 4323–4332 (2004). (PMID: 15294870)
Storm, E. E. et al. Dose-dependent functions of Fgf8 in regulating telencephalic patterning centers. Development 133, 1831–1844 (2006). (PMID: 16613831)
Borello, U. et al. Fgf15 promotes neurogenesis and opposes Fgf8 function during neocortical development. Neural Dev. 3, 17 (2008). (PMID: 186250632492847)
Hunt, C. P. J. et al. Understanding and modeling regional specification of the human ganglionic eminence. Stem Cell Rep. 18, 654–671 (2023).
Bridoux, L. et al. Hox paralogs selectively convert binding of ubiquitous transcription factors into tissue-specific patterns of enhancer activation. PLoS Genet. 16, e1009162 (2020). (PMID: 333158567769617)
Schulte, D. & Geerts, D. Meis transcription factors in development and disease. Development 146, dev174706 (2019). (PMID: 31416930)
Delgado, I. et al. Control of mouse limb initiation and antero-posterior patterning by Meis transcription factors. Nat. Commun. 12, 3086 (2021). (PMID: 340352678149412)
Selleri, L., Zappavigna, V. & Ferretti, E. ’Building a perfect body’: control of vertebrate organogenesis by PBX-dependent regulatory networks. Genes Dev. 33, 258–275 (2019). (PMID: 308245326411007)
Agoston, Z. et al. Meis2 is a Pax6 co-factor in neurogenesis and dopaminergic periglomerular fate specification in the adult olfactory bulb. Development 141, 28–38 (2014). (PMID: 24284204)
Hobert, O. & Westphal, H. Functions of LIM-homeobox genes. Trends Genet. 16, 75–83 (2000). (PMID: 10652534)
Zhang, Z. et al. The LIM homeodomain transcription factor LHX6: a transcriptional repressor that interacts with pituitary homeobox 2 (PITX2) to regulate odontogenesis. J. Biol. Chem. 288, 2485–2500 (2013). (PMID: 23229549)
Chapman, H. et al. Gsx transcription factors control neuronal versus glial specification in ventricular zone progenitors of the mouse lateral ganglionic eminence. Dev. Biol. 442, 115–126 (2018). (PMID: 299904756158017)
Ypsilanti, A. R. et al. Transcriptional network orchestrating regional patterning of cortical progenitors. Proc. Natl Acad. Sci. USA 118, e2024795118 (2021). (PMID: 349211128713794)
Delás, M. J. et al. Developmental cell fate choice in neural tube progenitors employs two distinct cis-regulatory strategies. Dev. Cell 58, 3–17 (2023).
Kim, S. et al. DNA-guided transcription factor cooperativity shapes face and limb mesenchyme. Cell 187, 692–711 (2024). (PMID: 38262408)
Saito, T. In vivo electroporation in the embryonic mouse central nervous system. Nat Protoc. 1, 1552–1558 (2006). (PMID: 17406448)
Borrell, V., Yoshimura, Y. & Callaway, E. M. Targeted gene delivery to telencephalic inhibitory neurons by directional in utero electroporation. J. Neurosci. Methods 143, 151–158 (2005). (PMID: 15814147)
Ding, S. et al. Efficient transposition of the piggyBac (PB) transposon in mammalian cells and mice. Cell 122, 473–483 (2005). (PMID: 16096065)
Zhao, L., Liu, Z., Levy, S. F. & Wu, S. Bartender: a fast and accurate clustering algorithm to count barcode reads. Bioinformatics 34, 739–747 (2018). (PMID: 29069318)
Replogle, J. M. et al. Combinatorial single-cell CRISPR screens by direct guide RNA capture and targeted sequencing. Nat. Biotechnol. 38, 954–961 (2020). (PMID: 322313367416462)
Zheng, G. X. Y. et al. Massively parallel digital transcriptional profiling of single cells. Nat. Commun. 8, 14049 (2017). (PMID: 280916015241818)
La Manno, G. et al. Molecular architecture of the developing mouse brain. Nature 596, 92–96 (2021). (PMID: 34321664)
Saunders, A. et al. Molecular diversity and specializations among the cells of the adult mouse brain. Cell 174, 1015–1030 (2018).
Yang, S. et al. Decontamination of ambient RNA in single-cell RNA-seq with DecontX. Genome Biol. 21, 57 (2020). (PMID: 321387707059395)
Friedman, J., Hastie, T. & Tibshirani, R. Regularization paths for generalized linear models via coordinate descent. J. Stat. Softw. 33, 1–22 (2010). (PMID: 208087282929880)
Squair, J. W. et al. Confronting false discoveries in single-cell differential expression. Nat. Commun. 12, 5692 (2021). (PMID: 345840918479118)
Weinreb, C., Rodriguez-Fraticelli, A., Camargo, F. D. & Klein, A. M. Lineage tracing on transcriptional landscapes links state to fate during differentiation. Science 367, eaaw3381 (2020). (PMID: 319741597608074)
Kuleshov, M. V. et al. Enrichr: a comprehensive gene set enrichment analysis web server 2016 update. Nucleic Acids Res. 44, W90–W97 (2016). (PMID: 271419614987924)
Mercader, N., Tanaka, E. M. & Torres, M. Proximodistal identity during vertebrate limb regeneration is regulated by meis homeodomain proteins. Development 132, 4131–4142 (2005). (PMID: 16107473)
Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with bowtie 2. Nat. Methods 9, 357–359 (2012). (PMID: 223882863322381)
Feng, J., Liu, T., Qin, B., Zhang, Y. & Liu, X. S. Identifying ChIP–seq enrichment using macs. Nat. Protoc. 7, 1728–1740 (2012). (PMID: 22936215)
Meylan, P., Dreos, R., Ambrosini, G., Groux, R. & Bucher, P. EPD in 2020: enhanced data visualization and extension to ncRNA promoters. Nucleic Acids Res. 48, D65–D69 (2020). (PMID: 31680159)
Robinson, J. T. et al. Integrative genomics viewer. Nat. Biotechnol. 29, 24–26 (2011). (PMID: 212210953346182)
Heinz, S. et al. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol. Cell 38, 576–589 (2010). (PMID: 205134322898526)
Whitington, T., Frith, M. C., Johnson, J. & Bailey, T. L. Inferring transcription factor complexes from ChIP–seq data. Nucleic Acids Res. 39, e98 (2011). (PMID: 216022623159476)
معلومات مُعتمدة: ERC-2018-STG EC | EU Framework Programme for Research and Innovation H2020 | H2020 Priority Excellent Science | H2020 European Research Council (H2020 Excellent Science - European Research Council); 803984 EC | EU Framework Programme for Research and Innovation H2020 | H2020 Priority Excellent Science | H2020 European Research Council (H2020 Excellent Science - European Research Council); 01EW1605 EC | EU Framework Programme for Research and Innovation H2020 | H2020 Priority Excellent Science | H2020 European Research Council (H2020 Excellent Science - European Research Council)
المشرفين على المادة: 0 (Homeodomain Proteins)
0 (Transcription Factors)
0 (LIM-Homeodomain Proteins)
0 (LHX6 protein, mouse)
0 (Nerve Tissue Proteins)
تواريخ الأحداث: Date Created: 20240326 Date Completed: 20240512 Latest Revision: 20240520
رمز التحديث: 20240521
مُعرف محوري في PubMed: PMC11088997
DOI: 10.1038/s41593-024-01611-9
PMID: 38528203
قاعدة البيانات: MEDLINE
الوصف
تدمد:1546-1726
DOI:10.1038/s41593-024-01611-9