Dynamic expression of NR2F1 and SOX2 in developing and adult human cortex: comparison with cortical malformations.


Journal

Brain structure & function
ISSN: 1863-2661
Titre abrégé: Brain Struct Funct
Pays: Germany
ID NLM: 101282001

Informations de publication

Date de publication:
May 2021
Historique:
received: 03 09 2020
accepted: 22 02 2021
pubmed: 5 3 2021
medline: 1 12 2021
entrez: 4 3 2021
Statut: ppublish

Résumé

The neocortex, the most recently evolved brain region in mammals, is characterized by its unique areal and laminar organization. Distinct cortical layers and areas can be identified by the presence of graded expression of transcription factors and molecular determinants defining neuronal identity. However, little is known about the expression of key master genes orchestrating human cortical development. In this study, we explored the expression dynamics of NR2F1 and SOX2, key cortical genes whose mutations in human patients cause severe neurodevelopmental syndromes. We focused on physiological conditions, spanning from mid-late gestational ages to adulthood in unaffected specimens, but also investigated gene expression in a pathological context, a developmental cortical malformation termed focal cortical dysplasia (FCD). We found that NR2F1 follows an antero-dorsal

Identifiants

pubmed: 33661352
doi: 10.1007/s00429-021-02242-7
pii: 10.1007/s00429-021-02242-7
doi:

Substances chimiques

COUP Transcription Factor I 0
NR2F1 protein, human 0
SOX2 protein, human 0
SOXB1 Transcription Factors 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

1303-1322

Subventions

Organisme : European Research Area Networks (ERA-NET) Neuron II
ID : RE7-n.363/2016
Organisme : European Research Area Networks (ERA-NET) Neuron II
ID : ANR-15-NEUR-0002-04

Références

Al-Kateb H, Shimony JS, Vineyard M, Manwaring L, Kulkarni S, Shinawi M (2013) NR2F1 haploinsufficiency is associated with optic atrophy, dysmorphism and global developmental delay. Am J Med Genet A 161A(2):377–381. https://doi.org/10.1002/ajmg.a.35650
doi: 10.1002/ajmg.a.35650 pubmed: 23300014
Alfano C, Magrinelli E, Harb K, Hevner RF, Studer M (2014a) Postmitotic control of sensory area specification during neocortical development. Nat Commun 5:5632. https://doi.org/10.1038/ncomms6632
doi: 10.1038/ncomms6632 pubmed: 25476200
Alfano C, Magrinelli E, Harb K, Studer M (2014b) The nuclear receptors COUP-TF: a long-lasting experience in forebrain assembly. Cell Mol Life Sci CMLS 71(1):43–62. https://doi.org/10.1007/s00018-013-1320-6
doi: 10.1007/s00018-013-1320-6 pubmed: 23525662
Alfano C, Studer M (2013) Neocortical arealization: evolution, mechanisms, and open questions. Dev Neurobiol 73(6):411–447. https://doi.org/10.1002/dneu.22067
doi: 10.1002/dneu.22067 pubmed: 23239642
Alfano C, Viola L, Heng JI, Pirozzi M, Clarkson M, Flore G, De Maio A, Schedl A, Guillemot F, Studer M (2011) COUP-TFI promotes radial migration and proper morphology of callosal projection neurons by repressing Rnd2 expression. Development 138(21):4685–4697. https://doi.org/10.1242/dev.068031
doi: 10.1242/dev.068031 pubmed: 21965613
Alzu’bi A, Lindsay SJ, Harkin LF, McIntyre J, Lisgo SN, Clowry GJ (2017) The transcription factors COUP-TFI and COUP-TFII have distinct roles in arealisation and GABAergic interneuron specification in the early human fetal telencephalon. Cereb Cortex 27(10):4971–4987. https://doi.org/10.1093/cercor/bhx185
doi: 10.1093/cercor/bhx185 pubmed: 28922831 pmcid: 5903418
Armentano M, Chou SJ, Tomassy GS, Leingartner A, O’Leary DD, Studer M (2007) COUP-TFI regulates the balance of cortical patterning between frontal/motor and sensory areas. Nat Neurosci 10(10):1277–1286. https://doi.org/10.1038/nn1958
doi: 10.1038/nn1958 pubmed: 17828260
Armentano M, Filosa A, Andolfi G, Studer M (2006) COUP-TFI is required for the formation of commissural projections in the forebrain by regulating axonal growth. Development 133(21):4151–4162. https://doi.org/10.1242/dev.02600
doi: 10.1242/dev.02600 pubmed: 17021036
Arshad A, Vose LR, Vinukonda G, Hu F, Yoshikawa K, Csiszar A, Brumberg JC, Ballabh P (2016) Extended production of cortical interneurons into the third trimester of human gestation. Cereb Cortex 26(5):2242–2256. https://doi.org/10.1093/cercor/bhv074
doi: 10.1093/cercor/bhv074 pubmed: 25882040
Baer K, Eriksson PS, Faull RL, Rees MI, Curtis MA (2007) Sox-2 is expressed by glial and progenitor cells and Pax-6 is expressed by neuroblasts in the human subventricular zone. Exp Neurol 204(2):828–831. https://doi.org/10.1016/j.expneurol.2006.12.008
doi: 10.1016/j.expneurol.2006.12.008 pubmed: 17291498
Bani-Yaghoub M, Tremblay RG, Lei JX, Zhang D, Zurakowski B, Sandhu JK, Smith B, Ribecco-Lutkiewicz M, Kennedy J, Walker PR, Sikorska M (2006) Role of Sox2 in the development of the mouse neocortex. Dev Biol 295(1):52–66. https://doi.org/10.1016/j.ydbio.2006.03.007
doi: 10.1016/j.ydbio.2006.03.007 pubmed: 16631155
Beccari L, Marco-Ferreres R, Bovolenta P (2013) The logic of gene regulatory networks in early vertebrate forebrain patterning. Mech Dev 130(2–3):95–111. https://doi.org/10.1016/j.mod.2012.10.004
doi: 10.1016/j.mod.2012.10.004 pubmed: 23111324
Bertacchi M, Gruart A, Kaimakis P, Allet C, Serra L, Giacobini P, Delgado-Garcia JM, Bovolenta P, Studer M (2019a) Mouse Nr2f1 haploinsufficiency unveils new pathological mechanisms of a human optic atrophy syndrome. EMBO Mol Med 11(8):e10291. https://doi.org/10.15252/emmm.201910291
doi: 10.15252/emmm.201910291 pubmed: 31318166 pmcid: 6685104
Bertacchi M, Parisot J, Studer M (2019b) The pleiotropic transcriptional regulator COUP-TFI plays multiple roles in neural development and disease. Brain Res 1705:75–94. https://doi.org/10.1016/j.brainres.2018.04.024
doi: 10.1016/j.brainres.2018.04.024 pubmed: 29709504
Bertacchi M, Romano AL, Loubat A, Tran Mau-Them F, Willems M, Faivre L, Khau van Kien P, Perrin L, Devillard F, Sorlin A, Kuentz P, Philippe C, Garde A, Neri F, Di Giaimo R, Oliviero S, Cappello S, D’Incerti L, Frassoni C, Studer M (2020) NR2F1 regulates regional progenitor dynamics in the mouse neocortex and cortical gyrification in BBSOAS patients. EMBO J 39(13):e104163. https://doi.org/10.15252/embj.2019104163
doi: 10.15252/embj.2019104163 pubmed: 32484994 pmcid: 7327499
Bertolini JA, Favaro R, Zhu Y, Pagin M, Ngan CY, Wong CH, Tjong H, Vermunt MW, Martynoga B, Barone C, Mariani J, Cardozo MJ, Tabanera N, Zambelli F, Mercurio S, Ottolenghi S, Robson P, Creyghton MP, Bovolenta P, Pavesi G, Guillemot F, Nicolis SK, Wei CL (2019) Mapping the global chromatin connectivity network for Sox2 function in neural stem cell maintenance. Cell Stem Cell 24(3):462-476e466. https://doi.org/10.1016/j.stem.2019.02.004
doi: 10.1016/j.stem.2019.02.004 pubmed: 30849367 pmcid: 6506828
Blumcke I, Spreafico R, Haaker G, Coras R, Kobow K, Bien CG, Pfafflin M, Elger C, Widman G, Schramm J, Becker A, Braun KP, Leijten F, Baayen JC, Aronica E, Chassoux F, Hamer H, Stefan H, Rossler K, Thom M, Walker MC, Sisodiya SM, Duncan JS, McEvoy AW, Pieper T, Holthausen H, Kudernatsch M, Meencke HJ, Kahane P, Schulze-Bonhage A, Zentner J, Heiland DH, Urbach H, Steinhoff BJ, Bast T, Tassi L, Lo Russo G, Ozkara C, Oz B, Krsek P, Vogelgesang S, Runge U, Lerche H, Weber Y, Honavar M, Pimentel J, Arzimanoglou A, Ulate-Campos A, Noachtar S, Hartl E, Schijns O, Guerrini R, Barba C, Jacques TS, Cross JH, Feucht M, Muhlebner A, Grunwald T, Trinka E, Winkler PA, Gil-Nagel A, Toledano Delgado R, Mayer T, Lutz M, Zountsas B, Garganis K, Rosenow F, Hermsen A, von Oertzen TJ, Diepgen TL, Avanzini G, Consortium E (2017) Histopathological findings in brain tissue obtained during epilepsy surgery. N Engl J Med 377(17):1648–1656. https://doi.org/10.1056/NEJMoa1703784
doi: 10.1056/NEJMoa1703784 pubmed: 29069555
Blumcke I, Thom M, Aronica E, Armstrong DD, Vinters HV, Palmini A, Jacques TS, Avanzini G, Barkovich AJ, Battaglia G, Becker A, Cepeda C, Cendes F, Colombo N, Crino P, Cross JH, Delalande O, Dubeau F, Duncan J, Guerrini R, Kahane P, Mathern G, Najm I, Ozkara C, Raybaud C, Represa A, Roper SN, Salamon N, Schulze-Bonhage A, Tassi L, Vezzani A, Spreafico R (2011) The clinicopathologic spectrum of focal cortical dysplasias: a consensus classification proposed by an ad hoc Task Force of the ILAE Diagnostic Methods Commission. Epilepsia 52(1):158–174. https://doi.org/10.1111/j.1528-1167.2010.02777.x
doi: 10.1111/j.1528-1167.2010.02777.x pubmed: 21219302
Bonzano S, Crisci I, Podlesny-Drabiniok A, Rolando C, Krezel W, Studer M, De Marchis S (2018) Neuron-astroglia cell fate decision in the adult mouse hippocampal neurogenic niche is cell-intrinsically controlled by COUP-TFI in vivo. Cell Rep 24(2):329–341. https://doi.org/10.1016/j.celrep.2018.06.044
doi: 10.1016/j.celrep.2018.06.044 pubmed: 29996095
Bosch DG, Boonstra FN, Gonzaga-Jauregui C, Xu M, de Ligt J, Jhangiani S, Wiszniewski W, Muzny DM, Yntema HG, Pfundt R, Vissers LE, Spruijt L, Blokland EA, Chen CA, Baylor-Hopkins Center for Mendelian G, Lewis RA, Tsai SY, Gibbs RA, Tsai MJ, Lupski JR, Zoghbi HY, Cremers FP, de Vries BB, Schaaf CP (2014) NR2F1 mutations cause optic atrophy with intellectual disability. Am J Hum Genet 94(2):303–309. https://doi.org/10.1016/j.ajhg.2014.01.002
doi: 10.1016/j.ajhg.2014.01.002 pubmed: 24462372 pmcid: 3928641
Cavallaro M, Mariani J, Lancini C, Latorre E, Caccia R, Gullo F, Valotta M, DeBiasi S, Spinardi L, Ronchi A, Wanke E, Brunelli S, Favaro R, Ottolenghi S, Nicolis SK (2008) Impaired generation of mature neurons by neural stem cells from hypomorphic Sox2 mutants. Development 135(3):541–557. https://doi.org/10.1242/dev.010801
doi: 10.1242/dev.010801 pubmed: 18171687
Cerrato V, Mercurio S, Leto K, Fuca E, Hoxha E, Bottes S, Pagin M, Milanese M, Ngan CY, Concina G, Ottolenghi S, Wei CL, Bonanno G, Pavesi G, Tempia F, Buffo A, Nicolis SK (2018) Sox2 conditional mutation in mouse causes ataxic symptoms, cerebellar vermis hypoplasia, and postnatal defects of Bergmann glia. Glia 66(9):1929–1946. https://doi.org/10.1002/glia.23448
doi: 10.1002/glia.23448 pubmed: 29732603
Chen CA, Bosch DG, Cho MT, Rosenfeld JA, Shinawi M, Lewis RA, Mann J, Jayakar P, Payne K, Walsh L, Moss T, Schreiber A, Schoonveld C, Monaghan KG, Elmslie F, Douglas G, Boonstra FN, Millan F, Cremers FP, McKnight D, Richard G, Juusola J, Kendall F, Ramsey K, Anyane-Yeboa K, Malkin E, Chung WK, Niyazov D, Pascual JM, Walkiewicz M, Veluchamy V, Li C, Hisama FM, de Vries BB, Schaaf C (2016) The expanding clinical phenotype of Bosch-Boonstra-Schaaf optic atrophy syndrome: 20 new cases and possible genotype-phenotype correlations. Genet Med 18(11):1143–1150. https://doi.org/10.1038/gim.2016.18
doi: 10.1038/gim.2016.18 pubmed: 26986877
Clowry GJ, Alzu’bi A, Harkin LF, Sarma S, Kerwin J, Lindsay SJ (2018) Charting the protomap of the human telencephalon. Semin Cell Dev Biol 76:3–14. https://doi.org/10.1016/j.semcdb.2017.08.033
doi: 10.1016/j.semcdb.2017.08.033 pubmed: 28834762
D’Gama AM, Woodworth MB, Hossain AA, Bizzotto S, Hatem NE, LaCoursiere CM, Najm I, Ying Z, Yang E, Barkovich AJ, Kwiatkowski DJ, Vinters HV, Madsen JR, Mathern GW, Blumcke I, Poduri A, Walsh CA (2017) Somatic mutations activating the mTOR pathway in dorsal telencephalic progenitors cause a continuum of cortical dysplasias. Cell Rep 21(13):3754–3766. https://doi.org/10.1016/j.celrep.2017.11.106
doi: 10.1016/j.celrep.2017.11.106 pubmed: 29281825 pmcid: 5752134
Del Pino I, Tocco C, Magrinelli E, Marcantoni A, Ferraguto C, Tomagra G, Bertacchi M, Alfano C, Leinekugel X, Frick A, Studer M (2020) COUP-TFI/Nr2f1 orchestrates intrinsic neuronal activity during development of the somatosensory cortex. Cereb Cortex. https://doi.org/10.1093/cercor/bhaa137
doi: 10.1093/cercor/bhaa137 pubmed: 32572460
Dennert N, Engels H, Cremer K, Becker J, Wohlleber E, Albrecht B, Ehret JK, Ludecke HJ, Suri M, Carignani G, Renieri A, Kukuk GM, Wieland T, Andrieux J, Strom TM, Wieczorek D, Dieux-Coeslier A, Zink AM (2017) De novo microdeletions and point mutations affecting SOX2 in three individuals with intellectual disability but without major eye malformations. Am J Med Genet A 173(2):435–443. https://doi.org/10.1002/ajmg.a.38034
doi: 10.1002/ajmg.a.38034 pubmed: 27862890
Dye CA, El Shawa H, Huffman KJ (2011) A lifespan analysis of intraneocortical connections and gene expression in the mouse II. Cereb Cortex 21(6):1331–1350. https://doi.org/10.1093/cercor/bhq213
doi: 10.1093/cercor/bhq213 pubmed: 21060113
Faedo A, Tomassy GS, Ruan Y, Teichmann H, Krauss S, Pleasure SJ, Tsai SY, Tsai MJ, Studer M, Rubenstein JL (2008) COUP-TFI coordinates cortical patterning, neurogenesis, and laminar fate and modulates MAPK/ERK, AKT, and beta-catenin signaling. Cereb Cortex 18(9):2117–2131. https://doi.org/10.1093/cercor/bhm238
doi: 10.1093/cercor/bhm238 pubmed: 18165280
Fantes JA, Boland E, Ramsay J, Donnai D, Splitt M, Goodship JA, Stewart H, Whiteford M, Gautier P, Harewood L, Holloway S, Sharkey F, Maher E, van Heyningen V, Clayton-Smith J, Fitzpatrick DR, Black GC (2008) FISH mapping of de novo apparently balanced chromosome rearrangements identifies characteristics associated with phenotypic abnormality. Am J Hum Genet 82(4):916–926. https://doi.org/10.1016/j.ajhg.2008.02.007
doi: 10.1016/j.ajhg.2008.02.007 pubmed: 18374296 pmcid: 2491339
Favaro R, Valotta M, Ferri AL, Latorre E, Mariani J, Giachino C, Lancini C, Tosetti V, Ottolenghi S, Taylor V, Nicolis SK (2009) Hippocampal development and neural stem cell maintenance require Sox2-dependent regulation of Shh. Nat Neurosci 12(10):1248–1256. https://doi.org/10.1038/nn.2397
doi: 10.1038/nn.2397 pubmed: 19734891
Feng R, Wen J (2015) Overview of the roles of Sox2 in stem cell and development. Biol Chem 396(8):883–891. https://doi.org/10.1515/hsz-2014-0317
doi: 10.1515/hsz-2014-0317 pubmed: 25781683
Fernandez V, Llinares-Benadero C, Borrell V (2016) Cerebral cortex expansion and folding: what have we learned? EMBO J 35(10):1021–1044. https://doi.org/10.15252/embj.201593701
doi: 10.15252/embj.201593701 pubmed: 27056680 pmcid: 4868950
Ferri A, Favaro R, Beccari L, Bertolini J, Mercurio S, Nieto-Lopez F, Verzeroli C, La Regina F, De Pietri TD, Ottolenghi S, Bovolenta P, Nicolis SK (2013) Sox2 is required for embryonic development of the ventral telencephalon through the activation of the ventral determinants Nkx2.1 and Shh. Development 140(6):1250–1261. https://doi.org/10.1242/dev.073411
doi: 10.1242/dev.073411 pubmed: 23444355
Ferri AL, Cavallaro M, Braida D, Di Cristofano A, Canta A, Vezzani A, Ottolenghi S, Pandolfi PP, Sala M, DeBiasi S, Nicolis SK (2004) Sox2 deficiency causes neurodegeneration and impaired neurogenesis in the adult mouse brain. Development 131(15):3805–3819. https://doi.org/10.1242/dev.01204
doi: 10.1242/dev.01204 pubmed: 15240551
Flore G, Di Ruberto G, Parisot J, Sannino S, Russo F, Illingworth EA, Studer M, De Leonibus E (2017) Gradient COUP-TFI expression Is required for functional organization of the hippocampal septo-temporal longitudinal axis. Cereb Cortex 27(2):1629–1643. https://doi.org/10.1093/cercor/bhv336
doi: 10.1093/cercor/bhv336 pubmed: 26813976
Graham V, Khudyakov J, Ellis P, Pevny L (2003) SOX2 functions to maintain neuronal progenitor identity. Neuron 39(5):749–765. https://doi.org/10.1016/s0896-6273(03)00497-5
doi: 10.1016/s0896-6273(03)00497-5 pubmed: 12948443
Hansen DV, Lui JH, Parker PR, Kriegstein AR (2010) Neurogenic radial glia in the outer subventricular zone of human neocortex. Nature 464(7288):554–561. https://doi.org/10.1038/nature08845
doi: 10.1038/nature08845 pubmed: 20154730
Holguera I, Desplan C (2018) Neuronal specification in space and time. Science 362(6411):176–180. https://doi.org/10.1126/science.aas9435
doi: 10.1126/science.aas9435 pubmed: 30309944 pmcid: 6368964
Hutton SR, Pevny LH (2011) SOX2 expression levels distinguish between neural progenitor populations of the developing dorsal telencephalon. Dev Biol 352(1):40–47. https://doi.org/10.1016/j.ydbio.2011.01.015
doi: 10.1016/j.ydbio.2011.01.015 pubmed: 21256837
Kaiwar C, Zimmermann MT, Ferber MJ, Niu Z, Urrutia RA, Klee EW, Babovic-Vuksanovic D (2017) Novel NR2F1 variants likely disrupt DNA binding: molecular modeling in two cases, review of published cases, genotype-phenotype correlation, and phenotypic expansion of the Bosch-Boonstra-Schaaf optic atrophy syndrome. Cold Spring Harb Mol Case Stud 3(6). https://doi.org/10.1101/mcs.a002162
Kondoh H, L-BReb (2016) Sox2, biology and role in development and disease. ISBN: 978-0-12-800352-7. Elsevier, Associated Press
Lamparello P, Baybis M, Pollard J, Hol EM, Eisenstat DD, Aronica E, Crino PB (2007) Developmental lineage of cell types in cortical dysplasia with balloon cells. Brain 130(Pt 9):2267–2276. https://doi.org/10.1093/brain/awm175
doi: 10.1093/brain/awm175 pubmed: 17711980
Liu Q, Dwyer ND, O’Leary DD (2000) Differential expression of COUP-TFI, CHL1, and two novel genes in developing neocortex identified by differential display PCR. J Neurosci 20(20):7682–7690
doi: 10.1523/JNEUROSCI.20-20-07682.2000
Lodato S, Rouaux C, Quast KB, Jantrachotechatchawan C, Studer M, Hensch TK, Arlotta P (2011) Excitatory projection neuron subtypes control the distribution of local inhibitory interneurons in the cerebral cortex. Neuron 69(4):763–779. https://doi.org/10.1016/j.neuron.2011.01.015
doi: 10.1016/j.neuron.2011.01.015 pubmed: 21338885 pmcid: 3061282
Lui JH, Hansen DV, Kriegstein AR (2011) Development and evolution of the human neocortex. Cell 146(1):18–36. https://doi.org/10.1016/j.cell.2011.06.030
doi: 10.1016/j.cell.2011.06.030 pubmed: 21729779 pmcid: 3610574
Ma T, Wang C, Wang L, Zhou X, Tian M, Zhang Q, Zhang Y, Li J, Liu Z, Cai Y, Liu F, You Y, Chen C, Campbell K, Song H, Ma L, Rubenstein JL, Yang Z (2013) Subcortical origins of human and monkey neocortical interneurons. Nat Neurosci 16(11):1588–1597. https://doi.org/10.1038/nn.3536
doi: 10.1038/nn.3536 pubmed: 24097041
Malik R, Johnston D (2017) Dendritic GIRK channels gate the integration window, plateau potentials, and induction of synaptic plasticity in dorsal but not ventral CA1 neurons. J Neurosci 37(14):3940–3955. https://doi.org/10.1523/JNEUROSCI.2784-16.2017
doi: 10.1523/JNEUROSCI.2784-16.2017 pubmed: 28280255 pmcid: 5394901
Malik S, Vinukonda G, Vose LR, Diamond D, Bhimavarapu BB, Hu F, Zia MT, Hevner R, Zecevic N, Ballabh P (2013) Neurogenesis continues in the third trimester of pregnancy and is suppressed by premature birth. J Neurosci 33(2):411–423. https://doi.org/10.1523/JNEUROSCI.4445-12.2013
doi: 10.1523/JNEUROSCI.4445-12.2013 pubmed: 23303921 pmcid: 3711635
Marsan E, Baulac S (2018) Review: mechanistic target of rapamycin (mTOR) pathway, focal cortical dysplasia and epilepsy. Neuropathol Appl Neurobiol 44(1):6–17. https://doi.org/10.1111/nan.12463
doi: 10.1111/nan.12463 pubmed: 29359340
Martin-Hernandez E, Rodriguez-Garcia ME, Chen CA, Cotrina-Vinagre FJ, Carnicero-Rodriguez P, Bellusci M, Schaaf CP, Martinez-Azorin F (2018) Mitochondrial involvement in a Bosch-Boonstra-Schaaf optic atrophy syndrome patient with a novel de novo NR2F1 gene mutation. J Hum Genet 63(4):525–528. https://doi.org/10.1038/s10038-017-0398-3
doi: 10.1038/s10038-017-0398-3 pubmed: 29410510
Mercurio S, Serra L, Motta A, Gesuita L, Sanchez-Arrones L, Inverardi F, Foglio B, Barone C, Kaimakis P, Martynoga B, Ottolenghi S, Studer M, Guillemot F, Frassoni C, Bovolenta P, Nicolis SK (2019a) Sox2 acts in thalamic neurons to control the development of retina-thalamus-cortex connectivity. iScience 15:257–273. https://doi.org/10.1016/j.isci.2019.04.030
doi: 10.1016/j.isci.2019.04.030 pubmed: 31082736 pmcid: 6517317
Mercurio S, Serra L, Nicolis SK (2019b) More than just stem cells: functional roles of the transcription factor Sox2 in differentiated glia and neurons. Int J Mol Sci 20(18):4540. https://doi.org/10.3390/ijms20184540
doi: 10.3390/ijms20184540 pmcid: 6769708
Molyneaux BJ, Arlotta P, Menezes JR, Macklis JD (2007) Neuronal subtype specification in the cerebral cortex. Nat Rev Neurosci 8(6):427–437. https://doi.org/10.1038/nrn2151
doi: 10.1038/nrn2151 pubmed: 17514196
Naka H, Nakamura S, Shimazaki T, Okano H (2008) Requirement for COUP-TFI and II in the temporal specification of neural stem cells in CNS development. Nat Neurosci 11(9):1014–1023. https://doi.org/10.1038/nn.2168
doi: 10.1038/nn.2168 pubmed: 19160499
Nowakowski TJ, Bhaduri A, Pollen AA, Alvarado B, Mostajo-Radji MA, Di Lullo E, Haeussler M, Sandoval-Espinosa C, Liu SJ, Velmeshev D, Ounadjela JR, Shuga J, Wang X, Lim DA, West JA, Leyrat AA, Kent WJ, Kriegstein AR (2017) Spatiotemporal gene expression trajectories reveal developmental hierarchies of the human cortex. Science 358(6368):1318–1323. https://doi.org/10.1126/science.aap8809
doi: 10.1126/science.aap8809 pubmed: 29217575 pmcid: 5991609
Nowakowski TJ, Pollen AA, Sandoval-Espinosa C, Kriegstein AR (2016) Transformation of the radial glia scaffold demarcates two stages of human cerebral cortex development. Neuron 91(6):1219–1227. https://doi.org/10.1016/j.neuron.2016.09.005
doi: 10.1016/j.neuron.2016.09.005 pubmed: 27657449 pmcid: 5087333
Oliver-De La Cruz J, Carrion-Navarro J, Garcia-Romero N, Gutierrez-Martin A, Lazaro-Ibanez E, Escobedo-Lucea C, Perona R, Belda-Iniesta C, Ayuso-Sacido A (2014) SOX2+ cell population from normal human brain white matter is able to generate mature oligodendrocytes. PLoS ONE 9(6):e99253. https://doi.org/10.1371/journal.pone.0099253
doi: 10.1371/journal.pone.0099253 pubmed: 24901457 pmcid: 4047120
Orlova KA, Tsai V, Baybis M, Heuer GG, Sisodiya S, Thom M, Strauss K, Aronica E, Storm PB, Crino PB (2010) Early progenitor cell marker expression distinguishes type II from type I focal cortical dysplasias. J Neuropathol Exp Neurol 69(8):850–863. https://doi.org/10.1097/NEN.0b013e3181eac1f5
doi: 10.1097/NEN.0b013e3181eac1f5 pubmed: 20613634 pmcid: 3474261
Pevny LH, Nicolis SK (2010) Sox2 roles in neural stem cells. Int J Biochem Cell Biol 42(3):421–424. https://doi.org/10.1016/j.biocel.2009.08.018
doi: 10.1016/j.biocel.2009.08.018 pubmed: 19733254
Pollen AA, Nowakowski TJ, Chen J, Retallack H, Sandoval-Espinosa C, Nicholas CR, Shuga J, Liu SJ, Oldham MC, Diaz A, Lim DA, Leyrat AA, West JA, Kriegstein AR (2015) Molecular identity of human outer radial glia during cortical development. Cell 163(1):55–67. https://doi.org/10.1016/j.cell.2015.09.004
doi: 10.1016/j.cell.2015.09.004 pubmed: 26406371 pmcid: 4583716
Rech ME, McCarthy JM, Chen CA, Edmond JC, Shah VS, Bosch DGM, Berry GT, Williams L, Madan-Khetarpal S, Niyazov D, Shaw-Smith C, Kovar EM, Lupo PJ, Schaaf CP (2020) Phenotypic expansion of Bosch-Boonstra-Schaaf optic atrophy syndrome and further evidence for genotype–phenotype correlations. Am J Med Genet A 182(6):1426–1437. https://doi.org/10.1002/ajmg.a.61580
doi: 10.1002/ajmg.a.61580 pubmed: 32275123
Sisodiya SM, Fauser S, Cross JH, Thom M (2009) Focal cortical dysplasia type II: biological features and clinical perspectives. Lancet Neurol 8(9):830–843. https://doi.org/10.1016/S1474-4422(09)70201-7
doi: 10.1016/S1474-4422(09)70201-7 pubmed: 19679275
Sisodiya SM, Ragge NK, Cavalleri GL, Hever A, Lorenz B, Schneider A, Williamson KA, Stevens JM, Free SL, Thompson PJ, van Heyningen V, Fitzpatrick DR (2006) Role of SOX2 mutations in human hippocampal malformations and epilepsy. Epilepsia 47(3):534–542. https://doi.org/10.1111/j.1528-1167.2006.00464.x
doi: 10.1111/j.1528-1167.2006.00464.x pubmed: 16529618
Tomassy GS, De Leonibus E, Jabaudon D, Lodato S, Alfano C, Mele A, Macklis JD, Studer M (2010) Area-specific temporal control of corticospinal motor neuron differentiation by COUP-TFI. Proc Natl Acad Sci USA 107(8):3576–3581. https://doi.org/10.1073/pnas.0911792107
doi: 10.1073/pnas.0911792107 pubmed: 20133588
Tripodi M, Filosa A, Armentano M, Studer M (2004) The COUP-TF nuclear receptors regulate cell migration in the mammalian basal forebrain. Development 131(24):6119–6129. https://doi.org/10.1242/dev.01530
doi: 10.1242/dev.01530 pubmed: 15548577
Yang X, Feng S, Tang K (2017) COUP-TF genes, human diseases, and the development of the central nervous system in murine models. Curr Top Dev Biol 125:275–301. https://doi.org/10.1016/bs.ctdb.2016.12.002
doi: 10.1016/bs.ctdb.2016.12.002 pubmed: 28527575
Zecevic N, Hu F, Jakovcevski I (2011) Interneurons in the developing human neocortex. Dev Neurobiol 71(1):18–33. https://doi.org/10.1002/dneu.20812
doi: 10.1002/dneu.20812 pubmed: 21154907 pmcid: 3117059
Zhang S, Rasai A, Wang Y, Xu J, Bannerman P, Erol D, Tsegaye D, Wang A, Soulika A, Zhan X, Guo F (2018a) The stem cell factor Sox2 is a positive timer of oligodendrocyte development in the postnatal murine spinal cord. Mol Neurobiol 55(12):9001–9015. https://doi.org/10.1007/s12035-018-1035-7
doi: 10.1007/s12035-018-1035-7 pubmed: 29623612 pmcid: 6173662
Zhang S, Zhu X, Gui X, Croteau C, Song L, Xu J, Wang A, Bannerman P, Guo F (2018b) Sox2 is essential for oligodendroglial proliferation and differentiation during postnatal brain myelination and CNS remyelination. J Neurosci 38(7):1802–1820. https://doi.org/10.1523/JNEUROSCI.1291-17.2018
doi: 10.1523/JNEUROSCI.1291-17.2018 pubmed: 29335358 pmcid: 5815459
Zhao C, Ma D, Zawadzka M, Fancy SP, Elis-Williams L, Bouvier G, Stockley JH, de Castro GM, Wang B, Jacobs S, Casaccia P, Franklin RJ (2015) Sox2 sustains recruitment of oligodendrocyte progenitor cells following CNS demyelination and primes them for differentiation during remyelination. J Neurosci 35(33):11482–11499. https://doi.org/10.1523/JNEUROSCI.3655-14.2015
doi: 10.1523/JNEUROSCI.3655-14.2015 pubmed: 26290228 pmcid: 6605237
Zhou C, Qiu Y, Pereira FA, Crair MC, Tsai SY, Tsai MJ (1999) The nuclear orphan receptor COUP-TFI is required for differentiation of subplate neurons and guidance of thalamocortical axons. Neuron 24(4):847–859. https://doi.org/10.1016/s0896-6273(00)81032-6
doi: 10.1016/s0896-6273(00)81032-6 pubmed: 10624948
Zhou C, Tsai SY, Tsai MJ (2001) COUP-TFI: an intrinsic factor for early regionalization of the neocortex. Genes Dev 15(16):2054–2059. https://doi.org/10.1101/gad.913601
doi: 10.1101/gad.913601 pubmed: 11511537 pmcid: 312763

Auteurs

Benedetta Foglio (B)

Clinical and Experimental Epileptology Unit, C/O AmadeoLab, Fondazione IRCCS Istituto Neurologico Carlo Besta, Via Amadeo 42, 20133, Milan, Italy.

Laura Rossini (L)

Clinical and Experimental Epileptology Unit, C/O AmadeoLab, Fondazione IRCCS Istituto Neurologico Carlo Besta, Via Amadeo 42, 20133, Milan, Italy.

Rita Garbelli (R)

Clinical and Experimental Epileptology Unit, C/O AmadeoLab, Fondazione IRCCS Istituto Neurologico Carlo Besta, Via Amadeo 42, 20133, Milan, Italy.

Maria Cristina Regondi (MC)

Clinical and Experimental Epileptology Unit, C/O AmadeoLab, Fondazione IRCCS Istituto Neurologico Carlo Besta, Via Amadeo 42, 20133, Milan, Italy.

Sara Mercurio (S)

Department of Biotechnology and Bioscience, University of Milan-Bicocca, Milan, Italy.

Michele Bertacchi (M)

Clinical and Experimental Epileptology Unit, C/O AmadeoLab, Fondazione IRCCS Istituto Neurologico Carlo Besta, Via Amadeo 42, 20133, Milan, Italy.
Université Côte d'Azur, CNRS, Inserm, iBV, Nice, France.

Laura Avagliano (L)

Departement of Health Sciences, San Paolo Hospital Medical School University of Milan, Milan, Italy.

Gaetano Bulfamante (G)

Departement of Health Sciences, San Paolo Hospital Medical School University of Milan, Milan, Italy.

Roland Coras (R)

Department of Neuropathology, University Hospital Erlangen, Erlangen, Germany.

Antonino Maiorana (A)

Department of Medical and Surgical Sciences, Institute of Pathology, University of Modena and Reggio Emilia, Modena, Italy.

Silvia Nicolis (S)

Department of Biotechnology and Bioscience, University of Milan-Bicocca, Milan, Italy.

Michèle Studer (M)

Université Côte d'Azur, CNRS, Inserm, iBV, Nice, France.

Carolina Frassoni (C)

Clinical and Experimental Epileptology Unit, C/O AmadeoLab, Fondazione IRCCS Istituto Neurologico Carlo Besta, Via Amadeo 42, 20133, Milan, Italy. carolina.frassoni@istituto-besta.it.

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