Abstract
During development, generation of neurons is coordinated by the sequential activation of gene expression programs by stage- and subtype-specific transcription factor networks. The SoxC group transcription factors, Sox4 and Sox11, have recently emerged as critical components of this network. Initially identified as survival and differentiation factors for neural precursors, SoxC factors have now been linked to a broader array of developmental processes including neuronal subtype specification, migration, dendritogenesis and establishment of neuronal projections, and are now being employed in experimental strategies for neuronal replacement and axonal regeneration in the diseased central nervous system. This review summarizes the current knowledge regarding SoxC factor function in CNS development and disease and their promise for regeneration.
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Bayraktar OA, Fuentealba LC, Alvarez-Buylla A, Rowitch DH (2014) Astrocyte development and heterogeneity. Cold Spring Harb Perspect Biol 7:a020362
Bergsland M, Werme M, Malewicz M, Perlmann T, Muhr J (2006) The establishment of neuronal properties is controlled by Sox4 and Sox11. Genes Dev 20:3475–3486
Bergsland M, Ramskold D, Zaouter C, Klum S, Sandberg R, Muhr J (2011) Sequentially acting Sox transcription factors in neural lineage development. Genes Dev 25:2453–2464
Bhattaram P, Penzo-Mendez A, Sock E, Colmenares C, Kaneko KJ, Vassilev A, Depamphilis ML, Wegner M, Lefebvre V (2010) Organogenesis relies on SoxC transcription factors for the survival of neural and mesenchymal progenitors. Nat Commun 1:9
Bhattaram P, Penzo-Mendez A, Kato K, Bandyopadhyay K, Gadi A, Taketo MM, Lefebvre V (2014) SOXC proteins amplify canonical WNT signaling to secure nonchondrocytic fates in skeletogenesis. J Cell Biol 207:657–671
Bicker S, Lackinger M, Weiss K, Schratt G (2014) MicroRNA-132, −134, and −138: a microRNA troika rules in neuronal dendrites. Cell Mol Life Sci 71:3987–4005
Chang KC, Hertz J, Zhang X, Jin XL, Shaw P, Derosa BA, Li JY, Venugopalan P, Valenzuela DA, Patel RD, Russano KR, Alshamekh SA, Sun C, Tenerelli K, Li C, Velmeshev D, Cheng Y, Boyce TM, Dreyfuss A, Uddin MS, Muller KJ, Dykxhoorn DM, Goldberg JL (2017) Novel regulatory mechanisms for the SoxC transcriptional network required for visual pathway development. J Neurosci 37:4967–4981
Chen C, Lee GA, Pourmorady A, Sock E, Donoghue MJ (2015) Orchestration of neuronal differentiation and progenitor pool expansion in the developing cortex by SoxC genes. J Neurosci 35:10629–10642
Chetty C, Dontula R, Gujrati M, Dinh DH, Lakka SS (2012) Blockade of SOX4 mediated DNA repair by SPARC enhances radioresponse in medulloblastoma. Cancer Lett 323:188–198
Cheung M, Abu-Elmagd M, Clevers H, Scotting PJ (2000) Roles of Sox4 in central nervous system development. Brain research. Mol Brain Res 79:180–191
Coffin GS, Siris E (1970) Mental retardation with absent fifth fingernail and terminal phalanx. Am J Dis Child 119:433–439
Curto GG, Gard C, Ribes V (2015) Structures and properties of PAX linked regulatory networks architecting and pacing the emergence of neuronal diversity. Semin Cell Dev Biol 44:75–86
Dasen JS, Jessell TM (2009) Hox networks and the origins of motor neuron diversity. Curr Top Dev Biol 88:169–200
de Bont JM, Kros JM, Passier MM, Reddingius RE, Sillevis Smitt PA, Luider TM, den Boer ML, Pieters R (2008) Differential expression and prognostic significance of SOX genes in pediatric medulloblastoma and ependymoma identified by microarray analysis. Neuro-Oncology 10:648–660
Dy P, Penzo-Mendez A, Wang H, Pedraza CE, Macklin WB, Lefebvre V (2008) The three SoxC proteins--Sox4, Sox11 and Sox12--exhibit overlapping expression patterns and molecular properties. Nucleic Acids Res 36:3101–3117
Feng W, Khan MA, Bellvis P, Zhu Z, Bernhardt O, Herold-Mende C, Liu HK (2013) The chromatin remodeler CHD7 regulates adult neurogenesis via activation of SoxC transcription factors. Cell Stem Cell 13:62–72
Guillemot F (2007) Spatial and temporal specification of neural fates by transcription factor codes. Development 134:3771–3780
Guo Y, Liu S, Zhang X, Wang L, Zhang X, Hao A, Han A, Yang J (2014) Sox11 promotes endogenous neurogenesis and locomotor recovery in mice spinal cord injury. Biochem Biophys Res Commun 446:830–835
Haslinger A, Schwarz TJ, Covic M, Lie DC (2009) Expression of Sox11 in adult neurogenic niches suggests a stage-specific role in adult neurogenesis. Eur J Neurosci 29:2103–2114
Hempel A, Pagnamenta AT, Blyth M, Mansour S, McConnell V, Kou I, Ikegawa S, Tsurusaki Y, Matsumoto N, Lo-Castro A, Plessis G, Albrecht B, Battaglia A, Taylor JC, Howard MF, Keays D, Sohal AS, Kuhl SJ, Kini U, McNeill A (2016) Deletions and de novo mutations of SOX11 are associated with a neurodevelopmental disorder with features of coffin-Siris syndrome. J Med Genet 53:152–162
Hide T, Takezaki T, Nakatani Y, Nakamura H, Kuratsu J, Kondo T (2009) Sox11 prevents tumorigenesis of glioma-initiating cells by inducing neuronal differentiation. Cancer Res 69:7953–7959
Hoshiba Y, Toda T, Ebisu H, Wakimoto M, Yanagi S, Kawasaki H (2016) Sox11 balances Dendritic morphogenesis with neuronal migration in the developing cerebral cortex. J Neurosci 36:5775–5784
Hui SP, Sengupta D, Lee SG, Sen T, Kundu S, Mathavan S, Ghosh S (2014) Genome wide expression profiling during spinal cord regeneration identifies comprehensive cellular responses in zebrafish. PLoS ONE 9:e84212
Hyodo-Miura J, Urushiyama S, Nagai S, Nishita M, Ueno N, Shibuya H (2002) Involvement of NLK and Sox11 in neural induction in Xenopus development. Genes Cells 7:487–496
Ikushima H, Todo T, Ino Y, Takahashi M, Miyazawa K, Miyazono K (2009) Autocrine TGF-beta signaling maintains tumorigenicity of glioma-initiating cells through Sry-related HMG-box factors. Cell Stem Cell 5:504–514
Jang SM, Kim JW, Kim CH, An JH, Johnson A, Song PI, Rhee S, Choi KH (2015) KAT5-mediated SOX4 acetylation orchestrates chromatin remodeling during myoblast differentiation. Cell Death Dis 6:e1857
Jankowski MP, Cornuet PK, McIlwrath S, Koerber HR, Albers KM (2006) SRY-box containing gene 11 (Sox11) transcription factor is required for neuron survival and neurite growth. Neuroscience 143:501–514
Jankowski MP, McIlwrath SL, Jing X, Cornuet PK, Salerno KM, Koerber HR, Albers KM (2009) Sox11 transcription factor modulates peripheral nerve regeneration in adult mice. Brain Res 1256:43–54
Jayaprakash N, Wang Z, Hoeynck B, Krueger N, Kramer A, Balle E, Wheeler DS, Wheeler RA, Blackmore MG (2016) Optogenetic interrogation of functional synapse formation by Corticospinal tract axons in the injured spinal cord. J Neurosci 36:5877–5890
Jiang Y, Ding Q, Xie X, Libby RT, Lefebvre V, Gan L (2013) Transcription factors SOX4 and SOX11 function redundantly to regulate the development of mouse retinal ganglion cells. J Biol Chem 288:18429–18438
Jing X, Wang T, Huang S, Glorioso JC, Albers KM (2012) The transcription factor Sox11 promotes nerve regeneration through activation of the regeneration-associated gene Sprr1a. Exp Neurol 233:221–232
Johnson MB, Walsh CA (2017) Cerebral cortical neuron diversity and development at single-cell resolution. Curr Opin Neurobiol 42:9–16
Kanaan NM, Collier TJ, Cole-Strauss A, Grabinski T, Mattingly ZR, Winn ME, Steece-Collier K, Sortwell CE, Manfredsson FP, Lipton JW (2015) The longitudinal transcriptomic response of the substantia nigra to intrastriatal 6-hydroxydopamine reveals significant upregulation of regeneration-associated genes. PLoS ONE 10:e0127768
Kim DK, Han SB, Hong ST, Choi YJ, Sun W, Geum D, Kim H (2008) Expression of Sox11 and Brn transcription factors during development and following transient forebrain ischemia in the rat. Neurosci Lett 433:259–264
Koo JW, Mazei-Robison MS, Chaudhury D, Juarez B, LaPlant Q, Ferguson D, Feng J, Sun H, Scobie KN, Damez-Werno D, Crumiller M, Ohnishi YN, Ohnishi YH, Mouzon E, Dietz DM, Lobo MK, Neve RL, Russo SJ, Han MH, Nestler EJ (2012) BDNF is a negative modulator of morphine action. Science 338:124–128
Korkolopoulou P, Levidou G, El-Habr EA, Adamopoulos C, Fragkou P, Boviatsis E, Themistocleous MS, Petraki K, Vrettakos G, Sakalidou M, Samaras V, Zisakis A, Saetta A, Chatziandreou I, Patsouris E, Piperi C (2013) Sox11 expression in astrocytic gliomas: correlation with nestin/c-met/IDH1-R132H expression phenotypes, p-Stat-3 and survival. Br J Cancer 108:2142–2152
Kosho T, Miyake N, Carey JC (2014) Coffin-Siris syndrome and related disorders involving components of the BAF (mSWI/SNF) complex: historical review and recent advances using next generation sequencing. American journal of medical genetics part C, seminars in medical. Genetics 166C:241–251
Koumangoye RB, Andl T, Taubenslag KJ, Zilberman ST, Taylor CJ, Loomans HA, Andl CD (2015) SOX4 interacts with EZH2 and HDAC3 to suppress microRNA-31 in invasive esophageal cancer cells. Mol Cancer 14:24
Kuhlbrodt K, Herbarth B, Sock E, Enderich J, Hermans-Borgmeyer I, Wegner M (1998) Cooperative function of POU proteins and SOX proteins in glial cells. J Biol Chem 273:16050–16057
Kuwajima T, Soares CA, Sitko AA, Lefebvre V, Mason C (2017) SoxC transcription factors promote Contralateral retinal ganglion cell differentiation and axon guidance in the mouse visual system. Neuron 93:1110–1125 e1115
Lai HC, Seal RP, Johnson JE (2016) Making sense out of spinal cord somatosensory development. Development 143:3434–3448
Lamouille S, Xu J, Derynck R (2014) Molecular mechanisms of epithelial-mesenchymal transition. Nat Rev Mol Cell Biol 15:178–196
Li Y, Wang J, Zheng Y, Zhao Y, Guo M, Li Y, Bao Q, Zhang Y, Yang L, Li Q (2012) Sox11 modulates neocortical development by regulating the proliferation and neuronal differentiation of cortical intermediate precursors. Acta Biochim Biophys Sin 44:660–668
Li L, Li Q, Chen X, Xu M, Li X, Nie L, Chen N, Gong J, Mao Q, Zhou Q (2015) SOX4 is overexpressed in diffusely infiltrating astrocytoma and confers poor prognosis. Neuropathology 35:510–517
Lim S, Bhinge A, Bragado Alonso S, Aksoy I, Aprea J, Cheok CF, Calegari F, Stanton LW, Kaldis P (2017) Cdk-dependent phosphorylation of Sox2 at serine 39 regulates neurogenesis. Mol Cell Biol
Lin B, Madan A, Yoon JG, Fang X, Yan X, Kim TK, Hwang D, Hood L, Foltz G (2010) Massively parallel signature sequencing and bioinformatics analysis identifies up-regulation of TGFBI and SOX4 in human glioblastoma. PLoS ONE 5:e10210
Liu ML, Zang T, Zou Y, Chang JC, Gibson JR, Huber KM, Zhang CL (2013) Small molecules enable neurogenin 2 to efficiently convert human fibroblasts into cholinergic neurons. Nat Commun 4:2183
Lopez AJ, Wood MA (2015) Role of nucleosome remodeling in neurodevelopmental and intellectual disability disorders. Front Behav Neurosci 9:100
Mir S, Cai W, Carlson SW, Saatman KE, Andres DA (2017) IGF-1 mediated Neurogenesis involves a novel RIT1/Akt/Sox2 Cascade. Sci Rep 7:3283
Mu L, Berti L, Masserdotti G, Covic M, Michaelidis TM, Doberauer K, Merz K, Rehfeld F, Haslinger A, Wegner M, Sock E, Lefebvre V, Couillard-Despres S, Aigner L, Berninger B, Lie DC (2012) SoxC transcription factors are required for neuronal differentiation in adult hippocampal neurogenesis. J Neurosci 32:3067–3080
Mu Z, Zhang S, He C, Hou H, Liu D, Hu N, Xu H (2017) Expression of SoxC transcription factors during Zebrafish retinal and optic nerve regeneration. Neurosci Bull 33:53–61
Muralidharan B, Khatri Z, Maheshwari U, Gupta R, Roy B, Pradhan SJ, Karmodiya K, Padmanabhan H, Shetty AS, Balaji C, Kolthur-Seetharam U, Macklis JD, Galande S, Tole S (2017) LHX2 interacts with the NuRD complex and regulates cortical neuron subtype determinants Fezf2 and Sox11. J Neurosci 37:194–203
Nakagawa Y, Shimogori T (2012) Diversity of thalamic progenitor cells and postmitotic neurons. Eur J Neurosci 35:1554–1562
Ninkovic J, Steiner-Mezzadri A, Jawerka M, Akinci U, Masserdotti G, Petricca S, Fischer J, von Holst A, Beckers J, Lie CD, Petrik D, Miller E, Tang J, Wu J, Lefebvre V, Demmers J, Eisch A, Metzger D, Crabtree G, Irmler M, Poot R, Gotz M (2013) The BAF complex interacts with Pax6 in adult neural progenitors to establish a neurogenic cross-regulatory transcriptional network. Cell Stem Cell 13:403–418
Norsworthy MW, Bei F, Kawaguchi R, Wang Q, Tran NM, Li Y, Brommer B, Zhang Y, Wang C, Sanes JR, Coppola G, He Z (2017) Sox11 expression promotes regeneration of some retinal ganglion cell types but kills others. Neuron 94:1112–1120 e1114
Parvani JG, Schiemann WP (2013) Sox4, EMT programs, and the metastatic progression of breast cancers: mastering the masters of EMT. Breast Cancer Res 15:R72
Pevny L, Placzek M (2005) SOX genes and neural progenitor identity. Curr Opin Neurobiol 15:7–13
Poulin JF, Tasic B, Hjerling-Leffler J, Trimarchi JM, Awatramani R (2016) Disentangling neural cell diversity using single-cell transcriptomics. Nat Neurosci 19:1131–1141
Rajman M, Metge F, Fiore R, Khudayberdiev S, Aksoy-Aksel A, Bicker S, Ruedell Reschke C, Raoof R, Brennan GP, Delanty N, Farrell MA, O'Brien DF, Bauer S, Norwood B, Veno MT, Kruger M, Braun T, Kjems J, Rosenow F, Henshall DC, Dieterich C, Schratt G (2017) A microRNA-129-5p/Rbfox crosstalk coordinates homeostatic downscaling of excitatory synapses. EMBO J 36:1770–1787
Ravasi T, Suzuki H, Cannistraci CV, Katayama S, Bajic VB, Tan K, Akalin A, Schmeier S, Kanamori-Katayama M, Bertin N, Carninci P, Daub CO, Forrest AR, Gough J, Grimmond S, Han JH, Hashimoto T, Hide W, Hofmann O, Kamburov A, Kaur M, Kawaji H, Kubosaki A, Lassmann T, van Nimwegen E, MacPherson CR, Ogawa C, Radovanovic A, Schwartz A, Teasdale RD, Tegner J, Lenhard B, Teichmann SA, Arakawa T, Ninomiya N, Murakami K, Tagami M, Fukuda S, Imamura K, Kai C, Ishihara R, Kitazume Y, Kawai J, Hume DA, Ideker T, Hayashizaki Y (2010) An atlas of combinatorial transcriptional regulation in mouse and man. Cell 140:744–752
Salerno KM, Jing X, Diges CM, Cornuet PK, Glorioso JC, Albers KM (2012) Sox11 modulates brain-derived neurotrophic factor expression in an exon promoter-specific manner. J Neurosci Res 90:1011–1019
Salerno KM, Jing X, Diges CM, Davis BM, Albers KM (2013) TRAF family member-associated NF-kappa B activator (TANK) expression increases in injured sensory neurons and is transcriptionally regulated by Sox11. Neuroscience 231:28–37
Sandberg M, Kallstrom M, Muhr J (2005) Sox21 promotes the progression of vertebrate neurogenesis. Nat Neurosci 8:995–1001
Santen GW, Aten E, Sun Y, Almomani R, Gilissen C, Nielsen M, Kant SG, Snoeck IN, Peeters EA, Hilhorst-Hofstee Y, Wessels MW, den Hollander NS, Ruivenkamp CA, van Ommen GJ, Breuning MH, den Dunnen JT, van Haeringen A, Kriek M (2012) Mutations in SWI/SNF chromatin remodeling complex gene ARID1B cause coffin-Siris syndrome. Nat Genet 44:379–380
Shim S, Kwan KY, Li M, Lefebvre V, Sestan N (2012) Cis-regulatory control of corticospinal system development and evolution. Nature 486:74–79
Smith DK, Yang J, Liu ML, Zhang CL (2016) Small molecules modulate chromatin accessibility to promote NEUROG2-mediated fibroblast-to-neuron reprogramming. Stem Cell Rep 7:955–969
Su Z, Zang T, Liu ML, Wang LL, Niu W, Zhang CL (2014) Reprogramming the fate of human glioma cells to impede brain tumor development. Cell Death Dis 5:e1463
Sun W, Park KW, Choe J, Rhyu IJ, Kim IH, Park SK, Choi B, Choi SH, Park SH, Kim H (2005) Identification of novel electroconvulsive shock-induced and activity-dependent genes in the rat brain. Biochem Biophys Res Commun 327:848–856
Tanabe K, Bonilla I, Winkles JA, Strittmatter SM (2003) Fibroblast growth factor-inducible-14 is induced in axotomized neurons and promotes neurite outgrowth. J Neurosci 23:9675–9686
Tanaka S, Kamachi Y, Tanouchi A, Hamada H, Jing N, Kondoh H (2004) Interplay of SOX and POU factors in regulation of the nestin gene in neural primordial cells. Mol Cell Biol 24:8834–8846
Thein DC, Thalhammer JM, Hartwig AC, Crenshaw EB 3rd, Lefebvre V, Wegner M, Sock E (2010) The closely related transcription factors Sox4 and Sox11 function as survival factors during spinal cord development. J Neurochem 115:131–141
Tiwari N, Tiwari VK, Waldmeier L, Balwierz PJ, Arnold P, Pachkov M, Meyer-Schaller N, Schubeler D, van Nimwegen E, Christofori G (2013) Sox4 is a master regulator of epithelial-mesenchymal transition by controlling Ezh2 expression and epigenetic reprogramming. Cancer Cell 23:768–783
Tomassy GS, Fossati V (2014) How big is the myelinating orchestra? Cellular diversity within the oligodendrocyte lineage: facts and hypotheses. Front Cell Neurosci 8:201
Tsurusaki Y, Okamoto N, Ohashi H, Kosho T, Imai Y, Hibi-Ko Y, Kaname T, Naritomi K, Kawame H, Wakui K, Fukushima Y, Homma T, Kato M, Hiraki Y, Yamagata T, Yano S, Mizuno S, Sakazume S, Ishii T, Nagai T, Shiina M, Ogata K, Ohta T, Niikawa N, Miyatake S, Okada I, Mizuguchi T, Doi H, Saitsu H, Miyake N, Matsumoto N (2012) Mutations affecting components of the SWI/SNF complex cause coffin-Siris syndrome. Nat Genet 44:376–378
Tsurusaki Y, Koshimizu E, Ohashi H, Phadke S, Kou I, Shiina M, Suzuki T, Okamoto N, Imamura S, Yamashita M, Watanabe S, Yoshiura K, Kodera H, Miyatake S, Nakashima M, Saitsu H, Ogata K, Ikegawa S, Miyake N, Matsumoto N (2014) De novo SOX11 mutations cause coffin-Siris syndrome. Nat Commun 5:4011
Usui A, Iwagawa T, Mochizuki Y, Iida A, Wegner M, Murakami A, Watanabe S (2013a) Expression of Sox4 and Sox11 is regulated by multiple mechanisms during retinal development. FEBS Lett 587:358–363
Usui A, Mochizuki Y, Iida A, Miyauchi E, Satoh S, Sock E, Nakauchi H, Aburatani H, Murakami A, Wegner M, Watanabe S (2013b) The early retinal progenitor-expressed gene Sox11 regulates the timing of the differentiation of retinal cells. Development 140:740–750
Veldman MB, Bemben MA, Thompson RC, Goldman D (2007) Gene expression analysis of zebrafish retinal ganglion cells during optic nerve regeneration identifies KLF6a and KLF7a as important regulators of axon regeneration. Dev Biol 312:596–612
Waldron-Roby E, Hoerauf J, Arbez N, Zhu S, Kulcsar K, Ross CA (2015) Sox11 reduces Caspase-6 cleavage and activity. PLoS ONE 10:e0141439
Wang Y, Lin L, Lai H, Parada LF, Lei L (2013) Transcription factor Sox11 is essential for both embryonic and adult neurogenesis. Dev Dyn 242:638–653
Wang Z, Reynolds A, Kirry A, Nienhaus C, Blackmore MG (2015) Overexpression of Sox11 promotes corticospinal tract regeneration after spinal injury while interfering with functional recovery. J Neurosci 35:3139–3145
Wegner M (2010) All purpose Sox: the many roles of Sox proteins in gene expression. Int J Biochem Cell Biol 42:381–390
Welsbie DS, Mitchell KL, Jaskula-Ranga V, Sluch VM, Yang Z, Kim J, Buehler E, Patel A, Martin SE, Zhang PW, Ge Y, Duan Y, Fuller J, Kim BJ, Hamed E, Chamling X, Lei L, Fraser IDC, Ronai ZA, Berlinicke CA, Zack DJ (2017) Enhanced functional genomic screening identifies novel mediators of dual Leucine zipper Kinase-dependent injury Signaling in neurons. Neuron 94:1142–1154 e1146
Wiebe MS, Nowling TK, Rizzino A (2003) Identification of novel domains within Sox-2 and Sox-11 involved in autoinhibition of DNA binding and partnership specificity. J Biol Chem 278:17901–17911
Wieczorek D, Bogershausen N, Beleggia F, Steiner-Haldenstatt S, Pohl E, Li Y, Milz E, Martin M, Thiele H, Altmuller J, Alanay Y, Kayserili H, Klein-Hitpass L, Bohringer S, Wollstein A, Albrecht B, Boduroglu K, Caliebe A, Chrzanowska K, Cogulu O, Cristofoli F, Czeschik JC, Devriendt K, Dotti MT, Elcioglu N, Gener B, Goecke TO, Krajewska-Walasek M, Guillen-Navarro E, Hayek J, Houge G, Kilic E, Simsek-Kiper PO, Lopez-Gonzalez V, Kuechler A, Lyonnet S, Mari F, Marozza A, Mathieu Dramard M, Mikat B, Morin G, Morice-Picard F, Ozkinay F, Rauch A, Renieri A, Tinschert S, Utine GE, Vilain C, Vivarelli R, Zweier C, Nurnberg P, Rahmann S, Vermeesch J, Ludecke HJ, Zeschnigk M, Wollnik B (2013) A comprehensive molecular study on coffin-Siris and Nicolaides-Baraitser syndromes identifies a broad molecular and clinical spectrum converging on altered chromatin remodeling. Hum Mol Genet 22:5121–5135
Zhang J, Jiang H, Shao J, Mao R, Liu J, Ma Y, Fang X, Zhao N, Zheng S, Lin B (2014) SOX4 inhibits GBM cell growth and induces G0/G1 cell cycle arrest through Akt-p53 axis. BMC Neurol 14:207
Zhou Q, Liu M, Xia X, Gong T, Feng J, Liu W, Liu Y, Zhen B, Wang Y, Ding C, Qin J (2017) A mouse tissue transcription factor atlas. Nat Commun 8:15089
Zweier C, Kraus C, Brueton L, Cole T, Degenhardt F, Engels H, Gillessen-Kaesbach G, Graul-Neumann L, Horn D, Hoyer J, Just W, Rauch A, Reis A, Wollnik B, Zeschnigk M, Ludecke HJ, Wieczorek D (2013) A new face of Borjeson-Forssman-Lehmann syndrome? De novo mutations in PHF6 in seven females with a distinct phenotype. J Med Genet 50:838–847
Acknowledgments
This work was supported by grants from the German Research Foundation (LI 858/9-1 to D.C.L), the Bavarian Research Network “ForIPS”, the University Hospital Erlangen (IZKF grants E12, E16, and E21 to D.C.L.). A.K. and S.T. are members of the research training group 2162 “Neurodevelopment and Vulnerability of the Central Nervous System” of the Deutsche Forschungsgemeinschaft (DFG GRK2162/1). The authors declare no competing financial interests.
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Kavyanifar, A., Turan, S. & Lie, D.C. SoxC transcription factors: multifunctional regulators of neurodevelopment. Cell Tissue Res 371, 91–103 (2018). https://doi.org/10.1007/s00441-017-2708-7
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DOI: https://doi.org/10.1007/s00441-017-2708-7