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Open Access 01-11-2013 | Original Article

Postnatal isoform switch and protein localization of LEF1 and TCF7L2 transcription factors in cortical, thalamic, and mesencephalic regions of the adult mouse brain

Authors: A. Nagalski, M. Irimia, L. Szewczyk, J. L. Ferran, K. Misztal, J. Kuznicki, M. B. Wisniewska

Published in: Brain Structure and Function | Issue 6/2013

Abstract

β-Catenin signaling, leading to the activation of lymphoid enhancer-binding factor 1/T cell factor (LEF1/TCF) transcription factors, plays a well-established role in transcription regulation during development and tissue homeostasis. In the adult organism, the activity of this pathway has been found in stem cell niches and postmitotic thalamic neurons. Recently, studies show that mutations in components of β-catenin signaling networks have been associated with several psychiatric disorders, indicating the involvement of β-catenin and LEF1/TCF proteins in the proper functioning of the brain. Here, we report a comprehensive analysis of LEF1/TCF protein localization and the expression profile of their isoforms in cortical, thalamic, and midbrain regions in mice. We detected LEF1 and TCF7L2 proteins in neurons of the thalamus and dorsal midbrain, i.e., subcortical regions specialized in the integration of diverse sources of sensory information. These neurons also exhibited nuclear localization of β-catenin, suggesting the involvement of β-catenin/LEF1/TCF7L2 in the regulation of gene expression in these regions. Analysis of alternative splicing and promoter usage identified brain-specific TCF7L2 isoforms and revealed a developmentally coordinated transition in the composition of LEF1 and TCF7L2 isoforms. In the case of TCF7L2, the typical brain isoforms lack the so-called C clamp; in addition, the dominant-negative isoforms are predominant in the embryonic thalamus but disappear postnatally. The present study provides a necessary framework to understand the role of LEF1/TCF factors in thalamic and midbrain development until adulthood and predicts that the regulatory role of these proteins in the adult brain is significantly different from their role in the embryonic brain or other non-neural tissues.

Aizawa H, Amo R, Okamoto H (2011) Phylogeny and ontogeny of the habenular structure. Front Neurosci 5:138PubMed

Alkelai A, Greenbaum L, Lupoli S et al (2012) Association of the type 2 diabetes mellitus susceptibility gene, TCF7L2, with schizophrenia in an Arab-Israeli family sample. PLoS ONE 7:e29228PubMed

Angers S, Moon RT (2009) Proximal events in Wnt signal transduction. Nat Rev Mol Cell Biol 10:468–477PubMed

Arce L, Yokoyama NN, Waterman ML (2006) Diversity of LEF/TCF action in development and disease. Oncogene 25:7492–7504PubMed

Archbold HC, Yang YX, Chen L, Cadigan KM (2012) How do they do Wnt they do?: regulation of transcription by the Wnt/β-catenin pathway. Acta Physiol (Oxf) 204:74–109

Atcha FA, Syed A, Wu B et al (2007) A unique DNA binding domain converts T-cell factors into strong Wnt effectors. Mol Cell Biol 27:8352–8363PubMed

Balmelle N, Zamarreño N, Krangel MS, Hernández-Munain C (2004) Developmental activation of the TCR alpha enhancer requires functional collaboration among proteins bound inside and outside the core enhancer. J Immunol 173:5054–5063PubMed

Bandler R, Shipley MT (1994) Columnar organization in the midbrain periaqueductal gray: modules for emotional expression? Trends Neurosci 17:379–389PubMed

Barolo S (2006) Transgenic Wnt/TCF pathway reporters: all you need is Lef? Oncogene 25:7505–7511PubMed

Basso MA, Uhlrich D, Bickford ME (2005) Cortical function: a view from the thalamus. Neuron 45:485–488PubMed

Bianco IH, Wilson SW (2009) The habenular nuclei: a conserved asymmetric relay station in the vertebrate brain. Philos Trans R Soc Lond B Biol Sci 364:1005–1020PubMed

Bluske KK, Kawakami Y, Koyano-Nakagawa N, Nakagawa Y (2009) Differential activity of Wnt/beta-catenin signaling in the embryonic mouse thalamus. Dev Dyn 238:3297–3309PubMed

Bluske KK, Vue TY, Kawakami Y, Taketo MM, Yoshikawa K, Johnson JE, Nakagawa Y (2012) β-Catenin signaling specifies progenitor cell identity in parallel with Shh signaling in the developing mammalian thalamus. Development 139:2692–2702

Braun MM, Etheridge A, Bernard A, Robertson CP, Roelink H (2003) Wnt signaling is required at distinct stages of development for the induction of the posterior forebrain. Development 130:5579–5587PubMed

Brawand D, Soumillon M, Necsulea A et al (2011) The evolution of gene expression levels in mammalian organs. Nature 478:343–348PubMed

Bruhn L, Munnerlyn A, Grosschedl R (1997) ALY, a context-dependent coactivator of LEF-1 and AML-1, is required for TCRalpha enhancer function. Genes Dev 11:640–653PubMed

Byne W, Hazlett EA, Buchsbaum MS, Kemether E (2009) The thalamus and schizophrenia: current status of research. Acta Neuropathol 117:347–368PubMed

Carlsson P, Waterman ML, Jones KA (1993) The hLEF/TCF-1 alpha HMG protein contains a context-dependent transcriptional activation domain that induces the TCR alpha enhancer in T cells. Genes Dev 7:2418–2430PubMed

Chang MV, Chang JL, Gangopadhyay A, Shearer A, Cadigan KM (2008) Activation of wingless targets requires bipartite recognition of DNA by TCF. Curr Biol 18:1877–1881PubMed

Chen L, Guo Q, Li JY (2009) Transcription factor Gbx2 acts cell-nonautonomously to regulate the formation of lineage-restriction boundaries of the thalamus. Development 136:1317–1326PubMed

Cho EA, Dressler GR (1998) TCF-4 binds beta-catenin and is expressed in distinct regions of the embryonic brain and limbs. Mech Dev 77:9–18PubMed

Ciani L, Salinas PC (2005) WNTs in the vertebrate nervous system: from patterning to neuronal connectivity. Nat Rev Neurosci 6:351–362PubMed

Cronenwett WJ, Csernansky J (2010) Thalamic pathology in schizophrenia. Curr Top Behav Neurosci 4:509–528PubMed

Cui DH, Jiang KD, Jiang SD, Xu YF, Yao H (2005) The tumor suppressor adenomatous polyposis coli gene is associated with susceptibility to schizophrenia. Mol Psychiatry 10:669–677PubMed

Cuppini C, Ursino M, Magosso E, Rowland BA, Stein BE (2010) An emergent model of multisensory integration in superior colliculus neurons. Front Integr Neurosci 4:6PubMed

De Biasi S, Amadeo A, Arcelli P, Frassoni C, Spreafico R (1997) Postnatal development of GABA-immunoreactive terminals in the reticular and ventrobasal nuclei of the rat thalamus: a light and electron microscopic study. Neuroscience 76:503–515PubMed

Dommett EJ, Overton PG, Greenfield SA (2009) Drug therapies for attentional disorders alter the signal-to-noise ratio in the superior colliculus. Neuroscience 164:1369–1376PubMed

Duval A, Rolland S, Tubacher E, Bui H, Thomas G, Hamelin R (2000) The human T-cell transcription factor-4 gene: structure, extensive characterization of alternative splicings, and mutational analysis in colorectal cancer cell lines. Cancer Res 60:3872–3879PubMed

Eade KT, Fancher HA, Ridyard MS, Allan DW (2012) Developmental transcriptional networks are required to maintain neuronal subtype identity in the mature nervous system. PLoS Genet 8:e1002501PubMed

Ellis JD, Barrios-Rodiles M, Colak R et al (2012) Tissue-specific alternative splicing remodels protein–protein interaction networks. Mol Cell 46:884–892PubMed

Fancy SP, Baranzini SE, Zhao C et al (2009) Dysregulation of the Wnt pathway inhibits timely myelination and remyelination in the mammalian CNS. Genes Dev 23:1571–1585PubMed

Ferran JL, Sánchez-Arrones L, Sandoval JE, Puelles L (2007) A model of early molecular regionalization in the chicken embryonic pretectum. J Comp Neurol 505:379–403PubMed

Flames N, Hobert O (2009) Gene regulatory logic of dopamine neuron differentiation. Nature 458:885–889PubMed

Floyd NS, Price JL, Ferry AT, Keay KA, Bandler R (2000) Orbitomedial prefrontal cortical projections to distinct longitudinal columns of the periaqueductal gray in the rat. J Comp Neurol 422:556–578PubMed

Fowler CD, Kenny PJ (2012) Habenular signaling in nicotine reinforcement. Neuropsychopharmacology 37:306–307PubMed

Freese JL, Pino D, Pleasure SJ (2010) Wnt signaling in development and disease. Neurobiol Dis 38:148–153PubMed

Galceran J, Miyashita-Lin EM, Devaney E, Rubenstein JL, Grosschedl R (2000) Hippocampus development and generation of dentate gyrus granule cells is regulated by LEF1. Development 127:469–482PubMed

Ghogomu SM, van Venrooy S, Ritthaler M, Wedlich D, Gradl D (2006) HIC-5 is a novel repressor of lymphoid enhancer factor/T-cell factor-driven transcription. J Biol Chem 281:1755–1764PubMed

Giese K, Kingsley C, Kirshner JR, Grosschedl R (1995) Assembly and function of a TCR alpha enhancer complex is dependent on LEF-1-induced DNA bending and multiple protein–protein interactions. Genes Dev 9:995–1008PubMed

Gradl D, König A, Wedlich D (2002) Functional diversity of Xenopus lymphoid enhancer factor/T-cell factor transcription factors relies on combinations of activating and repressing elements. J Biol Chem 277:14159–14171PubMed

Grigoryan T, Wend P, Klaus A, Birchmeier W (2008) Deciphering the function of canonical Wnt signals in development and disease: conditional loss- and gain-of-function mutations of beta-catenin in mice. Genes Dev 22:2308–2341PubMed

Guller Y, Ferrarelli F, Shackman AJ et al (2012) Probing thalamic integrity in schizophrenia using concurrent transcranial magnetic stimulation and functional magnetic resonance imaging. Arch Gen Psychiatry. doi:archgenpsychiatry.2012.23

Haegebarth A, Clevers H (2009) Wnt signaling, lgr5, and stem cells in the intestine and skin. Am J Pathol 174:715–721PubMed

Hagemann AI, Scholpp S (2012) The tale of the three brothers—Shh, Wnt, and Fgf during development of the thalamus. Front Neurosci 6:76PubMed

Hallikas O, Palin K, Sinjushina N, Rautiainen R, Partanen J, Ukkonen E, Taipale J (2006) Genome-wide prediction of mammalian enhancers based on analysis of transcription-factor binding affinity. Cell 124:47–59PubMed

Hansen T, Ingason A, Djurovic S et al (2011) At-risk variant in TCF7L2 for type II diabetes increases risk of schizophrenia. Biol Psychiatry 70:59–63PubMed

Hecht A, Stemmler MP (2003) Identification of a promoter-specific transcriptional activation domain at the C terminus of the Wnt effector protein T-cell factor 4. J Biol Chem 278:3776–3785PubMed

Hikosaka O (2010) The habenula: from stress evasion to value-based decision-making. Nat Rev Neurosci 11:503–513PubMed

Hoeppner LH, Secreto FJ, Razidlo DF, Whitney TJ, Westendorf JJ (2011) Lef1DeltaN binds beta-catenin and increases osteoblast activity and trabecular bone mass. J Biol Chem 286:10950–10959PubMed

Hovanes K, Li TW, Waterman ML (2000) The human LEF-1 gene contains a promoter preferentially active in lymphocytes and encodes multiple isoforms derived from alternative splicing. Nucleic Acids Res 28:1994–2003PubMed

Hovanes K, Li TW, Munguia JE et al (2001) Beta-catenin-sensitive isoforms of lymphoid enhancer factor-1 are selectively expressed in colon cancer. Nat Genet 28:53–57PubMed

Hoverter NP, Ting JH, Sundaresh S, Baldi P, Waterman ML (2012) A WNT/p21 circuit directed by the C-clamp, a sequence-specific DNA binding domain in TCFs. Mol Cell Biol. doi:MCB.06769-11 PubMed

Jones EG (2009) Synchrony in the interconnected circuitry of the thalamus and cerebral cortex. Ann N Y Acad Sci 1157:10–23PubMed

Jones EG, Rubenstein JL (2004) Expression of regulatory genes during differentiation of thalamic nuclei in mouse and monkey. J Comp Neurol 477:55–80PubMed

Kang DH, Kwon KW, Gu BM, Choi JS, Jang JH, Kwon JS (2008) Structural abnormalities of the right inferior colliculus in schizophrenia. Psychiatry Res 164:160–165PubMed

Keay KA, Bandler R (2001) Parallel circuits mediating distinct emotional coping reactions to different types of stress. Neurosci Biobehav Rev 25:669–678PubMed

Kidd FL, Isaac JT (1999) Developmental and activity-dependent regulation of kainate receptors at thalamocortical synapses. Nature 400:569–573PubMed

Kishimoto M, Ujike H, Okahisa Y et al (2008) The Frizzled 3 gene is associated with methamphetamine psychosis in the Japanese population. Behav Brain Funct 4:37PubMed

Klingel S, Morath I, Strietz J, Menzel K, Holstein TW, Gradl D (2012) Subfunctionalization and neofunctionalization of vertebrate Lef/Tcf transcription factors. Dev Biol 368:44–53PubMed

Korinek V, Barker N, Moerer P, van Donselaar E, Huls G, Peters PJ, Clevers H (1998a) Depletion of epithelial stem-cell compartments in the small intestine of mice lacking Tcf-4. Nat Genet 19:379–383PubMed

Korinek V, Barker N, Willert K et al (1998b) Two members of the Tcf family implicated in Wnt/beta-catenin signaling during embryogenesis in the mouse. Mol Cell Biol 18:1248–1256PubMed

Kratsios P, Stolfi A, Levine M, Hobert O (2012) Coordinated regulation of cholinergic motor neuron traits through a conserved terminal selector gene. Nat Neurosci 15:205–214

Krauzlis RJ, Liston D, Carello CD (2004) Target selection and the superior colliculus: goals, choices and hypotheses. Vision Res 44:1445–1451PubMed

Krout KE, Loewy AD (2000) Periaqueductal gray matter projections to midline and intralaminar thalamic nuclei of the rat. J Comp Neurol 424:111–141PubMed

Krout KE, Loewy AD, Westby GW, Redgrave P (2001) Superior colliculus projections to midline and intralaminar thalamic nuclei of the rat. J Comp Neurol 431:198–216PubMed

Kuwabara T, Hsieh J, Muotri A et al (2009) Wnt-mediated activation of NeuroD1 and retro-elements during adult neurogenesis. Nat Neurosci 12:1097–1105PubMed

Langer TP, Lund RD (1974) The upper layers of the superior colliculus of the rat: a Golgi study. J Comp Neurol 158:418–435PubMed

Lee S, Lee CE, Elias CF, Elmquist JK (2009) Expression of the diabetes-associated gene TCF7L2 in adult mouse brain. J Comp Neurol 517:925–939PubMed

Li M, Mo Y, Luo XJ et al (2011) Genetic association and identification of a functional SNP at GSK3β for schizophrenia susceptibility. Schizophr Res 133:165–171PubMed

Lie DC, Colamarino SA, Song HJ et al (2005) Wnt signalling regulates adult hippocampal neurogenesis. Nature 437:1370–1375PubMed

Liu F, van den Broek O, Destrée O, Hoppler S (2005) Distinct roles for Xenopus Tcf/Lef genes in mediating specific responses to Wnt/beta-catenin signalling in mesoderm development. Development 132:5375–5385PubMed

Liu C, Maejima T, Wyler SC, Casadesus G, Herlitze S, Deneris ES (2010) Pet-1 is required across different stages of life to regulate serotonergic function. Nat Neurosci 13:1190–1198PubMed

Logan CY, Nusse R (2004) The Wnt signaling pathway in development and disease. Annu Rev Cell Dev Biol 20:781–810. doi:10.1146/annurev.cellbio.20.010403.113126 PubMed

Lorente-Cánovas B, Marín F, Corral-San-Miguel R, Hidalgo-Sánchez M, Ferrán JL, Puelles L, Aroca P (2012) Multiple origins, migratory paths and molecular profiles of cells populating the avian interpeduncular nucleus. Dev Biol 361:12–26PubMed

Lucas JJ, Hernández F, Avila J (1999) Nuclear localization of beta-catenin in adult mouse thalamus correlates with low levels of GSK-3beta. NeuroReport 10:2699–2703PubMed

MacDonald BT, Tamai K, He X (2009) Wnt/beta-catenin signaling: components, mechanisms, and diseases. Dev Cell 17:9–26PubMed

Mahmoudi T, Boj SF, Hatzis P et al (2010) The leukemia-associated Mllt10/Af10-Dot1 l are Tcf4/β-catenin coactivators essential for intestinal homeostasis. PLoS Biol 8:e1000539PubMed

Mallory MJ, Jackson J, Weber B, Chi A, Heyd F, Lynch KW (2011) Signal- and development-dependent alternative splicing of LEF1 in T cells is controlled by CELF2. Mol Cell Biol 31:2184–2195PubMed

Maretto S, Cordenonsi M, Dupont S et al (2003) Mapping Wnt/beta-catenin signaling during mouse development and in colorectal tumors. Proc Natl Acad Sci USA 100:3299–3304PubMed

May PJ (2006) The mammalian superior colliculus: laminar structure and connections. Prog Brain Res 151:321–378PubMed

Mayall TP, Sheridan PL, Montminy MR, Jones KA (1997) Distinct roles for P-CREB and LEF-1 in TCR alpha enhancer assembly and activation on chromatin templates in vitro. Genes Dev 11:887–899PubMed

McMahon AP, Bradley A (1990) The Wnt-1 (int-1) proto-oncogene is required for development of a large region of the mouse brain. Cell 62:1073–1085PubMed

McMahon AP, Joyner AL, Bradley A, McMahon JA (1992) The midbrain-hindbrain phenotype of Wnt-1-/Wnt-1- mice results from stepwise deletion of engrailed-expressing cells by 9.5 days postcoitum. Cell 69:581–595PubMed

Merchán P, Bardet SM, Puelles L, Ferran JL (2011) Comparison of pretectal genoarchitectonic pattern between quail and chicken embryos. Front Neuroanat 5:23PubMed

Misztal K, Wisniewska MB, Ambrozkiewicz M, Nagalski A, Kuznicki J (2011) WNT protein-independent constitutive nuclear localization of beta-catenin protein and its low degradation rate in thalamic neurons. J Biol Chem 286:31781–31788PubMed

Morona R, Ferran JL, Puelles L, González A (2011) Embryonic genoarchitecture of the pretectum in Xenopus laevis: a conserved pattern in tetrapods. J Comp Neurol 519:1024–1050PubMed

Mukhopadhyay M, Shtrom S, Rodriguez-Esteban C et al (2001) Dickkopf1 is required for embryonic head induction and limb morphogenesis in the mouse. Dev Cell 1:423–434PubMed

Nazwar TA, Glassmann A, Schilling K (2009) Expression and molecular diversity of Tcf7l2 in the developing murine cerebellum and brain. J Neurosci Res 87:1532–1546PubMed

Niehrs C (2010) On growth and form: a Cartesian coordinate system of Wnt and BMP signaling specifies bilaterian body axes. Development 137:845–857PubMed

Norton WT, Poduslo SE (1971) Neuronal perikarya and astroglia of rat brain: chemical composition during myelination. J Lipid Res 12:84–90PubMed

Noutel J, Hong YK, Leu B, Kang E, Chen C (2011) Experience-dependent retinogeniculate synapse remodeling is abnormal in MeCP2-deficient mice. Neuron 70:35–42PubMed

Oosterwegel M, van de Wetering M, Timmerman J, Kruisbeek A, Destree O, Meijlink F, Clevers H (1993) Differential expression of the HMG box factors TCF-1 and LEF-1 during murine embryogenesis. Development 118:439–448PubMed

O’Roak BJ, Vives L, Girirajan S et al (2012) Sporadic autism exomes reveal a highly interconnected protein network of de novo mutations. Nature. doi:nature10989 PubMed

Parri HR, Crunelli V (2002) Astrocytes, spontaneity, and the developing thalamus. J Physiol Paris 96:221–230PubMed

Petersen CP, Reddien PW (2009) Wnt signaling and the polarity of the primary body axis. Cell 139:1056–1068PubMed

Peukert D, Weber S, Lumsden A, Scholpp S (2011) Lhx2 and Lhx9 determine neuronal differentiation and compartition in the caudal forebrain by regulating Wnt signaling. PLoS Biol 9:e1001218PubMed

Pinault D (2011) Dysfunctional thalamus-related networks in schizophrenia. Schizophr Bull 37:238–243PubMed

Pinson KI, Brennan J, Monkley S, Avery BJ, Skarnes WC (2000) An LDL-receptor-related protein mediates Wnt signalling in mice. Nature 407:535–538PubMed

Pratt T, Davey JW, Nowakowski TJ et al (2012) The expression and activity of β-catenin in the thalamus and its projections to the cerebral cortex in the mouse embryo. BMC Neurosci 13:20PubMed

Proitsi P, Li T, Hamilton G et al (2008) Positional pathway screen of wnt signaling genes in schizophrenia: association with DKK4. Biol Psychiatry 63:13–16PubMed

Puelles E, Martinez-de-la-Torre M, Watson C (2011) Midbrain. Elsevier, San Diego, pp 337–359

Pukrop T, Gradl D, Henningfeld KA, Knochel W, Wedlich D, Kuhl M (2001) Identification of two regulatory elements within the high mobility group box transcription factor XTCF-4. J Biol Chem 276:8968–8978PubMed

Quinlan R, Graf M, Mason I, Lumsden A, Kiecker C (2009) Complex and dynamic patterns of Wnt pathway gene expression in the developing chick forebrain. Neural Dev 4:35PubMed

Ramoa AS, McCormick DA (1994) Developmental changes in electrophysiological properties of LGNd neurons during reorganization of retinogeniculate connections. J Neurosci 14:2089–2097PubMed

Roose J, Huls G, van Beest M et al (1999) Synergy between tumor suppressor APC and the beta-catenin-Tcf4 target Tcf1. Science 285:1923–1926PubMed

Rukov JL, Irimia M, Mørk S, Lund VK, Vinther J, Arctander P (2007) High qualitative and quantitative conservation of alternative splicing in Caenorhabditis elegans and Caenorhabditis briggsae. Mol Biol Evol 24:909–917PubMed

Savic D, Distler MG, Sokoloff G, Shanahan NA, Dulawa SC, Palmer AA, Nobrega MA (2011) Modulation of Tcf7l2 expression alters behavior in mice. PLoS ONE 6:e26897PubMed

Sherman SM, Guillery RW (2002) The role of the thalamus in the flow of information to the cortex. Philos Trans R Soc Lond B Biol Sci 357:1695–1708PubMed

Shimogori T, VanSant J, Paik E, Grove EA (2004) Members of the Wnt, Fz, and Frp gene families expressed in postnatal mouse cerebral cortex. J Comp Neurol 473:496–510PubMed

Shimogori T, Lee DA, Miranda-Angulo A et al (2010) A genomic atlas of mouse hypothalamic development. Nat Neurosci 13:767–775PubMed

Steriade M (1997) Synchronized activities of coupled oscillators in the cerebral cortex and thalamus at different levels of vigilance. Cereb Cortex 7:583–604PubMed

Thomas KR, Capecchi MR (1990) Targeted disruption of the murine int-1 proto-oncogene resulting in severe abnormalities in midbrain and cerebellar development. Nature 346:847–850PubMed

Vacik T, Stubbs JL, Lemke G (2011) A novel mechanism for the transcriptional regulation of Wnt signaling in development. Genes Dev 25:1783–1795PubMed

Vadlamudi U, Espinoza HM, Ganga M, Martin DM, Liu X, Engelhardt JF, Amendt BA (2005) PITX2, beta-catenin and LEF-1 interact to synergistically regulate the LEF-1 promoter. J Cell Sci 118:1129–1137PubMed

van Beest M, Dooijes D, van De Wetering M, Kjaerulff S, Bonvin A, Nielsen O, Clevers H (2000) Sequence-specific high mobility group box factors recognize 10–12-base pair minor groove motifs. J Biol Chem 275:27266–27273PubMed

Van de Wetering M, Castrop J, Korinek V, Clevers H (1996) Extensive alternative splicing and dual promoter usage generate Tcf-1 protein isoforms with differential transcription control properties. Mol Cell Biol 16:745–752PubMed

van de Wetering M, Cavallo R, Dooijes D et al (1997) Armadillo coactivates transcription driven by the product of the Drosophila segment polarity gene dTCF. Cell 88:789–799PubMed

Van der Werf YD, Witter MP, Groenewegen HJ (2002) The intralaminar and midline nuclei of the thalamus. Anatomical and functional evidence for participation in processes of arousal and awareness. Brain Res Brain Res Rev 39:107–140PubMed

Vue TY, Aaker J, Taniguchi A et al (2007) Characterization of progenitor domains in the developing mouse thalamus. J Comp Neurol 505:73–91PubMed

Waterman ML, Fischer WH, Jones KA (1991) A thymus-specific member of the HMG protein family regulates the human T cell receptor C alpha enhancer. Genes Dev 5:656–669PubMed

Weise A, Bruser K, Elfert S, Wallmen B, Wittel Y, Wöhrle S, Hecht A (2010) Alternative splicing of Tcf7l2 transcripts generates protein variants with differential promoter-binding and transcriptional activation properties at Wnt/beta-catenin targets. Nucleic Acids Res 38:1964–1981PubMed

Wend P, Holland JD, Ziebold U, Birchmeier W (2010) Wnt signaling in stem and cancer stem cells. Semin Cell Dev Biol 21:855–863PubMed

Wisniewska MB, Misztal K, Michowski W et al (2010) LEF1/beta-catenin complex regulates transcription of the Cav3.1 calcium channel gene (Cacna1 g) in thalamic neurons of the adult brain. J Neurosci 30:4957–4969PubMed

Yamaguchi TP (2001) Heads or tails: Wnts and anterior-posterior patterning. Curr Biol 11:R713–R724PubMed

Ye F, Chen Y, Hoang T et al (2009) HDAC1 and HDAC2 regulate oligodendrocyte differentiation by disrupting the beta-catenin-TCF interaction. Nat Neurosci 12:829–838PubMed

Yin Y, White AC, Huh SH, Hilton MJ, Kanazawa H, Long F, Ornitz DM (2008) An FGF-WNT gene regulatory network controls lung mesenchyme development. Dev Biol 319:426–436PubMed

Young RM, Reyes AE, Allende ML (2002) Expression and splice variant analysis of the zebrafish tcf4 transcription factor. Mech Dev 117:269–273PubMed

Zhou CJ, Pinson KI, Pleasure SJ (2004) Severe defects in dorsal thalamic development in low-density lipoprotein receptor-related protein-6 mutants. J Neurosci 24:7632–7639PubMed

Title: Postnatal isoform switch and protein localization of LEF1 and TCF7L2 transcription factors in cortical, thalamic, and mesencephalic regions of the adult mouse brain
Authors: A. Nagalski
M. Irimia
L. Szewczyk
J. L. Ferran
K. Misztal
J. Kuznicki
M. B. Wisniewska
Publication date: 01-11-2013
Publisher: Springer Berlin Heidelberg
Published in: Brain Structure and Function / Issue 6/2013
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-012-0474-6

Keynote webinar | Spotlight on sleep in brain health

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Postnatal isoform switch and protein localization of LEF1 and TCF7L2 transcription factors in cortical, thalamic, and mesencephalic regions of the adult mouse brain

Abstract

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Abstract

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