Issue
Notch Signaling and MicroRNA: The Dynamic Duo Steering Between Neurogenesis and Glioblastomas
Corresponding Author(s) : Javad Sharifi-Rad
Cellular and Molecular Biology,
Vol. 67 No. 2: Issue 2
Abstract
Keywords
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- Dexter JS. The analysis of a case of continuous variation in Drosophila by a study of its linkage relations. The American Naturalist 1914; 48(576): 712-758.
- Artavanis-Tsakonas S, Muskavitch M, Yedvobnick B. Molecular cloning of Notch, a locus affecting neurogenesis in Drosophila melanogaster. Proceedings of the National Academy of Sciences 1983; 80(7): 1977-1981.
- Kopan R, Ilagan MXG. The canonical Notch signaling pathway: unfolding the activation mechanism. Cell 2009; 137(2): 216-233.
- Henrique D, Schweisguth F. Mechanisms of Notch signaling: a simple logic deployed in time and space. Development 2019; 146(3): dev172148.
- Basak O, Giachino C, Fiorini E, MacDonald HR, Taylor V. Neurogenic subventricular zone stem/progenitor cells are Notch1-dependent in their active but not quiescent state. J Neurosci 2012; 32(16): 5654-5666.
- Gaiano N, Fishell G. The role of notch in promoting glial and neural stem cell fates. Annu Rev Neurosci 2002; 25(1): 471-490.
- Bellec K, Gicquel I, Le Borgne R. The Clathrin adaptor AP-1 and the Rab-stabilizing chaperone Stratum act in two parallel pathways to control the activation of the Notch pathway in Drosophila. bioRxiv 2019: 645580.
- Rebay I, Fleming RJ, Fehon RG, Cherbas L, Cherbas P, Artavanis-Tsakonas S. Specific EGF repeats of Notch mediate interactions with Delta and Serrate: implications for Notch as a multifunctional receptor. Cell 1991; 67(4): 687-699.
- Andersson ER, Lendahl U. Therapeutic modulation of Notch signalling”are we there yet? Nature reviews Drug discovery 2014; 13(5): 357.
- Ogawa M. A New Type of O-Glucose Modification by POGLUT2 and POGLUT3 Controls Notch Signaling and Trafficking. Trends in Glycoscience and Glycotechnology 2019; 31(179): E53-E54.
- Mumm JS, Kopan R. Notch signaling: from the outside in. Dev Biol 2000; 228(2): 151-165.
- Jarrett SM, Seegar TC, Andrews M et al. Molecular basis for feedback inhibition of Notch signaling by the Notch regulated ankyrin repeat protein NRARP. bioRxiv 2019: 645937.
- Borggrefe T, Oswald F. The Notch signaling pathway: transcriptional regulation at Notch target genes. Cell Mol Life Sci 2009; 66(10): 1631-1646.
- Guenther MG, Barak O, Lazar MA. The SMRT and N-CoR corepressors are activating cofactors for histone deacetylase 3. Mol Cell Biol 2001; 21(18): 6091-6101.
- Okubo Y, Ohtake F, Igarashi K et al. Tuning of Neural Development Via Lateral Inhibition by Bi-Directional Notch-Delta Signaling. Available at SSRN 3351827 2019.
- Ohtsuka T, Ishibashi M, Gradwohl G, Nakanishi S, Guillemot F, Kageyama R. Hes1 and Hes5 as notch effectors in mammalian neuronal differentiation. The EMBO journal 1999; 18(8): 2196-2207.
- Bertrand N, Castro DS, Guillemot F. Proneural genes and the specification of neural cell types. Nature Reviews Neuroscience 2002; 3(7): 517.
- Gao J, Van Meter M, Lopez SH et al. Therapeutic targeting of Notch signaling and immune checkpoint blockade in a spontaneous, genetically-heterogeneous mouse model of T-cell acute lymphoblastic leukemia. Disease models & mechanisms 2019: dmm. 040931.
- Harris L, Guillemot F. HES1, two programs: promoting the quiescence and proliferation of adult neural stem cells. Genes & development 2019; 33(9-10): 479-481.
- Ross SE, Greenberg ME, Stiles CD. Basic helix-loop-helix factors in cortical development. Neuron 2003; 39(1): 13-25.
- Nandagopal N, Santat LA, Elowitz MB. Cis-activation in the Notch signaling pathway. eLife 2019; 8: e37880.
- Castro DS, Skowronska-Krawczyk D, Armant O et al. Proneural bHLH and Brn proteins coregulate a neurogenic program through cooperative binding to a conserved DNA motif. Dev Cell 2006; 11(6): 831-844.
- Shimojo H, Ohtsuka T, Kageyama R. Oscillations in notch signaling regulate maintenance of neural progenitors. Neuron 2008; 58(1): 52-64.
- Imayoshi I, Isomura A, Harima Y et al. Oscillatory control of factors determining multipotency and fate in mouse neural progenitors. Science 2013; 342(6163): 1203-1208.
- Haines N, Irvine KD. Glycosylation regulates Notch signalling. Nature reviews Molecular cell biology 2003; 4(10): 786.
- Fortini ME. Notch signaling: the core pathway and its posttranslational regulation. Dev Cell 2009; 16(5): 633-647.
- Li Y, Li L, Irvine KD, Baker NE. Notch activity in neural cells triggered by a mutant allele with altered glycosylation. Development 2003; 130(13): 2829-2840.
- Song Y, Willer JR, Scherer PC et al. Neural and synaptic defects in slytherin, a zebrafish model for human congenital disorders of glycosylation. PLoS One 2010; 5(10): e13743.
- Chi Z, Zhang J, Tokunaga A et al. Botch promotes neurogenesis by antagonizing Notch. Dev Cell 2012; 22(4): 707-720.
- Couturier L, Vodovar N, Schweisguth F. Endocytosis by Numb breaks Notch symmetry at cytokinesis. Nat Cell Biol 2012; 14(2): 131.
- Kressmann S, Campos C, Castanon I, Fürthauer M, González-Gaitán M. Directional Notch trafficking in Sara endosomes during asymmetric cell division in the spinal cord. Nat Cell Biol 2015; 17(3): 333.
- Bekri A, Liao M, Drapeau P. Glycine regulates neural stem cell proliferation during development via Lnx1-dependent Notch signaling. Frontiers in molecular neuroscience 2019; 12.
- Ohtsuka T, Kageyama R. Regulation of temporal properties of neural stem cells and transition timing of neurogenesis and gliogenesis during mammalian neocortical development. Paper presented at: Seminars in cell & developmental biology, 2019.
- Shi Y, Zhao X, Hsieh J et al. MicroRNA regulation of neural stem cells and neurogenesis. J Neurosci 2010; 30(45): 14931-14936.
- Zhao X, Ueba T, Christie BR et al. Mice lacking methyl-CpG binding protein 1 have deficits in adult neurogenesis and hippocampal function. Proceedings of the National Academy of Sciences 2003; 100(11): 6777-6782.
- Hitoshi S, Ishino Y, Kumar A et al. Mammalian Gcm genes induce Hes5 expression by active DNA demethylation and induce neural stem cells. Nat Neurosci 2011; 14(8): 957.
- Kim M, Park Y-K, Kang T-W et al. Dynamic changes in DNA methylation and hydroxymethylation when hES cells undergo differentiation toward a neuronal lineage. Hum Mol Genet 2013; 23(3): 657-667.
- Zhang Z, Gao F, Kang X et al. Exploring the potential relationship between Notch pathway genes expression and their promoter methylation in mice hippocampal neurogenesis. Brain Res Bull 2015; 113: 8-16.
- Kouzarides T. Chromatin modifications and their function. Cell 2007; 128(4): 693-705.
- Oswald F, Täuber B, Dobner T et al. p300 acts as a transcriptional coactivator for mammalian Notch-1. Mol Cell Biol 2001; 21(22): 7761-7774.
- Kurooka H, Honjo T. Functional interaction between the mouse notch1 intracellular region and histone acetyltransferases PCAF and GCN5. J Biol Chem 2000; 275(22): 17211-17220.
- Kao H-Y, Ordentlich P, Koyano-Nakagawa N et al. A histone deacetylase corepressor complex regulates the Notch signal transduction pathway. Genes Dev 1998; 12(15): 2269-2277.
- Yamaguchi M, Tonou-Fujimori N, Komori A et al. Histone deacetylase 1 regulates retinal neurogenesis in zebrafish by suppressing Wnt and Notch signaling pathways. Development 2005; 132(13): 3027-3043.
- Wang J, Scully K, Zhu X et al. Opposing LSD1 complexes function in developmental gene activation and repression programmes. Nature 2007; 446(7138): 882.
- Miyazono K, Maeda S, Imamura T. BMP receptor signaling: transcriptional targets, regulation of signals, and signaling cross-talk. Cytokine & growth factor reviews 2005; 16(3): 251-263.
- Wu Z, Wu Y, Tian Y et al. Differential effects of miR"‘34c"‘3p and miR"‘34c"‘5p on the proliferation, apoptosis and invasion of glioma cells. Oncology letters 2013; 6(5): 1447-1452.
- Imayoshi I, Sakamoto M, Yamaguchi M, Mori K, Kageyama R. Essential roles of Notch signaling in maintenance of neural stem cells in developing and adult brains. Journal of Neuroscience 2010; 30(9): 3489-3498.
- Hatakeyama J, Kageyama R. Notch1 expression is spatiotemporally correlated with neurogenesis and negatively regulated by Notch1-independent Hes genes in the developing nervous system. Cereb Cortex 2006; 16(suppl_1): i132-i137.
- Zechner D, Fujita Y, Hülsken J et al. β-Catenin signals regulate cell growth and the balance between progenitor cell expansion and differentiation in the nervous system. Developmental biology 2003; 258(2): 406-418.
- Clevers H, Loh KM, Nusse R. An integral program for tissue renewal and regeneration: Wnt signaling and stem cell control. science 2014; 346(6205): 1248012.
- Komiya Y, Habas R. Wnt signal transduction pathways. Organogenesis 2008; 4(2): 68-75.
- Kim D, Hwang I, Muller F, Paik J. Functional regulation of FoxO1 in neural stem cell differentiation. Cell death and differentiation 2015; 22(12): 2034.
- Brandt MD, Maass A, Kempermann G, Storch A. Physical exercise increases Notch activity, proliferation and cell cycle exit of type"3 progenitor cells in adult hippocampal neurogenesis. Eur J Neurosci 2010; 32(8): 1256-1264.
- Ables JL, DeCarolis NA, Johnson MA et al. Notch1 is required for maintenance of the reservoir of adult hippocampal stem cells. J Neurosci 2010; 30(31): 10484-10492.
- Louis DN, Ohgaki H, Wiestler OD et al. The 2007 WHO classification of tumours of the central nervous system. Acta neuropathologica 2007; 114(2): 97-109.
- Wen PY, Kesari S. Malignant gliomas in adults. New Engl J Med 2008; 359(5): 492-507.
- Bralten LB, French PJ. Genetic alterations in glioma. Cancers 2011; 3(1): 1129-1140.
- Yoshida J. Molecular neurosurgery using gene therapy to treat malignant glioma. Nagoya journal of medical science 1996; 59: 97-106.
- Chen J, Li Y, Yu T-S et al. A restricted cell population propagates glioblastoma growth after chemotherapy. Nature 2012; 488(7412): 522.
- Patterson M, Gaeta X, Loo K et al. let-7 miRNAs can act through notch to regulate human gliogenesis. Stem cell reports 2014; 3(5): 758-773.
- Fan X, Mikolaenko I, Elhassan I et al. Notch1 and notch2 have opposite effects on embryonal brain tumor growth. Cancer Res 2004; 64(21): 7787-7793.
- Liau BB, Sievers C, Donohue LK et al. Adaptive chromatin remodeling drives glioblastoma stem cell plasticity and drug tolerance. Cell stem cell 2017; 20(2): 233-246. e237.
- Suzuki H, Aoki K, Chiba K et al. Mutational landscape and clonal architecture in grade II and III gliomas. Nat Genet 2015; 47(5): 458.
- Giachino C, Boulay J-L, Ivanek R et al. A tumor suppressor function for notch signaling in forebrain tumor subtypes. Cancer Cell 2015; 28(6): 730-742.
- Network CGAR. Comprehensive, integrative genomic analysis of diffuse lower-grade gliomas. New Engl J Med 2015; 372(26): 2481-2498.
- Stupp R, Mason WP, Van Den Bent MJ et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. New Engl J Med 2005; 352(10): 987-996.
- Purow BW, Haque RM, Noel MW et al. Expression of Notch-1 and its ligands, Delta-like-1 and Jagged-1, is critical for glioma cell survival and proliferation. Cancer Res 2005; 65(6): 2353-2363.
- Kanamori M, Kawaguchi T, Nigro JM et al. Contribution of Notch signaling activation to human glioblastoma multiforme. J Neurosurg 2007; 106(3): 417-427.
- Xu P, Zhang A, Jiang R et al. The different role of Notch1 and Notch2 in astrocytic gliomas. PloS one 2013; 8(1): e53654.
- Leins A, Riva P, Lindstedt R, Davidoff MS, Mehraein P, Weis S. Expression of tenascin"C in various human brain tumors and its relevance for survival in patients with astrocytoma. Cancer 2003; 98(11): 2430-2439.
- Sivasankaran B, Degen M, Ghaffari A et al. Tenascin-C is a novel RBPJκ-induced target gene for Notch signaling in gliomas. Cancer Res 2009; 69(2): 458-465.
- Bonev B, Pisco A, Papalopulu N. MicroRNA-9 reveals regional diversity of neural progenitors along the anterior-posterior axis. Developmental cell 2011; 20(1): 19-32.
- Bonev B, Stanley P, Papalopulu N. MicroRNA-9 modulates Hes1 ultradian oscillations by forming a double-negative feedback loop. Cell reports 2012; 2(1): 10-18.
- Roese-Koerner B, Stappert L, Berger T et al. Reciprocal Regulation between Bifunctional miR-9/9∗ and its Transcriptional Modulator Notch in Human Neural Stem Cell Self-Renewal and Differentiation. Stem cell reports 2016; 7(2): 207-219.
- Fineberg SK, Datta P, Stein CS, Davidson BL. MiR-34a represses Numbl in murine neural progenitor cells and antagonizes neuronal differentiation. PloS one 2012; 7(6): e38562.
- Wang H, Sun T, Hu J et al. miR-33a promotes glioma-initiating cell self-renewal via PKA and NOTCH pathways. The Journal of clinical investigation 2014; 124(10): 4489-4502.
- Zhao K, Wang Q, Wang Y et al. EGFR/c-myc axis regulates TGFβ/Hippo/Notch pathway via epigenetic silencing miR-524 in gliomas. Cancer letters 2017; 406: 12-21.
- Jin Z, Zhan T, Tao J et al. MicroRNA-34a induces transdifferentiation of glioma stem cells into vascular endothelial cells by targeting Notch pathway. Bioscience, biotechnology, and biochemistry 2017; 81(10): 1899-1907.
- Turchi L, Debruyne DN, Almairac F et al. Tumorigenic potential of miR"18A* in glioma initiating cells requires NOTCH"1 signaling. Stem Cells 2013; 31(7): 1252-1265.
- Huber RM, Rajski M, Sivasankaran B, Moncayo G, Hemmings BA, Merlo A. Deltex-1 activates mitotic signaling and proliferation and increases the clonogenic and invasive potential of U373 and LN18 glioblastoma cells and correlates with patient survival. PLoS One 2013; 8(2): e57793.
- Song H, Zhang Y, Liu N, Zhao S, Kong Y, Yuan L. miR-92a-3p exerts various effects in glioma and glioma stem-like cells specifically targeting CDH1/β-catenin and Notch-1/Akt signaling pathways. International journal of molecular sciences 2016; 17(11): 1799.
- Li Y, Guessous F, Zhang Y et al. MicroRNA-34a inhibits glioblastoma growth by targeting multiple oncogenes. Cancer Res 2009; 69(19): 7569-7576.
- Di Bari M, Bevilacqua V, De Jaco A et al. Mir-34a-5p mediates cross-talk between M2 muscarinic receptors and Notch-1/EGFR pathways in U87MG glioblastoma cells: implication in cell proliferation. International journal of molecular sciences 2018; 19(6): 1631.
- Chen L, Zhang R, Li P et al. P53-induced microRNA-107 inhibits proliferation of glioma cells and down-regulates the expression of CDK6 and Notch-2. Neuroscience letters 2013; 534: 327-332.
- Chen L, Zhang W, Yan W et al. The putative tumor suppressor miR-524–5p directly targets Jagged-1 and Hes-1 in glioma. Carcinogenesis 2012; 33(11): 2276-2282.
- Ruan J, Lou S, Dai Q, Mao D, Ji J, Sun X. Tumor suppressor miR-181c attenuates proliferation, invasion, and self-renewal abilities in glioblastoma. Neuroreport 2015; 26(2): 66-73.
- Wong H-KA, El Fatimy R, Onodera C et al. The Cancer Genome Atlas analysis predicts microRNA for targeting cancer growth and vascularization in glioblastoma. Mol Ther 2015; 23(7): 1234-1247.
- Kefas B, Comeau L, Floyd DH et al. The neuronal microRNA miR-326 acts in a feedback loop with notch and has therapeutic potential against brain tumors. Journal of Neuroscience 2009; 29(48): 15161-15168.
- Du Y, Li J, Xu T, Zhou D-D, Zhang L, Wang X. MicroRNA-145 induces apoptosis of glioma cells by targeting BNIP3 and Notch signaling. Oncotarget 2017; 8(37): 61510.
- Corada M, Orsenigo F, Bhat GP et al. Fine-Tuning of Sox17 and Canonical Wnt Coordinates the Permeability Properties of the Blood-Brain Barrier. Circul Res 2019; 124(4): 511-525.
- Kim J, Ahn SI, Kim Y. Nanotherapeutics engineered to cross the blood-brain barrier for advanced drug delivery to the central nervous system. Journal of Industrial and Engineering Chemistry 2019.
- Maués L, Alves G, Couto N et al. Flavonoids from the Amazon plant Brosimum acutifolium induce C6 glioma cell line apoptosis by disrupting mitochondrial membrane potential and reducing AKT phosphorylation. Biomed Pharmacother 2019; 113: 108728.
- Sansalone L, Veliz EA, Myrthil NG et al. Novel Curcumin Inspired Bis-Chalcone Promotes Endoplasmic Reticulum Stress and Glioblastoma Neurosphere Cell Death. Cancers 2019; 11(3): 357.
References
Dexter JS. The analysis of a case of continuous variation in Drosophila by a study of its linkage relations. The American Naturalist 1914; 48(576): 712-758.
Artavanis-Tsakonas S, Muskavitch M, Yedvobnick B. Molecular cloning of Notch, a locus affecting neurogenesis in Drosophila melanogaster. Proceedings of the National Academy of Sciences 1983; 80(7): 1977-1981.
Kopan R, Ilagan MXG. The canonical Notch signaling pathway: unfolding the activation mechanism. Cell 2009; 137(2): 216-233.
Henrique D, Schweisguth F. Mechanisms of Notch signaling: a simple logic deployed in time and space. Development 2019; 146(3): dev172148.
Basak O, Giachino C, Fiorini E, MacDonald HR, Taylor V. Neurogenic subventricular zone stem/progenitor cells are Notch1-dependent in their active but not quiescent state. J Neurosci 2012; 32(16): 5654-5666.
Gaiano N, Fishell G. The role of notch in promoting glial and neural stem cell fates. Annu Rev Neurosci 2002; 25(1): 471-490.
Bellec K, Gicquel I, Le Borgne R. The Clathrin adaptor AP-1 and the Rab-stabilizing chaperone Stratum act in two parallel pathways to control the activation of the Notch pathway in Drosophila. bioRxiv 2019: 645580.
Rebay I, Fleming RJ, Fehon RG, Cherbas L, Cherbas P, Artavanis-Tsakonas S. Specific EGF repeats of Notch mediate interactions with Delta and Serrate: implications for Notch as a multifunctional receptor. Cell 1991; 67(4): 687-699.
Andersson ER, Lendahl U. Therapeutic modulation of Notch signalling”are we there yet? Nature reviews Drug discovery 2014; 13(5): 357.
Ogawa M. A New Type of O-Glucose Modification by POGLUT2 and POGLUT3 Controls Notch Signaling and Trafficking. Trends in Glycoscience and Glycotechnology 2019; 31(179): E53-E54.
Mumm JS, Kopan R. Notch signaling: from the outside in. Dev Biol 2000; 228(2): 151-165.
Jarrett SM, Seegar TC, Andrews M et al. Molecular basis for feedback inhibition of Notch signaling by the Notch regulated ankyrin repeat protein NRARP. bioRxiv 2019: 645937.
Borggrefe T, Oswald F. The Notch signaling pathway: transcriptional regulation at Notch target genes. Cell Mol Life Sci 2009; 66(10): 1631-1646.
Guenther MG, Barak O, Lazar MA. The SMRT and N-CoR corepressors are activating cofactors for histone deacetylase 3. Mol Cell Biol 2001; 21(18): 6091-6101.
Okubo Y, Ohtake F, Igarashi K et al. Tuning of Neural Development Via Lateral Inhibition by Bi-Directional Notch-Delta Signaling. Available at SSRN 3351827 2019.
Ohtsuka T, Ishibashi M, Gradwohl G, Nakanishi S, Guillemot F, Kageyama R. Hes1 and Hes5 as notch effectors in mammalian neuronal differentiation. The EMBO journal 1999; 18(8): 2196-2207.
Bertrand N, Castro DS, Guillemot F. Proneural genes and the specification of neural cell types. Nature Reviews Neuroscience 2002; 3(7): 517.
Gao J, Van Meter M, Lopez SH et al. Therapeutic targeting of Notch signaling and immune checkpoint blockade in a spontaneous, genetically-heterogeneous mouse model of T-cell acute lymphoblastic leukemia. Disease models & mechanisms 2019: dmm. 040931.
Harris L, Guillemot F. HES1, two programs: promoting the quiescence and proliferation of adult neural stem cells. Genes & development 2019; 33(9-10): 479-481.
Ross SE, Greenberg ME, Stiles CD. Basic helix-loop-helix factors in cortical development. Neuron 2003; 39(1): 13-25.
Nandagopal N, Santat LA, Elowitz MB. Cis-activation in the Notch signaling pathway. eLife 2019; 8: e37880.
Castro DS, Skowronska-Krawczyk D, Armant O et al. Proneural bHLH and Brn proteins coregulate a neurogenic program through cooperative binding to a conserved DNA motif. Dev Cell 2006; 11(6): 831-844.
Shimojo H, Ohtsuka T, Kageyama R. Oscillations in notch signaling regulate maintenance of neural progenitors. Neuron 2008; 58(1): 52-64.
Imayoshi I, Isomura A, Harima Y et al. Oscillatory control of factors determining multipotency and fate in mouse neural progenitors. Science 2013; 342(6163): 1203-1208.
Haines N, Irvine KD. Glycosylation regulates Notch signalling. Nature reviews Molecular cell biology 2003; 4(10): 786.
Fortini ME. Notch signaling: the core pathway and its posttranslational regulation. Dev Cell 2009; 16(5): 633-647.
Li Y, Li L, Irvine KD, Baker NE. Notch activity in neural cells triggered by a mutant allele with altered glycosylation. Development 2003; 130(13): 2829-2840.
Song Y, Willer JR, Scherer PC et al. Neural and synaptic defects in slytherin, a zebrafish model for human congenital disorders of glycosylation. PLoS One 2010; 5(10): e13743.
Chi Z, Zhang J, Tokunaga A et al. Botch promotes neurogenesis by antagonizing Notch. Dev Cell 2012; 22(4): 707-720.
Couturier L, Vodovar N, Schweisguth F. Endocytosis by Numb breaks Notch symmetry at cytokinesis. Nat Cell Biol 2012; 14(2): 131.
Kressmann S, Campos C, Castanon I, Fürthauer M, González-Gaitán M. Directional Notch trafficking in Sara endosomes during asymmetric cell division in the spinal cord. Nat Cell Biol 2015; 17(3): 333.
Bekri A, Liao M, Drapeau P. Glycine regulates neural stem cell proliferation during development via Lnx1-dependent Notch signaling. Frontiers in molecular neuroscience 2019; 12.
Ohtsuka T, Kageyama R. Regulation of temporal properties of neural stem cells and transition timing of neurogenesis and gliogenesis during mammalian neocortical development. Paper presented at: Seminars in cell & developmental biology, 2019.
Shi Y, Zhao X, Hsieh J et al. MicroRNA regulation of neural stem cells and neurogenesis. J Neurosci 2010; 30(45): 14931-14936.
Zhao X, Ueba T, Christie BR et al. Mice lacking methyl-CpG binding protein 1 have deficits in adult neurogenesis and hippocampal function. Proceedings of the National Academy of Sciences 2003; 100(11): 6777-6782.
Hitoshi S, Ishino Y, Kumar A et al. Mammalian Gcm genes induce Hes5 expression by active DNA demethylation and induce neural stem cells. Nat Neurosci 2011; 14(8): 957.
Kim M, Park Y-K, Kang T-W et al. Dynamic changes in DNA methylation and hydroxymethylation when hES cells undergo differentiation toward a neuronal lineage. Hum Mol Genet 2013; 23(3): 657-667.
Zhang Z, Gao F, Kang X et al. Exploring the potential relationship between Notch pathway genes expression and their promoter methylation in mice hippocampal neurogenesis. Brain Res Bull 2015; 113: 8-16.
Kouzarides T. Chromatin modifications and their function. Cell 2007; 128(4): 693-705.
Oswald F, Täuber B, Dobner T et al. p300 acts as a transcriptional coactivator for mammalian Notch-1. Mol Cell Biol 2001; 21(22): 7761-7774.
Kurooka H, Honjo T. Functional interaction between the mouse notch1 intracellular region and histone acetyltransferases PCAF and GCN5. J Biol Chem 2000; 275(22): 17211-17220.
Kao H-Y, Ordentlich P, Koyano-Nakagawa N et al. A histone deacetylase corepressor complex regulates the Notch signal transduction pathway. Genes Dev 1998; 12(15): 2269-2277.
Yamaguchi M, Tonou-Fujimori N, Komori A et al. Histone deacetylase 1 regulates retinal neurogenesis in zebrafish by suppressing Wnt and Notch signaling pathways. Development 2005; 132(13): 3027-3043.
Wang J, Scully K, Zhu X et al. Opposing LSD1 complexes function in developmental gene activation and repression programmes. Nature 2007; 446(7138): 882.
Miyazono K, Maeda S, Imamura T. BMP receptor signaling: transcriptional targets, regulation of signals, and signaling cross-talk. Cytokine & growth factor reviews 2005; 16(3): 251-263.
Wu Z, Wu Y, Tian Y et al. Differential effects of miR"‘34c"‘3p and miR"‘34c"‘5p on the proliferation, apoptosis and invasion of glioma cells. Oncology letters 2013; 6(5): 1447-1452.
Imayoshi I, Sakamoto M, Yamaguchi M, Mori K, Kageyama R. Essential roles of Notch signaling in maintenance of neural stem cells in developing and adult brains. Journal of Neuroscience 2010; 30(9): 3489-3498.
Hatakeyama J, Kageyama R. Notch1 expression is spatiotemporally correlated with neurogenesis and negatively regulated by Notch1-independent Hes genes in the developing nervous system. Cereb Cortex 2006; 16(suppl_1): i132-i137.
Zechner D, Fujita Y, Hülsken J et al. β-Catenin signals regulate cell growth and the balance between progenitor cell expansion and differentiation in the nervous system. Developmental biology 2003; 258(2): 406-418.
Clevers H, Loh KM, Nusse R. An integral program for tissue renewal and regeneration: Wnt signaling and stem cell control. science 2014; 346(6205): 1248012.
Komiya Y, Habas R. Wnt signal transduction pathways. Organogenesis 2008; 4(2): 68-75.
Kim D, Hwang I, Muller F, Paik J. Functional regulation of FoxO1 in neural stem cell differentiation. Cell death and differentiation 2015; 22(12): 2034.
Brandt MD, Maass A, Kempermann G, Storch A. Physical exercise increases Notch activity, proliferation and cell cycle exit of type"3 progenitor cells in adult hippocampal neurogenesis. Eur J Neurosci 2010; 32(8): 1256-1264.
Ables JL, DeCarolis NA, Johnson MA et al. Notch1 is required for maintenance of the reservoir of adult hippocampal stem cells. J Neurosci 2010; 30(31): 10484-10492.
Louis DN, Ohgaki H, Wiestler OD et al. The 2007 WHO classification of tumours of the central nervous system. Acta neuropathologica 2007; 114(2): 97-109.
Wen PY, Kesari S. Malignant gliomas in adults. New Engl J Med 2008; 359(5): 492-507.
Bralten LB, French PJ. Genetic alterations in glioma. Cancers 2011; 3(1): 1129-1140.
Yoshida J. Molecular neurosurgery using gene therapy to treat malignant glioma. Nagoya journal of medical science 1996; 59: 97-106.
Chen J, Li Y, Yu T-S et al. A restricted cell population propagates glioblastoma growth after chemotherapy. Nature 2012; 488(7412): 522.
Patterson M, Gaeta X, Loo K et al. let-7 miRNAs can act through notch to regulate human gliogenesis. Stem cell reports 2014; 3(5): 758-773.
Fan X, Mikolaenko I, Elhassan I et al. Notch1 and notch2 have opposite effects on embryonal brain tumor growth. Cancer Res 2004; 64(21): 7787-7793.
Liau BB, Sievers C, Donohue LK et al. Adaptive chromatin remodeling drives glioblastoma stem cell plasticity and drug tolerance. Cell stem cell 2017; 20(2): 233-246. e237.
Suzuki H, Aoki K, Chiba K et al. Mutational landscape and clonal architecture in grade II and III gliomas. Nat Genet 2015; 47(5): 458.
Giachino C, Boulay J-L, Ivanek R et al. A tumor suppressor function for notch signaling in forebrain tumor subtypes. Cancer Cell 2015; 28(6): 730-742.
Network CGAR. Comprehensive, integrative genomic analysis of diffuse lower-grade gliomas. New Engl J Med 2015; 372(26): 2481-2498.
Stupp R, Mason WP, Van Den Bent MJ et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. New Engl J Med 2005; 352(10): 987-996.
Purow BW, Haque RM, Noel MW et al. Expression of Notch-1 and its ligands, Delta-like-1 and Jagged-1, is critical for glioma cell survival and proliferation. Cancer Res 2005; 65(6): 2353-2363.
Kanamori M, Kawaguchi T, Nigro JM et al. Contribution of Notch signaling activation to human glioblastoma multiforme. J Neurosurg 2007; 106(3): 417-427.
Xu P, Zhang A, Jiang R et al. The different role of Notch1 and Notch2 in astrocytic gliomas. PloS one 2013; 8(1): e53654.
Leins A, Riva P, Lindstedt R, Davidoff MS, Mehraein P, Weis S. Expression of tenascin"C in various human brain tumors and its relevance for survival in patients with astrocytoma. Cancer 2003; 98(11): 2430-2439.
Sivasankaran B, Degen M, Ghaffari A et al. Tenascin-C is a novel RBPJκ-induced target gene for Notch signaling in gliomas. Cancer Res 2009; 69(2): 458-465.
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