Acknowledgement
We would like to thank Sylvia Kanzler and Cornelia Mai for their excellent technical assistance. The work was supported in part by the DFG through the Collaborative Research Center 655 (SFB655) 'Cells into tissues: stem cell and progenitor commitment and interactions during tissue formation' (SFB 655, project A23) to A.S. and the Bundesministerium fur Bildung und Forschung (BMBF) through the NBL-3 program (to A.S.).
References
- Storch A, Paul G, Csete M, Boehm BO, Carvey PM, Kupsch A, Schwarz J. Long-term proliferation and dopaminergic differentiation of human mesencephalic neural precursor cells. Exp Neurol 2001;170:317-325 https://doi.org/10.1006/exnr.2001.7706
- Studer L, Csete M, Lee SH, Kabbani N, Walikonis J, Wold B, McKay R. Enhanced proliferation, survival, and dopaminergic differentiation of CNS precursors in lowered oxygen. J Neurosci 2000;20:7377-7383 https://doi.org/10.1523/JNEUROSCI.20-19-07377.2000
- Milosevic J, Maisel M, Wegner F, Leuchtenberger J, Wenger RH, Gerlach M, Storch A, Schwarz J. Lack of hypoxia-inducible factor-1 alpha impairs midbrain neural precursor cells involving vascular endothelial growth factor signaling. J Neurosci 2007;27:412-421 https://doi.org/10.1523/JNEUROSCI.2482-06.2007
- Silver I, Erecinska M. Oxygen and ion concentrations in normoxic and hypoxic brain cells. Adv Exp Med Biol 1998;454:7-16 https://doi.org/10.1007/978-1-4615-4863-8_2
- Semenza GL, Wang GL. A nuclear factor induced by hypoxia via de novo protein synthesis binds to the human erythropoietin gene enhancer at a site required for transcriptional activation. Mol Cell Biol 1992;12:5447-5454 https://doi.org/10.1128/MCB.12.12.5447
- Semenza GL. Hypoxia-inducible factor 1: master regulator of O2 homeostasis. Curr Opin Genet Dev 1998;8:588-594 https://doi.org/10.1016/S0959-437X(98)80016-6
- Tomita S, Ueno M, Sakamoto M, Kitahama Y, Ueki M, Maekawa N, Sakamoto H, Gassmann M, Kageyama R, Ueda N, Gonzalez FJ, Takahama Y. Defective brain development in mice lacking the Hif-1 alpha gene in neural cells. Mol Cell Biol 2003;23:6739-6749 https://doi.org/10.1128/MCB.23.19.6739-6749.2003
- Lange C, Turrero Garcia M, Decimo I, Bifari F, Eelen G, Quaegebeur A, Boon R, Zhao H, Boeckx B, Chang J, Wu C, Le Noble F, Lambrechts D, Dewerchin M, Kuo CJ, Huttner WB, Carmeliet P. Relief of hypoxia by angiogenesis promotes neural stem cell differentiation by targeting glycolysis. EMBO J 2016;35:924-941 https://doi.org/10.15252/embj.201592372
- Androutsellis-Theotokis A, Leker RR, Soldner F, Hoeppner DJ, Ravin R, Poser SW, Rueger MA, Bae SK, Kittappa R, McKay RD. Notch signalling regulates stem cell numbers in vitro and in vivo. Nature 2006;442:823-826 https://doi.org/10.1038/nature04940
- Yoon K, Gaiano N. Notch signaling in the mammalian central nervous system: insights from mouse mutants. Nat Neurosci 2005;8:709-715 https://doi.org/10.1038/nn1475
- Marinopoulou E, Biga V, Sabherwal N, Miller A, Desai J, Adamson AD, Papalopulu N. HES1 protein oscillations are necessary for neural stem cells to exit from quiescence. iScience 2021;24:103198
- Ochi S, Imaizumi Y, Shimojo H, Miyachi H, Kageyama R. Oscillatory expression of Hes1 regulates cell proliferation and neuronal differentiation in the embryonic brain. Development 2020;147:dev182204
- Ishibashi M, Moriyoshi K, Sasai Y, Shiota K, Nakanishi S, Kageyama R. Persistent expression of helix-loop-helix factor HES-1 prevents mammalian neural differentiation in the central nervous system. EMBO J 1994;13:1799-1805 https://doi.org/10.1002/j.1460-2075.1994.tb06448.x
- Louvi A, Artavanis-Tsakonas S. Notch signalling in vertebrate neural development. Nat Rev Neurosci 2006;7:93-102 https://doi.org/10.1038/nrn1847
- Gustafsson MV, Zheng X, Pereira T, Gradin K, Jin S, Lundkvist J, Ruas JL, Poellinger L, Lendahl U, Bondesson M. Hypoxia requires notch signaling to maintain the undifferentiated cell state. Dev Cell 2005;9:617-628 https://doi.org/10.1016/j.devcel.2005.09.010
- Pistollato F, Rampazzo E, Persano L, Abbadi S, Frasson C, Denaro L, D'Avella D, Panchision DM, Della Puppa A, Scienza R, Basso G. Interaction of hypoxia-inducible factor-1α and Notch signaling regulates medulloblastoma precursor proliferation and fate. Stem Cells 2010;28:1918-1929 https://doi.org/10.1002/stem.518
- Vecera J, Prochazkova J, Sumberova V, Panska V, Paculova H, Lanova MK, Masek J, Bohaciakova D, Andersson ER, Pachernik J. Hypoxia/Hif1α prevents premature neuronal differentiation of neural stem cells through the activation of Hes1. Stem Cell Res 2020;45:101770
- Braunschweig L, Lanto J, Meyer AK, Markert F, Storch A. Serial gene expression profiling of neural stem cells shows transcriptome switch by long-term physioxia from metabolic adaption to cell signaling profile. Stem Cells Int 2022;2022:6718640
- Braunschweig L, Meyer AK, Wagenfuhr L, Storch A. Oxygen regulates proliferation of neural stem cells through Wnt/β-catenin signalling. Mol Cell Neurosci 2015;67:84-92 https://doi.org/10.1016/j.mcn.2015.06.006
- Meyer AK, Jarosch A, Schurig K, Nuesslein I, Kissenkotter S, Storch A. Fetal mouse mesencephalic NPCs generate dopaminergic neurons from post-mitotic precursors and maintain long-term neural but not dopaminergic potential in vitro. Brain Res 2012;1474:8-18 https://doi.org/10.1016/j.brainres.2012.07.034
- Suzuki M, Yamamoto M, Sugimoto A, Nakamura S, Motoda R, Orita K. Delta-4 expression on a stromal cell line is augmented by interleukin-6 via STAT3 activation. Exp Hematol 2006;34:1143-1150 https://doi.org/10.1016/j.exphem.2006.04.027
- Asgrimsdottir ES, Arenas E. Midbrain dopaminergic neuron development at the single cell level: In vivo and in stem cells. Front Cell Dev Biol 2020;8:463
- Calegari F, Huttner WB. An inhibition of cyclin-dependent kinases that lengthens, but does not arrest, neuroepithelial cell cycle induces premature neurogenesis. J Cell Sci 2003;116(Pt 24):4947-4955 https://doi.org/10.1242/jcs.00825
- Hartmann C, Herling L, Hartmann A, Kockritz V, Fuellen G, Walter M, Hermann A. Systematic estimation of biological age of in vitro cell culture systems by an age-associated marker panel. Front Aging 2023;4:1129107
- Borghese L, Dolezalova D, Opitz T, Haupt S, Leinhaas A, Steinfarz B, Koch P, Edenhofer F, Hampl A, Brustle O. Inhibition of notch signaling in human embryonic stem cell-derived neural stem cells delays G1/S phase transition and accelerates neuronal differentiation in vitro and in vivo. Stem Cells 2010;28:955-964 https://doi.org/10.1002/stem.408
- Kaise T, Kageyama R. Hes1 oscillation frequency correlates with activation of neural stem cells. Gene Expr Patterns 2021;40:119170
- Blackwood CA. Jagged1 is essential for radial glial maintenance in the cortical proliferative zone. Neuroscience 2019;413:230-238 https://doi.org/10.1016/j.neuroscience.2019.05.062
- Kageyama R, Niwa Y, Shimojo H, Kobayashi T, Ohtsuka T. Ultradian oscillations in Notch signaling regulate dynamic biological events. Curr Top Dev Biol 2010;92:311-331 https://doi.org/10.1016/S0070-2153(10)92010-3
- Niola F, Zhao X, Singh D, Castano A, Sullivan R, Lauria M, Nam HS, Zhuang Y, Benezra R, Di Bernardo D, Iavarone A, Lasorella A. Id proteins synchronize stemness and anchorage to the niche of neural stem cells. Nat Cell Biol 2012;14:477-487 https://doi.org/10.1038/ncb2490
- Boareto M, Iber D, Taylor V. Differential interactions between Notch and ID factors control neurogenesis by modulating Hes factor autoregulation. Development. 2017;144:3465-3474 https://doi.org/10.1242/dev.152520
- Nelson BR, Hodge RD, Daza RA, Tripathi PP, Arnold SJ, Millen KJ, Hevner RF. Intermediate progenitors support migration of neural stem cells into dentate gyrus outer neurogenic niches. Elife 2020;9:e53777
- Chin MT, Maemura K, Fukumoto S, Jain MK, Layne MD, Watanabe M, Hsieh CM, Lee ME. Cardiovascular basic helix loop helix factor 1, a novel transcriptional repressor expressed preferentially in the developing and adult cardiovascular system. J Biol Chem 2000;275:6381-6387 https://doi.org/10.1074/jbc.275.9.6381
- Park DM, Jung J, Masjkur J, Makrogkikas S, Ebermann D, Saha S, Rogliano R, Paolillo N, Pacioni S, McKay RD, Poser S, Androutsellis-Theotokis A. Hes3 regulates cell number in cultures from glioblastoma multiforme with stem cell characteristics. Sci Rep 2013;3:1095
- Nishimura M, Isaka F, Ishibashi M, Tomita K, Tsuda H, Nakanishi S, Kageyama R. Structure, chromosomal locus, and promoter of mouse Hes2 gene, a homologue of Drosophila hairy and Enhancer of split. Genomics 1998;49:69-75 https://doi.org/10.1006/geno.1998.5213
- Lobov IB, Renard RA, Papadopoulos N, Gale NW, Thurston G, Yancopoulos GD, Wiegand SJ. Delta-like ligand 4 (Dll4) is induced by VEGF as a negative regulator of angiogenic sprouting. Proc Natl Acad Sci U S A 2007;104:3219-3224 https://doi.org/10.1073/pnas.0611206104
- Hitoshi S, Alexson T, Tropepe V, Donoviel D, Elia AJ, Nye JS, Conlon RA, Mak TW, Bernstein A, van der Kooy D. Notch pathway molecules are essential for the maintenance, but not the generation, of mammalian neural stem cells. Genes Dev 2002;16:846-858 https://doi.org/10.1101/gad.975202
- Pistollato F, Rampazzo E, Abbadi S, Della Puppa A, Scienza R, D'Avella D, Denaro L, Te Kronnie G, Panchision DM, Basso G. Molecular mechanisms of HIF-1alpha modulation induced by oxygen tension and BMP2 in glioblastoma derived cells. PLoS One 2009;4:e6206
- Gaiano N, Fishell G. The role of notch in promoting glial and neural stem cell fates. Annu Rev Neurosci 2002;25:471-490 https://doi.org/10.1146/annurev.neuro.25.030702.130823
- Kaufmann MR, Barth S, Konietzko U, Wu B, Egger S, Kunze R, Marti HH, Hick M, Muller U, Camenisch G, Wenger RH. Dysregulation of hypoxia-inducible factor by presenilin/γ-secretase loss-of-function mutations. J Neurosci 2013;33:1915-1926 https://doi.org/10.1523/JNEUROSCI.3402-12.2013
- Mukherjee T, Kim WS, Mandal L, Banerjee U. Interaction between Notch and Hif-alpha in development and survival of Drosophila blood cells. Science 2011;332:1210-1213 https://doi.org/10.1126/science.1199643
- Takahashi T, Nowakowski RS, Caviness VS Jr. The cell cycle of the pseudostratified ventricular epithelium of the embryonic murine cerebral wall. J Neurosci 1995;15:6046-6057 https://doi.org/10.1523/JNEUROSCI.15-09-06046.1995
- Semenza GL. Hypoxia. Cross talk between oxygen sensing and the cell cycle machinery. Am J Physiol Cell Physiol 2011;301:C550-C552 https://doi.org/10.1152/ajpcell.00176.2011
- Bertoli C, Skotheim JM, de Bruin RA. Control of cell cycle transcription during G1 and S phases. Nat Rev Mol Cell Biol 2013;14:518-528 https://doi.org/10.1038/nrm3629
- Lopez-Otin C, Blasco MA, Partridge L, Serrano M, Kroemer G. The hallmarks of aging. Cell 2013;153:1194-1217 https://doi.org/10.1016/j.cell.2013.05.039