Wang, Wei
[UCL]
Jossin, Yves
[UCL]
Chai, Guoliang
[UCL]
Lien, Wen-Hui
[UCL]
Tissir, Fadel
[UCL]
Goffinet, André
[UCL]
Sequential generation of neurons and glial cells during development is critical for the wiring and function of the cerebral cortex. This process requires accurate coordination of neural progenitor cell (NPC) fate decisions, by NPC-autonomous mechanisms as well as by negative feedback from neurons. Here, we show that neurogenesis is protracted and gliogenesis decreased in mice with mutations of genes Celsr3 and Fzd3. This phenotype is not due to gene inactivation in progenitors, but rather in immature cortical neurons. Mutant neurons are unable to upregulate expression of Jag1 in response to cortical Wnt7, resulting in blunted activation of Notch signalling in NPC. Thus, Celsr3 and Fzd3 enable immature neurons to respond to Wnt7, upregulate Jag1 and thereby facilitate feedback signals that tune the timing of NPC fate decisions via Notch activation.
- Kriegstein Arnold, Alvarez-Buylla Arturo, The Glial Nature of Embryonic and Adult Neural Stem Cells, 10.1146/annurev.neuro.051508.135600
- Noctor S. C., J. Neurosci., 22, 3161 (2002)
- Florio M., Huttner W. B., Neural progenitors, neurogenesis and the evolution of the neocortex, 10.1242/dev.090571
- Paridaen J. T., Huttner W. B., Neurogenesis during development of the vertebrate central nervous system, 10.1002/embr.201438447
- Rakic Pasko, Ayoub Albert E., Breunig Joshua J., Dominguez Martin H., Decision by division: making cortical maps, 10.1016/j.tins.2009.01.007
- Rowitch David H., Kriegstein Arnold R., Developmental genetics of vertebrate glial–cell specification, 10.1038/nature09611
- Gaspard Nicolas, Bouschet Tristan, Hourez Raphael, Dimidschstein Jordane, Naeije Gilles, van den Ameele Jelle, Espuny-Camacho Ira, Herpoel Adèle, Passante Lara, Schiffmann Serge N., Gaillard Afsaneh, Vanderhaeghen Pierre, An intrinsic mechanism of corticogenesis from embryonic stem cells, 10.1038/nature07287
- Shen Qin, Wang Yue, Dimos John T, Fasano Christopher A, Phoenix Timothy N, Lemischka Ihor R, Ivanova Natalia B, Stifani Stefano, Morrisey Edward E, Temple Sally, The timing of cortical neurogenesis is encoded within lineages of individual progenitor cells, 10.1038/nn1694
- Eiraku Mototsugu, Watanabe Kiichi, Matsuo-Takasaki Mami, Kawada Masako, Yonemura Shigenobu, Matsumura Michiru, Wataya Takafumi, Nishiyama Ayaka, Muguruma Keiko, Sasai Yoshiki, Self-Organized Formation of Polarized Cortical Tissues from ESCs and Its Active Manipulation by Extrinsic Signals, 10.1016/j.stem.2008.09.002
- Lehtinen Maria K., Zappaterra Mauro W., Chen Xi, Yang Yawei J., Hill Anthony D., Lun Melody, Maynard Thomas, Gonzalez Dilenny, Kim Seonhee, Ye Ping, D'Ercole A. Joseph, Wong Eric T., LaMantia Anthony S., Walsh Christopher A., The Cerebrospinal Fluid Provides a Proliferative Niche for Neural Progenitor Cells, 10.1016/j.neuron.2011.01.023
- Namihira Masakazu, Kohyama Jun, Semi Katsunori, Sanosaka Tsukasa, Deneen Benjamin, Taga Tetsuya, Nakashima Kinichi, Committed Neuronal Precursors Confer Astrocytic Potential on Residual Neural Precursor Cells, 10.1016/j.devcel.2008.12.014
- Parthasarathy S., Srivatsa S., Nityanandam A., Tarabykin V., Ntf3 acts downstream of Sip1 in cortical postmitotic neurons to control progenitor cell fate through feedback signaling, 10.1242/dev.114173
- Miller Freda D., Gauthier Andrée S., Timing Is Everything: Making Neurons versus Glia in the Developing Cortex, 10.1016/j.neuron.2007.04.019
- Seuntjens Eve, Nityanandam Anjana, Miquelajauregui Amaya, Debruyn Joke, Stryjewska Agata, Goebbels Sandra, Nave Klaus-Armin, Huylebroeck Danny, Tarabykin Victor, Sip1 regulates sequential fate decisions by feedback signaling from postmitotic neurons to progenitors, 10.1038/nn.2409
- Nelson B. R., Hodge R. D., Bedogni F., Hevner R. F., Dynamic Interactions between Intermediate Neurogenic Progenitors and Radial Glia in Embryonic Mouse Neocortex: Potential Role in Dll1-Notch Signaling, 10.1523/jneurosci.0791-13.2013
- Barnabé-Heider Fanie, Wasylnka Julie A., Fernandes Karl J.L., Porsche Christian, Sendtner Michael, Kaplan David R., Miller Freda D., Evidence that Embryonic Neurons Regulate the Onset of Cortical Gliogenesis via Cardiotrophin-1, 10.1016/j.neuron.2005.08.037
- Bonni A., Regulation of Gliogenesis in the Central Nervous System by the JAK-STAT Signaling Pathway, 10.1126/science.278.5337.477
- Uemura Atsumi, Takizawa Takumi, Ochiai Wataru, Yanagisawa Makoto, Nakashima Kinichi, Taga Tetsuya, CARDIOTROPHIN-LIKE CYTOKINE INDUCES ASTROCYTE DIFFERENTIATION OF FETAL NEUROEPITHELIAL CELLS VIA ACTIVATION OF STAT3, 10.1006/cyto.2002.1006
- Li Xiaoyan, Newbern Jason M., Wu Yaohong, Morgan-Smith Meghan, Zhong Jian, Charron Jean, Snider William D., MEK Is a Key Regulator of Gliogenesis in the Developing Brain, 10.1016/j.neuron.2012.08.031
- Nakashima K., Takizawa T., Ochiai W., Yanagisawa M., Hisatsune T., Nakafuku M., Miyazono K., Kishimoto T., Kageyama R., Taga T., BMP2-mediated alteration in the developmental pathway of fetal mouse brain cells from neurogenesis to astrocytogenesis, 10.1073/pnas.101109698
- Toma K., Kumamoto T., Hanashima C., The Timing of Upper-Layer Neurogenesis Is Conferred by Sequential Derepression and Negative Feedback from Deep-Layer Neurons, 10.1523/jneurosci.2334-14.2014
- Pierfelice Tarran, Alberi Lavinia, Gaiano Nicholas, Notch in the Vertebrate Nervous System: An Old Dog with New Tricks, 10.1016/j.neuron.2011.02.031
- Louvi Angeliki, Artavanis-Tsakonas Spyros, Notch signalling in vertebrate neural development, 10.1038/nrn1847
- 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, 10.1523/jneurosci.4987-09.2010
- Mizutani K.-i., Progenitors resume generating neurons after temporary inhibition of neurogenesis by Notch activation in the mammalian cerebral cortex, 10.1242/dev.01693
- Park S., Lee C., Sabharwal P., Zhang M., Meyers C. L. F., Sockanathan S., GDE2 Promotes Neurogenesis by Glycosylphosphatidylinositol-Anchor Cleavage of RECK, 10.1126/science.1231921
- Chai Guoliang, Goffinet Andre M., Tissir Fadel, Celsr3 and Fzd3 in axon guidance, 10.1016/j.biocel.2015.03.013
- Yang Yingzi, Mlodzik Marek, Wnt-Frizzled/Planar Cell Polarity Signaling: Cellular Orientation by Facing the Wind (Wnt), 10.1146/annurev-cellbio-100814-125315
- Tissir Fadel, Goffinet André M., Shaping the nervous system: role of the core planar cell polarity genes, 10.1038/nrn3525
- Tissir Fadel, Goffinet André M., Expression of planar cell polarity genes during development of the mouse CNS, 10.1111/j.1460-9568.2006.04596.x
- Goebbels Sandra, Bormuth Ingo, Bode Ulli, Hermanson Ola, Schwab Markus H., Nave Klaus-Armin, Genetic targeting of principal neurons in neocortex and hippocampus of NEX-Cre mice, 10.1002/dvg.20256
- Tissir Fadel, Bar Isabelle, Jossin Yves, Goffinet Andre M, Protocadherin Celsr3 is crucial in axonal tract development, 10.1038/nn1428
- Wang Y., J. Neurosci., 22, 8563 (2002)
- Dehay C., J. Neurosci., 21, 201 (2001)
- Zhou L., Bar I., Achouri Y., Campbell K., De Backer O., Hebert J. M., Jones K., Kessaris N., de Rouvroit C. L., O'Leary D., Richardson W. D., Goffinet A. M., Tissir F., Early Forebrain Wiring: Genetic Dissection Using Conditional Celsr3 Mutant Mice, 10.1126/science.1155244
- Chenn A., Regulation of Cerebral Cortical Size by Control of Cell Cycle Exit in Neural Precursors, 10.1126/science.1074192
- Martynoga Ben, Morrison Harris, Price David J., Mason John O., Foxg1 is required for specification of ventral telencephalon and region-specific regulation of dorsal telencephalic precursor proliferation and apoptosis, 10.1016/j.ydbio.2005.04.005
- Xue Y., Gao X., Lindsell C. E., Norton C. R., Chang B., Hicks C., Gendron-Maguire M., Rand E. B., Weinmaster G., Gridley T., Embryonic Lethality and Vascular Defects in Mice Lacking the Notch Ligand Jagged1, 10.1093/hmg/8.5.723
- Rouaux Caroline, Arlotta Paola, Direct lineage reprogramming of post-mitotic callosal neurons into corticofugal neurons in vivo, 10.1038/ncb2660
- Estrach S., Ambler C. A., Lo Celso C. L., Hozumi K., Watt F. M., Jagged 1 is a -catenin target gene required for ectopic hair follicle formation in adult epidermis, 10.1242/dev.02644
- Yamanaka H., JNK functions in the non-canonical Wnt pathway to regulate convergent extension movements in vertebrates, 10.1093/embo-reports/kvf008
- Kawaguchi D., Yoshimatsu T., Hozumi K., Gotoh Y., Selection of differentiating cells by different levels of delta-like 1 among neural precursor cells in the developing mouse telencephalon, 10.1242/dev.024570
- Curtin John A., Quint Elizabeth, Tsipouri Vicky, Arkell Ruth M., Cattanach Bruce, Copp Andrew J., Henderson Deborah J., Spurr Nigel, Stanier Philip, Fisher Elizabeth M., Nolan Patrick M., Steel Karen P., Brown Steve D.M., Gray Ian C., Murdoch Jennifer N., Mutation of Celsr1 Disrupts Planar Polarity of Inner Ear Hair Cells and Causes Severe Neural Tube Defects in the Mouse, 10.1016/s0960-9822(03)00374-9
- Qu W.-M., Xu X.-H., Yan M.-M., Wang Y.-Q., Urade Y., Huang Z.-L., Essential Role of Dopamine D2 Receptor in the Maintenance of Wakefulness, But Not in Homeostatic Regulation of Sleep, in Mice, 10.1523/jneurosci.4936-09.2010
- Wang Y., The Role of Frizzled3 and Frizzled6 in Neural Tube Closure and in the Planar Polarity of Inner-Ear Sensory Hair Cells, 10.1523/jneurosci.4698-05.2005
- Chai Guoliang, Zhou Libing, Manto Mario, Helmbacher Françoise, Clotman Frédéric, Goffinet André M, Tissir Fadel, Celsr3 is required in motor neurons to steer their axons in the hindlimb, 10.1038/nn.3784
- Hua Zhong L, Smallwood Philip M, Nathans Jeremy, Frizzled3 controls axonal development in distinct populations of cranial and spinal motor neurons, 10.7554/elife.01482
- Mandai Kenji, Reimert Dorothy V., Ginty David D., Linx Mediates Interaxonal Interactions and Formation of the Internal Capsule, 10.1016/j.neuron.2014.05.020
- Qu Y., Huang Y., Feng J., Alvarez-Bolado G., Grove E. A., Yang Y., Tissir F., Zhou L., Goffinet A. M., Genetic evidence that Celsr3 and Celsr2, together with Fzd3, regulate forebrain wiring in a Vangl-independent manner, 10.1073/pnas.1402105111
- Wu Jun, Roman Angel-Carlos, Carvajal-Gonzalez Jose Maria, Mlodzik Marek, Wg and Wnt4 provide long-range directional input to planar cell polarity orientation in Drosophila, 10.1038/ncb2806
- Lyuksyutova A. I., Anterior-Posterior Guidance of Commissural Axons by Wnt-Frizzled Signaling, 10.1126/science.1089610
- Sokol Sergei Y., Spatial and temporal aspects of Wnt signaling and planar cell polarity during vertebrate embryonic development, 10.1016/j.semcdb.2015.05.002
- Delaunay Delphine, Cortay Véronique, Patti Dorothée, Knoblauch Kenneth, Dehay Colette, Mitotic Spindle Asymmetry: A Wnt/PCP-Regulated Mechanism Generating Asymmetrical Division in Cortical Precursors, 10.1016/j.celrep.2013.12.026
- Cooper Michael T. D., Bray Sarah J., Frizzled regulation of Notch signalling polarizes cell fate in the Drosophila eye, 10.1038/17395
- Fanto Manolis, Mlodzik Marek, Asymmetric Notch activation specifies photoreceptors R3 and R4 and planar polarity in the Drosophila eye, 10.1038/17389
- Tomlinson A., Development, 126, 5725 (1999)
- Wehrli M., Development, 125, 1421 (1998)
- Koutelou Evangelia, Sato Shigeo, Tomomori-Sato Chieri, Florens Laurence, Swanson Selene K., Washburn Michael P., Kokkinaki Maria, Conaway Ronald C., Conaway Joan W., Moschonas Nicholas K., Neuralized-like 1 (Neurl1) Targeted to the Plasma Membrane byN-Myristoylation Regulates the Notch Ligand Jagged1, 10.1074/jbc.m706974200
- Jossin Yves, Cooper Jonathan A, Reelin, Rap1 and N-cadherin orient the migration of multipolar neurons in the developing neocortex, 10.1038/nn.2816
Bibliographic reference |
Wang, Wei ; Jossin, Yves ; Chai, Guoliang ; Lien, Wen-Hui ; Tissir, Fadel ; et. al. Feedback regulation of apical progenitor fate by immature neurons through Wnt7-Celsr3-Fzd3 signalling.. In: Nature Communications, Vol. 7, p. 10936 (2016) |
Permanent URL |
http://hdl.handle.net/2078.1/172409 |