Principles of progenitor temporal patterning in the developing invertebrate and vertebrate nervous system

[en] During the development of the central nervous system, progenitors successively generate distinct types of neurons which assemble into the circuits that underlie our ability to interact with the environment. Spatial and temporal patterning mechanisms are partially evolutionarily conserved processes that allow generation of neuronal diversity from a limited set of progenitors. Here, we review examples of temporal patterning in neuronal progenitors in the Drosophila ventral nerve cord and in the mammalian cerebral cortex. We discuss cell-autonomous mechanisms and environmental influences on the temporal transitions of neuronal progenitors. Identifying the principles controlling the temporal specification of progenitors across species, as highlighted here, may help understand the evolutionary constraints over brain circuit design and function. © 2019 Elsevier Ltd

Disciplines :

Genetics & genetic processes

Author, co-author :

Oberst, Polina ^✱; Department of Basic Neurosciences, University of Geneva, Switzerland

Agirman, Gulistan ^✱; Université de Liège - ULiège > Neurosciences-Molecular Regulation of Neurogenesis

Jabaudon, Denis ^✱; Department of Basic Neurosciences, University of Geneva, Switzerland, Department of Neurology, Geneva University Hospital, Geneva, Switzerland

^✱ These authors have contributed equally to this work.

Language :

English

Title :

Principles of progenitor temporal patterning in the developing invertebrate and vertebrate nervous system

Publication date :

2019

Journal title :

Current Opinion in Neurobiology

ISSN :

0959-4388

Publisher :

Elsevier Ltd

Volume :

Pages :

185-193

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 23 August 2019

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565 (3 by ULiège)

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Bibliography

Jeong, H., Tiwari, V.K., Exploring the complexity of cortical development using single-cell transcriptomics. Front Neurosci, 12, 2018, 31.
Kohwi, M., Doe, C.Q., Temporal fate specification and neural progenitor competence during development. Nat Rev Neurosci 14 (2013), 823–838.
Guillemot, F., Spatial and temporal specification of neural fates by transcription factor codes. Development 134 (2007), 3771–3780.
Dastjerdi, F.V., Consalez, G.G., Hawkes, R., Pattern formation during development of the embryonic cerebellum. Front Neuroanat, 6, 2012, 10.
Hu, J.S., Vogt, D., Sandberg, M., Rubenstein, J.L., Cortical interneuron development: a tale of time and space. Development 144 (2017), 3867–3878.
Urbach, R., Technau, G.M., Neuroblast formation and patterning during early brain development in Drosophila. Bioessays 26 (2004), 739–751.
Borello, U., Pierani, A., Patterning the cerebral cortex: traveling with morphogens. Curr Opin Genet Dev 20 (2010), 408–415.
Azzarelli, R., Hardwick, L.J.A., Philpott, A., Emergence of neuronal diversity from patterning of telencephalic progenitors. Wiley Interdiscip Rev Dev Biol 4 (2015), 197–214.
Holguera, I., Desplan, C., Neuronal specification in space and time. Science 362 (2018), 176–180.
Doe, C.Q., Temporal patterning in the Drosophila CNS. Annu Rev Cell Dev Biol 33 (2017), 219–240.
Li, X., Chen, Z., Desplan, C., Temporal patterning of neural progenitors in Drosophila. Curr Top Dev Biol 105 (2013), 69–96.
Miyares, R.L., Lee, T., Temporal control of Drosophila central nervous system development. Curr Opin Neurobiol 56 (2018), 24–32.
Skeath, J.B., Thor, S., Genetic control of Drosophila nerve cord development. Curr Opin Neurobiol 13 (2003), 8–15.
Truman, J.W., Bate, M., Spatial and temporal patterns of neurogenesis in the central nervous system of Drosophila melanogaster. Dev Biol 125 (1988), 145–157.
Prokop, A., Technau, G.M., The origin of postembryonic neuroblasts in the ventral nerve cord of Drosophila melanogaster. Development 111 (1991), 79–88.
Brody, T., Odenwald, W.F., Programmed transformations in neuroblast gene expression during Drosophila CNS lineage development. Dev Biol 226 (2000), 34–44.
Isshiki, T., Pearson, B., Holbrook, S., Doe, C.Q., Drosophila neuroblasts sequentially express transcription factors which specify the temporal identity of their neuronal progeny. Cell 106 (2001), 511–521.
Kambadur, R., Koizumi, K., Stivers, C., Nagle, J., Poole, S.J., Odenwald, W.F., Regulation of POU genes by castor and hunchback establishes layered compartments in the Drosophila CNS. Genes Dev 12 (1998), 246–260.
Jabaudon, D., Fate and freedom in developing neocortical circuits. Nat Commun, 8, 2017, 16042.
Greig, L.C., Woodworth, M.B., Galazo, M.J., Padmanabhan, H., Macklis, J.D., Molecular logic of neocortical projection neuron specification, development and diversity. Nat Rev Neurosci 14 (2013), 755–769.
Elliott, J., Jolicoeur, C., Ramamurthy, V., Cayouette, M., Ikaros confers early temporal competence to mouse retinal progenitor cells. Neuron 60 (2008), 26–39.
Alsio, J.M., Tarchini, B., Cayouette, M., Livesey, F.J., Ikaros promotes early-born neuronal fates in the cerebral cortex. Proc Natl Acad Sci U S A 110 (2013), E716–E725.
Mattar, P., Ericson, J., Blackshaw, S., Cayouette, M., A conserved regulatory logic controls temporal identity in mouse neural progenitors. Neuron 85 (2015), 497–504.
Bello, B.C., Izergina, N., Caussinus, E., Reichert, H., Amplification of neural stem cell proliferation by intermediate progenitor cells in Drosophila brain development. Neural Dev, 3, 2008, 5.
Boone, J.Q., Doe, C.Q., Identification of Drosophila type II neuroblast lineages containing transit amplifying ganglion mother cells. Dev Neurobiol 68 (2008), 1185–1195.
Bayraktar, O.A., Doe, C.Q., Combinatorial temporal patterning in progenitors expands neural diversity. Nature 498 (2013), 449–455.
Grosskortenhaus, R., Pearson, B.J., Marusich, A., Doe, C.Q., Regulation of temporal identity transitions in Drosophila neuroblasts. Dev Cell 8 (2005), 193–202.
Kanai, M.I., Okabe, M., Hiromi, Y., Seven-up controls switching of transcription factors that specify temporal identities of Drosophila neuroblasts. Dev Cell 8 (2005), 203–213.
Mettler, U., Vogler, G., Urban, J., Timing of identity: spatiotemporal regulation of hunchback in neuroblast lineages of Drosophila by Seven-up and prospero. Development 133 (2006), 429–437.
Kohwi, M., Hiebert, L.S., Doe, C.Q., The pipsqueak-domain proteins Distal antenna and Distal antenna-related restrict Hunchback neuroblast expression and early-born neuronal identity. Development 138 (2011), 1727–1735.
Naka, H., Nakamura, S., Shimazaki, T., Okano, H., Requirement for COUP-TFI and II in the temporal specification of neural stem cells in CNS development. Nat Neurosci 11 (2008), 1014–1023.
Okamoto, M., Miyata, T., Konno, D., Ueda, H.R., Kasukawa, T., Hashimoto, M., Matsuzaki, F., Kawaguchi, A., Cell-cycle-independent transitions in temporal identity of mammalian neural progenitor cells. Nat Commun, 7, 2016, 11349 This study identified subsets of temporally regulated genes in cortical progenitors and showed that temporal transitions occur even in cell cycle arrested progenitors. It also showed that temporal transitions of in vitro cultured progenitors strongly depend on culture conditions, highlighting the importance of extrinsic feedback cues to temporal progression of progenitors.
Syed, M.H., Mark, B., Doe, C.Q., Steroid hormone induction of temporal gene expression in Drosophila brain neuroblasts generates neuronal and glial diversity. eLife, 6, 2017 This study identified novel tTFs in larval central brain neuroblasts and was the first to show that extrinsic signaling via ecdysone receptors is necessary for a major transition from early to late neuroblast temporal state.
Syed, M.H., Mark, B., Doe, C.Q., Playing well with others: extrinsic cues regulate neural progenitor temporal identity to generate neuronal diversity. Trends Genet 33 (2017), 933–942.
Pearson, B.J., Doe, C.Q., Regulation of neuroblast competence in Drosophila. Nature 425 (2003), 624–628.
Cleary, M.D., Doe, C.Q., Regulation of neuroblast competence: multiple temporal identity factors specify distinct neuronal fates within a single early competence window. Genes Dev 20 (2006), 429–434.
Kohwi, M., Lupton, J.R., Lai, S.-L., Miller, M.R., Doe, C.Q., Developmentally regulated subnuclear genome reorganization restricts neural progenitor competence in Drosophila. Cell 152 (2013), 97–108.
Touma, J.J., Weckerle, F.F., Cleary, M.D., Drosophila polycomb complexes restrict neuroblast competence to generate motoneurons. Development 139 (2012), 657–666.
Pereira, J.D., Sansom, S.N., Smith, J., Dobenecker, M.-W., Tarakhovsky, A., Livesey, F.J., Ezh2, the histone methyltransferase of PRC2, regulates the balance between self-renewal and differentiation in the cerebral cortex. Proc Natl Acad Sci U S A 107 (2010), 15957–15962.
Morimoto-Suzki, N., Hirabayashi, Y., Tyssowski, K., Shinga, J., Vidal, M., Koseki, H., Gotoh, Y., The polycomb component Ring1B regulates the timed termination of subcerebral projection neuron production during mouse neocortical development. Development 141 (2014), 4343–4353.
Farnsworth, D.R., Bayraktar, O.A., Doe, C.Q., Aging neural progenitors lose competence to respond to mitogenic notch signaling. Curr Biol 25 (2015), 3058–3068.
Gao, P., Postiglione, M.P., Krieger, T.G., Hernandez, L., Wang, C., Han, Z., Streicher, C., Papusheva, E., Insolera, R., Chugh, K., et al. Deterministic progenitor behavior and unitary production of neurons in the neocortex. Cell 159 (2014), 775–788.
Guo, C., Eckler, M.J., McKenna, W.L., McKinsey, G.L., Rubenstein, J.L.R., Chen, B., Fezf2 expression identifies a multipotent progenitor for neocortical projection neurons, astrocytes, and oligodendrocytes. Neuron 80 (2013), 1167–1174.
Franco, S.J., Gil-Sanz, C., Martinez-Garay, I., Espinosa, A., Harkins-Perry, S.R., Ramos, C., Müller, U., Fate-restricted neural progenitors in the mammalian cerebral cortex. Science 337 (2012), 746–749.
Yuzwa, S.A., Borrett, M.J., Innes, B.T., Voronova, A., Ketela, T., Kaplan, D.R., Bader, G.D., Miller, F.D., Developmental emergence of adult neural stem cells as revealed by single-cell transcriptional profiling. Cell Rep 21 (2017), 3970–3986.
Telley, L., Agirman, G., Prados, J., Fievre, S., Oberst, P., Vitali, I., Nguyen, L., Dayer, A., Jabaudon, D., Single-cell transcriptional dynamics and origins of neuronal diversity in the developing mouse neocortex. bioRxiv, 2018, 10.1101/409458.
Gaspard, N., Bouschet, T., Hourez, R., Dimidschstein, J., Naeije, G., van den Ameele, J., Espuny-Camacho, I., Herpoel, A., Passante, L., Schiffmann, S.N., et al. An intrinsic mechanism of corticogenesis from embryonic stem cells. Nature 455 (2008), 351–357.
Espuny-Camacho, I., Michelsen, K.A., Gall, D., Linaro, D., Hasche, A., Bonnefont, J., Bali, C., Orduz, D., Bilheu, A., Herpoel, A., et al. Pyramidal neurons derived from human pluripotent stem cells integrate efficiently into mouse brain circuits in vivo. Neuron 77 (2013), 440–456.
Camp, J.G., Badsha, F., Florio, M., Kanton, S., Gerber, T., Wilsch-Bräuninger, M., Lewitus, E., Sykes, A., Hevers, W., Lancaster, M., et al. Human cerebral organoids recapitulate gene expression programs of fetal neocortex development. Proc Natl Acad Sci U S A 112 (2015), 15672–15677.
McConnell, S.K., Fates of visual cortical neurons in the ferret after isochronic and heterochronic transplantation. J Neurosci 3 (1988), 945–974.
Mcconnell, S.K., Kaznowski, C.E., Cell cycle dependence of laminar determination in developing neocortex. Science 254 (1991), 282–285.
Frantz, G.D., McConnell, S.K., Restriction of late cerebral cortical progenitors to an upper-layer fate. Neuron 17 (1996), 55–61.
Oberst, P., Fievre, S., Baumann, N., Concetti, C., Jabaudon, D., Apical progenitors remain multipotent throughout cortical neurogenesis. bioRxiv, 2018, 10.1101/478891.
Hanashima, C., Li, S.C., Shen, L., Lai, E., Fishell, G., Foxg1 suppresses early cortical cell fate. Science 303 (2004), 56–59.
Fame, R.M., MacDonald, J.L., Macklis, J.D., Development, specification, and diversity of callosal projection neurons. Trends Neurosci 34 (2011), 41–50.
McKenna, W.L., Betancourt, J., Larkin, K.A., Abrams, B., Guo, C., Rubenstein, J.L.R., Chen, B., Tbr1 and Fezf2 regulate alternate corticofugal neuronal identities during neocortical development. J Neurosci 31 (2011), 549–564.
Chen, B., Wang, S.S., Hattox, A.M., Rayburn, H., Nelson, S.B., McConnell, S.K., The Fezf2-Ctip2 genetic pathway regulates the fate choice of subcortical projection neurons in the developing cerebral cortex. Proc Natl Acad Sci U S A 105 (2008), 11382–11387.
Han, W., Kwan, K.Y., Shim, S., Lam, M.M.S., Shin, Y., Xu, X., Zhu, Y., Li, M., Sestan, N., TBR1 directly represses Fezf2 to control the laminar origin and development of the corticospinal tract. Proc Natl Acad Sci U S A 108 (2011), 3041–3046.
Srinivasan, K., Leone, D.P., Bateson, R.K., Dobreva, G., Kohwi, Y., Kohwi-Shigematsu, T., Grosschedl, R., McConnell, S.K., A network of genetic repression and derepression specifies projection fates in the developing neocortex. Proc Natl Acad Sci U S A 109 (2012), 19071–19078.
Zahr, S.K., Yang, G., Kazan, H., Borrett, M.J., Yuzwa, S.A., Voronova, A., Kaplan, D.R., Miller, F.D., A translational repression complex in developing mammalian neural stem cells that regulates neuronal specification. Neuron 97 (2018), 520–537.e6 This study showed that apical progenitors are transcriptionally bimodal as they express identifiers of both deep and superficial layer neurons at the mRNA level, but the translation of the inappropriate marker is inhibited by a translational repressive complex.
Azim, E., Shnider, S.J., Cederquist, G.Y., Sohur, U.S., Macklis, J.D., Lmo4 and Clim1 progressively delineate cortical projection neuron subtypes during development. Cereb Cortex 19 (2009), 62–69.
Yoon, K.-J., Vissers, C., Ming, G.-L., Song, H., Epigenetics and epitranscriptomics in temporal patterning of cortical neural progenitor competence. J Cell Biol 217 (2018), 1901–1914.
Sanosaka, T., Imamura, T., Hamazaki, N., Chai, M., Igarashi, K., Ideta-Otsuka, M., Miura, F., Ito, T., Fujii, N., Ikeo, K., et al. DNA methylome analysis identifies transcription factor-based epigenomic signatures of multilineage competence in neural stem/progenitor cells. Cell Rep 20 (2017), 2992–3003 This study reported the DNA methylation dynamics of cortical progenitors along corticogenesis and identified waves of demethylation coinciding with the neurogenic and gliogenic period.
Takizawa, T., Nakashima, K., Namihira, M., Ochiai, W., Uemura, A., Yanagisawa, M., Fujita, N., Nakao, M., Taga, T., DNA methylation is a critical cell-intrinsic determinant of astrocyte differentiation in the fetal brain. Dev Cell 1 (2001), 749–758.
Fan, G., Martinowich, K., Chin, M.H., He, F., Fouse, S.D., Hutnick, L., Hattori, D., Ge, W., Shen, Y., Wu, H., et al. DNA methylation controls the timing of astrogliogenesis through regulation of JAK-STAT signaling. Development 132 (2005), 3345–3356.
He, F., Ge, W., Martinowich, K., Becker-Catania, S., Coskun, V., Zhu, W., Wu, H., Castro, D., Guillemot, F., Fan, G., et al. A positive autoregulatory loop of Jak-STAT signaling controls the onset of astrogliogenesis. Nat Neurosci 8 (2005), 616–625.
Hirabayashi, Y., Suzki, N., Tsuboi, M., Endo, T.A., Toyoda, T., Shinga, J., Koseki, H., Vidal, M., Gotoh, Y., Polycomb limits the neurogenic competence of neural precursor cells to promote astrogenic fate transition. Neuron 63 (2009), 600–613.
Vitali, I., Fièvre, S., Telley, L., Oberst, P., Bariselli, S., Frangeul, L., Baumann, N., McMahon, J.J., Klingler, E., Bocchi, R., et al. Progenitor hyperpolarization regulates the sequential generation of neuronal subtypes in the developing neocortex. Cell 174 (2018), 1264–1276.e15 This study showed that bioelectric membrane properties are permissive for temporal progression of cortical apical progenitors and that hyperpolarization leads to a forward shift in apical progenitor temporal state via inhibition of Wnt-beta-catenin signaling.
Smith, R.S., Kenny, C.J., Ganesh, V., Jang, A., Borges-Monroy, R., Partlow, J.N., Hill, R.S., Shin, T., Chen, A.Y., Doan, R.N., et al. Sodium channel SCN3A (NaV1.3) regulation of human cerebral cortical folding and oral motor development. Neuron 99 (2018), 905–913.e7 This study showed that the voltage-gated sodium channel Na V 1.3 plays an important role in the prenatal development of human cortical areas and that mutations in Na V 1.3 disrupts cortical folding.
Zappaterra, M.D., Lisgo, S.N., Lindsay, S., Gygi, S.P., Walsh, C.A., Ballif, B.A., A comparative proteomic analysis of human and rat embryonic cerebrospinal fluid. J Proteome Res 6 (2007), 3537–3548.
Lehtinen, M.K., Zappaterra, M.W., Chen, X., Yang, Y.J., Hill, A.D., Lun, M., Maynard, T., Gonzalez, D., Kim, S., Ye, P., et al. The cerebrospinal fluid provides a proliferative niche for neural progenitor cells. Neuron 69 (2011), 893–905.
Lehtinen, M.K., Walsh, C.A., Neurogenesis at the brain-cerebrospinal fluid interface. Annu Rev Cell Dev Biol 27 (2011), 653–679.
Chau, K.F., Springel, M.W., Broadbelt, K.G., Park, H.-Y., Topal, S., Lun, M.P., Mullan, H., Maynard, T., Steen, H., LaMantia, A.S., et al. Progressive differentiation and instructive capacities of amniotic fluid and cerebrospinal fluid proteomes following neural tube closure. Dev Cell 35 (2015), 789–802.
Pouchelon, G., Frangeul, L., Rijli, F.M., Jabaudon, D., Patterning of pre-thalamic somatosensory pathways. Eur J Neurosci 35 (2012), 1533–1539.
Vue, T.Y., Lee, M., Tan, Y.E., Werkhoven, Z., Wang, L., Nakagawa, Y., Thalamic control of neocortical area formation in mice. J Neurosci 33 (2013), 8442–8453.
Dehay, C., Savatier, P., Cortay, V., Kennedy, H., Cell-cycle kinetics of neocortical precursors are influenced by embryonic thalamic axons. J Neurosci 21 (2001), 201–214.
Seuntjens, E., Nityanandam, A., Miquelajauregui, A., Debruyn, J., Stryjewska, A., Goebbels, S., Nave, K.-A., Huylebroeck, D., Tarabykin, V., Sip1 regulates sequential fate decisions by feedback signaling from postmitotic neurons to progenitors. Nat Neurosci 12 (2009), 1373–1380.
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. Development 141 (2014), 3324–3330.
Toma, K., Kumamoto, T., Hanashima, C., The timing of upper-layer neurogenesis is conferred by sequential derepression and negative feedback from deep-layer neurons. J Neurosci 34 (2014), 13259–13276.
Ozair, M.Z., Kirst, C., van den Berg, B.L., Ruzo, A., Rito, T., Brivanlou, A.H., hPSC modeling reveals that fate selection of cortical deep projection neurons occurs in the subplate. Cell Stem Cell 23 (2018), 60–73.e6 This study highlights the importance of the transient expansion of the subplate in primate corticogenesis as subplate neurons can be modulated postmitotically by Wnt-signaling to specify into all classes of deep layer projecting neurons.
Ohtaka-Maruyama, C., Okamoto, M., Endo, K., Oshima, M., Kaneko, N., Yura, K., Okado, H., Miyata, T., Maeda, N., Synaptic transmission from subplate neurons controls radial migration of neocortical neurons. Science 360 (2018), 313–317 This study showed that in the developing cortex, subplate neurons develop transient synapses to contact migrating neurons and instruct their multipolar to bipolar morphological transition.