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

Oberst, Polina; Agirman, Gulistan; Jabaudon, Denis

doi:10.1016/j.conb.2019.03.004

Cited by 57 publications

(38 citation statements)

References 81 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…In the Drosophila nervous system, individual neuroblasts produce a characteristic temporal series of distinct neuronal subtypes (Doe, 2017). Similar mechanisms have been documented in some regions of the vertebrate nervous system (Cepko, 2014; Holguera and Desplan, 2018; Oberst et al, 2019). For example, in the cortex distinct subtypes of glutamatergic neurons are sequentially generated (Jabaudon, 2017; Telley et al, 2019), in the hindbrain first motor neurons (MNs) and later serotonergic neurons are generated from the same set of progenitors (Pattyn et al, 2003), while in the midbrain, the production of ocular MNs is followed by red nucleus neurons (Deng et al, 2011).…”

Section: Introductionsupporting

confidence: 78%

“…Similar processes are believed to underlie the temporal patterning of tissues in the vertebrate nervous system, however, the transcriptional programs that mediate this process are still relatively poorly understood (Holguera and Desplan, 2018;Oberst et al, 2019). We therefore asked if similar principles apply to the spinal cord.…”

Section: Conserved Temporal Patterning Of Midbrain Hindbrain and Spimentioning

confidence: 99%

See 1 more Smart Citation

Temporal patterning of the central nervous system by a shared transcription factor code

Sagner

Zhang

Watson

et al. 2020

Preprint

View full text Add to dashboard Cite

The molecular mechanisms that ensure the reproducible generation of neuronal diversity in the vertebrate nervous system are incompletely understood. Here we provide evidence of a temporal patterning program consisting of cohorts of transcription factors expressed in neurons generated at successive developmental timepoints. This program acts in parallel to spatial patterning, diversifying neurons throughout the nervous system and in neurons differentiated in-vitro from stem cells. We demonstrate the TGFβ signalling pathway controls the pace of the temporal program. Furthermore, targeted perturbation of components of the temporal program, Nfia and Nfib, reveals their requirement for the generation of late-born neuronal subtypes. Together, our results provide evidence for the existence of a previously unappreciated global temporal program of neuronal subtype identity and suggest that the integration of spatial and temporal patterning programs diversifies and organises neuronal subtypes in the vertebrate nervous system.

show abstract

Section: Introductionsupporting

confidence: 78%

Section: Conserved Temporal Patterning Of Midbrain Hindbrain and Spimentioning

confidence: 99%

Temporal patterning of the central nervous system by a shared transcription factor code

Sagner

Zhang

Watson

et al. 2020

Preprint

View full text Add to dashboard Cite

show abstract

“…More broadly, the temporal generation of distinct 288 types of neurons or glia from the same progenitor domain is a widely used strategy to increase 289 cell diversity in the nervous system (Dias et al, 2014;Kohwi and Doe, 2013;Oberst et al, 2019a;290 Rossi et al, 2017). Extrinsic cues play important roles in the unfolding of these temporal 291 sequences (Kawaguchi, 2019;Oberst et al, 2019a;Oberst et al, 2019b;Syed et al, 2017;Tiberi 292 et al, 2012). Extrinsic manipulation of the temporality of these lineages should improve the 293 generation of early and late-born cells for both basic research, disease modeling and cell therapy.…”

Section: Discussion 248mentioning

confidence: 99%

Dynamic extrinsic pacing of theHOXclock in human axial progenitors controls motor neuron subtype specification

Mouilleau

Vaslin

Gribaudo

et al. 2020

Preprint

View full text Add to dashboard Cite

Rostro-caudal patterning of vertebrates depends on the temporally progressive activation of HOX 1 genes within axial stem cells that fuel axial embryo elongation. Whether HOX genes sequential 2 activation, the "HOX clock", is paced by intrinsic chromatin-based timing mechanisms or by 3 temporal changes in extrinsic cues remains unclear. Here, we studied HOX clock pacing in 4 human pluripotent stem cells differentiating into spinal cord motor neuron subtypes which are 5 progenies of axial progenitors. We show that the progressive activation of caudal HOX genes in 6 axial progenitors is controlled by a dynamic increase in FGF signaling. Blocking FGF pathway 7 stalled induction of HOX genes, while precocious increase in FGF alone, or with GDF11 ligand, 8 accelerated the HOX clock. Cells differentiated under accelerated HOX induction generated 9 appropriate posterior motor neuron subtypes found along the human embryonic spinal cord. The 10 HOX clock is thus dynamically paced by exposure parameters to secreted cues. Its manipulation 11 by extrinsic factors alleviates temporal requirements to provide unprecedented synchronized 12 access to human cells of multiple, defined, rostro-caudal identities for basic and translational 13 applications. , et al. (2013). Accelerated highyield generation of limb-innervating motor neurons from human stem cells. J. Neurosci. 33, 574-586. ., et al. (2019). Stem cell-derived cranial and spinal motor neurons reveal proteostatic differences between ALS resistant and sensitive motor neurons. Elife 8,.

show abstract

“…Understanding how cells measure and react to the progression of time (temporal progression) is not straightforward. Considering the Drosophila nervous system development, a limited set of feed-forward cross-regulated transcription factors (TFs) appears to be sufficient to generate a reproducible temporal sequence of transcriptional events [ 27 , 28 , 29 , 30 , 31 ]. For the sake of brevity, we will exclusively highlight a few examples of temporal patterning progression in the Drosophila CNS to extrapolate the general mechanisms of cell-autonomous temporal patterning.…”

Section: Regulation Of Cns Temporal Patterningmentioning

confidence: 99%

Emerging Roles of Single-Cell Multi-Omics in Studying Developmental Temporal Patterning

Lopes

Magrinelli

Telley

2020

IJMS

View full text Add to dashboard Cite

The complexity of brain structure and function is rooted in the precise spatial and temporal regulation of selective developmental events. During neurogenesis, both vertebrates and invertebrates generate a wide variety of specialized cell types through the expansion and specification of a restricted set of neuronal progenitors. Temporal patterning of neural progenitors rests on fine regulation between cell-intrinsic and cell-extrinsic mechanisms. The rapid emergence of high-throughput single-cell technologies combined with elaborate computational analysis has started to provide us with unprecedented biological insights related to temporal patterning in the developing central nervous system (CNS). Here, we present an overview of recent advances in Drosophila and vertebrates, focusing both on cell-intrinsic mechanisms and environmental influences. We then describe the various multi-omics approaches that have strongly contributed to our current understanding and discuss perspectives on the various -omics approaches that hold great potential for the future of temporal patterning research.

show abstract

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

Cited by 57 publications

References 81 publications

Temporal patterning of the central nervous system by a shared transcription factor code

Temporal patterning of the central nervous system by a shared transcription factor code

Dynamic extrinsic pacing of theHOXclock in human axial progenitors controls motor neuron subtype specification

Emerging Roles of Single-Cell Multi-Omics in Studying Developmental Temporal Patterning

Contact Info

Product

Resources

About