Glia maintain follower neuron survival during Drosophila CNS development

Development ◽  
2000 ◽  
Vol 127 (2) ◽  
pp. 237-244 ◽  
Author(s):  
G.E. Booth ◽  
E.F. Kinrade ◽  
A. Hidalgo
Keyword(s):  
Axon Guidance ◽  
Neuronal Survival ◽  
Cell Number ◽  
Cns Development ◽  
Neuronal Fate ◽  
Missing Gene ◽  
Pioneer Neurons ◽  
Longitudinal Axon ◽  
Glial Function ◽  
Embryonic Cns

While survival of CNS neurons appears to depend on multiple neuronal and non-neuronal factors, it remains largely unknown how neuronal survival is controlled during development. Here we show that glia regulate neuronal survival during formation of the Drosophila embryonic CNS. When glial function is impaired either by mutation of the glial cells missing gene, which transforms glia toward a neuronal fate, or by targeted genetic glial ablation, neuronal death is induced non-autonomously. Pioneer neurons, which establish the first longitudinal axon fascicles, are insensitive to glial depletion whereas the later extending follower neurons die. This differential requirement of neurons for glia is instructive in patterning and links control of cell number with axon guidance during CNS development.

Targeted neuronal ablation: the role of pioneer neurons in guidance and fasciculation in the CNS of Drosophila

Development ◽  
1997 ◽  
Vol 124 (17) ◽  
pp. 3253-3262 ◽  
Author(s):  
A. Hidalgo ◽  
A.H. Brand
Keyword(s):  
Temporal Profile ◽  
Pioneer Neurons ◽  
Longitudinal Axon ◽  
Pioneer Neuron ◽  
Embryonic Cns

Although pioneer neurons are the first to delineate the axon pathways, it is uncertain whether they have unique pathfinding abilities. As a first step in defining the role of pioneer neurons in the Drosophila embryonic CNS, we describe the temporal profile and trajectory of the axons of four pioneer neurons and show that they differ from previously published reports. We show, by targeted ablation of one, two, three or four pioneer neurons at a time, that (1) no single pioneer neuron is essential for axon tract formation, (2) the interaction between two pioneers is necessary for the establishment of each fascicle and (3) pioneer neurons function synergistically to establish the longitudinal axon tracts, to guide the fasciculation of follower neurons along specific fascicles and to prevent axons from crossing the midline.

scholarly journals Proteolytic cleavage of Slit by the Tolkin protease converts an axon repulsion cue to an axon growth cue in vivo

Development ◽  
2020 ◽  
Vol 147 (20) ◽  
pp. dev196055
Author(s):  
Riley Kellermeyer ◽  
Leah M. Heydman ◽  
Taylor Gillis ◽  
Grant S. Mastick ◽  
Minmin Song ◽  
...  
Keyword(s):  
Axon Guidance ◽  
Axon Growth ◽  
Biologically Active ◽  
Longitudinal Axon ◽  
Axon Repulsion ◽  
Embryonic Cns ◽  
Cns Midline ◽  
Primary Substrate

ABSTRACTSlit is a secreted protein that has a canonical function of repelling growing axons from the CNS midline. The full-length Slit (Slit-FL) is cleaved into Slit-N and Slit-C fragments, which have potentially distinct functions via different receptors. Here, we report that the BMP-1/Tolloid family metalloprotease Tolkin (Tok) is responsible for Slit proteolysis in vivo and in vitro. In Drosophilatok mutants lacking Slit cleavage, midline repulsion of axons occurs normally, confirming that Slit-FL is sufficient to repel axons. However, longitudinal axon guidance is highly disrupted in tok mutants and can be rescued by midline expression of Slit-N, suggesting that Slit is the primary substrate for Tok in the embryonic CNS. Transgenic restoration of Slit-N or Slit-C does not repel axons in Slit-null flies. Slit-FL and Slit-N are both biologically active cues with distinct axon guidance functions in vivo. Slit signaling is used in diverse biological processes; therefore, differentiating between Slit-FL and Slit fragments will be essential for evaluating Slit function in broader contexts.

Glia dictate pioneer axon trajectories in the Drosophila embryonic CNS

Development ◽  
2000 ◽  
Vol 127 (2) ◽  
pp. 393-402 ◽  
Author(s):  
A. Hidalgo ◽  
G.E. Booth
Keyword(s):  
Axon Guidance ◽  
Molecular Mechanisms ◽  
Neuronal Cell ◽  
Cell Types ◽  
Growth Cones ◽  
Neuronal Cell Bodies ◽  
Direct Formation ◽  
Pioneer Neurons ◽  
Embryonic Cns ◽  
Made In

Whereas considerable progress has been made in understanding the molecular mechanisms of axon guidance across the midline, it is still unclear how the axonal trajectories of longitudinal pioneer neurons, which never cross the midline, are established. Here we show that longitudinal glia of the embryonic Drosophila CNS direct formation of pioneer axon pathways. By ablation and analysis of glial cells missing mutants, we demonstrate that glia are required for two kinds of processes. Firstly, glia are required for growth cone guidance, although this requirement is not absolute. We show that the route of extending growth cones is rich in neuronal cell bodies and glia, and also in long processes from both these cell types. Interactions between neurons, glia and their long processes orient extending growth cones. Secondly, glia direct the fasciculation and defasciculation of axons, which pattern the pioneer pathways. Together these events are essential for the selective fasciculation of follower axons along the longitudinal pathways.

scholarly journals The microRNA miR-124 antagonizes the anti-neural REST/SCP1 pathway during embryonic CNS development

2007 ◽  
Vol 21 (7) ◽  
pp. 744-749 ◽  
Author(s):  
J. Visvanathan ◽  
S. Lee ◽  
B. Lee ◽  
J. W. Lee ◽  
S.-K. Lee
Keyword(s):  
Cns Development ◽  
Embryonic Cns

scholarly journals The Slit-binding Ig1 domain is required for multiple axon guidance activities of Drosophila Robo2

2021 ◽  
Author(s):  
LaFreda J. Howard ◽  
Marie C. Reichert ◽  
Timothy A. Evans
Keyword(s):  
Axon Guidance ◽  
Lateral Position ◽  
Commissural Axons ◽  
Lateral Zone ◽  
Guidance Receptors ◽  
Longitudinal Axon ◽  
A Cell ◽  
Pathway Formation ◽  
Embryonic Neurons

Drosophila Robo2 is a member of the evolutionarily conserved Roundabout (Robo) family of axon guidance receptors. The canonical role of Robo receptors is to signal midline repulsion in response to their cognate Slit ligands, which bind to the N-terminal Ig1 domain in most Robo family members. In the Drosophila embryonic ventral nerve cord, Robo1 and Robo2 cooperate to signal Slit-dependent midline repulsion, while Robo2 also regulates the medial-lateral position of longitudinal axon pathways and acts non-autonomously to promote midline crossing of commissural axons. Although it is clear that Robo2 signals midline repulsion in response to Slit, it is less clear whether Robo2's other activities are also Slit-dependent. To determine which of Robo2's axon guidance roles depend on its Slit-binding Ig1 domain, we have used a CRISPR/Cas9-based strategy replace the endogenous robo2 gene with a robo2 variant from which the Ig1 domain has been deleted (robo2ΔIg1). We compare the expression and localization of Robo2ΔIg1 protein with that of full-length Robo2 in embryonic neurons in vivo, and examine its ability to substitute for Robo2 to mediate midline repulsion and lateral axon pathway formation. We find that removal of the Ig1 domain from Robo2ΔIg1 disrupts both of these axon guidance activities. In addition, we find that the Ig1 domain of Robo2 is required for its proper subcellular localization in embryonic neurons, a role that is not shared by the Ig1 domain of Robo1. Finally, we report that although FasII-positive lateral axons are misguided in embryos expressing Robo2ΔIg1, the axons that normally express Robo2 are correctly guided to the lateral zone, suggesting that Robo2 may guide lateral longitudinal axons through a cell non-autonomous mechanism.

scholarly journals Drosophila Embryonic CNS Development: Neurogenesis, Gliogenesis, Cell Fate, and Differentiation

Genetics ◽  
2019 ◽  
Vol 213 (4) ◽  
pp. 1111-1144 ◽  
Author(s):  
Stephen T. Crews
Keyword(s):  
Nervous System ◽  
Cell Fate ◽  
Molecular Genetic ◽  
Cell Fate Specification ◽  
Cns Development ◽  
Fate Specification ◽  
The Past ◽  
New Concepts ◽  
Embryonic Cns ◽  
Complex Organ

The Drosophila embryonic central nervous system (CNS) is a complex organ consisting of ∼15,000 neurons and glia that is generated in ∼1 day of development. For the past 40 years, Drosophila developmental neuroscientists have described each step of CNS development in precise molecular genetic detail. This has led to an understanding of how an intricate nervous system emerges from a single cell. These studies have also provided important, new concepts in developmental biology, and provided an essential model for understanding similar processes in other organisms. In this article, the key genes that guide Drosophila CNS development and how they function is reviewed. Features of CNS development covered in this review are neurogenesis, gliogenesis, cell fate specification, and differentiation.

NMDA receptor activity determines neuronal fate: location or number?

2015 ◽  
Vol 26 (1) ◽  
Author(s):  
Xianju Zhou ◽  
Zhouyou Chen ◽  
Wenwei Yun ◽  
Hongbing Wang
Keyword(s):  
Neuronal Death ◽  
Neuronal Damage ◽  
Neuronal Survival ◽  
Neurological Diseases ◽  
Synaptic Activity ◽  
Neuronal Fate ◽  
Mutual Antagonism ◽  
Nmdar Activation ◽  
Excessive Activation

AbstractIt is widely believed that the proper activation of N-methyl-D-aspartate (NMDA) receptors (NMDARs) promotes neuronal survival, whereas an excessive activation of NMDARs leads to neuronal damage. NMDARs are found at both synaptic and extrasynaptic sites. One current prevailing theory proposes the dichotomy of NMDAR activity. The role of the two population receptors is mutual antagonism. The activation of synaptic NMDARs, such as synaptic activity at physiological levels, promotes neuronal survival. However, the activation of extrasynaptic NMDARs occurring during stroke, brain injury, and chronic neurological diseases contributes to neuronal death. Thus, the location of NMDARs determines the neuronal fate. However, the theory is greatly challenged. Several studies suggested that synaptic NMDARs are involved in neuronal death. Recently, our work further showed that the coactivation of synaptic and extrasynaptic NMDARs contributes to neuronal death under neuronal insults. Therefore, we propose that the magnitude and duration of NMDAR activation determines the neuronal fate. More interestingly, there appears to be some subtle differences in the affinity between synaptic and extrasynaptic NMDARs, shedding light on the development of selective drugs to block extrasynaptic NMDARs.

scholarly journals The DOCK Protein Sponge Binds to ELMO and Functions in Drosophila Embryonic CNS Development

PLoS ONE ◽  
2011 ◽  
Vol 6 (1) ◽  
pp. e16120 ◽  
Author(s):  
Bridget Biersmith ◽  
Ze Liu ◽  
Kenneth Bauman ◽  
Erika R. Geisbrecht
Keyword(s):  
Cns Development ◽  
Embryonic Cns

Longitudinal axon guidance

2006 ◽  
Vol 16 (1) ◽  
pp. 35-39 ◽  
Author(s):  
Esther T Stoeckli
Keyword(s):  
Axon Guidance ◽  
Longitudinal Axon

scholarly journals Prolonged Minocycline Treatment Impairs Motor Neuronal Survival and Glial Function in Organotypic Rat Spinal Cord Cultures

PLoS ONE ◽  
2013 ◽  
Vol 8 (8) ◽  
pp. e73422 ◽  
Author(s):  
Josephine Pinkernelle ◽  
Hisham Fansa ◽  
Uwe Ebmeyer ◽  
Gerburg Keilhoff
Keyword(s):  
Spinal Cord ◽  
Neuronal Survival ◽  
Rat Spinal Cord ◽  
Minocycline Treatment ◽  
Glial Function
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