Neuronal NADPH oxidase 2 regulates growth cone guidance downstream of slit2/robo2.
Animals
Brain-Derived Neurotrophic Factor
Growth Cones
Intracellular Signaling Peptides and Proteins
/ chemistry
NADPH Oxidase 2
Netrin-1
/ chemistry
Reactive Oxygen Species
/ chemistry
Receptors, Immunologic
/ chemistry
Retinal Ganglion Cells
/ chemistry
Zebrafish
/ genetics
Zebrafish Proteins
/ chemistry
NADPH oxidase
Robo2
axon growth and guidance
hydrogen peroxide
optic chiasm
optic tectum
reactive oxygen species
retinal ganglion cell
slit2
Journal
Developmental neurobiology
ISSN: 1932-846X
Titre abrégé: Dev Neurobiol
Pays: United States
ID NLM: 101300215
Informations de publication
Date de publication:
01 2021
01 2021
Historique:
received:
21
07
2020
revised:
10
10
2020
accepted:
09
11
2020
pubmed:
17
11
2020
medline:
22
1
2022
entrez:
16
11
2020
Statut:
ppublish
Résumé
NADPH oxidases (Nox) are membrane-bound multi-subunit protein complexes producing reactive oxygen species (ROS) that regulate many cellular processes. Emerging evidence suggests that Nox-derived ROS also control neuronal development and axonal outgrowth. However, whether Nox act downstream of receptors for axonal growth and guidance cues is presently unknown. To answer this question, we cultured retinal ganglion cells (RGCs) derived from zebrafish embryos and exposed these neurons to netrin-1, slit2, and brain-derived neurotrophic factor (BDNF). To test the role of Nox in cue-mediated growth and guidance, we either pharmacologically inhibited Nox or investigated neurons from mutant fish that are deficient in Nox2. We found that slit2-mediated growth cone collapse, and axonal retraction were eliminated by Nox inhibition. Though we did not see an effect of either BDNF or netrin-1 on growth rates, growth in the presence of netrin-1 was reduced by Nox inhibition. Furthermore, attractive and repulsive growth cone turning in response to gradients of BDNF, netrin-1, and slit2, respectively, were eliminated when Nox was inhibited in vitro. ROS biosensor imaging showed that slit2 treatment increased growth cone hydrogen peroxide levels via mechanisms involving Nox2 activation. We also investigated the possible relationship between Nox2 and slit2/Robo2 signaling in vivo. astray/nox2 double heterozygote larvae exhibited decreased area of tectal innervation as compared to individual heterozygotes, suggesting both Nox2 and Robo2 are required for establishment of retinotectal connections. Our results provide evidence that Nox2 acts downstream of slit2/Robo2 by mediating growth and guidance of developing zebrafish RGC neurons.
Identifiants
pubmed: 33191581
doi: 10.1002/dneu.22791
pmc: PMC8204904
mid: NIHMS1704316
doi:
Substances chimiques
Brain-Derived Neurotrophic Factor
0
Intracellular Signaling Peptides and Proteins
0
Reactive Oxygen Species
0
Receptors, Immunologic
0
Slit2 protein, zebrafish
0
Zebrafish Proteins
0
robo2 protein, zebrafish
0
Netrin-1
158651-98-0
NADPH Oxidase 2
EC 1.6.3.-
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
3-21Subventions
Organisme : NINDS NIH HHS
ID : R01 NS117701
Pays : United States
Organisme : Office of the Executive Vice President for Research and Partnerships at Purdue University
ID : 210362
Organisme : Division of Integrative Organismal Systems
ID : 1146944-IOS
Organisme : Wellcome Trust
ID : 209911
Pays : United Kingdom
Organisme : Indiana Traumatic Spinal Cord and Brain Injury Research Fund
ID : 20000289
Informations de copyright
© 2020 Wiley Periodicals LLC.
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