Embryonic ethanol exposure disrupts craniofacial neuromuscular integration in zebrafish larvae

Forming a vertebrate head involves the meticulous integration of multiple tissue types during development. Prenatal alcohol exposure is known to cause a variety of birth defects, especially to tissues in the vertebrate head. However, a systematic analysis of coordinated defects across tissues in the...

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Main Authors: Ritika Ghosal, Gissela Borrego-Soto, Johann K. Eberhart
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-02-01
Series:Frontiers in Physiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fphys.2023.1131075/full
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author Ritika Ghosal
Gissela Borrego-Soto
Johann K. Eberhart
author_facet Ritika Ghosal
Gissela Borrego-Soto
Johann K. Eberhart
author_sort Ritika Ghosal
collection DOAJ
description Forming a vertebrate head involves the meticulous integration of multiple tissue types during development. Prenatal alcohol exposure is known to cause a variety of birth defects, especially to tissues in the vertebrate head. However, a systematic analysis of coordinated defects across tissues in the head is lacking. Here, we delineate the effects of ethanol on individual tissue types and their integration during craniofacial development. We found that exposure to 1% ethanol induced ectopic cranial muscle and nerve defects with only slight effects on skeletal pattern. Ectopic muscles were, however, unaccompanied by ectopic tendons and could be partially rescued by anesthetizing the larvae before muscle fibers appeared. This finding suggests that the ectopic muscles result from fiber detachment and are not due to an underlying muscle patterning defect. Interestingly, immobilization did not rescue the nerve defects, thus ethanol has an independent effect on each tissue even though they are linked in developmental time and space. Time-course experiments demonstrated an increase in nerve defects with ethanol exposure between 48hpf-4dpf. Time-lapse imaging confirmed the absence of nerve pathfinding or misrouting defects until 48hpf. These results indicate that ethanol-induced nerve defects occur at the time of muscle innervation and after musculoskeletal patterning. Further, we investigated the effect of ethanol on the neuromuscular junctions of the craniofacial muscles and found a reduced number of postsynaptic receptors with no significant effect on the presynaptic terminals. Our study shows that craniofacial soft tissues are particularly susceptible to ethanol-induced damage and that these defects appear independent from one another. Thus, the effects of ethanol on the vertebrate head appear highly pleiotropic.
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spelling doaj.art-70e88e55c030465fa142160eccc79d542023-02-07T08:44:45ZengFrontiers Media S.A.Frontiers in Physiology1664-042X2023-02-011410.3389/fphys.2023.11310751131075Embryonic ethanol exposure disrupts craniofacial neuromuscular integration in zebrafish larvaeRitika GhosalGissela Borrego-SotoJohann K. EberhartForming a vertebrate head involves the meticulous integration of multiple tissue types during development. Prenatal alcohol exposure is known to cause a variety of birth defects, especially to tissues in the vertebrate head. However, a systematic analysis of coordinated defects across tissues in the head is lacking. Here, we delineate the effects of ethanol on individual tissue types and their integration during craniofacial development. We found that exposure to 1% ethanol induced ectopic cranial muscle and nerve defects with only slight effects on skeletal pattern. Ectopic muscles were, however, unaccompanied by ectopic tendons and could be partially rescued by anesthetizing the larvae before muscle fibers appeared. This finding suggests that the ectopic muscles result from fiber detachment and are not due to an underlying muscle patterning defect. Interestingly, immobilization did not rescue the nerve defects, thus ethanol has an independent effect on each tissue even though they are linked in developmental time and space. Time-course experiments demonstrated an increase in nerve defects with ethanol exposure between 48hpf-4dpf. Time-lapse imaging confirmed the absence of nerve pathfinding or misrouting defects until 48hpf. These results indicate that ethanol-induced nerve defects occur at the time of muscle innervation and after musculoskeletal patterning. Further, we investigated the effect of ethanol on the neuromuscular junctions of the craniofacial muscles and found a reduced number of postsynaptic receptors with no significant effect on the presynaptic terminals. Our study shows that craniofacial soft tissues are particularly susceptible to ethanol-induced damage and that these defects appear independent from one another. Thus, the effects of ethanol on the vertebrate head appear highly pleiotropic.https://www.frontiersin.org/articles/10.3389/fphys.2023.1131075/fullethanolcranial nervesneuromuscular junctionmotor neuronteratogencraniofacial
spellingShingle Ritika Ghosal
Gissela Borrego-Soto
Johann K. Eberhart
Embryonic ethanol exposure disrupts craniofacial neuromuscular integration in zebrafish larvae
Frontiers in Physiology
ethanol
cranial nerves
neuromuscular junction
motor neuron
teratogen
craniofacial
title Embryonic ethanol exposure disrupts craniofacial neuromuscular integration in zebrafish larvae
title_full Embryonic ethanol exposure disrupts craniofacial neuromuscular integration in zebrafish larvae
title_fullStr Embryonic ethanol exposure disrupts craniofacial neuromuscular integration in zebrafish larvae
title_full_unstemmed Embryonic ethanol exposure disrupts craniofacial neuromuscular integration in zebrafish larvae
title_short Embryonic ethanol exposure disrupts craniofacial neuromuscular integration in zebrafish larvae
title_sort embryonic ethanol exposure disrupts craniofacial neuromuscular integration in zebrafish larvae
topic ethanol
cranial nerves
neuromuscular junction
motor neuron
teratogen
craniofacial
url https://www.frontiersin.org/articles/10.3389/fphys.2023.1131075/full
work_keys_str_mv AT ritikaghosal embryonicethanolexposuredisruptscraniofacialneuromuscularintegrationinzebrafishlarvae
AT gisselaborregosoto embryonicethanolexposuredisruptscraniofacialneuromuscularintegrationinzebrafishlarvae
AT johannkeberhart embryonicethanolexposuredisruptscraniofacialneuromuscularintegrationinzebrafishlarvae