Migration of Zebrafish Spinal Motor Nerves into the Periphery Requires Multiple Myotome-Derived Cues

Zeller, Jörg; Schneider, Valérie; Malayaman, Saniniuj; Higashijima, Shin‐ichi; Okamoto, Hitoshi; Gui, Jian‐Fang; Lin, Shuo; Granato, Michael

doi:10.1006/dbio.2002.0852

Cited by 67 publications

(69 citation statements)

References 52 publications

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“…Abnormal ECM organization was observed in the motor path of the zebrafish unp/MuSK mutant (Zhang et al, 2004). Immunoreactivity of the glycoprotein tenascin-C and chondroitin sulfate, but not laminin and heparan sulfate (Zhang et al, 2004), was markedly reduced in unp/MuSK mutants.…”

Section: Discussionmentioning

confidence: 96%

“…A batch of 18 hpf fixed embryos derived from a heterozygous incross of unplugged tbb72 mutants (Zhang et al, 2004) that were outcrossed with the HB9-GFP transgenic line were kindly provided by Michael Granato (University of Pennsylvania, Philadelphia). For genotyping, genomic DNA was grossly extracted by 10 min incubation at 95°C in 50 mM NaOH, followed by pH adjustment with 1 M Tris-HCl, pH 8 (1:10 final dilution).…”

Section: Methodsmentioning

confidence: 99%

“…Unplugged/MuSK signaling has been shown to mediate growth cone guidance by organizing deposition of ECM components (tenascin-C and CSPG) in the motor path (Zhang et al, 2004;. We thus reasoned that unplugged/ MuSK signaling might be responsible for COLXV-B deposition and organization in this region.…”

Section: Expression and Extracellular Deposition Of Col15a1b/colxv-b mentioning

confidence: 99%

“…Slow muscle precursors (adaxial cells) and muscle pioneers (MPs), a subset of Engrailed-expressing slow muscle cells, both play a critical role in motor axonogenesis (Melançon et al, 1997;Zhang and Granato, 2000). Adaxial cells, which are located adjacent to the notochord before somitogenesis, represent an important source of various extracellular matrix (ECM) components of the motor path.…”

Section: Introductionmentioning

confidence: 99%

“…Adaxial cells, which are located adjacent to the notochord before somitogenesis, represent an important source of various extracellular matrix (ECM) components of the motor path. As such, the glycoprotein tenascin-C and chondroitin sulfate proteoglycans (CSPGs) (Bernhardt and Schachner, 2000;Zhang et al, 2004), both expressed by adaxial cells, have been recognized as important short-range guidance cues for axon outgrowth.…”

Section: Introductionmentioning

confidence: 99%

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Slow Muscle Precursors Lay Down a Collagen XV Matrix Fingerprint to Guide Motor Axon Navigation

2016

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The extracellular matrix (ECM) provides local positional information to guide motoneuron axons toward their muscle target. Collagen XV is a basement membrane component mainly expressed in skeletal muscle. We have identified two zebrafish paralogs of the human COL15A1 gene, col15a1aandcol15a1b,whichdisplaydistinctexpressionpatterns.Hereweshowthatcol15a1bisexpressedanddepositedinthemotorpathECM by slow muscle precursors also called adaxial cells. We further demonstrate that collagen XV-B deposition is both temporally and spatially regulated before motor axon extension from the spinal cord in such a way that it remains in this region after the adaxial cells have migrated toward the periphery of the myotome. Loss-and gain-of-function experiments in zebrafish embryos demonstrate that col15a1b expression and subsequent collagen XV-B deposition and organization in the motor path ECM depend on a previously undescribed two-step mechanism involving Hedgehog/Gli and unplugged/MuSK signaling pathways. In silico analysis predicts a putative Gli binding site in the col15a1b proximal promoter. Using col15a1b promoter-reporter constructs, we demonstrate that col15a1b participates in the slow muscle genetic program as a direct target of Hedgehog/Gli signaling. Loss and gain of col15a1b function provoke pathfinding errors in primary and secondary motoneuron axons both at and beyond the choice point where axon pathway selection takes place. These defects result in muscle atrophy and compromised swimming behavior, a phenotype partially rescued by injection of a smyhc1:col15a1b construct. These reveal an unexpected and novel role for collagen XV in motor axon pathfinding and neuromuscular development.

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Section: Discussionmentioning

confidence: 96%

Section: Methodsmentioning

confidence: 99%

Section: Expression and Extracellular Deposition Of Col15a1b/colxv-b mentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Slow Muscle Precursors Lay Down a Collagen XV Matrix Fingerprint to Guide Motor Axon Navigation

2016

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Synaptotagmin I and II are present in distinct subsets of central synapses

Fox

Sanes

2007

J of Comparative Neurology

167

190

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Synaptotagmin 1 and 2 (syt 1, syt 2) are synaptic vesicle-associated membrane proteins that act as calcium sensors for fast neurotransmitter release from presynaptic nerve terminals. Here we show that widely used monoclonal antibodies, mab 48 and znp-1, stain nerve terminals in multiple species and, in mouse, recognize syt 1 and syt 2, respectively. With these antibodies, we examined the synaptic localization of these synaptotagmin isoforms in the mouse central nervous system. Syt 1 and syt 2 are localized predominantly to different subsets of synapses in retina, hippocampus, cerebellum, and median nucleus of the trapezoid body (MNTB). In the MNTB, syt 1 and syt 2 are present in different presynaptic terminals on the same postsynaptic principal neuron. In retina, horizontal and OFF-bipolar cell terminals contain syt 2, whereas most other terminals contain syt 1. Syt 1 localization in the immature retina resembles that seen in adult; however, syt 2 localization appears strikingly different at perinatal ages and continues to change dramatically prior to eye opening. For example, starburst amacrine cells, which lack syt 2 in adult retina, transiently express syt 2 during the first 2 postnatal weeks. In addition to differences in spatial and temporal distribution, species-specific differences in synaptotagmin localization were observed in retina and cerebellum. The cell-, temporal-, and species-specific expression of synaptotagmin isoforms suggests that each may have distinct functions in neurotransmitter release.

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Secondary motoneurons in juvenile and adult zebrafish: Axonal pathfinding errors caused by embryonic nicotine exposure

Menelaou

Svoboda

2008

J of Comparative Neurology

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Nicotine is a drug of abuse that has been reported to have many adverse effects on the developing nervous system. We previously demonstrated that embryonic exposure to nicotine alters axonal pathfinding of spinal secondary motoneurons in zebrafish. We hypothesize that these changes will persist into adulthood. The Tg(isl1:GFP) line of zebrafish, which expresses green fluorescent protein (GFP) in a subtype of spinal secondary motoneurons, was used to investigate potential long-term consequences of nicotine exposure on motoneuron development. Anatomical characterization of Tg(isl1:GFP) zebrafish ranging between 3 and 30 days postfertilization (dpf) was initially performed in fixed tissue to characterize axonal trajectories in larval and juvenile fish. Tg(isl1:GFP) embryos were transiently exposed to 5–30 μM nicotine. They were then rescued from nicotine and raised into later stages of life (3–30 dpf) and fixed for microscopic examination. Morphological analysis revealed that nicotine-induced abnormalities in secondary motoneuron anatomy were still evident in juvenile fish. Live imaging of Tg(isl1:GFP) zebrafish using fluorescent stereomicroscopy revealed that the nicotine-induced changes in motoneuron axonal pathfinding persisted into adulthood. We detected abnormalities in 37-dpf fish that were transiently exposed to nicotine as embryos. These fish were subsequently imaged over a 7-week period of time until they were ≈3 months of age. These pathfinding errors of spinal secondary motoneuron axons detected at 37 dpf persisted within the same fish until 86 dpf, the latest age analyzed. These findings indicate that exposure to nicotine during embryonic development can have permanent consequences for motoneuron anatomy in zebrafish. J. Comp. Neurol. 512:305–322, 2009. © 2008 Wiley-Liss, Inc.

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Migration of Zebrafish Spinal Motor Nerves into the Periphery Requires Multiple Myotome-Derived Cues

Cited by 67 publications

References 52 publications

Slow Muscle Precursors Lay Down a Collagen XV Matrix Fingerprint to Guide Motor Axon Navigation

Slow Muscle Precursors Lay Down a Collagen XV Matrix Fingerprint to Guide Motor Axon Navigation

Synaptotagmin I and II are present in distinct subsets of central synapses

Secondary motoneurons in juvenile and adult zebrafish: Axonal pathfinding errors caused by embryonic nicotine exposure

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