PUBLICATION

Synaptic-like Vesicles Facilitate Pioneer Axon Invasion

Authors
Nichols, E.L., Smith, C.J.
ID
ZDB-PUB-190807-1
Date
2019
Source
Current biology : CB   29(16): 2652-2664.e4 (Journal)
Registered Authors
Keywords
DREZ, axon guidance, development, dorsal root ganglia, invasion, matrix metalloproteinase, synaptic vesicles, zebrafish
MeSH Terms
  • Animals
  • Axons/physiology*
  • Ganglia, Spinal/physiology*
  • Growth Cones/physiology*
  • Synaptic Vesicles/physiology*
  • Zebrafish/physiology*
(all 6)
PubMed
31378609 Full text @ Curr. Biol.
Abstract
Synaptic vesicles are indispensable for neuronal communication in mature circuits. Synaptic vesicle biogenesis must be concurrent with axon navigation for synaptogenesis, but whether synaptic vesicles are functionally employed in circuit formation before synaptogenesis is poorly understood. Here, we use time-lapse imaging and transgenesis in zebrafish to visualize the role of synaptic-like vesicles in navigation of dorsal root ganglia pioneer axons. We identify that synaptic-like vesicles accumulate in the central growth cone as the pioneer axon breaches the spinal boundary at the dorsal root entry zone. Inhibition of vesicle release with cell-specific tetanus toxin expression results in pioneer axon pathfinding defects and altered spinal entry. We further show that the matrix metalloproteinase (MMP) mmp14a is required in pioneer axons to navigate across the boundary of the spinal cord and, with super-resolution microscopy, is positioned with synaptic vesicles at the boundary. Manipulations of concurrent actin reorganization reveal that actin remodeling drives vesicle release and subsequent MMP activity. Together, these data point to an indispensable role for synaptic-like vesicles at specific points in axon navigation as regulators of growth cone microenvironment.
Genes / Markers
Marker Marker Type Name
gmpr2GENEguanosine monophosphate reductase 2
mmp14aGENEmatrix metallopeptidase 14a (membrane-inserted)
sypbGENEsynaptophysin b
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Figures
Figure Gallery (3 images)
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Expression
Gene Antibody Fish Conditions Stage Qualifier Anatomy Assay Figure
EGFPscz059Tg; w61Tgstandard conditionsProtruding-mouthIHC
EGFPw61TgcontrolLong-pecIHC
GFPco19Tg; mu271Tgchemical treatment by environment: ilomastatLong-pec to Protruding-mouthIFL
GFPco19Tg; mu271Tgstandard conditionsLong-pecIHC
GFPco19Tg; mu271TgcontrolLong-pec to Protruding-mouthIFL
GFPco19Tg; mu271Tgchemical treatment by environment: ilomastatLong-pec to Protruding-mouthIFL
GFPco19Tg; mu271TgcontrolLong-pec to Protruding-mouthIFL
GFPco19Tg; uq1esTgstandard conditionsLong-pecIHC
GFPco19Tg; uq1esTgcontrolLong-pec to Protruding-mouthIFL
GFPco19Tg; uq1esTgchemical treatment by environment: paclitaxelLong-pec to Protruding-mouthIFL
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Phenotype
Fish Conditions Stage Phenotype Figure
co19Tg; mu271Tgchemical treatment by environment: ilomastatLong-pec to Protruding-mouth
co19Tg; uq1esTgchemical treatment by environment: SU6656Long-pec to Protruding-mouth
mi2001Tg; vu234Tgchemical treatment by environment: ilomastatLong-pec to Protruding-mouth
pd1028Tg; vu234Tgchemical treatment by environment: ilomastatLong-pec to Protruding-mouth
1 - 4 of 4
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Mutations / Transgenics
Allele Construct Type Affected Genomic Region
co19TgTransgenic Insertion
    hzm1EtTransgenic Insertion
      mi2001TgTransgenic Insertion
        mu271TgTransgenic Insertion
          pd1028TgTransgenic Insertion
            scz059TgTransgenic Insertion
              uq1esTgTransgenic Insertion
                uva22TgTransgenic Insertion
                  vu234TgTransgenic Insertion
                    w61TgTransgenic Insertion
                      1 - 10 of 10
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                      Human Disease / Model
                      No data available
                      Sequence Targeting Reagents
                      Target Reagent Reagent Type
                      mmp14aCRISPR1-mmp14aCRISPR
                      1 - 1 of 1
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                      Fish
                      Fish
                      co19Tg; mu271Tg
                      co19Tg; uq1esTg
                      co19Tg; uq1esTg; vu234Tg
                      mi2001Tg; vu234Tg
                      pd1028Tg; vu234Tg
                      scz059Tg; w61Tg
                      w61Tg
                      1 - 7 of 7
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                      Antibodies
                      Orthology
                      No data available
                      Engineered Foreign Genes
                      Marker Marker Type Name
                      CeruleanEFGCerulean
                      EGFPEFGEGFP
                      GAL4EFGGAL4
                      GAL4TA4EFGGAL4TA4
                      GFPEFGGFP
                      mCherryEFGmCherry
                      mRFPEFGmRFP
                      NTREFGNTR
                      1 - 8 of 8
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                      Mapping
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                      Citation
                      Nichols, E.L., Smith, C.J. (2019) Synaptic-like Vesicles Facilitate Pioneer Axon Invasion. Current biology : CB. 29(16):2652-2664.e4.