Cell type-specific requirements for heparan sulfate biosynthesis at the Drosophila neuromuscular junction: effects on synapse function, membrane trafficking, and mitochondrial localization.

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  • Author(s): Ren Y;Ren Y; Kirkpatrick CA; Rawson JM; Sun M; Selleck SB
  • Source:
    The Journal of neuroscience : the official journal of the Society for Neuroscience [J Neurosci] 2009 Jul 01; Vol. 29 (26), pp. 8539-50.
  • Publication Type:
    Journal Article; Research Support, N.I.H., Extramural
  • Language:
    English
  • Additional Information
    • Source:
      Publisher: Society for Neuroscience Country of Publication: United States NLM ID: 8102140 Publication Model: Print Cited Medium: Internet ISSN: 1529-2401 (Electronic) Linking ISSN: 02706474 NLM ISO Abbreviation: J Neurosci Subsets: MEDLINE
    • Publication Information:
      Publication: Washington, DC : Society for Neuroscience
      Original Publication: [Baltimore, Md.] : The Society, c1981-
    • Subject Terms:
      Cell Movement/*physiology ; Heparitin Sulfate/*biosynthesis ; Mitochondria/*metabolism ; Neuromuscular Junction/*physiology ; Neurons/*classification ; Neurons/*physiology; Animals ; Animals, Genetically Modified ; Behavior, Animal/physiology ; Cell Communication/physiology ; Cell Movement/genetics ; Drosophila ; Drosophila Proteins/genetics ; Drosophila Proteins/metabolism ; Endocytosis/genetics ; Excitatory Postsynaptic Potentials/drug effects ; Excitatory Postsynaptic Potentials/physiology ; Gene Expression Regulation/physiology ; Green Fluorescent Proteins/genetics ; Heparan Sulfate Proteoglycans/biosynthesis ; Heparan Sulfate Proteoglycans/genetics ; Heparan Sulfate Proteoglycans/metabolism ; Heparitin Sulfate/genetics ; Horseradish Peroxidase/metabolism ; Larva ; Locomotion/physiology ; Microscopy, Electron, Transmission/methods ; Mitochondria/ultrastructure ; Muscle, Skeletal/metabolism ; Muscle, Skeletal/ultrastructure ; Mutation ; Neuromuscular Junction/cytology ; Neuromuscular Junction/ultrastructure
    • Abstract:
      Heparan sulfate proteoglycans (HSPGs) are concentrated at neuromuscular synapses in many species, including Drosophila. We have established the physiological and patterning functions of HSPGs at the Drosophila neuromuscular junction by using mutations that block heparan sulfate synthesis or sulfation to compromise HSPG function. The mutant animals showed defects in synaptic physiology and morphology suggesting that HSPGs function both presynaptically and postsynaptically; these defects could be rescued by appropriate transgene expression. Of particular interest were selective disruptions of mitochondrial localization, abnormal distributions of Golgi and endoplasmic reticulum markers in the muscle, and a markedly increased level of stimulus-dependent endocytosis in the motoneuron. Our data support the emerging view that HSPG functions are not limited to the cell surface and matrix environments, but also affect a diverse set of cellular processes including membrane trafficking and organelle distributions.
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    • Grant Information:
      GM054832 United States GM NIGMS NIH HHS; R01 GM067208-04 United States GM NIGMS NIH HHS; GM067208 United States GM NIGMS NIH HHS; R01 GM067208 United States GM NIGMS NIH HHS; R01 GM054832 United States GM NIGMS NIH HHS
    • Accession Number:
      0 (Drosophila Proteins)
      0 (Heparan Sulfate Proteoglycans)
      147336-22-9 (Green Fluorescent Proteins)
      9050-30-0 (Heparitin Sulfate)
      EC 1.11.1.- (Horseradish Peroxidase)
    • Publication Date:
      Date Created: 20090703 Date Completed: 20090720 Latest Revision: 20211020
    • Publication Date:
      20231215
    • Accession Number:
      PMC3849837
    • Accession Number:
      10.1523/JNEUROSCI.5587-08.2009
    • Accession Number:
      19571145