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PMID: 19786572 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Autophagy promotes synapse development in Drosophila.

The Journal of cell biology ·Vol. 187 ·No. 1 ·2009-10-05 ·Pages 71-9

Shen W, Ganetzky B

Abstract

Autophagy, a lysosome-dependent degradation mechanism, mediates many biological processes, including cellular stress responses and neuroprotection. In this study, we demonstrate that autophagy positively regulates development of the Drosophila melanogaster larval neuromuscular junction (NMJ). Autophagy induces an NMJ overgrowth phenotype closely resembling that of highwire (hiw), an E3 ubiquitin ligase mutant. Moreover, like hiw, autophagy-induced NMJ overgrowth is suppressed by wallenda (wnd) and by a dominant-negative c-Jun NH(2)-terminal kinase (bsk(DN)). We show that autophagy promotes NMJ growth by reducing Hiw levels. Thus, autophagy and the ubiquitin-proteasome system converge in regulating synaptic development. Because autophagy is triggered in response to many environmental cues, our findings suggest that it is perfectly positioned to link environmental conditions with synaptic growth and plasticity.

MeSH Terms
Amines/metabolism Animals Autophagy/genetics Drosophila/genetics,metabolism,physiology Drosophila Proteins/genetics,metabolism Fluorescein-5-isothiocyanate/metabolism Fluorescent Dyes/metabolism Horseradish Peroxidase/metabolism Immunohistochemistry JNK Mitogen-Activated Protein Kinases/genetics,metabolism Larva/genetics,metabolism,physiology MAP Kinase Kinase Kinases/genetics,metabolism Mutation Nerve Tissue Proteins/genetics,metabolism Neuromuscular Junction/genetics,metabolism Synapses/genetics,metabolism,physiology
Chemicals
Amines Drosophila Proteins Fluorescent Dyes HIW protein, Drosophila Nerve Tissue Proteins Red DND-99 Horseradish Peroxidase JNK Mitogen-Activated Protein Kinases MAP Kinase Kinase Kinases wnd protein, Drosophila Fluorescein-5-isothiocyanate
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Shen Wei
Laboratory of Genetics, University of Wisconsin-Madison, Madison, WI 53706, USA.
Ganetzky Barry
References (34)
34 references, click to expand
  1. The role of autophagy in cardiomyocytes in the basal state and in response to hemodynamic stress.
    Nat Med. 2007 May;13(5):619-24 PMID: 17450150
  2. Autophagy in the pathogenesis of disease.
    Cell. 2008 Jan 11;132(1):27-42 PMID: 18191218
  3. Jun mediates Frizzled-induced R3/R4 cell fate distinction and planar polarity determination in the Drosophila eye.
    Development. 2000 Aug;127(16):3619-29 PMID: 10903185
  4. Development by self-digestion: molecular mechanisms and biological functions of autophagy.
    Dev Cell. 2004 Apr;6(4):463-77 PMID: 15068787
  5. Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice.
    Nature. 2006 Jun 15;441(7095):885-9 PMID: 16625204
  6. SEPA-1 mediates the specific recognition and degradation of P granule components by autophagy in C. elegans.
    Cell. 2009 Jan 23;136(2):308-21 PMID: 19167332
  7. UNC-51/ATG1 kinase regulates axonal transport by mediating motor-cargo assembly.
    Genes Dev. 2008 Dec 1;22(23):3292-307 PMID: 19056884
  8. The Drosophila Wnt, wingless, provides an essential signal for pre- and postsynaptic differentiation.
    Cell. 2002 Nov 1;111(3):319-30 PMID: 12419243
  9. ATG1, an autophagy regulator, inhibits cell growth by negatively regulating S6 kinase.
    EMBO Rep. 2007 Apr;8(4):360-5 PMID: 17347671
  10. Role and regulation of starvation-induced autophagy in the Drosophila fat body.
    Dev Cell. 2004 Aug;7(2):167-78 PMID: 15296714
  11. Potential therapeutic applications of autophagy.
    Nat Rev Drug Discov. 2007 Apr;6(4):304-12 PMID: 17396135
  12. Direct induction of autophagy by Atg1 inhibits cell growth and induces apoptotic cell death.
    Curr Biol. 2007 Jan 9;17(1):1-11 PMID: 17208179
  13. Altering Drosophila S6 kinase activity is consistent with a role for S6 kinase in growth.
    Genesis. 2002 Sep-Oct;34(1-2):83-5 PMID: 12324955
  14. wishful thinking encodes a BMP type II receptor that regulates synaptic growth in Drosophila.
    Neuron. 2002 Feb 14;33(4):545-58 PMID: 11856529
  15. Suppression of polyglutamine-mediated neurodegeneration in Drosophila by the molecular chaperone HSP70.
    Nat Genet. 1999 Dec;23(4):425-8 PMID: 10581028
  16. Altered synaptic development and active zone spacing in endocytosis mutants.
    Curr Biol. 2006 Mar 21;16(6):591-8 PMID: 16546084
  17. The Berkeley Drosophila Genome Project gene disruption project: Single P-element insertions mutating 25% of vital Drosophila genes.
    Genetics. 1999 Sep;153(1):135-77 PMID: 10471706
  18. Growth arrest and autophagy are required for salivary gland cell degradation in Drosophila.
    Cell. 2007 Dec 14;131(6):1137-48 PMID: 18083103
  19. Synaptic development: insights from Drosophila.
    Curr Opin Neurobiol. 2007 Feb;17(1):35-42 PMID: 17229568
  20. Mechanisms of TSC-mediated control of synapse assembly and axon guidance.
    PLoS One. 2007 Apr 18;2(4):e375 PMID: 17440611
  21. A Drosophila kinesin required for synaptic bouton formation and synaptic vesicle transport.
    Nat Neurosci. 2007 Aug;10(8):980-9 PMID: 17643120
  22. Genetic dissection of structural and functional components of synaptic plasticity. I. Fasciclin II controls synaptic stabilization and growth.
    Neuron. 1996 Oct;17(4):641-54 PMID: 8893022
  23. Highwire restrains synaptic growth by attenuating a MAP kinase signal.
    Neuron. 2006 Jul 6;51(1):57-69 PMID: 16815332
  24. Highwire function at the Drosophila neuromuscular junction: spatial, structural, and temporal requirements.
    J Neurosci. 2005 Oct 19;25(42):9557-66 PMID: 16237161
  25. Unc-51 controls active zone density and protein composition by downregulating ERK signaling.
    J Neurosci. 2009 Jan 14;29(2):517-28 PMID: 19144852
  26. Presynaptic terminals independently regulate synaptic clustering and autophagy of GABAA receptors in Caenorhabditis elegans.
    J Neurosci. 2006 Feb 8;26(6):1711-20 PMID: 16467519
  27. Nervous wreck and Cdc42 cooperate to regulate endocytic actin assembly during synaptic growth.
    J Neurosci. 2008 Aug 13;28(33):8316-25 PMID: 18701694
  28. Nervous wreck, an SH3 adaptor protein that interacts with Wsp, regulates synaptic growth in Drosophila.
    Neuron. 2004 Feb 19;41(4):521-34 PMID: 14980202
  29. Dap160/intersectin acts as a stabilizing scaffold required for synaptic development and vesicle endocytosis.
    Neuron. 2004 Jul 22;43(2):193-205 PMID: 15260956
  30. Dap160/intersectin scaffolds the periactive zone to achieve high-fidelity endocytosis and normal synaptic growth.
    Neuron. 2004 Jul 22;43(2):207-19 PMID: 15260957
  31. Identification and characterization of a SUMO-1 conjugation system that modifies neuronal calcium/calmodulin-dependent protein kinase II in Drosophila melanogaster.
    J Biol Chem. 2000 Dec 29;275(52):40765-76 PMID: 10995744
  32. Highwire regulates synaptic growth in Drosophila.
    Neuron. 2000 May;26(2):313-29 PMID: 10839352
  33. Derailed regulates development of the Drosophila neuromuscular junction.
    Dev Neurobiol. 2008 Feb 1;68(2):152-65 PMID: 17963254
  34. Nervous wreck interacts with thickveins and the endocytic machinery to attenuate retrograde BMP signaling during synaptic growth.
    Neuron. 2008 May 22;58(4):507-18 PMID: 18498733
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
1540-8140
Published
2009-10-05
Epub
2009-00-28
Pages
71-9
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2762098
Subset
IM
Grants
NINDS NIH HHS · R01 NS015390 · United States
NINDS NIH HHS · NS15390 · United States
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