Glia and muscle sculpt neuromuscular arbors by engulfing destabilized synaptic boutons and shed presynaptic debris

Yuly Fuentes-Medel, Mary Logan, James Ashley, Bulent Ataman, Vivian Budnik, Marc Freeman

Research output: Contribution to journalArticle

85 Citations (Scopus)

Abstract

Synapse remodeling is an extremely dynamic process, often regulated by neural activity. Here we show during activitydependent synaptic growth at the Drosophila NMJ many immature synaptic boutons fail to form stable postsynaptic contacts, are selectively shed from the parent arbor, and degenerate or disappear from the neuromuscular junction (NMJ). Surprisingly, we also observe the widespread appearance of presynaptically derived "debris" during normal synaptic growth. The shedding of both immature boutons and presynaptic debris is enhanced by high-frequency stimulation of motorneurons, indicating that their formation is modulated by neural activity. Interestingly, we find that glia dynamically invade the NMJ and, working together with muscle cells, phagocytose shed presynaptic material. Suppressing engulfment activity in glia or muscle by disrupting the Draper/Ced-6 pathway results in a dramatic accumulation of presynaptic debris, and synaptic growth in turn is severely compromised. Thus actively growing NMJ arbors appear to constitutively generate an excessive number of immature boutons, eliminate those that are not stabilized through a shedding process, and normal synaptic expansion requires the continuous clearance of this material by both glia and muscle cells.

Original languageEnglish (US)
Article numbere1000184
JournalPLoS Biology
Volume7
Issue number8
DOIs
StatePublished - Aug 2009
Externally publishedYes

Fingerprint

Neuromuscular Junction
Presynaptic Terminals
Debris
Neuroglia
Muscle
immatures
Muscles
muscles
myocytes
Cells
Muscle Cells
Growth
sheds
synapse
phagocytosis
Cytophagocytosis
Drosophila
Synapses

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Immunology and Microbiology(all)
  • Neuroscience(all)

Cite this

Glia and muscle sculpt neuromuscular arbors by engulfing destabilized synaptic boutons and shed presynaptic debris. / Fuentes-Medel, Yuly; Logan, Mary; Ashley, James; Ataman, Bulent; Budnik, Vivian; Freeman, Marc.

In: PLoS Biology, Vol. 7, No. 8, e1000184, 08.2009.

Research output: Contribution to journalArticle

@article{b455224b8c054938934c30ae651b161d,
title = "Glia and muscle sculpt neuromuscular arbors by engulfing destabilized synaptic boutons and shed presynaptic debris",
abstract = "Synapse remodeling is an extremely dynamic process, often regulated by neural activity. Here we show during activitydependent synaptic growth at the Drosophila NMJ many immature synaptic boutons fail to form stable postsynaptic contacts, are selectively shed from the parent arbor, and degenerate or disappear from the neuromuscular junction (NMJ). Surprisingly, we also observe the widespread appearance of presynaptically derived {"}debris{"} during normal synaptic growth. The shedding of both immature boutons and presynaptic debris is enhanced by high-frequency stimulation of motorneurons, indicating that their formation is modulated by neural activity. Interestingly, we find that glia dynamically invade the NMJ and, working together with muscle cells, phagocytose shed presynaptic material. Suppressing engulfment activity in glia or muscle by disrupting the Draper/Ced-6 pathway results in a dramatic accumulation of presynaptic debris, and synaptic growth in turn is severely compromised. Thus actively growing NMJ arbors appear to constitutively generate an excessive number of immature boutons, eliminate those that are not stabilized through a shedding process, and normal synaptic expansion requires the continuous clearance of this material by both glia and muscle cells.",
author = "Yuly Fuentes-Medel and Mary Logan and James Ashley and Bulent Ataman and Vivian Budnik and Marc Freeman",
year = "2009",
month = "8",
doi = "10.1371/journal.pbio.1000184",
language = "English (US)",
volume = "7",
journal = "PLoS Biology",
issn = "1544-9173",
publisher = "Public Library of Science",
number = "8",

}

TY - JOUR

T1 - Glia and muscle sculpt neuromuscular arbors by engulfing destabilized synaptic boutons and shed presynaptic debris

AU - Fuentes-Medel, Yuly

AU - Logan, Mary

AU - Ashley, James

AU - Ataman, Bulent

AU - Budnik, Vivian

AU - Freeman, Marc

PY - 2009/8

Y1 - 2009/8

N2 - Synapse remodeling is an extremely dynamic process, often regulated by neural activity. Here we show during activitydependent synaptic growth at the Drosophila NMJ many immature synaptic boutons fail to form stable postsynaptic contacts, are selectively shed from the parent arbor, and degenerate or disappear from the neuromuscular junction (NMJ). Surprisingly, we also observe the widespread appearance of presynaptically derived "debris" during normal synaptic growth. The shedding of both immature boutons and presynaptic debris is enhanced by high-frequency stimulation of motorneurons, indicating that their formation is modulated by neural activity. Interestingly, we find that glia dynamically invade the NMJ and, working together with muscle cells, phagocytose shed presynaptic material. Suppressing engulfment activity in glia or muscle by disrupting the Draper/Ced-6 pathway results in a dramatic accumulation of presynaptic debris, and synaptic growth in turn is severely compromised. Thus actively growing NMJ arbors appear to constitutively generate an excessive number of immature boutons, eliminate those that are not stabilized through a shedding process, and normal synaptic expansion requires the continuous clearance of this material by both glia and muscle cells.

AB - Synapse remodeling is an extremely dynamic process, often regulated by neural activity. Here we show during activitydependent synaptic growth at the Drosophila NMJ many immature synaptic boutons fail to form stable postsynaptic contacts, are selectively shed from the parent arbor, and degenerate or disappear from the neuromuscular junction (NMJ). Surprisingly, we also observe the widespread appearance of presynaptically derived "debris" during normal synaptic growth. The shedding of both immature boutons and presynaptic debris is enhanced by high-frequency stimulation of motorneurons, indicating that their formation is modulated by neural activity. Interestingly, we find that glia dynamically invade the NMJ and, working together with muscle cells, phagocytose shed presynaptic material. Suppressing engulfment activity in glia or muscle by disrupting the Draper/Ced-6 pathway results in a dramatic accumulation of presynaptic debris, and synaptic growth in turn is severely compromised. Thus actively growing NMJ arbors appear to constitutively generate an excessive number of immature boutons, eliminate those that are not stabilized through a shedding process, and normal synaptic expansion requires the continuous clearance of this material by both glia and muscle cells.

UR - http://www.scopus.com/inward/record.url?scp=69349095671&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=69349095671&partnerID=8YFLogxK

U2 - 10.1371/journal.pbio.1000184

DO - 10.1371/journal.pbio.1000184

M3 - Article

C2 - 19707574

AN - SCOPUS:69349095671

VL - 7

JO - PLoS Biology

JF - PLoS Biology

SN - 1544-9173

IS - 8

M1 - e1000184

ER -