Actin- and dynamin-dependent maturation of bulk endocytosis restores neurotransmission following synaptic depletion

Nguyen, Tam H., Maucort, Guillaume, Sullivan, Robert K. P., Schenning, Mitja, Lavidis, Nickolas A., McCluskey, Adam, Robinson, Phillip J. and Meunier, Frederic A. (2012) Actin- and dynamin-dependent maturation of bulk endocytosis restores neurotransmission following synaptic depletion. PLoS One, 7 5 Article No.e36913: .


Author Nguyen, Tam H.
Maucort, Guillaume
Sullivan, Robert K. P.
Schenning, Mitja
Lavidis, Nickolas A.
McCluskey, Adam
Robinson, Phillip J.
Meunier, Frederic A.
Title Actin- and dynamin-dependent maturation of bulk endocytosis restores neurotransmission following synaptic depletion
Journal name PLoS One  (ERA 2012 Listed)    (ERA 2010 Rank A)   Check publisher's open access policy
Publication date 2012-05-22
Sub-type Article
DOI 10.1371/journal.pone.0036913
Volume number 7
Issue number 5 Article No.e36913
ISSN 1932-6203
Total pages 15
Place of publication San Francisco CA , United States
Publisher Public Library of Science
Collection year 2013
Language eng
Formatted abstract Bulk endocytosis contributes to the maintenance of neurotransmission at the amphibian neuromuscular junction by regenerating synaptic vesicles. How nerve terminals internalize adequate portions of the presynaptic membrane when bulk
endocytosis is initiated before the end of a sustained stimulation is unknown. A maturation process, occurring at the end of the stimulation, is hypothesised to precisely restore the pools of synaptic vesicles. Using confocal time-lapse microscopy of FM1-43-labeled nerve terminals at the amphibian neuromuscular junction, we confirm that bulk endocytosis is initiated during a sustained tetanic stimulation and reveal that shortly after the end of the stimulation, nerve terminals undergo a maturation process. This includes a transient bulging of the plasma membrane, followed by the development of large intraterminal FM1-43-positive donut-like structures comprising large bulk membrane cisternae surrounded by recycling vesicles. The degree of bulging increased with stimulation frequency and the plasmalemma surface retrieved following the transient bulging correlated with the surface membrane internalized in bulk cisternae and recycling vesicles. Dyngo-4a, a
potent dynamin inhibitor, did not block the initiation, but prevented the maturation of bulk endocytosis. In contrast, cytochalasin D, an inhibitor of actin polymerization, hindered both the initiation and maturation processes. Both inhibitors hampered the functional recovery of neurotransmission after synaptic depletion. Our data confirm that initiation of bulk endocytosis occurs during stimulation and demonstrates that a delayed maturation process controlled by actin and dynamin underpins the coupling between exocytosis and bulk endocytosis.
Keyword Cell membrane
Neurotransmission
Nerve stimulation
Q-Index Code C1
Q-Index Status Confirmed Code
Institutional Status UQ

 
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Created: Wed, 11 Jul 2012, 11:42:01 EST by Debra McMurtrie on behalf of Queensland Brain Institute