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

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 i...

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Autores principales:	Tam H Nguyen, Guillaume Maucort, Robert K P Sullivan, Mitja Schenning, Nickolas A Lavidis, Adam McCluskey, Phillip J Robinson, Frederic A Meunier
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2012
Materias:	Medicine R Science Q
Acceso en línea:	https://doaj.org/article/bd5b422326d54c5f9c5181a427970d7e
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spelling	oai:doaj.org-article:bd5b422326d54c5f9c5181a427970d7e2021-11-18T07:17:52ZActin- and dynamin-dependent maturation of bulk endocytosis restores neurotransmission following synaptic depletion.1932-620310.1371/journal.pone.0036913https://doaj.org/article/bd5b422326d54c5f9c5181a427970d7e2012-01-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/22629340/pdf/?tool=EBIhttps://doaj.org/toc/1932-6203Bulk 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.Tam H NguyenGuillaume MaucortRobert K P SullivanMitja SchenningNickolas A LavidisAdam McCluskeyPhillip J RobinsonFrederic A MeunierPublic Library of Science (PLoS)articleMedicineRScienceQENPLoS ONE, Vol 7, Iss 5, p e36913 (2012)
institution	DOAJ
collection	DOAJ
language	EN
topic	Medicine R Science Q
spellingShingle	Medicine R Science Q Tam H Nguyen Guillaume Maucort Robert K P Sullivan Mitja Schenning Nickolas A Lavidis Adam McCluskey Phillip J Robinson Frederic A Meunier Actin- and dynamin-dependent maturation of bulk endocytosis restores neurotransmission following synaptic depletion.
description	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.
format	article
author	Tam H Nguyen Guillaume Maucort Robert K P Sullivan Mitja Schenning Nickolas A Lavidis Adam McCluskey Phillip J Robinson Frederic A Meunier
author_facet	Tam H Nguyen Guillaume Maucort Robert K P Sullivan Mitja Schenning Nickolas A Lavidis Adam McCluskey Phillip J Robinson Frederic A Meunier
author_sort	Tam H Nguyen
title	Actin- and dynamin-dependent maturation of bulk endocytosis restores neurotransmission following synaptic depletion.
title_short	Actin- and dynamin-dependent maturation of bulk endocytosis restores neurotransmission following synaptic depletion.
title_full	Actin- and dynamin-dependent maturation of bulk endocytosis restores neurotransmission following synaptic depletion.
title_fullStr	Actin- and dynamin-dependent maturation of bulk endocytosis restores neurotransmission following synaptic depletion.
title_full_unstemmed	Actin- and dynamin-dependent maturation of bulk endocytosis restores neurotransmission following synaptic depletion.
title_sort	actin- and dynamin-dependent maturation of bulk endocytosis restores neurotransmission following synaptic depletion.
publisher	Public Library of Science (PLoS)
publishDate	2012
url	https://doaj.org/article/bd5b422326d54c5f9c5181a427970d7e
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Actin- and dynamin-dependent maturation of bulk endocytosis restores neurotransmission following synaptic depletion.

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