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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| 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. |
| doi_str_mv | 10.1371/journal.pone.0036913 |
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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.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0036913</identifier><identifier>PMID: 22629340</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Actin ; Actins - metabolism ; Animals ; Biology ; Bufo marinus ; Bulk polymerization ; Cell Membrane - metabolism ; Cytochalasin D ; Data recovery ; Depletion ; Drosophila ; Dynamin ; Dynamins - metabolism ; Endocytosis ; Endocytosis - physiology ; Exocytosis ; Inhibitors ; Insects ; Maturation ; Medicine ; Microscopy ; Muscle proteins ; Nerve endings ; Nervous system ; Neurotransmission ; Physics ; Plasma membranes ; Polymerization ; Protein turnover ; Pyridinium Compounds ; Quaternary Ammonium Compounds ; Recovery of function ; Stimulation ; Synapses - metabolism ; Synaptic Transmission - physiology ; Synaptic vesicles ; Synaptic Vesicles - metabolism ; Terminals ; Vesicles</subject><ispartof>PloS one, 2012-05, Vol.7 (5), p.e36913-e36913</ispartof><rights>COPYRIGHT 2012 Public Library of Science</rights><rights>2012 Nguyen et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>Nguyen et al. 2012</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c692t-8e1d9f975b5530b44585440b19d9ce7277dba0ec0dab91b296d091d63053821f3</citedby><cites>FETCH-LOGICAL-c692t-8e1d9f975b5530b44585440b19d9ce7277dba0ec0dab91b296d091d63053821f3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3358275/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3358275/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23847,27903,27904,53769,53771,79346,79347</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/22629340$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Cookson, Mark R.</contributor><creatorcontrib>Nguyen, Tam H</creatorcontrib><creatorcontrib>Maucort, Guillaume</creatorcontrib><creatorcontrib>Sullivan, Robert K P</creatorcontrib><creatorcontrib>Schenning, Mitja</creatorcontrib><creatorcontrib>Lavidis, Nickolas A</creatorcontrib><creatorcontrib>McCluskey, Adam</creatorcontrib><creatorcontrib>Robinson, Phillip J</creatorcontrib><creatorcontrib>Meunier, Frederic A</creatorcontrib><title>Actin- and dynamin-dependent maturation of bulk endocytosis restores neurotransmission following synaptic depletion</title><title>PloS one</title><addtitle>PLoS One</addtitle><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.</description><subject>Actin</subject><subject>Actins - metabolism</subject><subject>Animals</subject><subject>Biology</subject><subject>Bufo marinus</subject><subject>Bulk polymerization</subject><subject>Cell Membrane - metabolism</subject><subject>Cytochalasin D</subject><subject>Data recovery</subject><subject>Depletion</subject><subject>Drosophila</subject><subject>Dynamin</subject><subject>Dynamins - metabolism</subject><subject>Endocytosis</subject><subject>Endocytosis - physiology</subject><subject>Exocytosis</subject><subject>Inhibitors</subject><subject>Insects</subject><subject>Maturation</subject><subject>Medicine</subject><subject>Microscopy</subject><subject>Muscle proteins</subject><subject>Nerve endings</subject><subject>Nervous system</subject><subject>Neurotransmission</subject><subject>Physics</subject><subject>Plasma membranes</subject><subject>Polymerization</subject><subject>Protein turnover</subject><subject>Pyridinium Compounds</subject><subject>Quaternary Ammonium Compounds</subject><subject>Recovery of function</subject><subject>Stimulation</subject><subject>Synapses - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Nguyen, Tam H</au><au>Maucort, Guillaume</au><au>Sullivan, Robert K P</au><au>Schenning, Mitja</au><au>Lavidis, Nickolas A</au><au>McCluskey, Adam</au><au>Robinson, Phillip J</au><au>Meunier, Frederic A</au><au>Cookson, Mark R.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Actin- and dynamin-dependent maturation of bulk endocytosis restores neurotransmission following synaptic depletion</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2012-05-22</date><risdate>2012</risdate><volume>7</volume><issue>5</issue><spage>e36913</spage><epage>e36913</epage><pages>e36913-e36913</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><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.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>22629340</pmid><doi>10.1371/journal.pone.0036913</doi><tpages>e36913</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Actin Actins - metabolism Animals Biology Bufo marinus Bulk polymerization Cell Membrane - metabolism Cytochalasin D Data recovery Depletion Drosophila Dynamin Dynamins - metabolism Endocytosis Endocytosis - physiology Exocytosis Inhibitors Insects Maturation Medicine Microscopy Muscle proteins Nerve endings Nervous system Neurotransmission Physics Plasma membranes Polymerization Protein turnover Pyridinium Compounds Quaternary Ammonium Compounds Recovery of function Stimulation Synapses - metabolism Synaptic Transmission - physiology Synaptic vesicles Synaptic Vesicles - metabolism Terminals Vesicles |
| title | Actin- and dynamin-dependent maturation of bulk endocytosis restores neurotransmission following synaptic depletion |
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