TY - JOUR
T1 - Fast, Temperature-Sensitive and Clathrin-Independent Endocytosis at Central Synapses
AU - Delvendahl, Igor
AU - Vyleta, Nicholas P.
AU - von Gersdorff, Henrique
AU - Hallermann, Stefan
N1 - Publisher Copyright:
© 2016 Elsevier Inc.
PY - 2016/5/4
Y1 - 2016/5/4
N2 - The fusion of neurotransmitter-filled vesicles during synaptic transmission is balanced by endocytotic membrane retrieval. Despite extensive research, the speed and mechanisms of synaptic vesicle endocytosis have remained controversial. Here, we establish low-noise time-resolved membrane capacitance measurements that allow monitoring changes in surface membrane area elicited by single action potentials and stronger stimuli with high-temporal resolution at physiological temperature in individual bona-fide mature central synapses. We show that single action potentials trigger very rapid endocytosis, retrieving presynaptic membrane with a time constant of 470 ms. This fast endocytosis is independent of clathrin but mediated by dynamin and actin. In contrast, stronger stimuli evoke a slower mode of endocytosis that is clathrin, dynamin, and actin dependent. Furthermore, the speed of endocytosis is highly temperature dependent with a Q10 of ~3.5. These results demonstrate that distinct molecular modes of endocytosis with markedly different kinetics operate at central synapses. Membrane retrieval of fused synaptic vesicles by endocytosis is essential for synaptic function. Using time-resolved presynaptic membrane capacitance measurements at physiological temperature, Delvendahl et al. show that single action potentials trigger fast and clathrin-independent endocytosis at mature central synapses.
AB - The fusion of neurotransmitter-filled vesicles during synaptic transmission is balanced by endocytotic membrane retrieval. Despite extensive research, the speed and mechanisms of synaptic vesicle endocytosis have remained controversial. Here, we establish low-noise time-resolved membrane capacitance measurements that allow monitoring changes in surface membrane area elicited by single action potentials and stronger stimuli with high-temporal resolution at physiological temperature in individual bona-fide mature central synapses. We show that single action potentials trigger very rapid endocytosis, retrieving presynaptic membrane with a time constant of 470 ms. This fast endocytosis is independent of clathrin but mediated by dynamin and actin. In contrast, stronger stimuli evoke a slower mode of endocytosis that is clathrin, dynamin, and actin dependent. Furthermore, the speed of endocytosis is highly temperature dependent with a Q10 of ~3.5. These results demonstrate that distinct molecular modes of endocytosis with markedly different kinetics operate at central synapses. Membrane retrieval of fused synaptic vesicles by endocytosis is essential for synaptic function. Using time-resolved presynaptic membrane capacitance measurements at physiological temperature, Delvendahl et al. show that single action potentials trigger fast and clathrin-independent endocytosis at mature central synapses.
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U2 - 10.1016/j.neuron.2016.03.013
DO - 10.1016/j.neuron.2016.03.013
M3 - Article
C2 - 27146271
AN - SCOPUS:84963516702
SN - 0896-6273
VL - 90
SP - 492
EP - 498
JO - Neuron
JF - Neuron
IS - 3
ER -