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Research Articles, Development/Plasticity/Repair

Cav2.2 Channels Sustain Vesicle Recruitment at a Mature Glutamatergic Synapse

Magdalena Wender, Grit Bornschein, Simone Brachtendorf, Stefan Hallermann, Jens Eilers and Hartmut Schmidt
Journal of Neuroscience 31 May 2023, 43 (22) 4005-4018; DOI: https://doi.org/10.1523/JNEUROSCI.1279-22.2023
Magdalena Wender
Carl Ludwig Institute for Physiology, Medical Faculty, Leipzig University, 04103 Leipzig, Germany
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Grit Bornschein
Carl Ludwig Institute for Physiology, Medical Faculty, Leipzig University, 04103 Leipzig, Germany
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Simone Brachtendorf
Carl Ludwig Institute for Physiology, Medical Faculty, Leipzig University, 04103 Leipzig, Germany
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Stefan Hallermann
Carl Ludwig Institute for Physiology, Medical Faculty, Leipzig University, 04103 Leipzig, Germany
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Jens Eilers
Carl Ludwig Institute for Physiology, Medical Faculty, Leipzig University, 04103 Leipzig, Germany
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Hartmut Schmidt
Carl Ludwig Institute for Physiology, Medical Faculty, Leipzig University, 04103 Leipzig, Germany
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Abstract

The composition of voltage-gated Ca2+ channel (Cav) subtypes that gate action potential (AP)-evoked release changes during the development of mammalian CNS synapses. Cav2.2 and Cav2.3 lose their function in gating-evoked release during postnatal synapse maturation. In mature boutons, Cav2.1 currents provide the almost exclusive trigger for evoked release, and Cav2.3 currents are required for the induction of presynaptic long-term potentiation. However, the functional significance of Cav2.2 remained elusive in mature boutons, although they remain present at active zones and continue contributing significantly to presynaptic Ca2+ influx. Here, we addressed the functional significance of Cav2.2 and Cav2.3 at mature parallel-fiber (PF) to Purkinje neuron synapses of mice of either sex. These synapses are known to exhibit the corresponding developmental Cav subtype changes in gating release. We addressed two hypotheses, namely that Cav2.2 and Cav2.3 are involved in triggering spontaneous glutamate release and that they are engaged in vesicle recruitment during repetitive evoked release. We found that spontaneous miniature release is Ca2+ dependent. However, experiments with Cav subtype-specific blockers excluded the spontaneous opening of Cavs as the Ca2+ source for spontaneous glutamate release. Thus, neither Cav2.2 nor Cav2.3 controls spontaneous release from PF boutons. Furthermore, vesicle recruitment during brief bursts of APs was also independent of Ca2+ influx through Cav2.2 and Cav2.3. However, Cav2.2, but not Cav2.3, currents significantly boosted vesicle recruitment during sustained high-frequency synaptic transmission. Thus, in mature PF boutons Cav2.2 channels are specifically required to sustain synaptic transmission during prolonged neuronal activity.

SIGNIFICANCE STATEMENT At young CNS synapses, action potential-evoked release is gated via three subtypes of voltage-gated Ca2+ channels: Cav2.1, Cav2.2, and Cav2.3. During postnatal maturation, Cav2.2 and Cav2.3 lose their function in gating evoked release, such that at mature synapses Cav2.1 provides the almost exclusive source for triggering evoked release. Cav2.3 currents are required for the induction of presynaptic long-term potentiation. However, the function of the still abundant Cav2.2 in mature boutons remained largely elusive. Here, we studied mature cerebellar parallel-fiber synapses and found that Cav2.2 does not control spontaneous release. However, Ca2+ influx through Cav2.2 significantly boosted vesicle recruitment during trains of action potentials. Thus, Cav2.2 in mature parallel-fiber boutons participate in sustaining synaptic transmission during prolonged activity.

  • calcium channels
  • facilitation
  • N-type
  • parallel fiber
  • plasticity
  • vesicle recruitment

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The Journal of Neuroscience: 43 (22)
Journal of Neuroscience
Vol. 43, Issue 22
31 May 2023
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Cav2.2 Channels Sustain Vesicle Recruitment at a Mature Glutamatergic Synapse
Magdalena Wender, Grit Bornschein, Simone Brachtendorf, Stefan Hallermann, Jens Eilers, Hartmut Schmidt
Journal of Neuroscience 31 May 2023, 43 (22) 4005-4018; DOI: 10.1523/JNEUROSCI.1279-22.2023

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Cav2.2 Channels Sustain Vesicle Recruitment at a Mature Glutamatergic Synapse
Magdalena Wender, Grit Bornschein, Simone Brachtendorf, Stefan Hallermann, Jens Eilers, Hartmut Schmidt
Journal of Neuroscience 31 May 2023, 43 (22) 4005-4018; DOI: 10.1523/JNEUROSCI.1279-22.2023
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Keywords

  • calcium channels
  • facilitation
  • N-type
  • parallel fiber
  • plasticity
  • vesicle recruitment

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