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Featured ArticleArticles, Cellular/Molecular

The Active Zone Protein Family ELKS Supports Ca2+ Influx at Nerve Terminals of Inhibitory Hippocampal Neurons

Changliang Liu, Lydia S. Bickford, Richard G. Held, Hajnalka Nyitrai, Thomas C. Südhof and Pascal S. Kaeser
Journal of Neuroscience 10 September 2014, 34 (37) 12289-12303; DOI: https://doi.org/10.1523/JNEUROSCI.0999-14.2014
Changliang Liu
1Department of Neurobiology, Harvard Medical School, Boston, Massachusetts 02115, and
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Lydia S. Bickford
1Department of Neurobiology, Harvard Medical School, Boston, Massachusetts 02115, and
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Richard G. Held
1Department of Neurobiology, Harvard Medical School, Boston, Massachusetts 02115, and
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Hajnalka Nyitrai
1Department of Neurobiology, Harvard Medical School, Boston, Massachusetts 02115, and
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Thomas C. Südhof
2Department of Molecular and Cellular Physiology and
3Howard Hughes Medical Institute, Stanford University, Stanford, California 94305
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Pascal S. Kaeser
1Department of Neurobiology, Harvard Medical School, Boston, Massachusetts 02115, and
2Department of Molecular and Cellular Physiology and
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Abstract

In a presynaptic nerve terminal, synaptic vesicle exocytosis is restricted to specialized sites called active zones. At these sites, neurotransmitter release is determined by the number of releasable vesicles and their probability of release. Proteins at the active zone set these parameters by controlling the presynaptic Ca2+ signal, and through docking and priming of synaptic vesicles. Vertebrate ELKS proteins are enriched at presynaptic active zones, but their functions are not well understood. ELKS proteins are produced by two genes in vertebrates, and each gene contributes ∼50% to total brain ELKS. We generated knock-out mice for ELKS1 and found that its constitutive removal causes lethality. To bypass lethality, and to circumvent redundancy between ELKS1 and ELKS2 in synaptic transmission, we used a conditional genetic approach to remove both genes in cultured hippocampal neurons after synapses are established. Simultaneous removal of ELKS1 and ELKS2 resulted in a 50% decrease of neurotransmitter release at inhibitory synapses, paralleled by a reduction in release probability. Removal of ELKS did not affect synapse numbers or their electron microscopic appearance. Using Ca2+ imaging, we found that loss of ELKS caused a 30% reduction in single action potential-triggered Ca2+ influx in inhibitory nerve terminals, consistent with the deficits in synaptic transmission and release probability. Unlike deletion of the active zone proteins RIM, RIM-BP, or bruchpilot, ELKS removal did not lead to a measurable reduction in presynaptic Ca2+ channel levels. Our results reveal that ELKS is required for normal Ca2+ influx at nerve terminals of inhibitory hippocampal neurons.

  • active zone
  • calcium
  • ELKS
  • knock-out
  • priming
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The Journal of Neuroscience: 34 (37)
Journal of Neuroscience
Vol. 34, Issue 37
10 Sep 2014
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The Active Zone Protein Family ELKS Supports Ca2+ Influx at Nerve Terminals of Inhibitory Hippocampal Neurons
Changliang Liu, Lydia S. Bickford, Richard G. Held, Hajnalka Nyitrai, Thomas C. Südhof, Pascal S. Kaeser
Journal of Neuroscience 10 September 2014, 34 (37) 12289-12303; DOI: 10.1523/JNEUROSCI.0999-14.2014

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The Active Zone Protein Family ELKS Supports Ca2+ Influx at Nerve Terminals of Inhibitory Hippocampal Neurons
Changliang Liu, Lydia S. Bickford, Richard G. Held, Hajnalka Nyitrai, Thomas C. Südhof, Pascal S. Kaeser
Journal of Neuroscience 10 September 2014, 34 (37) 12289-12303; DOI: 10.1523/JNEUROSCI.0999-14.2014
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Keywords

  • active zone
  • calcium
  • ELKS
  • knock-out
  • priming

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