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The Journal of Neuroscience, April 1, 2003, 23(7):2538
Imaging Calcium Entry Sites and Ribbon Structures in Two
Presynaptic Cells
David
Zenisek1,
Viviana
Davila2,
Lei
Wan2, and
Wolfhard
Almers2
1 Department of Cellular and Molecular Physiology, Yale
University School of Medicine, New Haven, Connecticut 06520, and
2 Vollum Institute, Portland, Oregon 97201
We investigated the location of calcium entry sites and synaptic
ribbons in the type-Mb goldfish bipolar neuron and the bullfrog saccular hair cell. Cells were loaded with a fast calcium indicator (Fluo-3 or Fluo-5F) and an excess of a high-affinity but slow Ca buffer
(EGTA). The cell surface was imaged by evanescent field microscopy.
Small fluorescent "hot spots" representing calcium entry sites
appeared abruptly when a voltage step opened Ca channels and
disappeared or dimmed abruptly when Ca channels closed. In bipolar
cells, the fluorescence of hot spots tracked the calcium influx. Hair
cells showed similar Ca hot spots. Synaptic ribbons or dense bodies
were labeled by immunofluorescence with an antibody that recognizes the
ribbon protein ribeye. The antibody labeled punctate structures beneath
the plasma membrane. In both bipolar neurons and hair cells, the number
of Ca entry sites was similar or identical to that of ribbons or dense
bodies, consistent with the idea that calcium-channel clusters reside
near ribbons, and that both mark active zones. In bipolar cells, the
number of Ca entry sites and ribeye-positive fluorescent spots is also
strikingly similar to that of exocytic active zones but significantly
less than the number of total exocytic sites including solitary fusion events outside active zones. We suggest that in bipolar terminals, active zones, Ca entry sites, and synaptic ribbons all colocalize, but
also that a significant number of vesicles can fuse outside active
zones and, hence, independently of synaptic ribbons.
Key words:
calcium microdomains; ribeye; exocytosis; retina; bipolar cell; hair cell; evanescent field
Copyright © 2003 Society for Neuroscience 0270-6474/03/2372538-11$05.00/0
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|
|
|
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|
|
|
|
|
|
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|
|
|
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[Full Text]
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