Large-conductance calcium-activated potassium channels in Purkinje cell plasma membranes are clustered at sites of hypolemmal microdomains Journal Article


Author(s): Kaufmann, Walter; Ferraguti, Francesco; Fukazawa, Yugo; Kasugai, Yu; Shigemoto, Ryuichi; Laake, Petter; Sexton, Joseph A; Ruth, Peter; Wietzorrek, Georg; Knaus, Hans G; Storm, Johan F; Ottersen, Ole P
Article Title: Large-conductance calcium-activated potassium channels in Purkinje cell plasma membranes are clustered at sites of hypolemmal microdomains
Affiliation
Abstract: Calcium-activated potassium channels have been shown to be critically involved in neuronal function, but an elucidation of their detailed roles awaits identification of the microdomains where they are located. This study was undertaken to unravel the precise subcellular distribution of the large-conductance calcium-activated potassium channels (called BK, KCa1.1, or Slo1) in the somatodendritic compartment of cerebellar Purkinje cells by means of postembedding immunogold cytochemistry and SDS-digested freeze-fracture replica labeling (SDS-FRL). We found BK channels to be unevenly distributed over the Purkinje cell plasma membrane. At distal dendritic compartments, BK channels were scattered over the plasma membrane of dendritic shafts and spines but absent from postsynaptic densities. At the soma and proximal dendrites, BK channels formed two distinct pools. One pool was scattered over the plasma membrane, whereas the other pool was clustered in plasma membrane domains overlying subsurface cisterns. The labeling density ratio of clustered to scattered channels was about 60:1, established in SDS-FRL. Subsurface cisterns, also called hypolemmal cisterns, are subcompartments of the endoplasmic reticulum likely representing calciosomes that unload and refill Ca2+ independently. Purkinje cell subsurface cisterns are enriched in inositol 1,4,5-triphosphate receptors that mediate the effects of several neurotransmitters, hormones, and growth factors by releasing Ca2+ into the cytosol, generating local Ca2+ sparks. Such increases in cytosolic [Ca2+] may be sufficient for BK channel activation. Clustered BK channels in the plasma membrane may thus participate in building a functional unit (plasmerosome) with the underlying calciosome that contributes significantly to local signaling in Purkinje cells.
Keywords: BK channels; Calciosome; Plasmerosome; Postembedding immunogold; SDS-FRL; Subsurface cisterns
Journal Title: Journal of Comparative Neurology
Volume: 515
Issue 2
ISSN: 0021-9967
Publisher: Wiley-Blackwell  
Date Published: 2009-07-10
Start Page: 215
End Page: 230
DOI: 10.1002/cne.22066
Open access: no