Similarity of junctions between plasma membranes and endoplasmic reticulum in muscle and neurons.

Abstract

The structure of membranes at junctions between the plasma membrane and underlying cisterns of endoplasmic reticulum in amphioxus muscle and mouse cerebellar neurons was studied using the freeze-fracture technique. In amphioxus muscle, subsurface cisterns of sarcoplasmic reticulum form junctions with the surface membrane at the level of the sarcomere I bands. On the protoplasmic leaflet of the sarcolemma overlying these junctions were aggregates of large particles. On the protoplasmic leaflet of the membranes of cerebellar basket, stellate, and Purkinje cells there were similar aggregates of large particles. In both tissues, the corresponding external membrane halves had arrays of pits apparently complementary to the aggregates of large particles. Cross fractures through junctions showed that the particle aggregates in neuronal and muscle membranes were consistently located over intracellular cisterns closely applied to the plasma membrane. Thus, a similar plasma membrane specialization is found at subsurface cisterns in mammalian neurons and amphioxus muscle. This similarity supports the hypothesis that subsurface cisterns in neurons, like those in muscle, couple some intracellular activity to the electrical activity of the plasma membrane.Junctions between the surface or transverse tubule membrane and the endoplasmic, or sarcoplasmic, reticulum of muscle are thought to mediate excitation contraction coupling (12,34,39). Junctions between the surface membrane and regions of endoplasmic reticulum (ER), known as subsurface cisterns, are also present in neurons (38). Their similarity to the junctions in muscle has been noted (27, 38), but the functions of subsurface cisterns in neurons are unknown. We have used the freeze-fracture technique to compare the structure of the membranes participating in these junctions in striated muscle from the chordate, amphioxus, to their structure in neurons of the mammalian cerebellar cortex. The morphologic similarities apparent in thin sections are paralleled by similarities in the arrays of membrane particles revealed by freeze-fracturing the membranes at these junctions. These further similarities lend support to the suggestion (19,20,38) that subsurface cistern junctions may function in neurons, as in muscle, to couple excitatory events at the surface membrane with intracellular activities. A preliminary report of our results has been presented (25). MATERIALS AND METHODSAmphioxus Branchiostoma californiensis were obtained from Pacific Bio-marine Supply Co., Venice, Calif., and maintained in cold natural seawater for short periods

Deficiency in parvalbumin, but not in calbindin D-28k upregulates mitochondrial volume and decreases smooth endoplasmic reticulum surface selectively in a peripheral, subplasmalemmal region in the soma of Purkinje cells

“…In specialized sPL regions, junctional ER in close proximity to mitochondria exists (Henkart et al, 1976) and local Ca 2ϩ signaling appears to be "independent" of the bulk cytosolic Ca 2ϩ signaling (Arnon et al, 2000). In PVϪ/Ϫ PC somata, sPL-sER compartments were decreased by approximately 35%.…”

“…No ultrastructural distinction between described junctional ER (in PC characterized by an orientation parallel to the plasma membrane and the gap to the plasma membrane filled with "fuzzy" material (Henkart et al, 1976)) and other sER compartments was attempted. In the morphometric measurements all sER structures within a shell of 0.5 m were considered for the analyses.…”

Local subplasma membrane Ca 2+ signals detected by a tethered Ca 2+ sensor

“…ATP-and 5HT-evoked Ca 2ϩ signals involve primarily inositol trisphosphate-mediated S͞ER Ca 2ϩ release. Thus, it appears that EGTA greatly reduced diffusion of Ca 2ϩ to the PM, even at the PM-S͞ER junctions, where the two membranes are Յ20 nm apart (6)(7)(8).…”

“…These PM-S͞ER units play a unique role in excitation-contraction coupling (5). A comparable structural and functional relationship exists between certain PM microdomains and the underlying ''junctional'' S͞ER (jS͞ER) in other cell types, including neurons (6,7) and vascular smooth muscle cells (8). Furthermore, coimmunoprecipitation data from the brain provide evidence of large structural complexes that include PM, S͞ER, and cytoskeletal proteins in glia and neurons (4,9).…”

Ca 2+ sparks and secretion in dorsal root ganglion neurons

“…Intriguingly, in many vertebrate and invertebrate neurons of both the CNS and peripheral systems, including DRG, specialized regions of the ER, dubbed subsurface cisternae (SSC), come into direct apposition to the plasma membrane, forming nanoscopic junctions reminiscent of the dyads or triads in muscles (16,17). At places of SSC, Ca 2ϩ release might occur spontaneously or it can be coupled to local Ca 2ϩ entry via the CICR mechanism and, consequentially, elevate local Ca 2ϩ concentrations to trigger exocytosis of nearby vesicles.…”