Introduction
The endoplasmic reticulum of most eukaryotic cells contains
relatively high levels of Ca
2+
and represent an important source
for Ca
2+
release into cytosol in response to stimulation of cells
by a variety of agonists (Berridge et al., 2000). There are many
components involved in the organisation of intracellular Ca
2+
stores. Ca
2+
pumps of the sarcoplasmic endoplasmic reticulum
Ca
2+
ATPases (SERCAs) family accumulate Ca
2+
into the
lumen of the endoplasmic reticulum, where specific Ca
2+
-
binding proteins (such as calsequestrin and calreticulin)
provide an efficient mechanisms of storage, mediated by their
high capacity and low affinity for Ca
2+
(Pozzan et al., 1994;
Sorrentino and Rizzuto, 2001). Ca
2+
accumulated in the
intracellular stores of the endoplasmic reticulum is released
into the cytosol through Ca
2+
-release-specific channels in
connection with intracellular signalling mechanisms. Two
distinct families of intracellular Ca
2+
-release channels,
ryanodine receptors (RyRs) and inositol (1,4,5)-trisphosphate
receptors [Ins(1,4,5)P
3
Rs] are known (Sorrentino et al., 2000;
Patel et al., 1999). In cells, like neurons and muscle cells,
where Ca
2+
-mediated signalling is highly developed, these
Ca
2+
-release proteins are selectively localised to specific
regions of the cells (Franzini-Armstrong and Protasi, 1997;
Golovina and Blaustein, 1997; Petersen et al., 2001). The
sarcoplasmic reticulum of skeletal muscle cells is a highly
organised network of tubules that is well characterised with
respect to the redistribution of proteins involved in Ca
2+
homeostasis. In this context, RyRs are selectively localised in
the region of the junctional membranes of the terminal
cisternae (i.e. the part of the sarcoplasmic reticulum facing the
t-tubule). RyRs appear to be part of a large multi-protein
complex, where calsequestrin, triadin, junctin are the best-
characterised components. By contrast, SERCAs are mainly
excluded from junctional membranes and are found mostly in
the longitudinal SR (Franzini-Armstrong and Protasi, 1997).
Selective redistribution of intracellular Ca
2+
-release channels
within the endoplasmic reticulum of neurons has been reported
(Berridge, 1998). In pancreatic acinar cells, co-localisation of
SERCA pumps and intracellular Ca
2+
-release channels seems
to be discontinuous in most of the endoplasmic reticulum, with
evidence for clustering in some regions (Petersen et al., 2001).
Obviously, the subcellular localisation of intracellular Ca
2+
-
release channels may significantly affect their contribution to
Ca
2+
signalling (Berridge et al., 1998; Berridge et al., 2000).
However, in many other cells, intracellular Ca
2+
-release
channels are less evidently restricted in their localisation within
the endoplasmic reticulum.
We report here on experiments with human HEK 293 cells
transfected with either the RyR type 1 (RYR1) or the type 3
(RyR3) isoforms. Since epithelial HEK 293 are not a cell type
specialised for RyR-mediated Ca
2+
release, we reasoned that
they might represent a good model to study the localisation and
the activity of RyR channels in a non-specialised endoplasmic
reticulum (i.e. in contrast to the sarcoplasmic reticulum). In
2497
Ryanodine receptors (RyRs) are expressed on the
endoplasmic reticulum of many cells, where they form
intracellular Ca
2+
-release channels that participate in the
generation of intracellular Ca
2+
signals. Here we report
studies on the intracellular localisation and functional
properties of transfected RyR1 or RyR3 channels in HEK
293 cells. Immunofluorescence studies indicated that both
RyR1 and RyR3 did not form clusters but were
homogeneously distributed throughout the endoplasmic
reticulum. Ca
2+
release experiments showed that
transfected RyR1 and RyR3 channels responded to
caffeine, although with different sensitivity, generating a
global release of Ca
2+
from the entire endoplasmic
reticulum. However, video imaging and confocal
microscopy analysis revealed that, in RyR3-expressing
cells, local spontaneous Ca
2+
release events were observed.
No such spontaneous activity was observed in RyR1-
expressing cells or in control cells. Interestingly, the
spontaneous release events observed in RyR3-expressing
cells were restricted to one or two regions of the
endoplasmic reticulum, suggesting the formation of a
further subcellular organisation of RyR3 in Ca
2+
release
units. These results demonstrate that different RyR
isoforms can engage in the generation of distinct
intracellular Ca
2+
signals in HEK 293 cells.
Key words: Ryanodine receptor channels, Calcium signalling,
Calcium stores, Endoplasmic sarcoplasmic reticulum, Calcium
release
Summary
RyR1 and RyR3 isoforms provide distinct intracellular
Ca
2+
signals in HEK 293 cells
Daniela Rossi
1
, Ilenia Simeoni
1
, Marcella Micheli
1
, Martin Bootman
2
, Peter Lipp
2
, Paul D. Allen
3
and
Vincenzo Sorrentino
1,
*
1
Molecular Medicine Section, Department of Neuroscience, University of Siena, via Aldo Moro 5, 53100 Siena, Italy
2
Laboratory of Molecular Signalling, The Babraham Institute, Babraham, Cambridge CB2 4AT, UK
3
Department of Anesthesia Brigham and Women’s Hospital, Boston, MA 02115, USA
*Author for correspondence (e-mail: v.sorrentino@unisi.it)
Accepted 18 March 2002
Journal of Cell Science 115, 2497-2504 (2002) © The Company of Biologists Ltd
Research Article