INTRODUCTION
C
A
2+
-RELEASE/RYANODINE RECEPTOR CHANNELS (RyR
channels) are massive integral membrane proteins (~2.3
MDa) present in endo/sarcoplasmic reticulum membranes as
homotetramers (9). Ca
2+
release through these channels has a
central role in Ca
2+
signaling. Through Ca
2+
-induced Ca
2+
re-
lease (CICR), RyR channels can amplify Ca
2+
entry signals
and can also efficiently propagate Ca
2+
signals to other cell
locations or organelles, such as mitochondria or nuclei (35).
These properties place RyR channels at the center of several
important processes elicited by cellular Ca
2+
signals. Some of
them occur in all cells, such as apoptosis and necrosis,
whereas others are cell-specific and include events as diverse
as contraction, secretion, fertilization, and neuronal plastic-
ity. Consequently, RyR channel function is extensively regu-
lated by small ions and molecules (e.g., Ca
2+
, Mg
2+
, or ade-
nine nucleotides) and protein–protein interactions (e.g.,
calmodulin) (10, 25, 31). Additionally, RyR channels are also
regulated by phosphorylation/dephosphorylation events (28)
and by redox modifications, as detailed below.
Mammalian RyR1 channels are likely to act as cellular
redox sensors. They contain a few cysteine residues that react
with pharmacological or endogenous redox-active molecules
at physiological pH (6, 8, 32, 40, 46, 47). Moreover, RyR1
redox modifications have a profound effect on RyR1-medi-
ated Ca
2+
release and single-channel activity (14, 17, 27). Ad-
ditionally, the RyR1 protein is susceptible to S-nitrosylation
870
1
FONDAP Center for Molecular Studies of the Cell, Facultad de Medicina, Universidad de Chile, Casilla 70005, Santiago 7, Chile.
2
Department of Molecular Physiology and Biophysics, Baylor College of Medicine, Houston, TX.
Effects of S-Glutathionylation and S-Nitrosylation on
Calmodulin Binding to Triads and FKBP12 Binding to
Type 1 Calcium Release Channels
PAULA ARACENA,
1,2
WEI TANG,
2
SUSAN L. HAMILTON,
2
and CECILIA HIDALGO
1
ABSTRACT
This study shows that the combination of glutathione (GSH) plus hydrogen peroxide (H
2
O
2
) promotes the S-
glutathionylation of ryanodine receptor type 1 (RyR1) Ca
2+
release channels, and confirms their joint S-glu-
tathionylation and S-nitrosylation by S-nitrosoglutathione (GSNO). In addition, we show that
35
S-labeled 12-
kDa FK506-binding protein ([
35
S]FKBP12) bound with a K
d
of 13.1 nM to RyR1 present in triads or heavy
sarcoplasmic reticulum vesicles; RyR1 S-nitrosylation by NOR-3 or GSNO, but not S-glutathionylation, spe-
cifically increased by four- to fivefold this K
d
value. RyR1 redox modifications also increased the K
d
of
[
35
S]calmodulin binding to triads without affecting B
max
. RyR1 S-glutathionylation (induced by GSH plus
H
2
O
2
) or RyR1 S-nitrosylation (produced by NOR-3) increased by approximately six- or twofold, respectively,
the K
d
of apocalmodulin (apoCaM) or Ca
2+
-calmodulin (CaCaM) binding to triads. Likewise, the combined S-
glutathionylation and S-nitrosylation of RyR1 induced by GSNO increased by fourfold the K
d
of CaCaM
binding to triads and abolished apoCaM binding. As both FKBP12 and CaCaM inhibit RyR1, decreased
FKBP12 binding to RyR1 and/or decreased CaCaM binding to either RyR1 or dihydropyridine receptor in
triad preparations may cause the reported enhanced activation of Ca
2+
-induced Ca
2+
release kinetics medi-
ated by S-glutathionylation/S-nitrosylation. We discuss possible consequences of these redox modifications on
RyR1-mediated Ca
2+
release in physiological or pathological conditions. Antioxid. Redox Signal. 7, 870–881.
Forum Original Research Communication
ANTIOXIDANTS & REDOX SIGNALING
Volume 7, Numbers 7 & 8, 2005
© Mary Ann Liebert, Inc.