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1 Research Institute of Liver Disease, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430030, China; and 2 Departments of Pharmacology and Toxicology and Physiology, Medical College of Wisconsin, Milwaukee, Wisconsin 53226
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ABSTRACT |
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 TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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cADP ribose (cADPR) serves as second messenger to activate the ryanodine receptors (RyRs) of the sarcoplasmic reticulum (SR) and mobilize intracellular Ca2+ in vascular smooth muscle cells. However, the mechanisms mediating the effect of cADPR remain unknown. The present study was designed to determine whether FK-506 binding protein 12.6 (FKBP12.6), an accessory protein of the RyRs, plays a role in cADPR-induced activation of the RyRs. A 12.6-kDa protein was detected in bovine coronary arterial smooth muscle (BCASM) and cultured CASM cells by being immunoblotted with an antibody against FKBP12, which also reacted with FKBP12.6. With the use of planar lipid bilayer clamping techniques, FK-506 (0.01-10 µM) significantly increased the open probability (NPO) of reconstituted RyR/Ca2+ release channels from the SR of CASM. This FK-506-induced activation of RyR/Ca2+ release channels was abolished by pretreatment with anti-FKBP12 antibody. The RyRs activator cADPR (0.1-10 µM) markedly increased the activity of RyR/Ca2+ release channels. In the presence of FK-506, cADPR did not further increase the NPO of RyR/Ca2+ release channels. Addition of anti-FKBP12 antibody also completely blocked cADPR-induced activation of these channels, and removal of FKBP12.6 by preincubation with FK-506 and subsequent gradient centrifugation abolished cADPR-induced increase in the NPO of RyR/Ca2+ release channels. We conclude that FKBP12.6 plays a critical role in mediating cADPR-induced activation of RyR/Ca2+ release channels from the SR of BCASM.
second messenger; Ca2+ mobilization; sarcoplasmic reticulum; nucleotide
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INTRODUCTION |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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cADP RIBOSE (cADPR), a specific metabolite of nicotinamide adenine dinucleotide (NAD), mobilizes intracellular Ca2+ by a mechanism completely independent of D-myo-inositol 1,4,5-trisphosphate [Ins(1,4,5)P3]. This cADPR-mediated Ca2+ signaling participates in the regulation of a variety of physiological functions in different tissue and cells (8, 9, 14, 20, 22, 24, 28). Recent studies (18, 21, 23) have indicated that cADPR induces Ca2+ release through the activation of the ryanodine receptors (RyRs) of the sarcoplasmic reticulum (SR). However, the mechanism by which cADPR activates RyRs on the SR is poorly understood.
There is increasing evidence indicating that FK-506 binding proteins (FKBP) play an important role in the regulation of the RyRs activation and the resulting Ca2+ release from the SR (5, 6, 13). FKBP12 is a ubiquitous 12-kDa cytosolic protein. As an accessory protein, each FKBP12 can bind to one RyR monomer (1, 12, 32, 37, 38) and its activity can be inhibited by the immunosuppressants FK-506 and rapamycin (2, 7, 10, 11). It has been demonstrated (4, 39) that the Ca2+ release from the SR was inhibited when FKBP12 bound to the RyR and vice versa. FK-506, as a ligand, binds to and consequently dissociates FKBP12 from the RyRs, resulting in the RyRs activation and Ca2+ release (3). A recent study (35) reported that cADPR is able to bind to FKBP12.6-like FK-506 and results in activation of the RyRs.
In vascular smooth muscle cells (SMCs), the RyRs have been reported (15-17, 30, 31) to mediate Ins(1,4,5)P3-independent Ca2+ release from the SR and in this way participate in the control of vascular tone. Recent studies in our laboratory and by others have demonstrated that cADPR serves as an endogenous activator of the RyRs to stimulate Ca2+ release from the SR in vascular SMCs. However, the mechanism by which cADPR activates the RyRs on the SR has yet to be clarified. The present study was designed to test the hypothesis that cADPR produces Ca2+ release from the SR by binding to FKBP12.6 and consequently activating RyR/Ca2+ release channels in bovine coronary arterial smooth muscle (BCASM).
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MATERIALS AND METHODS |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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Preparation of the SR membrane and removal of FKBP12.6 from
bovine coronary arteries.
Coronary arteries were dissected from the bovine heart, and the
SR-enriched microsomes (SR membrane) of these arteries were prepared as
described previously (26). Briefly, the dissected coronary
arteries were cut into very small pieces and homogenized with Tenbroeck
tissue grinders in ice-cold 3-(N-morpholino)propanesulfonic acid (MOPS) buffer containing 0.9% NaCl, 10 mM MOPS (pH 7.0), 2 µM
leupeptin, and 0.8 µM benzamidine. The homogenate was centrifuged at
4,000 g for 20 min at 4°C and the supernatant was further
centrifuged at 8,000 g for 20 min at 4°C. The supernatant
was then collected and centrifuged at 40,000 g for 30 min,
and the pellet, termed "SR membrane," was resuspended in
buffer A composed of 0.9% NaCl, 0.3 M sucrose, 5 µg/ml
leupeptin, and phenylmethylsulfonyl fluoride (PMSF). These SR membranes
were aliquoted, frozen in liquid N2, and stored at 
80°C
until used. To remove FKBP12.6 from the RyRs, the SR membranes were
incubated with FK-506 (10 µM) in buffer A at 37°C for 15 min. FK-506 incubation mixtures were then centrifuged at 54,000 g for 15 min to remove the FK-506-FKBP12.6 complex in the
supernatant and washed once by recentrifugation using buffer A. The pellet was resuspended in buffer A at a protein
concentration of 2 mg/ml, termed "FKBP12.6-stripped SR" (1,
2). To determine whether cADPR can induce dissociation of
FKBP12.6 from the RyRs, cADPR was used to incubate with SR of BCASM and
the resultant pellet was termed "cADPR-FKBP12.6-stripped SR."
Western blot analysis. Western blot analysis was performed as described in our previous studies (25, 27). Briefly, 40 µg of proteins from cultured SMCs and SR from BCASM and FKBP12.6-stripped SR were subjected to sodium dodecyl sulfate-polyacrylamide gel electrophoresis (12% running gel) after being heated at 100°C for 5 min. The proteins were electrophoretically transferred at 30 V overnight onto a nitrocellulose membrane. The membrane was incubated with a polyclonal antibody against the synthetic FKBP12 peptide (ABR) for 6 h at room temperature. After being washed three times with Tris-buffered saline-Tween 20, the membrane was incubated for 1 h with 1:1,000 horseradish peroxidase-labeled goat anti-rabbit IgG. To detect immunoreactive bands, 2 ml of enhanced chemiluminescence detection solution 1 and 2 (1:1) (ECL; Amersham) were added directly to the blots on the surface-carrying proteins, and the membrane was wrapped in Saran Wrap and then exposed to Kodak Omat film.
Reconstitution of RyR/Ca2+ into
planar lipid bilayer.
The coronary arterial SR membranes enriched in RyR/Ca2+
release channels were reconstituted into planar lipid bilayers as we have previously described (26). In brief,
phosphatidyl-ethanolamine and phosphatidyl-serine (1:1) were dissolved
in decane (25 mg/ml) and used to form a planar lipid bilayer in a
250-µm aperture between two chambers filled with cis and
trans solutions, respectively. The SR membranes (50-100
µg protein) were added into the cis solution, which
corresponded to the cytosolic side of the SR RyR/Ca2+
release channels. The trans solution represented the luminal side of these SR RyR/Ca2+ release channels. The recording
solution in the cis chamber was 300 mM Cs+
methanesulfonate and 10 mM MOPS (pH 7.2). The trans solution was the same as cis solution except that Cs+
methanesulfonate was 50 mM before fusion and 300 mM after fusion. In
this configuration, Cs+ flows from the luminal
(trans) to the cytosolic (cis) side at negative
holding potentials. Cs+ was chosen instead of
Ca2+ as the charge carrier to precisely control
[Ca2+] around the channel, to increase the channel
conductance
(gCs+/gCa2+ = 2), and to avoid interference from K+ channels present in
the SR membrane. The Cl
channels were blocked by the
replacement of Cl with the impermeant anion methanesulfonate.
RyR/Ca2+ release channel activity was detected in a
symmetrical Cs+ methanesulfonate solution (300 mM) in all
experiments. To increase the channel activity, 1 µM free
Ca2+ in the cis solution was adjusted by adding
Ca2+ standard solution containing CaCl2 and
EGTA as previously described (26, 30).
Recordings of RyR/Ca2+ release channel currents. An Integrating Bilayer Clamp Amplifier (model BC-525C; Warner) was used to record single channel currents in the bilayer. The amplifier output signals were filtered at 1 kHz with an eight-pole Bessel filter (Frequency Devices). Currents were digitized at a sampling rate of 10 kHz and stored on a Micron Pentium III computer for off-line analysis. Data acquisition and analysis were performed with pCLAMP software (version 8, Axon Instruments). The open probability (NPO) of the channels in the lipid bilayer was determined from recordings of 3-5 min, as described previously in our patch-clamp studies (26, 29). All lipid bilayer experiments were performed at room temperature (~20°C).
With the use of this bilayer preparation, the effects of FK-506 on the activity of RyR/Ca2+ release channels were first determined. After a 3-min control recording period at holding potentials of40 mV, a series of concentrations of FK-506 was added
into the bath solution, and RyR/Ca2+ release channel
currents were recorded at each 3-min interval in the presence or
absence of anti-FKBP12 antibody. Addition of IgG in the bath solution
served as a negative control.
In another series of experiments, FK-506 was substituted for cADPR to
determine the role of FKBP12.6 in cADPR-induced activation of
RyR/Ca2+ release channels. The effects of cADPR on
RyR/Ca2+ release channel activity were also examined in the
absence or presence of FK-506 in the cis solution. To
further address whether cADPR-induced activation of the
RyR/Ca2+ release channels is associated with FKBP12.6, the
FKBP12.6-stripped SR or cADPR-FKBP12.6-stripped SR was reconstituted
into a planar lipid bilayer, and the activity of RyR/Ca2+
release channels was recorded in the presence of FK-506, cADPR, or
ryanodine, respectively. All these compounds used in these experiments
were added into the cis solution, and currents were recorded
at holding potentials at 40 mV. The concentrations of FK-506, cADPR,
and other compounds were chosen based on previous studies showing that
they effectively altered the RyRs activity (26, 31, 34,
35).
Statistics. Data are presented as means ± SE. The significance of the differences in mean values between and within multiple groups was examined using analysis of variance for repeated measures, followed by Duncan's multiple-range tests. Student's t-test was used to evaluate statistical significance of differences between two paired observations. P < 0.05 was considered statistically significant.
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RESULTS |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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Identification of FKBP12.6 in BCASM.
To confirm the presence of FKBP12.6, Western blot analysis was
performed on lysates of cultured SMCs, SR from BCASM, and
FKBP12.6-stripped SR using a polyclonal anti-FKBP12 antibody. As shown
in Fig. 1A, one 12.6-kDa
protein was recognized by this antibody in both SMC lysates and SR of
BCASM. However, this 12.6-kDa protein band was completely blocked in
the FKBP12.6-stripped SR (Fig. 1). These results suggest that FKBP12.6
was present in BCASM.
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Effect of FK-506 on activity of reconstituted
RyR/Ca2+ release channels from BCASM.
Representative recordings of RyR/Ca2+ release channels
before and after the addition of FK-506 into the cis
solution are presented in Fig.
2A. FK-506 significantly
increased the activity of these channels and resulted in subconductance
opening of these channels. As shown in Fig. 2B, FK-506 at
concentrations of 0.1-100 µmol/l produced a 1.8- to 7.1-fold
increase in the NPO of RyR/Ca2+
release channels. A significant increase was seen at the lowest concentration of FK-506 studied (0.1 µmol/l) (P < 0.05).
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Effect of anti-FKBP12 antibody on FK-506-induced activation of
reconstituted RyR/Ca2+ release channels
from BCASM.
FK-506 increased the activity of RyR/Ca2+ release channels
in the absence of the antibody against FKBP12 (1:1,000) or rabbit IgG
(Fig. 3). Pretreatment of the SR membrane
with an antibody against FKBP12.6 markedly inhibited FK-506-induced
activation of RyR/Ca2+ release channels. In contrast to
marked effect of anti-FKBP12, rabbit IgG had no effect on
FK-506-induced activation of RyR/Ca2+ release channels.
Figure 3B summarizes the effect of anti-FKBP12 and IgG on
FK-506-induced increase in the NPO of
RyR/Ca2+ release channels from BCASM. The anti-FKBP12
antibody substantially blocked the stimulatory effect of FK-506 on
RyR/Ca2+ release channels.
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Effect of anti-FKBP12 antibody on cADPR-induced activation of
reconstituted RyR/Ca2+ release channels
from BCASM.
As shown in Fig. 4, cADPR increased the
activity of RyR/Ca2+ release channels from the SR in a
concentration-related manner. It was found that pretreatment of the SR
membrane with an antibody against FKBP12 markedly inhibited
cADPR-induced activation of RyR/Ca2+ release channels (Fig.
4A). However, rabbit IgG had no effect on cADPR-induced
activation of these channels. Figure 4B summarizes the
effect of cADPR-induced increase in the NPO of
RyR/Ca2+ release channels from the SR pretreated with
anti-FKBP12 antibody or IgG. A concentration-dependent increase in the
NPO of RyR/Ca2+ release channels was
markedly blocked by anti-FKBP12 antibody.
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Effect of FK-506 on cADPR-induced activation of reconstituted SR
Ca2+ release channels from BCASM.
Figure 5 shows the effects of cADPR on
the SR RyR/Ca2+ release channels in the presence or absence
of FK-506 (10 µM). cADPR significantly increased the activity of
these channels in a concentration-dependent manner in the absence of
FK-506. In the presence of FK-506, however, cADPR-induced increase in
the NPO of RyR/Ca2+ release channels
was completely abolished, suggesting that cADPR may activate
RyR/Ca2+ release channels through the same mechanism as
FK-506.
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Effect of FKBP12.6-depletion from SR membranes on cADPR- or
FK-506-induced activation of RyR/Ca2+
release channels.
As shown in Fig. 6A, removal
of FKBP12.6 from the SR preparation by FK-506 binding and high-speed
centrifugation completely abolished the stimulatory effect of both
FK-506 and cADPR. Even the highest concentration of FK-506 or cADPR had
no effect on the activity of RyR/Ca2+ release channels in
the FKBP12.6-stripped SR preparation. However, a low concentration of
ryanodine (0.1 µM) markedly increased RyR/Ca2+ release
channel activity in this FKBP12.6-stripped SR preparation. The typical
stimulatory effect of ryanodine with subconductance opening was
observed. The NPO of these SR
RyR/Ca2+ release channels, including subconductance, was
markedly increased (Fig. 6B). As shown in Fig.
7A, removal of FKBP12.6 from
the SR preparation by cADPR also completely abolished both FK-506- and cADPR-induced activation of RyR/Ca2+ release channels.
However, a low concentration of ryanodine (0.1 µM) still markedly
increased RyR/Ca2+ release channel activity in this
cADPR-FKBP12.6-stripped SR preparation. The NPO
of these SR RyR/Ca2+ release channels, including
subconductance was markedly increased (Fig. 7B).
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DISCUSSION |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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In the present study, Western blot analysis was performed to confirm the presence of FKBP12.6, an accessory protein of the RyRs, in BCASM. A 12.6-kDa immunoreactive band was detected in both smooth muscle cell lysates and coronary arterial SR. Preincubation of SR with FK-506 completely blocked this 12.6-kDa immunoreactive band. These results provide direct evidence that FKBP12.6 is present in coronary arterial smooth muscle and the presence of FKBP12.6 may serve as a regulatory protein to control the activity of the RyRs on the SR of these SMCs.
To determine whether FKBP12.6 is involved in regulation of the RyRs on the SR of BCASM, we used lipid bilayer channel reconstitution technique to examine the effects of FK-506, a FKBP ligand on the activity of reconstituted RyR/Ca2+ release channels from the SR of BCASM. FK-506 was found to concentration-dependently increase the activity of these channels, indicating that FK-506 activates the RyRs in coronary arterial smooth muscle. These results suggest that activation of FKBP12.6 is of importance in the regulation of activity of RyR/Ca2+ release channels in BCASM.
To confirm that the effects of FK-506 on RyR/Ca2+ release channel activity of the SR are associated with FKBP12.6, a specific anti-FKBP12 antibody was added into the cis solution to examine whether FK-506-induced activation of RyR/Ca2+ release channels can be blocked. As predicted, the anti-FKBP12 antibody substantially blocked FK-506-induced activation of RyR/Ca2+ release channels, whereas IgG had no effect on the FK-506-induced activation of these channels. These findings further demonstrate that FKBP12.6 is the isoform of FKBPs that regulate the activity of RyR/Ca2+ release channels in BCASM. Recent studies (32) have indicated that there are five types of FKBPs in different mammalian cells, including FKBP12, -12.6, -13, -25, -38, and -52. FKBP12 binds to the RyRs and thereby participates in the regulation of the RyRs activation on the SR of myocardial or skeletal muscle cells (12, 32, 33, 37). It has been reported (3) that RyR/Ca2+ release channels on the SR can be inhibited when FKBP12 binds to the RyRs. FK-506, a ligand of FKBPs can bind to both FKBP12 and FKBP12.6, dissociate and release these proteins from the RyRs, whereby the RyRs are activated and Ca2+ released from the SR (35). This study demonstrates for the first time that this accessory protein is also present in vascular smooth muscle and it is functioning as an inhibitory protein of the RyRs. However, the endogenous ligand or activator of this accessory protein remains unknown. Because cADPR-induced Ca2+ release is associated with the activation of RyR/Ca2+ release channels (14, 15, 19, 26, 34-36) and cADPR cannot directly bind to the RyRs (35), we were wondering whether cADPR serves as an endogenous ligand of FKBP12.6 in vascular SMCs.
To answer this question, a series of experiments were performed to determine the role of FKBP12.6 in cADPR-induced activation of reconstituted RyR/Ca2+ release channels from BCASM. It was found that addition of cADPR into the cis solution significantly increased the NPO of these Ca2+ release channels. In the presence of anti-FKBP12 antibody, cADPR-induced activation of these channels was significantly blunted. Similarly, in the FK-506-treated bilayer, cADPR was without further effect on RyR/Ca2+ release channel activity. These results suggest that cADPR may dissociate FKBP12.6 from the RyRs and thereby activate these SR receptors. Because cADPR is produced within vascular SMCs, it may be an endogenous ligand for FKBP12.6, dissociate this protein from the RyRs, and activate RyR/Ca2+ release channels. To further confirm the role of FKBP12.6 in cADPR-induced activation of RyR/Ca2+ release channels, FKBP12.6-stripped SR membranes prepared by prebinding of FK-506 and subsequent high-speed centrifugation were used to reconstitute the RyR/Ca2+ release channels on the lipid bilayer, and the effects of cADPR on the activity of RyR/Ca2+ release channels were examined. In this FKBP12.6-stripped SR membrane, both FK-506 and cADPR had no effect on the NPO of RyR/Ca2+ release channels. This blockade of FK-506 or cADPR effect is associated with the removal of FKBP12.6 because ryanodine, a direct binding ligand of the RyRs, still activates these RyR/Ca2+ release channels. We also found that removal of FKBP12.6 from the SR membrane by cADPR completely abolished both FK-506- and cADPR-induced activation of RyR/Ca2+ release channels, but had no effect on ryanodine-induced activation of these channels. These results strongly indicate that cADPR does not work to release Ca2+ from the SR by direct binding to the RyRs and FKBP12.6 is the target of cADPR in coronary arterial SMCs. In this regard, a recent study (35) using ligand-binding techniques also demonstrated that cADPR is able to bind to FKBP12.6 in islet microsomes. The present study further provides functional evidence that cADPR activates the RyRs to release Ca2+ through FKBP12.6.
In summary, the present demonstrated that FKBP12.6 is present in BCASM and cultured SMCs and that cADPR activated RyR/Ca2+ release channels through FKBP12.6 on the SR of BCASM. These results suggest that cADPR produces Ca2+ mobilization from the SR in BCASM by stimulation of FKBP12.6 dissociation from the RyRs.
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ACKNOWLEDGEMENTS |
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The authors thank Fujisawa Healthcare for providing FK-506 for this study and Gretchen Barg for secretarial assistance.
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FOOTNOTES |
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10.1152/ajpheart.00843.2001
This study was supported by National Heart, Lung, and Blood Institute Grants HL-57244 and HL-51055. P.-L. Li is a recipient of American Heart Association Established Investigator Award 9940167N.
Address for reprint requests and other correspondence: P.-L. Li, Dept. of Pharmacology and Toxicology, Medical College of Wisconsin, 8701 Watertown Plank Rd., Milwaukee, WI 53226 (E-mail: pli{at}post.its.mcw.edu).
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
Received 28 May 2001; accepted in final form 17 December 2001.
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REFERENCES |
|---|
|
TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
|
|---|
1.
Ahern, GP,
Junankar PR,
and
Dulhunty AF.
Subconductance states in single-channel activity of skeletal muscle ryanodine receptors after removal of FKBP 12.
Biophys J
72:
146-162,
1997
2.
Ahern, GP,
Junankar PR,
and
Dulhunty AF.
Ryanodine receptors from rabbit skeletal muscle are reversibly activated by rapamycin.
Neurosci Lett
225:
81-84,
1997[ISI][Medline].
3.
Bielefeldt, K,
Sharma RV,
Whiteis C,
Yedidag E,
and
Abboud FM.
Tacrolimus (FK506) modulates calcium release and contractility of intestinal smooth muscle.
Cell Calcium
22:
507-514,
1997[ISI][Medline].
4.
Brillantes, AB,
Ondrias K,
Scott A,
Kobrinsky E,
Ondriasova E,
Moschella MC,
Jayaraman T,
Landers M,
Ehrlich BE,
and
Marks AR.
Stabilization of calcium release channel (ryanodine receptor) function by FK506-binding protein.
Cell
77:
513-523,
1994[ISI][Medline].
5.
Fleischer, S,
and
Inui M.
Biochemistry and biophysics of excitation-contraction coupling.
Ann Rev Biophys Chem
18:
333-364,
1989[ISI][Medline].
6.
Franzini-Armstrong, C,
and
Protasi F.
Ryanodine receptors of striated muscles: a complex channel capable of multiple interactions.
Pharmacol Rev
77:
699-729,
1997.
7.
Galat, A.
Peptidylproline cis-trans-isomerases: immunophilins.
Eur J Biochem
216:
689-707,
1993[ISI][Medline].
8.
Galione, A.
Cyclic ADP-ribose, the ADP-ribosyl cyclase pathway and calcium signalling.
Mol Cell Endocrinol
98:
125-131,
1994[ISI][Medline].
9.
Galione, A,
Lee HC,
and
Busa WB.
Ca2+-induced Ca2+ release in sea urchin egg homo-genates and its modulation by cyclic ADP-ribose.
Science
253:
1143-1146,
1991
10.
Harding, MW,
Galat A,
Uehling DE,
and
Schreiber SL.
A receptor for the immunosuppressant FK506 is a cis-trans peptidyl-prolyl isomerase.
Nature
341:
758-760,
1989[Medline].
11.
Ito, K,
Ikemoto T,
and
Takakura S.
Involvement of Ca2+ influx-induced Ca2+ release in contractions of intact vascular smooth muscles.
Am J Physiol Heart Circ Physiol
261:
H1464-H1470,
1991
12.
Jayaraman, T,
Brillantes AM,
Timerman AP,
Fleischer S,
Erdjument-Bromage H,
Tempst P,
and
Marks AR.
FK506 binding protein associated with the calcium release channel (ryanodine receptor).
J Biol Chem
267:
9474-9477,
1992
13.
Kamishima, T,
and
McCarron JG.
Regulation of the cytosolic Ca2+ concentration by Ca2+ stores in single smooth muscle cells from rat cerebral arteries.
J Physiol (Lond)
501:
497-508,
1997[ISI][Medline].
14.
Kannan, MS,
Fenton AM,
Prakash YS,
and
Sieck GC.
Cyclic ADP-ribose stimulates sarcoplasmic reticulum calcium release in porcine coronary artery smooth muscle.
Am J Physiol Heart Circ Physiol
270:
H801-H806,
1996
15.
Kannan, MS,
Prakash YS,
Brenner T,
Mickelson JR,
and
Sieck GC.
Role of ryanodine receptor channels in Ca2+ oscillations of porcine tracheal smooth muscle.
Am J Physiol Lung Cell Mol Physiol
272:
L659-L664,
1997
16.
Knot, HJ,
Standen NB,
and
Nelson MT.
Ryanodine receptors regulate arterial diameter and wall [Ca2+] in cerebral arteries of rat via Ca2+-dependent K+ channels.
J Physiol (Lond)
508:
211-221,
1998
17.
Lahouratate, P,
Guibert J,
and
Faivre JF.
cADP-ribose releases Ca2+ from cardiac sarcoplasmic reticulum independently of ryanodine receptor.
Am J Physiol Heart Circ Physiol
273:
H1082-H1089,
1997
18.
Lee, HC.
Specific binding of cyclic ADP-ribose to calcium-storing microsomes from sea urchin eggs.
J Biol Chem
266:
2276-2281,
1991
19.
Lee, HC.
Potentiation of calcium- and caffeine-induced calcium release by cyclic ADP-ribose.
J Biol Chem
268:
293-299,
1993
20.
Lee, HC.
Cyclic ADP-ribose: a calcium mobilazing metabolite of NAD+.
Mol Cell Biochem
138:
229-235,
1994[ISI][Medline].
21.
Lee, HC.
Multiple calcium stores: separate but interesting.
Science
40:
1,
2000.
22.
Lee, HC,
and
Aarhus R.
Wide distribution of an enzyme that catalyzes the hydrolysis of cyclic ADP-ribose.
Biochim Biophys Acta
1164:
68-74,
1993[Medline].
23.
Lee, HC,
Aarhus R,
Graeff R,
Gurnack ME,
and
Walseth TF.
Cyclic ADP ribose activation of the ryanodine receptor is mediated by calmodulin.
Nature
370:
307-309,
1994[Medline].
24.
Lee, HC,
Aarhus R,
and
Gruff RM.
Sensitization of calcium-induced calcium release by cyclic ADP-ribose and calmodulin.
J Biol Chem
270:
9060-9066,
1995
25.
Li, P-L,
Chen CL,
Bortel R,
and
Campbell WB.
11,12-Epoxyeicosatrienoic acids stimulates endogenous mono-ADP-ribosylation in bovine coronary arterial smooth muscle.
Circ Res
85:
349-356,
1999
26.
Li, P-L,
Tang WX,
Valdivia HH,
Zou AP,
and
Campbell WB.
Cyclic ADP-ribose activates reconstituted ryanodine receptors from coronary arterial smooth muscle.
Am J Physiol Heart Circ Physiol
280:
H208-H215,
2001
27.
Li, P-L,
Zou AP,
Al-kayed NJ,
Rusch NJ,
and
Harder DR.
Guanine nucleotide-binding protein in aortic smooth muscle from hypertensive rats.
Hypertension
23:
914-918,
1994
28.
Li, P-L,
Zou AP,
and
Campbell WB.
Metabolism and actions of ADP-riboses in coronary arterial smooth muscle.
Adv Exp Med Biol
419:
437-441,
1997[ISI][Medline].
29.
Li, P-L,
Zou AP,
and
Campbell WB.
Regulation of the KCa channel activity by cyclic ADP-riboses and ADP-ribose in bovine coronary arterial smooth muscle.
Am J Physiol Heart Circ Physiol
275:
H1002-H1010,
1998
30.
Lokuta, AJ,
Meyers MB,
Sander PR,
Fishman GI,
and
Valdivia HH.
Modulation of cardiac ryanodine receptor by sorcin.
J Biol Chem
272:
25333-25338,
1997
31.
Lynn, S,
and
Gillespie JI.
Basic properties of a novel ryanodine-sensitive, caffeine-insensitive calcium-induced calcium release mechanism in permeabilized human vascular smooth muscle cells.
FEBS Lett
367:
23-27,
1995[ISI][Medline].
32.
Marks, AR.
Cellular function of immunophilins.
Physiol Rev
76:
631-649,
1996
33.
Mayrleitner, M,
Timerman AP,
Wiederrecht G,
and
Fleischer S.
The calcium release channel of sarcoplasmic reticulum is modulated by FK-506 binding protein: effect of FKBP12 on single channel activity of the skeletal muscle ryanodine receptor.
Cell Calcium
15:
99-108,
1994[ISI][Medline].
34.
Meszaros, LG,
Bak J,
and
Chiu A.
Cyclic ADP-ribose as an endogenous regulator of the non-skeletal type ryanodine receptor Ca2+ channel.
Nature
364:
76-79,
1993[Medline].
35.
Noguchi, N,
Takasawa S,
Nata K,
Tohgo A,
Kato I,
Ikehata F,
Yonekura H,
and
Okamoto H.
Cyclic ADP-ribose binds to FK506-binding protein 12.6 to release Ca2+ from islet microsome.
J Biol Chem
272:
3133-3136,
1997
36.
Sitsapesan, R,
McGarry SJ,
and
Williams AJ.
Cyclic ADP-ribose, the ryanodine receptor and Ca2+ release.
Trends Pharmacol Sci
16:
386-391,
1995[Medline].
37.
Timerman, AP,
Ogunbumni E,
Freund E,
Wiederrecht G,
Marks AR,
and
Fleischer S.
The calcium release channel of sarcoplasmic reticulum is modulated by FK506-binding protein. Dissociation and reconstitution of FKBP12 to the calcium release channel of skeletal muscle sarcoplasmic reticulum.
J Biol Chem
268:
22992-22999,
1993
38.
Timerman, AP,
Wiederrecht G,
Marcy A,
and
Fleischer S.
Characterization of an exchange reaction between soluble FKBP12 and the FKBP ryanodine receptor complex. Modulation by FKBP mutants deficient in peptidyl-prolyl isomerase activity.
J Biol Chem
270:
2451-2459,
1995
39.
Valdivia, HH.
Modulation of intracellular Ca2+ level in the heart by sorcin and FKBP 12, two accessory proteins of ryanodine receptors.
Trends Pharmacol Sci
19:
479-482,
1998[Medline].
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