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J. Biol. Chem., Vol. 276, Issue 33, 30724-30728, August 17, 2001
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From the
Received for publication, April 25, 2001, and in revised form, May 24, 2001
Reperfusion after myocardial ischemia is
associated with a rapid influx of calcium, leading to activation of
various enzymes including calpain. Isolated perfused adult
rabbit hearts subjected to global ischemia and reperfusion were
studied. Calpain or a calpain-like activity was activated within 15 min
after reperfusion, and preconditioning suppressed calpain activation.
In contrast, caspase activation was not detected although cytochrome
c was released after ischemia and reperfusion. The
pro-apoptotic BH3-only Bcl-2 family member, Bid, was cleaved during
ischemia/reperfusion in the adult rabbit heart. Recombinant Bid was
cleaved by calpain to a fragment that was able to mediate cytochrome
c release. The calpain cleavage site was mapped to a region
within Bid that is extremely susceptible to proteolysis. These
findings suggest that there is cross-talk between apoptotic and
necrotic pathways in myocardial ischemia/reperfusion injury.
Reperfusion after ischemia is accompanied by a rapid
influx of calcium. Prevention of calcium influx is widely recognized in
order to protect the myocardium. Preconditioning, in which a brief
period of ischemia and reperfusion confers protection against a longer
episode of ischemia, preserves tissue viability through attenuation of
ionic fluxes (notably protons and calcium), preservation of energy
charge (less consumption of ATP), and a variety of less well
characterized enzymatic alterations (1-5). We have previously shown
that preconditioning attenuates cytoplasmic acidification and calcium
overload (3, 6). A variety of calcium-dependent enzymes are
activated after calcium influx, including the cysteine protease,
calpain. Calpain has been implicated as a mediator of contractile
dysfunction during ischemic injury, in part because of proteolysis of
structural proteins (7, 8). In addition, calpain has been reported to
cleave Bax to an 18-kDa fragment that mediates cytochrome c
release (9, 10), and calpain cleaves Bcl-xL to convert it
to a pro-apoptotic form (11).
Apoptosis has been reported to occur after ischemia/reperfusion injury,
indicated by DNA fragmentation and
TUNEL1 staining (12-16).
Preconditioning has been reported to reduce apoptosis (17). Caspase
activation in ischemic and reperfused rat heart has been reported using
an antibody that recognizes a neoepitope in activated caspase-3 (18).
Other studies examining apoptosis in neonatal cardiomyocytes have
described cytochrome c release and caspase activation (19,
20). In this study we report that calpain is activated shortly after
ischemia/reperfusion and that preconditioning attenuates calpain
activation. In addition, we demonstrate a connection between calpain
and mitochondrial dysfunction mediated by Bid.
Heart Perfusion and Ischemia/Reperfusion Protocol--
Male New
Zealand White rabbits (2.0-2.5 kg) were anesthetized and a midsternal
thoracotomy was performed. The heart was rapidly excised and mounted
onto a Langendorff heart perfusion apparatus using a protocol adapted
from Tsuchida et al. (21). The heart was perfused at a
constant pressure of 60 mm Hg with Krebs-Ringer buffer consisting of
(in mmol/liter) NaCl (118), KCl (4.75), KH2PO4 (1.18), MgSO4·7H2O (1.18),
CaCl2·2H2O (2.5), NaHCO3 (25),
and glucose (11). The perfusate was bubbled with a mixture of 95% O2 and 5% CO2 at 37 °C. Perfused hearts
were stabilized for 15 min and then subjected to global ischemia for 30 min by turning off the perfusion system. After 30 min of ischemia, the
perfusion system was restarted, and the hearts were reperfused for up
to 90 min. Ischemic preconditioning was induced by three 5-min cycles of no-flow ischemia and reperfusion immediately preceding the regular
ischemia and reperfusion. The efficacy of these interventions was
verified by measurement of creatine kinase release (Sigma Chemicals)
and infarct size measurement using triphenyl tetrazolium staining.2 All animal procedures
were approved by the Animal Care and Use Committee of The Scripps
Research Institute.
Preparation of Cytosolic Extracts and Mitochondria--
At the
end of perfusion, the ventricles were minced in 20 ml per heart of
ice-cold MSE buffer (225 mM mannitol, 75 mM
sucrose, 1.0 mM EGTA, 20 mM HEPES-KOH, pH 7.4).
The heart was further homogenized for 5 s at maximal power output
by PowerGen 125 (Fisher Scientific) equipped with a 10-mm diameter
rotor knife. The homogenate was centrifuged for 10 min at 600 × g to remove unbroken tissue and nuclei. The supernatant was
centrifuged twice for 10 min at 10,000 × g. The
postmitochondrial supernatant generally contains about 15 mg
protein/ml. The 10,000 × g mitochondrial pellet was
washed twice and resuspended in MSE buffer. The supernatant (crude
cytosol) was further centrifuged for 30 min at 100,000 × g to obtain particulate-free cytosol (S100) used for all
further experiments. The 10,000 × g pellet from the
previous centrifugation was resuspended in 10 ml of MSE buffer and
centrifuged for 10 min at 8,000 × g. This wash step
was repeated once. The final pellet of mitochondria was resuspended in
3 ml of MSE buffer, and the aliquots were stored at Calpain Activity Assay--
Calpain activity was measured using
50 µM Suc-Leu-Tyr-7-amino-4-methylcoumarin
(Suc-Leu-Tyr-AMC) as the substrate (Calbiochem, San Diego, CA). Cytosol
(20 µl = 100 µg of protein) was added to a 100-µl reaction
buffer (145 mM NaCl, 100 mM Tris-HCl, pH 7.3).
AMC release was measured over 1 h at room temperature by fluorimetry (Molecular Devices) using 360-nm excitation and 430-nm emission filters. Standard curves were generated for each experiment using known concentrations of AMC. Calpain activity was expressed as
nmol AMC released/min/mg protein. All measurements were made in
triplicate and repeated with extracts from hearts in two independent experiments.
Bid Cleavage Assays--
Recombinant GST-Bid (1 µg) was added
to cytosol containing cardiac lysate (200 µg), recombinant caspase-8
(Pharmingen), or calpain I (Calbiochem) (1 µg) as specified and
incubated for 1 h at 30 °C. The reaction mixtures were boiled
in sample buffer, resolved by electrophoresis on 16% polyacrylamide
gels (Novex), and detected by immunoblotting.
Bid-mediated Cytochrome c Release Assay--
GST-Bid (50 ng) and
calpain I (1 µg) were added to a 10-µl reaction buffer consisting
of 300 mM sucrose, 20 mM MOPS, 1 mM EGTA, and 0.1% bovine serum albumin, pH 7.4 in the presence of 2 mM Ca2+. After 1 h incubation at 30 °C,
4 mM EDTA was added to chelate Ca2+.
Mitochondria (100 µg of protein) prepared from Jurkat cells by
nitrogen cavitation were added to the reaction mixture and further
incubated for 10 min at 30 °C. Mitochondria were pelleted by
centrifugation at 10,000 × g for 10 min, and the
supernatant and pellet were assessed by immunoblotting for cytochrome
c. The concentration of GST-Bid used in these assays was
determined by titration to be insufficient to induce cytochrome
c release without proteolytic activation.
Western Blot Analysis--
Samples containing equal amounts of
protein were subjected to electrophoresis on 4-20% gradient
polyacrylamide gels (Novex) and then transferred to nitrocellulose
membrane (Millipore Corp). After blocking in 5% nonfat milk and 0.05%
Tween 20 in phosphate-buffered saline, blots were incubated with
antibodies to cytochrome c (Pharmingen) and Bid and a signal
amplification system (Vector Labs). Polyclonal anti-Bid antiserum was
generated in rabbits using as immunogen NH2-CSDNSFRRELDALGHELPVLAPQ-amide peptide corresponding to
residues 28-50 of huBid and coupled via the N-terminal cysteine
residue to maleimide-activated ovalbumin (OVA) (Pierce, Inc.). New
Zealand White female rabbits were injected subcutaneously with a
mixture of 0.25 ml of OVA-peptide (1 mg/ml) and 0.5 ml of Freund's
complete adjuvant (dose divided over 10 injections sites) and then
boosted 3 times at weekly intervals followed by another 3-20 boosts at monthly intervals with 0.25 mg of OVA-peptide in Freund's incomplete adjuvant, before collecting blood and obtaining immune serum. The Bid
antibody was used at a dilution of 1:1000.
We utilized a model of global ischemia in the isolated
buffer-perfused rabbit hearts to evaluate biochemical events of cell death. We established that ischemic preconditioning, consisting of 3 cycles of 5 min of no-flow ischemia and 5 min of recovery, was able to
protect the heart against a 30-min ischemic episode followed by
reperfusion, as measured by creatine kinase release and reduction of
infarct size (Fig. 1). We used this model
to determine early events in the cell death pathway initiated by ischemia and to examine whether preconditioning would modulate those
events.
At the time of reperfusion, intracellular calcium levels rise steeply
(24, 25). Preconditioning has been shown to attenuate calcium
elevations (5), and measures that prevent calcium influx have also been
shown to be cardioprotective (5). Calpain is a cysteine protease that
undergoes autocatalytic processing in the presence of calcium, which
thus renders it independent of calcium. Calpains are also negatively
regulated by calpastatin. In the heart, a calpastatin homolog
high-molecular-weight calmodulin-binding protein (HMWCaMBP) has been
shown to undergo proteolysis by calpains during ischemia/reperfusion,
resulting in diminished calpain inhibitory activity (26, 27).
Consistent with many earlier reports, we found that calcium-independent
calpain or calpain-like activity could be detected in lysates from
ischemic but not control hearts after 15 min of reperfusion (Fig.
2). Preconditioning attenuated calpain
activity, suggesting that calpain may be an important determinant of
myocardial injury. Additional evidence that calpain is active at this
early time point is reflected in the cleavage of
Bid Is Cleaved by Calpain to an Active Fragment in
Vitro and during Myocardial Ischemia/Reperfusion*
,,,¶
Scripps Research Institute and the
§ Burnham Institute, La Jolla, California 92037
ABSTRACT
TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
INTRODUCTION
TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
MATERIALS AND METHODS
TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
80 °C. All
operations were carried out on ice or at 4 °C. Jurkat cell cells
were disrupted by nitrogen cavitation and cytosol and mitochondria were
prepared as previously described (23).
RESULTS
TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
View larger version (20K):
[in a new window]
Fig. 1.
Creatine kinase release after ischemia.
Creatine kinase released into the coronary outflow was measured for 15 min before ischemia and for the first 15 min of reperfusion after
ischemia (I/R) or preconditioned ischemia
(P/I/R). Control hearts (con) were perfused
continuously for the same amount of time. Mean and S.D. from four
hearts per condition are shown.
-spectrin in
ischemic lysates (Fig. 2, inset).
View larger version (15K):
[in a new window]
Fig. 2.
Calpain activation after
ischemia/reperfusion. Cleavage of the calpain substrate
Suc-Leu-Tyr-AMC was followed fluorometrically using 100 µg of
cytosolic extracts obtained from control (Con), ischemic
(I/R), and preconditioned (P/I/R) hearts after 15 min of reperfusion. The activity measured was fully inhibited by ALLN
but not ZVAD (not shown). Plots shown are averages (±S.E.) of
triplicates in separate experiments using independent sets of hearts.
Analysis of variance was used to determine p values (*,
p < 0.01; **, p < 0.05). The
inset demonstrates proteolysis of -spectrin in ischemic
lysates compared with control and preconditioned hearts. The antibody
does not detect fragments.
In contrast to the strong activation of calpain at this early time
point, we could not detect any evidence of caspase activation. DEVD-AMC
cleavage revealed no caspase activity, although latent caspase-3-like
activity could be revealed by the addition of catalytic amounts of
Granzyme B (Fig. 3). Immunoblotting for
caspase-9 and caspase-3 also failed to demonstrate proteolytic
processing after 15 and 90 min reperfusion (data not shown). However,
the amount of cytochrome c was increased in cytosol of
hearts subjected to 30 min of ischemia and 15 min of reperfusion (Fig.
4).
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We considered that calpain might interact with apoptotic pathways in
ischemia. Bid, a BH3-only member of the Bcl-2 family, is capable of
mediating cytochrome c release and is expressed in heart.
Bid is cleaved by caspase-8 to generate a truncated fragment, tBid,
which is capable of translocating to the mitochondria and mediating
cytochrome c release. Accordingly, we examined whether calpain could cleave Bid. As shown in Fig.
5, recombinant GST-Bid was cleaved by
caspase-8 or calpain I. GST-Bid cleavage by calpain gave rise to
fragments that were similar in size but not identical to those
generated by caspase-8 (Fig. 5). Sequencing of the amino terminus of
the fragment that differed in size from the caspase-8 fragments yielded
the sequence RIEA, which lies within the "bait loop" that has been
shown to be the region of cleavage by caspase-8, lysosomal proteases,
and granzyme B (Table I) (28).
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However, it was necessary to establish whether the calpain-cleaved Bid
fragments were capable of mediating cytochrome c release. We
determined the concentration of recombinant GST-Bid that was unable to
cause cytochrome c release without prior proteolytic cleavage (data not shown). This concentration of GST-Bid was then incubated with buffer, caspase-8, or calpain I in the presence of
mitochondria. After 10 min at 37 °C, the supernatant and pellet were
assessed for cytochrome c release. We found that recombinant calpain was able to cleave GST-Bid to fragments that were capable of
mediating cytochrome c release (Fig.
6). This effect could be blocked by the
early addition of ALLN (Fig. 6, lane 4). Calpain alone did
not cause cytochrome c release (not shown).
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Consistent with the observation that calpain-like activity is increased
with ischemia/reperfusion and with the demonstration that calpain could
cleave Bid in vitro to an active fragment, we were able to
detect proteolytic processing of Bid in cytosol from hearts subjected
to global ischemia and reperfusion (Fig. 7). The size of the processed fragments
corresponded closely to that observed in vitro for
calpain-mediated cleavage. Thus, calpain-mediated processing of Bid may
be responsible for cytochrome c release and subsequent
mitochondrial dysfunction.
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DISCUSSION |
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ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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Ischemia and reperfusion are associated with calpain activation, a finding that has been reported by many other groups. Recent interest has focused on biochemical pathways of apoptosis, and caspase activation has been reported to occur in ischemic and reperfused rat hearts (18). In these studies, we focused on early time points, because the commitment to cell death is made quite early. We were unable to detect caspase activation at these early time points. However, calpain activity was apparent as early as 15 min of reperfusion, and calcium-independent calpain activity was attenuated in preconditioned hearts. This observation underscores the importance of calpain in ischemic injury. Calpain exists as an inactive proenzyme consisting of 80-kDa and 29-kDa subunits, which undergo autolytic processing in the presence of calcium to 78-kDa and 18-kDa fragments, thereby greatly diminishing their requirement for calcium (reviewed in Ref. 29). Calpain is further regulated by association with an inhibitor, calpastatin, which can be degraded by calpain. Recently it was reported that calpastatin immunoreactivity and inhibitory activity was diminished in ischemic heart tissue (26, 27). It has already been shown that reperfusion is associated with a brisk drop in intracellular pH and an associated rise in calcium. Preconditioning suppresses these ionic alterations and would therefore be expected to attenuate calpain activation, as we have observed (3, 6).
We demonstrated that in vitro, calpain could cleave recombinant human Bid at a site that is consistent with the consensus site for calpain, which is characterized by Leu, Val, or Ile in the P2 position. However, the Leu is not conserved between mouse and human Bid, and it remains to be established whether Bid is generally a calpain substrate. The sequence of Bid in rabbits is not known. The site of cleavage lies within the "bait loop" between helix 2 and helix 3, which by virtue of its low-order structure is readily accessible to proteases. As suggested by Salvesen (28), Bid may serve as a general sensor of intracellular protease activation. Calpain has also been shown to cleave Bax to an 18-kDa fragment that is better able to bind to mitochondria and cause cytochrome c release (9, 10) and can also cleave Bcl-xL to a pro-apoptotic fragment (11). Cross-talk between necrotic (calpain) and apoptotic (caspase) pathways is complex. Calpain cleaves caspase-9 and -3, rendering them inactive. In contrast, calpain has been suggested to cleave and activate caspase-12 (11, 30).
We show that calpain is able to cleave Bid to its active form, leading
to cytochrome c release from mitochondria. Regardless of
whether cytochrome c serves to activate downstream caspases in the heart, the loss of cytochrome c from mitochondria is
likely to impair respiration. Release of additional resident proteins of the intermembrane space, including AIF, SMAC, and CIDE-B may contribute to apoptosis (31-34). Loss of mitochondrial metabolites such as NADH and enzymes such as creatine kinase will additionally impair ATP production by both mitochondria and glycolysis (35). Consistent with this, cytochrome c-dependent
respiration has been shown to be impaired in mitochondria from ischemic
and reperfused hearts (36, 37). Moreover, cytochrome c
release has been recognized to be a feature of ischemic injury for over
two decades (38, 39). Whereas Bid, a death-promoting member of the
Bcl-2 family, has been recognized to be an important signal
intermediate in some forms of apoptosis, its role in myocardial cell
death (necrosis or apoptosis) has not been examined. Bcl-2
overexpression has been shown to protect against some necrotic insults
(40), perhaps through its ability to antagonize the action of Bid.
However, it remains to be shown whether Bcl-2 or Bcl-xL is
able to bind and antagonize Bid generated by calpain proteolysis. These
findings link calcium influx and calpain activation to the
mitochondrial apoptotic pathway. The proposed pathway to cell death in
ischemic heart is shown in Fig. 8. Taken
together, these findings implicate calpain cleavage of Bid as a point
of cross-talk between ionic disturbances and apoptosis in myocardial
ischemia/reperfusion injury.
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ACKNOWLEDGEMENTS |
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The cDNA for GST-Bid was kindly provided by Tilman Oltersdorf of Idun Pharmaceuticals (La Jolla, CA). We thank the Scripps Research Institute Protein Core Facility for protein sequencing services. Oligonucleotide synthesis and DNA sequencing were performed in the Molecular and Experimental Medicine DNA Core Facility supported by the Sam and Rose Stein Endowment Fund. We gratefully acknowledge thoughtful discussions with Dr. Guy Salvesen (Burnham Institute).
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FOOTNOTES |
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* This work was supported in part by National Institutes of Health Grant 60590, the Pew Scholars in Biomedical Sciences Program (to R. A. G.) and National Institutes of Health Grant NS36821 (to S. K.).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.
¶ To whom correspondence should be addressed: Molecular & Experimental Medicine, MEM220, The Scripps Research Inst., 10550 North Torrey Pines Rd., La Jolla, CA 92037. Tel.: 858-784-9165; Fax: 858-784-8389; E-mail: robbieg@scripps.edu.
Published, JBC Papers in Press, June 12, 2001, DOI 10.1074/jbc.M103701200
2 J. M. Downey, www.usouthal.edu/ishr/help/ttc/2000.
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ABBREVIATIONS |
|---|
The abbreviations used are: TUNEL, terminal deoxynucleotidyl transferase dUTP nick-end labeling; MOPS, 4-morpholinepropanesulfonic acid; OVA, ovalbumin; GST, glutathione S-transferase; AMC, amino-4-methylcoumarin.
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ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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 Y. C. Jin, K. J. Kim, Y. M. Kim, Y. M. Ha, H. J. Kim, U. J. Yun, K. H. Bae, Y. S. Kim, S. S. Kang, H. G. Seo, et al. Anti-Apoptotic Effect of Magnolol in Myocardial Ischemia and Reperfusion Injury Requires Extracellular Signal-Regulated Kinase1/2 Pathways in Rat In Vivo Experimental Biology and Medicine, October 1, 2008; 233(10): 1280 - 1288. [Abstract] [Full Text] [PDF]
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 J. P. French, K. L. Hamilton, J. C. Quindry, Y. Lee, P. A. Upchurch, and S. K. Powers Exercise-induced protection against myocardial apoptosis and necrosis: MnSOD, calcium-handling proteins, and calpain FASEB J, August 1, 2008; 22(8): 2862 - 2871. [Abstract] [Full Text] [PDF]
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 E. Murphy and C. Steenbergen Mechanisms Underlying Acute Protection From Cardiac Ischemia-Reperfusion Injury Physiol Rev, April 1, 2008; 88(2): 581 - 609. [Abstract] [Full Text] [PDF]
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 P. S. Tang, M. Mura, R. Seth, and M. Liu Acute lung injury and cell death: how many ways can cells die? Am J Physiol Lung Cell Mol Physiol, April 1, 2008; 294(4): L632 - L641. [Abstract] [Full Text] [PDF]
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A. B. Gustafsson and R. A. Gottlieb Heart mitochondria: gates of life and death Cardiovasc Res, January 15, 2008; 77(2): 334 - 343. [Abstract] [Full Text] [PDF]
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 D. P. McKernan, M. B. Guerin, C. J. O'Brien, and T. G. Cotter A Key Role for Calpains in Retinal Ganglion Cell Death Invest. Ophthalmol. Vis. Sci., December 1, 2007; 48(12): 5420 - 5430. [Abstract] [Full Text] [PDF]
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 G. Cao, J. Xing, X. Xiao, A. K. F. Liou, Y. Gao, X.-M. Yin, R. S. B. Clark, S. H. Graham, and J. Chen Critical Role of Calpain I in Mitochondrial Release of Apoptosis-Inducing Factor in Ischemic Neuronal Injury J. Neurosci., August 29, 2007; 27(35): 9278 - 9293. [Abstract] [Full Text] [PDF]
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 D. Y. Jun, J. S. Kim, H. S. Park, C. R. Han, Z. Fang, M. H. Woo, I. K. Rhee, and Y. H. Kim Apoptogenic activity of auraptene of Zanthoxylum schinifolium toward human acute leukemia Jurkat T cells is associated with ER stress-mediated caspase-8 activation that stimulates mitochondria-dependent or -independent caspase cascade Carcinogenesis, June 1, 2007; 28(6): 1303 - 1313. [Abstract] [Full Text] [PDF]
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 A. S. Galvez, A. Diwan, A. M. Odley, H. S. Hahn, H. Osinska, J. G. Melendez, J. Robbins, R. A. Lynch, Y. Marreez, and G. W. Dorn II Cardiomyocyte Degeneration With Calpain Deficiency Reveals a Critical Role in Protein Homeostasis Circ. Res., April 13, 2007; 100(7): 1071 - 1078. [Abstract] [Full Text] [PDF]
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 E. Y. Yuen, Z. Gu, and Z. Yan Calpain regulation of AMPA receptor channels in cortical pyramidal neurons J. Physiol., April 1, 2007; 580(1): 241 - 254. [Abstract] [Full Text] [PDF]
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 A. B. Gustafsson and R. A. Gottlieb Bcl-2 family members and apoptosis, taken to heart Am J Physiol Cell Physiol, January 1, 2007; 292(1): C45 - C51. [Abstract] [Full Text] [PDF]
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Q. Chen, A. K. S. Camara, D. F. Stowe, C. L. Hoppel, and E. J. Lesnefsky Modulation of electron transport protects cardiac mitochondria and decreases myocardial injury during ischemia and reperfusion Am J Physiol Cell Physiol, January 1, 2007; 292(1): C137 - C147. [Abstract] [Full Text] [PDF]
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 Q. Chen, S. Moghaddas, C. L. Hoppel, and E. J. Lesnefsky Reversible Blockade of Electron Transport during Ischemia Protects Mitochondria and Decreases Myocardial Injury following Reperfusion J. Pharmacol. Exp. Ther., December 1, 2006; 319(3): 1405 - 1412. [Abstract] [Full Text] [PDF]
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D. D. Arrington, T. R. Van Vleet, and R. G. Schnellmann Calpain 10: a mitochondrial calpain and its role in calcium-induced mitochondrial dysfunction Am J Physiol Cell Physiol, December 1, 2006; 291(6): C1159 - C1171. [Abstract] [Full Text] [PDF]
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N. Shulga and J. G. Pastorino Acyl Coenzyme A-binding Protein Augments Bid-induced Mitochondrial Damage and Cell Death by Activating {micro}-Calpain J. Biol. Chem., October 13, 2006; 281(41): 30824 - 30833. [Abstract] [Full Text] [PDF]
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Y. Tan, C. Wu, T. De Veyra, and P. A. Greer Ubiquitous Calpains Promote Both Apoptosis and Survival Signals in Response to Different Cell Death Stimuli J. Biol. Chem., June 30, 2006; 281(26): 17689 - 17698. [Abstract] [Full Text] [PDF]
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 K. Fettucciari, I. Fetriconi, R. Mannucci, I. Nicoletti, A. Bartoli, S. Coaccioli, and P. Marconi Group B streptococcus induces macrophage apoptosis by calpain activation. J. Immunol., June 15, 2006; 176(12): 7542 - 7556. [Abstract] [Full Text] [PDF]
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Y. Tan, N. Dourdin, C. Wu, T. De Veyra, J. S. Elce, and P. A. Greer Ubiquitous Calpains Promote Caspase-12 and JNK Activation during Endoplasmic Reticulum Stress-induced Apoptosis J. Biol. Chem., June 9, 2006; 281(23): 16016 - 16024. [Abstract] [Full Text] [PDF]
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D. Garcia-Dorado, A. Rodriguez-Sinovas, M. Ruiz-Meana, J. Inserte, L. Agullo, and A. Cabestrero The end-effectors of preconditioning protection against myocardial cell death secondary to ischemia-reperfusion Cardiovasc Res, May 1, 2006; 70(2): 274 - 285. [Abstract] [Full Text] [PDF]
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M. W. Ward, M. Rehm, H. Duessmann, S. Kacmar, C. G. Concannon, and J. H. M. Prehn Real Time Single Cell Analysis of Bid Cleavage and Bid Translocation during Caspase-dependent and Neuronal Caspase-independent Apoptosis J. Biol. Chem., March 3, 2006; 281(9): 5837 - 5844. [Abstract] [Full Text] [PDF]
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K. von Wnuck Lipinski, P. Keul, S. Lucke, G. Heusch, J. Wohlschlaeger, H. A. Baba, and B. Levkau Degraded collagen induces calpain-mediated apoptosis and destruction of the X-chromosome-linked inhibitor of apoptosis (xIAP) in human vascular smooth muscle cells Cardiovasc Res, February 15, 2006; 69(3): 697 - 705. [Abstract] [Full Text] [PDF]
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C. Quiniou, F. Sennlaub, M. H. Beauchamp, D. Checchin, I. Lahaie, S. Brault, F. Gobeil Jr., M. Sirinyan, A. Kooli, P. Hardy, et al. Dominant Role for Calpain in Thromboxane-Induced Neuromicrovascular Endothelial Cytotoxicity J. Pharmacol. Exp. Ther., February 1, 2006; 316(2): 618 - 627. [Abstract] [Full Text] [PDF]
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Q. Chen, C. L. Hoppel, and E. J. Lesnefsky Blockade of Electron Transport before Cardiac Ischemia with the Reversible Inhibitor Amobarbital Protects Rat Heart Mitochondria J. Pharmacol. Exp. Ther., January 1, 2006; 316(1): 200 - 207. [Abstract] [Full Text] [PDF]
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Q. Wei, X.-M. Yin, M.-H. Wang, and Z. Dong Bid deficiency ameliorates ischemic renal failure and delays animal death in C57BL/6 mice Am J Physiol Renal Physiol, January 1, 2006; 290(1): F35 - F42. [Abstract] [Full Text] [PDF]
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J. P. French, J. C. Quindry, D. J. Falk, J. L. Staib, Y. Lee, K. K. W. Wang, and S. K. Powers Ischemia-reperfusion-induced calpain activation and SERCA2a degradation are attenuated by exercise training and calpain inhibition Am J Physiol Heart Circ Physiol, January 1, 2006; 290(1): H128 - H136. [Abstract] [Full Text] [PDF]
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 H. H. Boersma, B. L.J.H. Kietselaer, L. M.L. Stolk, A. Bennaghmouch, L. Hofstra, J. Narula, G. A.K. Heidendal, and C. P.M. Reutelingsperger Past, Present, and Future of Annexin A5: From Protein Discovery to Clinical Applications J. Nucl. Med., December 1, 2005; 46(12): 2035 - 2050. [Abstract] [Full Text] [PDF]
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H.-Y. Wu, E. Y. Yuen, Y.-F. Lu, M. Matsushita, H. Matsui, Z. Yan, and K. Tomizawa Regulation of N-Methyl-D-aspartate Receptors by Calpain in Cortical Neurons J. Biol. Chem., June 3, 2005; 280(22): 21588 - 21593. [Abstract] [Full Text] [PDF]
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R. Gottlieb ICE-ing the Heart Circ. Res., May 27, 2005; 96(10): 1036 - 1038. [Full Text] [PDF]
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 C. Leeuwenburgh, C. M. Gurley, B. A. Strotman, and E. E. Dupont-Versteegden Age-related differences in apoptosis with disuse atrophy in soleus muscle Am J Physiol Regulatory Integrative Comp Physiol, May 1, 2005; 288(5): R1288 - R1296. [Abstract] [Full Text] [PDF]
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D. Zhai, F. Luciano, X. Zhu, B. Guo, A. C. Satterthwait, and J. C. Reed Humanin Binds and Nullifies Bid Activity by Blocking Its Activation of Bax and Bak J. Biol. Chem., April 22, 2005; 280(16): 15815 - 15824. [Abstract] [Full Text] [PDF]
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J. Takano, M. Tomioka, S. Tsubuki, M. Higuchi, N. Iwata, S. Itohara, M. Maki, and T. C. Saido Calpain Mediates Excitotoxic DNA Fragmentation via Mitochondrial Pathways in Adult Brains: EVIDENCE FROM CALPASTATIN MUTANT MICE J. Biol. Chem., April 22, 2005; 280(16): 16175 - 16184. [Abstract] [Full Text] [PDF]
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C.-Y. Xiao, M. Chen, Z. Zsengeller, H. Li, L. Kiss, M. Kollai, and C. Szabo Poly(ADP-Ribose) Polymerase Promotes Cardiac Remodeling, Contractile Failure, and Translocation of Apoptosis-Inducing Factor in a Murine Experimental Model of Aortic Banding and Heart Failure J. Pharmacol. Exp. Ther., March 1, 2005; 312(3): 891 - 898. [Abstract] [Full Text] [PDF]
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 C. Vindis, M. Elbaz, I. Escargueil-Blanc, N. Auge, A. Heniquez, J.-C. Thiers, A. Negre-Salvayre, and R. Salvayre Two Distinct Calcium-Dependent Mitochondrial Pathways Are Involved in Oxidized LDL-Induced Apoptosis Arterioscler. Thromb. Vasc. Biol., March 1, 2005; 25(3): 639 - 645. [Abstract] [Full Text] [PDF]
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B. M. Polster, G. Basanez, A. Etxebarria, J. M. Hardwick, and D. G. Nicholls Calpain I Induces Cleavage and Release of Apoptosis-inducing Factor from Isolated Mitochondria J. Biol. Chem., February 25, 2005; 280(8): 6447 - 6454. [Abstract] [Full Text] [PDF]
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L. R. Aminova, J. C. Chavez, J. Lee, H. Ryu, A. Kung, J. C. LaManna, and R. R. Ratan Prosurvival and Prodeath Effects of Hypoxia-inducible Factor-1{alpha} Stabilization in a Murine Hippocampal Cell Line J. Biol. Chem., February 4, 2005; 280(5): 3996 - 4003. [Abstract] [Full Text] [PDF]
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C. L. Murriel, E. Churchill, K. Inagaki, L. I. Szweda, and D. Mochly-Rosen Protein Kinase C{delta} Activation Induces Apoptosis in Response to Cardiac Ischemia and Reperfusion Damage: A MECHANISM INVOLVING BAD AND THE MITOCHONDRIA J. Biol. Chem., November 12, 2004; 279(46): 47985 - 47991. [Abstract] [Full Text] [PDF]
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M. T. Crow, K. Mani, Y.-J. Nam, and R. N. Kitsis The Mitochondrial Death Pathway and Cardiac Myocyte Apoptosis Circ. Res., November 12, 2004; 95(10): 957 - 970. [Abstract] [Full Text] [PDF]
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H. Yamaguchi, J. Chen, K. Bhalla, and H.-G. Wang Regulation of Bax Activation and Apoptotic Response to Microtubule-damaging Agents by p53 Transcription-dependent and -independent Pathways J. Biol. Chem., September 17, 2004; 279(38): 39431 - 39437. [Abstract] [Full Text] [PDF]
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E. J. Lesnefsky, Q. Chen, T. J. Slabe, M. S. K. Stoll, P. E. Minkler, M. O. Hassan, B. Tandler, and C. L. Hoppel Ischemia, rather than reperfusion, inhibits respiration through cytochrome oxidase in the isolated, perfused rabbit heart: role of cardiolipin Am J Physiol Heart Circ Physiol, July 1, 2004; 287(1): H258 - H267. [Abstract] [Full Text] [PDF]
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 T.-H. Kim, Y. Zhao, W.-X. Ding, J. N. Shin, X. He, Y.-W. Seo, J. Chen, H. Rabinowich, A. A. Amoscato, and X.-M. Yin Bid-Cardiolipin Interaction at Mitochondrial Contact Site Contributes to Mitochondrial Cristae Reorganization and Cytochrome c Release Mol. Biol. Cell, July 1, 2004; 15(7): 3061 - 3072. [Abstract] [Full Text] [PDF]
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J. Gafni, E. Hermel, J. E. Young, C. L. Wellington, M. R. Hayden, and L. M. Ellerby Inhibition of Calpain Cleavage of Huntingtin Reduces Toxicity: ACCUMULATION OF CALPAIN/CASPASE FRAGMENTS IN THE NUCLEUS J. Biol. Chem., May 7, 2004; 279(19): 20211 - 20220. [Abstract] [Full Text] [PDF]
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Q. Wei, M. M. Alam, M.-H. Wang, F. Yu, and Z. Dong Bid activation in kidney cells following ATP depletion in vitro and ischemia in vivo Am J Physiol Renal Physiol, April 1, 2004; 286(4): F803 - F809. [Abstract] [Full Text] [PDF]
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H.-Y. Wu, K. Tomizawa, Y. Oda, F.-Y. Wei, Y.-F. Lu, M. Matsushita, S.-T. Li, A. Moriwaki, and H. Matsui Critical Role of Calpain-mediated Cleavage of Calcineurin in Excitotoxic Neurodegeneration J. Biol. Chem., February 6, 2004; 279(6): 4929 - 4940. [Abstract] [Full Text] [PDF]
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T. Cirman, K. Oresic, G. D. Mazovec, V. Turk, J. C. Reed, R. M. Myers, G. S. Salvesen, and B. Turk Selective Disruption of Lysosomes in HeLa Cells Triggers Apoptosis Mediated by Cleavage of Bid by Multiple Papain-like Lysosomal Cathepsins J. Biol. Chem., January 30, 2004; 279(5): 3578 - 3587. [Abstract] [Full Text] [PDF]
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 T. Zhang, S. Miyamoto, and J. H. Brown Cardiomyocyte Calcium and Calcium/Calmodulin-dependent Protein Kinase II: Friends or Foes? Recent Prog. Horm. Res., January 1, 2004; 59(1): 141 - 168. [Abstract] [Full Text]
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D. M. Valks, T. J. Kemp, and A. Clerk Regulation of Bcl-xL Expression by H2O2 in Cardiac Myocytes J. Biol. Chem., July 3, 2003; 278(28): 25542 - 25547. [Abstract] [Full Text] [PDF]
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M. D. Esposti, G. Ferry, P. Masdehors, J. A. Boutin, J. A. Hickman, and C. Dive Post-translational Modification of Bid Has Differential Effects on Its Susceptibility to Cleavage by Caspase 8 or Caspase 3 J. Biol. Chem., April 25, 2003; 278(18): 15749 - 15757. [Abstract] [Full Text] [PDF]
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S. Gil-Parrado, O. Popp, T. A. Knoch, S. Zahler, F. Bestvater, M. Felgentrager, A. Holloschi, A. Fernandez-Montalvan, E. A. Auerswald, H. Fritz, et al. Subcellular Localization and in Vivo Subunit Interactions of Ubiquitous {micro}-Calpain J. Biol. Chem., April 25, 2003; 278(18): 16336 - 16346. [Abstract] [Full Text] [PDF]
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R. W. Neumar, Y. A. Xu, H. Gada, R. P. Guttmann, and R. Siman Cross-talk between Calpain and Caspase Proteolytic Systems During Neuronal Apoptosis J. Biol. Chem., April 11, 2003; 278(16): 14162 - 14167. [Abstract] [Full Text] [PDF]
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 H. Yamaguchi, K. Bhalla, and H.-G. Wang Bax Plays a Pivotal Role in Thapsigargin-induced Apoptosis of Human Colon Cancer HCT116 Cells by Controlling Smac/Diablo and Omi/HtrA2 Release from Mitochondria Cancer Res., April 1, 2003; 63(7): 1483 - 1489. [Abstract] [Full Text] [PDF]
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R. Sarig, Y. Zaltsman, R. C. Marcellus, R. Flavell, T. W. Mak, and A. Gross BID-D59A Is a Potent Inducer of Apoptosis in Primary Embryonic Fibroblasts J. Biol. Chem., March 14, 2003; 278(12): 10707 - 10715. [Abstract] [Full Text] [PDF]
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T. L. Vanden Hoek, Y. Qin, K. Wojcik, C.-Q. Li, Z.-H. Shao, T. Anderson, L. B. Becker, and K. J. Hamann Reperfusion, not simulated ischemia, initiates intrinsic apoptosis injury in chick cardiomyocytes Am J Physiol Heart Circ Physiol, January 1, 2003; 284(1): H141 - H150. [Abstract] [Full Text] [PDF]
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S. Kobayashi, K. Yamashita, T. Takeoka, T. Ohtsuki, Y. Suzuki, R. Takahashi, K. Yamamoto, S. H. Kaufmann, T. Uchiyama, M. Sasada, et al. Calpain-mediated X-linked Inhibitor of Apoptosis Degradation in Neutrophil Apoptosis and Its Impairment in Chronic Neutrophilic Leukemia J. Biol. Chem., September 6, 2002; 277(37): 33968 - 33977. [Abstract] [Full Text] [PDF]
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B. H. Han, D. Xu, J. Choi, Y. Han, S. Xanthoudakis, S. Roy, J. Tam, J. Vaillancourt, J. Colucci, R. Siman, et al. Selective, Reversible Caspase-3 Inhibitor Is Neuroprotective and Reveals Distinct Pathways of Cell Death after Neonatal Hypoxic-ischemic Brain Injury J. Biol. Chem., August 9, 2002; 277(33): 30128 - 30136. [Abstract] [Full Text] [PDF]
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 A. Robert, M.-J. Miron, C. Champagne, M.-C. Gingras, P. E. Branton, and J. N. Lavoie Distinct cell death pathways triggered by the adenovirus early region 4 ORF 4 protein J. Cell Biol., August 5, 2002; 158(3): 519 - 528. [Abstract] [Full Text] [PDF]
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M. Chen, D.-J. Won, S. Krajewski, and R. A. Gottlieb Calpain and Mitochondria in Ischemia/Reperfusion Injury J. Biol. Chem., August 2, 2002; 277(32): 29181 - 29186. [Abstract] [Full Text] [PDF]
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S. Gil-Parrado, A. Fernandez-Montalvan, I. Assfalg-Machleidt, O. Popp, F. Bestvater, A. Holloschi, T. A. Knoch, E. A. Auerswald, K. Welsh, J. C. Reed, et al. Ionomycin-activated Calpain Triggers Apoptosis. A PROBABLE ROLE FOR Bcl-2 FAMILY MEMBERS J. Biol. Chem., July 19, 2002; 277(30): 27217 - 27226. [Abstract] [Full Text] [PDF]
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Y. Ohnuma, T. Miura, T. Miki, M. Tanno, A. Kuno, A. Tsuchida, and K. Shimamoto Opening of mitochondrial KATP channel occurs downstream of PKC-epsilon activation in the mechanism of preconditioning Am J Physiol Heart Circ Physiol, July 1, 2002; 283(1): H440 - H447. [Abstract] [Full Text] [PDF]
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 A. Mandic, K. Viktorsson, L. Strandberg, T. Heiden, J. Hansson, S. Linder, and M. C. Shoshan Calpain-Mediated Bid Cleavage and Calpain-Independent Bak Modulation: Two Separate Pathways in Cisplatin-Induced Apoptosis Mol. Cell. Biol., May 1, 2002; 22(9): 3003 - 3013. [Abstract] [Full Text] [PDF]
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T. M. Scarabelli, A. Stephanou, E. Pasini, L. Comini, R. Raddino, R. A. Knight, and D. S. Latchman Different Signaling Pathways Induce Apoptosis in Endothelial Cells and Cardiac Myocytes During Ischemia/Reperfusion Injury Circ. Res., April 5, 2002; 90(6): 745 - 748. [Abstract] [Full Text] [PDF]
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C. GILL, R. MESTRIL, and A. SAMALI Losing heart: the role of apoptosis in heart disease--a novel therapeutic target? FASEB J, February 1, 2002; 16(2): 135 - 146. [Abstract] [Full Text] [PDF]
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 N. Plesnila, S. Zinkel, D. A. Le, S. Amin-Hanjani, Y. Wu, J. Qiu, A. Chiarugi, S. S. Thomas, D. S. Kohane, S. J. Korsmeyer, et al. BID mediates neuronal cell death after oxygen/ glucose deprivation and focal cerebral ischemia PNAS, December 6, 2001; (2001) 261323298. [Abstract] [Full Text] [PDF]
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N. Plesnila, S. Zinkel, D. A. Le, S. Amin-Hanjani, Y. Wu, J. Qiu, A. Chiarugi, S. S. Thomas, D. S. Kohane, S. J. Korsmeyer, et al. BID mediates neuronal cell death after oxygen/ glucose deprivation and focal cerebral ischemia PNAS, December 18, 2001; 98(26): 15318 - 15323. [Abstract] [Full Text] [PDF]
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T. M. Scarabelli, A. Stephanou, E. Pasini, L. Comini, R. Raddino, R. A. Knight, and D. S. Latchman Different Signaling Pathways Induce Apoptosis in Endothelial Cells and Cardiac Myocytes During Ischemia/Reperfusion Injury Circ. Res., April 5, 2002; 90(6): 745 - 748. [Abstract] [Full Text] [PDF]
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