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(Received for publication, July 28, 1997)
From the Center for Apoptosis Research and the Department of
Microbiology and Immunology, Kimmel Cancer Institute, Thomas Jefferson
University, Philadelphia, Pennsylvania 19107 and the ¶ MRC
Toxicology Unit, Hodgkin Building, University of Leicester,
Leicester, LE1 9HN United Kingdom
ABSTRACT A human receptor for the cytotoxic ligand TRAIL
(TRAIL receptor-1, designated DR4) was identified recently as a member
of the tumor necrosis factor receptor family. In this report we
describe the identification of two additional human TRAIL receptors,
TRAIL receptor-2 and TRAIL receptor-3, that belong to the tumor
necrosis factor receptor family. Interestingly, TRAIL receptor-2 but
not TRAIL receptor-3 contains a cytoplasmic "death domain"
necessary for induction of apoptosis and is hence designated death
receptor-5 (DR5). Like DR4, DR5 engages the apoptotic pathway
independent of the adaptor molecule FADD/MORT1. Because of its lack of
a death domain, TRAIL receptor-3 is not capable of inducing apoptosis. However, by competing for TRAIL, it is capable of inhibiting
TRAIL-induced apoptosis. Thus, TRAIL receptor-3 may function as an
antagonistic decoy receptor to attenuate the cytotoxic effect of TRAIL
in most tissues that are TRAIL+, DR4+,
and DR5+.
INTRODUCTION Apoptosis is an intrinsic and fundamental biological process that
plays a critical role in the normal development of multicellular organisms and in maintaining tissue homeostasis (1). Consequently, deregulation of apoptosis may contribute to diseases such as cancer and
neurodegenerative disorders (2). Some of the well known regulators of
apoptosis are cytokines of the tumor necrosis factor (TNF)1 ligand family, such as
Fas ligand (Fas L) and TNF, which induce apoptosis by activation of
their corresponding receptors, Fas and TNFR-1 (3). These two receptors
belong to a rapidly expanding family (collectively known as the TNF
receptor family) containing at least 11 known members (3, 4). Members
of this family contain an extracellular ligand-binding domain, of 2-6
cysteine-rich repeats, which is about 25% conserved between different
family members. The cytoplasmic region is less conserved between
various members except for a stretch of about 80 amino acids present in Fas, TNFR-1, DR3/Wsl-1/Apo-3/TRAMP, CAR-1, and DR4 (Refs. 3 and 4 and
references therein). This intracellular region, which has been
designated the cytoplasmic "death domain," is responsible for
transducing the death signal.
Activation of Fas results in recruitment of the Fas-associated death
domain-containing molecule FADD/MORT1 to the receptor complex (5-7).
The resulting signaling complex then triggers activation of the caspase
apoptotic pathway through interaction of the N-terminal death effector
domain of FADD with the corresponding motifs in the prodomain of
caspase-8 (Mch5/MACH/FLICE) and probably caspase-10 (Mch4) (8-11). In
contrast to Fas, activation of TNFR-1 or DR3 results in recruitment of
another death domain-containing adaptor molecule known as TRADD (12,
13). TRADD can associate with a number of signaling molecules,
including FADD, TRAF2, and RIP, and as a result can transduce an
apoptotic signal as well as activate NF- Recently, a new member of the TNF family known as TRAIL or Apo-2 ligand
was identified and shown to induce apoptosis in a variety of tumor cell
lines (16-18). A human receptor for TRAIL was also recently identified
and designated DR4 (4). DR4 contains a cytoplasmic death domain, and
like Fas, it induces apoptosis but not NF- Here, we report the identification of two additional human receptors
for the cytotoxic ligand TRAIL (designated DR5 and TRAIL-R3). These
represent as yet undescribed members of the TNF receptor family.
Interestingly, DR5 but not TRAIL-R3 contains a cytoplasmic death domain
necessary for induction of apoptosis, and like DR-4, DR5 engages the
apoptotic pathway independent of the adaptor molecule FADD/MORT1.
TRAIL-R3 on the other hand, can bind TRAIL but does not induce
apoptosis and thus may function as an antagonistic receptor.
MATERIALS AND METHODS The full-length DR5 cDNA was cloned
from a human Jurkat Uni-ZAP XR cDNA library (10) by PCR using
specific primers derived from the nucleotide sequences of human
GenBankTM EST clones 650744 and 664665. Similarly, TRAIL-R3 was cloned
by PCR using specific primers derived from the nucleotide sequences of
human GenBankTM EST clones 470799, 129137, and 504745.
T7-epitope tagging was done as
described recently (19). To generate N-terminal Flag-tagged receptor
and receptor mutants, PCR-generated cDNAs encoding Fas, DR4, DR4 These were done as described recently (19).
Recombinant soluble TRAIL with
N-terminal T7 and His6 tags was obtained by nickel affinity
purification from bacteria transformed with a pET28c-TRAIL (residues 95 to 281) vector. Receptor-Fc chimeras were obtained by harvesting
conditioned media of 293 cells transfected with constructs encoding
Fas-, DR4-, DR5-, or TRAIL-R3-Fc fusion proteins as described (4).
Binding of TRAIL to the receptor-Fc chimeras was performed as described
(4).
RESULTS AND DISCUSSION To identify
additional members of the TNF receptor family, we searched the
GenBankTM EST data base for sequences that are homologous to the TRAIL
receptor-1, DR4. Several EST clones were identified, and their 3
The second cDNA encodes a protein of 299 amino acids with overall
~40 and 36% identity to DR4 and DR5, respectively (Fig. 1B). This protein contains a putative N-terminal signal
peptide (amino acids Northern blot analysis of equivalent amounts of mRNA
samples from normal human tissues and tumor cell lines with a DR5
riboprobe detected a ~4-kilobase transcript in all the samples (Fig.
1D, upper panels). Interestingly, the amount of
DR5 transcript was at least 100-fold more in most tumor cell lines than
in normal tissues. Autoradiography for less than 2 h was
sufficient to detect the DR5 message in tumor cell lines, compared with
48 h in the case of the normal tissues. Other normal tissues such
as testes, ovary, colon, small intestine, and lymphoid tissues had
detectable but low expression of DR5 transcript (not shown), similar to
that observed in the normal tissues shown in Fig. 1D. The
TRAIL-R3 riboprobe detected ~a 5-kilobase message in both normal
human tissues and tumor cell lines (Fig. 1D, lower
panels). A significantly elevated expression of TRAIL-R3 mRNA
in normal compared with tumor cells was observed. Given the activities
of these two receptors (see below), this could explain the high
sensitivity of tumor cell lines to TRAIL compared with normal cells
(16-18).
Because of the high degree of sequence homology between the
extracellular domains of DR4, DR5, and TRAIL-R3, we decided to test
whether DR5 and TRAIL-R3 are capable of binding TRAIL. The extracellular ligand-binding domains of Fas, DR4, DR5, and TRAIL-R3 were expressed as fusion proteins with the Fc region of mouse IgG (Fig.
2A, lower panel).
As shown in Fig. 2A (upper panel), DR4-Fc,
DR5-Fc, and TRAIL-R3-Fc were all capable of binding TRAIL to the same
extent (lanes DR5-Fc, DR4-Fc, and
TR3-Fc). As expected Fas-Fc was unable to bind TRAIL
(lane 4). Furthermore, DR4-Fc, DR5-Fc, and TRAIL-R3-Fc but
not Fas-Fc were capable of blocking TRAIL-induced apoptosis in MCF7
cells (Fig. 2B). These data suggest that, like DR4, DR5 and
TRAIL-R3 are receptors for TRAIL.
Ectopic
expression of death domain-containing members of the TNF receptor
family induces apoptosis in a ligand-independent manner. Consistent
with this observation, we found that transient expression of DR5 in
MCF7 or 293 cells triggers apoptosis (Fig. 3, A and B). The
level of apoptosis induction was similar to that observed with DR4.
(Fig. 3A). Induction of apoptosis was dependent on the
presence of the cytoplasmic death domain, because deletion of this
domain abolished the ability of DR4 and DR5 to induce apoptosis (Fig.
3, A and B). Accordingly, TRAIL-R3, which does not naturally contain a death domain, was also incapable of inducing apoptosis (Fig. 3, A and B). Interestingly,
transient expression of TRAIL-R3 in MCF7 cells significantly blocked
TRAIL-induced apoptosis (Fig. 3C), suggesting that it may
function as an antagonistic decoy receptor.
Like DR4 and the other TNF receptor family members, DR5-induced
apoptosis was efficiently blocked by the caspase inhibitors z-VAD-fmk
and CrmA (Fig. 3D). DR4- and DR5-induced apoptosis was also
significantly inhibited by the dominant negative inhibitors FLAME-1
(also known as Casper, FLIP, I-FLICE, and CASH) (Refs. 19 and 21 and
references therein), caspase-8-DN, and caspase-10-DN (Fig.
3E). Among these, caspase-10-DN was the most effective in blocking DR4- and DR5-induced apoptosis. Inhibition of DR4- and DR5-induced apoptosis by FLAME-1 is consistent with recent observations that TRAIL-induced apoptosis is blocked by expression of FLIP (FLAME-1)
(22). These data also suggest that the upstream caspases-8 and -10 are
involved in both the DR4 and DR5 death signaling pathways.
Death domain containing adaptor molecules such
as FADD/MORT1, CRADD/RAIDD, TRADD, and RIP are recruited by some
members of the TNF receptor family to engage the upstream caspases (3, 19). Using co-immunoprecipitation experiments, we tested if DR5 could
interact with these molecules to transmit the apoptotic signal. Unlike
Fas, DR5 did not interact with FADD or CRADD (Fig. 4A) nor with RIP or TRADD
(data not shown). A similar observation was reported with DR4 (4).
Interestingly, full-length Fas, DR4, and DR5, but not death
domain-deleted mutants, were all capable of forming complexes with
caspase-8, caspase-10, and FLAME-1 (Fig. 4B). Because these
proteins do not interact directly, this suggests that formation of
these complexes would require an adaptor molecule distinct from
FADD.
Taken together, we report the identification of DR5 and TRAIL-R3 as two
new receptors for the cytotoxic ligand TRAIL. Consistent with the
observation that TRAIL-induced apoptosis is independent of FADD (18),
we show that DR5, like DR4 (4), does not bind FADD. However, both
receptors recruit the upstream caspases-8 and -10 and the
anti-apoptotic protein FLAME-1, suggesting that an as yet unidentified
adaptor molecule is involved in the mechanism of apoptosis signaling by
these receptors. Because TRAIL-R3 does not contain a cytoplasmic death
domain and is capable of attenuating the cytotoxicity of TRAIL, it may
function physiologically as an antagonist to DR4 and DR5. A correlation
may exist between the high sensitivity of tumor cells to TRAIL and the
elevated levels of DR5 in these cells. Further analysis of the
regulation of DR4, DR5, and TRAIL-R3 expression in normal and tumor
cells should lead to a better understanding of their normal
physiological function.
FOOTNOTES The nucleotide sequence(s) reported in this paper has been submitted to the GenBankTM/EMBL Data Bank with accession number(s) AF020501 and AF020502. ACKNOWLEDGEMENTS We thank Drs. T. C. Tsang and W. J. LaRochelle for the pRSC vector and the Fc encoding plasmid MMTneu-HFc,
respectively.
REFERENCES
Volume 272, Number 41,
Issue of October 10, 1997
pp. 25417-25420
©1997 by The American Society for Biochemistry and Molecular Biology, Inc.
COMMUNICATION:
§,,,
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS AND DISCUSSION
FOOTNOTES
ACKNOWLEDGEMENTS
REFERENCES
B (14, 15). Consequently,
engagement of TNFR-1 or DR3 can signal an array of diverse biological
activities.
B activation. However,
unlike Fas, TNFR-1, and DR3, DR4 does not recruit FADD to the receptor
complex and thus signals death independently of FADD (4).
(residues 86 to 351), DR5, and DR5 (residues 1 to 268) were inserted
in a modified pcDNA-3 vector that allowed for in-frame fusion with
a Flag epitope tag that is preceded by Fas signal peptide. To generate
C-terminal Fc-tagged receptors, PCR generated cDNAs encoding Fas
(residues 
16 to 158), DR4 (residues 86 to 217, with N-terminal Fas
signal peptide-Flag tag), DR5 (residues 51 to 133), and TRAIL-R3
(residues 63 to 217) extracellular domains were inserted into a
modified pcDNA3 vector that allowed for in-frame fusion with the Fc
portion of the mouse IgG. For apoptosis assays we used the mammalian
double expression vector pRSC (20), which allows for expression of lacZ under the Rous sarcoma virus promoter, and the test
cDNA (DR4, DR4, DR5, DR5, TRAIL-R3) under the CMV promoter.
CrmA, FLAME-1, caspase-8-DN (C345A), or caspase-10-DN (C358A) (19) were
expressed using pcDNA3 (Invitrogen).
and
5 sequences were compiled. Based on the compiled sequences, PCR
primers were generated and used to clone two cDNAs that encode two
new DR4-related sequences (Fig. 1,
A and B). The first cDNA encodes a protein of
411 amino acids with an overall ~59% identity to DR4 (Fig.
1A). Its predicted domain structure is highly related to DR4
and the other members of the TNF receptor family. It contains a
putative N-terminal signal peptide (amino acids 51 to 1) followed
by an extracellular domain containing two cysteine-rich pseudorepeats.
Following the extracellular domain is a transmembrane domain (amino
acids 132 to 152) and a cytoplasmic domain. Within the cytoplasmic
domain there is a stretch of 67 amino acids (amino acids 273 to 339)
comprising a death domain homology region (Fig. 1C). Based
on these criteria and its apoptotic activity (see below) the new
protein was designated death receptor-5 (DR5).
Fig. 1.
Sequence analysis and tissue distribution of
DR5 and TRAIL-R3. Predicted amino acid sequences of human DR5
(A) and TRAIL-R3 (B) are shown. The mature DR5
and TRAIL-R3 are predicted to start at Glu+1 and
Tyr+1 (indicated by black diamonds),
respectively. The putative signal peptide and transmembrane domains are
single- and double-underlined, respectively. The five identical repeats
in the extracellular domain of TRAIL-R3 (B) are marked by
black triangles. The intracellular cytoplasmic death domain
of DR5 (A) is boxed. C, colinear
alignment of the death domains of members of the TNF receptor family.
Identical residues in at least three of six sequences are
shaded. The death domain of DR5 is 64, 30, 30, 20, and 31%
identical to the corresponding domains in DR4, DR3, TNFR-1, Fas, and
CAR1 respectively. D, Northern blot analysis of the
expression of DR5 (upper panels) and TRAIL-R3 (lower
panels) mRNAs in normal tissues and tumor cell lines. X-ray film exposure time in the two lower panels and the
upper left panel is 48 h, whereas in the upper
right panel it is 2 h. The cell lines are: HL-60,
promyelocytic leukemia; HeLa cell S3, K-562, chronic myelogenous
leukemia; MOLT-4, lymphoblastic leukemia; Raji, Burkitt's lymphoma;
SW480, colorectal adenocarcinoma; A549, lung carcinoma; and G361,
melanoma. The numbers on the left indicate kilobases.
[View Larger Version of this Image (56K GIF file)]
63 to 1) followed by an extracellular domain
containing two cysteine-rich pseudorepeats and five nearly identical
PAAEETMN(T)TSPGTPA repeats. Following the extracellular domain is a
C-terminal transmembrane domain (amino acids 217 to 236). Unlike DR4
and DR5, this molecule does not contain a cytoplasmic domain. Based on
these criteria and its ability to bind TRAIL (see below), this protein
was designated TRAIL-R3.
Fig. 2.
The extracellular domains of DR5 and TRAIL-R3
bind TRAIL and can block TRAIL-induced apoptosis. A,
conditioned media from cultures of 293 cells transfected for 72 h
with empty vector (lane 1) or DR5 (lane 2), DR4
(lane 3), Fas (lane 4), or TRAIL-R3 (TR3-Fc)
(lane 5) extracellular domain-Fc fusion proteins were incubated with purified soluble T7-His6-TRAIL and then
immunoprecipitated with anti-mouse IgG-agarose. After extensive washing
the samples were analyzed by SDS-polyacrylamide gel electrophoresis and
immunoblotted with a horseradish peroxidase-conjugated T7-antibody
(upper panel). The corresponding receptor-Fc fusions in the
conditioned media were also immunoblotted with anti-mouse Fc antibody
(lower panel). B, aliquots of conditioned media
containing receptor-Fc fusion proteins or no fusion protein
(Vector) were incubated with equivalent amount of soluble
TRAIL (250 ng/ml) and then added to MCF7 cells. Cells were stained
8 h later with propidium iodide, and the nuclei were examined by
fluorescence microscopy. The graph shows the percentage of apoptotic
nuclei (mean ± S.D.) as a function of total nuclei counted under
each condition (n = 3).
[View Larger Version of this Image (22K GIF file)]
Fig. 3.
Expression of DR5 but not TRAIL-R3 induces
apoptosis in human cells. MCF7 (A) and 293 (B) cells were transfected with the indicated
pRSC-lacZ constructs. 30 h after transfection cells were stained with 
-galactosidase and examined for morphological signs of apoptosis. The graphs show the percentage of round blue apoptotic cells (mean ± S.D.) as a function of total blue cells under each condition (n 
3). C, ectopic
expression of TRAIL-R3 attenuates TRAIL-induced apoptosis in MCF7
cells. MCF7 cells were transfected with TRAIL-R3 or vector alone for
36 h and then treated with soluble TRAIL (250 ng/ml) for 8 h.
The data are represented as in A and B, after
subtracting the background killing (12-15%) as a result of
transfection. D and E, DR4- and DR5-induced
apoptosis is inhibited by the caspase inhibitors, z-VAD-fmk and CrmA
(D), and by the dominant negative inhibitors, caspase-8-DN,
caspase-10-DN, and FLAME-1 (E). MCF7 cells were transfected
with DR4 or DR5 expression constructs in the presence of z-VAD-fmk (20 µM) or co-transfected with a 4-fold excess of a CrmA,
caspase-8-DN, caspase-10-DN, or FLAME-1 construct or an empty vector.
The data are represented as in A and B.
[View Larger Version of this Image (51K GIF file)]
Fig. 4.
In vivo interactions of DR5.
A, DR5 does not recruit FADD or CRADD. 293 cells were
transfected with expression plasmids encoding T7 epitope-tagged CRADD
or FADD and Flag epitope-tagged Fas or DR5. After 36 h, extracts
were prepared and immunoprecipitated with a monoclonal antibody to the
Flag epitope. The immunoprecipitates (upper panel) and the
corresponding cellular extracts (lower panel) were analyzed
by SDS-polyacrylamide gel electrophoresis and immunoblotted with a
horseradish peroxidase-conjugated T7 antibody. B, caspase-8, caspase-10, and FLAME-1 are recruited to the Fas, DR4, and DR5 signaling complexes. 293 cells were co-transfected with the indicated Flag constructs and plasmids encoding T7-caspase-10 (upper
panel), T7-caspase-8 (middle panel), or T7-FLAME-1
(lower panel) and then immunoprecipitated and detected as in
A.
[View Larger Version of this Image (22K GIF file)]
These three authors contributed equally to this work.
§
Supported by the Medical Research Council, Toxicology Unit, United
Kingdom.
To whom correspondence should be addressed: Kimmel Cancer
Inst., Bluemle Life Sciences Bldg., 904, Thomas Jefferson University, 233 S. 10th St., Philadelphia, PA 19107. Tel.: 215-503-4632; Fax: 215-923-1098; E-mail: E_Alnemri{at}lac.jci.tju.edu.
1
The abbreviations used are: TNF, tumor necrosis
factor; TNFR, TNF receptor; PCR, polymerase chain reaction; EST,
expressed sequence tag; TRAIL-R, TRAIL receptor.
©1997 by The American Society for Biochemistry and Molecular Biology, Inc.
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S. J. Cohen, R. B. Cohen, and N. J. Meropol Targeting Signal Transduction Pathways in Colorectal Cancer--More Than Skin Deep J. Clin. Oncol., August 10, 2005; 23(23): 5374 - 5385. [Abstract] [Full Text] [PDF]
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T. Shiraishi, T. Yoshida, S. Nakata, M. Horinaka, M. Wakada, Y. Mizutani, T. Miki, and T. Sakai Tunicamycin Enhances Tumor Necrosis Factor-Related Apoptosis-Inducing Ligand-Induced Apoptosis in Human Prostate Cancer Cells Cancer Res., July 15, 2005; 65(14): 6364 - 6370. [Abstract] [Full Text] [PDF]
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 S. Klucking, A. S. Collins, and J. A. T. Young Avian Sarcoma and Leukosis Virus Cytopathic Effect in the Absence of TVB Death Domain Signaling J. Virol., July 1, 2005; 79(13): 8243 - 8248. [Abstract] [Full Text] [PDF]
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T. Yoshida, T. Shiraishi, S. Nakata, M. Horinaka, M. Wakada, Y. Mizutani, T. Miki, and T. Sakai Proteasome Inhibitor MG132 Induces Death Receptor 5 through CCAAT/Enhancer-Binding Protein Homologous Protein Cancer Res., July 1, 2005; 65(13): 5662 - 5667. [Abstract] [Full Text] [PDF]
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E. Bremer, D. F. Samplonius, M. Peipp, L. van Genne, B.-J. Kroesen, G. H. Fey, M. Gramatzki, L. F.M.H. de Leij, and W. Helfrich Target Cell-Restricted Apoptosis Induction of Acute Leukemic T Cells by a Recombinant Tumor Necrosis Factor-Related Apoptosis-Inducing Ligand Fusion Protein with Specificity for Human CD7 Cancer Res., April 15, 2005; 65(8): 3380 - 3388. [Abstract] [Full Text] [PDF]
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N. Finnberg, J. J. Gruber, P. Fei, D. Rudolph, A. Bric, S.-H. Kim, T. F. Burns, H. Ajuha, R. Page, G. S. Wu, et al. DR5 Knockout Mice Are Compromised in Radiation-Induced Apoptosis Mol. Cell. Biol., March 1, 2005; 25(5): 2000 - 2013. [Abstract] [Full Text] [PDF]
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T.-G. Jin, A. Kurakin, N. Benhaga, K. Abe, M. Mohseni, F. Sandra, K. Song, B. K. Kay, and R. Khosravi-Far Fas-associated Protein with Death Domain (FADD)-independent Recruitment of c-FLIPL to Death Receptor 5 J. Biol. Chem., December 31, 2004; 279(53): 55594 - 55601. [Abstract] [Full Text] [PDF]
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H. Yamaguchi and H.-G. Wang CHOP Is Involved in Endoplasmic Reticulum Stress-induced Apoptosis by Enhancing DR5 Expression in Human Carcinoma Cells J. Biol. Chem., October 29, 2004; 279(44): 45495 - 45502. [Abstract] [Full Text] [PDF]
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T. J. Jang, H. J. Kang, J. R. Kim, and C. H. Yang Non-steroidal anti-inflammatory drug activated gene (NAG-1) expression is closely related to death receptor-4 and -5 induction, which may explain sulindac sulfide induced gastric cancer cell apoptosis Carcinogenesis, October 1, 2004; 25(10): 1853 - 1858. [Abstract] [Full Text] [PDF]
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S. Wang and W. S. El-Deiry Inducible Silencing of KILLER/DR5 In vivo Promotes Bioluminescent Colon Tumor Xenograft Growth and Confers Resistance to Chemotherapeutic Agent 5-Fluorouracil Cancer Res., September 15, 2004; 64(18): 6666 - 6672. [Abstract] [Full Text] [PDF]
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Z. Jin, E. R. McDonald III, D. T. Dicker, and W. S. El-Deiry Deficient Tumor Necrosis Factor-related Apoptosis-inducing Ligand (TRAIL) Death Receptor Transport to the Cell Surface in Human Colon Cancer Cells Selected for Resistance to TRAIL-induced Apoptosis J. Biol. Chem., August 20, 2004; 279(34): 35829 - 35839. [Abstract] [Full Text] [PDF]
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R. Kassis, F. Larrous, J. Estaquier, and H. Bourhy Lyssavirus Matrix Protein Induces Apoptosis by a TRAIL-Dependent Mechanism Involving Caspase-8 Activation J. Virol., June 15, 2004; 78(12): 6543 - 6555. [Abstract] [Full Text] [PDF]
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 D. C. Spierings, E. G. de Vries, E. Vellenga, F. A. van den Heuvel, J. J. Koornstra, J. Wesseling, H. Hollema, and S. de Jong Tissue Distribution of the Death Ligand TRAIL and Its Receptors J. Histochem. Cytochem., June 1, 2004; 52(6): 821 - 831. [Abstract] [Full Text] [PDF]
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 H. M. Beere `The stress of dying': the role of heat shock proteins in the regulation of apoptosis J. Cell Sci., June 1, 2004; 117(13): 2641 - 2651. [Abstract] [Full Text] [PDF]
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M. Taniai, A. Grambihler, H. Higuchi, N. Werneburg, S. F. Bronk, D. J. Farrugia, S. H. Kaufmann, and G. J. Gores Mcl-1 Mediates Tumor Necrosis Factor-Related Apoptosis-Inducing Ligand Resistance in Human Cholangiocarcinoma Cells Cancer Res., May 15, 2004; 64(10): 3517 - 3524. [Abstract] [Full Text] [PDF]
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K. Shah, C.-H. Tung, K. Yang, R. Weissleder, and X. O. Breakefield Inducible Release of TRAIL Fusion Proteins from a Proapoptotic Form for Tumor Therapy Cancer Res., May 1, 2004; 64(9): 3236 - 3242. [Abstract] [Full Text] [PDF]
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 E. R. McDonald III and W. S. El-Deiry Suppression of caspase-8- and -10-associated RING proteins results in sensitization to death ligands and inhibition of tumor cell growth PNAS, April 20, 2004; 101(16): 6170 - 6175. [Abstract] [Full Text] [PDF]
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 J.T. Bridgham and A.L. Johnson Alternatively Spliced Variants of Gallus gallus TNFRSF23 Are Expressed in the Ovary and Differentially Regulated by Cell Signaling Pathways Biol Reprod, April 1, 2004; 70(4): 972 - 979. [Abstract] [Full Text] [PDF]
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C. R. de Almodovar, C. Ruiz-Ruiz, A. Rodriguez, G. Ortiz-Ferron, J. M. Redondo, and A. Lopez-Rivas Tumor Necrosis Factor-related Apoptosis-inducing Ligand (TRAIL) Decoy Receptor TRAIL-R3 Is Up-regulated by p53 in Breast Tumor Cells through a Mechanism Involving an Intronic p53-binding Site J. Biol. Chem., February 6, 2004; 279(6): 4093 - 4101. [Abstract] [Full Text] [PDF]
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X. Bian, T. D. Giordano, H.-J. Lin, G. Solomon, V. P. Castle, and A. W. Opipari Jr. Chemotherapy-induced Apoptosis of S-type Neuroblastoma Cells Requires Caspase-9 and Is Augmented by CD95/Fas Stimulation J. Biol. Chem., February 6, 2004; 279(6): 4663 - 4669. [Abstract] [Full Text] [PDF]
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 R. Grataroli, D. Vindrieux, J. Selva, C. Felsenheld, A. Ruffion, M. Decaussin, and M. Benahmed Characterization of tumour necrosis factor-{alpha}-related apoptosis-inducing ligand and its receptors in the adult human testis Mol. Hum. Reprod., February 1, 2004; 10(2): 123 - 128. [Abstract] [Full Text] [PDF]
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N. Harper, M. A. Hughes, S. N. Farrow, G. M. Cohen, and M. MacFarlane Protein Kinase C Modulates Tumor Necrosis Factor-related Apoptosis-inducing Ligand-induced Apoptosis by Targeting the Apical Events of Death Receptor Signaling J. Biol. Chem., November 7, 2003; 278(45): 44338 - 44347. [Abstract] [Full Text] [PDF]
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D. J. Buchsbaum, T. Zhou, W. E. Grizzle, P. G. Oliver, C. J. Hammond, S. Zhang, M. Carpenter, and A. F. LoBuglio Antitumor Efficacy of TRA-8 Anti-DR5 Monoclonal Antibody Alone or in Combination with Chemotherapy and/or Radiation Therapy in a Human Breast Cancer Model Clin. Cancer Res., September 1, 2003; 9(10): 3731 - 3741. [Abstract] [Full Text] [PDF]
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S. Ray and A. Almasan Apoptosis Induction in Prostate Cancer Cells and Xenografts by Combined Treatment with Apo2 Ligand/Tumor Necrosis Factor-related Apoptosis-inducing Ligand and CPT-11 Cancer Res., August 1, 2003; 63(15): 4713 - 4723. [Abstract] [Full Text] [PDF]
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N. Harper, M. Hughes, M. MacFarlane, and G. M. Cohen Fas-associated Death Domain Protein and Caspase-8 Are Not Recruited to the Tumor Necrosis Factor Receptor 1 Signaling Complex during Tumor Necrosis Factor-induced Apoptosis J. Biol. Chem., July 3, 2003; 278(28): 25534 - 25541. [Abstract] [Full Text] [PDF]
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S. L. Planey, M. T. Abrams, N. M. Robertson, and G. Litwack Role of Apical Caspases and Glucocorticoid-regulated Genes in Glucocorticoid-induced Apoptosis of Pre-B Leukemic Cells Cancer Res., January 1, 2003; 63(1): 172 - 178. [Abstract] [Full Text] [PDF]
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J. Strater, U. Hinz, H. Walczak, G. Mechtersheimer, K. Koretz, C. Herfarth, P. Moller, and T. Lehnert Expression of TRAIL and TRAIL Receptors in Colon Carcinoma: TRAIL-R1 Is an Independent Prognostic Parameter Clin. Cancer Res., December 1, 2002; 8(12): 3734 - 3740. [Abstract] [Full Text] [PDF]
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 N. M. Robertson, J. G. Zangrilli, A. Steplewski, A. Hastie, R. G. Lindemeyer, M. A. Planeta, M. K. Smith, N. Innocent, A. Musani, R. Pascual, et al. Differential Expression of TRAIL and TRAIL Receptors in Allergic Asthmatics Following Segmental Antigen Challenge: Evidence for a Role of TRAIL in Eosinophil Survival J. Immunol., November 15, 2002; 169(10): 5986 - 5996. [Abstract] [Full Text] [PDF]
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 M. Matysiak, A. Jurewicz, D. Jaskolski, and K. Selmaj TRAIL induces death of human oligodendrocytes isolated from adult brain Brain, November 1, 2002; 125(11): 2469 - 2480. [Abstract] [Full Text] [PDF]
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T. Naka, K. Sugamura, B. L. Hylander, M. B. Widmer, Y. M. Rustum, and E. A. Repasky Effects of Tumor Necrosis Factor-related Apoptosis-inducing Ligand Alone and in Combination with Chemotherapeutic Agents on Patients' Colon Tumors Grown in SCID Mice Cancer Res., October 15, 2002; 62(20): 5800 - 5806. [Abstract] [Full Text] [PDF]
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M. MacFarlane, W. Merrison, S. B. Bratton, and G. M. Cohen Proteasome-mediated Degradation of Smac during Apoptosis: XIAP Promotes Smac Ubiquitination in Vitro J. Biol. Chem., September 20, 2002; 277(39): 36611 - 36616. [Abstract] [Full Text] [PDF]
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B. J. Kim, M.-S. Kim, K.-B. Kim, K.-W. Kim, Y.-M. Hong, I.-K. Kim, H.-W. Lee, and Y.-K. Jung Sensitizing effects of cadmium on TNF-{alpha}- and TRAIL-mediated apoptosis of NIH3T3 cells with distinct expression patterns of p53 Carcinogenesis, September 1, 2002; 23(9): 1411 - 1417. [Abstract] [Full Text] [PDF]
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C. Xiao, B. F. Yang, N. Asadi, F. Beguinot, and C. Hao Tumor Necrosis Factor-related Apoptosis-inducing Ligand-induced Death-inducing Signaling Complex and Its Modulation by c-FLIP and PED/PEA-15 in Glioma Cells J. Biol. Chem., July 5, 2002; 277(28): 25020 - 25025. [Abstract] [Full Text] [PDF]
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R. Grataroli, D. Vindrieux, A. Gougeon, and M. Benahmed Expression of Tumor Necrosis Factor-{alpha}-Related Apoptosis-Inducing Ligand and Its Receptors in Rat Testis During Development Biol Reprod, June 1, 2002; 66(6): 1707 - 1715. [Abstract] [Full Text] [PDF]
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D. J. Knauss and J. A. T. Young A Fifteen-Amino-Acid TVB Peptide Serves as a Minimal Soluble Receptor for Subgroup B Avian Leukosis and Sarcoma Viruses J. Virol., May 3, 2002; 76(11): 5404 - 5410. [Abstract] [Full Text] [PDF]
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Y. Guo, S. M. Srinivasula, A. Druilhe, T. Fernandes-Alnemri, and E. S. Alnemri Caspase-2 Induces Apoptosis by Releasing Proapoptotic Proteins from Mitochondria J. Biol. Chem., April 12, 2002; 277(16): 13430 - 13437. [Abstract] [Full Text] [PDF]
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S. Mazumder, B. Gong, Q. Chen, J. A. Drazba, J. C. Buchsbaum, and A. Almasan Proteolytic Cleavage of Cyclin E Leads to Inactivation of Associated Kinase Activity and Amplification of Apoptosis in Hematopoietic Cells Mol. Cell. Biol., April 1, 2002; 22(7): 2398 - 2409. [Abstract] [Full Text] [PDF]
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M. M. van Noesel, S. van Bezouw, G. S. Salomons, P. A. Voute, R. Pieters, S. B. Baylin, J. G. Herman, and R. Versteeg Tumor-specific Down-Regulation of the Tumor Necrosis Factor-related Apoptosis-inducing Ligand Decoy Receptors DcR1 and DcR2 Is Associated with Dense Promoter Hypermethylation Cancer Res., April 1, 2002; 62(7): 2157 - 2161. [Abstract] [Full Text] [PDF]
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 A. Yndestad, J. Kristian Damas, H. Geir Eiken, T. Holm, T. Haug, S. Simonsen, S. S. Froland, L. Gullestad, and P. Aukrust Increased gene expression of tumor necrosis factor superfamily ligands in peripheral blood mononuclear cells during chronic heart failure Cardiovasc Res, April 1, 2002; 54(1): 175 - 182. [Abstract] [Full Text] [PDF]
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M. D. Southall, J. S. Isenberg, H. Nakshatri, Q. Yi, Y. Pei, D. F. Spandau, and J. B. Travers The Platelet-activating Factor Receptor Protects Epidermal Cells from Tumor Necrosis Factor (TNF) alpha and TNF-related Apoptosis-inducing Ligand-induced Apoptosis through an NF-kappa B-dependent Process J. Biol. Chem., November 30, 2001; 276(49): 45548 - 45554. [Abstract] [Full Text] [PDF]
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F. C. Kischkel, D. A. Lawrence, A. Tinel, H. LeBlanc, A. Virmani, P. Schow, A. Gazdar, J. Blenis, D. Arnott, and A. Ashkenazi Death Receptor Recruitment of Endogenous Caspase-10 and Apoptosis Initiation in the Absence of Caspase-8 J. Biol. Chem., November 30, 2001; 276(49): 46639 - 46646. [Abstract] [Full Text] [PDF]
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 Q. Chen, B. Gong, A. S. Mahmoud-Ahmed, A. Zhou, E. D. Hsi, M. Hussein, and A. Almasan Apo2L/TRAIL and Bcl-2-related proteins regulate type I interferon-induced apoptosis in multiple myeloma Blood, October 1, 2001; 98(7): 2183 - 2192. [Abstract] [Full Text] [PDF]
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T. M. Baetu, H. Kwon, S. Sharma, N. Grandvaux, and J. Hiscott Disruption of NF-{kappa}B Signaling Reveals a Novel Role for NF-{kappa}B in the Regulation of TNF-Related Apoptosis-Inducing Ligand Expression J. Immunol., September 15, 2001; 167(6): 3164 - 3173. [Abstract] [Full Text] [PDF]
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Y. Huang, Q. He, M. J. Hillman, R. Rong, and M. S. Sheikh Sulindac Sulfide-induced Apoptosis Involves Death Receptor 5 and the Caspase 8-dependent Pathway in Human Colon and Prostate Cancer Cells Cancer Res., September 1, 2001; 61(18): 6918 - 6924. [Abstract] [Full Text] [PDF]
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I. F. Pollack, M. Erff, and A. Ashkenazi Direct Stimulation of Apoptotic Signaling by Soluble Apo2L/Tumor Necrosis Factor-related Apoptosis-inducing Ligand Leads to Selective Killing of Glioma Cells Clin. Cancer Res., May 1, 2001; 7(5): 1362 - 1369. [Abstract] [Full Text]
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S. Liu, Y. Yu, M. Zhang, W. Wang, and X. Cao The Involvement of TNF-{{alpha}}-Related Apoptosis-Inducing Ligand in the Enhanced Cytotoxicity of IFN-{{beta}}-Stimulated Human Dendritic Cells to Tumor Cells J. Immunol., May 1, 2001; 166(9): 5407 - 5415. [Abstract] [Full Text] [PDF]
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H. B. Adkins, S. C. Blacklow, and J. A. T. Young Two Functionally Distinct Forms of a Retroviral Receptor Explain the Nonreciprocal Receptor Interference among Subgroups B, D, and E Avian Leukosis Viruses J. Virol., April 15, 2001; 75(8): 3520 - 3526. [Abstract] [Full Text]
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R. D. Pettersen, G. Bernard, M. K. Olafsen, M. Pourtein, and S. O. Lie CD99 Signals Caspase-Independent T Cell Death J. Immunol., April 15, 2001; 166(8): 4931 - 4942. [Abstract] [Full Text] [PDF]
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 D. L. Roberts, W. Merrison, M. MacFarlane, and G. M. Cohen The Inhibitor of Apoptosis Protein-binding Domain of Smac Is Not Essential for its Proapoptotic Activity J. Cell Biol., April 2, 2001; 153(1): 221 - 228. [Abstract] [Full Text] [PDF]
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D.-W. Seol, J. Li, M.-H. Seol, S.-Y. Park, R. V. Talanian, and T. R. Billiar Signaling Events Triggered by Tumor Necrosis Factor-related Apoptosis-inducing Ligand (TRAIL): Caspase-8 Is Required for TRAIL-induced Apoptosis Cancer Res., February 1, 2001; 61(3): 1138 - 1143. [Abstract] [Full Text]
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B. Gong and A. Almasan Apo2 Ligand/TNF-related Apoptosis-inducing Ligand and Death Receptor 5 Mediate the Apoptotic Signaling Induced by Ionizing Radiation in Leukemic Cells Cancer Res., October 1, 2000; 60(20): 5754 - 5760. [Abstract] [Full Text]
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T. S. Griffith, R. D. Anderson, B. L. Davidson, R. D. Williams, and T. L. Ratliff Adenoviral-Mediated Transfer of the TNF-Related Apoptosis-Inducing Ligand/Apo-2 Ligand Gene Induces Tumor Cell Apoptosis J. Immunol., September 1, 2000; 165(5): 2886 - 2894. [Abstract] [Full Text] [PDF]
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 L. O. Roberts, A. J. Boxall, L. J. Lewis, G. J. Belsham, and G. E. N. Kass Caspases are not involved in the cleavage of translation initiation factor eIF4GI during picornavirus infection J. Gen. Virol., July 1, 2000; 81(7): 1703 - 1707. [Abstract] [Full Text]
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D.-W. Seol and T. R. Billiar Cysteine 230 Modulates Tumor Necrosis Factor-related Apoptosis-inducing Ligand Activity Cancer Res., June 1, 2000; 60(12): 3152 - 3154. [Abstract] [Full Text]
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R. Yu, S. Mandlekar, S. Ruben, J. Ni, and A-N. T. Kong Tumor Necrosis Factor-related Apoptosis-inducing Ligand-mediated Apoptosis in Androgen-independent Prostate Cancer Cells Cancer Res., May 1, 2000; 60(9): 2384 - 2389. [Abstract] [Full Text]
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 B. R. Gochuico, J. Zhang, B. Y. Ma, A. Marshak-Rothstein, and A. Fine TRAIL expression in vascular smooth muscle Am J Physiol Lung Cell Mol Physiol, May 1, 2000; 278(5): L1045 - L1050. [Abstract] [Full Text] [PDF]
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H. B. Adkins, J. Brojatsch, and J. A. T. Young Identification and Characterization of a Shared TNFR-Related Receptor for Subgroup B, D, and E Avian Leukosis Viruses Reveal Cysteine Residues Required Specifically for Subgroup E Viral Entry J. Virol., April 15, 2000; 74(8): 3572 - 3578. [Abstract] [Full Text]
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J. M. Zapata, S.-i. Matsuzawa, A. Godzik, E. Leo, S. A. Wasserman, and J. C. Reed The Drosophila Tumor Necrosis Factor Receptor-associated Factor-1 (DTRAF1) Interacts with Pelle and Regulates NFkappa B Activity J. Biol. Chem., April 14, 2000; 275(16): 12102 - 12107. [Abstract] [Full Text] [PDF]
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 T. Yoshida, T. Higuchi, H. Hagiyama, A. Strasser, K. Nishioka, and T. Tsubata Rapid B cell apoptosis induced by antigen receptor ligation does not require Fas (CD95/APO-1), the adaptor protein FADD/MORT1 or CrmA-sensitive caspases but is defective in both MRL-+/+ and MRL-lpr/lpr mice Int. Immunol., April 1, 2000; 12(4): 517 - 526. [Abstract] [Full Text] [PDF]
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 S. Y. Hsu and A. J. W. Hsueh Tissue-Specific Bcl-2 Protein Partners in Apoptosis: An Ovarian Paradigm Physiol Rev, April 1, 2000; 80(2): 593 - 614. [Abstract] [Full Text] [PDF]
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M. MacFarlane, W. Merrison, D. Dinsdale, and G. M. Cohen Active Caspases and Cleaved Cytokeratins Are Sequestered into Cytoplasmic Inclusions in TRAIL-induced Apoptosis J. Cell Biol., March 20, 2000; 148(6): 1239 - 1254. [Abstract] [Full Text] [PDF]
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M. Stoneley, S. A. Chappell, C. L. Jopling, M. Dickens, M. MacFarlane, and A. E. Willis c-Myc Protein Synthesis Is Initiated from the Internal Ribosome Entry Segment during Apoptosis Mol. Cell. Biol., February 15, 2000; 20(4): 1162 - 1169. [Abstract] [Full Text]
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G. Kienzle and J. von Kempis CD137 (ILA/4-1BB), expressed by primary human monocytes, induces monocyte activation and apoptosis of B lymphocytes Int. Immunol., January 1, 2000; 12(1): 73 - 82. [Abstract] [Full Text] [PDF]
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S. H. Lee, M. S. Shin, H. S. Kim, H. K. Lee, W. S. Park, S. Y. Kim, J. H. Lee, S. Y. Han, J. Y. Park, R. R. Oh, et al. Alterations of the DR5/TRAIL Receptor 2 Gene in Non-Small Cell Lung Cancers Cancer Res., November 1, 1999; 59(22): 5683 - 5686. [Abstract] [Full Text] [PDF]
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W.-H. Hu, H. Johnson, and H.-B. Shu Tumor Necrosis Factor-related Apoptosis-inducing Ligand Receptors Signal NF-kappa B and JNK Activation and Apoptosis through Distinct Pathways J. Biol. Chem., October 22, 1999; 274(43): 30603 - 30610. [Abstract] [Full Text] [PDF]
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J. D. Bretz, M. Rymaszewski, P. L. Arscott, A. Myc, K. B. Ain, N. W. Thompson, and J. R. Baker Jr. TRAIL Death Pathway Expression and Induction in Thyroid Follicular Cells J. Biol. Chem., August 13, 1999; 274(33): 23627 - 23632. [Abstract] [Full Text] [PDF]
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L. M. Sedger, D. M. Shows, R. A. Blanton, J. J. Peschon, R. G. Goodwin, D. Cosman, and S. R. Wiley IFN-{gamma} Mediates a Novel Antiviral Activity Through Dynamic Modulation of TRAIL and TRAIL Receptor Expression J. Immunol., July 15, 1999; 163(2): 920 - 926. [Abstract] [Full Text] [PDF]
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S. M. Srinivasula, M. Ahmad, J.-h. Lin, J.-L. Poyet, T. Fernandes-Alnemri, P. N. Tsichlis, and E. S. Alnemri CLAP, a Novel Caspase Recruitment Domain-containing Protein in the Tumor Necrosis Factor Receptor Pathway, Regulates NF-kappa B Activation and Apoptosis J. Biol. Chem., June 18, 1999; 274(25): 17946 - 17954. [Abstract] [Full Text] [PDF]
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G. S. Wu, T. F. Burns, Y. Zhan, E. S. Alnemri, and W. S. El-Deiry Molecular Cloning and Functional Analysis of the Mouse Homologue of the KILLER/DR5 Tumor Necrosis Factor-related Apoptosis-inducing Ligand (TRAIL) Death Receptor Cancer Res., June 1, 1999; 59(12): 2770 - 2775. [Abstract] [Full Text] [PDF]
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T. A. Phillips, J. Ni, G. Pan, S. M. Ruben, Y.-F. Wei, J. L. Pace, and J. S. Hunt TRAIL (Apo-2L) and TRAIL Receptors in Human Placentas: Implications for Immune Privilege J. Immunol., May 15, 1999; 162(10): 6053 - 6059. [Abstract] [Full Text] [PDF]
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S. Mori, K. Murakami-Mori, S. Nakamura, A. Ashkenazi, and B. Bonavida Sensitization of AIDS-Kaposi's Sarcoma Cells to Apo-2 Ligand-Induced Apoptosis by Actinomycin D J. Immunol., May 1, 1999; 162(9): 5616 - 5623. [Abstract] [Full Text] [PDF]
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B. Kwon, K.-Y. Yu, J. Ni, G.-L. Yu, I.-K. Jang, Y.-J. Kim, L. Xing, D. Liu, S.-X. Wang, and B. S. Kwon Identification of a Novel Activation-inducible Protein of the Tumor Necrosis Factor Receptor Superfamily and Its Ligand J. Biol. Chem., March 5, 1999; 274(10): 6056 - 6061. [Abstract] [Full Text] [PDF]
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N. Kayagaki, N. Yamaguchi, M. Nakayama, A. Kawasaki, H. Akiba, K. Okumura, and H. Yagita Involvement of TNF-Related Apoptosis-Inducing Ligand in Human CD4+ T Cell-Mediated Cytotoxicity J. Immunol., March 1, 1999; 162(5): 2639 - 2647. [Abstract] [Full Text] [PDF]
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M. M. Keane, S. A. Ettenberg, M. M. Nau, E. K. Russell, and S. Lipkowitz Chemotherapy Augments TRAIL-induced Apoptosis in Breast Cell Lines Cancer Res., February 1, 1999; 59(3): 734 - 741. [Abstract] [Full Text] [PDF]
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J. Spielman, R. K. Lee, and E. R. Podack Perforin/Fas-Ligand Double Deficiency Is Associated with Macrophage Expansion and Severe Pancreatitis J. Immunol., December 15, 1998; 161(12): 7063 - 7070. [Abstract] [Full Text] [PDF]
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F. Muhlenbeck, E. Haas, R. Schwenzer, G. Schubert, M. Grell, C. Smith, P. Scheurich, and H. Wajant TRAIL/Apo2L Activates c-Jun NH2-terminal Kinase (JNK) via Caspase-dependent and Caspase-independent Pathways J. Biol. Chem., December 4, 1998; 273(49): 33091 - 33098. [Abstract] [Full Text] [PDF]
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