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Laboratory of Molecular Oncology and Cell Cycle Regulation, Howard Hughes Medical Institute, Departments of Medicine, Pharmacology, Genetics, Cancer Center, and the Institute for Human Gene Therapy, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania 19104
The
tumor necrosis factor-related apoptosis-inducing ligand (TRAIL or
Apo2L) is a potent inducer of death of cancer but not normal cells,
which suggests its potential use as a tumor-specific antineoplastic
agent. TRAIL binds to the proapoptotic death receptors DR4 and the
p53-regulated proapoptotic KILLER/DR5 as well as to the decoy receptors
TRID and TRUNDD. In the present studies, we identified a subgroup of
TRAIL-resistant cancer cell lines characterized by low or absent basal
DR4 or high expression of the caspase activation inhibitor FLIP. Four
of five TRAIL-sensitive cell lines expressed high levels of DR4 mRNA
and protein, whereas six of six TRAIL-resistant cell lines expressed
low or undetectable levels of DR4 (
2;
P < 0.01). FLIP expression appeared elevated in
five of six (83%) TRAIL-resistant cell lines and only one of five
(20%) TRAIL-sensitive cells (2; P < 0.05). Two TRAIL-resistant lines that expressed DR4 contained an
A-to-G alteration in the death domain encoding arginine instead of
lysine at codon 441. The K441R polymorphism is present in 20% of the
normal population and can inhibit DR4-mediated cell killing in a
dominant-negative fashion. The expression level of KILLER/DR5, TRID,
TRUNDD or TRID, and TRUNDD did not correlate with TRAIL sensitivity
(P > 0.05). These results suggest that the major
determinants for TRAIL sensitivity may be the expression level of DR4
and FLIP. TRAIL-resistant cells became susceptible to TRAIL-mediated
apoptosis in the presence of doxorubicin. In TRAIL-sensitive cells,
caspases 8, 9, and 3 were activated after TRAIL treatment, but in
TRAIL-resistant cells, they were activated only by the combination of
TRAIL and doxorubicin. Our results suggest: (a)
evaluation of tumor DR4 and FLIP expression and host DR4 codon 441
status could be potentially useful predictors of TRAIL sensitivity, and
(b) doxorubicin, in combination with TRAIL, may
effectively promote caspase activation in TRAIL-resistant tumors.
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