Cited by 201Cell death mechanisms and regulationCancer-related Molecular PathwaysNF-κB Signaling Pathways

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X-Linked Inhibitor of Apoptosis Protein (XIAP) Is a Nonredundant Modulator of Tumor Necrosis Factor-Related Apoptosis-Inducing Ligand (TRAIL)- Mediated Apoptosis in Human Cancer Cells

Cummins, Jordan M., Kohli, Manu, Rago, Carlo, Kinzler, Kenneth W., Vogelstein, Bert, Bunz, Fred·2004·Cancer Research

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Abstract

Although the tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) has been shown to play an important role in the immunosurveillance of neoplasia, apoptotic factors that modulate the sensitivity of cancer cells to TRAIL are poorly understood. The inhibitor of apoptosis proteins (IAPs) have generated considerable interest as potential targets for cancer therapy, but the lack of a phenotype in X-linked IAP (XIAP) knockout mice has generated speculation that IAP function may be redundant. Using gene targeting technology, we show that disruption of the gene encoding XIAP in human cancer cells did not interfere with basal proliferation, but caused a remarkable sensitivity to TRAIL. These results demonstrate that XIAP is a nonredundant modulator of TRAIL-mediated apoptosis and provide a rationale for XIAP as a therapeutic target.

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Background
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Influential
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BackgroundMethodResultInfluential
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Method
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Background
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Self-citation
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Background
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Background
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Background
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Influential
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Self-citation
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Result
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Peroxisome Proliferator-Activated Receptor-γ Contributes to the Inhibitory Effects of Embelin on Colon Carcinogenesis
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Background
Novel SMAC-mimetics synergistically stimulate melanoma cell death in combination with TRAIL and Bortezomib
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Background
A Smac-mimetic sensitizes prostate cancer cells to TRAIL-induced apoptosis via modulating both IAPs and NF-kappaB
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Background
XIAP Inhibition and Generation of Reactive Oxygen Species Enhances TRAIL Sensitivity in Inflammatory Breast Cancer Cells
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Acquired TRAIL resistance in human breast cancer cells are caused by the sustained cFLIPL and XIAP protein levels and ERK activation
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Method
The Chinese Herb Isolate Isorhapontigenin Induces Apoptosis in Human Cancer Cells by Down-regulating Overexpression of Antiapoptotic Protein XIAP
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Recurrent Genomic Alterations With Impact on Survival in Colorectal Cancer Identified by Genome-Wide Array Comparative Genomic Hybridization
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SMAC/Diablo -dependent apoptosis induced by nonsteroidal antiinflammatory drugs (NSAIDs) in colon cancer cells
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Self-citation
Lyapunov exponents and phase diagrams reveal multi‐factorial control over TRAIL‐induced apoptosis
Aldridge, B. B., Gaudet, S., Lauffenburger, D. A., & Sorger, P. K. (2011) · Molecular Systems Biology · doi:10.1038/msb.2011.85 · Cited by 65
“Our findings may also explain why XIAP-null mice have few obvious defects (Harlin et al, 2001; Cummins et al, 2004): in the absence of XIAP, cells may simply alter the balance between type I and type II phenotypes.”
Influential
Regulating TRAIL Receptor-Induced Cell Death at the Membrane: A Deadly Discussion
Shirley, S., Morizot, A., & Micheau, O. (2011) · Recent Patents on Anti-Cancer Drug Discovery · doi:10.2174/157489211796957757 · Cited by 66
“TRAIL-induced cell death can efficiently be regulated at the receptor level by antagonistic receptors [53], at the proximal level by c-FLIP [113] or further downstream by Bcl-2 family members [114] or inhibitors such as XIAP [115, 116] or Survivin [117] Fig.”
Background
Therapeutic Potential and Molecular Mechanism of a Novel, Potent, Nonpeptide, Smac Mimetic SM-164 in Combination with TRAIL for Cancer Treatment
Lü, J., McEachern, D., Sun, H., Bai, L., Peng, Y., Qiu, S., Miller, R. S., Liao, J., Han, Y., Liu, M., et al. (2011) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-10-0864 · Cited by 66
Frequent Alteration of XAF1 in Human Colorectal Cancers: Implication for Tumor Cell Resistance to Apoptotic Stresses
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Application of XIAP Antisense to Cancer and Other Proliferative Disorders: Development of AEG35156/ GEM®640
LaCasse, E. C., Kandimalla, E. R., Winocour, P. D., SULLIVAN, T., Agrawal, S., Gillard, J. W., & Durkin, J. P. (2005) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1359.032 · Cited by 63
Potent antileukemic interactions between flavopiridol and TRAIL/Apo2L involve flavopiridol-mediated XIAP downregulation
Rosato, R. R., Dai, Y., Almenara, J. A., Maggio, S. C., & Grant, S. (2004) · Leukemia · doi:10.1038/sj.leu.2403491 · Cited by 63
Inducible Resistance of Tumor Cells to Tumor Necrosis Factor–Related Apoptosis-Inducing Ligand Receptor 2–Mediated Apoptosis by Generation of a Blockade at the Death Domain Function
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Targeting death receptors for TRAIL by agents designed by Mother Nature
Prasad, S., Kim, J. H., Gupta, S. C., & Aggarwal, B. B. (2014) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2014.07.004 · Cited by 61
Sensitization of pancreatic carcinoma cells for γ-irradiation-induced apoptosis by XIAP inhibition
Giagkousiklidis, S., Vellanki, S. H., Debatin, K., & Fulda, S. (2007) · Oncogene · doi:10.1038/sj.onc.1210502 · Cited by 58
“This is in line with results reported by our group and other investigators that silencing of XIAP or overexpression of Smac did not trigger apoptosis in the absence of an additional apoptotic stimulus in many cancer cells including pancreatic carcinoma (Holcik et al., 2000; Guo et al., 2002; Fulda et al., 2002; Cummin…”
BackgroundResult
Loss of ataxia telangiectasia mutated– and Rad3-related function potentiates the effects of chemotherapeutic drugs on cancer cell survival
Wilsker, D. F., & Bunz, F. (2007) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-06-0679 · Cited by 57
Self-citation
Association of cooking oil fumes exposure with lung cancer: Involvement of inhibitor of apoptosis proteins in cell survival and proliferation in vitro
Hung, H., Wu, W.-J., Cheng, Y., Wu, T.-C., Chang, K., & Lee, H. (2006) · Mutation Research/Genetic Toxicology and Environmental Mutagenesis · doi:10.1016/j.mrgentox.2006.12.005 · Cited by 55
Combined inhibition of FLIP and XIAP induces Bax-independent apoptosis in type II colorectal cancer cells
Wilson, T. R., McEwan, M. V., McLaughlin, K. M., Clorennec, C. L., Allen, W. L., Fennell, D. A., Johnston, P. G., & Longley, D. B. (2008) · Oncogene · doi:10.1038/onc.2008.366 · Cited by 53
“Earlier studies have shown that HCT116 or DLD-1 cells in which XIAP expression has been downregulated exhibit increased caspase 3 cleavage and apoptosis in response to TRAIL (Cummins et al., 2004).”
Background
Fragment-Based Design of Small Molecule X-Linked Inhibitor of Apoptosis Protein Inhibitors
Huang, J., Zhang, Z., Wu, B., Cellitti, J. F., Zhang, X., Dahl, R. S., Shiau, C., Welsh, K., Emdadi, A., Stebbins, J. L., et al. (2008) · Journal of Medicinal Chemistry · doi:10.1021/jm8006992 · Cited by 56
Targeting cell death signaling in colorectal cancer: Current strategies and future perspectives
Koehler, B. C. (2014) · World Journal of Gastroenterology · doi:10.3748/wjg.v20.i8.1923 · Cited by 55
Pulling the plug on a cancer cell by eliminating XIAP with AEG35156
LaCasse, E. C. (2012) · Cancer Letters · doi:10.1016/j.canlet.2012.06.015 · Cited by 54
Lysosomal destabilization and cathepsin B contributes for cytochrome c release and caspase activation in embelin‐induced apoptosis
Joy, B., Sivadasan, R., Abraham, E. T., John, M., Sobhan, P. K., Seervi, M., & Santhoshkumar, T. R. (2009) · Molecular Carcinogenesis · doi:10.1002/mc.20599 · Cited by 55
Inhibition of MKK7–JNK by the TOR Signaling Pathway Regulator-Like Protein Contributes to Resistance of HCC Cells to TRAIL-Induced Apoptosis
Song, I. S., Jun, S. Y., Na, H., Kim, H., Jung, S. Y., Ha, G., Park, Y., Long, L. Z., Yu, D., Kim, J., et al. (2012) · Gastroenterology · doi:10.1053/j.gastro.2012.07.103 · Cited by 52
“6 Ci [ -32P] ATP, 2 g GST-c-Jun (1-76), and 2 g GST-JNK1 at 30°C for 30 minutes.”
Influential
The flavonolignan silibinin potentiates TRAIL-induced apoptosis in human colon adenocarcinoma and in derived TRAIL-resistant metastatic cells
Kauntz, H., Bousserouel, S., Gossé, F., & Raul, F. (2012) · APOPTOSIS · doi:10.1007/s10495-012-0731-4 · Cited by 52
Acquired resistance to TRAIL-induced apoptosis in human ovarian cancer cells is conferred by increased turnover of mature caspase-3
Lane, D. A., Côté, M., Grondin, R., Couture, M.-C., & Piché, A. (2006) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-05-0362 · Cited by 50
Oxidative stress-driven DR5 upregulation restores TRAIL/Apo2L sensitivity induced by iron oxide nanoparticles in colorectal cancer
Shi, Y., Wang, J., Liu, J., Lin, G., Xie, F., Pang, X., Pei, Y., Cheng, Y., Zhang, Y., Lin, Z., et al. (2019) · Biomaterials · doi:10.1016/j.biomaterials.2019.119753 · Cited by 51
Double inhibition of XIAP and Bcl-2 axis is beneficial for retrieving sensitivity of renal cell cancer to apoptosis
Bilim, V. N., Yuuki, K., Itoi, T., Muto, A., Kato, T., Nagaoka, A., Motoyama, T., & Tomita, Y. (2008) · British Journal of Cancer · doi:10.1038/sj.bjc.6604268 · Cited by 50
“The knockout phenotype can be revealed only under specific conditions in some tissues and cells (Cummins et al, 2004; Conte et al, 2006; Zhao et al, 2007).”
Background
TRAIL‐Induced Apoptosis
Corazza, N., Kassahn, D., Jakob, S., Badmann, A., & Brunner, T. (2009) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2009.04905.x · Cited by 48
Anti-tumor activity of the X-linked inhibitor of apoptosis (XIAP) inhibitor embelin in gastric cancer cells
Wang, D., Sun, Y., Ye, F., Li, W., Kharbuja, P., Gao, L., Zhang, D. Y., & Suo, J. (2013) · Molecular and Cellular Biochemistry · doi:10.1007/s11010-013-1853-x · Cited by 49
“XIAP expression is elevated in many cancers, including lung, ovarian, colon, and kidney cancers, and myeloid leukemia [12–18].”
Background
Cytoprotective effects of IAPs revealed by a small molecule antagonist
Galbán, S., Hwang, C., Rumble, J. M., Oetjen, K. A., Wright, C. W., Boudreault, A., Durkin, J. P., Gillard, J. W., Jaquith, J. B., Morris, S. J., et al. (2008) · Biochemical Journal · doi:10.1042/bj20081677 · Cited by 49
“To explore this question, we utilized the HCT116 human colon carcinoma cell line and a derivative line in which the XIAP gene had been disrupted by homologous recombination [27].”
BackgroundMethodResultInfluential
CDX2 has tumorigenic potential in the human colon cancer cell lines LOVO and SW48
Dang, L. H., Chen, F., Ying, C., Chun, S. Y., Knock, S. A., Appelman, H. D., & Dang, D. T. (2005) · Oncogene · doi:10.1038/sj.onc.1209247 · Cited by 50
“The strategy is as previously described (Chan et al., 2002; Cummins et al., 2004a, b; Kohli et al., 2004; Dang et al., 2005).”
Method
Sulindac sulfide–induced apoptosis is enhanced by a small-molecule Bcl-2 inhibitor and by TRAIL in human colon cancer cells overexpressing Bcl-2
Sinicrope, F. A., & Penington, R. C. (2005) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-05-0137 · Cited by 49
“SW480 cells carry mutated p53 (49), as do HCT-15 cells.”
Background
Low expression of pro-apoptotic proteins Bax, Bak and Smac indicates prolonged progression-free survival in chemotherapy-treated metastatic melanoma
Guttà, C., Rahman, A., Aura, C. M., Dynoodt, P., Charles, E. M., Hirschenhahn, E., Joseph, J., Wouters, J., de Chaumont, C., Rafferty, M., et al. (2020) · Cell Death and Disease · doi:10.1038/s41419-020-2309-3 · Cited by 50
Caspase-8 as a Regulator of Tumor Cell Motility
Graf, R. P., Keller, N., Barbero, S., & Stupack, D. G. (2014) · Current Molecular Medicine · doi:10.2174/1566524014666140128111951 · Cited by 48
The role of XIAP in resistance to TNF-related apoptosis-inducing ligand (TRAIL) in Leukemia
Saraei, R., Soleimani, M., Akbari, A. A. M., Hagh, M. F., Hassanzadeh, A., & Solali, S. (2018) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2018.08.065 · Cited by 49
Combined modality therapy with TRAIL or agonistic death receptor antibodies
Amm, H. M., Oliver, P. G., Lee, C. H., Li, Y., & Buchsbaum, D. J. (2011) · Cancer Biology & Therapy · doi:10.4161/cbt.11.5.14671 · Cited by 47
Clinical significance of Smac/DIABLO expression in colorectal cancer
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17-Allylamino-17-demethoxygeldanamycin overcomes TRAIL resistance in colon cancer cell lines
Vasilevskaya, I. A., & O'Dwyer, P. J. (2005) · Biochemical Pharmacology · doi:10.1016/j.bcp.2005.05.018 · Cited by 46
The Chinese Herb Isolate Yuanhuacine (YHL-14) Induces G2/M Arrest in Human Cancer Cells by Up-regulating p21 Protein Expression through an p53 Protein-independent Cascade
Zhang, R., Wang, Y., Li, J., Jin, H., Song, S., & Huang, C. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.513960 · Cited by 44
“The dominant negative mutant of p38 kinase (DN-p38) was a gift from Dr. Mercedes Rincon (Department of Medicine, University of Vermont, Burlington, VT) and has been used in our previous studies (18, 19, 20).”
BackgroundInfluential
Carnosic acid cooperates with tamoxifen to induce apoptosis associated with Caspase-3 activation in breast cancer cells in vitro and in vivo
Han, N., Zhou, Q., Huang, Q., & Liu, K. (2017) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2017.01.084 · Cited by 45
Cytosolic Gram-negative bacteria prevent apoptosis by inhibition of effector caspases through lipopolysaccharide
Günther, S. D., Fritsch, M., Seeger, J. M., Schiffmann, L. M., Snipas, S. J., Coutelle, M., Kufer, T. A., Higgins, P. G., Hornung, V., Bernardini, M. L., et al. (2019) · Nature Microbiology · doi:10.1038/s41564-019-0620-5 · Cited by 45
Cell death pathways – potential therapeutic targets
MacFarlane, M. (2009) · Xenobiotica · doi:10.1080/00498250903137990 · Cited by 46
“We, and others, have shown that knockdown of XIAP by antisense oligonucleotides or RNAi strategies induces apoptosis in cancer cell lines and promotes the synergistic killing of cancer cells by TRAIL (Cummins et al. 2004; Hughes et al. unpublished observations).”
Background
Bortezomib Sensitizes Non–Hodgkin's Lymphoma Cells to Apoptosis Induced by Antibodies to Tumor Necrosis Factor–Related Apoptosis-Inducing Ligand (TRAIL) Receptors TRAIL-R1 and TRAIL-R2
Smith, M. R., Jin, F., & Joshi, I. D. (2007) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-07-0982 · Cited by 44

Authors: Cummins, J. M., Kohli, M., Rago, C., Kinzler, K. W., Vogelstein, B., & Bunz, F.
Affiliations: Johns Hopkins University (US)
Sidney Kimmel Cancer Center (US)
Howard Hughes Medical Institute (US)
ORCID: Kohli, Manu
Kinzler, Kenneth W.
Vogelstein, Bert
Bunz, Fred
Venue: Cancer Research
Publisher: American Association for Cancer Research (AACR)
Published: 2004-05-01
Volume: 64
Issue: 9
Pages: 3006-3008
ISSN: 0008-5472 (ISSN-L)
1538-7445
DOI: 10.1158/0008-5472.can-04-0046
OpenAlex: W2074501845
Cited by: 200
References: 14
Citations by year: 2026: 1 · 2024: 1 · 2023: 4 · 2022: 2 · 2021: 2 · 2020: 4 · 2019: 7 · 2018: 2 · 2017: 10 · 2016: 4 · 2015: 4 · 2014: 16 · 2013: 8 · 2012: 18
FWCI: 6.53
Type: journal article
Language: en
Open access: closed
Locations: Cancer Research (publishedVersion)
PubMed (publishedVersion)
Funders: National Cancer Institute (CA43460)
National Institute of General Medical Sciences (T32GM007309, GM07309)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
Health Sciences › Medicine › Oncology › Cancer-related Molecular Pathways
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › NF-κB Signaling Pathways
Keywords: XIAP, inhibitor of apoptosis proteins, TRAIL, TRAIL resistance, apoptosis, cancer cells, gene targeting, cancer therapy targets, immune surveillance
MeSH terms: Cell Survival, Colonic Neoplasms, Humans, Membrane Glycoproteins, Proteins, Tumor Necrosis Factor-alpha, Apoptosis, Caspases, HCT116 Cells, Cell Line, Tumor, Apoptosis Regulatory Proteins, X-Linked Inhibitor of Apoptosis Protein, TNF-Related Apoptosis-Inducing Ligand

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X-Linked Inhibitor of Apoptosis Protein (XIAP) Is a Nonredundant Modulator of Tumor Necrosis Factor-Related Apoptosis-Inducing Ligand (TRAIL)- Mediated Apoptosis in Human Cancer Cells

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