Death and anti-death: tumour resistance to apoptosis (original) (raw)
Hanahan, D. & Weinberg, R. A. The hallmarks of cancer. Cell100, 57–70 (2000). CASPubMed Google Scholar
Krammer, P. H., Galle, P. R., Moller, P. & Debatin, K. M. CD95(APO-1/Fas)-mediated apoptosis in normal and malignant liver, colon, and hematopoietic cells. Adv. Cancer Res.75, 251–273 (1998). CASPubMed Google Scholar
Krammer, P. H. CD95(APO-1/Fas)-mediated apoptosis: live and let die. Adv. Immunol.71, 163–210 (1999). CASPubMed Google Scholar
Schmitz, I., Kirchhoff, S. & Krammer, P. H. Regulation of death receptor-mediated apoptosis pathways. Int. J. Biochem. Cell Biol.32, 1123–1136 (2000). CASPubMed Google Scholar
Pitti, R. M. et al. Genomic amplification of a decoy receptor for Fas ligand in lung and colon cancer. Nature396, 699–703 (1998).Identification of the decoy receptor DcR3 that inhibits CD95L-induced apoptosis. DcR3 is amplified in tumours. CASPubMed Google Scholar
Yu, K. Y. et al. A newly identified member of tumor necrosis factor receptor superfamily (TR6) suppresses LIGHT-mediated apoptosis. J. Biol. Chem.274, 13733–13736 (1999). CASPubMed Google Scholar
Sprick, M. R. et al. FADD/MORT1 and caspase-8 are recruited to TRAIL receptors 1 and 2 and are essential for apoptosis mediated by TRAIL receptor 2. Immunity12, 599–609 (2000). CASPubMed Google Scholar
Kischkel, F. C. et al. Cytotoxicity-dependent APO-1 (Fas/CD95)-associated proteins form a death-inducing signaling complex (DISC) with the receptor. EMBO J.14, 5579–5588 (1995).The first description of the death-inducing signalling complex (DISC) in death receptor-mediated apoptosis. CASPubMedPubMed Central Google Scholar
Kischkel, F. C. et al. Death receptor recruitment of endogenous caspase-10 and apoptosis initiation in the absence of caspase-8. J. Biol. Chem.276, 46639–46646 (2001). CASPubMed Google Scholar
Scaffidi, C. et al. Two CD95 (APO-1/Fas) signaling pathways. EMBO J.17, 1675–1687 (1998).Clarifies the role of mitochondria in death-receptor-mediated apoptosis. CASPubMedPubMed Central Google Scholar
Zamzami, N. & Kroemer, G. The mitochondrion in apoptosis: how Pandora's box opens. Nature Rev. Mol. Cell Biol.2, 67–71 (2001). CAS Google Scholar
Martinou, J. C. & Green, D. R. Breaking the mitochondrial barrier. Nature Rev. Mol. Cell Biol.2, 63–67 (2001). CAS Google Scholar
Rathmell, J. C. & Thompson, C. B. The central effectors of cell death in the immune system. Annu. Rev. Immunol.17, 781–828 (1999). CASPubMed Google Scholar
Savill, J. & Fadok, V. Corpse clearance defines the meaning of cell death. Nature407, 784–788 (2000). CASPubMed Google Scholar
Borner, C. & Monney, L. Apoptosis without caspases: an inefficient molecular guillotine? Cell Death Differ.6, 497–507 (1999). CASPubMed Google Scholar
Xiang, J., Chao, D. T. & Korsmeyer, S. J. BAX-induced cell death may not require interleukin 1 β-converting enzyme-like proteases. Proc. Natl Acad. Sci. USA93, 14559–14563 (1996). ArticleCASPubMedPubMed Central Google Scholar
Sperandio, S., de Belle, I. & Bredesen, D. E. An alternative, nonapoptotic form of programmed cell death. Proc. Natl Acad. Sci. USA97, 14376–14381 (2000). CASPubMedPubMed Central Google Scholar
Krueger, A., Baumann, S., Krammer, P. H. & Kirchhoff, S. FLICE-inhibitory proteins: regulators of death receptor-mediated apoptosis. Mol. Cell. Biol.21, 8247–8254 (2001). CASPubMedPubMed Central Google Scholar
Deveraux, Q. L. & Reed, J. C. IAP family proteins — suppressors of apoptosis. Genes Dev.13, 239–252 (1999). CASPubMed Google Scholar
Verhagen, A. M. et al. Identification of DIABLO, a mammalian protein that promotes apoptosis by binding to and antagonizing IAP proteins. Cell102, 43–53 (2000). CASPubMed Google Scholar
Du, C., Fang, M., Li, Y., Li, L. & Wang, X. Smac, a mitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition. Cell102, 33–42 (2000). CASPubMed Google Scholar
Evan, G. I. & Vousden, K. H. Proliferation, cell cycle and apoptosis in cancer. Nature411, 342–348 (2001). CASPubMed Google Scholar
Evan, G. I. et al. Induction of apoptosis in fibroblasts by c-myc protein. Cell69, 119–128 (1992). CASPubMed Google Scholar
Bissonnette, R. P., Echeverri, F., Mahboubi, A. & Green, D. R. Apoptotic cell death induced by c-myc is inhibited by bcl-2. Nature359, 552–554 (1992).References24and69–73showed that anti-apoptotic proteins are important oncogenes by reporting the oncogenic potential of BCL2. CASPubMed Google Scholar
Harrington, E. A., Bennett, M. R., Fanidi, A. & Evan, G. I. c-Myc-induced apoptosis in fibroblasts is inhibited by specific cytokines. EMBO J.13, 3286–3295 (1994). CASPubMedPubMed Central Google Scholar
Sabbatini, P., Lin, J., Levine, A. J. & White, E. Essential role for p53-mediated transcription in E1A-induced apoptosis. Genes Dev.9, 2184–2192 (1995). CASPubMed Google Scholar
Stambolic, V., Mak, T. W. & Woodgett, J. R. Modulation of cellular apoptotic potential: contributions to oncogenesis. Oncogene18, 6094–6103 (1999). CASPubMed Google Scholar
Datta, S. R., Brunet, A. & Greenberg, M. E. Cellular survival: a play in three Akts. Genes Dev.13, 2905–2927 (1999). CASPubMed Google Scholar
Frisch, S. M. & Screaton, R. A. Anoikis mechanisms. Curr. Opin. Cell Biol.13, 555–562 (2001). CASPubMed Google Scholar
Frisch, S. M. & Francis, H. Disruption of epithelial cell-matrix interactions induces apoptosis. J. Cell Biol.124, 619–626 (1994). CASPubMed Google Scholar
Khwaja, A., Rodriguez-Viciana, P., Wennstrom, S., Warne, P. H. & Downward, J. Matrix adhesion and Ras transformation both activate a phosphoinositide 3-OH kinase and protein kinase B/Akt cellular survival pathway. EMBO J.16, 2783–2793 (1997). CASPubMedPubMed Central Google Scholar
Puthalakath, H., Huang, D. C., O'Reilly, L. A., King, S. M. & Strasser, A. The proapoptotic activity of the Bcl-2 family member Bim is regulated by interaction with the dynein motor complex. Mol. Cell3, 287–296 (1999). CASPubMed Google Scholar
Puthalakath, H. et al. Bmf: a proapoptotic BH3-only protein regulated by interaction with the myosin V actin motor complex, activated by anoikis. Science293, 1829–1832 (2001). CASPubMed Google Scholar
Oulton, R. & Harrington, L. Telomeres, telomerase, and cancer: life on the edge of genomic stability. Curr. Opin. Oncol.12, 74–81 (2000). CASPubMed Google Scholar
Hahn, W. C. et al. Inhibition of telomerase limits the growth of human cancer cells. Nature Med.5, 1164–1170 (1999). CASPubMed Google Scholar
Zhang, X., Mar, V., Zhou, W., Harrington, L. & Robinson, M. O. Telomere shortening and apoptosis in telomerase-inhibited human tumor cells. Genes Dev.13, 2388–2399 (1999). CASPubMedPubMed Central Google Scholar
Chin, L. et al. p53 deficiency rescues the adverse effects of telomere loss and cooperates with telomere dysfunction to accelerate carcinogenesis. Cell97, 527–538 (1999). CASPubMed Google Scholar
Shresta, S., Pham, C. T., Thomas, D. A., Graubert, T. A. & Ley, T. J. How do cytotoxic lymphocytes kill their targets? Curr. Opin. Immunol.10, 581–587 (1998). CASPubMed Google Scholar
Kagi, D. et al. Cytotoxicity mediated by T cells and natural killer cells is greatly impaired in perforin-deficient mice. Nature369, 31–37 (1994). CASPubMed Google Scholar
Heusel, J. W., Wesselschmidt, R. L., Shresta, S., Russell, J. H. & Ley, T. J. Cytotoxic lymphocytes require granzyme B for the rapid induction of DNA fragmentation and apoptosis in allogeneic target cells. Cell76, 977–987 (1994). CASPubMed Google Scholar
Medema, J. P. et al. Cleavage of FLICE (caspase-8) by granzyme B during cytotoxic T lymphocyte-induced apoptosis. Eur. J. Immunol.27, 3492–3498 (1997). CASPubMed Google Scholar
Heibein, J. A. et al. Granzyme B-mediated cytochrome c release is regulated by the Bcl-2 family members Bid and Bax. J. Exp. Med.192, 1391–1402 (2000). CASPubMedPubMed Central Google Scholar
Rouvier, E., Luciani, M. F. & Golstein, P. Fas involvement in Ca2+-independent T cell-mediated cytotoxicity. J. Exp. Med.177, 195–200 (1993). CASPubMed Google Scholar
Li, J. H. et al. The regulation of CD95 ligand expression and function in CTL. J. Immunol.161, 3943–3949 (1998). CASPubMed Google Scholar
Herr, I. & Debatin, K. M. Cellular stress response and apoptosis in cancer therapy. Blood98, 2603–2614 (2001). CASPubMed Google Scholar
Stahnke, K., Fulda, S., Friesen, C., Strauss, G. & Debatin, K. M. Activation of apoptosis pathways in peripheral blood lymphocytes by in vivo chemotherapy. Blood98, 3066–3073 (2001). CASPubMed Google Scholar
Ryan, K. M., Phillips, A. C. & Vousden, K. H. Regulation and function of the p53 tumor suppressor protein. Curr. Opin. Cell Biol.13, 332–337 (2001). CASPubMed Google Scholar
Sherr, C. J. The INK4A/ARF network in tumour suppression. Nature Rev. Mol. Cell Biol.2, 731–737 (2001). CAS Google Scholar
Miyashita, T. & Reed, J. C. Tumor suppressor p53 is a direct transcriptional activator of the human bax gene. Cell80, 293–299 (1995). CASPubMed Google Scholar
Oda, E. et al. Noxa, a BH3-only member of the Bcl-2 family and candidate mediator of p53-induced apoptosis. Science288, 1053–1058 (2000). CASPubMed Google Scholar
Nakano, K. & Vousden, K. H. PUMA, a novel proapoptotic gene, is induced by p53. Mol. Cell7, 683–694 (2001). CASPubMed Google Scholar
Oda, K. et al. p53AIP1, a potential mediator of p53-dependent apoptosis, and its regulation by Ser-46-phosphorylated p53. Cell102, 849–862 (2000). CASPubMed Google Scholar
Muller, M. et al. p53 activates the CD95 (APO-1/Fas) gene in response to DNA damage by anticancer drugs. J. Exp. Med.188, 2033–2045 (1998). CASPubMedPubMed Central Google Scholar
Guan, B., Yue, P., Clayman, G. L. & Sun, S. Y. Evidence that the death receptor DR4 is a DNA damage-inducible, p53-regulated gene. J. Cell Physiol.188, 98–105 (2001). CASPubMed Google Scholar
Wu, G. S. et al. KILLER/DR5 is a DNA damage-inducible p53-regulated death receptor gene. Nature Genet.17, 141–143 (1997). CASPubMed Google Scholar
Caelles, C., Helmberg, A. & Karin, M. p53-dependent apoptosis in the absence of transcriptional activation of p53-target genes. Nature370, 220–223 (1994). CASPubMed Google Scholar
Soengas, M. S. et al. Apaf-1 and caspase-9 in p53-dependent apoptosis and tumor inhibition. Science284, 156–159 (1999). CASPubMed Google Scholar
Bennett, M. et al. Cell surface trafficking of Fas: a rapid mechanism of p53-mediated apoptosis. Science282, 290–293 (1998). CASPubMed Google Scholar
Hug, H. et al. Reactive oxygen intermediates are involved in the induction of CD95 ligand mRNA expression by cytostatic drugs in hepatoma cells. J. Biol. Chem.272, 28191–28193 (1997). CASPubMed Google Scholar
Friesen, C., Herr, I., Krammer, P. H. & Debatin, K. M. Involvement of the CD95 (APO-1/FAS) receptor/ligand system in drug- induced apoptosis in leukemia cells. Nature Med.2, 574–577 (1996).Provides evidence that the CD95 system is involved in drug-induced apoptosis and so identifies one particular mechanism by which apoptosis is caused by anticancer drugs at the molecular level. CASPubMed Google Scholar
Fulda, S. et al. Activation of the CD95 (APO-1/Fas) pathway in drug- and γ-irradiation-induced apoptosis of brain tumor cells. Cell Death Differ.5, 884–893 (1998). CASPubMed Google Scholar
Muller, M. et al. Drug-induced apoptosis in hepatoma cells is mediated by the CD95 (APO-1/Fas) receptor/ligand system and involves activation of wild-type p53. J. Clin. Invest.99, 403–413 (1997). CASPubMedPubMed Central Google Scholar
Muller, M., Scaffidi, C. A., Galle, P. R., Stremmel, W. & Krammer, P. H. The role of p53 and the CD95 (APO-1/Fas) death system in chemotherapy-induced apoptosis. Eur. Cytokine Netw.9, 685–686 (1998). CASPubMed Google Scholar
Eichhorst, S. T. et al. A novel AP-1 element in the CD95 ligand promoter is required for induction of apoptosis in hepatocellular carcinoma cells upon treatment with anticancer drugs. Mol. Cell. Biol.20, 7826–7837 (2000). CASPubMedPubMed Central Google Scholar
Newton, K. & Strasser, A. Ionizing radiation and chemotherapeutic drugs induce apoptosis in lymphocytes in the absence of Fas or FADD/MORT1 signaling. Implications for cancer therapy. J. Exp. Med.191, 195–200 (2000). CASPubMedPubMed Central Google Scholar
Yeh, W. C. et al. FADD: essential for embryo development and signaling from some, but not all, inducers of apoptosis. Science279, 1954–1958 (1998). CASPubMed Google Scholar
Wesselborg, S., Engels, I. H., Rossmann, E., Los, M. & Schulze-Osthoff, K. Anticancer drugs induce caspase-8/FLICE activation and apoptosis in the absence of CD95 receptor/ligand interaction. Blood93, 3053–3063 (1999). CASPubMed Google Scholar
Fulda, S. et al. Betulinic acid triggers CD95 (APO-1/Fas)- and p53-independent apoptosis via activation of caspases in neuroectodermal tumors. Cancer Res.57, 4956–4964 (1997). CASPubMed Google Scholar
Tsujimoto, Y., Cossman, J., Jaffe, E. & Croce, C. M. Involvement of the BCL-2 gene in human follicular lymphoma. Science228, 1440–1443 (1985). CASPubMed Google Scholar
McDonnell, T. J. et al. BCL-2-immunoglobulin transgenic mice demonstrate extended B cell survival and follicular lymphoproliferation. Cell57, 79–88 (1989). CASPubMed Google Scholar
Reed, J. C., Cuddy, M., Slabiak, T., Croce, C. M. & Nowell, P. C. Oncogenic potential of BCL-2 demonstrated by gene transfer. Nature336, 259–261 (1988). CASPubMed Google Scholar
Strasser, A., Harris, A. W., Bath, M. L. & Cory, S. Novel primitive lymphoid tumours induced in transgenic mice by cooperation between MYC and BCL-2. Nature348, 331–333 (1990). CASPubMed Google Scholar
Vaux, D. L., Cory, S. & Adams, J. M. BCL-2 gene promotes haemopoietic cell survival and cooperates with c-MYC to immortalize pre-B cells. Nature335, 440–442 (1988). CASPubMed Google Scholar
Kogan, S. C. et al. BCL-2 cooperates with promyelocytic leukemia retinoic acid receptor alpha chimeric protein (PMLRARα) to block neutrophil differentiation and initiate acute leukemia. J. Exp. Med.193, 531–543 (2001). CASPubMedPubMed Central Google Scholar
Weller, M., Malipiero, U., Aguzzi, A., Reed, J. C. & Fontana, A. Protooncogene bcl-2 gene transfer abrogates Fas/APO-1 antibody-mediated apoptosis of human malignant glioma cells and confers resistance to chemotherapeutic drugs and therapeutic irradiation. J. Clin. Invest.95, 2633–2643 (1995). CASPubMedPubMed Central Google Scholar
Campos, L. et al. High expression of BCL-2 protein in acute myeloid leukemia cells is associated with poor response to chemotherapy. Blood81, 3091–3096 (1993). CASPubMed Google Scholar
Hermine, O. et al. Prognostic significance of BCL-2 protein expression in aggressive non- Hodgkin's lymphoma. Groupe d'Etude des Lymphomes de l'Adulte (GELA). Blood87, 265–272 (1996). CASPubMed Google Scholar
Miyashita, T. & Reed, J. C. BCL-2 gene transfer increases relative resistance of S49.1 and WEHI7.2 lymphoid cells to cell death and DNA fragmentation induced by glucocorticoids and multiple chemotherapeutic drugs. Cancer Res.52, 5407–5411 (1992). CASPubMed Google Scholar
Schmitt, C. A., Rosenthal, C. T. & Lowe, S. W. Genetic analysis of chemoresistance in primary murine lymphomas. Nature Med.6, 1029–1035 (2000). CASPubMed Google Scholar
Findley, H. W., Gu, L., Yeager, A. M. & Zhou, M. Expression and regulation of BCL-2, BCL-XL, and BAX correlate with p53 status and sensitivity to apoptosis in childhood acute lymphoblastic leukemia. Blood89, 2986–2993 (1997). CASPubMed Google Scholar
Coustan-Smith, E. et al. Clinical relevance of BCL-2 overexpression in childhood acute lymphoblastic leukemia. Blood87, 1140–1146 (1996). CASPubMed Google Scholar
Henderson, S. et al. Epstein-Barr virus-coded BHRF1 protein, a viral homologue of Bcl-2, protects human B cells from programmed cell death. Proc. Natl Acad. Sci. USA90, 8479–8483 (1993). CASPubMedPubMed Central Google Scholar
Tarodi, B., Subramanian, T. & Chinnadurai, G. Epstein-Barr virus BHRF1 protein protects against cell death induced by DNA-damaging agents and heterologous viral infection. Virology201, 404–407 (1994). CASPubMed Google Scholar
Sarid, R., Sato, T., Bohenzky, R. A., Russo, J. J. & Chang, Y. Kaposi's sarcoma-associated herpesvirus encodes a functional bcl-2 homologue. Nature Med.3, 293–298 (1997). CASPubMed Google Scholar
Boise, L. H. et al. BCL-X, a BCL-2-related gene that functions as a dominant regulator of apoptotic cell death. Cell74, 597–608 (1993). CASPubMed Google Scholar
Dole, M. G. et al. BCL-XL is expressed in neuroblastoma cells and modulates chemotherapy-induced apoptosis. Cancer Res.55, 2576–2582 (1995). CASPubMed Google Scholar
Nagane, M., Levitzki, A., Gazit, A., Cavenee, W. K. & Huang, H. J. Drug resistance of human glioblastoma cells conferred by a tumor-specific mutant epidermal growth factor receptor through modulation of BCL-XL and caspase-3-like proteases. Proc. Natl Acad. Sci. USA95, 5724–5729 (1998). CASPubMedPubMed Central Google Scholar
Minn, A. J., Rudin, C. M., Boise, L. H. & Thompson, C. B. Expression of BCL-XL can confer a multidrug resistance phenotype. Blood86, 1903–1910 (1995). CASPubMed Google Scholar
Zhou, P., Qian, L., Kozopas, K. M. & Craig, R. W. MCL-1, a BCL-2 family member, delays the death of hematopoietic cells under a variety of apoptosis-inducing conditions. Blood89, 630–643 (1997). CASPubMed Google Scholar
Kaufmann, S. H. et al. Elevated expression of the apoptotic regulator MCL-1 at the time of leukemic relapse. Blood91, 991–1000 (1998). CASPubMed Google Scholar
Irmler, M. et al. Inhibition of death receptor signals by cellular FLIP. Nature388, 190–195 (1997).Describes the identification of the two forms of cellular FLIP and the expression of FLIPLin melanomas. CASPubMed Google Scholar
Mueller, C. M. & Scott, D. W. Distinct molecular mechanisms of Fas resistance in murine B lymphoma cells. J. Immunol.165, 1854–1862 (2000). CASPubMed Google Scholar
Tepper, C. G. & Seldin, M. F. Modulation of caspase-8 and FLICE-inhibitory protein expression as a potential mechanism of Epstein–Barr virus tumorigenesis in Burkitt's lymphoma. Blood94, 1727–1737 (1999). CASPubMed Google Scholar
Thome, M. et al. Viral FLICE-inhibitory proteins (FLIPs) prevent apoptosis induced by death receptors. Nature386, 517–521 (1997). CASPubMed Google Scholar
Hu, S., Vincenz, C., Ni, J., Gentz, R. & Dixit, V. M. I-FLICE, a novel inhibitor of tumor necrosis factor receptor-1- and CD-95-induced apoptosis. J. Biol. Chem.272, 17255–17257 (1997). CASPubMed Google Scholar
Bertin, J. et al. Death effector domain-containing herpesvirus and poxvirus proteins inhibit both Fas- and TNFR1-induced apoptosis. Proc. Natl Acad. Sci. USA94, 1172–1176 (1997). CASPubMedPubMed Central Google Scholar
Sturzl, M. et al. Expression of K13/v-FLIP gene of human herpesvirus 8 and apoptosis in Kaposi's sarcoma spindle cells. J. Natl Cancer Inst.91, 1725–1733 (1999). CASPubMed Google Scholar
Kataoka, T. et al. FLIP prevents apoptosis induced by death receptors but not by perforin/granzyme B, chemotherapeutic drugs, and γ irradiation. J. Immunol.161, 3936–3942 (1998). CASPubMed Google Scholar
Medema, J. P., de Jong, J., van Hall, T., Melief, C. J. & Offringa, R. Immune escape of tumors in vivo by expression of cellular FLICE- inhibitory protein. J. Exp. Med.190, 1033–1038 (1999).Showed that expression of FLIP is a mechanism for immune escape of tumorsin vivo. CASPubMedPubMed Central Google Scholar
Djerbi, M. et al. The inhibitor of death receptor signaling, FLICE-inhibitory protein defines a new class of tumor progression factors. J. Exp. Med.190, 1025–1032 (1999). CASPubMedPubMed Central Google Scholar
Taylor, M. A. et al. Inhibition of the death receptor pathway by cFLIP confers partial engraftment of MHC class I-deficient stem cells and reduces tumor clearance in perforin-deficient mice. J. Immunol.167, 4230–4237 (2001). CASPubMed Google Scholar
Cheng, J. et al. Protection from Fas-mediated apoptosis by a soluble form of the Fas molecule. Science263, 1759–1762 (1994). CASPubMed Google Scholar
Midis, G. P., Shen, Y. & Owen-Schaub, L. B. Elevated soluble Fas (sFas) levels in nonhematopoietic human malignancy. Cancer Res.56, 3870–3874 (1996). CASPubMed Google Scholar
Ugurel, S., Rappl, G., Tilgen, W. & Reinhold, U. Increased soluble CD95 (sFas/CD95) serum level correlates with poor prognosis in melanoma patients. Clin. Cancer Res.7, 1282–1286 (2001). CASPubMed Google Scholar
Gerharz, C. D. et al. Resistance to CD95 (APO-1/Fas)-mediated apoptosis in human renal cell carcinomas: an important factor for evasion from negative growth control. Lab. Invest.79, 1521–1534 (1999). CASPubMed Google Scholar
Roth, W. et al. Soluble decoy receptor 3 is expressed by malignant gliomas and suppresses CD95 ligand-induced apoptosis and chemotaxis. Cancer Res.61, 2759–2765 (2001). CASPubMed Google Scholar
Ambrosini, G., Adida, C. & Altieri, D. C. A novel anti-apoptosis gene, survivin, expressed in cancer and lymphoma. Nature Med.3, 917–921 (1997).Identifies the IAP-family member survivin and shows that some IAPs are overexpressed in cancers. CASPubMed Google Scholar
Adida, C., Berrebi, D., Peuchmaur, M., Reyes-Mugica, M. & Altieri, D. C. Anti-apoptosis gene, survivin, and prognosis of neuroblastoma. Lancet351, 882–883 (1998). CASPubMed Google Scholar
Grossman, D. et al. Transgenic expression of survivin in keratinocytes counteracts UVB-induced apoptosis and cooperates with loss of p53. J. Clin. Invest.108, 991–999 (2001). CASPubMedPubMed Central Google Scholar
Grossman, D., Kim, P. J., Schechner, J. S. & Altieri, D. C. Inhibition of melanoma tumor growth in vivo by survivin targeting. Proc. Natl Acad. Sci. USA98, 635–640 (2001). CASPubMedPubMed Central Google Scholar
Mesri, M., Wall, N. R., Li, J., Kim, R. W. & Altieri, D. C. Cancer gene therapy using a survivin mutant adenovirus. J. Clin. Invest108, 981–990 (2001). CASPubMedPubMed Central Google Scholar
Dierlamm, J. et al. The apoptosis inhibitor gene API2 and a novel 18q gene, MLT, are recurrently rearranged in the t(11;18)(q21;q21) associated with mucosa-associated lymphoid tissue lymphomas. Blood93, 3601–3609 (1999). CASPubMed Google Scholar
Vucic, D., Stennicke, H. R., Pisabarro, M. T., Salvesen, G. S. & Dixit, V. M. ML-IAP, a novel inhibitor of apoptosis that is preferentially expressed in human melanomas. Curr. Biol.10, 1359–1366 (2000). CASPubMed Google Scholar
Medema, J. P. et al. Blockade of the granzyme B/perforin pathway through overexpression of the serine protease inhibitor PI-9/SPI-6 constitutes a mechanism for immune escape by tumors. Proc. Natl Acad. Sci. USA98, 11515–11520 (2001). CASPubMedPubMed Central Google Scholar
Rampino, N. et al. Somatic frameshift mutations in the BAX gene in colon cancers of the microsatellite mutator phenotype. Science275, 967–969 (1997). CASPubMed Google Scholar
Meijerink, J. P. et al. Hematopoietic malignancies demonstrate loss-of-function mutations of BAX. Blood91, 2991–2997 (1998). CASPubMed Google Scholar
Molenaar, J. J. et al. Microsatellite instability and frameshift mutations in BAX and transforming growth factor-β RII genes are very uncommon in acute lymphoblastic leukemia in vivo but not in cell lines. Blood92, 230–233 (1998). CASPubMed Google Scholar
Krajewski, S. et al. Reduced expression of proapoptotic gene BAX is associated with poor response rates to combination chemotherapy and shorter survival in women with metastatic breast adenocarcinoma. Cancer Res.55, 4471–4478 (1995). CASPubMed Google Scholar
Yin, C., Knudson, C. M., Korsmeyer, S. J. & Van Dyke, T. Bax suppresses tumorigenesis and stimulates apoptosis in vivo. Nature385, 637–640 (1997). CASPubMed Google Scholar
Bargou, R. C. et al. Overexpression of the death-promoting gene Bax-α which is downregulated in breast cancer restores sensitivity to different apoptotic stimuli and reduces tumor growth in SCID mice. J. Clin. Invest.97, 2651–2659 (1996). CASPubMedPubMed Central Google Scholar
Ionov, Y., Yamamoto, H., Krajewski, S., Reed, J. C. & Perucho, M. Mutational inactivation of the proapoptotic gene BAX confers selective advantage during tumor clonal evolution. Proc. Natl Acad. Sci. USA97, 10872–10877 (2000). CASPubMedPubMed Central Google Scholar
Soengas, M. S. et al. Inactivation of the apoptosis effector Apaf-1 in malignant melanoma. Nature409, 207–211 (2001).Showed that metastatic melanomas acquire resistance to chemotherapy by losing APAF1 expression. CASPubMed Google Scholar
Teitz, T. et al. Caspase-8 is deleted or silenced preferentially in childhood neuroblastomas with amplification of MYCN. Nature Med.6, 529–535 (2000). CASPubMed Google Scholar
Strand, S. et al. Lymphocyte apoptosis induced by CD95 (APO-1/Fas) ligand-expressing tumor cells — a mechanism of immune evasion? Nature Med.2, 1361–1366 (1996).Showed that tumour cells can evade immune attack by downregulation of the CD95 receptor and killing of lymphocytes through expression of CD95L. CASPubMed Google Scholar
Moller, P. et al. Expression of APO-1 (CD95), a member of the NGF/TNF receptor superfamily, in normal and neoplastic colon epithelium. Int. J. Cancer57, 371–377 (1994). CASPubMed Google Scholar
Leithauser, F. et al. Constitutive and induced expression of APO-1, a new member of the nerve growth factor/tumor necrosis factor receptor superfamily, in normal and neoplastic cells. Lab. Invest.69, 415–429 (1993). CASPubMed Google Scholar
Volkmann, M. et al. Loss of CD95 expression is linked to most but not all p53 mutants in European hepatocellular carcinoma. J. Mol. Med.79, 594–600 (2001). CASPubMed Google Scholar
Peli, J. et al. Oncogenic Ras inhibits Fas ligand-mediated apoptosis by downregulating the expression of Fas. EMBO J.18, 1824–1831 (1999). CASPubMedPubMed Central Google Scholar
Maeda, T. et al. Fas gene mutation in the progression of adult T cell leukemia. J. Exp. Med.189, 1063–1071 (1999). CASPubMedPubMed Central Google Scholar
Landowski, T. H., Qu, N., Buyuksal, I., Painter, J. S. & Dalton, W. S. Mutations in the Fas antigen in patients with multiple myeloma. Blood90, 4266–4270 (1997). CASPubMed Google Scholar
Cascino, I., Papoff, G., De Maria, R., Testi, R. & Ruberti, G. Fas/Apo-1 (CD95) receptor lacking the intracytoplasmic signaling domain protects tumor cells from Fas-mediated apoptosis. J. Immunol.156, 13–17 (1996). CASPubMed Google Scholar
Straus, S. E. et al. The development of lymphomas in families with autoimmune lymphoproliferative syndrome with germline Fas mutations and defective lymphocyte apoptosis. Blood98, 194–200 (2001). CASPubMed Google Scholar
Shin, M. S. et al. Mutations of tumor necrosis factor-related apoptosis-inducing ligand receptor 1 (TRAIL-R1) and receptor 2 (TRAIL-R2) genes in metastatic breast cancers. Cancer Res.61, 4942–4946 (2001). CASPubMed Google Scholar
Fisher, M. J. et al. Nucleotide substitution in the ectodomain of trail receptor DR4 is associated with lung cancer and head and neck cancer. Clin. Cancer Res.7, 1688–1697 (2001). CASPubMed Google Scholar
Pai, S. I. et al. Rare loss-of-function mutation of a death receptor gene in head and neck cancer. Cancer Res58, 3513–3518 (1998). CASPubMed Google Scholar
Lee, S. H. et al. Alterations of the DR5/TRAIL receptor 2 gene in non-small cell lung cancers. Cancer Res.59, 5683–5686 (1999). CASPubMed Google Scholar
Liston, P. et al. Identification of XAF1 as an antagonist of XIAP anti-caspase activity. Nature Cell Biol.3, 128–133 (2001). CASPubMed Google Scholar
Lowe, S. W. et al. p53 status and the efficacy of cancer therapy in vivo. Science266, 807–810 (1994).Showed that tumours can acquire resistance to therapy by mutation or deficiency of p53. CASPubMed Google Scholar
Lee, J. M. & Bernstein, A. p53 mutations increase resistance to ionizing radiation. Proc. Natl Acad. Sci. USA90, 5742–5746 (1993). CASPubMedPubMed Central Google Scholar
Aas, T. et al. Specific P53 mutations are associated with de novo resistance to doxorubicin in breast cancer patients. Nature Med.2, 811–814 (1996). CASPubMed Google Scholar
Bunz, F. et al. Disruption of p53 in human cancer cells alters the responses to therapeutic agents. J. Clin. Invest.104, 263–269 (1999). CASPubMedPubMed Central Google Scholar
Schmitt, C. A., McCurrach, M. E., de Stanchina, E., Wallace-Brodeur, R. R. & Lowe, S. W. INK4A/ARF mutations accelerate lymphomagenesis and promote chemoresistance by disabling p53. Genes Dev.13, 2670–2677 (1999). CASPubMedPubMed Central Google Scholar
Samuels-Lev, Y. et al. ASPP proteins specifically stimulate the apoptotic function of p53. Mol. Cell8, 781–794 (2001). CASPubMed Google Scholar
Kauffmann-Zeh, A. et al. Suppression of c-Myc-induced apoptosis by Ras signalling through PI(3)K and PKB. Nature385, 544–548 (1997). CASPubMed Google Scholar
Chang, H. W. et al. Transformation of chicken cells by the gene encoding the catalytic subunit of PI 3-kinase. Science276, 1848–1850 (1997). CASPubMed Google Scholar
Shayesteh, L. et al. PIK3CA is implicated as an oncogene in ovarian cancer. Nature Genet.21, 99–102 (1999). CASPubMed Google Scholar
Podsypanina, K. et al. Mutation of Pten/Mmac1 in mice causes neoplasia in multiple organ systems. Proc. Natl Acad. Sci. USA96, 1563–1568 (1999). CASPubMedPubMed Central Google Scholar
Suzuki, A. et al. High cancer susceptibility and embryonic lethality associated with mutation of the PTEN tumor suppressor gene in mice. Curr. Biol.8, 1169–1178 (1998). CASPubMed Google Scholar
Steck, P. A. et al. Identification of a candidate tumour suppressor gene, MMAC1, at chromosome 10q23. 3 that is mutated in multiple advanced cancers. Nature Genet.15, 356–362 (1997). CASPubMed Google Scholar
Cheng, J. Q. et al. AKT2, a putative oncogene encoding a member of a subfamily of protein-serine/threonine kinases, is amplified in human ovarian carcinomas. Proc. Natl Acad. Sci. USA89, 9267–9271 (1992). CASPubMedPubMed Central Google Scholar
Persidis, A. Cancer multidrug resistance. Nature Biotechnol.17, 94–95 (1999). CAS Google Scholar
Cole, S. P. et al. Overexpression of a transporter gene in a multidrug-resistant human lung cancer cell line. Science258, 1650–1654 (1992). CASPubMed Google Scholar
Johnstone, R. W., Cretney, E. & Smyth, M. J. P-glycoprotein protects leukemia cells against caspase-dependent, but not caspase-independent, cell death. Blood93, 1075–1085 (1999). CASPubMed Google Scholar
Smyth, M. J., Krasovskis, E., Sutton, V. R. & Johnstone, R. W. The drug efflux protein, P-glycoprotein, additionally protects drug-resistant tumor cells from multiple forms of caspase-dependent apoptosis. Proc. Natl Acad. Sci. USA95, 7024–7029 (1998). CASPubMedPubMed Central Google Scholar
Bours, V. et al. Nuclear factor-κB, cancer, and apoptosis. Biochem. Pharmacol.60, 1085–1089 (2000). CASPubMed Google Scholar
Rayet, B. & Gelinas, C. Aberrant REL/NF-κB genes and activity in human cancer. Oncogene18, 6938–6947 (1999). CASPubMed Google Scholar
Wood, K. M., Roff, M. & Hay, R. T. Defective IκBα in Hodgkin cell lines with constitutively active NF-κB. Oncogene16, 2131–2139 (1998). CASPubMed Google Scholar
Sethi, T. et al. Extracellular matrix proteins protect small cell lung cancer cells against apoptosis: a mechanism for small cell lung cancer growth and drug resistance in vivo. Nature Med.5, 662–668 (1999). CASPubMed Google Scholar
Catlett-Falcone, R. et al. Constitutive activation of STAT3 signaling confers resistance to apoptosis in human U266 myeloma cells. Immunity10, 105–115 (1999). CASPubMed Google Scholar
Nicholson, D. W. From bench to clinic with apoptosis-based therapeutic agents. Nature407, 810–816 (2000). CASPubMed Google Scholar
Walczak, H. et al. Tumoricidal activity of tumor necrosis factor-related apoptosis- inducing ligand in vivo. Nature Med.5, 157–163 (1999).Showed that a recombinant form of TRAIL (LZ-TRAIL) could suppress tumour growthin vivowithout affecting normal tissue. CASPubMed Google Scholar
Keane, M. M., Ettenberg, S. A., Nau, M. M., Russell, E. K. & Lipkowitz, S. Chemotherapy augments TRAIL-induced apoptosis in breast cell lines. Cancer Res.59, 734–741 (1999). CASPubMed Google Scholar
Chinnaiyan, A. M. et al. Combined effect of tumor necrosis factor-related apoptosis-inducing ligand and ionizing radiation in breast cancer therapy. Proc. Natl Acad. Sci. USA97, 1754–1759 (2000). CASPubMedPubMed Central Google Scholar
Nagane, M. et al. Increased death receptor 5 expression by chemotherapeutic agents in human gliomas causes synergistic cytotoxicity with tumor necrosis factor-related apoptosis-inducing ligand in vitro and in vivo. Cancer Res.60, 847–853 (2000). CASPubMed Google Scholar
Fransen, L., Van der Heyden, J., Ruysschaert, R. & Fiers, W. Recombinant tumor necrosis factor: its effect and its synergism with interferon-γ on a variety of normal and transformed human cell lines. Eur. J. Cancer Clin. Oncol.22, 419–426 (1986). CASPubMed Google Scholar
Lienard, D., Ewalenko, P., Delmotte, J. J., Renard, N. & Lejeune, F. J. High-dose recombinant tumor necrosis factor alpha in combination with interferon γ and melphalan in isolation perfusion of the limbs for melanoma and sarcoma. J. Clin. Oncol.10, 52–60 (1992). CASPubMed Google Scholar
Daniel, P. T., Wieder, T., Sturm, I. & Schulze-Osthoff, K. The kiss of death: promises and failures of death receptors and ligands in cancer therapy. Leukemia15, 1022–1032 (2001). CASPubMed Google Scholar
Ellerby, H. M. et al. Anti-cancer activity of targeted pro-apoptotic peptides. Nature Med.5, 1032–1038 (1999). CASPubMed Google Scholar
Jansen, B. et al. BCL-2 antisense therapy chemosensitizes human melanoma in SCID mice. Nature Med.4, 232–234 (1998). CASPubMed Google Scholar
Waters, J. S. et al. Phase I clinical and pharmacokinetic study of BCL-2 antisense oligonucleotide therapy in patients with non-Hodgkin's lymphoma. J. Clin. Oncol.18, 1812–1823 (2000). CASPubMed Google Scholar
Taylor, J. K., Zhang, Q. Q., Wyatt, J. R. & Dean, N. M. Induction of endogenous BCL-xS through the control of Bcl-X pre-mRNA splicing by antisense oligonucleotides. Nature Biotechnol.17, 1097–1100 (1999). CAS Google Scholar
Zamore, P. D. RNA interference: listening to the sound of silence. Nature Struct. Biol.8, 746–750 (2001). CASPubMed Google Scholar
Bullock, A. N. & Fersht, A. R. Rescuing the function of mutant p53. Nature Rev. Cancer1, 68–76 (2001). CAS Google Scholar
Yang, C., Cirielli, C., Capogrossi, M. C. & Passaniti, A. Adenovirus-mediated wild-type p53 expression induces apoptosis and suppresses tumorigenesis of prostatic tumor cells. Cancer Res.55, 4210–4213 (1995). CASPubMed Google Scholar
Asgari, K. et al. Inhibition of the growth of pre-established subcutaneous tumor nodules of human prostate cancer cells by single injection of the recombinant adenovirus p53 expression vector. Int. J. Cancer71, 377–382 (1997). CASPubMed Google Scholar
Wang, C. Y., Cusack, J. C. Jr, Liu, R. & Baldwin, A. S. Jr. Control of inducible chemoresistance: enhanced anti-tumor therapy through increased apoptosis by inhibition of NF-κB. Nature Med.5, 412–417 (1999). PubMed Google Scholar
Huang, D. C. & Strasser, A. BH3-only proteins-essential initiators of apoptotic cell death. Cell103, 839–842 (2000). CASPubMed Google Scholar
Datta, S. R. et al. AKT phosphorylation of BAD couples survival signals to the cell- intrinsic death machinery. Cell91, 231–241 (1997). CASPubMed Google Scholar
Vogt, C. Untersuchungen über die Entwicklungsgeschichte der Geburtshelferkroete (Alytes obstetricians) (Jent & Gassmann, Solothurn, 1842). Google Scholar