Direct Repression of FLIP Expression by c-myc Is a Major Determinant of TRAIL Sensitivity

REFERENCES

• Amanullah, A., Liebermann D. A., and Hoffman B.. 2002. Deregulated c-Myc prematurely recruits both type I and II CD95/Fas apoptotic pathways associated with terminal myeloid differentiation. Oncogene 21:1600–1610.
   PubMed Web of Science ®Google Scholar
• Ashkenazi, A. 2002. Targeting death and decoy receptors of the tumour-necrosis factor superfamily. Nat. Rev. Cancer 2:420–430.
   PubMed Web of Science ®Google Scholar
• Ashkenazi, A., and Dixit V. M.. 1998. Death receptors: signaling and modulation. Science 281:1305–1308.
   PubMed Web of Science ®Google Scholar
• Ashkenazi, A., Pai R. C., Fong S., Leung S., Lawrence D. A., Marsters S. A., Blackie C., Chang L., McMurtrey A. E., Hebert A., DeForge L., Koumenis I. L., Lewis D., Harris L., Bussiere J., Koeppen H., Shahrokh Z., and Schwall R. H.. 1999. Safety and antitumor activity of recombinant soluble Apo2 ligand. J. Clin. Investig. 104:155–162.
   PubMed Web of Science ®Google Scholar
• Aza-Blanc, P., Cooper C. L., Wagner K., Batalov S., Deveraux Q. L., and Cooke M. P.. 2003. Identification of modulators of TRAIL-induced apoptosis via RNAi-based phenotypic screening. Mol. Cell 12:627–637.
   PubMed Web of Science ®Google Scholar
• Baran-Marszak, F., Fagard R., Girard B., Camilleri-Broet S., Zeng F., Lenoir G. M., Raphael M., and Feuillard J.. 2002. Gene array identification of Epstein Barr virus-regulated cellular genes in EBV-converted Burkitt lymphoma cell lines. Lab. Investig. 82:1463–1479.
   PubMedGoogle Scholar
• Blagosklonny, M. V., Prabhu N. S., and El-Deiry W. S.. 1997. Defects in p21 WAF1/CIP1, Rb, and c-myc signaling in phorbol ester-resistant cancer cells. Cancer Res. 57:320–325.
   PubMedGoogle Scholar
• Boyd, K. E., and Farnham P. J.. 1997. Myc versus USF: discrimination at the cad gene is determined by core promoter elements. Mol. Cell. Biol. 17:2529–2537.
   PubMed Web of Science ®Google Scholar
• Bullani, R. R., Huard B., Viard-Leveugle I., Byers H. R., Irmler M., Saurat J. H., Tschopp J., and French L. E.. 2001. Selective expression of FLIP in malignant melanocytic skin lesions. J. Investig. Dermatol. 117:360–364.
   PubMed Web of Science ®Google Scholar
• Burns, T., Bernhard E., and El-Diery W.. 2001. Tissue specific expression of p53 target genes suggests a key role for KILLER/DR5 in p53-dependent apoptosis in vivo. Oncogene 20:4601–4612.
   PubMed Web of Science ®Google Scholar
• Burns, T. F., and El-Deiry W. S.. 2001. Identification of inhibitors of TRAIL- induced death (ITIDs) in the TRAIL-sensitive colon carcinoma cell line SW480 using a genetic approach. J. Biol. Chem. 276:37879–37886.
   PubMed Web of Science ®Google Scholar
• Butler, J. E., and Kadonaga J. T.. 2002. The RNA polymerase II core promoter: a key component in the regulation of gene expression. Genes Dev. 16:2583–2592.
   PubMed Web of Science ®Google Scholar
• Chang, D. W., Xing Z., Pan Y., Algeciras-Schimnich A., Barnhart B. C., Yaish-Ohad S., Peter M. E., and Yang X.. 2002. c-FLIP(L) is a dual function regulator for caspase-8 activation and CD95-mediated apoptosis. EMBO J. 21:3704–3714.
   PubMed Web of Science ®Google Scholar
• Danielian, P. S., White R., Hoare S. A., Fawell S. E., and Parker M. G.. 1993. Identification of residues in the estrogen receptor that confer differential sensitivity to estrogen and hydroxytamoxifen. Mol. Endocrinol. 7:232–240.
   PubMedGoogle Scholar
• Djerbi, M., Screpanti V., Catrina A. I., Bogen B., Biberfeld P., and Grandien A.. 1999. The inhibitor of death receptor signaling, FLICE-inhibitory protein defines a new class of tumor progression factors. J. Exp. Med. 190:1025–1032.
   PubMed Web of Science ®Google Scholar
• Eischen, C. M., Packham G., Nip J., Fee B. E., Hiebert S. W., Zambetti G. P., and Cleveland J. L.. 2001. Bcl-2 is an apoptotic target suppressed by both c-Myc and E2F-1. Oncogene 20:6983–6993.
   PubMed Web of Science ®Google Scholar
• Eischen, C. M., Roussel M. F., Korsmeyer S. J., and Cleveland J. L.. 2001. Bax loss impairs Myc-induced apoptosis and circumvents the selection of p53 mutations during Myc-mediated lymphomagenesis. Mol. Cell. Biol. 21:7653–7662.
   PubMed Web of Science ®Google Scholar
• Eischen, C. M., Woo D., Roussel M. F., and Cleveland J. L.. 2001. Apoptosis triggered by Myc-induced suppression of Bcl-X(L) or Bcl-2 is bypassed during lymphomagenesis. Mol. Cell. Biol. 21:5063–5070.
   PubMed Web of Science ®Google Scholar
• Elbashir, S. M., Harborth J., Lendeckel W., Yalcin A., Weber K., and Tuschl T.. 2001. Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411:494–498.
   PubMed Web of Science ®Google Scholar
• El-Deiry, W. S. 2001. Insights into cancer therapeutic design based on p53 and TRAIL receptor signaling. Cell Death Differ 8:1066–1075.
   PubMed Web of Science ®Google Scholar
• Evan, G. I., Wyllie A. H., Gilbert C. S., Littlewood T. D., Land H., Brooks M., Waters C. M., Penn L. Z., and Hancock D. C.. 1992. Induction of apoptosis in fibroblasts by c-myc protein. Cell 69:119–128.
   PubMed Web of Science ®Google Scholar
• Fernandez, P. C., Frank S. R., Wang L., Schroeder M., Liu S., Greene J., Cocito A., and Amati B.. 2003. Genomic targets of the human c-Myc protein. Genes Dev. 17:1115–1129.
   PubMed Web of Science ®Google Scholar
• Hadano, S., Yanagisawa Y., Skaug J., Fichter K., Nasir J., Martindale D., Koop B. F., Scherer S. W., Nicholson D. W., Rouleau G. A., Ikeda J., and Hayden M. R.. 2001. Cloning and characterization of three novel genes, ALS2CR1, ALS2CR2, and ALS2CR3, in the juvenile amyotrophic lateral sclerosis (ALS2) critical region at chromosome 2q33-q34: candidate genes for ALS2. Genomics 71:200–213.
   PubMed Web of Science ®Google Scholar
• He, T. C., Zhou S., da Costa L. T., Yu J., Kinzler K. W., and Vogelstein B.. 1998. A simplified system for generating recombinant adenoviruses. Proc. Natl. Acad. Sci. USA 95:2509–2514.
   PubMed Web of Science ®Google Scholar
• Hueber, A. O., Zornig M., Lyon D., Suda T., Nagata S., and Evan G. I.. 1997. Requirement for the CD95 receptor-ligand pathway in c-Myc-induced apoptosis. Science 278:1305–1309.
   PubMed Web of Science ®Google Scholar
• Ichikawa, K., Liu W., Zhao L., Wang Z., Liu D., Ohtsuka T., Zhang H., Mountz J. D., Koopman W. J., Kimberly R. P., and Zhou T.. 2001. Tumoricidal activity of a novel anti-human DR5 monoclonal antibody without hepatocyte cytotoxicity. Nat. Med. 7:954–960.
   PubMed Web of Science ®Google Scholar
• Irmler, M., Thome M., Hahne M., Schneider P., Hofmann K., Steiner V., Bodmer J. L., Schroter M., Burns K., Mattmann C., Rimoldi D., French L. E., and Tschopp J.. 1997. Inhibition of death receptor signals by cellular FLIP. Nature 388:190–195.
   PubMed Web of Science ®Google Scholar
• Jin, Z., Dicker D. T., and El-Deiry W. S.. 2002. Enhanced sensitivity of G1 arrested human cancer cells suggests a novel therapeutic strategy using a combination of simvastatin and TRAIL. Cell Cycle 1:82–89.
   PubMed Web of Science ®Google Scholar
• Jo, M., Kim T. H., Seol D. W., Esplen J. E., Dorko K., Billiar T. R., and Strom S. C.. 2000. Apoptosis induced in normal human hepatocytes by tumor necrosis factor-related apoptosis-inducing ligand. Nat. Med. 6:564–567.
   PubMed Web of Science ®Google Scholar
• Juin, P., Hueber A. O., Littlewood T., and Evan G.. 1999. c-Myc-induced sensitization to apoptosis is mediated through cytochrome c release. Genes Dev. 13:1367–1381.
   PubMed Web of Science ®Google Scholar
• Juin, P., Hunt A., Littlewood T., Griffiths B., Swigart L. B., Korsmeyer S., and Evan G.. 2002. c-Myc functionally cooperates with Bax to induce apoptosis. Mol. Cell. Biol. 22:6158–6169.
   PubMedGoogle Scholar
• Kim, I. K., Jung Y. K., Noh D. Y., Song Y. S., Choi C. H., Oh B. H., and Masuda E. S.. 2003. Functional screening of genes suppressing TRAIL-induced apoptosis: distinct inhibitory activities of Bcl-XL and Bcl-2. Br. J. Cancer 88:910–917.
   PubMedGoogle Scholar
• Kim, K., Fisher M. J., Xu S.-Q., and El-Deiry W. S.. 2000. Molecular determinants of response to TRAIL in killing of normal and cancer cells. Clin. Cancer Res. 6:335–346.
   PubMed Web of Science ®Google Scholar
• Klefstrom, J., Vastrik I., Saksela E., Valle J., Eilers M., and Alitalo K.. 1994. c-Myc induces cellular susceptibility to the cytotoxic action of TNF-alpha. EMBO J. 13:5442–5450.
   PubMed Web of Science ®Google Scholar
• Krueger, A., Baumann S., Krammer P. H., and Kirchhoff S.. 2001. FLICE- inhibitory proteins: regulators of death receptor-mediated apoptosis. Mol. Cell. Biol. 21:8247–8254.
   PubMed Web of Science ®Google Scholar
• Krueger, A., Schmitz I., Baumann S., Krammer P. H., and Kirchhoff S.. 2001. Cellular FLICE-inhibitory protein splice variants inhibit different steps of caspase-8 activation at the CD95 death-inducing signaling complex. J. Biol. Chem. 276:20633–20640.
   PubMed Web of Science ®Google Scholar
• Lawrence, D., Shahrokh Z., Marsters S., Achilles K., Shih D., Mounho B., Hillan K., Totpal K., DeForge L., Schow P., Hooley J., Sherwood S., Pai R., Leung S., Khan L., Gliniak B., Bussiere J., Smith C. A., Strom S. S., Kelley S., Fox J. A., Thomas D., and Ashkenazi A.. 2001. Differential hepatocyte toxicity of recombinant Apo2L/TRAIL versions. Nat. Med. 7:383–385.
   PubMed Web of Science ®Google Scholar
• Littlewood, T. D., Hancock D. C., Danielian P. S., Parker M. G., and Evan G. I.. 1995. A modified oestrogen receptor ligand-binding domain as an improved switch for the regulation of heterologous proteins. Nucleic Acids Res. 23:1686–1690.
   PubMed Web of Science ®Google Scholar
• Lutz, W., Fulda S., Jeremias I., Debatin K. M., and Schwab M.. 1998. MycN and IFNgamma cooperate in apoptosis of human neuroblastoma cells. Oncogene 17:339–346.
   PubMed Web of Science ®Google Scholar
• MacLachlan, T. K., and El-Deiry W. S.. 2003. Identification of DNA-binding of tumor suppressor genes by chromatin immunoprecipitation. Methods Mol. Biol. 223:129–133.
   PubMedGoogle Scholar
• Maclean, K. H., Keller U. B., Rodriguez-Galindo C., Nilsson J. A., and Cleveland J. L.. 2003. c-Myc augments gamma irradiation-induced apoptosis by suppressing Bcl-XL. Mol. Cell. Biol. 23:7256–7270.
   PubMed Web of Science ®Google Scholar
• Magrath, I. 1990. The pathogenesis of Burkitt's lymphoma. Adv. Cancer Res. 55:133–270.
   PubMedGoogle Scholar
• Medema, J. P., de Jong J., van Hall T., Melief C. J., and Offringa R.. 1999. Immune escape of tumors in vivo by expression of cellular FLICE-inhibitory protein. J. Exp. Med. 190:1033–1038.
   PubMed Web of Science ®Google Scholar
• Menssen, A., and Hermeking H.. 2002. Characterization of the c-MYC- regulated transcriptome by SAGE: identification and analysis of c-MYC target genes. Proc. Natl. Acad. Sci. USA 99:6274–6279.
   PubMed Web of Science ®Google Scholar
• Micheau, O., Thome M., Schneider P., Holler N., Tschopp J., Nicholson D. W., Briand C., and Grutter M. G.. 2002. The long form of FLIP is an activator of caspase-8 at the Fas death-inducing signaling complex. J. Biol. Chem. 277:45162–45171.
   PubMedGoogle Scholar
• Mitchell, K. O., and El-Deiry W. S.. 1999. Overexpression of c-Myc inhibits p21WAF1/CIP1 expression and induces S-phase entry in 12-O-tetradecanoylphorbol-13-acetate (TPA)-sensitive human cancer cells. Cell Growth Differ. 10:223–230.
   PubMedGoogle Scholar
• Mitchell, K. O., Ricci M. S., Miyashita T., Dicker D. T., Jin Z., Reed J. C., and El-Deiry W. S.. 2000. Bax is a transcriptional target and mediator of c-myc- induced apoptosis. Cancer Res. 60:6318–6325.
   PubMed Web of Science ®Google Scholar
• Mouzakiti, A., and Packham G.. 2003. Regulation of tumour necrosis factor- related apoptosis-inducing ligand (TRAIL)-induced apoptosis in Burkitt's lymphoma cell lines. Br. J. Haematol. 122:61–69.
   PubMedGoogle Scholar
• Nesbit, C. E., Tersak J. M., and Prochownik E. V.. 1999. MYC oncogenes and human neoplastic disease. Oncogene 18:3004–3016.
   PubMed Web of Science ®Google Scholar
• Ngo, C. V., Gee M., Akhtar N., Yu D., Volpert O., Auerbach R., and Thomas-Tikhonenko A.. 2000. An in vivo function for the transforming Myc protein: elicitation of the angiogenic phenotype. Cell Growth Differ. 11:201–210.
   PubMedGoogle Scholar
• Ozoren, N., Fisher M. J., Kim K., Liu C. X., Genin A., Shifman Y., Dicker D. T., Spinner N. B., Lisitsyn N. A., and El-Deiry W. S.. 2000. Homozygous deletion of the death receptor DR4 gene in a nasopharyngeal cancer cell line is associated with TRAIL resistance. Int. J. Oncol. 16:917–925.
   PubMed Web of Science ®Google Scholar
• Ozoren, N., Kim K., Burns T. F., Dicker D. T., Moscioni A. D., and El- Deiry W. S.. 2000. The caspase 9 inhibitor Z-LEHD-FMK protects human liver cells while permitting death of cancer cells exposed to tumor necrosis factor-related apoptosis-inducing ligand. Cancer Res. 60:6259–6265.
   PubMed Web of Science ®Google Scholar
• Pear, W. S., Miller J. P., Xu L., Pui J. C., Soffer B., Quackenbush R. C., Pendergast A. M., Bronson R., Aster J. C., Scott M. L., and Baltimore D.. 1998. Efficient and rapid induction of a chronic myelogenous leukemia-like myeloproliferative disease in mice receiving P210 bcr/abl-transduced bone marrow. Blood 92:3780–3792.
   PubMed Web of Science ®Google Scholar
• Pelengaris, S., Khan M., and Evan G.. 2002. c-myc: more than just a matter of life and death. Nat. Rev. Cancer 2:764–776.
   PubMed Web of Science ®Google Scholar
• Prabhu, N. S., Blagosklonny M. V., Zeng Y.-U., Wu G. S., Waldman T., and El-Deiry W. S.. 1996. Suppression of cancer cell growth by adenovirus expressing p21WAF1/CIP1 deficient in PCNA interaction. Clin. Cancer Res. 2:1221–1229.
   PubMedGoogle Scholar
• Roth, W., Isenmann S., Naumann U., Kugler S., Bahr M., Dichgans J., Ashkenazi A., and Weller M.. 1999. Locoregional Apo2L/TRAIL eradicates intracranial human malignant glioma xenografts in athymic mice in the absence of neurotoxicity. Biochem. Biophys. Res. Commun. 265:479–483.
   PubMed Web of Science ®Google Scholar
• Ruf, I. K., Rhyne P. W., Yang H., Borza C. M., Hutt-Fletcher L. M., Cleveland J. L., and Sample J. T.. 1999. Epstein-Barr virus regulates c-Myc, apoptosis, and tumorigenicity in Burkitt lymphoma. Mol. Cell. Biol. 19:1651–1660.
   PubMedGoogle Scholar
• Sevignani, C., Wlodarski P., Kirillova J., Mercer W. E., Danielson K. G., Iozzo R. V., and Calabretta B.. 1998. Tumorigenic conversion of p53-deficient colon epithelial cells by an activated Ki-ras gene. J. Clin. Investig. 101:1572–1580.
   PubMedGoogle Scholar
• Shivapurkar, N., Reddy J., Matta H., Sathyanarayana U. G., Huang C. X., Toyooka S., Minna J. D., Chaudhary P. M., and Gazdar A. F.. 2002. Loss of expression of death-inducing signaling complex (DISC) components in lung cancer cell lines and the influence of MYC amplification. Oncogene 21:8510–8514.
   PubMed Web of Science ®Google Scholar
• Soucie, E. L., Annis M. G., Sedivy J., Filmus J., Leber B., Andrews D. W., and Penn L. Z.. 2001. Myc potentiates apoptosis by stimulating Bax activity at the mitochondria. Mol. Cell. Biol. 21:4725–4736.
   PubMedGoogle Scholar
• Tepper, C. G., and Seldin M. F.. 1999. Modulation of caspase-8 and FLICE- inhibitory protein expression as a potential mechanism of Epstein-Barr virus tumorigenesis in Burkitt's lymphoma. Blood 94:1727–1737.
   PubMed Web of Science ®Google Scholar
• Thomas, R. K., Kallenborn A., Wickenhauser C., Schultze J. L., Draube A., Vockerodt M., Re D., Diehl V., and Wolf J.. 2002. Constitutive expression of c- FLIP in Hodgkin and Reed-Sternberg cells. Am. J. Pathol. 160:1521–1528.
   PubMed Web of Science ®Google Scholar
• Thome, M., Schneider P., Hofmann K., Fickenscher H., Meinl E., Neipel F., Mattmann C., Burns K., Bodmer J. L., Schroter M., Scaffidi C., Krammer P. H., Peter M. E., and Tschopp J.. 1997. Viral FLICE-inhibitory proteins (FLIPs) prevent apoptosis induced by death receptors. Nature 386:517–521.
   PubMed Web of Science ®Google Scholar
• Walczak, H., Miller R. E., Ariail K., Gliniak B., Griffith T. S., Kubin M., Chin W., Jones J., Woodward A., Le T., Smith C., Smolak P., Goodwin R. G., Rauch C. T., Schuh J. C., and Lynch D. H.. 1999. Tumoricidal activity of tumor necrosis factor-related apoptosis-inducing ligand in vivo. Nat. Med. 5:157–163.
   PubMed Web of Science ®Google Scholar
• Wanzel, M., Herold S., and Eilers M.. 2003. Transcriptional repression by Myc. Trends Cell Biol. 13:146–150.
   PubMedGoogle Scholar
• Woods, D., Parry D., Cherwinski H., Bosch E., Lees E., and McMahon M.. 1997. Raf-induced proliferation or cell cycle arrest is determined by the level of Raf activity with arrest mediated by p21Cip1. Mol. Cell. Biol. 17:5598–5611.
   PubMed Web of Science ®Google Scholar
• Wu, G. S., and El-Deiry W. S.. 1996. Apoptotic death of tumor cells correlates with chemosensitivity, independent of p53 or bcl-2. Clin Cancer Res. 2:623–633.
   PubMedGoogle Scholar
• Xu, D., Popov N., Hou M., Wang Q., Bjorkholm M., Gruber A., Menkel A. R., and Henriksson M.. 2001. Switch from Myc/Max to Mad1/Max binding and decrease in histone acetylation at the telomerase reverse transcriptase promoter during differentiation of HL60 cells. Proc. Natl. Acad. Sci. USA 98:3826–3831.
   PubMed Web of Science ®Google Scholar
• Yu, D., Allman D., Goldschmidt M. H., Atchison M. L., Monroe J. G., and Thomas-Tikhonenko A.. 2003. Oscillation between B-lymphoid and myeloid lineages in Myc-induced hematopoietic tumors following spontaneous silencing/reactivation of the EBF/Pax5 pathway. Blood 101:1950–1955.
   PubMedGoogle Scholar
• Yu, D., and Thomas-Tikhonenko A.. 2002. A non-transgenic mouse model for B-cell lymphoma: in vivo infection of p53-null bone marrow progenitors by a Myc retrovirus is sufficient for tumorigenesis. Oncogene 21:1922–1927.
   PubMedGoogle Scholar
• Zeller, K. I., Jegga A. G., Aronow B. J., O'Donnell K. A., and Dang C. V.. 2003. An integrated database of genes responsive to the Myc oncogenic transcription factor: identification of direct genomic targets. Genome Biol. 4:R69.
   PubMed Web of Science ®Google Scholar