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

REFERENCES

• Angel, P., Allegretto, E. A., Okino, S. T., Hattori, K., Boyle, W. J., Hunter, T., and Karin, M.. 1988. Oncogene jun encodes a sequence-specific trans-activator similar to AP-1. Nature 332:166–171
   PubMed Web of Science ®Google Scholar
• Angel, P., Hattori, K., Smeal, T., and Karin, M.. 1988. The jun proto-oncogene is positively autoregulated by its product, Jun/AP-1. Cell 55:875–885
   PubMed Web of Science ®Google Scholar
• Behrens, A., Sibilia, M., and Wagner, E. F.. 1999. Amino-terminal phosphorylation of c-Jun regulates stress-induced apoptosis and cellular proliferation. Nat. Genet. 21:326–329
   PubMed Web of Science ®Google Scholar
• Berndt, C., Mopps, B., Angermuller, S., Gierschik, P., and Krammer, P. H.. 1998. CXCR4 and CD4 mediate a rapid CD95-independent cell death in CD4(+) T cells. Proc. Natl. Acad. Sci. USA 95:12556–12561
   PubMed Web of Science ®Google Scholar
• Berry, M. N., and Friend, D. S.. 1969. High-yield preparation of isolated rat liver parenchymal cells: a biochemical and fine structural study. J. Cell Biol. 43:506–520
   PubMed Web of Science ®Google Scholar
• Brunner, T., Mogil, R. J., LaFace, D., Yoo, N. J., Mahboubi, A., Echeverri, F., Martin, S. J., Force, W. R., Lynch, D. H., Ware, C. F. et al. 1995. Cell-autonomous Fas (CD95)/Fas-ligand interaction mediates activation-induced apoptosis in T-cell hybridomas. Nature 373:441–444
   PubMed Web of Science ®Google Scholar
• Caricchio, R., Reap, E. A., and Cohen, P. L.. 1998. Fas/Fas ligand interactions are involved in ultraviolet-B-induced human lymphocyte apoptosis. J. Immunol. 161:241–251
   PubMed Web of Science ®Google Scholar
• Chan, H., Bartos, D. P., and Owen-Schaub, L. B.. 1999. Activation-dependent transcriptional regulation of the human Fas promoter requires NF-kappaB p50-p65 recruitment. Mol. Cell. Biol. 19:2098–2108
   PubMed Web of Science ®Google Scholar
• Chen, C., and Okayama, H.. 1987. High-efficiency transformation of mammalian cells by plasmid DNA. Mol. Cell. Biol. 7:2745–2752
   PubMed Web of Science ®Google Scholar
• Chen, Z., Seimiya, H., Naito, M., Mashima, T., Kizaki, A., Dan, S., Imaizumi, M., Ichijo, H., Miyazono, K., and Tsuruo, T.. 1999. ASK1 mediates apoptotic cell death induced by genotoxic stress. Oncogene 18:173–180
   PubMed Web of Science ®Google Scholar
• Dhein, J., Walczak, H., Baumler, C., Debatin, K. M., and Krammer, P. H.. 1995. Autocrine T-cell suicide mediated by APO-1/(Fas/CD95). Nature 373:438–441
   PubMed Web of Science ®Google Scholar
• Dignam, J. D., Lebovitz, R. M., and Roeder, R. G.. 1983. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11:1475–1489
   PubMed Web of Science ®Google Scholar
• Eferl, R., Sibilia, M., Hilberg, F., Fuchsbichler, A., Kufferath, I., Guertl, B., Zenz, R., Wagner, E. F., and Zatloukal, K.. 1999. Functions of c-Jun in liver and heart development. J. Cell Biol. 145:1049–1061
   PubMedGoogle Scholar
• Elkeles, A., Juven-Gershon, T., Israeli, D., Wilder, S., Zalcenstein, A., and Oren, M.. 1999. The c-fos proto-oncogene is a target for transactivation by the p53 tumor suppressor. Mol. Cell. Biol. 19:2594–2600
   PubMed Web of Science ®Google Scholar
• Faris, M., Kokot, N., Latinis, K., Kasibhatla, S., Green, D. R., Koretzky, G. A., and Nel, A.. 1998. The c-Jun N-terminal kinase cascade plays a role in stress-induced apoptosis in Jurkat cells by up-regulating Fas ligand expression. J. Immunol. 160:134–144
   PubMed Web of Science ®Google Scholar
• Faris, M., Latinis, K. M., Kempiak, S. J., Koretzky, G. A., and Nel, A.. 1998. Stress-induced Fas ligand expression in T cells is mediated through a MEK kinase 1-regulated response element in the Fas ligand promoter. Mol. Cell. Biol. 18:5414–5424
   PubMedGoogle Scholar
• Fisher, D. E.. 1994. Apoptosis in cancer therapy: crossing the threshold. Cell 78:539–542
   PubMed Web of Science ®Google Scholar
• Friesen, C., Herr, I., Krammer, P. H., and Debatin, K. M.. 1996. Involvement of the CD95 (APO-1/FAS) receptor/ligand system in drug-induced apoptosis in leukemia cells. Nat. Med. 2:574–577
   PubMed Web of Science ®Google Scholar
• Fuchs, S. Y., Adler, V., Pincus, M. R., and Ronai, Z.. 1998. MEKK1/JNK signaling stabilizes and activates p53. Proc. Natl. Acad. Sci. USA 95:10541–10546
   PubMed Web of Science ®Google Scholar
• Fulda, S., Scaffidi, C., Pietsch, T., Krammer, P. H., Peter, M. E., and Debatin, K. M.. 1998. Activation of the CD95 (APO-1/Fas) pathway in drug- and gamma-irradiation-induced apoptosis of brain tumor cells. Cell Death Differ. 5:884–893
   PubMed Web of Science ®Google Scholar
• Gibson, S., Widmann, C., and Johnson, G. L.. 1999. Differential involvement of MEK kinase 1 (MEKK1) in the induction of apoptosis in response to microtubule-targeted drugs versus DNA damaging agents. J. Biol. Chem. 274:10916–10922
   PubMed Web of Science ®Google Scholar
• Gibson, S. B., Oyer, R., Spalding, A. C., Anderson, S. M., and Johnson, G. L.. 2000. Increased expression of death receptors 4 and 5 synergizes the apoptosis response to combined treatment with etoposide and TRAIL. Mol. Cell. Biol. 20:205–212
   PubMed Web of Science ®Google Scholar
• Griffith, T. S., Brunner, T., Fletcher, S. M., Green, D. R., and Ferguson, T. A.. 1995. Fas ligand-induced apoptosis as a mechanism of immune privilege. Science 270:1189–1192
   PubMed Web of Science ®Google Scholar
• Hakem, R., Hakem, A., Duncan, G. S., Henderson, J. T., Woo, M., Soengas, M. S., Elia, A., De la Pompa, J. L., Kagi, D., Khoo, W., Potter, J., Yoshida, R., Kaufman, S. A., Lowe, S. W., Penninger, J. M., and Mak, T. W.. 1998. Differential requirement for caspase 9 in apoptotic pathways in vivo. Cell 94:339–352
   PubMed Web of Science ®Google Scholar
• Herr, I., Wilhelm, D., Bohler, T., Angel, P., and Debatin, K. M.. 1999. JNK/SAPK activity is not sufficient for anticancer therapy-induced apoptosis involving CD95-L, TRAIL and TNF-alpha. Int. J. Cancer 80:417–424
   PubMedGoogle Scholar
• Hill, L. L., Ouhtit, A., Loughlin, S. M., Kripke, M. L., Ananthaswamy, H. N., and Owen-Schaub, L. B.. 1999. Fas ligand: a sensor for DNA damage critical in skin cancer etiology. Science 285:898–900
   PubMed Web of Science ®Google Scholar
• Houghton, J. A., Harwood, F. G., and Tillman, D. M.. 1997. Thymineless death in colon carcinoma cells is mediated via fas signaling. Proc. Natl. Acad. Sci. USA 94:8144–8149
   PubMed Web of Science ®Google Scholar
• Kasibhatla, S., Brunner, T., Genestier, L., Echeverri, F., Mahboubi, A., and Green, D. R.. 1998. DNA damaging agents induce expression of Fas ligand and subsequent apoptosis in T lymphocytes via the activation of NF-kappa B and AP-1. Mol. Cell 1:543–551
   PubMed Web of Science ®Google Scholar
• Kastan, M. B., Onyekwere, O., Sidransky, D., Vogelstein, B., and Craig, R. W.. 1991. Participation of p53 protein in the cellular response to DNA damage. Cancer Res. 51:6304–6311
   PubMed Web of Science ®Google Scholar
• Klas, C., Debatin, K. M., Jonker, R. R., and Krammer, P. H.. 1993. Activation interferes with the APO-1 pathway in mature human T cells. Int. Immunol. 5:625–630
   PubMed Web of Science ®Google Scholar
• Kolbus, A., Herr, I., Schreiber, M., Debatin, K. M., Wagner, E. F., and Angel, P.. 2000. c-Jun-dependent CD95-L expression is a rate-limiting step in the induction of apoptosis by alkylating agents. Mol. Cell. Biol. 20:575–582
   PubMedGoogle Scholar
• Krammer, P. H.. 1999. CD95(APO-1/Fas)-mediated apoptosis: live and let die. Adv. Immunol. 71:163–210
   PubMedGoogle Scholar
• Krammer, P. H., Galle, P. R., Moller, P., and Debatin, K. M.. 1998. CD95(APO-1/Fas)-mediated apoptosis in normal and malignant liver, colon, and hematopoietic cells. Adv. Cancer Res. 75:251–273
   PubMed Web of Science ®Google Scholar
• Kuida, K., Haydar, T. F., Kuan, C. Y., Gu, Y., Taya, C., Karasuyama, H., Su, M. S., Rakic, P., and Flavell, R. A.. 1998. Reduced apoptosis and cytochrome c-mediated caspase activation in mice lacking caspase 9. Cell 94:325–337
   PubMed Web of Science ®Google Scholar
• Latinis, K. M., Norian, L. A., Eliason, S. L., and Koretzky, G. A.. 1997. Two NFAT transcription factor binding sites participate in the regulation of CD95 (Fas) ligand expression in activated human T cells. J. Biol. Chem. 272:31427–31434
   PubMedGoogle Scholar
• Lee, L. F., Li, G., Templeton, D. J., and Ting, J. P.. 1998. Paclitaxel (Taxol)-induced gene expression and cell death are both mediated by the activation of c-Jun NH2-terminal kinase (JNK/SAPK). J. Biol. Chem. 273:28253–28260
   PubMed Web of Science ®Google Scholar
• Le-Niculescu, H., Bonfoco, E., Kasuya, Y., Claret, F. X., Green, D. R., and Karin, M.. 1999. Withdrawal of survival factors results in activation of the JNK pathway in neuronal cells leading to Fas ligand induction and cell death. Mol. Cell. Biol. 19:751–763
   PubMed Web of Science ®Google Scholar
• Leppa, S., Saffrich, R., Ansorge, W., and Bohmann, D.. 1998. Differential regulation of c-Jun by ERK and JNK during PC12 cell differentiation. EMBO J. 17:4404–4413
   PubMed Web of Science ®Google Scholar
• Levine, A. J.. 1997. p53, the cellular gatekeeper for growth and division. Cell 88:323–331
   PubMed Web of Science ®Google Scholar
• Li, N., and Karin, M.. 1998. Ionizing radiation and short wavelength UV activate NF-kappaB through two distinct mechanisms. Proc. Natl. Acad. Sci. USA 95:13012–13017
   PubMed Web of Science ®Google Scholar
• Li-Weber, M., Laur, O., Hekele, A., Coy, J., Walczak, H., and Krammer, P. H.. 1998. A regulatory element in the CD95 (APO-1/Fas) ligand promoter is essential for responsiveness to TCR-mediated activation. Eur. J. Immunol. 28:2373–2383
   PubMedGoogle Scholar
• Los, M., Wesselborg, S., and Schulze-Osthoff, K.. 1999. The role of caspases in development, immunity, and apoptotic signal transduction: lessons from knockout mice. Immunity 10:629–639
   PubMed Web of Science ®Google Scholar
• Lowe, S. W., Ruley, H. E., Jacks, T., and Housman, D. E.. 1993. p53-dependent apoptosis modulates the cytotoxicity of anticancer agents. Cell 74:957–967
   PubMed Web of Science ®Google Scholar
• Marks-Konczalik, J., Chu, S. C., and Moss, J.. 1998. Cytokine-mediated transcriptional induction of the human inducible nitric oxide synthase gene requires both activator protein 1 and nuclear factor kappaB-binding sites. J. Biol. Chem. 273:22201–22208
   PubMed Web of Science ®Google Scholar
• Matsui, K., Xiao, S., Fine, A., and Ju, S. T.. 2000. Role of activator protein-1 in TCR-mediated regulation of the murine fas1 promoter. J. Immunol. 164:3002–3008
   PubMedGoogle Scholar
• McClure, R. F., Heppelmann, C. J., and Paya, C. V.. 1999. Constitutive Fas ligand gene transcription in Sertoli cells is regulated by Sp1. J. Biol. Chem. 274:7756–7762
   PubMed Web of Science ®Google Scholar
• Muller, M., Strand, S., Hug, H., Heinemann, E. M., Walczak, H., Hofmann, W. J., Stremmel, W., Krammer, P. H., and Galle, P. R.. 1997. 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. Investig. 99:403–413
   PubMed Web of Science ®Google Scholar
• Muller, M., Wilder, S., Bannasch, D., Israeli, D., Lehlbach, K., Li-Weber, M., Friedman, S. L., Galle, P. R., Stremmel, W., Oren, M., and Krammer, P. H.. 1998. p53 activates the CD95 (APO-1/Fas) gene in response to DNA damage by anticancer drugs. J. Exp. Med. 188:2033–2045
   PubMed Web of Science ®Google Scholar
• Nagata, S., and Golstein, P.. 1995. The Fas death factor. Science 267:1449–1456
   PubMed Web of Science ®Google Scholar
• Neubauer, K., Eichhorst, S. T., Wilfling, T., Buchenau, M., Xia, L., and Ramadori, G.. 1998. Sinusoidal intercellular adhesion molecule-1 up-regulation precedes the accumulation of leukocyte function antigen-1-positive cells and tissue necrosis in a model of carbontetrachloride-induced acute rat liver injury. Lab. Investig. 78:185–194
   PubMed Web of Science ®Google Scholar
• Newton, K., and Strasser, A.. 2000. Ionizing radiation and chemotherapeutic drugs induce apoptosis in lymphocytes in the absence of Fas of FADD/MORT1 signaling: implications for cancer therapy. J. Exp. Med. 191:195–200
   PubMed Web of Science ®Google Scholar
• Nicoletti, I., Migliorati, G., Pagliacci, M. C., Grignani, F., and Riccardi, C.. 1991. A rapid and simple method for measuring thymocyte apoptosis by propidium iodide staining and flow cytometry. J. Immunol. Methods 139:271–279
   PubMed Web of Science ®Google Scholar
• Nishina, H., Vaz, C., Billia, P., Nghiem, M., Sasaki, T., De la Pompa, J. L., Furlonger, K., Paige, C., Hui, C., Fischer, K. D., Kishimoto, H., Iwatsubo, T., Katada, T., Woodgett, J. R., and Penninger, J. M.. 1999. Defective liver formation and liver cell apoptosis in mice lacking the stress signaling kinase SEK1/MKK4. Development 126:505–516
   PubMedGoogle Scholar
• Norian, L. A., Latinis, K. M., and Koretzky, G. A.. 1998. A newly identified response element in the CD95 ligand promoter contributes to optimal inducibility in activated T lymphocytes. J. Immunol. 161:1078–1082
   PubMedGoogle Scholar
• Peter, M. E., Scaffidi, C., Medema, J. P., Kischkel, F., and Krammer, P. H.. 1999. The death receptors. Results Probl. Cell Differ. 23:25–63
   PubMedGoogle Scholar
• Preston, G. A., Lyon, T. T., Yin, Y., Lang, J. E., Solomon, G., Annab, L., Srinivasan, D. G., Alcorta, D. A., and Barrett, J. C.. 1996. Induction of apoptosis by c-Fos protein. Mol. Cell. Biol. 16:211–218
   PubMed Web of Science ®Google Scholar
• Radler-Pohl, A., Sachsenmaier, C., Gebel, S., Auer, H. P., Bruder, J. T., Rapp, U., Angel, P., Rahmsdorf, H. J., and Herrlich, P.. 1993. UV-induced activation of AP-1 involves obligatory extranuclear steps including Raf-1 kinase. EMBO J. 12:1005–1012
   PubMedGoogle Scholar
• Sanchez-Perez, I., and Perona, R.. 1999. Lack of c-Jun activity increases survival to cisplatin. FEBS Lett. 453:151–158
   PubMedGoogle Scholar
• Scaffidi, C., Fulda, S., Srinivasan, A., Friesen, C., Li, F., Tomaselli, K. J., Debatin, K. M., Krammer, P. H., and Peter, M. E.. 1998. Two CD95 (APO-1/Fas) signaling pathways. EMBO J. 17:1675–1687
   PubMed Web of Science ®Google Scholar
• Schroder, A. J., Blaheta, R. A., Scholz, M., Encke, A., and Markus, B. H.. 1994. Isolation and separation of human adult hepatocytes from resected liver: cellular yield and purity using different methods. ZBL Chir. 119:127–138
   PubMedGoogle Scholar
• Sheard, M. A., Vojtesek, B., Janakova, L., Kovarik, J., and Zaloudik, J.. 1997. Up-regulation of Fas (CD95) in human p53 wild-type cancer cells treated with ionizing radiation. Int. J. Cancer 73:757–762
   PubMed Web of Science ®Google Scholar
• Srivastava, R. K., Sasaki, C. Y., Hardwick, J. M., and Longo, D. L.. 1999. Bcl-2-mediated drug resistance: inhibition of apoptosis by blocking nuclear factor of activated T lymphocytes (NFAT)-induced Fas ligand transcription. J. Exp. Med. 190:253–265
   PubMedGoogle Scholar
• van Dam, H., Wilhelm, D., Herr, I., Steffen, A., Herrlich, P., and Angel, P.. 1995. ATF-2 is preferentially activated by stress-activated protein kinases to mediate c-jun induction in response to genotoxic agents. EMBO J. 14:1798–1811
   PubMed Web of Science ®Google Scholar
• Varfolomeev, E. E., Schuchmann, M., Luria, V., Chiannilkulchai, N., Beckmann, J. S., Mett, I. L., Rebrikov, D., Brodianski, V. M., Kemper, O. C., Kollet, O., Lapidot, T., Soffer, D., Sobe, T., Avraham, K. B., Goncharov, T., Holtmann, H., Lonai, P., and Wallach, D.. 1998. Targeted disruption of the mouse Caspase 8 gene ablates cell death induction by the TNF receptors, Fas/Apo1, and DR3 and is lethal prenatally. Immunity 9:267–276
   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
• Widmann, C., Gerwins, P., Johnson, N. L., Jarpe, M. B., and Johnson, G. L.. 1998. MEK kinase 1, a substrate for DEVD-directed caspases, is involved in genotoxin-induced apoptosis. Mol. Cell. Biol. 18:2416–2429
   PubMed Web of Science ®Google Scholar
• Wilhelm, D., Bender, K., Knebel, A., and Angel, P.. 1997. The level of intracellular glutathione is a key regulator for the induction of stress-activated signal transduction pathways including Jun N-terminal protein kinases and p38 kinase by alkylating agents. Mol. Cell. Biol. 17:4792–4800
   PubMed Web of Science ®Google Scholar
• Williams, B. A., Makrigiannis, A. P., Blay, J., and Hoskin, D. W.. 1997. Treatment of the P815 murine mastocytoma with cisplatin or etoposide up-regulates cell-surface Fas (CD95) expression and increases sensitivity to anti-Fas antibody-mediated cytotoxicity and to lysis by anti-CD3-activated killer-T cells. Int. J. Cancer 73:416–423
   PubMedGoogle Scholar
• Wisdom, R., Johnson, R. S., and Moore, C.. 1999. c-Jun regulates cell cycle progression and apoptosis by distinct mechanisms. EMBO J. 18:188–197
   PubMed Web of Science ®Google Scholar
• Yoshida, H., Kong, Y. Y., Yoshida, R., Elia, A. J., Hakem, A., Hakem, R., Penninger, J. M., and Mak, T. W.. 1998. Apaf1 is required for mitochondrial pathways of apoptosis and brain development. Cell 94:739–750
   PubMed Web of Science ®Google Scholar
• Yujiri, T., Sather, S., Fanger, G. R., and Johnson, G. L.. 1998. Role of MEKK1 in cell survival and activation of JNK and ERK pathways defined by targeted gene disruption. Science 282:1911–1914
   PubMed Web of Science ®Google Scholar
• Zanke, B. W., Rubie, E. A., Winnett, E., Chan, J., Randall, S., Parsons, M., Boudreau, K., McInnis, M., Yan, M., Templeton, D. J., and Woodgett, J. R.. 1996. Mammalian mitogen-activated protein kinase pathways are regulated through formation of specific kinase-activator complexes. J. Biol. Chem. 271:29876–29881
   PubMed Web of Science ®Google Scholar