Viral FLIP Enhances Wnt Signaling Downstream of Stabilized β-Catenin, Leading to Control of Cell Growth

REFERENCES

• Aberle, H., A. Bauer, J. Stappert, A. Kispert, and R. Kemler. 1997. beta-catenin is a target for the ubiquitin-proteasome pathway. EMBO J. 16:3797–3804.
   PubMed Web of Science ®Google Scholar
• An, J., Y. Sun, R. Sun, and M. B. Rettig. 2003. Kaposi's sarcoma-associated herpesvirus encoded vFLIP induces cellular IL-6 expression: the role of the NF-kappaB and JNK/AP1 pathways. Oncogene 22:3371–3385.
   PubMedGoogle Scholar
• Balachandran, S., C. N. Kim, W. C. Yeh, T. W. Mak, K. Bhalla, and G. N. Barber. 1998. Activation of the dsRNA-dependent protein kinase, PKR, induces apoptosis through FADD-mediated death signaling. EMBO J. 17:6888–6902.
   PubMed Web of Science ®Google Scholar
• Behrens, J., J. P. von Kries, M. Kuhl, L. Bruhn, D. Wedlich, R. Grosschedl, and W. Birchmeier. 1996. Functional interaction of beta-catenin with the transcription factor LEF-1. Nature 382:638–642.
   PubMed Web of Science ®Google Scholar
• Belanger, C., A. Gravel, A. Tomoiu, M. E. Janelle, J. Gosselin, M. J. Tremblay, and L. Flamand. 2001. Human herpesvirus 8 viral FLICE-inhibitory protein inhibits Fas-mediated apoptosis through binding and prevention of procaspase-8 maturation. J. Hum. Virol. 4:62–73.
   PubMedGoogle Scholar
• Bertin, J., R. C. Armstrong, S. Ottilie, D. A. Martin, Y. Wang, S. Banks, G. H. Wang, T. G. Senkevich, E. S. Alnemri, B. Moss, M. J. Lenardo, K. J. Tomaselli, and J. I. Cohen. 1997. Death effector domain-containing herpesvirus and poxvirus proteins inhibit both Fas- and TNFR1-induced apoptosis. Proc. Natl. Acad. Sci. USA 94:1172–1176.
   PubMed Web of Science ®Google Scholar
• Boldin, M. P., T. M. Goncharov, Y. V. Goltsev, and D. Wallach. 1996. Involvement of MACH, a novel MORT1/FADD-interacting protease, in Fas/APO-1- and TNF receptor-induced cell death. Cell 85:803–815.
   PubMed Web of Science ®Google Scholar
• Cadigan, K. M., and R. Nusse. 1997. Wnt signaling: a common theme in animal development. Genes Dev. 11:3286–3305.
   PubMed Web of Science ®Google Scholar
• Chaudhary, P. M., A. Jasmin, M. T. Eby, and L. Hood. 1999. Modulation of the NF-kappa B pathway by virally encoded death effector domains-containing proteins. Oncogene 18:5738–5746.
   PubMed Web of Science ®Google Scholar
• Chinnaiyan, A. M., K. O'Rourke, M. Tewari, and V. M. Dixit. 1995. FADD, a novel death domain-containing protein, interacts with the death domain of Fas and initiates apoptosis. Cell 81:505–512.
   PubMed Web of Science ®Google Scholar
• Djerbi, M., V. Screpanti, A. I. Catrina, B. Bogen, P. Biberfeld, and A. Grandien. 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
• Field, N., W. Low, M. Daniels, S. Howell, L. Daviet, C. Boshoff, and M. Collins. 2003. KSHV vFLIP binds to IKK-gamma to activate IKK. J. Cell Sci. 116:3721–3728.
   PubMed Web of Science ®Google Scholar
• Goltsev, Y. V., A. V. Kovalenko, E. Arnold, E. E. Varfolomeev, V. M. Brodianskii, and D. Wallach. 1997. CASH, a novel caspase homologue with death effector domains. J. Biol. Chem. 272:19641–19644.
   PubMed Web of Science ®Google Scholar
• Gounari, F., I. Aifantis, K. Khazaie, S. Hoeflinger, N. Harada, M. M. Taketo, and H. von Boehmer. 2001. Somatic activation of beta-catenin bypasses pre-TCR signaling and TCR selection in thymocyte development. Nat. Immunol. 2:863–869.
   PubMedGoogle Scholar
• Guasparri, I., S. A. Keller, and E. Cesarman. 2004. KSHV vFLIP is essential for the survival of infected lymphoma cells. J. Exp. Med. 199:993–1003.
   PubMed Web of Science ®Google Scholar
• Han, D. K., P. M. Chaudhary, M. E. Wright, C. Friedman, B. J. Trask, R. T. Riedel, D. G. Baskin, S. M. Schwartz, and L. Hood. 1997. MRIT, a novel death-effector domain-containing protein, interacts with caspases and BclXL and initiates cell death. Proc. Natl. Acad. Sci. USA 94:11333–11338.
   PubMed Web of Science ®Google Scholar
• Hecht, A., and M. P. Stemmler. 2003. Identification of a promoter-specific transcriptional activation domain at the C terminus of the Wnt effector protein T-cell factor 4. J. Biol. Chem. 278:3776–3785.
   PubMedGoogle Scholar
• Hu, S., C. Vincenz, M. Buller, and V. M. Dixit. 1997. A novel family of viral death effector domain-containing molecules that inhibit both CD-95- and tumor necrosis factor receptor-1-induced apoptosis. J. Biol. Chem. 272:9621–9624.
   PubMed Web of Science ®Google Scholar
• Irmler, M., M. Thome, M. Hahne, P. Schneider, K. Hofmann, V. Steiner, J. L. Bodmer, M. Schroter, K. Burns, C. Mattmann, D. Rimoldi, L. E. French, and J. Tschopp. 1997. Inhibition of death receptor signals by cellular FLIP. Nature 388:190–195.
   PubMed Web of Science ®Google Scholar
• Itoh, N., S. Yonehara, A. Ishii, M. Yonehara, S. Mizushima, M. Sameshima, A. Hase, Y. Seto, and S. Nagata. 1991. The polypeptide encoded by the cDNA for human cell surface antigen Fas can mediate apoptosis. Cell 66:233–243.
   PubMed Web of Science ®Google Scholar
• Itoh, N., S. Yonehara, J. Schreurs, D. M. Gorman, K. Maruyama, A. Ishii, I. Yahara, K. Arai, and A. Miyajima. 1990. Cloning of an interleukin-3 receptor gene: a member of a distinct receptor gene family. Science 247:324–327.
   PubMed Web of Science ®Google Scholar
• Kataoka, T., R. C. Budd, N. Holler, M. Thome, F. Martinon, M. Irmler, K. Burns, M. Hahne, N. Kennedy, M. Kovacsovics, and J. Tschopp. 2000. The caspase-8 inhibitor FLIP promotes activation of NF-kappaB and Erk signaling pathways. Curr. Biol. 10:640–648.
   PubMed Web of Science ®Google Scholar
• Kazama, H., and S. Yonehara. 2000. Oncogenic K-Ras and basic fibroblast growth factor prevent Fas-mediated apoptosis in fibroblasts through activation of mitogen-activated protein kinase. J. Cell Biol. 148:557–566.
   PubMed Web of Science ®Google Scholar
• Kikuchi, A. 2000. Regulation of beta-catenin signaling in the Wnt pathway. Biochem. Biophys. Res. Commun. 268:243–248.
   PubMed Web of Science ®Google Scholar
• Kolligs, F. T., G. Hu, C. V. Dang, and E. R. Fearon. 1999. Neoplastic transformation of RK3E by mutant β-catenin requires deregulation of Tcf/Lef transcription but not activation of c-myc expression. Mol. Cell. Biol. 19:5696–5706.
   PubMedGoogle Scholar
• Korinek, V., N. Barker, P. J. Morin, D. van Wichen, R. de Weger, K. W. Kinzler, B. Vogelstein, and H. Clevers. 1997. Constitutive transcriptional activation by a beta-catenin-Tcf complex in APC−/− colon carcinoma. Science 275:1784–1787.
   PubMed Web of Science ®Google Scholar
• Lee, K. K., T. Ohyama, N. Yajima, S. Tsubuki, and S. Yonehara. 2001. MST, a physiological caspase substrate, highly sensitizes apoptosis both upstream and downstream of caspase activation. J. Biol. Chem. 276:19276–19285.
   PubMedGoogle Scholar
• Liu, L., M. T. Eby, N. Rathore, S. K. Sinha, A. Kumar, and P. M. Chaudhary. 2002. The human herpes virus 8-encoded viral FLICE inhibitory protein physically associates with and persistently activates the Ikappa B kinase complex. J. Biol. Chem. 277:13745–13751.
   PubMed Web of Science ®Google Scholar
• Logan, C. Y., and R. Nusse. 2004. The Wnt signaling pathway in development and disease. Annu. Rev. Cell Dev. Biol. 20:781–810.
   PubMed Web of Science ®Google Scholar
• Matta, H., and P. M. Chaudhary. 2004. Activation of alternative NF-kappa B pathway by human herpes virus 8-encoded Fas-associated death domain-like IL-1 beta-converting enzyme inhibitory protein (vFLIP). Proc. Natl. Acad. Sci. USA 101:9399–9404.
   PubMed Web of Science ®Google Scholar
• Medema, J. P., C. Scaffidi, F. C. Kischkel, A. Shevchenko, M. Mann, P. H. Krammer, and M. E. Peter. 1997. FLICE is activated by association with the CD95 death-inducing signaling complex (DISC). EMBO J. 16:2794–2804.
   PubMed Web of Science ®Google Scholar
• Molenaar, M., M. van de Wetering, M. Oosterwegel, J. Peterson-Maduro, S. Godsave, V. Korinek, J. Roose, O. Destree, and H. Clevers. 1996. XTcf-3 transcription factor mediates beta-catenin-induced axis formation in Xenopus embryos. Cell 86:391–399.
   PubMed Web of Science ®Google Scholar
• Muzio, M., A. M. Chinnaiyan, F. C. Kischkel, K. O'Rourke, A. Shevchenko, J. Ni, C. Scaffidi, J. D. Bretz, M. Zhang, R. Gentz, M. Mann, P. H. Krammer, M. E. Peter, and V. M. Dixit. 1996. FLICE, a novel FADD-homologous ICE/CED-3-like protease, is recruited to the CD95 (Fas/APO-1) death-inducing signaling complex. Cell 85:817–827.
   PubMed Web of Science ®Google Scholar
• Nagata, S. 1999. Fas ligand-induced apoptosis. Annu. Rev. Genet. 33:29–55.
   PubMed Web of Science ®Google Scholar
• Naito, M., R. Katayama, T. Ishioka, A. Suga, K. Takubo, M. Nanjo, C. Hashimoto, M. Taira, S. Takada, R. Takada, M. Kitagawa, S.-I. Matsuzawa, J. C. Reed, and T. Tsuruo. 2004. Cellular FLIP inhibits β-catenin ubiquitylation and enhances Wnt signaling. Mol. Cell. Biol. 24:8418–8427.
   PubMedGoogle Scholar
• OhYama, T., S. Tsukumo, N. Yajima, K. Sakamaki, and S. Yonehara. 2000. Reduction of thymocyte numbers in transgenic mice expressing viral FLICE-inhibitory protein in a Fas-independent manner. Microbiol. Immunol. 44:289–297.
   PubMed Web of Science ®Google Scholar
• Peifer, M., and P. Polakis. 2000. Wnt signaling in oncogenesis and embryogenesis—a look outside the nucleus. Science 287:1606–1609.
   PubMed Web of Science ®Google Scholar
• Prinos, P., S. Joseph, K. Oh, B. I. Meyer, P. Gruss, and D. Lohnes. 2001. Multiple pathways governing Cdx1 expression during murine development. Dev. Biol. 239:257–269.
   PubMedGoogle Scholar
• Sakamaki, K., T. Inoue, M. Asano, K. Sudo, H. Kazama, J. Sakagami, S. Sakata, M. Ozaki, S. Nakamura, S. Toyokuni, N. Osumi, Y. Iwakura, and S. Yonehara. 2002. Ex vivo whole-embryo culture of caspase-8-deficient embryos normalize their aberrant phenotypes in the developing neural tube and heart. Cell Death Differ. 9:1196–1206.
   PubMedGoogle Scholar
• Sekiya, T., S. Adachi, K. Kohu, T. Yamada, O. Higuchi, Y. Furukawa, Y. Nakamura, T. Nakamura, K. Tashiro, S. Kuhara, S. Ohwada, and T. Akiyama. 2004. Identification of BMP and activin membrane-bound inhibitor (BAMBI), an inhibitor of transforming growth factor-beta signaling, as a target of the beta-catenin pathway in colorectal tumor cells. J. Biol. Chem. 279:6840–6846.
   PubMed Web of Science ®Google Scholar
• Shibamoto, S., K. Higano, R. Takada, F. Ito, M. Takeichi, and S. Takada. 1998. Cytoskeletal reorganization by soluble Wnt-3a protein signalling. Genes Cells 3:659–670.
   PubMed Web of Science ®Google Scholar
• Shtutman, M., J. Zhurinsky, I. Simcha, C. Albanese, M. D'Amico, R. Pestell, and A. Ben-Ze'ev. 1999. The cyclin D1 gene is a target of the beta-catenin/LEF-1 pathway. Proc. Natl. Acad. Sci. USA 96:5522–5527.
   PubMed Web of Science ®Google Scholar
• Shu, H. B., D. R. Halpin, and D. V. Goeddel. 1997. Casper is a FADD- and caspase-related inducer of apoptosis. Immunity 6:751–763.
   PubMed Web of Science ®Google Scholar
• Slusarski, D. C., J. Yang-Snyder, W. B. Busa, and R. T. Moon. 1997. Modulation of embryonic intracellular Ca2+ signaling by Wnt-5A. Dev. Biol. 182:114–120.
   PubMed Web of Science ®Google Scholar
• Staal, F. J., J. Meeldijk, P. Moerer, P. Jay, B. C. van de Weerdt, S. Vainio, G. P. Nolan, and H. Clevers. 2001. Wnt signaling is required for thymocyte development and activates Tcf-1 mediated transcription. Eur. J. Immunol. 31:285–293.
   PubMedGoogle Scholar
• Sun, Q., S. Zachariah, and P. M. Chaudhary. 2003. The human herpes virus 8-encoded viral FLICE-inhibitory protein induces cellular transformation via NF-kappaB activation. J. Biol. Chem. 278:52437–52445.
   PubMed Web of Science ®Google Scholar
• Tago, K., T. Nakamura, M. Nishita, J. Hyodo, S. Nagai, Y. Murata, S. Adachi, S. Ohwada, Y. Morishita, H. Shibuya, and T. Akiyama. 2000. Inhibition of Wnt signaling by ICAT, a novel beta-catenin-interacting protein. Genes Dev. 14:1741–1749.
   PubMedGoogle Scholar
• Tetsu, O., and F. McCormick. 1999. Beta-catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature 398:422–426.
   PubMed Web of Science ®Google Scholar
• Thome, M., P. Schneider, K. Hofmann, H. Fickenscher, E. Meinl, F. Neipel, C. Mattmann, K. Burns, J. L. Bodmer, M. Schroter, C. Scaffidi, P. H. Krammer, M. E. Peter, and J. Tschopp. 1997. Viral FLICE-inhibitory proteins (FLIPs) prevent apoptosis induced by death receptors. Nature 386:517–521.
   PubMed Web of Science ®Google Scholar
• Thome, M., and J. Tschopp. 2001. Regulation of lymphocyte proliferation and death by FLIP. Nat. Rev. Immunol. 1:50–58.
   PubMedGoogle Scholar
• Tsukumo, S. I., and S. Yonehara. 1999. Requirement of cooperative functions of two repeated death effector domains in caspase-8 and in MC159 for induction and inhibition of apoptosis, respectively. Genes Cells 4:541–549.
   PubMedGoogle Scholar
• Ueda, Y., M. Hijikata, S. Takagi, R. Takada, S. Takada, T. Chiba, and K. Shimotohno. 2002. Wnt/beta-catenin signaling suppresses apoptosis in low serum medium and induces morphologic change in rodent fibroblasts. Int. J. Cancer 99:681–688.
   PubMed Web of Science ®Google Scholar
• van de Wetering, M., R. Cavallo, D. Dooijes, M. van Beest, J. van Es, J. Loureiro, A. Ypma, D. Hursh, T. Jones, A. Bejsovec, M. Peifer, M. Mortin, and H. Clevers. 1997. Armadillo coactivates transcription driven by the product of the Drosophila segment polarity gene dTCF. Cell 88:789–799.
   PubMed Web of Science ®Google Scholar
• Wu, Z., M. Roberts, M. Porter, F. Walker, E. J. Wherry, J. Kelly, M. Gadina, E. M. Silva, G. A. DosReis, M. F. Lopes, J. O'Shea, W. J. Leonard, R. Ahmed, and R. M. Siegel. 2004. Viral FLIP impairs survival of activated T cells and generation of CD8+ T cell memory. J. Immunol. 172:6313–6323.
   PubMed Web of Science ®Google Scholar
• Yanagawa, S., F. van Leeuwen, A. Wodarz, J. Klingensmith, and R. Nusse. 1995. The dishevelled protein is modified by wingless signaling in Drosophila. Genes Dev. 9:1087–1097.
   PubMed Web of Science ®Google Scholar
• Yeh, W. C., J. L. Pompa, M. E. McCurrach, H. B. Shu, A. J. Elia, A. Shahinian, M. Ng, A. Wakeham, W. Khoo, K. Mitchell, W. S. El-Deiry, S. W. Lowe, D. V. Goeddel, and T. W. Mak. 1998. FADD: essential for embryo development and signaling from some, but not all, inducers of apoptosis. Science 279:1954–1958.
   PubMed Web of Science ®Google Scholar
• Yonehara, S., A. Ishii, and M. Yonehara. 1989. A cell-killing monoclonal antibody (anti-Fas) to a cell surface antigen co-downregulated with the receptor of tumor necrosis factor. J. Exp. Med. 169:1747–1756.
   PubMed Web of Science ®Google Scholar
• Yonehara, S., A. Ishii, M. Yonehara, S. Koyasu, A. Miyajima, J. Schreurs, K. Arai, and I. Yahara. 1990. Identification of a cell surface 105 kd protein (Aic-2 antigen) which binds interleukin-3. Int. Immunol. 2:143–150.
   PubMed Web of Science ®Google Scholar