Death Receptor-Induced Activation of Initiator Caspase 8 Is Antagonized by Serine/Threonine Kinase PAK4

REFERENCES

• Abo, A., J. Qu, M. S. Cammarano, C. Dan, A. Fritsch, V. Baud, B. Belisle, and A. Minden. 1998. PAK4, a novel effector for Cdc42Hs, is implicated in the reorganization of the actin cytoskeleton and in the formation of filopodia. EMBO J. 17: 6527–6540.
   PubMed Web of Science ®Google Scholar
• Ashkenazi, A., and V. M. Dixit. 1998. Death receptors: signaling and modulation. Science 281: 1305–1308.
   PubMed Web of Science ®Google Scholar
• Bagrodia, S., and R. A. Cerione. 1999. PAK to the future. Trends Cell Biol. 9: 350–355.
   PubMedGoogle Scholar
• Bagrodia, S., S. J. Taylor, C. L. Creasy, J. Chernoff, and R. A. Cerione. 1995. Identification of a mouse p21Cdc42/Rac activated kinase. J. Biol. Chem. 270: 22731–22737.
   PubMedGoogle Scholar
• Beg, A. A., and D. Baltimore. 1996. An essential role for NF-kappaB in preventing TNF-alpha-induced cell death. Science 274: 782–784.
   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
• Boldin, M. P., E. E. Varfolomeev, Z. Pancer, I. L. Mett, J. H. Camonis, and D. Wallach. 1995. A novel protein that interacts with the death domain of Fas/APO1 contains a sequence motif related to the death domain. J. Biol. Chem. 270: 7795–7798.
   PubMed Web of Science ®Google Scholar
• Brown, J. L., L. Stowers, M. Baer, J. Trejo, S. Coughlin, and J. Chant. 1996. Human Ste20 homologue hPAK1 links GTPases to the JNK MAP kinase pathway. Curr. Biol. 6: 598–605.
   PubMed Web of Science ®Google Scholar
• Budihardjo, I., H. Oliver, M. Lutter, X. Luo, and X. Wang. 1999. Biochemical pathways of caspase activation during apoptosis. Annu. Rev. Cell Dev. Biol. 15: 269–290.
   PubMed Web of Science ®Google Scholar
• Burbelo, P. D., D. Drechsel, and A. Hall. 1995. A conserved binding motif defines numerous candidate target proteins for both Cdc42 and Rac GTPases. J. Biol. Chem. 270: 29071–29074.
   PubMed Web of Science ®Google Scholar
• Callow, M. G., F. Clairvoyant, S. Zhu, B. Schryver, D. B. Whyte, J. R. Bischoff, B. Jallal, and T. Smeal. 2002. Requirement for PAK4 in the anchorage-independent growth of human cancer cell lines. J. Biol. Chem. 277: 550–558.
   PubMed Web of Science ®Google Scholar
• Cantley, L. C. 2002. The phosphoinositide 3-kinase pathway. Science 296: 1655–1657.
   PubMed Web of Science ®Google Scholar
• Chang, D. W., Z. Xing, Y. Pan, A. Algeciras-Schimnich, B. C. Barnhart, S. Yaish-Ohad, M. E. Peter, and X. Yang. 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
• 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
• Dan, C., N. Nath, M. Liberto, and A. Minden. 2002. PAK5, a new brain-specific kinase, promotes neurite outgrowth in N1E-115 cells. Mol. Cell. Biol. 22: 567–577.
   PubMed Web of Science ®Google Scholar
• Daniels, R. H., and G. M. Bokoch. 1999. p21-activated protein kinase: a crucial component of morphological signaling? Trends Biochem. Sci. 24: 350–355.
   PubMed Web of Science ®Google Scholar
• Daniels, R. H., P. S. Hall, and G. M. Bokoch. 1998. Membrane targeting of p21-activated kinase 1 (PAK1) induces neurite outgrowth from PC12 cells. EMBO J. 17: 754–764.
   PubMed Web of Science ®Google Scholar
• Datta, S. R., A. Brunet, and M. E. Greenberg. 1999. Cellular survival: a play in three Akts. Genes Dev. 13: 2905–2927.
   PubMed Web of Science ®Google Scholar
• Datta, S. R., H. Dudek, X. Tao, S. Masters, H. Fu, Y. Gotoh, and M. E. Greenberg. 1997. Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 91: 231–241.
   PubMed Web of Science ®Google Scholar
• Downward, J. 1999. How BAD phosphorylation is good for survival. Nat. Cell Biol. 1: E33–E35.
   PubMed Web of Science ®Google Scholar
• Downward, J. 1998. Ras signalling and apoptosis. Curr. Opin. Genet. Dev. 8: 49–54.
   PubMed Web of Science ®Google Scholar
• Foo, S. Y., and G. P. Nolan. 1999. NF-kappaB to the rescue: RELs, apoptosis and cellular transformation. Trends Genet. 15: 229–235.
   PubMed Web of Science ®Google Scholar
• Gnesutta, N., J. Qu, and A. G. Minden. 2001. The serine/threonine kinase PAK4 prevents caspase activation and protects cells from apoptosis. J. Biol. Chem. 276: 14414–14419.
   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
• Gomez-Angelats, M., and J. A. Cidlowski. 2001. Protein kinase C regulates FADD recruitment and death-inducing signaling complex formation in Fas/CD95-induced apoptosis. J. Biol. Chem. 276: 44944–44952.
   PubMedGoogle Scholar
• Green, D., and G. Kroemer. 1998. The central executioners of apoptosis: caspases or mitochondria? Trends Cell Biol. 8: 267–271.
   PubMed Web of Science ®Google Scholar
• Green, D. R. 1998. Apoptotic pathways: the roads to ruin. Cell 94: 695–698.
   PubMed Web of Science ®Google Scholar
• Green, D. R., and G. I. Evan. 2002. A matter of life and death. Cancer Cell 1: 19–30.
   PubMed Web of Science ®Google Scholar
• Gross, A., X. M. Yin, K. Wang, M. C. Wei, J. Jockel, C. Milliman, H. Erdjument-Bromage, P. Tempst, and S. J. Korsmeyer. 1999. Caspase cleaved BID targets mitochondria and is required for cytochrome c release, while BCL-XL prevents this release but not tumor necrosis factor-R1/Fas death. J. Biol. Chem. 274: 1156–1163.
   PubMed Web of Science ®Google Scholar
• Holmstrom, T. H., I. Schmitz, T. S. Soderstrom, M. Poukkula, V. L. Johnson, S. C. Chow, P. H. Krammer, and J. E. Eriksson. 2000. MAPK/ERK signaling in activated T cells inhibits CD95/Fas-mediated apoptosis downstream of DISC assembly. EMBO J. 19: 5418–5428.
   PubMed Web of Science ®Google Scholar
• Hsu, H., J. Huang, H. B. Shu, V. Baichwal, and D. V. Goeddel. 1996. TNF-dependent recruitment of the protein kinase RIP to the TNF receptor-1 signaling complex. Immunity 4: 387–396.
   PubMed Web of Science ®Google Scholar
• Hsu, H., H. B. Shu, M. G. Pan, and D. V. Goeddel. 1996. TRADD-TRAF2 and TRADD-FADD interactions define two distinct TNF receptor 1 signal transduction pathways. Cell 84: 299–308.
   PubMed Web of Science ®Google Scholar
• Hsu, H., J. Xiong, and D. V. Goeddel. 1995. The TNF receptor 1-associated protein TRADD signals cell death and NF-kappa B activation. Cell 81: 495–504.
   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
• Jaffer, Z. M., and J. Chernoff. 2002. p21-activated kinases: three more join the Pak. Int. J. Biochem. Cell Biol. 34: 713–717.
   PubMed Web of Science ®Google Scholar
• Jakobi, R., E. Moertl, and M. A. Koeppel. 2001. p21-activated protein kinase gamma-PAK suppresses programmed cell death of BALB3T3 fibroblasts. J. Biol. Chem. 276: 16624–16634.
   PubMed Web of Science ®Google Scholar
• Jones, R. G., A. R. Elford, M. J. Parsons, L. Wu, C. M. Krawczyk, W. C. Yeh, R. Hakem, R. Rottapel, J. R. Woodgett, and P. S. Ohashi. 2002. CD28-dependent activation of protein kinase B/Akt blocks Fas-mediated apoptosis by preventing death-inducing signaling complex assembly. J. Exp. Med. 196: 335–348.
   PubMed Web of Science ®Google Scholar
• Jones, S. J., E. C. Ledgerwood, J. B. Prins, J. Galbraith, D. R. Johnson, J. S. Pober, and J. R. Bradley. 1999. TNF recruits TRADD to the plasma membrane but not the trans-Golgi network, the principal subcellular location of TNF-R1. J. Immunol. 162: 1042–1048.
   PubMedGoogle Scholar
• Juo, P., C. J. Kuo, J. Yuan, and J. Blenis. 1998. Essential requirement for caspase-8/FLICE in the initiation of the Fas-induced apoptotic cascade. Curr. Biol. 8: 1001–1008.
   PubMed Web of Science ®Google Scholar
• Kirchhoff, S., W. W. Muller, A. Krueger, I. Schmitz, and P. H. Krammer. 2000. TCR-mediated up-regulation of c-FLIPshort correlates with resistance toward CD95-mediated apoptosis by blocking death-inducing signaling complex activity. J. Immunol. 165: 6293–6300.
   PubMedGoogle Scholar
• Kischkel, F. C., S. Hellbardt, I. Behrmann, M. Germer, M. Pawlita, P. H. Krammer, and M. E. Peter. 1995. Cytotoxicity-dependent APO-1 (Fas/CD95)-associated proteins form a death-inducing signaling complex (DISC) with the receptor. EMBO J. 14: 5579–5588.
   PubMed Web of Science ®Google Scholar
• Lee, N., H. MacDonald, C. Reinhard, R. Halenbeck, A. Roulston, T. Shi, and L. T. Williams. 1997. Activation of hPAK65 by caspase cleavage induces some of the morphological and biochemical changes of apoptosis. Proc. Natl. Acad. Sci. USA 94: 13642–13647.
   PubMed Web of Science ®Google Scholar
• Li, H., H. Zhu, C.-J. Xy, and J. Yuan. 1998. Cleavage of BID by caspase 8 mediates the mitochondrial damage in the fas pathway of apoptosis. Cell 94: 491–501.
   PubMed Web of Science ®Google Scholar
• Liu, Z. G., H. Hsu, D. V. Goeddel, and M. Karin. 1996. Dissection of TNF receptor 1 effector functions: JNK activation is not linked to apoptosis while NF-kappaB activation prevents cell death. Cell 87: 565–576.
   PubMed Web of Science ®Google Scholar
• Luo, L., I. Budihardjo, H. Zou, C. Slaughter, and X. Wang. 1998. Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell 94: 481–490.
   PubMed Web of Science ®Google Scholar
• Madrid, L. V., C. Y. Wang, D. C. Guttridge, A. J. Schottelius, A. S. Baldwin, Jr., and M. W. Mayo. 2000. Akt suppresses apoptosis by stimulating the transactivation potential of the RelA/p65 subunit of NF-kappaB. Mol. Cell. Biol. 20: 1626–1638.
   PubMed Web of Science ®Google Scholar
• Manser, E., T. Leung, H. Salihuddin, Z. S. Zhao, and L. Lim. 1994. A brain serine/threonine protein kinase activated by Cdc42 and Rac1. Nature 367: 40–46.
   PubMed Web of Science ®Google Scholar
• Martin, G. A., G. Bollag, F. McCormick, and A. Abo. 1995. A novel serine kinase activated by rac1/CDC42Hs-dependent autophosphorylation is related to PAK65 and STE20. EMBO J. 14: 1970–1978.
   PubMedGoogle 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
• 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
• Muzio, M., B. R. Stockwell, H. R. Stennicke, G. S. Salvesen, and V. M. Dixit. 1998. An induced proximity model for caspase-8 activation. J. Biol. Chem. 273: 2926–2930.
   PubMed Web of Science ®Google Scholar
• Nagata, S. 1997. Apoptosis by death factor. Cell 88: 355–365.
   PubMed Web of Science ®Google Scholar
• Pandey, A., I. Dan, T. Z. Kristiansen, N. M. Watanabe, J. Voldby, E. Kajikawa, R. Khosravi-Far, B. Blagoev, and M. Mann. 2002. Cloning and characterization of PAK5, a novel member of mammalianp21-activated kinase-II subfamily that is predominantly expressed in brain. Oncogene 21: 3939–3948.
   PubMed Web of Science ®Google Scholar
• Perez, D., and E. White. 2000. TNF-alpha signals apoptosis through a bid-dependent conformational change in Bax that is inhibited by E1B 19K. Mol. Cell 6: 53–63.
   PubMed Web of Science ®Google Scholar
• Qu, J., M. S. Cammarano, Q. Shi, K. C. Ha, P. de Lanerolle, and A. Minden. 2001. Activated PAK4 regulates cell adhesion and anchorage-independent growth. Mol. Cell. Biol. 21: 3523–3533.
   PubMedGoogle Scholar
• Raff, M. C. 1992. Social controls on cell survival and cell death. Nature 356: 397–400.
   PubMed Web of Science ®Google Scholar
• Romashkova, J. A., and S. S. Makarov. 1999. NF-kappaB is a target of AKT in anti-apoptotic PDGF signalling. Nature 401: 86–90.
   PubMed Web of Science ®Google Scholar
• Rudel, T., and G. M. Bokoch. 1997. Membrane and morphological changes in apoptotic cells regulated by caspase-mediated activation of PAK2. Science 276: 1571–1574.
   PubMed Web of Science ®Google Scholar
• Salvesen, G. S., and V. M. Dixit. 1997. Caspases: intracellular signaling by proteolysis. Cell 91: 443–446.
   PubMed Web of Science ®Google Scholar
• Scaffidi, C., S. Fulda, A. Srinivasan, C. Friesen, F. Li, K. J. Tomaselli, K. M. Debatin, P. H. Krammer, and M. E. Peter. 1998. Two CD95 (APO-1/Fas) signaling pathways. EMBO J. 17: 1675–1687.
   PubMed Web of Science ®Google Scholar
• Scaffidi, C., I. Schmitz, P. H. Krammer, and M. E. Peter. 1999. The role of c-FLIP in modulation of CD95-induced apoptosis. J. Biol. Chem. 274: 1541–1548.
   PubMed Web of Science ®Google Scholar
• Schurmann, A., A. F. Mooney, L. C. Sanders, M. A. Sells, H. G. Wang, J. C. Reed, and G. M. Bokoch. 2000. p21-activated kinase 1 phosphorylates the death agonist bad and protects cells from apoptosis. Mol. Cell. Biol. 20: 453–461.
   PubMed Web of Science ®Google Scholar
• Sells, M. A., and J. Chernoff. 1997. Emerging from the Pak: the p21-activated protein kinase family. Trends Cell Biol. 7: 162–167.
   PubMed Web of Science ®Google Scholar
• Sells, M. A., U. G. Knaus, S. Bagrodia, D. M. Ambrose, G. M. Bokoch, and J. Chernoff. 1997. Human p21-activated kinase (Pak1) regulates actin organization in mammalian cells. Curr. Biol. 7: 202–210.
   PubMed Web of Science ®Google Scholar
• Shu, H. B., M. Takeuchi, and D. V. Goeddel. 1996. The tumor necrosis factor receptor 2 signal transducers TRAF2 and c-IAP1 are components of the tumor necrosis factor receptor 1 signaling complex. Proc. Natl. Acad. Sci. USA 93: 13973–13978.
   PubMed Web of Science ®Google Scholar
• Stanger, B. Z., P. Leder, T. H. Lee, E. Kim, and B. Seed. 1995. RIP: a novel protein containing a death domain that interacts with Fas/APO-1 (CD95) in yeast and causes cell death. Cell 81: 513–523.
   PubMed Web of Science ®Google Scholar
• Tang, Y., H. Zhou, A. Chen, R. N. Pittman, and J. Field. 2000. The Akt proto-oncogene links Ras to Pak and cell survival signals. J. Biol. Chem. 275: 9106–9109.
   PubMed Web of Science ®Google Scholar
• Thornberry, N. A., and Y. Lazebnik. 1998. Caspases: enemies within. Science 281: 1312–1316.
   PubMed Web of Science ®Google Scholar
• Varadhachary, A. S., M. Edidin, A. M. Hanlon, M. E. Peter, P. H. Krammer, and P. Salgame. 2001. Phosphatidylinositol 3′-kinase blocks CD95 aggregation and caspase-8 cleavage at the death-inducing signaling complex by modulating lateral diffusion of CD95. J. Immunol. 166: 6564–6569.
   PubMed Web of Science ®Google Scholar
• Varadhachary, A. S., M. E. Peter, S. N. Perdow, P. H. Krammer, and P. Salgame. 1999. Selective up-regulation of phosphatidylinositol 3′-kinase activity in Th2 cells inhibits caspase-8 cleavage at the death-inducing complex: a mechanism for Th2 resistance from Fas-mediated apoptosis. J. Immunol. 163: 4772–4779.
   PubMed Web of Science ®Google Scholar
• Varfolomeev, E. E., M. Schuchmann, V. Luria, N. Chiannilkulchai, J. S. Beckmann, I. L. Mett, D. Rebrikov, V. M. Brodianski, O. C. Kemper, O. Kollet, T. Lapidot, D. Soffer, T. Sobe, K. B. Avraham, T. Goncharov, H. Holtmann, P. Lonai, and D. Wallach. 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
• Wallach, D., E. E. Varfolomeev, N. L. Malinin, Y. V. Goltsev, A. V. Kovalenko, and M. P. Boldin. 1999. Tumor necrosis factor receptor and Fas signaling mechanisms. Annu. Rev. Immunol. 17: 331–367.
   PubMed Web of Science ®Google Scholar
• Walter, B. N., Z. Huang, R. Jakobi, P. T. Tuazon, E. S. Alnemri, G. Litwack, and J. A. Traugh. 1998. Cleavage and activation of p21-activated protein kinase gamma-PAK by CPP32 (caspase 3). Effects of autophosphorylation on activity. J. Biol. Chem. 273: 28733–28739.
   PubMed Web of Science ®Google Scholar
• Wolf, D., V. Witte, B. Laffert, K. Blume, E. Stromer, S. Trapp, P. d'Aloja, A. Schurmann, and A. S. Baur. 2001. HIV-1 Nef associated PAK and PI3-kinases stimulate Akt-independent Bad-phosphorylation to induce anti-apoptotic signals. Nat. Med. 7: 1217–1224.
   PubMed Web of Science ®Google Scholar
• Yang, F., X. Li, M. Sharma, M. Zarnegar, B. Lim, and Z. Sun. 2001. Androgen receptor specifically interacts with a novel p21-activated kinase, PAK6. J. Biol. Chem. 276: 15345–15353.
   PubMed Web of Science ®Google Scholar
• Yin, X. M., K. Wang, A. Gross, Y. Zhao, S. Zinkel, B. Klocke, K. A. Roth, and S. J. Korsmeyer. 1999. Bid-deficient mice are resistant to Fas-induced hepatocellular apoptosis. Nature 400: 886–891.
   PubMed Web of Science ®Google Scholar
• Zhang, S. Q., A. Kovalenko, G. Cantarella, and D. Wallach. 2000. Recruitment of the IKK signalosome to the p55 TNF receptor: RIP and A20 bind to NEMO (IKKgamma) upon receptor stimulation. Immunity 12: 301–311.
   PubMedGoogle Scholar