The HECT-Type E3 Ubiquitin Ligase AIP2 Inhibits Activation-Induced T-Cell Death by Catalyzing EGR2 Ubiquitination

REFERENCES

• Anandasabapathy, N., G. S. Ford, D. Bloom, C. Holness, V. Paragas, C. Seroogy, H. Skrenta, M. Hollenhorst, C. G. Fathman, and L. Soares. 2003. GRAIL: an E3 ubiquitin ligase that inhibits cytokine gene transcription is expressed in anergic CD4+ T cells. Immunity 18:535–547.
   PubMed Web of Science ®Google Scholar
• Bachmaier, K., C. Krawczyk, I. Kozieradzki, Y. Y. Kong, T. Sasaki, A. Oliveira-dos-Santos, S. Mariathasan, D. Bouchard, A. Wakeham, A. Itie, J. Le, P. S. Ohashi, I. Sarosi, H. Nishina, S. Lipkowitz, and J. M. Penninger. 2000. Negative regulation of lymphocyte activation and autoimmunity by the molecular adaptor Cbl-b. Nature 403:211–216.
   PubMed Web of Science ®Google Scholar
• Carattino, M. D., R. S. Edinger, H. J. Grieser, R. Wise, D. Neumann, U. Schlattner, J. P. Johnson, T. R. Kleyman, and K. R. Hallows. 2005. Epithelial sodium channel inhibition by AMP-activated protein kinase in oocytes and polarized renal epithelial cells. J. Biol. Chem. 280:17608–17616.
   PubMedGoogle Scholar
• Chavrier, P., M. Zerial, P. Lemaire, J. Almendral, R. Bravo, and P. Charnay. 1988. A gene encoding a protein with zinc fingers is activated during G0/G1 transition in cultured cells. EMBO J. 7:29–35.
   PubMed Web of Science ®Google Scholar
• Chiang, Y. J., H. K. Kole, K. Brown, M. Naramura, S. Fukuhara, R. J. Hu, I. K. Jang, J. S. Gutkind, E. Shevach, and H. Gu. 2000. Cbl-b regulates the CD28 dependence of T-cell activation. Nature 403:216–220.
   PubMed Web of Science ®Google Scholar
• Crosby, S. D., R. A. Veile, H. Donis-Keller, J. M. Baraban, R. V. Bhat, K. S. Simburger, and J. Milbrandt. 1992. Neural-specific expression, genomic structure, and chromosomal localization of the gene encoding the zinc-finger transcription factor NGFI-C. Proc. Natl. Acad. Sci. USA 89:4739–4743.
   PubMedGoogle Scholar
• Delgado, M., and D. Ganea. 2001. Vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide inhibit expression of Fas ligand in activated T lymphocytes by regulating c-Myc, NF-kappa B, NF-AT, and early growth factors 2/3. J. Immunol. 166:1028–1040.
   PubMedGoogle Scholar
• Droin, N. M., M. J. Pinkoski, E. Dejardin, and D. R. Green. 2003. Egr family members regulate nonlymphoid expression of Fas ligand, TRAIL, and tumor necrosis factor during immune responses. Mol. Cell. Biol. 23:7638–7647.
   PubMed Web of Science ®Google Scholar
• Dzialo-Hatton, R., J. Milbrandt, R. D. Hockett, Jr., and C. T. Weaver. 2001. Differential expression of Fas ligand in Th1 and Th2 cells is regulated by early growth response gene and NF-AT family members. J. Immunol. 166:4534–4542.
   PubMed Web of Science ®Google Scholar
• Fang, D., C. Elly, B. Gao, N. Fang, Y. Altman, C. Joazeiro, T. Hunter, N. Copeland, N. Jenkins, and Y. C. Liu. 2002. Dysregulation of T lymphocyte function in itchy mice: a role for Itch in TH2 differentiation. Nat. Immunol. 3:281–287.
   PubMed Web of Science ®Google Scholar
• Fang, D., and T. K. Kerppola. 2004. Ubiquitin-mediated fluorescence complementation reveals that Jun ubiquitinated by Itch/AIP4 is localized to lysosomes. Proc. Natl. Acad. Sci. USA 101:14782–14787.
   PubMedGoogle Scholar
• Fang, D., H. Y. Wang, N. Fang, Y. Altman, C. Elly, and Y. C. Liu. 2001. Cbl-b, a RING-type E3 ubiquitin ligase, targets phosphatidylinositol 3-kinase for ubiquitination in T cells. J. Biol. Chem. 276:4872–4878.
   PubMed Web of Science ®Google Scholar
• Gao, B., S. M. Lee, and D. Fang. 2006. The tyrosine kinase c-Abl protects c-Jun from ubiquitination-mediated degradation in T cells. J. Biol. Chem. 281:29711–29718.
   PubMedGoogle Scholar
• Gao, M., T. Labuda, Y. Xia, E. Gallagher, D. Fang, Y. C. Liu, and M. Karin. 2004. Jun turnover is controlled through JNK-dependent phosphorylation of the E3 ligase Itch. Science 306:271–275.
   PubMed Web of Science ®Google Scholar
• Gillian, A. L., and J. Svaren. 2004. The Ddx20/DP103 dead box protein represses transcriptional activation by Egr2/Krox-20. J. Biol. Chem. 279:9056–9063.
   PubMedGoogle Scholar
• Green, D. R., N. Droin, and M. Pinkoski. 2003. Activation-induced cell death in T cells. Immunol. Rev. 193:70–81.
   PubMed Web of Science ®Google Scholar
• Harris, J. E., K. D. Bishop, N. E. Phillips, J. P. Mordes, D. L. Greiner, A. A. Rossini, and M. P. Czech. 2004. Early growth response gene-2, a zinc-finger transcription factor, is required for full induction of clonal anergy in CD4+ T cells. J. Immunol. 173:7331–7338.
   PubMedGoogle Scholar
• Heissmeyer, V., F. Macian, S. H. Im, R. Varma, S. Feske, K. Venuprasad, H. Gu, Y. C. Liu, M. L. Dustin, and A. Rao. 2004. Calcineurin imposes T cell unresponsiveness through targeted proteolysis of signaling proteins. Nat. Immunol. 5:255–265.
   PubMed Web of Science ®Google Scholar
• Huibregtse, J. M., M. Scheffner, S. Beaudenon, and P. M. Howley. 1995. A family of proteins structurally and functionally related to the E6-AP ubiquitin-protein ligase. Proc. Natl. Acad. Sci. USA 92:2563–2567.
   PubMed Web of Science ®Google Scholar
• Jackson, P. K., A. G. Eldridge, E. Freed, L. Furstenthal, J. Y. Hsu, B. K. Kaiser, and J. D. Reimann. 2000. The lore of the RINGs: substrate recognition and catalysis by ubiquitin ligases. Trends Cell Biol. 10:429–439.
   PubMed Web of Science ®Google Scholar
• Joseph, L. J., M. M. Le Beau, G. A. Jamieson, Jr., S. Acharya, T. B. Shows, J. D. Rowley, and V. P. Sukhatme. 1988. Molecular cloning, sequencing, and mapping of EGR2, a human early growth response gene encoding a protein with “zinc-binding finger” structure. Proc. Natl. Acad. Sci. USA 85:7164–7168.
   PubMed Web of Science ®Google Scholar
• Kavurma, M. M., and L. M. Khachigian. 2003. Signaling and transcriptional control of Fas ligand gene expression. Cell Death Differ. 10:36–44.
   PubMed Web of Science ®Google Scholar
• Lemaire, P., O. Revelant, R. Bravo, and P. Charnay. 1988. Two mouse genes encoding potential transcription factors with identical DNA-binding domains are activated by growth factors in cultured cells. Proc. Natl. Acad. Sci. USA 85:4691–4695.
   PubMed Web of Science ®Google Scholar
• Liu, Y. C., J. Penninger, and M. Karin. 2005. Immunity by ubiquitylation: a reversible process of modification. Nat. Rev. Immunol. 5:941–952.
   PubMed Web of Science ®Google Scholar
• Lynch, D. H., M. L. Watson, M. R. Alderson, P. R. Baum, R. E. Miller, T. Tough, M. Gibson, T. Davis-Smith, C. A. Smith, K. Hunter, et al. 1994. The mouse Fas-ligand gene is mutated in gld mice and is part of a TNF family gene cluster. Immunity 1:131–136.
   PubMed Web of Science ®Google Scholar
• Macias, M. J., M. Hyvonen, E. Baraldi, J. Schultz, M. Sudol, M. Saraste, and H. Oschkinat. 1996. Structure of the WW domain of a kinase-associated protein complexed with a proline-rich peptide. Nature 382:646–649.
   PubMed Web of Science ®Google Scholar
• Macias, M. J., S. Wiesner, and M. Sudol. 2002. WW and SH3 domains, two different scaffolds to recognize proline-rich ligands. FEBS Lett. 513:30–37.
   PubMed Web of Science ®Google Scholar
• Martin-Serrano, J., S. W. Eastman, W. Chung, and P. D. Bieniasz. 2005. HECT ubiquitin ligases link viral and cellular PPXY motifs to the vacuolar protein-sorting pathway. J. Cell Biol. 168:89–101.
   PubMed Web of Science ®Google Scholar
• McDonald, F. J., A. H. Western, J. D. McNeil, B. C. Thomas, D. R. Olson, and P. M. Snyder. 2002. Ubiquitin-protein ligase WWP2 binds to and downregulates the epithelial Na(+) channel. Am. J. Physiol. Renal Physiol. 283:F431–F436.
   PubMedGoogle Scholar
• Mittelstadt, P. R., and J. D. Ashwell. 1999. Role of Egr-2 in up-regulation of Fas ligand in normal T cells and aberrant double-negative lpr and gld T cells. J. Biol. Chem. 274:3222–3227.
   PubMedGoogle Scholar
• Morita, S., T. Kojima, and T. Kitamura. 2000. Plat-E: an efficient and stable system for transient packaging of retroviruses. Gene Ther. 7:1063–1066.
   PubMed Web of Science ®Google Scholar
• Mueller, D. L. 2004. E3 ubiquitin ligases as T cell anergy factors. Nat. Immunol. 5:883–890.
   PubMedGoogle Scholar
• Naramura, M., H. K. Kole, R. J. Hu, and H. Gu. 1998. Altered thymic positive selection and intracellular signals in Cbl-deficient mice. Proc. Natl. Acad. Sci. USA 95:15547–15552.
   PubMed Web of Science ®Google Scholar
• O'Donovan, K. J., W. G. Tourtellotte, J. Millbrandt, and J. M. Baraban. 1999. The EGR family of transcription-regulatory factors: progress at the interface of molecular and systems neuroscience. Trends Neurosci. 22:167–173.
   PubMed Web of Science ®Google Scholar
• Rengarajan, J., P. R. Mittelstadt, H. W. Mages, A. J. Gerth, R. A. Kroczek, J. D. Ashwell, and L. H. Glimcher. 2000. Sequential involvement of NFAT and Egr transcription factors in FasL regulation. Immunity 12:293–300.
   PubMed Web of Science ®Google Scholar
• Rougier, J. S., M. X. van Bemmelen, M. C. Bruce, T. Jespersen, B. Gavillet, F. Apotheloz, S. Cordonier, O. Staub, D. Rotin, and H. Abriel. 2005. Molecular determinants of voltage-gated sodium channel regulation by the Nedd4/Nedd4-like proteins. Am. J. Physiol. Cell Physiol. 288:C692–C701.
   PubMed Web of Science ®Google Scholar
• Safford, M., S. Collins, M. A. Lutz, A. Allen, C. T. Huang, J. Kowalski, A. Blackford, M. R. Horton, C. Drake, R. H. Schwartz, and J. D. Powell. 2005. Egr-2 and Egr-3 are negative regulators of T cell activation. Nat. Immunol. 6:472–480.
   PubMed Web of Science ®Google Scholar
• Sudol, M. 1996. The WW module competes with the SH3 domain? Trends Biochem. Sci. 21:161–163.
   PubMedGoogle Scholar
• Takahashi, T., M. Tanaka, C. I. Brannan, N. A. Jenkins, N. G. Copeland, T. Suda, and S. Nagata. 1994. Generalized lymphoproliferative disease in mice, caused by a point mutation in the Fas ligand. Cell 76:969–976.
   PubMed Web of Science ®Google Scholar
• Watanabe-Fukunaga, R., C. I. Brannan, N. G. Copeland, N. A. Jenkins, and S. Nagata. 1992. Lymphoproliferation disorder in mice explained by defects in Fas antigen that mediates apoptosis. Nature 356:314–317.
   PubMed Web of Science ®Google Scholar
• Wood, J. D., J. Yuan, R. L. Margolis, V. Colomer, K. Duan, J. Kushi, Z. Kaminsky, J. J. Kleiderlein, A. H. Sharp, and C. A. Ross. 1998. Atrophin-1, the DRPLA gene product, interacts with two families of WW domain-containing proteins. Mol. Cell. Neurosci. 11:149–160.
   PubMedGoogle Scholar
• Wu, J., L. Joseph, V. P. Sukhatme, and K. K. Kidd. 1988. A HindIII polymorphism identified by the human early growth response gene 2 (EGR2) on chromosome 10. Nucleic Acids Res. 16:11855.
   PubMedGoogle Scholar
• Xu, H. M., B. Liao, Q. J. Zhang, B. B. Wang, H. Li, X. M. Zhong, H. Z. Sheng, Y. X. Zhao, Y. M. Zhao, and Y. Jin. 2004. Wwp2, an E3 ubiquitin ligase that targets transcription factor Oct-4 for ubiquitination. J. Biol. Chem. 279:23495–23503.
   PubMedGoogle Scholar
• Yang, Y., B. Dong, P. R. Mittelstadt, H. Xiao, and J. D. Ashwell. 2002. HIV Tat binds Egr proteins and enhances Egr-dependent transactivation of the Fas ligand promoter. J. Biol. Chem. 277:19482–19487.
   PubMed Web of Science ®Google Scholar
• Yoo, Y. G., and M. O. Lee. 2004. Hepatitis B virus X protein induces expression of Fas ligand gene through enhancing transcriptional activity of early growth response factor. J. Biol. Chem. 279:36242–36249.
   PubMed Web of Science ®Google Scholar