CARMA1 is required for Akt-mediated NF-κB activation in T cells

Molecular and Cellular Biology

Volumn 26, Issue 6, 2006, Pages 2327-2336

  Narayan, Preeti ^a   Holt, Brittany ^a   Tosti, Richard ^a   Kane, Lawrence P ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEIN; CD28 ANTIGEN; CELL PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MUCOSA ASSOCIATED LYMPHOID TISSUE LYMPHOMA TRANSLOCATION PROTEIN 1; PROTEIN BCL 10; PROTEIN CARMA1; PROTEIN KINASE B; PROTEIN KINASE C; PROTEIN KINASE INHIBITOR; PROTEIN SERINE THREONINE KINASE; RECEPTOR; T LYMPHOCYTE RECEPTOR; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVATION; EVOLUTION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN INDUCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANTIGENS, CD28; APOPTOSIS REGULATORY PROTEINS; BENZYLAMINES; CARD SIGNALING ADAPTOR PROTEINS; CELLS, CULTURED; ENZYME INHIBITORS; GUANYLATE CYCLASE; HUMANS; I-KAPPA B KINASE; I-KAPPA B PROTEINS; JURKAT CELLS; NF-KAPPA B; NFATC TRANSCRIPTION FACTORS; ONCOGENE PROTEIN V-AKT; PHOSPHORYLATION; PTEN PHOSPHOHYDROLASE; QUINOXALINES; RECEPTORS, ANTIGEN, T-CELL; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; TETRADECANOYLPHORBOL ACETATE;

EID: 33644772836     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.26.6.2327-2336.2006     Document Type: Article

References (50)

1. Alessi, D. R., F. B. Caudwell, M. Andjelkovic, B. A. Hemmings, and P. Cohen. 1996. Molecular basis for the substrate specificity of protein kinase B: comparison with MAPKAP kinase-1 and p70 S6 kinase. FEBS Lett. 399: 333-338.
2. Barnett, S. F., M. T. Bilodeau, and C. W. Lindsley. 2005. The Akt/PKB family of protein kinases: a review of small molecule inhibitors and progress towards target validation. Curr. Top. Med. Chem. 5:109-125.
3. Barnett, S. F., D. Defeo-Jones, S. Fu, P. J. Hancock, K. M. Haskell, R. E. Jones, J. A. Kahana, A. M. Kral, K. Leander, L. L. Lee, J. Malinowski, E. M. McAvoy, D. D. Nahas, R. G. Robinson, and H. E. Huber. 2005. Identification and characterization of pleckstrin-homology-domain-dependent and isoenzyme-specific Akt inhibitors. Biochem. J. 385:399-408.
4. Bauer, B., N. Krumbock, F. Fresser, F. Hochholdinger, M. Spitaler, A. Simm, F. Uberall, B. Schraven, and G. Baier. 2001. Complex formation and cooperation of protein kinase Cθ and Akt1/protein kinase Bα in the NF-κB transactivation cascade in Jurkat T cells. J. Biol. Chem. 276:31627-31634.
5. H2 differentiation and PKC-θ-mediated activation of NF-κB1. Immunity 21:693-706.
6. Chen, L. F., and W. C. Greene. 2004. Shaping the nuclear action of NF-κB. Nat. Rev. Mol. Cell. Biol. 5:392-401.
7. DeFeo-Jones, D., S. F. Barnett, S. Fu, P. J. Hancock, K. M. Haskell, K. R. Leander, E. McAvoy, R. G. Robinson, M. E. Duggan, C. W. Lindsley, Z. Zhao, H. E. Huber, and R. E. Jones. 2005. Tumor cell sensitization to apoptotic stimuli by selective inhibition of specific Akt/PKB family members. Mol. Cancer Ther. 4:271-279.
8. Egawa, T., B. Albrecht, B. Favier, M. J. Sunshine, K. Mirchandani, W. O'Brien, M. Thome, and D. R. Littman. 2003. Requirement for CARMA1 in antigen receptor-induced NF-κB activation and lymphocyte proliferation. Curr. Biol. 13:1252-1258.
9. Gustin, J. A., O. N. Ozes, H. Akca, R. Pincheira, L. D. Mayo, Q. Li, J. R. Guzman, C. K. Korgaonkar, and D. B. Donner. 2004. Cell type-specific expression of the IκB kinases determines the significance of phosphatidylinositol 3-kinase/Akt signaling to NF-κB activation. J. Biol. Chem. 279:1615-1620.
10. Hanada, M., J. Feng, and B. A. Hemmings. 2004. Structure, regulation and function of PKB/AKT-a major therapeutic target. Biochim. Biophys. Acta 1697:3-16.
11. Hara, H., C. Bakal, T. Wada, D. Bouchard, R. Rottapel, T. Saito, and J. M. Penninger. 2004. The molecular adapter Carma1 controls entry of IκB kinase into the central immune synapse. J. Exp. Med. 200:1167-1177.
12. Hara, H., T. Wada, C. Bakal, I. Kozieradzki, S. Suzuki, N. Suzuki, M. Nghiem, E. K. Griffiths, C. Krawczyk, B. Bauer, F. D'Acquisto, S. Ghosh, W. C. Yeh, G. Baier, R. Rottapel, and J. M. Penninger. 2003. The MAGUK family protein CARD11 is essential for lymphocyte activation. Immunity 18:763-775.
13. Huang, Y., R. P. Wernyj, D. D. Norton, P. Precht, M. C. Seminario, and R. L. Wange. 2005. Modulation of specific protein expression levels by PTEN: identification of AKAP121, DHFR, G3BP, Rap1, and RCC1 as potential targets of PTEN. Oncogene 24:3819-3829.
14. Jiang, T., and Y. Qiu. 2003. Interaction between Src and a C-terminal proline-rich motif of Akt is required for Akt activation. J. Biol. Chem. 278:15789-15793.
15. 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.
16. L levels in vivo. J. Exp. Med. 191:1721-1734.
17. Jones, R. G., S. D. Saibil, J. M. Pun, A. R. Elford, M. Bonnard, M. Pellegrini, S. Arya, M. E. Parsons, C. M. Krawczyk, S. Gerondakis, W. C. Yeh, J. R. Woodgett, M. R. Boothby, and P. S. Ohashi. 2005. NF-κB couples protein kinase B/Akt signaling to distinct survival pathways and the regulation of lymphocyte homeostasis in vivo. J. Immunol. 175:3790-3799.
18. Kane, L. P., P. G. Andres, K. C. Howland, A. K. Abbas, and A. Weiss. 2001. Akt provides the CD28 co-stimulatory signal for upregulation of IL-2 and IFN-γ but not Th2 cytokines. Nat. Immunol. 2:37-14.
19. Kane, L. P., J. Lin, and A. Weiss. 2002. It's all Rel-ative: NF-κB and CD28 costimulation of T-cell activation. Trends Immunol. 23:413-420.
20. Kane, L. P., M. N. Mollenauer, and A. Weiss. 2004. A proline-rich motif in the C terminus of Akt contributes to its localization in the immunological synapse. J. Immunol. 172:5441-5449.
21. Kane, L. P., M. N. Mollenauer, Z. Xu, C. W. Turck, and A. Weiss. 2002. Akt-dependent phosphorylation specifically regulates Cot induction of NF-κB-dependent transcription. Mol. Cell. Biol. 22:5962-5974.
22. Kane, L. P., V. S. S. Shapiro, D. Stokoe, and A. Weiss. 1999. Induction of NF-κB by the Akt/PKB kinase. Curr. Biol. 9:601-604.
23. Kane, L. P., and A. Weiss. 2003. The PI-3 kinase/Akt pathway and T cell activation: pleiotropic pathways downstream of PIP3. Immunol. Rev. 192:7-20.
24. Karin, M. 1999. How NF-κB is activated: the role of the IκB kinase (IKK) complex. Oncogene 18:6867-6874.
25. Karin, M., and Y. Ben-Neriah. 2000. Phosphorylation meets ubiquitination: the control of NF-κB activity. Annu. Rev. Immunol. 18:621-663.
26. Lee, K.-Y., F. D'Acquisto, M. S. Hayden, J.-H. Shim, and S. Ghosh. 2005. PDK1 nucleates T cell receptor-induced signaling complex for NF-κB activation. Science 308:114-118.
27. Li, Q., and I. M. Verma. 2002. NF-κB regulation in the immune system. Nat. Rev. Immunol. 2:725-734.
28. 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-κB. Mol. Cell. Biol. 20:1626-1638.
29. Newton, K., and V. M. Dixit. 2003. Mice lacking the CARD of CARMA1 exhibit defective B lymphocyte development and impaired proliferation of their B and T lymphocytes. Curr. Biol. 13:1247-1251.
30. Nicholson, K. M., and N. G. Anderson. 2002. The protein kinase B/Akt signalling pathway in human malignancy. Cell. Signal. 14:381-395.
31. Ozes, O. N., L. D. Mayo, J. A. Gustin, S. R. Pfeffer, L. M. Pfeffer, and D. B. Donner. 1999. NF-κB activation by tumour necrosis factor requires the Akt serine-threonine kinase. Nature 401:82-85.
32. Romashkova, J. A., and S. S. Makarov. 1999. NF-κB is a target of AKT in anti-apoptotic PDGF signalling. Nature 401:86-90.
33. Ruefli-Brasse, A. A., W. P. Lee, S. Hurst, and V. M. Dixit. 2004. Rip2 participates in Bcl10 signaling and T-cell receptor-mediated NF-κB activation. J. Biol. Chem. 279:1570-1574.
34. Shan, X., M. J. Czar, S. C. Bunnell, P. Liu, Y. Liu, P. L. Schwartzberg, and R. L. Wange. 2000. Deficiency of PTEN in Jurkat T cells causes constitutive localization of Itk to the plasma membrane and hyperresponsiveness to CD3 stimulation. Mol. Cell. Biol. 20:6945-6957.
35. Shapiro, V. S., K. E. Truitt, J. B. Imboden, and A. Weiss. 1997. CD28 mediates transcriptional upregulation of the interleukin-2 (IL-2) promoter through a composite element containing the CD28RE and NF-IL-2B AP-1 sites. Mol. Cell. Biol. 17:4051-1058.
36. Sizemore, N., S. Leung, and G. R. Stark. 1999. Activation of phosphatidylinositol 3-kinase in response to interleukin-1 leads to phosphorylation and activation of the NF-κB p65/RelA subunit. Mol. Cell. Biol. 19:4798-4805.
37. Steinbrecher, K. A., W. Wilson III, P. C. Cogswell, and A. S. Baldwin. 2005. Glycogen synthase kinase 3β functions to specify gene-specific, NF-κB-dependent transcription. Mol. Cell. Biol. 25:8444-8455.
38. Stilo, R., D. Liguoro, B. Di Jeso, S. Formisano, E. Consiglio, A. Leonardi, and P. Vito. 2004. Physical and functional interaction of CARMA1 and CARMA3 with Iκ kinase γ-NFκB essential modulator. J. Biol. Chem. 279: 34323-34331.
39. Su, H., N. Bidere, L. Zheng, A. Cubre, K. Sakai, J. Dale, L. Salmena, R. Hakem, S. Straus, and M. Lenardo. 2005. Requirement for caspase-8 in NF-κB activation by antigen receptor. Science 307:1465-1468.
40. Sun, L., L. Deng, C. K. Ea, Z. P. Xia, and Z. J. Chen. 2004. The TRAF6 ubiquitin ligase and TAK1 kinase mediate IKK activation by BCL10 and MALT1 in T lymphocytes. Mol. Cell 14:289-301.
41. Thome, M. 2004. CARMA1, BCL-10 and MALT1 in lymphocyte development and activation. Nat. Rev. Immunol. 4:348-359.
42. Thome, M., O. Gaide, O. Micheau, F. Martinon, D. Bonnet, M. Gonzalez, and J. Tschopp. 2001. Equine herpesvirus protein E10 induces membrane recruitment and phosphorylation of its cellular homologue, bcl-10. J. Cell Biol. 152:1115-1122.
43. Tomlinson, M. G., L. P. Kane, J. Su, T. A. Kadlecek, M. N. Mollenauer, and A. Weiss. 2004. Expression and function of Tec, Itk, and Btk in lymphocytes: evidence for a unique role for Tec. Mol. Cell. Biol. 24:2455-2466.
44. van Oers, N. S., and Z. J. Chen. 2005. Cell biology. Kinasing and clipping down the NF-κB trail. Science 308:65-66.
45. Vivanco, I., and C. L. Sawyers. 2002. The phosphatidylinositol 3-kinase AKT pathway in human cancer. Nat. Rev. Cancer 2:489-501.
46. Vivarelli, M. S., D. McDonald, M. Miller, N. Cusson, M. Kelliher, and R. S. Geha. 2004. RIP links TLR4 to Akt and is essential for cell survival in response to LPS stimulation. J. Exp. Med. 200:399-404.
47. Wang, D., R. Matsumoto, Y. You, T. Che, X. Y. Lin, S. L. Gaffen, and X. Lin. 2004. CD3/CD28 costimulation-induced NF-κB activation is mediated by recruitment of protein kinase C-θ, Bcl10, and IκB kinase β to the immunological synapse through CARMA1. Mol. Cell. Biol. 24:164-171.
48. Wang, D., Y. You, S. M. Case, L. M. McAllister-Lucas, L. Wang, P. S. DiStefano, G. Nunez, J. Bertin, and X. Lin. 2002. A requirement for CARMA1 in TCR-induced NF-κB activation. Nat. Immunol. 3:830-835.
49. Zhao, Z., W. H. Leister, R. G. Robinson, S. F. Barnett, D. Defeo-Jones, R. E. Jones, G. D. Hartman, J. R. Huff, H. E. Huber, M. E. Duggan, and C. W. Lindsley. 2005. Discovery of 2,3,5-trisubstituted pyridine derivatives as potent Akt1 and Akt2 dual inhibitors. Bioorg. Med. Chem. Lett. 15:905-909.
50. Zhou, H., I. Wertz, K. O'Rourke, M. Ultsch, S. Seshagiri, M. Eby, W. Xiao, and V. M. Dixit. 2004. Bcl10 activates the NF-κB pathway through ubiquitination of NEMO. Nature 427:167-171.