PTEN permits acute increases in D3-phosphoinositide levels following TCR stimulation but inhibits distal signaling events by reducing the basal activity of Akt

European Journal of Immunology

Volumn 34, Issue 11, 2004, Pages 3165-3175

  Seminario, Maria Cristina ^a   Precht, Patricia ^a   Bunnell, Stephen C ^b,c   Warren, Sarah E ^a   Morris, Christa M ^a   Taub, Dennis ^a   Wange, Ronald L ^a  

^a NATIONAL INSTITUTE ON AGING   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

^c TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cellular activation; PTEN; Signal transduction; T cell receptors; T lymphocytes

Indexed keywords

CALCIUM ION; CD69 ANTIGEN; GLYCOGEN SYNTHASE KINASE 3; INTERLEUKIN 2; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITIDE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PHOSPHOLIPASE C; PROTEIN KINASE B; T LYMPHOCYTE RECEPTOR; TRANSCRIPTION FACTOR NFAT;

ANTIGEN EXPRESSION; ARTICLE; CALCIUM TRANSPORT; CONTROLLED STUDY; CORRELATION ANALYSIS; CYTOKINE PRODUCTION; CYTOTOXICITY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; LYMPHOMA CELL LINE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION;

ANDROSTADIENES; ANTIGENS, CD; ANTIGENS, DIFFERENTIATION, T-LYMPHOCYTE; CALCIUM; DNA-BINDING PROTEINS; GLYCOGEN SYNTHASE KINASE 3; HUMANS; INTERLEUKIN-2; JURKAT CELLS; MICROSCOPY, CONFOCAL; MITOGEN-ACTIVATED PROTEIN KINASE 1; NFATC TRANSCRIPTION FACTORS; NUCLEAR PROTEINS; PHOSPHATIDYLINOSITOL PHOSPHATES; PHOSPHOLIPASE C; PHOSPHOLIPASE C GAMMA; PHOSPHORIC MONOESTER HYDROLASES; PROTEIN KINASE INHIBITORS; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; PTEN PHOSPHOHYDROLASE; RECEPTORS, ANTIGEN, T-CELL; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TUMOR SUPPRESSOR PROTEINS;

EID: 9244248593     PISSN: 00142980     EISSN: None     Source Type: Journal    
DOI: 10.1002/eji.200425206     Document Type: Article

References (41)

1. Ward, S. G. and Cantrell, D. A., Phosphoinositide 3-kinases in T lymphocyte activation. Curr. Opin. Immunol. 2001. 13: 332-338.
2. Seminario, M. C. and Wange, R. L., Lipid phosphatases in the regulation of T cell activation: living up to their PTEN-tial. Immunol. Rev. 2003. 192: 80-97.
3. Suzuki, A., Yamaguchi, M. T., Ohteki, T., Sasaki, T., Kaisho, T., Kimura, Y., Yoshida, R., Wakeham, A., Higuchi, T., Fukumoto, M. et al., T cell-specific loss of Pten leads to defects in central and peripheral tolerance. Immunity 2001. 14: 523-534.
4. Borlado, L. R., Redondo, C., Alvarez, B., Jimenez, C., Criado, L. M., Flores, J., Marcos, M. A., Martinez, A., Balomenos, D. and Carrera, A. C., Increased phosphoinositide 3-kinase activity induces a lymphoproliferative disorder and contributes to tumor generation in vivo. FASEB J. 2000. 14: 895-903.
5. Okkenhaug, K., Bilancio, A., Farjot, G., Priddle, H., Sancho, S., Peskett, E., Pearce, W., Meek, S. E., Salpekar, A., Waterfield, M. D. et al., Impaired B and T cell antigen receptor signaling in p110δ PI 3-kinase mutant mice. Science 2002. 297: 1031-1034.
6. Sasaki, T., Irie-Sasaki, J., Jones, R. G., Oliveira dos Santos A. J., Stanford, W. L., Bolon, B., Wakeham, A., Itie, A., Bouchard, D., Kozieradzki, I. et al., Function of PI3Kγ in thymocyte development, T cell activation, and neutrophil migration. Science 2000. 287: 1040-1046.
7. Hirsch, E., Katanaev, V. L., Garlanda, C., Azzolino, O., Pirola, L., Silengo, L., Sozzani, S., Mantovani, A., Altruda, F. and Wymann, M. P., Central role for G protein-coupled phosphoinositide 3-kinase γ in inflammation. Science 2000. 287: 1049-1053.
8. Reynolds, L. F., Smyth, L. A., Norton, T., Freshney, N., Downward, J., Kioussis, D. and Tybulewicz, V. L., Vav1 transduces T cell receptor signals to the activation of phospholipase C-γ1 via phosphoinositide 3-kinase-dependent and - independent pathways. J. Exp. Med. 2002. 195: 1103-1114.
9. Von Willebrand, M., Jascur, T., Bonnefoy-Berard, N., Yano, H., Altman, A., Matsuda, Y. and Mustelin, T., Inhibition of phosphatidylinositol 3-kinase blocks T cell antigen receptor/CD3-induced activation of the mitogen-activated kinase Erk2. Eur. J. Biochem. 1996. 235: 828-835.
10. Sakai, A., Thieblemont, C., Wellmann, A., Jaffe, E. S. and Raffeld, M., PTEN gene alterations in lymphoid neoplasms. Blood 1998. 92: 3410-3415.
11. Shan, X., Czar, M. J., Bunnell, S. C., Liu, P., Liu, Y., Schwartzberg, P. L. and Wange, R. L., Deficiency of PTEN in Jurkat T cells causes constitutive localization of itk to the plasma membrane and hyperresponsiveness to CD3 stimulation. Mol. Cell. Biol. 2000. 20: 6945-6957.
12. Xu, Z., Stokoe, D., Kane, L. P. and Weiss, A., The inducible expression of the tumor suppressor gene PTEN promotes apoptosis and decreases cell size by inhibiting the PI3K/Akt pathway in Jurkat T cells. Cell Growth Differ. 2002. 13: 285-296.
13. Wang, X., Gjorloff-Wingren, A., Saxena, M., Pathan, N., Reed, J. C. and Mustelin, T., The tumor suppressor PTEN regulates T cell survival and antigen receptor signaling by acting as a phosphatidylinositol 3-phosphatase. J. Immunol. 2000. 164: 1934-1939.
14. Seminario, M. C., Precht, P., Wersto, R. P., Gorospe, M. and Wange, R. L., PTEN expression in PTEN-null leukaemic T cell lines leads to reduced proliferation via slowed cell cycle progression. Oncogene 2003. 22: 8195-8204.
15. Freeburn, R. W., Wright, K. L., Burgess, S. J., Astoul, E., Cantrell, D. A. and Ward, S. G., Evidence that SHIP-1 contributes to phosphatidylinositol 3,4,5-trisphosphate metabolism in T lymphocytes and can regulate novel phosphoinositide 3-kinase effectors. J. Immunol. 2002. 162: 5441-5450
16. Barz, C., Nagel, T., Truitt, K. E. and Imboden, J. B., Mutational analysis of CD28-mediated costimulation of Jun-N-terminal kinase and IL-2 production. J. Immunol. 1998. 161: 5366-5372.
17. Servant, G., Weiner, O. D., Herzmark, P., Balla, T., Sedat, J. W. and Bourne, H. R., Polarization of chemoattractant receptor signaling during neutrophil chemotaxis. Science 2000. 287: 1037-1040.
18. Varnai, P., Rother, K. I. and Balla, T., Phosphatidylinositol 3-kinase-dependent membrane association of the Bruton's tyrosine kinase pleckstrin homology domain visualized in single living cells. J. Biol. Chem. 1999. 274: 10983-10989.
19. Bunnell, S. C., Hong, D. I., Kardon, J. R., Yamazaki, T., McGlade, C. J., Barr, V. A. and Samelson, L. E., T cell receptor ligation induces the formation of dynamically regulated signaling assemblies. J. Cell Biol. 2002. 158: 1263-1275.
20. Beals, C. R., Sheridan, C. M., Turck, C. W., Gardner, P. and Crabtree, G. R., Nuclear export of NF-ATc enhanced by glycogen synthase kinase-3. Science 1997. 275: 1930-1934.
21. Boyle, W. J., Smeal, T., Defize, L. H., Angel, P., Woodgett, J. R., Karin, M. and Hunter, T., Activation of protein kinase C decreases phosphorylation of c-Jun at sites that negatively regulate its DNA-binding activity. Cell 1991. 64: 573-584.
22. de Groot, R. P., Auwerx, J., Bourouis, M. and Sassone-Corsi, P., Negative regulation of Jun/AP-1: conserved function of glycogen synthase kinase 3 and the Drosophila kinase shaggy. Oncogene 1993. 8: 841-847.
23. Nikolakaki, E., Coffer, P. J., Hemelsoet, R., Woodgett, J. R. and Defize, L. H., Glycogen synthase kinase 3 phosphorylates Jun family members in vitro and negatively regulates their transactivating potential in intact cells. Oncogene 1993. 8: 833-840.
24. Ohteki, T., Parsons, M., Zakarian, A., Jones, R. G., Nguyen, L. T., Woodgett, J. R. and Ohashi, P. S., Negative regulation of T cell proliferation and interleukin 2 production by the serine threonine kinase GSK-3. J. Exp. Med. 2000. 192: 99-104.
25. Klein, P. S. and Melton, D. A., A molecular mechanism for the effect of lithium on development. Proc. Natl. Acad. Sci. U. S. A. 1996. 93: 8455-8459.
26. Ebinu, J. O., Stang, S. L., Teixeira, C., Bottorff, D. A., Hooton, J., Blumberg, P. M., Barry, M., Bleakley, R. C., Ostergaard, H. L. and Stone, J. C., RasGRP links T-cell receptor signaling to Ras. Blood 2000. 95: 3199-3203.
27. Gu, J., Tamura, M., Pankov, R., Danen, E. H., Takino, T., Matsumoto, K. and Yamada, K. M., Shc and FAK differentially regulate cell motility and directionality modulated by PTEN. J. Cell Biol. 1999. 146: 389-403.
28. Iwashima, M., Takamatsu, M., Yamagishi, H., Hatanaka, Y., Huang, Y. Y., McGinty, C., Yamasaki, S. and Koike, T., Genetic evidence for Shc requirement in TCR-induced c-Rel nuclear translocation and IL-2 expression. Proc. Natl. Acad. Sci. U. S. A. 2002. 99: 4544-4549.
29. Neal, J. W. and Clipstone, N. A., Glycogen synthase kinase-3 inhibits the DNA binding activity of NFATc. J. Biol. Chem. 2001. 276: 3666-3673.
30. Cross, D. A., Alessi, D. R., Cohen, P., Andjelkovich, M. and Hemmings, B. A., Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 1995. 378: 785-789.
31. Du, K. and Montminy, M., CREB is a regulatory target for the protein kinase Akt/PKB. J. Biol. Chem. 1998. 273: 32377-32379.
32. Kaptein, J. S., Yang, C. L., Lin, C. K., Nguyen, T. T., Chen, F. S. and Lad, P. M., Synergy between signal transduction pathways is obligatory for expression of c-fos in B and T cell lines: implication for c-fos control via surface immunoglobulin and T cell antigen receptors. Immunobiology 1995. 193: 465-485.
33. Kane, L. P., Shapiro, V. S., Stokoe, D. and Weiss, A., Induction of NF-κB by the Akt/PKB kinase. Curr. Biol. 1999. 9: 601-604.
34. Parsons, M. J., Jones, R. G., Tsao, M. S., Odermatt, B., Ohashi, P. S. and Woodgett, J. R., Expression of active protein kinase B in T cells perturbs both T and B cell homeostasis and promotes inflammation. J. Immunol. 2001. 167: 42-48.
35. Eder, A. M., Dominguez, L., Franke, T. F. and Ashwell, J. D., Phosphoinositide 3-kinase regulation of T cell receptor-mediated interleukin-2 gene expression in normal T cells. J. Biol. Chem. 1998. 273: 28025-28031.
36. Kane, L. P., Lin, J. and Weiss, A., It's all Rel-ative: NF-κB and CD28 costimulation of T-cell activation. Trends Immunol. 2002. 23: 413-420.
37. Gustin, J. A., Maehama, T., Dixon, J. E. and Donner, D. B., The PTEN tumor suppressor protein inhibits tumor necrosis factor-induced nuclear factor κB activity. J. Biol. Chem. 2001. 276: 27740-27744.
38. Kane, L. P., Andres, P. G., Howland, K. C., Abbas, A. K. and Weiss, A., Akt provides the CD28 costimulatory signal for up-regulation of IL-2 and IFN-γ but not TH2 cytokines. Nat. Immunol. 2001. 2: 37-44.
39. + regulatory T cells. J. Immunol. 2004. 172: 5287-5296.
40. Wange, R. L., Guitian, R., Isakov, N., Watts, J. D., Aebersold, R. and Samelson, L. E., Activating and inhibitory mutations in adjacent tyrosines in the kinase domain of ZAP-70. J. Biol. Chem. 1995. 270: 18730-18733.
41. Liu, K. Q., Bunnell, S. C., Gurniak, C. B. and Berg, L. J., T cell receptor-initiated calcium release is uncoupled from capacitative calcium entry in Itk-deficient T cells. J. Exp. Med. 1998. 187: 1721-1727.