Quantitative Network Signal Combinations Downstream of TCR Activation Can Predict IL2 Production Response1 (original) (raw)

Abstract

Proximal signaling events activated by TCR-peptide/MHC (TCR-pMHC) binding have been the focus of intense ongoing study, but understanding how the consequent downstream signaling networks integrate to govern ultimate avidity-appropriate TCR- pMHC T cell responses remains a crucial next challenge. We hypothesized that a quantitative combination of key downstream network signals across multiple pathways must encode the information generated by TCR

Loading...

Loading Preview

Sorry, preview is currently unavailable. You can download the paper by clicking the button above.

References (39)

  1. Lanzavecchia, A., G. Lezzi, and A. Viola. 1999. From TCR engagement to T cell activation: a kinetic view of T cell behavior. Cell 96: 1-4.
  2. Irvine, D. J., M. A. Purbhoo, M. Krogsgaard, and M. M. Davis. 2002. Direct observation of ligand recognition by T cells. Nature 419: 845-849.
  3. Krogsgaard, M., and M. M. Davis. 2005. How T cells 'see' antigen. Nat. Immu- nol. 6: 239 -245.
  4. Li, Q. J., A. R. Dinner, S. Qi, D. J. Irvine, J. B. Huppa, M. M. Davis, and A. K. Chakraborty. 2004. CD4 enhances T cell sensitivity to antigen by coordi- nating Lck accumulation at the immunological synapse. Nat. Immunol. 5: 791-799.
  5. Gascoigne, N. R., T. Zal, and S. M. Alam. 2001. T-cell receptor binding kinetics in T-cell development and activation. Expert Rev. Mol. Med. 2001: 1-17.
  6. Madrenas, J., R. L. Wange, J. L. Wang, N. Isakov, L. E. Samelson, and R. N. Germain. 1995. Zeta phosphorylation without ZAP-70 activation induced by TCR antagonists or partial agonists. Science 267: 515-518.
  7. Sloan-Lancaster, J., A. S. Shaw, J. B. Rothbard, and P. M. Allen. 1994. Partial T cell signalling: altered phospho-and lack of zap70 recruitment in APL-induced T cell anergy. Cell 79: 913-922.
  8. Germain, R. N., and I. Stefanova. 1999. The dynamics of T cell receptor signal- ling: complex orchestration and the key roles of tempo and cooperation. Annu. Rev. Immunol. 17: 467-522.
  9. Huang, Y., and R. L. Wange. 2004. T cell receptor signalling: beyond complex complexes. J. Biol. Chem. 279: 28827-28830.
  10. Jain, J., C. Loh, and A. Rao. 1995. Transcriptional regulation of the IL-2 gene. Curr. Opin. Immunol. 7: 333-342.
  11. Prudhomme, W., G. Q. Daley, P. Zandstra, and D. A. Lauffenburger. 2004. Mul- tivariate proteomic analysis of murine embryonic stem cell self-renewal versus differentiation signaling. Proc. Natl. Acad. Sci. USA 101: 2900 -2905.
  12. Janes, K. A., J. G. Albeck, S. Gaudet, P. K. Sorger, D. A. Lauffenburger, and M. B. Yaffe. 2005. A systems model of signaling identifies a molecular basis set for cytokine-induced apoptosis. Science 310: 1646 -1653.
  13. Wolf-Yadlin, A., N. Kumar, Y. Zhang, S. Hautaniemi, M. Zaman, H. D. Kim, V. Grantcharova, D. A. Lauffenburger, and F. M. White. 2006. Effects of HER2 overexpression on cell signaling networks governing proliferation and migration. Mol. Syst. Biol. 2: 54.
  14. Ideker, T., and D. Lauffenburger. 2003. Building with a scaffold: emerging strat- egies for high-to low-level cellular modelling. Trends Biotechnol. 21: 255-262.
  15. Janes, K. A., and D. A. Lauffenburger. 2006. A biological approach to compu- tational models of proteomic networks. Curr. Opin. Chem. Biol. 10: 73-80.
  16. Janes, K. A., J. R. Kelly, S. Gaudet, J. G. Albeck, P. K. Sorger, and D. A. Lauffenburger. 2004. Cue-signal-response analysis of TNF-induced apo- ptosis by partial least squares regression of dynamic multivariate data. J. Comput. Biol. 11: 544 -561.
  17. Gaudet, S., K. A. Janes, J. G. Albeck, E. A. Pace, D. A. Lauffenburger, and P. K. Sorger. 2005. A compendium of signals and responses triggered by prodeath and prosurvival cytokines. Mol. Cell Proteomics 4: 1569 -1590.
  18. Nicholson, L. B., H. Waldner, A. M. Carrizosa, A. Sette, M. Collins, and V. K. Kuchroo. 1998. Heteroclitic proliferative responses and changes in cyto- kine profile induced by altered peptides: implications for autoimmunity. Proc. Natl. Acad. Sci. USA 95: 264 -269.
  19. Munder, M., E. Bettelli, L. Monney, J. M. Slavik, L. B. Nicholson, and V. K. Kuchroo. 2002. Reduced self-reactivity of an autoreactive T cell after activation with cross-reactive non-self-ligand. J. Exp. Med. 196: 1151-1162.
  20. Janes, K. A., J. G. Albeck, L. X. Peng, P. K. Sorger, D. A. Lauffenburger, and M. B. Yaffe. 2003. A high-throughput quantitative multiplex kinase assay for monitoring information flow in signaling networks: application to sepsis-apop- tosis. Mol. Cell Proteomics 2: 463-473.
  21. Aube, A. C., J. Cabarrocas, J. Bauer, D. Philippe, P. Aubert, F. Doulay, R. Liblau, J. P. Galmiche, and M. Neunlist. 2006. Changes in enteric neurone phenotype and intestinal functions in a transgenic mouse model of enteric glia disruption. Gut 55: 630 -637.
  22. Wold, S., M. Sjostrom, and L. Eriksson. 2001. PLS-regression: a basic tool of chemometrics. Chemometrics and Intelligent Laboratory Systems 58: 109 -130.
  23. Illes, Z., H. Waldner, J. Reddy, E. Bettelli, L. B. Nicholson, and V. K. Kuchroo. 2005. T cell tolerance induced by cross-reactive TCR ligands can be broken by superagonist resulting in anti-inflammatory T cell cytokine production. J. Immu- nol. 175: 1491-1497.
  24. Kuchroo, V. K., A. C. Anderson, H. Waldner, M. Munder, E. Bettelli, and L. B. Nicholson. 2002. T cell response in experimental autoimmune encephalo- myelitis (EAE): role of self and cross-reactive antigens in shaping, tuning, and regulating the autopathogenic T cell repertoire. Annu. Rev. Immunol. 20: 101-123.
  25. Ashwell, J. D., R. E. Cunningham, P. D. Noguchi, and D. Hernandez. 1987. Cell growth cycle block of T cell hybridomas upon activation with antigen. J. Exp. Med. 165: 173-194.
  26. Abastado, J. P., Y. C. Lone, A. Casrouge, G. Boulot, and P. Kourilsky. 1995. Dimerization of soluble major histocompatibility complex-peptide complexes is sufficient for activation of T cell hybridoma and induction of unresponsiveness. J. Exp. Med. 182: 439 -447.
  27. Schmid, D. A., J. P. Depta, M. Luthi, and W. J. Pichler. 2006. Transfection of drug-specific T-cell receptors into hybridoma cells: tools to monitor drug inter- action with T-cell receptors and evaluate cross-reactivity to related compounds. Mol. Pharmacol. 70: 356 -365.
  28. Kersh, G. J., E. N. Kersh, D. H. Fremont, and P. M. Allen. 1998. High-and low-potency ligands with similar affinities for the TCR: the importance of kinet- ics in TCR signaling. Immunity 9: 817-826.
  29. Ortega-Perez, I., E. Cano, F. Were, M. Villar, J. Vazquez, and J. M. Redondo. 2005. c-Jun N-terminal kinase (JNK) positively regulates NFATc2 transactiva- tion through phosphorylation within the N-terminal regulatory domain. J. Biol. Chem. 280: 20867-20878.
  30. Marshall, C. J. 1995. Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation. Cell 80: 179 -185.
  31. Mariathasan, S., A. Zakarian, D. Bouchard, A. M. Michie, J. C. Zuniga-Pflucker, and P. S. Ohashi. 2001. Duration and strength of extracellular signal-regulated kinase signals are altered during positive versus negative thymocyte selection. J. Immunol. 167: 4966 -4973.
  32. Werlen, G., B. Hausmann, and E. Palmer. 2000. A motif in the ␣␤ T-cell receptor controls positive selection by modulating ERK activity. Nature 406: 422-426.
  33. Diehn, M., A. A. Alizadeh, O. J. Rando, C. L. Liu, K. Stankunas, D. Botstein, G. R. Crabtree, and P. O. Brown. 2002. Genomic expression programs and the integration of the CD28 costimulatory signal in T cell activation. Proc. Natl. Acad. Sci. USA 99: 11796 -11801.
  34. Patra, A. K., S. Y. Na, and U. Bommhardt. 2004. Active protein kinase B reg- ulates TCR responsiveness by modulating cytoplasmic-nuclear localization of NFAT and NF-B proteins. J. Immunol. 172: 4812-4820.
  35. Kane, L. P., V. S. Shapiro, D. Stokoe, and A. Weiss. 1999. Induction of NF-B by the Akt/PKB kinase. Curr. Biol. 9: 601-604.
  36. Kane, L. P., P. G. Andres, K. C. Howland, A. K. Abbas, and A. Weiss. 2001. Akt provides the CD28 costimulatory signal for up-regulation of IL-2 and IFN-␥ but not TH2 cytokines. Nat. Immunol. 2: 37-44.
  37. 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, et al. 2005. NF-B couples protein kinase B/Akt signaling to distinct survival pathways and the regulation of lymphocyte homeostasis in vivo. J. Immunol. 175: 3790 -3799.
  38. Jones, R. G., M. Parsons, M. Bonnard, V. S. Chan, W. C. Yeh, J. R. Woodgett, and P. S. Ohashi. 2000. Protein kinase B regulates T lymphocyte survival, nuclear factor B activation, and Bcl-X L levels in vivo. J. Exp. Med. 191: 1721-1734.
  39. Schade, A. E., and A. D. Levine. 2004. Cutting edge: extracellular signal-regu- lated kinases 1/2 function as integrators of TCR signal strength. J. Immunol. 172: 5828 -5832.