NFAT and NFκB activation in T lymphocytes: A model of differential activation of gene expression

Annals of Biomedical Engineering

Volumn 34, Issue 11, 2006, Pages 1712-1728

  Fisher, Wayne G ^a   Yang, Pei Chi ^b   Medikonduri, Ram K ^a   Jafri, M Saleet ^b,c  

^a UNIVERSITY OF TEXAS AT DALLAS   (United States)

^b GEORGE MASON UNIVERSITY   (United States)

^c UNIVERSITY OF MARYLAND BIOTECHNOLOGY INSTITUTE   (United States)

Author keywords

Calcium; Computational model; Immune response; T cell

Indexed keywords

ACTIVATION ENERGY; CONCENTRATION (PROCESS); DISSOCIATION; DRUG PRODUCTS; GENES; MATHEMATICAL MODELS; OSCILLATIONS;

DIACYL GLYCEROL (DAG); OSCILLATION FREQUENCIES; RESYNTHESIS RATE; TRANSLOCATION RATE;

CELL CULTURE;

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; TRANSCRIPTION FACTOR NFAT;

ANIMAL; ARTICLE; BIOLOGICAL MODEL; COMPUTER SIMULATION; GENE EXPRESSION; HUMAN; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; SIGNAL TRANSDUCTION; T LYMPHOCYTE;

ANIMALS; COMPUTER SIMULATION; GENE EXPRESSION; HUMANS; LYMPHOCYTE ACTIVATION; MODELS, IMMUNOLOGICAL; NF-KAPPA B; NFATC TRANSCRIPTION FACTORS; SIGNAL TRANSDUCTION; T-LYMPHOCYTES;

EID: 33750701480     PISSN: 00906964     EISSN: 15739686     Source Type: Journal    
DOI: 10.1007/s10439-006-9179-4     Document Type: Article

References (62)

1. Abbott, K. L., B. B. Friday, D. Thaloor, T. J. Murphy, and G. K. Pavlath. Activation and cellular localization of cyclosporine A-sensitive transcription factor NF-AT in skeletal muscle cells. Mol. Biol. Cell. 9:2905-2916, 1998.
2. Alberts, B., D. Bray, J. Lewis, M. Raff, K. Roberts, and J. D. Watson. Molecular Biology of the Cell. Garland Publishing, Inc., New York.
3. Ananthanarayanan, B., R. V. Stahelin, M. A. Digman, and W. Cho. Activation mechanisms of conventional protein kinase C isoforms are determined by the ligand affinity and conformational flexibility of their Cl domains. J. Biol. Chem. 278(47):46886-46894, 2003.
4. Aramburu, J., F. Garcia-Cozar, A. Raghavan, H. Okamura, A. Rao, and P. G. Hogan. Selective inhibition of NFAT activation by a peptide spanning the calcineurin targeting site of NFAT. Mol. Cell. 1:627-637, 1998.
5. Aramburu, J., M. B. Yaffe, C. López-Rodríguez, L. C. Cantley, P. G. Hogan, and A. Rao. Affinity-driven peptide selection of an NFAT inhibitor more selective than cyclosporin A. Science 285:2129-2133, 1999.
6. Arenzana-Seisdedos, F., P. Turpin, M. Rodriguez, D. Thomas, R. T. Hay, J.-L. Virelizier, and C. Dargemont. Nuclear localization of IκBα promotes active transport of NF-κB from the nucleus to the cytoplasm. J. Cell Sci. 110:369-378, 1997.
7. Baeuerle, P. A., and D. Baltimore. IκB: A specific inhibitor of NF-κB transcription factor. Science 242:540-546, 1988.
8. Baeuerle, P. A., and D. Baltimore. NF-κB: Ten years after. Cell 87:13-20, 1998.
9. Beals, C. R., C. M. Sheridan, C. W. Turck, P. Gardner, and G. R. Crabtree. Nuclear export of NF-ATc enhanced by glycogen synthase kinase-3. Science 275:1930-1933, 1997a.
10. Beals, C. R., N. A. Clipstone, S. N. Ho, and G. R. Crabtree. Nuclear localization of NF-ATc by a calcineurindependent, cyclosporin-sensitive intramolecular reaction. Genes Dev. 11:824-834, 1997b.
11. Berridge, M. J., and A. Galione. Cytosolic calcium oscillators. FASEB J. 2:3074-3082, 1988.
12. Birbach, A., P. Gold, B. R. Binder, E. Hofer, R. de Martin, and J. A. Schmid. Signaling molecules of the NF-κB pathway shuttle constitutively between cytoplasm and nucleus. J. Biol. Chem. 277:10842-10851, 2002.
13. Carlotti, F., R. Chapman, S. K. Dower, and E. E. Qwarnstrom. Activation of nuclear factor κB in single living cells. J. Biol. Chem. 274:37941-37949, 1999.
14. Carlotti, F., S. K. Dower, and E. E. Qwarnstrom. Dynamic shuttling of nuclear factor κB between the nucleus and cytoplasm as a consequence of inhibitor dissociation. J. Biol. Chem. 275:41028-41034, 2000.
15. Clipstone, N. A., and G. R. Crabtree. Identification of calcineurin as a key signalling enzyme in T-lymphocyte activation. Nature 357:695-697, 1992.
16. Coudronniere, N., M. Villalba, N. England, and A. Altman. NF-kappa B activation induced by T cell receptor/CD28 costimulation is mediated by protein kinase C-theta. Proc. Natl. Acad. Sci. USA 97(7):3394-3399, 2000.
17. 2+, calcineurin, and NF-AT. Cell 96:611-614, 1999.
18. Crabtree, G. R.. Calcium, calcineurin, and the control of transcription. J. Biol. Chem. 276:2313-2316, 2001.
19. Crabtree, G. R., and E. N. Olson. NFAT signaling: Choreographing the social lives of cells. Cell 109:S67-S79, 2002.
20. DiDonato, J. A., M. Hayakawa, D. M. Rothwarf, E. Zandi, and M. Karin. A cytokine-responsive IκB kinase that activates the transcription factor NF-κB. Nature 388:548-554, 1997.
21. i oscillations in T lymphocytes. J. Gen. Physiol. 103:365-388, 1994.
22. Dolmetsch, R. E., K. Xu, and R. S. Lewis. Calcium oscillations increase the efficiency and specificity of gene expression. Nature 392:933-936, 1998.
23. Feske, S., R. Draeger, H.-H. Peter, K. Eichmann, and A. Rao. The duration of nuclear residence of NFAT determines the pattern of cytokine expression in human SCID T cells. J. Immunol. 165:297-305, 2000.
24. Fiering, S., J. P. Northrop, G. P. Nolan, P. S. Mattila, G. R. Crabtree, and I. A. Herzenberg. Single cell assay of a transcription factor reveals a threshold in transcription activated by signals emanating from the T-cell antigen receptor. Genes. Dev. 4:1823-1834, 1990.
25. Ghosh, S., M. J. May, and E. B. Kopp. NF-κB and Rel proteins: Evolutionarily conserved mediators of immune responses. Annu. Rev. Immunol. 16:225-260, 1998.
26. Hoffmann, A., A. Levchenko, M. L. Scott, and D. Baltimore. The IκB-NF-κB signaling module: Temporal control and selective activation. Science 298:1241-1245, 2002.
27. Huang, T. T., N. Kudo, M. Yoshida, and S. Miyamoto. A nuclear export signal in the N-terminal regulatory domain of IκBα controls cytoplasmic localization of inactive NF-κB/IκBα complexes. Proc. Natl. Acad. Sci. USA 97:1014-1019, 2000.
28. Huang, J., P. Lo, T. Zal, N. R. J. Gascoigne, B. A. Smith, S. D. Levin, and H. M. Grey. CD28 plays a critical role in the segregation of PKC theta within the immunologic synapse. Proc. Natl. Acad. Sci. USA 99(14):9369-9373, 2002.
29. Kakalis, L. T., M. Kennedy, R. Sikkink, F. Rusnak, and I. M. Armitage. Characterization of the calcium-binding sites of calcineurin B. FEBS Lett. 362:55-58, 1995.
30. Kiani, A., A. Rao, and J. Aramburu. Manipulating immune responses with immunosuppressive agents that target NFAT. Immunity 12:359-372, 2000.
31. Klee, C. B., G. F. Draetta, and M. J. Hubbard. Calcineurin. Adv. Enzymol. Relat. Areas 61:149-200, 1988.
32. Klee, C. B., H. Ren, and X. Wang. Regulation of the calmodulin-stimulated protein phosphatase, calcineurin. J. Biol. Chem. 273:13367-13370, 1998.
33. Lin, X., A. O'Mahony, Y. Mu, R. Geleziunas, and W.C. Greene. Protein kinase C-theta participates in NF-kappaB activation induced by CD3-CD28 costimulation through selective activation of IkappaB kinase beta. Mol. Cell Biol. 20(8):2933-2940, 2000.
34. Loh, C., K.T.-Y. Shaw, J. Carew, J. P. B. Viola, C. Luo, B. A. Perrino, and A. Rao. Calcineurin binds the transcription factor NFAT1 and reversibly regulates its activities. J. Blol. Chem. 271:10884-10891, 1996.
35. Luo, C., K.T.-Y. Shaw, A. Raghavan, J. Aramburu, F. Garcia-Cozar, B.A. Perrino, P.G. Hogan, and A. Rao. Interaction of calcineurin with a domain of the transcription factor NFAT1 that controls nuclear import. Proc. Null. Acacl. Sci. 93:8907-8912, 1996.
36. Mercurio, F., H. Zhu, B. W. Murray, A. Shevchenko, B. L. Bennett, J. Li, D. B. Young, M. Barbosa, M. Mann, A. Manning, and A. Rao. IKK-1 and IKK-2: Cytokine-activated IκB kinases essential for NF-κB activation. Science 278:860-866, 1997.
37. 2+ influx signals into long term substrate phosphorylation through activation of two distinct classes of protein kinase C. J. Biol Chem. 278(11):9896-9904, 2003.
38. 2+-signaling cycle of a membrane-docking C2 domain. Biochemistry 36(40):12011-12018, 1997.
39. O'Keefe, S. J., J. Tamura, R. L. Kincaid, M. J. Tocci, and E. A. O'Neill. FK-506- and CsA-sensitive activation of the interleukin-2 promoter by calcineurin. Nature 357:692-694, 1992.
40. Okamura, H., J. Aramburu, C. Garcia-Rodriguez, J. P. Viola, A. Raghavan, M. Tahilia, X. Zhang, J. Qin, P. G. Hogan, and A. Rao. Concerted dephosphorylation of the transcription factor NFAT1 induces a conformational switch that regulates transcriptional activity. Mol. Cell. 6:539-550, 2000.
41. Park, S., U. Motonari, and G. L. Verdine. A second calcineurin binding site on the NFAT regulatory domain. Proc. Natl. Acad. Sci. USA 97:7130-7135, 2000.
42. 2+ mobilization and NFAT cell activation in primary mouse T cells. J. Exp. Med. 197:1525-1535, 2003.
43. Porter, C. M., M. A. Havens, and N. A. Clipstone. Identification of amino acid residues and protein kinases involved in the regulation of NFATc subcellular localization. J. Biol. Chem. 275:3543-3551, 2000.
44. Rao, A., C. Luo, and P. G. Hogan. Transcription factors of the NFAT family: Regulation and function. Annu. Rev. Immunol. 15:707-747, 1997.
45. Ruff, V. A., and K. L. Leach. Direct demonstration of NFATp dephosphorylation and nuclear localization in activated HT-2 cells using a specific NFATp polyclonal antibody. J. Biol. Chem. 270:22602-22607, 1995.
46. Salazar, C., and T. Höfer. Allosteric regulation of the transcription factor NFAT1 by multiple phosphorylation sites: A mathematical analysis. J. Mol. Biol. 327:31-45, 2003.
47. San-Antonio, B., M. A. iniguez, and M. Fresno. Protein kinase C phophorylates nuclear factor of activated T cells and regulates its transactivating activity. J. Biol. Chem. 277:27073-27080, 2002.
48. Schaeffer, E. M., and P. L. Schwartzberg. Tec family kinases in lymphocyte signaling and function. Curr. Opin. Immunol. 12:282-288, 2000.
49. Serfling, E., F. Berberich-Siebelt, S. Chuvpilo, E. Jankevics, S. Klein-Hessling, T. Twardzik, and A. Avots. The role of NF-AT transcription factors in T cell activation and differentiation. Biochim. Biophys. Acta 1498:1-18, 2000.
50. Shaw, J.-P., P. J. Utz, D. B. Durand, J. J. Toole, E. A. Emmel, and G. R. Crabtree. Identification of a putative regulator of early T cell activation genes. Science 241:202-205, 1988.
51. Shaw, K. T.-Y., A. M. Ho, A. Raghavan, J. Kim, J. Jain, J. Park, S. Sharma, A. Rao, and P. G. Hogan. Immunosuppressive drugs prevent a rapid dephosphorylation of transcription factor NFAT1 in stimulated immune cells. Proc. Natl, Acad, Sci. USA 92:11205-11209, 1995.
52. Shibasaki, F., E. R. Price, D. Milan, and F. McKeon. Role of kinases and the phosphatase calcineurin in the nuclear shuttling of transcription factor NF-AT4. Nature 382:370-373, 1996.
53. Szamel, M., A. Appel, R. Schwinzer, and K. Resch. Different protein kinase C isoenzymes regulate IL-2 receptor expression or IL-2 synthesis in human lymphocytes stimulated via the TCR. J. Immunol. 160(5):2207-2214, 1998.
54. 2+ signals and immunosuppression. Nature 383:837-840, 1996.
55. Trushin, S. A., K. N. Pennington, A. Algeciras-Schimnich, and C. V. Paya. Protein kinase C and calcineurin synergize to activate IκB kinase and NFκB in T Lymphocytes. J. Biol. Chem. 274:22923-22931, 1999.
56. Trushin, S. A., K. N. Pennington, E. M. Carmona, S. Asin, D. N. Savoy, D. D. Billadeau, and C. V. Paya. Protein kinase Cα (PKCα) acts upstream of PKCθ to activate IκB kinase and NF-κB in T lymphocytes. Mol. Cell. Biol. 23:7068-7081, 2003.
57. Villalba, M., and A. Altman. Protein Kinase C-θ (PKCθ), a Potential Drug Target for Therapeutic Intervention with Human T Cell Leukemias. Curr. Cancer Drug Targets 2(2):125-137, 2002.
58. Wechsler, A. S., M. C. Gordon, U. Dendorfer, and K. P. LeClair. Induction of IL-8 expression in T cell uses the CD28 costimulatory pathway. J. Immunol. 153:2515-2523, 1994.
59. Wesselborg, S., D. A. Fruman, J. K. Sagoo, B. E. Bierer, and S. J. Burakoff. Identification of a physical interaction between calcineurin and nuclear factor of activated T cells (NFATp). J. Biol. Chem. 271:1274-1277, 1996.
60. Yang, L., H. Chen, and E. Qwarnstrom. Degradation of IκBα is limited by a postphosphorylation/ubiquitination event. Biochem. Biophys. Res. Commun. 285:603-608, 2001.
61. Yaron, A., A. Hatzubai, M. Davis, I. Lavon, S. Amit, A. M. Manning, J. S. Andersen, M. Mann, F. Mercurio, and Y. Ben-Neriah. Identification of the receptor component of the Iκ-Bα-ubiquitin ligase. Nature 396:590-594, 1998.
62. Zhu, J., and F. McKeon. NF-AT activation requires suppression of Crm 1-dependent export by calcineurin. Nature 398:256-260, 1999.