Integration of calcium and cyclic AMP signaling pathways by 14-3-3

Molecular and Cellular Biology

Volumn 20, Issue 2, 2000, Pages 702-712

  Chow, Chi Wing ^a   Davis, Roger J ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; CYCLIC AMP; NUCLEAR FACTOR;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; TRANSCRIPTION REGULATION;

14-3-3 PROTEINS; AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; BUCLADESINE; CALCINEURIN; CALCIUM; CALCIUM SIGNALING; CELL LINE; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION; HUMANS; INTERLEUKIN-2; IONOMYCIN; MOLECULAR SEQUENCE DATA; MUTATION; NFATC TRANSCRIPTION FACTORS; NUCLEAR LOCALIZATION SIGNALS; NUCLEAR PROTEINS; PHOSPHORYLATION; PHOSPHOSERINE; PROTEINS; RECOMBINANT FUSION PROTEINS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TYROSINE 3-MONOOXYGENASE;

ANIMALIA; EUKARYOTA;

EID: 0033972906     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.20.2.702-712.2000     Document Type: Article

References (83)

1. Abbott, K. L., B. B. Friday, D. Thaloor, T. J. Murphy, and G. K. Pavlath. 1998. Activation and cellular localization of the cyclosporine A-sensitive transcription factor NF-AT in skeletal muscle cells. Mol. Biol. Cell 9:2905-2916.
2. Aitken, A. 1995. 14-3-3 proteins on the MAP. Trends Biochem. Sci. 20:95-97.
3. Aramburu, J., F. Garcia-Cozar, A. Raghavan, H. Okamura, A. Rao, and P. G. Hogan. 1998. Selective inhibition of NFAT activation by a peptide spanning the calcineurin targeting site of NFAT. Mol. Cell 1:627-637.
4. Beals, C. R., N. A. Clipstone, S. N. Ho, and G. R. Crabtree. 1997. Nuclear localization of NF-ATc by a calcineurin-dependent, cyclosporin-sensitive intramolecular interaction. Genes Dev. 11:824-834.
5. Beals, C. R., C. M. Sheridan, C. W. Turck, P. Gardner, and G. R. Crabtree. 1997. Nuclear export of NF-ATc enhanced by glycogen synthase kinase-3. Science 275:1930-1934.
6. Bodor, J., and J. F. Habener. 1998. Role of transcriptional repressor ICER in cyclic AMP-mediated attenuation of cytokine gene expression in human thymocytes. J. Biol. Chem. 273:9544-9551.
7. Bonnefoy-Berard, N., Y. C. Liu, M. von Willebrand, A. Sung, C. Elly, T. Mustelin, H. Yoshida, K. Ishizaka, and A. Altman. 1995. Inhibition of phosphatidylinositol 3-kinase activity by association with 14-3-3 proteins in T cells. Proc. Natl. Acad. Sci. USA 92:10142-10146.
8. Boyle, W. J., P. van der Geer, and T. Hunter. 1991. Phosphopeptide mapping and phosphoamino acid analysis by two-dimensional thin layer cellulose plates. Methods Enzymol. 201:110-149.
9. Brunet, A., A. Bonni, M. J. Zigmond, M. Z. Lin, P. Juo, L. S. Hu, M. J. Anderson, K. C. Arden, J. Blenis, and M. E. Greenberg. 1999. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96:857-868.
10. Chang, H. C., and G. M. Rubin. 1997. 14-3-3 epsilon positively regulates Ras-mediated signaling in Drosophila. Genes Dev. 11:1132-1139.
11. Chin, E. R., E. N. Olson, J. A. Richardson, Q. Yang, C. Humphries, J. M. Shelton, H. Wu, W. Zhu, R. Bassel-Duby, and R. S. Williams. 1998. A calcineurin-dependent transcriptional pathway controls skeletal muscle fiber type. Genes Dev. 12:2499-2509.
12. Chow, C.-W., M. Rincon, and R. J. Davis. 1999. Requirement of transcription factor NFAT for interleukin 2 expression. Mol. Cell. Biol. 19:2300-2307.
13. Chow, C. W., M. Rincon, J. Cavanagh, M. Dickens, and R. J. Davis. 1997. Nuclear accumulation of NFAT4 opposed by the JNK signal transduction pathway. Science 278:1638-1641.
14. Clipstone, N. A., and G. R. Crabtree. 1992. Identification of calcineurin as a key signalling enzyme in T-lymphocyte activation. Nature 357:695-697.
15. Crabtree, G. R., and N. A. Clipstone. 1994. Signal transmission between the plasma membrane and nucleus of T lymphocytes. Annu. Rev. Biochem. 63:1045-1083.
16. de la Pompa, J. L., L. A. Timmerman, H. Takimoto, H. Yoshida, A. J. Elia, E. Samper, J. Potter, A. Wakeham, L. Marengere, B. L. Langille, G. R. Crabtree, and T. W. Mak. 1998. Role of the NF-ATc transcription factor in morphogenesis of cardiac valves and septum. Nature 392:182-186.
17. Du, X., J. E. Fox, and S. Pei. 1996. Identification of a binding sequence for the 14-3-3 protein within the cytoplasmic domain of the adhesion receptor, platelet glycoprotein Ib alpha. J. Biol. Chem. 271:7362-7367.
18. Durand, D. B., J.-P. Shaw, M. R. Bush, R. E. Repogla, R. Belagaje, and G. R. Crabtree. 1988. Characterization of antigen receptor response elements within the interleukin-2 enhancer. Mol. Cell. Biol. 8:1715-1724.
19. Fantl, W. J., A. J. Muslin, A. Kikuchi, J. A. Martin, A. M. MacNicol, R. W. Gross, and L. T. Williams. 1994. Activation of Raf-1 by 14-3-3 proteins. Nature 371:612-614.
20. Flanagan, W. M., B. Corthesy, R. J. Bram, and G. R. Crabtree. 1991. Nuclear association of a T-cell transcription factor blocked by FK-506 and cyclosporin A. Nature 352:803-807.
21. Garcia-Cozar, F. J., H. Okamura, J. F. Aramburu, K. T. Y. Shaw, L. Pelletier, R. Showalter, E. Villafranca, and A. Rao. 1998. Two-site interaction of nuclear factor of activated T cells with activated calcineurin. J. Biol. Chem. 273:23877-23883.
22. Haraguchi, S., R. A. Good, and N. K. Day. 1995. Immunosuppressive retroviral peptides: cAMP and cytokine patterns. Immunol. Today 16:595-603.
23. Ho, A. M., J. Jain, A. Rao, and P. G. Hogan. 1994. Expression of the transcription factor NFATp in a neuronal cell line and in the murine nervous system. J. Biol. Chem. 269:28181-28186.
24. Ho, I. C., M. R. Hodge, J. W. Rooney, and L. H. Glimcher. 1996. The proto-oncogene c-maf is responsible for tissue-specific expression of interleukin-4. Cell 85:973-983.
25. Ho, S. N., D. J. Thomas, L. A. Timmerman, X. Li, U. Francke, and G. R. Crabtree. 1995. NFATc3, a lymphoid-specific NFATc family member that is calcium-regulated and exhibits distinct DNA binding specificity. J. Biol Chem. 270:19898-19907.
26. Hodge, M. R., A. M. Ranger, C. F. de la Brousse, T. Hoey, M. J. Grusby, and L. H. Glimcher. 1996. Hyperproliferation and dysregulation of IL-4 expression in NF-ATp-deficient mice. Immunity 4:397-405.
27. Hoey, T., Y. L. Sun, K. Williamson, and X. Xu. 1995. Isolation of two new members of the NF-AT gene family and functional characterization of the NF-AT proteins. Immunity 2:461-472.
28. Hsueh, Y.-P., and M.-Z. Lai. 1995. c-Jun N-terminal kinase but not mitogen-activated protein kinase is sensitive to cAMP inhibition in T lymphocytes. J. Biol. Chem. 270:18094-18098.
29. Jain, J., P. G. McCaffrey, Z. Miner, T. K. Kerppola, J. N. Lambert, G. L. Verdine, T. Curran, and A. Rao. 1993. The T-cell transcription factor NFATp is a substrate for calcineurin and interacts with Fos and Jun. Nature 365:352-355.
30. Kaffman, A., N. M. Rank, E. M. O'Neill, L. S. Huang, and E. K. O'Shea. 1998. The receptor Msn5 exports the phosphorylated transcription factor Pho4 out of the nucleus. Nature 396:482-486.
31. Kammer, G. M. 1988. The adenylate cyclase-cAMP-protein kinase A pathway and regulation of the immune response. Immunol. Today 9:222-229.
32. Kehlenbach, R. H., A. Dickmanns, and L. Gerace. 1998. Nucleocytoplasmic shuttling factors including Ran and CRM1 mediate nuclear export of NFAT in vitro. J. Cell Biol. 141:863-874.
33. Klemm, J. D., C. R. Beals, and G. R. Crabtree. 1997. Rapid targeting of nuclear proteins to the cytoplasm. Curr. Biol. 7:638-644.
34. Kockel, L., G. Vorbruggen, H. Jackle, M. Mlodzik, and D. Bohmann. 1997. Requirement for Drosophila 14-3-3 zeta in Raf-dependent photoreceptor development. Genes Dev. 11:1140-1147.
35. Komeili, A., and E. K. O'Shea. 1999. Roles of phosphorylation sites in regulating activity of the transcription factor Pho4. Science 284:977-980.
36. Ku, N. O., J. Liao, and M. B. Omary. 1998. Phosphorylation of human keratin 18 serine 33 regulates binding to 14-3-3 proteins. EMBO J. 17:1892-1906.
37. Latinis, K. M., L. A. Norian, S. L. Eliason, and G. A. Koretzky. 1997. Two NFAT transcription factor binding sites participate in the regulation of CD95 (Fas) ligand expression in activated human T cells. J. Biol. Chem. 272:31427-31434.
38. Li, B., C. Tournier, R. J. Davis, and R. A. Flavell. 1999. Regulation of IL-4 expression by the transcription factor JunB during T helper cell differentiation. EMBO J. 18:420-432.
39. Li, L., C. Yee, and J. A. Beavo. 1999. CD3-and CD28-dependent induction of PDE7 required for T cell activation. Science 283:848-851.
40. Liu, D., J. Bienkowska, C. Petosa, R. J. Collier, H. Fu, and R. Liddington. 1995. Crystal structure of the zeta isoform of the 14-3-3 protein. Nature 376:191-194.
41. Liu, Y. C., C. Elly, H. Yoshida, N. Bonnefoy-Berard, and A. Altman. 1996. Activation-modulated association of 14-3-3 proteins with Cbl in T cells. J. Biol. Chem. 271:14591-14595.
42. Liu, Y. C., Y. Liu, C. Elly, H. Yoshida, S. Lipkowitz, and A. Altman. 1997. Serine phosphorylation of Cbl induced by phorbol ester enhances its association with 14-3-3 proteins in T cells via a novel serine-rich 14-3-3-binding motif. J. Biol. Chem. 272:9979-9985.
43. Lopez-Girona, A., B. Furnari, O. Mondesert, and P. Russell. 1999. Nuclear localization of Cdc25 is regulated by DNA damage and a 14-3-3 protein. Nature 397:172-175.
44. Luo, C., K. T. Shaw, A. Raghavan, J. Aramburu, F. Garcia-Cozar, B. A. Perrino, P. G. Hogan, and A. Rao, 1996. Interaction of calcineurin with a domain of the transcription factor NFAT1 that controls nuclear import. Proc. Natl. Acad. Sci. USA 93:8907-8912.
45. Masuda, E. S., Y. Naito, H. Tokumitsu, D. Campbell, F. Saito, C. Hannum, K. Arai, and N. Arai. 1995. NFATx, a novel member of the nuclear factor of activated T cells family that is expressed predominantly in the thymus. Mol. Cell. Biol. 15:2697-2706.
46. Maurer, R. A. 1989. Both isoforms of the cAMP-dependent protein kinase catalytic subunit can activate transcription of the prolactin gene. J. Biol. Chem. 264:6870-6873.
47. McCaffrey, P. G., A. E. Goldfeld, and A. Rao. 1994. The role of NFATp in cyclosporin A-sensitive tumor necrosis factor-alpha gene transcription. J. Biol. Chem. 269:30445-30450.
48. McCaffrey, P. G., C. Luo, T. K. Kerppola, J. Jain, T. M. Badalian, A. M. Ho, E. Burgeon, W. S. Lane, J. N. Lambert, T. Curran, et al. 1993. Isolation of the cyclosporin-sensitive T cell transcription factor NFATp. Science 262: 7511-754.
49. Meller, N., Y. C. Liu, T. L. Collins, N. Bonnefoy-Berard, G. Baier, N. Isakov, and A. Altman. 1996. Direct interaction between protein kinase Cθ (PKCθ) and 14-3-3τ in T cells: 14-3-3 overexpression results in inhibition of PKCθ translocation and function. Mol. Cell. Biol. 16:5782-5791.
50. Molkentin, J. D., J. R. Lu, C. L. Antos, B. Markham, J. Richardson, J. Rabbins, S. R. Grant, and E. N. Olson. 1998. A calcineurin-dependent transcriptional pathway for cardiac hypertrophy. Cell 93:215-228.
51. Moore, B. W., and V. J. Perez (ed.). 1967. Specific acidic proteins of the nervous system. Prentice-Hall, Englewood Cliffs, N.J.
52. Munoz, E., A. M. Zubiaga, M. Merrow, N. P. Sauter, and B. T. Huber. 1990. Cholera toxin discriminates between T helper 1 and 2 cells in T cell receptor-mediated activation: role of cAMP in T cell proliferation. J. Exp. Med. 172:95-103.
53. Muslin, A. J., J. W. Tanner, P. M. Allen, and A. S. Shaw. 1996. Interaction of 14-3-3 with signaling proteins is mediated by the recognition of phosphoscrine. Cell 84:889-897.
54. Neumann, M., T. Grieshammer, S. Chuvpilo, B. Kneitz, M. Lohoff, A. Schimpl, B. R. Franza, Jr., and E. Serfling. 1995. Re1A/p65 is a molecular target for the immunosuppressive action of protein kinase A. EMBO J. 14:1991-21104.
55. Nielsen, P. J. 1991. Primary structure of a human protein kinase regulator protein. Biochim. Biophys. Acta 1088:425-428.
56. Northrop, J. P., S. N. Ho, L. Chen, D. J. Thomas, L. A. Timmerman, G. P. Nolan, A. Admon, and G. R. Crabtree. 1994. NF-AT components define a family of transcription factors targeted in T-cell activation. Nature 369:497-502.
57. Oukka, M., I. C. Ho, F. C. de la Brousse, T. Hoey, M. J. Grusby, and L. H. Glimcher. 1998. The transcription factor NFAT4 is involved in the generation and survival of T cells. Immunity 9:295-304.
58. Patel, M. D., L. E. Samelson, and R. D. Klausner. 1987. Multiple kinases and signal transduction: phosphorylation of the T cell antigen receptor complex. J. Biol. Chem. 262:5831-5838.
59. Peng, C. Y., P. R. Graves, R. S. Thoma, Z. Wu, A. S. Shaw, and H. Piwnica-Worms. 1997. Mitotic and G2 checkpoint control: regulation of 14-3-3 protein binding by phosphorylation of Cdc25C on serine-216. Science 277:1501-1505.
60. Perrino, B. A., Y. L. Fong, D. A. Bricky, Y. Saitoh, Y. Ushio, K. Fukunaga, E. Miyamoto, and T. R. Soderling. 1992. Characterization of the phosphatase activity of a baculovirus-expressed calcineurin A isoform. J. Biol. Chem. 267:15965-15969.
61. Ranger, A. M., M. J. Grusby, M. R. Hodge, E. M. Gravallese, F. C. de la Brousse, T. Hoey, C. Mickanin, H. S. Baldwin, and L. H. Glimcher. 1998. The transcription factor NF-ATc is essential for cardiac valve formation. Nature 392:186-190.
62. Rao, A., C. Luo, and P. G. Hogan. 1997. Transcription factors of the NFAT family: regulation and function. Annu. Rev. Immunol. 15:707-747.
63. Reuther, G. W., and A. M. Pendergast. 1996. The roles of 14-3-3 proteins in signal transduction. Vitam. Horm. 52:149-175.
64. Rittinger, K., J. Budman, J. Xu, S. Volinia, L. C. Cantley, S. J. Smerdon, S. J. Gamblin, and M. B. Yaffe. 1999. Structural analysis of 14-3-3 phosphopeptide complexes identifies a dual role for the nuclear export signal of 14-3-3 in ligand binding. Mol. Cell 4:1-20.
65. Roy, S., R. A. McPherson, A. Apolloni, J. Yan, A. Lane, J. Clyde-Smith, and J. F. Hancock. 1998. 14-3-3 facilitates Ras-dependent Raf-1 activation in vitro and in vivo. Mol. Cell. Biol. 18:3947-3955.
66. Ruhlmann, A., and A. Nordheim. 1997. Effects of the immunosuppressive drugs CsA and FK506 on intracellular signalling and gene regulation. Immunobiology 198:192-206.
67. Shaw, J. P., P. J. Utz, D. B. Durand, J. J. Toole, E. A. Emmel, and G. R. Crabtree. 1988. Identification of a putative regulator of early T cell activation genes. Science 241:202-205.
68. Shibasaki, F., E. R. Price, D. Milan, and F. McKeon. 1996. Role of kinases and phosphatase calcineurin in the nuclear shuttling of transcription factor NFAT4. Nature 382:370-373.
69. Siegel, M. D., D. H. Zhang, P. Ray, and A. Ray. 1995. Activation of the interleukin-5 promoter by cAMP in murine EL-4 cells requires the GATA-3 and CLE0 elements. J. Biol. Chem. 270:24548-24555.
70. Szabo, S. J., J. S. Gold, T. L. Murphy, and K. M. Murphy. 1993. Identification of cis-acting regulatory elements controlling interleukin-4 gene expression in T cells: roles for NF-Y and NF-ATc. Mol. Cell. Biol. 13:4793-4805.
71. Thorson, J. A., L. W. Yu, A. L. Hsu, N. Y. Shih, P. R. Graves, J. W. Tanner, P. M. Allen, H. Piwnica-Worms, and A. S. Shaw. 1998. 14-3-3 proteins are required for maintenance of Raf-1 phosphorylation and kinase activity. Mol. Cell. Biol. 18:5229-5238.
72. Timmerman, L. A., N. A. Clipstone, S. N. Ho, J. P. Northrop, and G. R. Crabtree. 1996. Rapid shuttling of NF-AT in discrimination of Ca2+ signals and immunosuppression. Nature 383:837-840.
73. Tsuruta, L., H. J. Lee, E. S. Masuda, N. Koyano-Nakagawa, N. Arai, K. Arai, and T. Yokota. 1995. Cyclic AMP inhibits expression of the IL-2 gene through the nuclear factor of activated T cells (NF-AT) site, and transfection of NF-AT cDNAs abrogates the sensitivity of EL-4 cells to cyclic AMP. J. Immunol. 154:5255-5264.
74. Tzivion, G., Z. Luo, and J. Avruch. 1998. A dimeric 14-3-3 protein is an essential cofactor for Raf kinase activity. Nature 394:88-92.
75. Uotila, P. 1996. The role of cyclic AMP and oxygen intermediates in the inhibition of cellular immunity in cancer. Cancer Immunol. Immunother. 43:1-9.
76. Wartmann, M., and R. Davis. 1994. The native structure of the activated Raf protein kinase is a membrane-bound multi-subunit complex. J. Biol. Chem. 269:6695-6701.
77. Xanthoudakis, S., J. P. Viola, K. T. Shaw, C. Luo, J. D. Wallace, P. T. Bozza, D. C. Luk, T. Curran, and A. Rao. 1996. An enhanced immune response in mice lacking the transcription factor NFAT1. Science 272:892-895.
78. Xiao, B., S. J. Smerdon, D. H. Jones, G. G. Dodson, Y. Soneji, A. Aitken, and S. J. Gamblin. 1995. Structure of a 14-3-3 protein and implications for coordination of multiple signalling pathways. Nature 376:188-191.
79. Yaffe, M. B., K. Rittinger, S. Volinia, P. R. Caron, A. Aitken, H. Leffers, S. J. Gamblin, S. J. Smerdon, and L. C. Cantley. 1997. The structural basis for 14-3-3:phosphopeptide binding specificity. Cell 91:961-971.
80. Zha, J., H. Harada, E. Yang, J. Jockel, and S. J. Korsmeyer. 1996. Serine phosphorylation of death agonist BAD in response to survival factor results in binding to 14-3-3 not BCL-X(L). Cell 87:619-628.
81. Zhang, S. H., R. Kobayashi, P. R. Graves, H. Piwnica-Worms, and N. K. Tonks. 1997. Serine phosphorylation-dependent association of the band 4.1-related protein-tyrosine phosphatase PTPH1 with 14-3-3beta protein. J. Biol. Chem. 272:27281-27287.
82. Zhu, J., and F. McKeon. 1999. NF-AT activation requires suppression of Crm1-dependent export by calcineurin. Nature 398:256-260.
83. Zhu, J., F. Shibasaki, R. Price, J. C. Guillemot, T. Yano, V. Dotsch, G. Wagner, P. Ferrara, and F. McKeon. 1998. Intramolecular masking of nuclear import signal on NF-AT4 by casein kinase 1 and MEKK1. Cell 93:851-861.