The leucine zipper domain controls the orientation of AP-1 in the NFAT·AP-1·DNA complex

Chemistry and Biology

Volumn 3, Issue 12, 1996, Pages 981-991

  Erlanson, Daniel A ^a   Chytil, Milan ^a   Verdine, Gregory L ^a  

^a HARVARD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 0030482408     PISSN: 10745521     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1074-5521(96)90165-9     Document Type: Article

References (94)

1. Tjian, R. & Maniatis, T. (1994). Transcriptional activation: a complex puzzle with few easy pieces. Cell 77, 5-8.
2. Sauer, F., Hansen, S.K. & Tjian, R. (1996). DNA template and activator-coactivator requirements for transcriptional synergism by Drosophila bicoid. Science 270, 1825-1828.
3. Sauer, F., Hansen, S.K. & Tjian, R. (1995). Multiple TAFIIs directing synergistic activation of transcription. Science 270, 1783-1788.
4. Xu, H.E., Kodadek, T. & Johnston, S.A. (1995). A single GAL4 dimer can maximally activate transcription under physiological conditions. Proc. Natl. Acad. Sci. USA 92, 7677-7680.
5. Miner, J.N. & Yamamoto, K.R. (1991). Regulatory crosstalk at composite response elements. Trends Biochem. Sci. 16, 423-426.
6. Diamond, M.I., Miner, J.N., Yoshinaga, S.K. & Yamamoto, K.R. (1990). Transcription factor interactions: selectors of positive or negative regulation from a single DNA element. Science 249, 1266-1272.
7. Wasylyk, B., Wasylyk, C., Flores, P., Begue, A., Leprince, D. & Stehelin, D. (1990). The c-ets proto-oncogenes encode transcription factors that cooperate with c-Fos and c-Jun for transcriptional activation. Nature 346, 191-193.
8. Du, W., Thanos, D. & Maniatis, T. (1993). Mechanisms of transcriptional synergism between distinct virus-inducible enhancer elements. Cell 74, 887-898.
9. Hill, C.S. & Treisman, R. (1995). Differential activation of c-Fos promoter elements by serum, lysophosphatidic acid, G proteins and polypeptide growth factors. EMBO J. 14, 5037-5047.
10. Stein, B., Cogswell, P. & Baldwin, A.S., Jr. (1993). Functional and physical associations between NF-κB and C/EBP family members: a Rel domain-bZIP interaction. Mol. Cell. Biol. 13, 3964-3974.
11. Wang, C.-Y., Bassuk, A.G., Boise, L.H., Thompson, C.B., Bravo, R. & Leiden, J.M. (1994). Activation of the granulocyte-macrophage colony-stimulating factor promoter in T cells requires cooperative binding of Elf-1 and AP-1 transcription factors. Mol. Cell. Biol. 14, 1153-1159.
12. Jain, J., McCaffrey, P.G., Valge-Archer, V.E. & Rao, A. (1992). Nuclear factor of activated T cells contains Fos and Jun. Nature 356, 801-804.
13. Jain, J., Miner, Z. & Rao, A. (1993). Analysis of the preexisting and nuclear forms of nuclear factor of activated T cells. J. Immunol. 151, 837-848.
14. Chen, L., et al., & Verdine, G.L (1995). Only one of the two DNA-bound orientations of AP-1 found in solution cooperates with NFATp. Curr. Biol. 5, 882-889.
15. Shaw, J.-P., Utz, P.J., Durand, D.B., Toole, J.J., Emmel, E.A. & Crabtree, G.R. (1988). Identification of a putative regulator of early T cell activation genes. Science 241, 202-205.
16. Rao, A. (1994). NFATp: a transcription factor required for the coordinate induction of several cytokine genes. Immunol. Today 15, 274-281.
17. Lee, W., Haslinger, A., Karin, M. & Tjian, R. (1987). Activation of transcription by two factors that bind promoter and enhancer sequences of the human metallothionein gene and SV40. Nature 325, 368-372.
18. Curran, T. & Franza, J. (1988). Fos and Jun: the AP-1 connection. Cell 55, 395-397.
19. Durand, D.B., Shaw, J.-P., Bush, M.R., Replogle, R.E., Belagaje, R. & Crabtree, G.R. (1988). Characterization of antigen receptor response elements within the interleukin-2 enhancer. Mol. Cell. Biol. 8, 1715-1724.
20. Crabtree, G.R. & Clipstone, N.A. (1994). Signal transmission between the plasma membrane and the nucleus of T lymphocytes. Annu. Rev. Biochem. 63, 1045-1083.
21. McCaffrey, P.G., et al., & Hogan, P.G. (1993). Isolation of the cyclosporin-sensitive T cell transcription factor NFATp. Science 262, 750-754.
22. Northrop, J.P., et al., & Crabtree, G.R. (1994). NFAT components define a family of transcription factors targeted in T cell activation. Nature 369, 497-502.
23. Ho, S.N., Thomas, D.J., Timmerman, L.A., Li, X., Francke, U. & Crabtree, G.R. (1995). NFATc3, a lymphoid-specific NFATc family member that is calcium-regulated and exhibits distinct DNA binding specificity. J. Biol. Chem. 270, 19898-19907.
24. Masuda, E.S., et al., & Arai, N. (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.
25. Hoey, T., Sun, Y.-L., Williamson, K. & Xu, X. (1995). Isolation of two new members of the NF-AT gene family and functional characterization of the NF-AT proteins. Immunity 2, 461-472.
26. Wolfe, S.A., et al., & Verdine, G.L. An unusual Rel-like architecture in the DNA-binding domain of NFATc. Nature, in press.
27. Flanagan, W.M., Corthésy, B., Bram, R.J. & Crabtree, G.R. (1991). Nuclear association of a T-cell transcription factor blocked by FK-506 and cyclosporin A. Nature 352, 803-807.
28. Shibasaki, F., Price, E.R., Milan, D. & McKeon, F. (1996). Role of kinases and the phosphatase calcineurin in the nuclear shuttling of transcription factor NF-AT4. Nature 382, 370-373.
29. Luo, C., et al., & Rao, A. (1996). Interaction of calcineurin with a domain of the transcription factor NFAT1 that controls nuclear import. Proc. Natl. Acad. Sci. USA 93, 8907-8912.
30. Liu, J., Farmer, J.D., Jr., Lane, W.S., Friedman, J., Weissman, I. & Schreiber, S.L. (1991). Calcineurin is a common target of cyclophilin-cyclosporin A and FKBP-FK506 complexes. Cell 66, 1-9.
31. Karin, M. (1995). The regulation of AP-1 activity by mitogen-activated protein kinases. J. Biol. Chem. 270, 16483-16486.
32. Landschulz, W.H., Johnson, P.F. & McKnight, S.L. (1988). The leucine zipper: a hypothetical structure common to a new class of DNA-binding proteins. Science 240, 1759-1764.
33. Sassone-Corsi, P., Ransone, L.J., Lamph, W.W. & Verma, I.M. (1988). Direct interaction between fos and jun nuclear oncoproteins: role of the 'leucine zipper' domain. Nature 336, 692-695.
34. Kouzarides, T. & Ziff, E. (1988). The role of the leucine zipper in the Fos-Jun interaction. Nature 336, 646-651.
35. Nakabeppu, Y. & Nathans, D. (1989). The basic region of Fos mediates specific DNA binding. EMBO J. 8, 3833-3841.
36. Angel, P. & Karin, M. (1991). The role of Jun, Fos and the AP-1 complex in cell proliferation and transformation. Biochim. Biophys. Acta 1072, 129-157.
37. Glover, J.N.M. & Harrison, S.C. (1994). The crystal structure of the heterodimeric bZip transcription factor c-Fos:c-Jun bound to DNA. Nature 373, 257-261.
38. Hurst, H.C. (1994). Transcription factors 1: bZip proteins. Protein Profile 1, 123-168.
39. Boise, L.H., et al., & Thompson, C.B. (1993). The NFAT-1 DNA binding complex in activated T cells contains Fra-1 and JunB. Mol. Cell. Biol. 13, 1911-1919.
40. McCaffrey, P.G., Jain, J., Jamieson, C., Sen, R. & Rao, A. (1992). A T cell nuclear factor resembling NF-AT binds to an NF-κB site and to the conserved lymphokine promoter sequence 'Cytokine-1'. J. Biol. Chem. 267, 1864-1871.
41. Peterson, B.R., Sun, L.J. & Verdine, G.L. (1996). A critical arginine residue mediates cooperativity in the contact interface between NFAT and AP-1. Proc. Natl. Acad. Sci. USA 93, 13671-13676.
42. Suckow, M., Von Wilcken-Bergmann, B. & Müller-Hill, B. (1993). The DNA binding specificity of the basic region of the yeast transcriptional activator GCN4 can be changed by substitution of a single amino acid. Nucl. Acids Res. 21, 2081-2086.
43. Dervan, P.B. (1986). Design of sequence-specific DNA-binding molecules. Science 232, 464-471.
44. 2 with DNA? J. Am. Chem. Soc. 117, 6428-6433.
45. Sluka, J.P., Horvath, S.J., Glasgow, A.C., Simon, M.I. & Dervan, P.B. (1990). Importance of minor-groove contacts for recognition of DNA by the binding domain of Hin recombinase. Biochemistry 29, 6551-6561.
46. Oakley, M.G. & Dervan, P.B. (1990). Structural motif of the GCN4 DNA binding domain characterized by affinity cleaving. Science 248, 847-850.
47. Oakley, M.G., Mrksich, M. & Dervan, P.B. (1992). Evidence that a minor groove-binding peptide and a major groove-binding protein can simultaneously occupy the same site. Biochemistry 31, 10969-10975.
48. Mack, D.P., Sluka, J.P., Shin, J.A., Griffin, J.H., Simon, M.I. & Dervan, P.B. (1990). Orientation of the putative recognition helix in the DNA-binding domain of Hin recombinase complexed with the Hix site. Biochemistry 29, 6561-6567.
49. Ebright, Y.W., Chen, Y., Pendergrast, P.S. & Ebright, R.H. (1992). Incorporation of an EDTA-metal complex at a rationally selected site within a protein: application to EDTA-iron DNA affinity cleaving with catabolite gene activator protein (CAP) and Cro. Biochemistry 31, 10664-10670.
50. Dumoulin, P., Ebright, R.H., Knegtel, R., Kaptein, R., Granger-Schnarr, M. & Schnarr, M. (1996). Structure of the LexA repressor-DNA complex probed by affinity cleavage and affinity photo-cross-linking. Biochemistry 35, 4279-4286.
51. Heilek, G.M., Marusak, R., Meares, C.F. & Noller, H.F. (1995). Directed hydroxyl radical probing of 16S rRNA using Fe(II) tethered to ribosomal protein S4. Proc. Natl. Acad. Sci. USA 92, 1113-1116.
52. Ghaim, J.B., Greiner, D.P., Meares, C.F. & Gennis, R.B. (1995). Proximity mapping the surface of a membrane protein using an artificial protease: demonstration that the quinone-binding domain of subunit I is near the amino-terminal region of subunit II of cytochrome bd. Biochemistry 34, 11311-11315.
53. Rana, T.M. & Meares, C.F. (1991). Iron chelate mediated proteolysis: protein structure dependence. J. Am. Chem. Soc. 113, 1859-1861.
54. Ermácora, M.R., Ledman, D.W. & Fox, R.O. (1996). Mapping the structure of a non-native state of staphylococcal nuclease. Nat. Struct. Biol. 3, 59-66.
55. Schepartz, A. & Cuenoud, B. (1990). Site-specific cleavage of the protein calmodulin using a trifluoperazine-based affinity reagent. J. Am. Chem. Soc. 112, 3247-3249.
56. Hoyer, D., Cho, H. & Schultz, P.G. (1990). A new strategy for selective protein cleavage. J. Am. Chem. Soc. 112, 3249-3250.
57. Dreyer, G.B. & Dervan, P.B. (1985). Sequence-specific cleavage of single-stranded DNA: oligodeoxynucleotide-EDTA·Fe(II). Proc. Natl. Acad. Sci. USA 82, 968-972.
58. Moser, H.E. & Dervan, P.B. (1987). Sequence-specific cleavage of double helical DNA by triple helix formation. Science 238, 645-650.
59. Rana, T.M. & Meares, C.F. (1990). Specific cleavage of a protein by an attached iron chelate. J. Am. Chem. Soc. 112, 2457-2458.
60. Haywood, M.M., Adrian, J.C., Jr. & Schepartz, A. (1995). Convenient syntheses of bifunctional metal chelates. J. Org. Chem. 60, 3924-3927.
61. Ermácora, M.R., Delfino, J.M., Cuenoud, B., Schepartz, A. & Fox, R.O. (1992). Conformation-dependent cleavage of staphylococcal nuclease with a disulfide-linked iron chelate. Proc. Natl. Acad. Sci. USA 89, 6383-6387.
62. Dawson, P.E., Muir, T.W., Clark-Lewis, I. & Kent, S.B.H. (1994). Synthesis of proteins by native chemical ligation. Science 266, 776-779.
63. Lu, W., Qasim, M.A. & Kent, S.B.H. (1996). Comparative total synthesis of turkey ovomucoid third domain by stepwise solid phase peptide synthesis and native chemical ligation. J. Am. Chem. Soc. 118, 8518-8523.
64. Friedman, M., Krull, L.H. & Cavins, J.F. (1970). The Chromatographic determination of cystine and cysteine residues in proteins as S-β-(4-pyridylethyl)cysteine. J. Biol. Chem. 245, 3868-3871.
65. Hirel, P.-H., Schmitter, J.-M., Dessen, P., Fayat, G. & Blanquet, S. (1989). Extent of amino-terminal methionine excision from Escherichia coli proteins is governed by the sidechain length of the penultimate amino acid. Proc. Natl. Acad. Sci. USA 86, 8247-8251.
66. Nagai, K. & Thøgersen, H.C. (1984). Generation of β-globin by sequence-specific proteolysis of a hybrid protein produced in Escherichia coli. Nature 309, 810-812.
67. Hochuli, E., Bannwarth, W., Döbeli, H., Gentz, R. & Stüber, D. (1988). Genetic approach to facilitate purification of recombinant proteins with a novel metal chelate absorbent. Biotechnology 6, 1321-1325.
68. Shiraishi, H., Kataoka, M., Morita, Y. & Umemoto, J. (1993). Interactions of hydroxyl radicals with tris(hydroxymethyl)aminomethane and Good's buffers containing hydroxymethyl or hydroxyethyl residues produce formaldehyde. Free Rad. Res. Commun. 19, 315-321.
69. Kemp, D.S. & Carey, R.I. (1993). Synthesis of a 39-peptide and a 25-peptide by thiol capture ligations: observation of a 40-fold rate acceleration of the intramolecular O,N-acyl-transfer reaction between peptide fragments bearing only cysteine protective groups. J. Org. Chem. 58, 2216.
70. Canne, L.E., Bark, S.J. & Kent, S.B.H. (1996). Extending the applicability of native chemical ligation. J. Am. Chem. Soc. 118, 5891-5896.
71. Lee, D.H., Granja, J.R., Martinez, J.A., Severin, K. & Ghadiri, M.R. (1996). A self-replicating peptide. Nature 382, 525-528.
72. Abate, C., Patel, L., Rauscher, F.J., III, & Curran, T. (1990). Redox regulation of Fos and Jun DNA-binding activity in vitro. Science 249, 1157-1161.
73. Geoghegan, K.F. & Stroh, J.G. (1992). Site-directed conjugation of nonpeptide groups to peptides and proteins via periodate oxidation of a 2-amino alcohol. Application to modification at N-terminal serine. Bioconj. Chem. 3, 138-146.
74. Ellenberger, T.E., Brandi, C.J., Struhl, K. & Harrison, S.C. (1992). The GCN4 basic region leucine zipper binds DNA as a dimer of uninterrupted α helices: crystal structure of the protein-DNA complex. Cell 71, 1223-1237.
75. König, P. & Richmond, T.J. (1993). The X-ray structure of the GCN4-bZIP bound to ATF/CREB site DNA shows the complex depends on DNA flexibility. J. Mol. Biol. 233, 139-154.
76. Ho, I.C., Hodge, M.R., Rooney, J.W. & Glimcher, L.H. (1996). The proto-oncogene c-maf is responsible for tissue-specific expression of interleukin-4. Cell 85, 973-983.
77. LeClair, K.P., Blanar, M.A. & Sharp, P.A. (1992). The p50 subunit of NF-κB associates with the NF-IL6 transcription factor. Proc. Natl. Acad. Sci. USA 89, 8145-8149.
78. Gong, Q., Huang, Z. & Wicks, W.D. (1995). Interaction of retinoblastoma gene product with transcription factors ATFa and ATF2. Arch. Biochem. Biophys. 319, 445-450.
79. Kaszubska, W., et al., & Whelan, J. (1993). Cyclic AMP-independent ATF family members interact with NF-κB and function in the activation of the E-selectin promoter in response to cytokines. Mol. Cell. Biol. 13, 7180-7190.
80. Ferré-D'Amaré, A., Prendergast, G., Ziff, E. & Burley, S. (1993). Recognition by Max of its cognate DNA through a dimeric b/HLH/Z domain. Nature 363, 38-45.
81. Ma, P.C.M., Rould, M.A., Weintraub, H. & Pabo, C.O. (1994). Crystal structure of MyoD bHLH domain-DNA complex: perspectives on DNA recognition and implications for transcriptional activation. Cell 77, 451-459.
82. Ellenberger, T.E., Fass, D., Arnaud, M. & Harrison, S.C. (1994). Crystal structure of transcription factor E47: E-box recognition by a basic region helix-loop-helix dimer. Genes Dev. 8, 970-980.
83. Pavletich, N.P. & Pabo, C.O. (1991). Zinc finger-DNA recognition: crystal structure of a Zif268-DNA complex at 2.1 Å. Science 252, 809-817.
84. Kaptein, R. (1992). Zinc-finger structures. Curr. Opin. Struct. Biol. 2, 109-115.
85. Luisi, B.F., Xu, W.X., Otwinowski, Z., Freedman, L.P., Yamamoto, K.R. & Sigler, P.B. (1991). Crystallographic analysis of the interaction of the glucocorticoid receptor with DMA. Nature 352, 497-505.
86. Schwabe, J.W.R., Chapman, L., Finch, J.T. & Rhodes, D. (1993). The crystal structure of the estrogen receptor DNA-binding domain bound to DNA: how receptors discriminate between their response elements. Cell 75, 567-578.
87. Wolberger, C., Vershon, A.K., Liu, B., Johnson, A.D. & Pabo, C.O. (1991). Crystal structure of a Matα2 homeodomain-operator complex suggests a general model for homeodomain-DNA interactions. Cell 67, 517-528.
88. Kissinger, C.R., Liu, B., Martin-Blanco, E., Kornberg, T.B. & Pabo, C.O. (1990). Crystal structure of an engrailed homeodomain-DNA complex at 2.8 Å resolution: a framework for understanding homeodomain-DNA interactions. Cell 63, 579-590.
89. Klemm, J.D., Rould, M.A., Aurora, R., Herr, W. & Pabo, C.O. (1994). Crystal structure of the Oct-1 POU domain bound to an octamer site: DNA recognition with tethered DNA-binding modules. Cell 77, 21-32.
90. Jordan, S.R. & Pabo, C.O. (1988). Structure of the lambda complex at 2.5 Å resolution: details of the repressor-operator interactions. Science 242, 893-899.
91. Aggarwal, A.K., Rodgers, D.W., Drottar, M., Ptashne, M. & Harrison, S.C. (1988). Recognition of a DNA operator by the repressor of phage 434: a view at high resolution. Science 242, 899-907.
92. Mondragón, A., Wolberger, C. & Harrison, S.C. (1989). Structure of phage 434 Cro protein at 2.35 Å resolution. J. Mol. Biol. 205, 179-188.
93. Sarkar, G. & Sommer, S.S. (1990). The 'megaprimer' method of site-directed mutagenesis. BioTechniques 8, 404-407.
94. Sodeoka, M., Larson, C.J., Chen, L., LeClair, K.P. & Verdine, G.L. (1993). A multifunctional plasmid for protein expression by ECPCR: overproduction of the p50 subunit of NF-κB. BioMed. Chem. Lett. 3, 1089-1094.