Recognition of NFATp/AP-1 composite elements within genes induced upon the activation of immune cells

Journal of Molecular Biology

Volumn 288, Issue 3, 1999, Pages 353-376

  Kel, Alexander ^a,b   Kel Margoulis, Olga ^a   Babenko, Vladimir ^a   Wingender, Edgar ^b  

^a INSTITUTE OF CYTOLOGY AND GENETICS   (Russian Federation)

^b HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

Author keywords

Composite elements; Computer assisted prediction; Immune response; NFATp AP 1

Indexed keywords

CALCIUM BINDING PROTEIN; CYTOKINE; CYTOKINE RECEPTOR; NUCLEAR FACTOR; TRANSCRIPTION FACTOR AP 1;

ARTICLE; CLUSTER ANALYSIS; GENE TARGETING; IMMUNOSTIMULATION; INTERNET; INTRON; PRIORITY JOURNAL; PROMOTER REGION; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TRANSCRIPTION INITIATION;

EID: 0033532171     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1999.2684     Document Type: Article

References (112)

1. Albanese C., Johnson J., Watanabe G., Eklund N., Vu D., Arnold A., Pestell R. G. Transforming p21ras mutants and c-Ets-2 activate the cyclin D1 promoter through distinguishable regions. J. Biol. Chem. 270:1995;23589-23597.
2. Arai K. I., Lee F., Miyajima A., Miyatake S., Arai N., Yokota T. Cytokines: coordinators of immune and inflammatory responses. Annu. Rev. Biochem. 59:1990;783-836.
3. Aramburu J., Azzoni L., Rao A., Perussia B. Activation and expression of the nuclear factors of activated T cells, NFATp and NFATc, in human natural killer cells: regulation upon CD16 ligand binding. J. Exp. Med. 182:1995;801-810.
4. Berg O. G., von Hippel P. H. Selection of DNA binding sites by regulatory proteins. Statistical-mechanical theory and aplication to operators and promoters. J. Mol. Biol. 193:1987;723-750.
5. Berg O. G., von Hippel P. H. Selection of DNA binding sites by regulatory proteins. II. The binding specificity of cyclic AMP receptor protein to recognition sites. J. Mol. Biol. 200:1988;709-723.
6. Boise L. H., Petryniak B., Mao X., June C. H., Wang C.-Y., Lindstein T., Bravo R., Kovary K., Leiden J. M., Thompson C. B. The NFAT-1 binding complex in activated T cells contains Fra-1 and JunB. Mol. Cell. Biol. 13:1993;1911-1919.
7. Brabletz T., Pietrowski I., Serfling E. The immunosuppressives FK 506 and cyclosporin A inhibit the generation of protein factors binding to the two purine boxes of the interleukin 2 enhancer. Nucl. Acids Res. 19:1991;61-67.
8. Brazma A., Vilo J., Ukkonen E. Finding transcription factor binding site combinations in the yeast genome. Mewes H. W., Frishman D. Proceedings of the German Conference on Bioinformatics GCB'97. 1997;57-60.
9. Bucher P. Weight matrix descriptions of four eukaryotic RNA polymerase II promoter elements derived from 502 unrelated promoter sequences. J. Mol. Biol. 212:1990;563-578.
10. Campbell P. M., Pimm J., Ramassar V., Halloran P. F. Identification of a calcium-inducible, cyclosporine sensitive element in the IFN-gamma promoter that is a potential NFAT binding site. Transplantation. 61:1996;933-939.
11. Casolaro V., Georas S. N., Song Z., Zubkoff I. D., Abdulkadir S. A., Thanos D., Ono S. J. Inhibition of NF-AT-dependent transcription by NF-kappa B: implications for differential gene expression in T helper cell subsets. Proc. Natl Acad. Sci., USA. 92:1995;11623-11627.
12. Chen L., Glover J. N., Hogan P. G., Rao A., Harrison S. C. Structure of the DNA-binding domains from NFAT, Fos and Jun bound specifically to DNA. Nature. 392:1998;42-48.
13. Chen Q. K., Hertz G. Z., Stormo G. D. MATRIX SEARCH 1.0: a computer program that scans DNA sequences for transcriptional elements using a database of weight matrices. Comput. Appl. Biosci. 11:1995;563-566.
14. Chin E., Olson E., Richardson J., Yang Q., Humphries C., Shelton J., Wu H., Zhu W., Bassel-Duby R., Williams S. A calcineurin-dependent transcriptional pathway controls skeletal muscle fiber type. Genes Dev. 12:1998;2499-2509.
15. Chuvpilo S., Schomberg C., Gerwig R., Heinfling A., Reeves R., Grummt F., Serfling E. Multiple closely-linked NFAT/octamer and HMG I(Y) binding sites are part of the interleukin-4 promoter. Nucl. Acids Res. 21:1993;5694-5704.
16. Cockerill P. N., Bert A. G., Jenkins F., Ryan G. R., Shannon M. F., Vadas M. A. Human granulocyte-macrophage colony-stimulating factor enhancer function is associated with cooperative interactions between AP-1 and NFATp/c. Mol. Cell. Biol. 15:1995;2071-2079.
17. Dalton S., Treisman R. Characterization of SAP-1, a protein recruited by serum response factor to the c-fos serum response element. Cell. 68:1992;597-612.
18. de la Pompa J. L., Timmerman L. A., Takimoto H., Yoshida H., Elia A. J., Samper E., Potter J., Wakeham A., Marengere L., Langille B. L., Crabtree G. R., Mak T. W. Role of the NF-ATc transcription factor in morphogenesis of cardiac valves and septum. Nature. 392:1998;182-186.
19. Dolganov G., Bort S., Lovett M., Burr J., Schubert L., Short D., McGurn M., Gibson C., Lewis D. B. Coexpression of the interleukin-13 and interleukin-4 genes correlates with their physical linkage in the cytokine gene cluster on human chromosome 5q23-31. Blood. 87:1996;3316-3326.
20. Duda R., Hart P. E. Pattern Classification and Scene Analysis. 1973;John Wiley & Sons. New York.
21. Duncliffe K. N., Bert A. G., Vadas M. A., Cockerill P. N. A T cell-specific enhancer in the interleukin-3 locus is activated cooperatively by Oct and NFAT elements within a DNase I-hypersensitive site. Immunity. 6:1997;175-185.
22. Duret L., Bucher P. H. Searching for regulatory elements in human noncoding sequences. Curr. Opin. Struct. Biol. 7:1997;399-406.
23. Fickett J. W. Quantative descrimination of MEF-2 sites. Mol. Cell. Biol. 16:1996;437-441.
24. Fickett J. W., Hatzigeorgiou A. G. Eukaryotic promoter recognition. Genome Res. 7:1997;861-878.
25. Fisch T. M., Prywes R., Simon M. C., Roeder R. G. Multiple sequence elements in the c-fos promoter mediate induction by cAMP. Genes Dev. 3:1989;198-211.
26. Fishburn. Utility Theory for Decision Making. 1970;Wiley, New York.
27. Flanagan W. M., Corthesy B., Bram R. J., Crabtree G. R. Nuclear association of a T-cell transcription factor blocked by FK-506 and cyclosporin A. Nature. 352:1991;803-807.
28. Frech K., Herrmann G., Werner T. Computer-assisted prediction, classification, and delimitation of protein binding sites in nucleic acids. Nucl. Acids Res. 21:1993;3117-3118.
29. Frech K., Quandt K., Werner T. Software for the analysis of DNA sequence elements of transcription. Comput. Appl. Biosci. 13:1997;89-97.
30. Granelli-Piperno A., McHugh P. Characterisation of a protein that regulates the DNA-binding activity of NF-AT, the nuclear factor of activated T cells. Proc. Natl Acad. Sci. USA. 88:1991;11431-11434.
31. Gumucio D. L., Shelton D. A., Zhu W., Millinoff D., Gray T., Bock J. H., Slightom J. L., Goodman M. Evolutionary strategies for the elucidation of cis and trans factors that regulate the developmental switching programs of the β-like globin genes. Mol. Phylogenet. Evol. 5:1996;18-32.
32. Heinemeyer T., Wingender E., Reuter I., Hermjakob H., Kel A. E., Kel O. V., Ignatieva E. V., Ananko E. A., Podkolodnaya O. A., Kolpakov F. A., Podkolodny N. L., Kolchanov N. A. Databases on transcriptional regulation: TRANSFAC, TRRD and COMPEL. Nucl. Acids Res. 26:1998;362-367.
33. Heinemeyer T., Chen X., Karas H., Kel A. E., Kel O. V., Liebich I., Meinhardt T., Reuter I., Schacherer F., Wingender E. Expanding the TRANSFAC database towards an expert system of regulatory molecular mechanisms. Nucl. Acids Res. 27:1999;318-322.
34. Ho I.-C., Hodge M. R., Rooney J. W., Glimcher L. H. The proto-oncogene c-maf is responsible for tissue-specific expression of interleukin-4. Cell. 85:1996;973-983.
35. Huang D., Shipman-Appasamy P. M., Orten D. J., Hinrichs S. H., Prystowsky M. B. Promoter activity of the proliferating-cell nuclear antigen gene is associated with inducible CRE-binding proteins in interleukin 2-stimulated T lymphocytes. Mol. Cell. Biol. 14:1994;4233-4243.
36. Ivanov V. N., Lee R. K., Podack E. R., Malek T. R. Regulation of Fas-dependent activation-induced T cell apoptosis by cAMP signaling: a potential role for transcription factor NF-kappa B. Oncogene. 14:1997;2455-2464.
37. Jain J., Miner Z., Rao A. Analysis of the preexisting and nuclear forms of nuclear factor of activated T cells. J. Immunol. 151:1993a;837-848.
38. Jain J., McCaffrey P. G., Miner Z., Kerppola T. K., Lambert J. N., Verdine G. L., Curran T., Rao A. The T-cell transcription factor NFATp is a substrate for calcineurin and interacts with Fos and Jun. Nature. 365:1993b;352-355.
39. Jain J., Burgeon E., Badalian T. M., Hogan P. G., Rao A. A similar DNA-binding motif in NFAT family proteins and the Rel homology region. J. Biol. Chem. 270:1995;4138-4145.
40. Janknecht R., Nordheim A. Elk-1 protein domains required for direct and SRF-assisted DNA-binding. Nucl. Acids Res. 20:1992;3317-3324.
41. Jarmin D. I., Kulmburg P. A., Huber N. E., Baumann G., Prieschl-Strassmayr E. E., Baumruker T. A transcription factor with AP3-like binding specificity mediates gene regulation after an allergic triggering with IgE and Ag in mouse mast cells. J. Immunol. 153:1994;5720-5729.
42. Jenkins F., Cockerill P. N., Bohnmann D., Shannon M. F. Multiple signals are required for function of the human granulocyte-macrophage colony-stimulating factor gene promoter in T cell. J. Immunol. 155:1995;1240-1251.
43. Karlin S., Macken C. Assessment of inhomogeneities in an E. coli physical map. Nucl. Acids Res. 19:1991;4241-4246.
44. Kel A. E., Ponomarenko M. P., Likhachev E. A., Orlov Yu. L., Ischenko I. V., Milanesi L., Kolchanov N. A. SITEVIDEO: a computer system for functional site analysis and recognition. Investigation of the human splice sites. Comput. Appl. Biosci. 9:1993a;617-627.
45. Kel A. E., Kolchanov N. A., Kapitonov V. V., Ponomarenko M. P., Likhachev E. A., Lim H. A., Milanesi L. Computer analysis and recognition of functional sites on the base of oligonucleotide patterns distributions. Cantor C. R., Lim H. A. Proceedings of the Second International Conference on on Bioinformatic, Supercomputing and Complex Genome Analysis. 1993b;521-543 World Scientific.
46. Kel A. E., Kondrakhin Y. V., Kolpakov P. A., Kel O. V., Romashenko A. G., Wingender E., Milanesi L., Kolchanov N. A. Computer tool FUNSITE for analysis of eukaryotic regulatory genomic sequences. Proceedings of the Third International Conference on Intelligent Systems for Molecular Biology. 1995;AAAIPress, California. p. 197-205.
47. Kel O. V., Kel A. E. Complex gene network in cell cycle regulation: central role of the E2F family of transcription factors. Mol. Biol. 31:1997;548-561.
48. Kel O. V., Romaschenko A. G., Kel A. E., Wingender E., Kolchanov N. A. A compilation of composite regulatory elements affecting gene transcription in vertebrates. Nucl. Acids Res. 23:1995;4097-4103.
49. Klein-Hessing S., Schneider G., Heinfling A., Chuvpilo S., Sofling E. HMG I(V) interferes with the DNA binding of NF-AT factors and the induction of interleukin 4 promoter in T cells. Proc. Natl Acad. Sci. USA. 93:1996;15311-15316.
50. Kolchanov N. A., Kel A. E. Deletions and duplications as factors of prokaryotic genome evolution. Computer Analysis of Genetic Macromolecules. Structure, Function and Evolution. 1993;World Scientific. p. 317-335.
51. Kolpakov F. A., Kel A. E., Ponomarenko M. P., Kolchanov N. A. High heterogeneity of higher eukaryotic gene promoters, transcribed by RNA polymerase II. Dokl Akad Nauk. 57:1997;693-695.
52. Kondrakhin Y. V., Kel . A. E., Kolchanov N. A., Romashchenko A. G., Milanesi L. Eukaryotic promoter recognition by binding sites for transcription factors. Comput. Appl. Biosci. 11:1995;477-488.
53. Ku D. H., Wen S. C., Engelhard A., Nicolaides N. C., Lipson K. E., Marino T. A., Calabretta B. c-myb transactivates cdc2 expression via Myb binding sites in the 5′-flanking region of the human cdc2 gene. J. Biol. Chem. 268:1993;2255-2259.
54. Latinis K. M., Carr L. L., Peterson E. J., Norian L. A., Eliason S. L., Koretzky G. A. Regulation of CD95 (Fas) ligand expression by TCR-mediated signaling vents. J. Immunol. 158:1997a;4602-4611.
55. Latinis K. M., Norian L. A., Eliason S. L., Koretzky G. A. Two NFAT transcription factor binding sites participate in the regulation of CD95 (Fas) ligand expression in activated human T cells. J. Biol. Chem. 272:1997b;31427-31434.
56. Lee H. J., Masuda E. S., Arai N., Arai K.-i., Yokota T. Definition of cis -regulatory elements of the mouse interleukin-5 gene promoter. J. Biol. Chem. 270:1995;17541-17550.
57. Linette G. P., Li Y., Roth K., Korsmeyer S. J. Cross talk between cell death and cell cycle progression: BCL-2 regulates NFAT-mediated activation. Proc. Natl Acad. Sci. USA. 93:1996;9545-9552.
58. Li-Weber M., Davydov I. V., Krafft H., Krammer P. H. The role of NF-Y and IRF-2 in the regulation of human IL-4 gene expression. J. Immunol. 153:1994;4122-4133.
59. Maggirwar S. B., Harhaj E. W., Sun S.-C. Regulation of the interleukin-2 CD28-responsive element by NF-Atp and various NF-kB/Rel transcription factors. Mol. Cell. Biol. 17:1997;2605-2614.
60. Marienfeld R., Neumann M., Chuvpilo S., Escher C., Kneitz B., Avots A., Schimpl A., Serfling E. Cyclosporin A interferes with the inducible degradation of NF-kappa B inhibitors, but not with the processing of p105/NF-kappa B1 in T cells. Eur. J. Immunol. 27:1997;1601-1609.
61. Masuda E. S., Tokumitsu H., Tsuboi A., Shlomai J., Hung P., Arai R.-I., Arai N. The granulocyte-macrophage colony-stimulating factor promoter cis -acting element CLE0 mediates induction signals in T cells and is recognized by factors related to AP-1 and NFAT. Mol. Cell. Biol. 13:1993;7399-7401.
62. Masuda E. S., Naito Y., Tokumitsu H., Campbell D., Saito F., Hannum C., Arai K., Arai N. NFATx, a novel member of the nuclear factor of activated T cells family that is expressed predominantly in the thymus. Mol. Cell. Biol. 15:1995;2697-2706.
63. McCaffrey P. G., Luo C., Kerppola T. K., Jain J., Badalian T. M., Ho A. M., Burgeon E., Lane W. S., Lambert J. N., Curran T., Verdine G., Rao A., Hogan P. G. Isolation of the cyclosporin-sensitive T cell transcription factor NFATp. Science. 262:1993;750-754.
64. Milanesi L., Muselli M., Arrigo P. Hamming clustering method for signals prediction in 5′ and 3′ regions of eukaryotic genes. Comput. Appl. Biosci. 12:1996;399-404.
65. Modiano J. F., Domenico G., Szepesi A., Lucas J. J., Gelfand E. W. Differential requirements for il-2 distiquish the expression and activity of the cyclin-dependent kinases Cdk4 and Cdk2 in human T-cells. J. Biol. Chem. 269:1994;32972-32978.
66. Molkentin J., Lu J-R., Antos C., Markham B., Richardson J., Robbins J., Grant S., Olson E. A calcineurin-dependent transcriptional pathway for cardiac hypertrophy. Cell. 93:1998;215-228.
67. Morice W. G., Wiederrecht G., Brunn G. J., Siekierka J. J., Abraham R. T. Paramycin inhibition of IL-2-dependent p33cdk2 kinase activation in T lymphocytes. J. Biol. Chem. 268:1993;22737-22745.
68. Northrop J. P., Ho S. N., Chen L., Thomas D. J., Timmerman L. A., Nolan G. P., Admon A., Crabtree G. R. NF-AT components define a family of transcription factors targeted in T-cell activation. Nature. 369:1994;497-502.
69. Nolan G. P. NF-AT-AP-1 and REL-bZIP: hybrid vigor and binding under the influence. Cell. 77:1994;795-798.
70. Oberg H. H., Lengl-Janssen B., Kabelitz D., Janssen O. Activation-induced T cell death: resistance or susceptibility correlate with cell surface fas ligand expression and T helper phenotype. Cell Immunol. 181:1997;93-100.
71. Perier R. C., Junier T., Bucher Ph. The eukarytoic promoter databas (EPD). Nucl. Acids Res. 26:1998;353-357.
72. Pickert L., Reuter I., Klawonn F., Wingender E. Transcription regulatory region analysis using signal detection and fuzzy clustering. Bioinformatics. 14:1998;244-251.
73. Prestridge D. S. SIGNAL SCAN: a computer program that scans DNA sequences for eukaryotic transcriptional elements. Comput. Appl. Biosci. 7:1991;203-206.
74. Prestridge D. S. Predicting pol II promoter sequences using transcription factor binding sites. J. Mol. Biol. 249:1995;923-932.
75. Prestridge D. S., Stormo G. SIGNAL SCAN 3.0: new database and program features. Comput. Appl. Biosci. 9:1993;113-115.
76. Prieschl E. E., Gouilleux-Gruart V., Walker C., Harrer N. E., Baumruker T. A nuclear factor of activated T-cell-like transcription factor in mast cells is involved in IL-5 gene regulation after IgE plus antigen stimulation. J. Immunol. 154:1995a;6112-6119.
77. Prieschl E. E., Pendl G. G., Harrer N. E., Baumruker T. p21ras links FceRI to NF-AT family member in mast cells. J. Immunol. 155:1995b;4963-4970.
78. Prieschl E. E., Pendl G. G., Elbe A., Serfling E., Harrer N. E., Stingl G., Baumruker T. Induction of the TNF-alpha promoter in the murine dendritic cell line 18 and the murine mast cell line CPII is differently regulated. J. Immunol. 157:1996;2645-2653.
79. Quandt K., Frech K., Karas H., Wingender E., Werner T. MatInd and MatInspector-new fast and versatile tools for detection of consensus matches in nucleotide sequence data. Nucl. Acids Res. 23:1995;4878-4884.
80. Ranger A. M., Grusby M. J., Hodge M. R., Gravallese E. M., de la Brousse F. C., Hoey T., Mickanin C., Baldwin H. S., Glimcher L. H. The transcription factor NF-ATc is essential for cardiac valve formation. Nature. 392:1998;186-190.
81. Rao A., Luo C., Hogan P. G. Transcription factors of the NFAT family: regulation and function. Annu. Rev. Immunol. 15:1997;707-747.
82. Reese M. G., Harris N. L., Eeckman F. H. Large scale sequencing specific neural networks for promoter and splice site recognition. Klein T., Hunter L. Proceedings of the Pacific Symposium on Biocomputing. 1996;World Scientific.
83. Rooney J. W., Hoey T., Glimcher L. H. Coordinate and cooperative roles for NF-AT and AP-1 in the regulation of the murine IL-4 gene. Immunity. 2:1995a;473-483.
84. Rooney J. W., Sun Y.-L., Glimcher L. H., Hoey T. Novel NFAT sites that mediate activation of the interleukin-2 promoter in response to T-cell receptor stimulation. Mol. Cell. Biol. 15:1995b;6299-6310.
85. Schneider T. D., Stormo G. D., Gold L., Ehrenfeucht A. Information content of binding sites on nucleotide sequences. J. Mol. Biol. 188:1986;415-431.
86. Schuh K., Twardzik T., Kneitz B., Heyer J., Schimpl A., Serfling E. The Interleukin 2 receptor alpha chain/CD25 promoter is a target for nuclear factor of activated T cells. J. Exp. Med. 188:1998;1-5.
87. Schubert L. A., King G., Cron R. Q., Lewis D. B., Aruffo A., Hollenbaugh D. The human gp39 promoter. Two distinct nuclear factors of activated T cell protein-binding elements contribute independently to transcriptional activation. J. Biol. Chem. 270:1995;29624-29627.
88. Seledtsov I. A., Solovyev V. V., Merkulova T. I. New elements of glucocorticoid-receptor binding sites of hormone-regulated genes. Biochim. Biophys. Acta. 1089:1991;367-376.
89. Serfling E., Barthelmas R., Pfeuffer I., Schenk B., Zarius S., Swoboda R., Mercurio F., Karin M. Ubiquitous and lymphocyte-specific factors are involved in the induction of the mouse interleukin 2 gene in T lymphocytes. EMBO J. 8:1989;465-473.
90. Serfling E., Avots A., Neumann M. The architecture of the interleukin-2 promoter: a reflection of T lymphocyte activation. Biochim. Biophys. Acta. 1263:1995;181-200.
91. Shaw J. P., Utz P. J., Durand D. B., Toole J. J., Emmel E. A., Crabtree G. R. Identification of a putative regulator of early T cell activation genes. Science. 241:1988;202-205.
92. Shaw P. Ternary complex formation over the c-fos serum response element: p62(SRF) exhibits dual component specificity with contact to DNA and an extended structure in the DNA-binding domain of p67(SRF). EMBO J. 11:1992;3011-3019.
93. Shibasaki F., Kondo E., Akagi T., McKeon F. Suppression of signalling through transcription factor NF-AT by interactions between calcineurin and Bcl-2. Nature. 386:1997;728-731.
94. Sica A., Dorman L., Viggiano V., Cippitelli M., Ghosh P., Rice N., Young H. A. Interaction of NF-kappaB and NFAT with the interferon-gamma promoter. J. Biol. Chem. 272:1997;30412-30420.
95. Solovyev V., Salamov A. The Gene-Finder computer tools for analysis of human and model organism genome sequences. Gaasterland T., Karp P., Karpus K., Ouzounis C., Sander C., Valencia A. Proceedings of the Fifth International Conference on Intelligent Systems for Molecular Biology. 1997;294-302 AAAI Press, Menlo Park.
96. Stranick K. S., Zambas D. N., Uss A. S., Egan R. W., Billah M. M., Umland S. P. Identification of transcription factor binding sites important in the regulation of the human interleukin-5 gene. J. Biol. Chem. 272:1997;16453-16465.
97. Takemoto N., Koyano-Nakagawa N., Arai N., Arai K., Yokota T. Four P-like elements are required for optimal transcription of the mouse IL-4 gene: involvement of a distinct set of nuclear factor of activated T cells and activator protein-1 family proteins. Int. Immunol. 9:1997;1329-1338.
98. Thompson C. B. Creation of immunoglobulin diversity by intrachromosomal gene conversion. Trends Genet. 8:1992;416-422.
99. Tronche F., Ringeisen F., Blumenfeld M., Yaniv M., Pontoglio M. Analysis of the distribution of binding sites for a tissue-specific transcription factor in the vertebrate genome. J. Mol. Biol. 266:1997;231-245.
100. Tsai E. Y., Jain J., Pesavento P. A., Rao A., Goldfeld A. E. Tumor necrosis factor alpha gene regulation in activated T cells involves ATF-2/Jun and NFATp. Mol. Cell. Biol. 16:1996a;459-467.
101. Tsai E. Y., Yie J., Thanos D., Goldfeld A. E. Cell-type-specific regulation of the human tumor necrosis factor alpha gene in B cells and T cells by NFATp and ATF-2/JUN. Mol. Cell. Biol. 16:1996b;5232-5244.
102. Tsytsykova A. V., Tsitsikov E. N., Geha R. S. The CD40L promoter contains nuclear factor of activated T cells-binding motifs which require AP-1 binding for activation of transcription. J. Biol. Chem. 271:1996;3763-3770.
103. Velcich A., Ziff E. B. Functional analysis of an isolated fos promoter element with AP-1 site homology reveals cell type-specific transcriptional properties. Mol. Cell. Biol. 10:1990;6273-6282.
104. Wasserman W. W., Fickett J. W. Identification of regulatory regions which confer muscle-specific gene expression. J. Mol. Biol. 278:1998;167-181.
105. Weiss A., Littman D. R. Signal transduction by lymphocyte antigen receptors. Cell. 76:1994;263-274.
106. Wingender E., Karas H., Knüppel R. TRANSFAC database as a bridge between sequence data libraries and biological function. Altman R. B., Dunker A. K., Hunter L., Klein T. E. Pacific Symposium on Biocomputing '97. 1996;477-485 World Scientific, Singapore.
107. Wingender E., Kel A. E., Kel O. V., Karas H., Heinemeyer T., Dietze P., Knueppel R., Romaschenko A. G., Kolchanov N. A. TRANSFAC, TRRD and COMPEL: toward a federated database system on transcriptional regulation. Nucl. Acids Res. 25:1997;265-268.
108. Wong B., Arron J., Choi Y. T cell receptor signals enhance susceptibility to Fas-mediated apoptosis. J. Exp. Med. 186:1997;1939-1944.
109. Yamamoto M., Yoshida M., Ono K., Fujita T., Ohtani-Fujita N., Sakai T., Nikaido T. Effect of tumor supressors on cell cycle-regulatory genes: RB supresses p34cdc2 expression and normal p53 supresses cyclin A expression. Exp. Cell Res. 210:1994;94-101.
110. Yang X. F., Weber G. F., Cantor H. A novel Bcl-x isoform connected to the T cell receptor regulates apoptosis in T cells. Immunity. 7:1997;629-639.
111. Yaseen N. R., Park J., Kerppola T., Curran T., Sharma S. A central role for Fos in human B- and T-cell NFAT (nuclear factor of activated T cells): an acidic region is required for in vitro assembly. Mol. Cell. Biol. 14:1994;6886-6895.
112. Zhu J., Liu J. S., Lawrence C. E. Bayesian adaptive sequence alignment algorithms. Bioinformatics. 14:1998;25-39.