c-Jun homodimers can function as a context-specific coactivator

Molecular and Cellular Biology

Volumn 27, Issue 8, 2007, Pages 2919-2933

  Grondin, Benoit ^a   Lefrancois, Martin ^a   Tremblay, Mathieu ^a   Saint Denis, Marianne ^a   Haman, André ^a   Waga, Kazuo ^c   Bédard, André ^d,f   Tenen, Daniel G ^e   Hoang, Trang ^a,b  

^a INSTITUTE FOR RESEARCH IN IMMUNOLOGY AND CANCER   (Canada)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

^c DOKKYO MEDICAL UNIVERSITY   (Japan)

^d YORK UNIVERSITY   (Canada)

^e HARVARD STEM CELL INSTITUTE   (United States)

^f MCMASTER UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CCAAT ENHANCER BINDING PROTEIN BETA; DNA; HOMODIMER; INTERLEUKIN 1BETA; PROTEIN C JUN; RNA POLYMERASE II; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR PU 1;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; CHROMATIN; COMPLEX FORMATION; CONTROLLED STUDY; DNA BINDING MOTIF; GENE EXPRESSION REGULATION; GENE LOCUS; GENE SEQUENCE; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ASSEMBLY; PROTEIN DNA BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; TRANSCRIPTION INITIATION;

AMINO ACID SEQUENCE; ANIMALS; CCAAT-ENHANCER-BINDING PROTEIN-BETA; CERCOPITHECUS AETHIOPS; COS CELLS; DIMERIZATION; DNA; GENE EXPRESSION; INTERLEUKIN-1BETA; MACROPHAGE ACTIVATION; MACROPHAGES; MICE; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; PROMOTER REGIONS (GENETICS); PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-JUN; RNA POLYMERASE II; TEMPLATES, GENETIC; TRANS-ACTIVATORS; UP-REGULATION;

EID: 34147197211     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00936-06     Document Type: Article

References (81)

1. Agalioti, T., G. Chen, and D. Thanos. 2002. Deciphering the transcriptional histone acetylation code for a human gene. Cell 111:381-392.
2. Agalioti, T., S. Lomvardas, B. Parekh, J. Yie, T. Maniatis, and D. Thanos. 2000. Ordered recruitment of chromatin modifying and general transcription factors to the IFN-beta promoter. Cell 103:667-678.
3. Allegretto, E. A., T. Smeal, P. Angel, B. M. Spiegelman, and M. Karin. 1990. DNA-binding activity of Jun is increased through its interaction with Fos. J. Cell Biochem. 42:193-206.
4. Angel, P., M. Imagawa, R. Chiu, B. Stein, R. J. Imbra, H. J. Rahmsdorf, C. Jonat, P. Herrlich, and M. Karin. 1987. Phorbol ester-inducible genes contain a common cis element recognized by a TPA-modulated trans-acting factor. Cell 49:729-739.
5. Bassuk, A. G., and J. M. Leiden. 1995. A direct physical association between ETS and AP-1 transcription factors in normal human T cells. Immunity 3:223-237.
6. Behre, G., A. J. Whitmarsh, M. P. Coghlan, T. Hoang, C. L. Carpenter, D. E. Zhang, R. J. Davis, and D. G. Tenen. 1999. c-Jun is a JNK-independent coactivator of the PU.1 transcription factor 15. J. Biol. Chem. 274:4939-4946.
7. Billia, F., M. Barbara, J. McEwen, M. Trevisan, and N. N. Iscove. 2001. Resolution of pluripotential intermediates in murine hematopoietic differentiation by global complementary DNA amplification from single cells: confirmation of assignments by expression profiling of cytokine receptor transcripts. Blood 97:2257-2268.
8. Bohmann, D., and R. Tjian. 1989. Biochemical analysis of transcriptional activation by Jun: differential activity of c- and v-Jun. Cell 59:709-717.
9. Buras, J. A., B. G. Monks, and M. J. Fenton. 1994. The NF-beta A-binding element, not an overlapping NF-IL-6-binding element, is required for maximal IL-1 beta gene expression 1. J. Immunol. 152:4444-4454.
10. Chinenov, Y., and T. K. Kerppola. 2001. Close encounters of many kinds: Fos-Jun interactions that mediate transcription regulatory specificity. Oncogene 20:2438-2452.
11. Chomczynski, P., and N. Sacchi. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162:156-159.
12. Choy, B., and M. R. Green. 1993. Eukaryotic activators function during multiple steps of preinitiation complex assembly. Nature 366:531-536.
13. DeKoter, R. P., and H. Singh. 2000. Regulation of B lymphocyte and macrophage development by graded expression of PU.1 5. Science 288:1439-1441.
14. Derijard, B., M. Hibi, I. H. Wu, T. Barrett, B. Su, T. Deng, M. Karin, and R. J. Davis. 1994. JNK1: a protein kinase stimulated by UV light and Ha-Ras that binds and phosphorylates the c-Jun activation domain. Cell 76:1025-1037.
15. Devary, Y., R. A. Gottlieb, L. F. Lau, and M. Karin. 1991. Rapid and preferential activation of the c-jun gene during the mammalian UV response. Mol. Cell. Biol. 11:2804-2811.
16. Drewett, V., H. Molina, A. Millar, S. Muller, F. von Hesler, and P. E. Shaw. 2001. DNA-bound transcription factor complexes analysed by mass-spectrometry: binding of novel proteins to the human c-fos SRE and related sequences. Nucleic Acids Res. 29:479-487.
17. Eberhardy, S. R., and P. J. Farnham. 2001. c-Myc mediates activation of the cad promoter via a post-RNA polymerase II recruitment mechanism. J. Biol. Chem. 276:48562-48571.
18. Eferl, R., and E. F. Wagner. 2003. AP-1: a double-edged sword in tumorigenesis. Nat. Rev. Cancer 3:859-868.
19. Glover, J. N., and S. C. Harrison. 1995. Crystal structure of the heterodimeric bZIP transcription factor c-Fos-c-Jun bound to DNA. Nature 373:257-261.
20. Grondin, B., and N. DeLuca. 2000. Herpes simplex virus type 1 ICP4 promotes transcription preinitiation complex formation by enhancing the binding of TFIID to DNA. J. Virol. 74:11504-11510.
21. Hahn, S. 2004. Structure and mechanism of the RNA polymerase II transcription machinery. Nat. Struct. Mol. Biol. 11:394-403.
22. Hambleton, J., S. L. Weinstein, L. Lem, and A. L. DeFranco. 1996. Activation of c-Jun N-terminal kinase in bacterial lipopolysaccharide-stimulated macrophages. Proc. Natl. Acad. Sci. USA 93:2774-2778.
23. Hawley, R. G., A. Z. Fong, M. Lu, and T. S. Hawley. 1994. The HOX11 homeobox-containing gene of human leukemia immortalizes murine hematopoietic precursors. Oncogene 9:1-12.
24. Herblot, S., A. M. Steff, P. Hugo, P. D. Aplan, and T. Hoang. 2000. SCL and LMO1 alter thymocyte differentiation: inhibition of E2A-HEB function and pre-T alpha chain expression. Nat. Immunol. 1:138-144.
25. Hoang, T., E. Paradis, G. Brady, F. Billia, K. Nakahara, N. N. Iscove, and I. R. Kirsch. 1996. Opposing effects of the basic helix-loop-helix transcription factor SCL on erythroid and monocytic differentiation. Blood 87:102-111.
26. Hohaus, S., M. S. Petrovick, M. T. Voso, Z. Sun, D. E. Zhang, and D. G. Tenen. 1995. PU.1 (Spi-1) and C/EBP alpha regulate expression of the granulocyte-macrophage colony-stimulating factor receptor alpha gene. Mol. Cell. Biol. 15:5830-5845.
27. Hsu, W., T. K. Kerppola, P. L. Chen, T. Curran, and S. Chen-Kiang. 1994. Fos and Jun repress transcription activation by NF-IL6 through association at the basic zipper region. Mol. Cell. Biol. 14:268-276.
28. Iwasaki, H., C. Somoza, H. Shigematsu, E. A. Duprez, J. Iwasaki-Arai, S. Mizuno, Y. Arinobu, K. Geary, P. Zhang, T. Dayaram, M. L. Fenyus, S. Elf, S. Chan, P. Kastner, C. S. Huettner, R. Murray, D. G. Tenen, and K. Akashi. 2005. Distinctive and indispensable roles of PU.1 in maintenance of hematopoietic stem cells and their differentiation. Blood 106:1590-1600.
29. Jacobson, R. H., A. G. Ladurner, D. S. King, and R. Tjian. 2000. Structure and function of a human TAFII250 double bromodomain module. Science 288:1422-1425.
30. Kim, T. K., and T. Maniatis. 1997. The mechanism of transcriptional synergy of an in vitro assembled interferon-beta enhanceosome. Mol. Cell 1:119-129.
31. Kitamura, T., T. Tange, T. Terasawa, S. Chiba, T. Kuwaki, K. Miyagawa, Y. F. Piao, K. Miyazono, A. Urabe, and F. Takaku. 1989. Establishment and characterization of a unique human cell line that proliferates dependency on GM-CSF, IL-3, or erythropoietin. J. Cell Physiol. 140:323-334.
32. Klemsz, M. J., S. R. McKercher, A. Celada, C. Van Beveren, and R. A. Maki. 1990. The macrophage and B cell-specific transcription factor PU.1 is related to the ETS oncogene. Cell 61:113-124.
33. Kominato, Y., D. Galson, W. R. Waterman, A. C. Webb, and P. E. Auron. 1995. Monocyte expression of the human prointerleukin 1 beta gene (IL1B) is dependent on promoter sequences which bind the hematopoietic transcription factor Spi-1/PU.1. Mol. Cell. Biol. 15:58-68.
34. Kowenz-Leutz, E., and A. Leutz. 1999. A C/EBP beta isoform recruits the SWI/SNF complex to activate myeloid genes. Mol. Cell 4:735-743.
35. Koyama, Y., Y. Tanaka, K. Saito, M. Abe, K. Nakatsuka, I. Morimoto, P. E. Auron, and S. Eto. 1996. Cross-linking of intercellular adhesion molecule 1 (CD54) induces AP-1 activation and IL-1beta transcription. J. Immunol. 157:5097-5103.
36. Krosl, G., G. He, M. Lefrancois, F. Charron, P. H. Romeo, P. Jolicoeur, I. R. Kirsch, M. Nemer, and T. Hoang. 1998. Transcription factor SCL is required for c-Kit expression and c-Kit function in hemopoietic cells. J. Exp. Med. 188:439-450.
37. Langridge, J., P. Langridge, and P. L. Bergquist. 1980. Extraction of nucleic acids from agarose gels. Anal. Biochem. 103:264-271.
38. Lecuyer, E., S. Herblot, M. Saint-Denis, R. Martin, C. G. Begley, C. Porcher, S. H. Orkin, and T. Hoang. 2002. The SCL complex regulates c-Kit expression in hematopoietic cells through functional interaction with Sp1. Blood 100:2430-2440.
39. Lemon, B., and R. Tjian. 2000. Orchestrated response: a symphony of transcription factors for gene control. Genes Dev. 14:2551-2569.
40. Li, A. C., F. R. Guidez, J. G. Collier, and C. K. Glass. 1998. The macrosialin promoter directs high levels of transcriptional activity in macrophages dependent on combinatorial interactions between PU.1 and c-Jun. J. Biol. Chem. 273:5389-5399.
41. Liang, M. D., Y. Zhang, D. McDevit, S. Marecki, and B. S. Nikolajczyk. 2006. The interleukin-1β gene is transcribed from a poised promoter architecture in monocytes. J. Biol. Chem. 281:9227-9237.
42. Listman, J. A., N. Wara-aswapati, J. E. Race, L. W. Blystone, N. Walker-Kopp, Z. Yang, and P. E. Auron. 2005. Conserved ETS domain arginines mediate DNA binding, nuclear localization, and a novel mode of bZIP interaction. J. Biol. Chem. 280:41421-41428.
43. Lively, T. N., T. N. Nguyen, S. K. Galasinski, and J. A. Goodrich. 2004. The basic leucine zipper domain of c-Jun functions in transcriptional activation through interaction with the N terminus of human TATA-binding protein-associated factor-1 (human TAF(II)250). J. Biol. Chem. 279:26257-26265.
44. Lomvardas, S., and D. Thanos. 2001. Nucleosome sliding via TBP DNA binding in vivo. Cell 106:685-696.
45. Lomvardas, S., and D. Thanos. 2002. Modifying gene expression programs by altering core promoter chromatin architecture. Cell 110:261-271.
46. Margueron, R., P. Trojer, and D. Reinberg. 2005. The key to development: interpreting the histone code? Curr. Opin. Genet. Dev. 15:163-176.
47. Martin, M. L., P. M. Lieberman, and T. Curran. 1996. Fos-Jun dimerization promotes interaction of the basic region with TFIIE-34 and TFIIF. Mol. Cell. Biol. 16:2110-2118.
48. McKercher, S. R., B. E. Torbett, K. L. Anderson, G. W. Henkel, D. J. Vestal, H. Baribault, M. Klemsz, A. J. Feeney, G. E. Wu, C. J. Paige, and R. A. Maki. 1996. Targeted disruption of the PU.1 gene results in multiple hematopoietic abnormalities. EMBO J. 15:5647-5658.
49. Mo, X., E. Kowenz-Leutz, H. Xu, and A. Leutz. 2004. Ras induces mediator complex exchange on C/EBP beta. Mol. Cell 13:241-250.
50. Moulton, K. S., K. Semple, H. Wu, and C. K. Glass. 1994. Cell-specific expression of the macrophage scavenger receptor gene is dependent on PU.1 and a composite AP-1/ets motif. Mol. Cell. Biol. 14:4408-4418.
51. Natsuka, S., S. Akira, Y. Nishio, S. Hashimoto, T. Sugita, H. Isshiki, and T. Kishimoto. 1992. Macrophage differentiation-specific expression of NF-IL6, a transcription factor for interleukin-6. Blood 79:460-466.
52. Nerlov, C., and T. Graf. 1998. PU.1 induces myeloid lineage commitment in multipotent hematopoietic progenitors. Genes Dev. 12:2403-2412.
53. Ness, S. A., E. Kowenz-Leutz, T. Casini, T. Graf, and A. Leutz. 1993. Myb and NF-M: combinatorial activators of myeloid genes in heterologous cell types. Genes Dev. 7:749-759.
54. Newman, J. R., and A. E. Keating. 2003. Comprehensive identification of human bZIP interactions with coiled-coil arrays. Science 300:2097-2101.
55. Ng, L., D. Forrest, and T. Curran. 1993. Differential roles for Fos and Jun in DNA-binding: redox-dependent and independent functions. Nucleic Acids Res. 21:5831-5837.
56. Nikolajczyk, B. S., J. A. Sanchez, and R. Sen. 1999. ETS protein-dependent accessibility changes at the immunoglobulin mu heavy chain enhancer. Immunity 11:11-20.
57. Ogawa, S., J. Lozach, K. Jepsen, D. Sawka-Verhelle, V. Perissi, R. Sasik, D. W. Rose, R. S. Johnson, M. G. Rosenfeld, and C. K. Glass. 2004. A nuclear receptor corepressor transcriptional checkpoint controlling activator protein 1-dependent gene networks required for macrophage activation. Proc. Natl. Acad. Sci. USA 101:14461-14466.
58. O'Neil, K. T., R. H. Hoess, and W. F. DeGrado. 1990. Design of DNA-binding peptides based on the leucine zipper motif. Science 249:774-778.
59. Papavassiliou, A. G., M. Treier, C. Chavrier, and D. Bohmann. 1992. Targeted degradation of c-Fos, but not v-Fos, by a phosphorylation- dependent signal on c-Jun. Science 258:1941-1944.
60. Petrovick, M. S., S. W. Hiebert, A. D. Friedman, C. J. Hetherington, D. G. Tenen, and D. E. Zhang. 1998. Multiple functional domains of AML1: PU.1 and C/EBPα synergize with different regions of AML1. Mol. Cell. Biol. 18:3915-3925.
61. PongubaIa, J. M., and M. L. Atchison. 1997. PU.1 can participate in an active enhancer complex without its transcriptional activation domain. Proc. Natl. Acad. Sci. USA 94:127-132.
62. Ptashne, M., and A. Gann. 1997. Transcriptional activation by recruitment. Nature 386:569-577.
63. Ranish, J. A., N. Yudkovsky, and S. Hahn. 1999. Intermediates in formation and activity of the RNA polymerase II preinitiation complex: holoenzyme recruitment and a postrecruitment role for the TATA box and TFIIB. Genes Dev. 13:49-63.
64. Rosmarin, A. G., D. Caprio, R. Levy, and C. Simkevich. 1995. CD18 (beta 2 leukocyte integrin) promoter requires PU.1 transcription factor for myeloid activity. Proc. Natl. Acad. Sci. USA. 92:801-805.
65. Ryseck, R. P., and R. Bravo. 1991. c-JUN, JUN B, and JUN D differ in their binding affinities to AP-1 and CRE consensus sequences: effect of FOS proteins. Oncogene 6:533-542.
66. Sandaltzopoulos, R., and P. B. Becker. 1994. Solid phase DNase I footprinting: quick and versatile. Nucleic Acids Res. 22:1511-1512.
67. Schwartz, C., K. Beck, S. Mink, M. Schmolke, B. Budde, D. Wenning, and K. H. Klempnauer. 2003. Recruitment of p300 by C/EBPbeta triggers phosphorylation of p300 and modulates coactivator activity. EMBO J. 22:882-892.
68. Scott, E. W., M. C. Simon, J. Anastasi, and H. Singh. 1994. Requirement of transcription factor PU.1 in the development of multiple hematopoietic lineages. Science 265:1573-1577.
69. Sherman, M. L., R. Datta, D. E. Hallahan, R. R. Weichselbaum, and D. W. Kufe. 1990. Ionizing radiation regulates expression of the c-jun protooncogene. Proc. Natl. Acad. Sci. USA. 87:5663-5666.
70. Shirakawa, F., K. Saito, C. A. Bonagura, D. L. Galson, M. J. Fenton, A. C. Webb, and P. E. Auron. 1993. The human prointerleukin 1 beta gene requires DNA sequences both proximal and distal to the transcription start site for tissue-specific induction. Mol. Cell. Biol. 13:1332-1344.
71. Shivdasani, R. A., and S. H. Orkin. 1996. The transcriptional control of hematopoiesis. Blood 87:4025-4039.
72. Shuman, J. D., C. R. Vinson, and S. L. McKnight. 1990. Evidence of changes in protease sensitivity and subunit exchange rate on DNA binding by C/EBP. Science 249:771-774.
73. Smith, S. E., and D. Bohmann. 1992. Functional dissection of AP-1 transcription factors using the Gal4 adaptor assay. Cell Growth Differ. 3:523-529.
74. Steidl, U., et al. 2006. Essential role of Jun family transcription factors in PU.1 knockdown-induced leukemic stem cells. Nat. Genet. 38:1269-1277.
75. Tanaka, T., S. Akira, K. Yoshida, M. Umemoto, Y. Yoneda, N. Shirafuji, H. Fujiwara, S. Suematsu, N. Yoshida, and T. Kishimoto. 1995. Targeted disruption of the NF-IL6 gene discloses its essential role in bacteria killing and tumor cytotoxicity by macrophages. Cell 80:353-361.
76. Treier, M., L. M. Staszewski, and D. Bohmann. 1994. Ubiquitin-dependent c-Jun degradation in vivo is mediated by the delta domain. Cell 78:787-798.
77. Vinson, C., M. Myakishev, A. Acharya, A. A. Mir, J. R. Moll, and M. Bonovich. 2002. Classification of human B-ZIP proteins based on dimerization properties. Mol. Cell. Biol. 22:6321-6335.
78. Wang, G., M. A. Balamotis, J. L. Stevens, Y. Yamaguchi, H. Handa, and A. J. Berk. 2005. Mediator requirement for both recruitment and postrecruitment steps in transcription initiation. Mol. Cell 17:683-694.
79. Weiss, C., S. Schneider, E. F. Wagner, X. Zhang, E. Seto, and D. Bohmann. 2003. JNK phosphorylation relieves HDAC3-dependent suppression of the transcriptional activity of c-Jun. EMBO J. 22:3686-3695.
80. Yamamoto, H., F. Kihara-Negishi, T. Yamada, Y. Hashimoto, and T. Oikawa. 1999. Physical and functional interactions between the transcription factor PU.1 and the coactivator CBP. Oncogene 18:1495-1501.
81. Yudkovsky, N., J. A. Ranish, and S. Hahn. 2000. A transcription reinitiation intermediate that is stabilized by activator. Nature 408:225-229.