Highly Cooperative Recruitment of Ets-1 and Release of Autoinhibition by Pax5

Journal of Molecular Biology

Volumn 392, Issue 2, 2009, Pages 452-464

  Fitzsimmons, Daniel ^a   Lukin, Kara ^a   Lutz, Ryan ^a   Garvie, Colin W ^b   Wolberger, Cynthia ^c   Hagman, James ^a  

^a NATIONAL JEWISH MEDICAL AND RESEARCH CENTER   (United States)

^b UNIVERSITY OF MARYLAND BALTIMORE COUNTY   (United States)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

autoinhibition; DNA binding; Ets; GABP; Pax

Indexed keywords

ALANINE; CD79A ANTIGEN; DNA; GA BINDING PROTEIN; GLUTAMINE; PROTEIN SUBUNIT; RECOMBINANT PROTEIN; TRANSCRIPTION FACTOR ETS 1; TRANSCRIPTION FACTOR PAX5;

ARTICLE; BINDING AFFINITY; BINDING SITE; DNA BINDING; ENZYME INHIBITION; HUMAN; MOLECULAR MECHANICS; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; TRANSCRIPTION REGULATION; WILD TYPE;

EID: 68949220764     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2009.07.028     Document Type: Article

References (44)

1. Hollenhorst P.C., Jones D.A., and Graves B.J. Expression profiles frame the promoter specificity dilemma of the ETS family of transcription factors. Nucleic Acids Res. 32 (2004) 5693-5702
2. Karim F.D., Urness L.D., Thummel C.S., Klemsz M.J., McKercher S.R., Celada A., et al. The ETS-domain: a new DNA-binding motif that recognizes a purine-rich core DNA sequence. Genes Dev. 4 (1990) 1451-1453
3. Thompson C.C., Brown T.A., and McKnight S.L. Convergence of Ets- and notch-related structural motifs in a heteromeric DNA binding complex. Science 253 (1991) 762-768
4. Batchelor A.H., Piper D.E., de la Brousse F.C., McKnight S.L., and Wolberger C. The structure of GABPα/β: an ETS domain-ankyrin repeat heterodimer bound to DNA. Science 279 (1998) 1037-1041
5. Chinenov Y., Henzl M., and Martin M.E. The α and β subunits of the GA-binding protein form a stable heterodimer in solution. J. Biol. Chem. 275 (2000) 7749-7756
6. Pufall M.A., and Graves B.J. Autoinhibitory domains: modular effectors of cellular regulation. Annu. Rev. Cell Dev. Biol. 18 (2002) 421-462
7. Lim F., Kraut N., Frampton J., and Graf T. DNA binding by c-Ets-1, but not v-Ets, is repressed by an intramolecular mechanism. EMBO J. 11 (1992) 643-652
8. Nye J.A., Petersen J.M., Gunther C.V., Jonsen M.D., and Graves B.J. Interaction of murine Ets-1 with GGA-binding sites establishes the ETS domain as a new DNA-binding motif. Genes Dev. 6 (1992) 975-990
9. Hagman J., and Grosschedl R. An inhibitory carboxyl-terminal domain in Ets-1 and Ets-2 mediates differential binding of ETS family factors to promoter sequences of the mb-1 gene. Proc. Natl Acad. Sci. USA 89 (1992) 8889-8893
10. Petersen J.M., Skalicky J.J., Donaldson L.W., McIntosh L.P., Alber T., and Graves B.J. Modulation of transcription factor Ets-1 DNA binding: DNA-induced unfolding of an α helix. Science 269 (1995) 1866-1869
11. Jonsen M.D., Petersen J.M., Xu Q.-P., and Graves B.J. Characterization of the cooperative function of inhibitory sequences in Ets-1. Mol. Cell. Biol. 16 (1996) 2065-2073
12. Garvie C.W., Pufall M.A., Graves B.J., and Wolberger C. Structural analysis of the autoinhibition of Ets-1 and its role in protein partnerships. J. Biol. Chem. 277 (2002) 45529-45536
13. Wotton D., Ghysdael J., Wang S., Speck N.A., and Owen M.J. Cooperative binding of Ets-1 and core binding factor to DNA. Mol. Cell. Biol. 14 (1994) 840-850
14. Sieweke M.H., Tekotte H., Jarosch U., and Graf T. Cooperative interaction of Ets-1 with USF-1 required for HIV-1 enhancer activity in T cells. EMBO J. 17 (1998) 1728-1739
15. Bassuk A.G., and Leiden J.M. A direct physical association between ETS and AP-1 transcription factors in normal human T cells. Immunity 3 (1995) 223-237
16. Dickinson L.A., Trauger J.W., Baird E.E., Dervan P.B., Graves B.J., and Gottesfeld J.M. Inhibition of Ets-1 DNA binding and ternary complex formation between Ets-1, NF-κB, and DNA by a designed DNA-binding ligand. J. Biol. Chem. 274 (1999) 12765-12773
17. Garvie C.W., Hagman J., and Wolberger C. Structural studies of Ets-1/Pax-5 complex formation on DNA. Mol. Cell 8 (2001) 1267-1276
18. Fitzsimmons D., Hodsdon W., Wheat W., Maira S.-M., Wasylyk B., and Hagman J. Pax-5 (BSAP) recruits Ets proto-oncogene family proteins to form functional ternary complexes on a B-cell-specific promoter. Genes Dev. 10 (1996) 2198-2211
19. Wheat W., Fitzsimmons D., Lennox H., Krautkramer S.R., Gentile L.N., McIntosh L.P., and Hagman J. The highly conserved β-hairpin of the paired DNA-binding domain is required for the assembly of Pax:Ets ternary complexes. Mol. Cell. Biol. 19 (1999) 2231-2241
20. Wehr R., and Gruss P. Pax and vertebrate development. Int. J. Dev. Biol. 40 (1996) 369-377
21. Barr F.G. Chromosomal translocations involving paired box transcription factors in human cancer. Int. J. Biochem. Cell Biol. 29 (1997) 1449-1461
22. Czerny T., Schaffner G., and Busslinger M. DNA sequence recognition by Pax proteins: bipartite structure of the paired domain and its binding site. Genes Dev. 7 (1993) 2048-2061
23. Urbánek P., Wang Z.-Q., Fetka I., Wagner E.F., and Busslinger M. Complete block of early B cell differentiation and altered patterning of the posterior midbrain in mice lacking Pax5/BSAP. Cell 79 (1994) 901-912
24. Hagman J., and Lukin K. Transcription factors drive B cell development. Curr. Opin. Immunol. 18 (2006) 127-134
25. Schebesta A., McManus S., Salvagiotto G., Delogu A., Busslinger G.A., and Busslinger M. Transcription factor Pax5 activates the chromatin of key genes involved in B cell signaling, adhesion, migration, and immune function. Immunity 27 (2007) 49-63
26. Nutt S.L., and Kee B.L. The transcriptional regulation of B cell lineage commitment. Immunity 26 (2007) 715-725
27. Horcher M., Souabni A., and Busslinger M. Pax5/BSAP maintains the identity of B cells in late B lymphopoiesis. Immunity 14 (2001) 779-790
28. Hagman J., and Lukin K. Early B cell factor 'pioneers' the way to B cell development. Trends Immunol. 26 (2005) 455-461
29. Maier H., Colbert J., Fitzsimmons D., Clark D.R., and Hagman J. Activation of the early B cell-specific mb-1 (Ig-α) gene by Pax-5 is dependent on an unmethylated Ets binding site. Mol. Cell. Biol. 23 (2003) 1946-1960
30. Maier H., Ostraat R., Parenti S., Fitzsimmons D., Abraham L.J., Garvie C.W., and Hagman J. Requirements for selective recruitment of Ets proteins and activation of mb-1/Ig-α gene transcription by Pax-5 (BSAP). Nucleic Acids Res. 31 (2003) 5483-5489
31. Adams B., Dorfler P., Aguzzi A., Kozmik Z., Urbanek P., Maurer-Fogy I., and Busslinger M. Pax-5 encodes the transcription factor BSAP and is expressed in B lymphocytes, the developing CNS, and adult testis. Genes Dev. 6 (1992) 1589-1607
32. Wang H., McIntosh L.P., and Graves B.J. Inhibitory module of Ets-1 allosterically regulates DNA binding through a dipole-facilitated phosphate contact. J. Biol. Chem. 277 (2002) 2225-2233
33. Eberhard D., and Busslinger M. The partial homeodomain of the transcription factor Pax-5(BSAP) is an interaction motif for the retinoblastoma and TATA-binding proteins. Cancer Res. 59 (1999) 1716s-1724s
34. Maitra S., and Atchison M.L. BSAP can repress enhancer activity by targeting PU.1 function. Mol. Cell. Biol. 20 (2000) 1911-1922
35. Pufall M.A., Lee G.M., Nelson M.L., Kang H.S., Velyvis A., Kay L.E., et al. Variable control of Ets-1 DNA binding by multiple phosphates in an unstructured region. Science 309 (2005) 142-145
36. Humphrey W., Dalke A., and Schulten K. VMD: visual molecular dynamics. J. Mol. Graphics 14 (1996) 27-28
37. Lee G.M., Donaldson L.W., Pufall M.A., Kang H.S., Pot I., Graves B.J., and McIntosh L.P. The structural and dynamic basis of Ets-1 DNA binding autoinhibition. J. Biol. Chem. 280 (2005) 1088-7099
38. Kopp J.L., Wilder P.J., Desler M., Kinarsky L., and Rizzino A. Different domains of the transcription factor ELF3 are required in a promoter-specific manner and multiple domains control its binding to DNA. J. Biol. Chem. 282 (2007) 3027-3041
39. Xue H.H., Bollenbacher-Reilley J., Wu Z., Spolski R., Jing X., Zhang Y.C., et al. The transcription factor GABP is a critical regulator of B lymphocyte development. Immunity 26 (2007) 421-431
40. Zhang X.K., Moussa O., LaRue A., Bradshaw S., Molano I., Spyropoulos D.D., et al. The transcription factor Fli-1 modulates marginal zone and follicular B cell development in mice. J. Immunol. 181 (2008) 1644-1654
41. Matus D.Q., Pang K., Daly M., and Martindale M.Q. Expression of Pax gene family members in the anthozoan cnidarian, Nematostella vectensis. Evol. Dev. 9 (2007) 25-38
42. Fitzsimmons D., Lutz R., Wheat W., Chamberlin H.M., and Hagman J. Highly conserved amino acids in Pax and Ets proteins are required for DNA binding and ternary complex assembly. Nucleic Acids Res. 29 (2001) 4154-4165
43. Gao H., Lukin K., Ramirez J., Fields S., Lopez D., and Hagman J. Opposing effects of SWI/SNF and Mi-2/NuRD chromatin remodeling complexes on epigenetic reprogramming by EBF and Pax5. Proc. Natl Acad. Sci. USA 106 (2009) 11258-11263
44. Cowley D.O., and Graves B.J. Phosphorylation represses Ets-1 DNA binding by reinforcing autoinhibition. Genes Dev. 14 (2000) 366-376