DNA Binding by GATA Transcription Factor Suggests Mechanisms of DNA Looping and Long-Range Gene Regulation

Cell Reports

Volumn 2, Issue 5, 2012, Pages 1197-1206

  Chen, Yongheng ^a,d   Bates, Darren L ^e   Dey, Raja ^a   Chen, Po Han ^a   Machado, Ana Carolina Dantas ^a   Laird Offringa, Ite A ^a,b,c   Rohs, Remo ^a,b   Chen, Lin ^a,b,d,e  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^d CENTRAL SOUTH UNIVERSITY   (China)

^e UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA FRAGMENT; PALINDROMIC DNA; TRANSCRIPTION FACTOR GATA; ZINC FINGER PROTEIN;

ARTICLE; BINDING AFFINITY; BINDING SITE; CRYSTAL STRUCTURE; DNA BINDING; DNA BINDING DOMAIN; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENE CONTROL; PRIORITY JOURNAL; PROTEIN DNA INTERACTION; PROTEIN DOMAIN; PROTEIN STABILITY;

AMINO ACID SEQUENCE; BASE SEQUENCE; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; DNA; FLUORESCENCE RESONANCE ENERGY TRANSFER; GATA TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION; HUMANS; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT; ZINC FINGERS;

EID: 84870397179     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2012.10.012     Document Type: Article

References (56)

1. Adams P.D., Grosse-Kunstleve R.W., Hung L.W., Ioerger T.R., McCoy A.J., Moriarty N.W., Read R.J., Sacchettini J.C., Sauter N.K., Terwilliger T.C. PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr. D Biol. Crystallogr. 2002, 58:1948-1954.
2. Bain D.L., Heneghan A.F., Connaghan-Jones K.D., Miura M.T. Nuclear receptor structure: implications for function. Annu. Rev. Physiol. 2007, 69:201-220.
3. Bandukwala H.S., Wu Y., Feuerer M., Chen Y., Barboza B., Ghosh S., Stroud J.C., Benoist C., Mathis D., Rao A., Chen L. Structure of a domain-swapped FOXP3 dimer on DNA and its function in regulatory T cells. Immunity 2011, 34:479-491.
4. Bates D.L., Chen Y., Kim G., Guo L., Chen L. Crystal structures of multiple GATA zinc fingers bound to DNA reveal new insights into DNA recognition and self-association by GATA. J. Mol. Biol. 2008, 381:1292-1306.
5. Brünger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., Jiang J.S., Kuszewski J., Nilges M., Pannu N.S., et al. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 1998, 54:905-921.
6. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 1994, 50:760-763. Collaborative Computational Project, Number 4.
7. Dasen J.S., O'Connell S.M., Flynn S.E., Treier M., Gleiberman A.S., Szeto D.P., Hooshmand F., Aggarwal A.K., Rosenfeld M.G. Reciprocal interactions of Pit1 and GATA2 mediate signaling gradient-induced determination of pituitary cell types. Cell 1999, 97:587-598.
8. Elrod-Erickson M., Benson T.E., Pabo C.O. High-resolution structures of variant Zif268 DNA complexes: implications for understanding zinc finger DNA recognition. Structure 1998, 6:451-464.
9. Ferreira R., Ohneda K., Yamamoto M., Philipsen S. GATA1 function, a paradigm for transcription factors in hematopoiesis. Mol. Cell. Biol. 2005, 25:1215-1227.
10. Fujiwara T., O'Geen H., Keles S., Blahnik K., Linnemann A.K., Kang Y.-A., Choi K., Farnham P.J., Bresnick E.H. Discovering hematopoietic mechanisms through genome-wide analysis of GATA factor chromatin occupancy. Mol. Cell 2009, 36:667-681.
11. George K.M., Leonard M.W., Roth M.E., Lieuw K.H., Kioussis D., Grosveld F., Engel J.D. Embryonic expression and cloning of the murine GATA-3 gene. Development 1994, 120:2673-2686.
12. Georgescu C., Longabaugh W.J.R., Scripture-Adams D.D., David-Fung E.-S., Yui M.A., Zarnegar M.A., Bolouri H., Rothenberg E.V. A gene regulatory network armature for T lymphocyte specification. Proc. Natl. Acad. Sci. USA 2008, 105:20100-20105.
13. Guo L., Han A., Bates D.L., Cao J., Chen L. Crystal structure of a conserved N-terminal domain of histone deacetylase 4 reveals functional insights into glutamine-rich domains. Proc. Natl. Acad. Sci. USA 2007, 104:4297-4302.
14. Harris R.C., Mackoy T., Dantas Machado A.C., Xu D., Rohs R., Fenley M.O. Opposites attract: shape and electrostatic complementarity in protein-DNA complexes. Innovations in Biomolecular Modeling and Simulations 2012, 53-80. The Royal Society of Chemistry, London. T. Schlick (Ed.).
15. Ho I.C., Vorhees P., Marin N., Oakley B.K., Tsai S.F., Orkin S.H., Leiden J.M. Human GATA-3: a lineage-restricted transcription factor that regulates the expression of the T cell receptor alpha gene. EMBO J. 1991, 10:1187-1192.
16. Honig B., Nicholls A. Classical electrostatics in biology and chemistry. Science 1995, 268:1144-1149.
17. Horiuchi S., Onodera A., Hosokawa H., Watanabe Y., Tanaka T., Sugano S., Suzuki Y., Nakayama T. Genome-wide analysis reveals unique regulation of transcription of Th2-specific genes by GATA3. J. Immunol. 2011, 186:6378-6389.
18. Jing H., Vakoc C.R., Ying L., Mandat S., Wang H., Zheng X., Blobel G.A. Exchange of GATA factors mediates transitions in looped chromatin organization at a developmentally regulated gene locus. Mol. Cell 2008, 29:232-242.
19. Jones T.A., Zou J.Y., Cowan S.W., Kjeldgaard M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A 1991, 47:110-119.
20. Kalhor R., Tjong H., Jayathilaka N., Alber F., Chen L. Genome architectures revealed by tethered chromosome conformation capture and population-based modeling. Nat. Biotechnol. 2012, 30:90-98.
21. Ko L.J., Engel J.D. DNA-binding specificities of the GATA transcription factor family. Mol. Cell. Biol. 1993, 13:4011-4022.
22. Lavery R., Sklenar H. Defining the structure of irregular nucleic-acids-conventions and principles. J. Biomol. Struct. Dyn 1989, 6:655-667.
23. Liew C.K., Simpson R.J.Y., Kwan A.H.Y., Crofts L.A., Loughlin F.E., Matthews J.M., Crossley M., Mackay J.P. Zinc fingers as protein recognition motifs: structural basis for the GATA-1/friend of GATA interaction. Proc. Natl. Acad. Sci. USA 2005, 102:583-588.
24. Luscombe N.M., Laskowski R.A., Thornton J.M. NUCPLOT: a program to generate schematic diagrams of protein-nucleic acid interactions. Nucleic Acids Res. 1997, 25:4940-4945.
25. Martin D.I., Orkin S.H. Transcriptional activation and DNA binding by the erythroid factor GF-1/NF-E1/Eryf 1. Genes Dev. 1990, 4:1886-1898.
26. Merika M., Orkin S.H. DNA-binding specificity of GATA family transcription factors. Mol. Cell. Biol. 1993, 13:3999-4010.
27. Molkentin J.D. The zinc finger-containing transcription factors GATA-4, -5, and -6. Ubiquitously expressed regulators of tissue-specific gene expression. J. Biol. Chem. 2000, 275:38949-38952.
28. Myszka D.G., Morton T.A. CLAMP: a biosensor kinetic data analysis program. Trends Biochem. Sci. 1998, 23:149-150.
29. Myszka D.G., Jonsen M.D., Graves B.J. Equilibrium analysis of high affinity interactions using BIACORE. Anal. Biochem. 1998, 265:326-330.
30. Newton A., Mackay J., Crossley M. The N-terminal zinc finger of the erythroid transcription factor GATA-1 binds GATC motifs in DNA. J. Biol. Chem. 2001, 276:35794-35801.
31. Omichinski J.G., Clore G.M., Schaad O., Felsenfeld G., Trainor C., Appella E., Stahl S.J., Gronenborn A.M. NMR structure of a specific DNA complex of Zn-containing DNA binding domain of GATA-1. Science 1993, 261:438-446.
32. Orkin S.H., Shivdasani R.A., Fujiwara Y., McDevitt M.A. Transcription factor GATA-1 in megakaryocyte development. Stem Cells 1998, 16(Suppl 2):79-83.
33. Otwinowski Z., Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 1997, 276:307-326.
34. Patient R.K., McGhee J.D. The GATA family (vertebrates and invertebrates). Curr. Opin. Genet. Dev. 2002, 12:416-422.
35. Pedone P.V., Omichinski J.G., Nony P., Trainor C., Gronenborn A.M., Clore G.M., Felsenfeld G. The N-terminal fingers of chicken GATA-2 and GATA-3 are independent sequence-specific DNA binding domains. EMBO J. 1997, 16:2874-2882.
36. Rohs R., West S.M., Sosinsky A., Liu P., Mann R.S., Honig B. The role of DNA shape in protein-DNA recognition. Nature 2009, 461:1248-1253.
37. Rohs R., Jin X., West S.M., Joshi R., Honig B., Mann R.S. Origins of specificity in protein-DNA recognition. Annu. Rev. Biochem. 2010, 79:233-269.
38. Shimizu R., Takahashi S., Ohneda K., Engel J.D., Yamamoto M. In vivo requirements for GATA-1 functional domains during primitive and definitive erythropoiesis. EMBO J. 2001, 20:5250-5260.
39. Song H., Suehiro J.-i., Kanki Y., Kawai Y., Inoue K., Daida H., Yano K., Ohhashi T., Oettgen P., Aird W.C., et al. Critical role for GATA3 in mediating Tie2 expression and function in large vessel endothelial cells. J. Biol. Chem. 2009, 284:29109-29124.
40. Spilianakis C.G., Lalioti M.D., Town T., Lee G.R., Flavell R.A. Interchromosomal associations between alternatively expressed loci. Nature 2005, 435:637-645.
41. Starich M.R., Wikström M., Arst H.N., Clore G.M., Gronenborn A.M. The solution structure of a fungal AREA protein-DNA complex: an alternative binding mode for the basic carboxyl tail of GATA factors. J. Mol. Biol. 1998, 277:605-620.
42. Stroud J.C., Chen L. Structure of NFAT bound to DNA as a monomer. J. Mol. Biol. 2003, 334:1009-1022.
43. Stroud J.C., Lopez-Rodriguez C., Rao A., Chen L. Structure of a TonEBP-DNA complex reveals DNA encircled by a transcription factor. Nat. Struct. Biol. 2002, 9:90-94.
44. Stroud J.C., Wu Y., Bates D.L., Han A., Nowick K., Paabo S., Tong H., Chen L. Structure of the forkhead domain of FOXP2 bound to DNA. Structure 2006, 14:159-166.
45. Trainor C.D., Omichinski J.G., Vandergon T.L., Gronenborn A.M., Clore G.M., Felsenfeld G. A palindromic regulatory site within vertebrate GATA-1 promoters requires both zinc fingers of the GATA-1 DNA-binding domain for high-affinity interaction. Mol. Cell. Biol. 1996, 16:2238-2247.
46. Tsai F.-Y., Orkin S.H. Transcription factor GATA-2 is required for proliferation/survival of early hematopoietic cells and mast cell formation, but not for erythroid and myeloid terminal differentiation. Blood 1997, 89:3636-3643.
47. Vakoc C.R., Letting D.L., Gheldof N., Sawado T., Bender M.A., Groudine M., Weiss M.J., Dekker J., Blobel G.A. Proximity among distant regulatory elements at the beta-globin locus requires GATA-1 and FOG-1. Mol. Cell 2005, 17:453-462.
48. Visvader J.E., Crossley M., Hill J., Orkin S.H., Adams J.M. The C-terminal zinc finger of GATA-1 or GATA-2 is sufficient to induce megakaryocytic differentiation of an early myeloid cell line. Mol. Cell. Biol. 1995, 15:634-641.
49. Wang Y., Su M.A., Wan Y.Y. An essential role of the transcription factor GATA-3 for the function of regulatory T cells. Immunity 2011, 35:337-348.
50. Watt A.J., Battle M.A., Li J., Duncan S.A. GATA4 is essential for formation of the proepicardium and regulates cardiogenesis. Proc. Natl. Acad. Sci. USA 2004, 101:12573-12578.
51. Wei G., Abraham B.J., Yagi R., Jothi R., Cui K., Sharma S., Narlikar L., Northrup D.L., Tang Q., Paul W.E., et al. Genome-wide analyses of transcription factor GATA3-mediated gene regulation in distinct T cell types. Immunity 2011, 35:299-311.
52. Weiss M.J., Orkin S.H. GATA transcription factors: key regulators of hematopoiesis. Exp. Hematol. 1995, 23:99-107.
53. Wuttke D.S., Foster M.P., Case D.A., Gottesfeld J.M., Wright P.E. Solution structure of the first three zinc fingers of TFIIIA bound to the cognate DNA sequence: determinants of affinity and sequence specificity. J. Mol. Biol. 1997, 273:183-206.
54. Yu C., Niakan K.K., Matsushita M., Stamatoyannopoulos G., Orkin S.H., Raskind W.H. X-linked thrombocytopenia with thalassemia from a mutation in the amino finger of GATA-1 affecting DNA binding rather than FOG-1 interaction. Blood 2002, 100:2040-2045.
55. Yu M., Riva L., Xie H., Schindler Y., Moran T.B., Cheng Y., Yu D., Hardison R., Weiss M.J., Orkin S.H., et al. Insights into GATA-1-mediated gene activation versus repression via genome-wide chromatin occupancy analysis. Mol. Cell 2009, 36:682-695.
56. Zheng W., Flavell R.A. The transcription factor GATA-3 is necessary and sufficient for Th2 cytokine gene expression in CD4 T cells. Cell 1997, 89:587-596.