DNA recognition by the RUNX1 transcription factor is mediated by an allosteric transition in the RUNT domain and by DNA bending

Structure

Volumn 10, Issue 10, 2002, Pages 1395-1407

  Bartfeld, Deborah ^a   Shimon, Linda ^b   Couture, Graeme C ^a   Frolow, Felix ^c   Levanon, Ditsa ^b   Groner, Yoram ^b   Shakked, Zippora ^a  

^a Department of Structural Biology ^*  (Israel)

^b WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^c TEL AVIV UNIVERSITY   (Israel)

Author keywords

Allosteric transition; Crystal structure; DNA conformation; Gene regulation; RUNX1 Runt domain

Indexed keywords

CURVED DNA; PROTEIN; PROTEIN CBFBETA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR RUNX1; UNCLASSIFIED DRUG;

ALLOSTERISM; AMINO ACID SEQUENCE; ARTICLE; BINDING SITE; CRYSTAL STRUCTURE; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DNA BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN INTERACTION;

ALLOSTERIC REGULATION; AMINO ACID SEQUENCE; CORE BINDING FACTOR ALPHA 2 SUBUNIT; CRYSTALLOGRAPHY, X-RAY; DNA; DNA-BINDING PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; PROTO-ONCOGENE PROTEINS; TRANSCRIPTION FACTORS;

EID: 0036774088     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0969-2126(02)00853-5     Document Type: Article

References (60)

1. Speck N.A., Stacy T. A new transcription factor family associated with human leukemias. Crit. Rev. Eukaryot. Gene Expr. 5:1995;337-364.
2. Downing J.R. The AML1-ETO chimaeric transcription factor in acute myeloid leukaemia. biology and clinical significance Br. J. Haematol. 106:1999;296-308.
3. Ito Y. Molecular basis of tissue-specific gene expression mediated by the runt domain transcription factor PEBP2/CBF. Genes Cells. 4:1999;685-696.
4. Levanon D., Negreanu V., Bernstein Y., Bar-Am I., Avivi L., Groner Y. AML1, AML2, and AML3, the human members of the runt domain gene-family. cDNA structure, expression, and chromosomal localization Genomics. 23:1994;425-432.
5. Ito Y., Bae S.-C. The Runt domain transcription factor, PEBP2/CBF, and its involvement in human leukemia. Yaniv M., Ghysdael J. Oncogenes as Transcriptional Regulators, Volume 2. 1997;Birkhauser Verlag, Basel. 107-132.pp.
6. Geoffroy V., Corral D.A., Zhou L., Lee B., Karsenty G. Genomic organization, expression of the human CBFA1 gene, and evidence for an alternative splicing event affecting protein function. Mamm. Genome. 9:1998;54-57.
7. Xiao Z.S., Thomas R., Hinson T.K., Quarles L.D. Genomic structure and isoform expression of the mouse, rat and human Cbfa1/Osf2 transcription factor. Gene. 214:1998;187-197.
8. Bangsow C., Rubins N., Glusman G., Bernstein Y., Negreanu V., Goldenberg D., Lotem J., Ben-Asher E., Lancet D., Levanon D.et al. The RUNX3 gene-sequence, structure and regulated expression. Gene. 279:2001;221-232.
9. Levanon D., Glusman G., Bangsow T., Ben-Asher E., Male D.A., Avidan N., Bangsow C., Hattori M., Taylor T.D., Taudien S.et al. Architecture and anatomy of the genomic locus encoding the human leukemia-associated transcription factor RUNX1/AML1. Gene. 262:2001;23-33.
10. Levanon D., Goldstein R.E., Bernstein Y., Tang H., Goldenberg D., Stifani S., Paroush Z., Groner Y. Transcriptional repression by AML1 and LEF-1 is mediated by the TLE/Groucho corepressors. Proc. Natl. Acad. Sci. USA. 95:1998;11590-11595.
11. Simeone A., Daga A., Calabi F. Expression of runt in the mouse embryo. Dev. Dyn. 203:1995;61-70.
12. Komori T., Yagi H., Nomura S., Yamaguchi A., Sasaki K., Deguchi K., Shimizu Y., Bronson R.T., Gao Y.H., Inada M.et al. Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell. 89:1997;755-764.
13. Otto F., Thornell A.P., Crompton T., Denzel A., Gilmour K.C., Rosewell I.R., Stamp G.W., Beddington R.S., Mundlos S., Olsen B.R.et al. Cbfa1, a candidate gene for cleidocranial dysplasia syndrome, is essential for osteoblast differentiation and bone development. Cell. 89:1997;765-771.
14. North T., Gu T.L., Stacy T., Wang Q., Howard L., Binder M., Marin-Padilla M., Speck N.A. Cbfa2 is required for the formation of intra-aortic hematopoietic clusters. Development. 126:1999;2563-2575.
15. Levanon D., Brenner O., Negreanu V., Bettoun D., Woolf E., Eilam R., Lotem J., Gat U., Otto F., Speck N.et al. Spatial and temporal expression pattern of Runx3 (Aml2) and Runx1 (Aml1) indicates non-redundant functions during mouse embryogenesis. Mech. Dev. 109:2001;413-417.
16. Ghozi M.C., Bernstein Y., Negreanu V., Levanon D., Groner Y. Expression of the human acute myeloid leukemia gene AML1 is regulated by two promoter regions. Proc. Natl. Acad. Sci. USA. 93:1996;1935-1940.
17. Pozner A., Goldenberg D., Negreanu V., Le S.Y., Elroy-Stein O., Levanon D., Groner Y. Transcription-coupled translation control of AML1/RUNX1 is mediated by cap- and internal ribosome entry site-dependent mechanisms. Mol. Cell. Biol. 20:2000;2297-2307.
18. Komori T., Kishimoto T. Cbfa1 in bone development. Curr. Opin. Genet. Dev. 8:1998;494-499.
19. Speck N.A., Stacy T., Wang Q., North T., Gu T.L., Miller J., Binder M., Marin-Padilla M. Core-binding factor. a central player in hematopoiesis and leukemia Cancer Res. 59:1999;1789s-1793s.
20. Karsenty G. Role of Cbfa1 in osteoblast differentiation and function. Semin. Cell Dev. Biol. 11:2000;343-346.
21. Tracey W.D., Speck N.A. Potential roles for RUNX1 and its orthologs in determining hematopoietic cell fate. Semin. Cell Dev. Biol. 11:2000;337-342.
22. Levanon D., Bettoun D., Harris-Cerruti C., Woolf E., Negreanu V., Eilam R., Bernstein Y., Goldenberg D., Xiao C., Fliegauf M.et al. The Runx3 transcription factor regulates development and survival of TrkC dorsal root ganglia neurons. EMBO J. 21:2002;3454-3463.
23. Berardi M.J., Sun C., Zehr M., Abildgaard F., Peng J., Speck N.A., Bushweller J.H. The Ig fold of the core binding factor alpha Runt domain is a member of a family of structurally and functionally related Ig-fold DNA-binding domains. Struct. 7:1999;1247-1256.
24. Nagata T., Gupta V., Sorce D., Kim W.Y., Sali A., Chait B.T., Shigesada K., Ito Y., Werner M.H. Immunoglobulin motif DNA recognition and heterodimerization of the PEBP2/CBF Runt domain. Nat. Struct. Biol. 6:1999;615-619.
25. Goger M., Gupta V., Kim W.Y., Shigesada K., Ito Y., Werner M.H. Molecular insights into PEBP2/CBF beta-SMMHC associated acute leukemia revealed from the structure of PEBP2/CBF beta. Nat. Struct. Biol. 6:1999;620-623.
26. Huang X., Peng J.W., Speck N.A., Bushweller J.H. Solution structure of core binding factor and map of the CBF binding site. Nat. Struct. Biol. 6:1999;624-627.
27. Wolf-Watz M., Grundstrom T., Hard T. Structure and backbone dynamics of Apo-CBFbeta in solution. Biochemistry. 40:2001;11423-11432.
28. Warren A.J., Bravo J., Williams R.L., Rabbitts T.H. Structural basis for the heterodimeric interaction between the acute leukaemia-associated transcription factors AML1 and CBFbeta. EMBO J. 19:2000;3004-3015.
29. Tahirov T.H., Inoue-Bungo T., Morii H., Fujikawa A., Sasaki M., Kimura K., Shiina M., Sato K., Kumasaka T., Yamamoto M.et al. Structural analyses of DNA recognition by the AML1/Runx-1 Runt domain and its allosteric control by CBFbeta. Cell. 104:2001;755-767.
30. Bravo J., Li Z., Speck N.A., Warren A.J. The leukemia-associated AML1 (Runx1)-CBF beta complex functions as a DNA-induced molecular clamp. Nat. Struct. Biol. 8:2001;371-378.
31. Nagata T., Werner M.H. Functional mutagenesis of AML1/RUNX1 and PEBP2 beta/CBF beta define distinct, non-overlapping sites for DNA recognition and heterodimerization by the Runt domain. J. Mol. Biol. 308:2001;191-203.
32. Perez-Alvarado G.C., Munnerlyn A., Dyson H.J., Grosschedl R., Wright P.E. Identification of the regions involved in DNA binding by the mouse PEBP2alpha protein. FEBS Lett. 470:2000;125-130.
33. Tang Y.Y., Crute B.E., Kelley J.J., Huang X., Yan J., Shi J., Hartman K.L., Laue T.M., Speck N.A., Bushweller J.H. Biophysical characterization of interactions between the core binding factor alpha and beta subunits and DNA. FEBS Lett. 470:2000;167-172.
34. Akamatsu Y., Tsukumo S., Kagoshima H., Tsurushita N., Shigesada K. A simple screening for mutant DNA binding proteins. application to murine transcription factor PEBP2alpha subunit, a founding member of the Runt domain protein family Gene. 185:1997;111-117.
35. Lee B., Thirunavukkarasu K., Zhou L., Pastore L., Baldini A., Hecht J., Geoffroy V., Ducy P., Karsenty G. Missense mutations abolishing DNA binding of the osteoblast-specific transcription factor OSF2/CBFA1 in cleidocranial dysplasia. Nat. Genet. 16:1997;307-310.
36. Quack I., Vonderstrass B., Stock M., Aylsworth A.S., Becker A., Brueton L., Lee P.J., Majewski F., Mulliken J.B., Suri M.et al. Mutation analysis of core binding factor A1 in patients with cleidocranial dysplasia. Am. J. Hum. Genet. 65:1999;1268-1278.
37. Zhou G., Chen Y., Zhou L., Thirunavukkarasu K., Hecht J., Chitayat D., Gelb B.D., Pirinen S., Berry S.A., Greenberg C.R.et al. CBFA1 mutation analysis and functional correlation with phenotypic variability in cleidocranial dysplasia. Hum. Mol. Genet. 8:1999;2311-2316.
38. Garvie C.W., Wolberger C. Recognition of specific DNA sequences. Mol. Cell. 8:2001;937-946.
39. Li L.H., Gergen J.P. Differential interactions between Brother proteins and Runt domain proteins in the Drosophila embryo and eye. Development. 126:1999;3313-3322.
40. Osato M., Asou N., Abdalla E., Hoshino K., Yamasaki H., Okubo T., Suzushima H., Takatsuki K., Kanno T., Shigesada K.et al. Biallelic and heterozygous point mutations in the runt domain of the AML1/PEBP2alphaB gene associated with myeloblastic leukemias. Blood. 93:1999;1817-1824.
41. Song W.J., Sullivan M.G., Legare R.D., Hutchings S., Tan X., Kufrin D., Ratajczak J., Resende I.C., Haworth C., Hock R.et al. Haploinsufficiency of CBFA2 causes familial thrombocytopenia with propensity to develop acute myelogenous leukaemia. Nat. Genet. 23:1999;166-175.
42. Imai Y., Kurokawa M., Izutsu K., Hangaishi A., Takeuchi K., Maki K., Ogawa S., Chiba S., Mitani K., Hirai H. Mutations of the AML1 gene in myelodysplastic syndrome and their functional implications in leukemogenesis. Blood. 96:2000;3154-3160.
43. Preudhomme C., Warot-Loze D., Roumier C., Grardel-Duflos N., Garand R., Lai J.L., Dastugue N., Macintyre E., Denis C., Bauters F.et al. High incidence of biallelic point mutations in the Runt domain of the AML1/PEBP2 alpha B gene in Mo acute myeloid leukemia and in myeloid malignancies with acquired trisomy 21. Blood. 96:2000;2862-2869.
44. Michaud J., Wu F., Osato M., Cottles G.M., Yanagida M., Asou N., Shigesada K., Ito Y., Benson K.F., Raskind W.H.et al. In vitro analyses of known and novel RUNX1/AML1 mutations in dominant familial platelet disorder with predisposition to acute myelogenous leukemia. implications for mechanisms of pathogenesis Blood. 99:2002;1364-1372.
45. Shakked Z., Guzikevich-Guerstein G., Frolow F., Rabinovich D., Joachimiak A., Sigler P.B. Determinants of repressor/operator recognition from the structure of the trp operator binding site. Nature. 368:1994;469-473.
46. Rozenberg H., Rabinovich D., Frolow F., Hegde R.S., Shakked Z. Structural code for DNA recognition revealed in crystal structures of papillomavirus E2-DNA targets. Proc. Natl. Acad. Sci. USA. 95:1998;15194-15199.
47. Hizver J., Rozenberg H., Frolow F., Rabinovich D., Shakked Z. DNA bending by an adenine-thymine tract and its role in gene regulation. Proc. Natl. Acad. Sci. USA. 98:2001;8490-8495.
48. Eisenstein M., Shakked Z. Hydration patterns and intermolecular interactions in A-DNA crystal structures. Implications for DNA recognition. J. Mol. Biol. 248:1995;662-678.
49. Crute B.E., Lewis A.F., Wu Z., Bushweller J.H., Speck N.A. Biochemical and biophysical properties of the core-binding factor alpha2 (AML1) DNA-binding domain. J. Biol. Chem. 271:1996;26251-26260.
50. Gu T.L., Goetz T.L., Graves B.J., Speck N.A. Auto-inhibition and partner proteins, core-binding factor beta (CBFbeta) and Ets-1, modulate DNA binding by CBFalpha2 (AML1). Mol. Cell. Biol. 20:2000;91-103.
51. Golling G., Li L., Pepling M., Stebbins M., Gergen J.P. Drosophila homologs of the proto-oncogene product PEBP2/CBF beta regulate the DNA-binding properties of Runt. Mol. Cell. Biol. 16:1996;932-942.
52. Olson W.K., Gorin A.A., Lu X.J., Hock L.M., Zhurkin V.B. DNA sequence-dependent deformability deduced from protein-DNA crystal complexes. Proc. Natl. Acad. Sci. USA. 95:1998;11163-11168.
53. Otwinowski Z., Minor W. Processing of X-ray diffraction data collected in oscillation mode. Carter C.W. Jr., Sweet R.M. Methods in Enzymology, Volume 276. Macromolecular Crystallography, Part A:1997;307-326 Academic Press, New York.
54. Rabinovich D., Rozenberg H., Shakked Z. Molecular replacement. the revival of the molecular Fourier transform method Acta Crystallogr. D Biol. Crystallogr. 54:1998;1336-1342.
55. Brunger 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 and NMR system. a new software suite for macromolecular structure determination Acta Crystallogr. D Biol. Crystallogr. 54:1998;905-921.
56. Rabinovich D., Shakked Z. A new approach to structure determination of large molecules by multidimensional search methods. Acta Crystallogr. A. 40:1984;195-200.
57. Chandrasekaran R., Arnott S. The structure of B-DNA in oriented fibers. J. Biomol. Struct. Dyn. 13:1996;1015-1027.
58. Kraulis P.J. Molscript. a program to produce both detailed and schematic plots of protein structures J. Appl. Crystallogr. 24:1991;946-950.
59. Merritt E.A., Murphy M.E.P. Raster3D Version 2.0. A program for photorealistic molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 50:1994;869-873.
60. Dickerson R.E. DNA bending. the prevalence of kinkiness and the virtues of normality Nucleic Acids Res. 26:1998;1906-1926.