Crystal structure of a POU/HMG/DNA ternary complex suggests differential assembly of Oct4 and Sox2 on two enhancers

Genes and Development

Volumn 17, Issue 16, 2003, Pages 2048-2059

  Reményi, Attila ^a,b,c   Lins, Katharina ^c   Nissen, L Johan ^b   Reinbold, Rolland ^c   Schöler, Hans R ^a,c   Wilmanns, Matthias ^b  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^b DESY   (Germany)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Crystal structure; FGF4 and UTF1 enhancers; HMG domain; Oct4; POU domain; Sox2

Indexed keywords

DNA; HIGH MOBILITY GROUP PROTEIN; OCTAMER TRANSCRIPTION FACTOR 4; PROTEIN SOX; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR POU; UNCLASSIFIED DRUG;

ARTICLE; COMPLEX FORMATION; CRYSTAL STRUCTURE; DIMERIZATION; DNA CONFORMATION; EMBRYO DEVELOPMENT; ENHANCER REGION; GENE TARGETING; MOLECULAR MECHANICS; MULTIGENE FAMILY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN STRUCTURE; TRANSCRIPTION REGULATION;

ANIMALS; BASE SEQUENCE; CRYSTALLOGRAPHY, X-RAY; DNA; DNA-BINDING PROTEINS; ENHANCER ELEMENTS (GENETICS); ESCHERICHIA COLI; FIBROBLAST GROWTH FACTORS; HIGH MOBILITY GROUP PROTEINS; HMGB PROTEINS; HUMANS; MICE; MODELS, MOLECULAR; MUTATION; NUCLEAR PROTEINS; NUCLEIC ACID CONFORMATION; OCTAMER TRANSCRIPTION FACTOR-3; PROTEIN CONFORMATION; TRANS-ACTIVATION (GENETICS); TRANS-ACTIVATORS; TRANSCRIPTION FACTORS;

MAMMALIA;

EID: 0042161878     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.269303     Document Type: Article

References (43)

1. Ambrosetti, D.C., Basilico, C., and Dailey, L. 1997. Synergistic activation of the fibroblast growth factor 4 enhancer by Sox2 and Oct-3 depends on protein-protein interactions facilitated by a specific spatial arrangement of factor binding sites. Mol. Cell. Biol. 17: 6321-6329.
2. Ambrosetti, D.C., Scholer, H.R., Dailey, L., and Basilico, C. 2000. Modulation of the activity of multiple transcriptional activation domains by the DNA binding domains mediates the synergistic action of Sox2 and Oct-3 on the fibroblast growth factor-4 enhancer. J. Biol. Chem. 275: 23387-23397.
3. Avilion, A.A., Nicolis, S.K., Pevny, L.H., Perez, L., Vivian, N., and Lovell-Badge, R. 2003. Multipotent cell lineages in early mouse development depend on SOX2 function. Genes & Dev. 17: 126-140.
4. Botquin, V., Hess, H., Fuhrmann, G., Anastassiadis, C., Gross, M.K., Vriend, G., and Scholer, H.R. 1998. New POU dimer configuration mediates antagonistic control of an osteopontin preimplantation enhancer by Oct-4 and Sox-2. Genes & Dev. 12: 2073-2090.
5. 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. 1998. Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54: 905-921.
6. Chasman, D., Cepek, K., Sharp, P.A., and Pabo, C.O. 1999. Crystal structure of an OCA-B peptide bound to an Oct-1 POU domain/octamer DNA complex: Specific recognition of a protein-DNA interface. Genes & Dev. 13: 2650-2657.
7. Dailey, L. and Basilico, C. 2001. Coevolution of HMG domains and homeodomains and the generation of transcriptional regulation by Sox/POU complexes. J. Cell Physiol. 186: 315-328.
8. Dailey, L., Yuan, H., and Basilico, C. 1994. Interaction between a novel F9-specific factor and octamer-binding proteins is required for cell-type-restricted activity of the fibroblast growth factor 4 enhancer. Mol. Cell. Biol. 14: 7758-7769.
9. De Santa Barbara, P., Bonneaud, N., Boizet, B., Desclozeaux, M., Moniot, B., Sudbeck, P., Scherer, G., Poulat, F., and Berta, P. 1998. Direct interaction of SRY-related protein SOX9 and steroidogenic factor 1 regulates transcription of the human anti-Mullerian hormone gene. Mol. Cell. Biol. 18: 6653-6665.
10. Herr, W. and Cleary, M.A. 1995. The POU domain: Versatility in transcriptional regulation by a flexible two-in-one DNA-binding domain. Genes & Dev. 9: 1679-1693.
11. Jones, T.A., Zou, J.Y., Cowan, S.W., and Kjeldgaard. 1991. Improved methods for binding protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A 47: 110-119.
12. Kamachi, Y., Cheah, K.S., and Kondoh, H. 1999. Mechanism of regulatory target selection by the SOX high-mobility-group domain proteins as revealed by comparison of SOX1/2/3 and SOX9. Mol. Cell. Biol. 19: 107-120.
13. Kamachi, Y., Uchikawa, M., and Kondoh, H. 2000. Pairing SOX off: With partners in the regulation of embryonic development. Trends Genet. 16: 182-187.
14. Kamachi, Y., Uchikawa, M., Tanouchi, A., Sekido, R., and Kondoh, H. 2001. Pax6 and SOX2 form a co-DNA-binding partner complex that regulates initiation of lens development. Genes & Dev. 15: 1272-1286.
15. Klemm, J.D., Rould, M.A., Aurora, R., Herr, W., and Pabo, C.O. 1994. Crystal structure of the Oct-1 POU domain bound to an octamer site: DNA recognition with tethered DNA-binding modules. Cell 77: 21-32.
16. Kuhlbrodt, K., Herbarth, B., Sock, E., Enderich, J., Hermans-Borgmeyer, I., and Wegner, M. 1998. Cooperative function of POU proteins and SOX proteins in glial cells. J. Biol. Chem. 273: 16050-16057.
17. La Fortelle, E. and Bricogne, G. 1997. Maximum-likelihood heavy-atom parameter refinement in the MIR and MAD method. In Methods in enzymology, macromolecular crystallography (eds. R.M. Sweet and C.W.J. Carter), pp. 472-494. Academic Press, New York.
18. Lavery, R. and Sklenar, H. 1988. The definition of generalized helicoidal parameters and of axis curvature for irregular nucleic acids. J. Biomol. Struct. Dyn. 6: 63-91.
19. Love, J.J., Li, X., Case, D.A., Giese, K., Grosschedl, R., and Wright, P.E. 1995. Structural basis for DNA bending by the architectural transcription factor LEF-1. Nature 376: 791-795.
20. Mansouri, A., Hallonet, M., and Gruss, P. 1996. Pax genes and their roles in cell differentiation and development. Curr. Opin. Cell Biol. 8: 851-857.
21. Mertin, S., McDowall, S.G., and Harley, V.R. 1999. The DNA-binding specificity of SOX9 and other SOX proteins. Nucleic Acids Res. 27: 1359-1364.
22. Murphy, F.V.T. and Churchill, M.E. 2000. Nonsequence-specific DNA recognition: A structural perspective. Structure Fold Des. 8: R83-R89.
23. Murphy, F.V.T., Sweet, R.M., and Churchill, M.E. 1999. The structure of a chromosomal high mobility group protein-DNA complex reveals sequence-neutral mechanisms important for non-sequence-specific DNA recognition. EMBO J. 18: 6610-6618.
24. Navaza, J. 1994. AMoRe: An automated package for molecular replacement. Acta Crystallogr. A 50: 157-163.
25. Nichols, J., Zevnik, B., Anastassiadis, K., Niwa, H., Klewe-Nebenius, D., Chambers, I., Scholer, H., and Smith, A. 1998. Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell 95: 379-391.
26. Nishimoto, M., Fukushima, A., Okuda, A., and Muramatsu, M. 1999. The gene for the embryonic stem cell coactivator UTF1 carries a regulatory element which selectively interacts with a complex composed of Oct-3/4 and Sox-2. Mol. Cell. Biol. 19: 5453-5465.
27. Niwa, H., Miyazaki, J., and Smith, A.G. 2000. Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nat. Genet. 24: 372-376.
28. Okuda, A., Fukushima, A., Nishimoto, M., Orimo, A., Yamagishi, T., Nabeshima, Y., Kuro-o, M., Boon, K., Keaveney, M., Stunnenberg, H.G., et al. 1998. UTF1, a novel transcriptional coactivator expressed in pluripotent embryonic stem cells and extra-embryonic cells. EMBO J. 17: 2019-2032.
29. Otwinowski, Z. and Minor, W. 1997. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymology A 276: 307-325.
30. Pevny, L.H. and Lovell-Badge, R. 1997. Sox genes find their feet. Curr. Opin. Genet. Dev. 7: 338-344.
31. Reményi, A., Pohl, E., Scholer, H.R., and Wilmanns, M. 2001a. Crystallization of redox-insensitive Octl POU domain with different DNA-response elements. Acta Crystallogr. D Biol. Crystallogr. 57: 1634-1638.
32. Reményi, A., Tomilin, A., Pohl, E., Lins, K., Philippsen, A., Reinbold, R., Scholer, H.R., and Wilmanns, M. 2001b. Differential dimer activities of the transcription factor Oct-1 by DNA-induced interface swapping. Mol. Cell 8: 569-580.
33. Reményi, A., Tomilin, A., Scholer, H.R., and Wilmanns, M. 2002. Differential activity by DNA-induced quarternary structures of POU transcription factors. Biochem. Pharmacol. 64: 979-984.
34. Schoorlemmer, J. and Kruijer, W. 1991. Octamer-dependent regulation of the kFGF gene in embryonal carcinoma and embryonic stem cells. Mech. Dev. 36: 75-86.
35. Scully, K.M., Jacobson, E.M., Jepsen, K., Lunyak, V., Viadiu, H., Carriere, C., Rose, D.W., Hooshmand, F., Aggarwal, A.K., and Rosenfeld, M.G. 2000. Allosteric effects of Pit-1 DNA sites on long-term repression in cell type specification. Science 290: 1127-1131.
36. Sheldrick, G.M. 1998. SHELX: Application to macromolecules. In Direct methods for solving macromolecular structures (ed. S. Fortier), pp. 401-411. Kluwer Academic Publishers, Dordrecht.
37. Soriano, N.S. and Russell, S. 1998. The Drosophila SOX-domain protein Dichaete is required for the development of the central nervous system midline. Development 125: 3989-3996.
38. Tomilin, A., Reményi, A., Lins, K., Bak, H., Leidel, S., Vriend, G., Wilmanns, M., and Scholer, H.R. 2000. Synergism with the coactivator OBF-1 (OCA-B, BOB-1) is mediated by a specific POU dimer configuration. Cell 103: 853-864.
39. Vriend, G. 1990. WHATIF: A molecular modeling and drug design program. J. Mol. Graph. 8: 52-56.
40. Wegner, M. 1999. From head to toes: The multiple facets of Sox proteins. Nucleic Acids Res. 27: 1409-1420.
41. Werner, M.H., Huth, J.R., Gronenborn, A.M., and Clore, G.M. 1995. Molecular basis of human 46X,Y sex reversal revealed from the three-dimensional solution structure of the human SRY-DNA complex. Cell 81: 705-714.
42. Yeom, Y.I., Fuhrmann, G., Ovitt, C.E., Brehm, A., Ohbo, K., Gross, M., Hubner, K., and Scholer, H.R. 1996. Germline regulatory element of Oct-4 specific for the totipotent cycle of embryonal cells. Development 122: 881-894.
43. Yuan, H., Corbi, N., Basilico, C., and Dailey, L. 1995. Developmental-specific activity of the FGF-4 enhancer requires the synergistic action of Sox2 and Oct-3. Genes & Dev. 9: 2635-2645.