Analysis of the solution structure of the homeodomain of rat thyroid transcription factor 1 by 1H-NMR spectroscopy and restrained molecular mechanics

European Journal of Biochemistry

Volumn 241, Issue 1, 1996, Pages 101-113

  Esposito, Gennaro ^a   Fogolari, Federico ^a   Damante, Giuseppe ^a   Formisano, Silvestro ^a   Tell, Gianluca ^a   Leonardi, Antonio ^a   Di Lauro, Roberto ^a   Viglino, Paolo ^a  

^a UNIVERSITY OF UDINE   (Italy)

Author keywords

DNA binding protein; Helix turn helix motif; Homeodomain structure; Protein NMR; Thyroid transcription factor 1 homeodomain

Indexed keywords

TRANSCRIPTION FACTOR;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ESCHERICHIA COLI; GENE EXPRESSION; MOLECULAR CLONING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN STRUCTURE; RAT; THYROID GLAND;

ANIMALIA; ESCHERICHIA COLI;

EID: 0029825305     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1432-1033.1996.0101t.x     Document Type: Article

References (68)

1. 1 baseline distortion and optimization of folding in multidimensional NMR spectra, J. Magn. Reson. 91, 174-178.
2. Bazzo, R. & Campbell, I. D. (1988) Pure-phase 2D homonuclear cross-polarization spectroscopy in liquids, J. Magn. Reson. 76, 358-361.
3. Bell, J. A., Becktel, W. J., Sauer, U., Baase, W. A. & Matthews, B. W. (1992) Dissection of helix capping in T4 lysozyme by structural and thermodynamic analysis of six amino acid substitutions at Thr59. Biochemistry 31, 3590-3596.
4. 1H nuclear magnetic resonance spectroscopy, J. Mol. Biol. 214, 183-197.
5. Billeter, M., Qian, Y. Q., Otting, G., Müller, M., Gehring, W. J. & Wüthrich, K. (1993) Determination of the nuclear magnetic resonance solution structure of an Antennapedia-DNA complex, J. Mol. Biol. 234, 1084-1097.
6. Bohinski, R. J., Di Lauro, R. & Whitselt, J. A. (1994) The lung-specific surfactant protein B gene promoter is a target for thyroid transcription factor 1 and hepatocyte nuclear factor 3. indicating common factors for organ-specific gene expression along the foregut axis. Mol. Cell Biol. 14, 5671-5681.
7. Braunschweiler, L. & Ernst, R. R. (1983) Coherence transfer by isotropic mixing : application to proton correlation spectroscopy, J. Magn. Reson. 53, 521-528.
8. Braunschweiler, L., Bodenhausen, G. & Ernst, R. R. (1983) Analysis of networks of coupled spins by multiple quantum NMR, Mol. Phys. 48, 535-560.
9. Ceska, T. A., Lamers, M., Monaci, P., Nicosia, A., Cortese, R. & Suck, D. (1993) The X-ray structure of an atypical homeodomain present in the rat liver factor LFB1/HNF1 and implications for DNA binding, EMBO J. 12, 1805-1810.
10. Clarke, N. D. (1995) Covariation of residues in homeodomain sequence family, Protein Sci. 4, 2269-2278.
11. Cox, M., van Tilborg, P. J. A., de Laat, W., Boelens, R., van Leeuwen, H. C., van der Vliet, P C. & Kaptein, R. (1995) Solution structure of the oct-1 POU homeodomain determined by NMR and restrained molecular dynamics, J. Biomol. NMR 6, 23-32.
12. Damante, G. & Di Lauro, R. (1991) Several regions of Antennapedia and thyroid transcription factor 1 homeodomains contribute to DNA binding specificity, Proc. Natl Acad Sci. USA 88, 5388-5392.
13. Damante, G., Tell, G., Formisano, S., Fabbro, D., Pellizzari, L. & Di Lauro, R. (1993) Effect of salt concentration on TTF-1 HD binding to specific and non-specific DNA sequences. Biochem. Biophys. Res. Commun. 197, 632-638.
14. Damante, G., Fabbro, D., Pellizzari, L., Civitareale, D., Guazzi, S., Poly-carpou-Schwarlz, M., Cauci, S., Quadrifoglio, F., Formisano, S. & Di Lauro, R. (1994) Sequence-specific DNA recognition by the thyroid transcription factor 1 homeodomain. Nucleic Acids Res. 22, 3075-3083.
15. Damante, G.. Tell, G., Leonardi, A., Fogolari, F., Bortolotti, N., Di Lauro, R. & Formisano, S. (1994b) Analysis of the conformational stability of rat TTF-1 homeodomain by circular dichroism. FERS Lett. 354, 293-296.
16. Damante, G., Pellizzari, L., Esposito, G., Fogolari, F., Viglino, P., Fabbro, D., Tell. G., Formisano, S. & Di Lauro, R. (1996) A molecular code dictates sequence-specific recognition by homeodomains. EMBO J. in the press.
17. Dayringer, H. E., Tramontano, A., Sprang, S. R. & Flelterick, R. J. (1986) Interactive program for visualization and modelling of proteins. nucleic acids and small molecules, J. Mol. Graphics 6, 82-87.
18. 1H-NMR spectra of ferrichrome. I. The non-amide protons, Biopolymers 17, 617-636.
19. 1H NMR spectra of proteins, Biochemistry 26, 5953-5958.
20. Ernst, R. R., Bodenhausen, G. & Wokaun. A. (1987) Principles of nuclear magnetic resonance in one and two dimensions, Clarendon Press, Oxford.
21. 1H NMR study of the solution structure of alamethicin. Biochemistry 26, 1043-1050.
22. Esposito, G. & Pastore, A. (1988) An alternative method for distance evaluation from NOESY spectra. J. Magn. Reson. 76, 331-336.
23. Esposito, G., Gibbons, W. A. & Bazzo, R. (1988) Phase coherence and solvent suppression in rotating-frame correlation experiments in liquids, J. Magn. Reson. 80, 523-527.
24. Fogolari, F., Esposito, G., Viglino, P., Damante, G. & Pastore, A. (1993) Homology model building of the thyroid transcription factor 1 homeodomain. Protein Eng. 6, 513-519.
25. Gehring, W. J. (1987) Homeo boxes in the study of development, Science 236, 1245-1252.
26. Gehring, W. J., Affolter, M. & Bürglin, T. (1994a) Homeodomain proteins, Annu. Rev. Biochem. 63, 487-526.
27. Gehring, W. J., Qian, Y. Q., Billcter, M., Furukubo-Tokunaga, K., Schier, A. F., Resendez-Perez, D., Affolter, M., Otting, G. & Wüthrich, K. (1994b) Homeodomain-DNA recognition, Cell 78, 211-223.
28. 1H spin system identification in macromolecules, J Am. Chem. Soc. 110, 7870-7872.
29. Guazzi, S., Price, M., De Felice, M., Damante, G., Mattei, M.-G. & Di Lauro, R. (1990) Thyroid nuclear factor 1 (TTF-1) contains a homeodomain and displays a novel DNA binding specificity. EMBO J. 9, 3631-3639.
30. Güntert, P., Braun, W. & Wüthrich, K. (1991a) Efficient computation of three-dimensional protein structure in solution from nuclear magnetic resonance data using the program DIANA and the supporting programs CALIBA. HABAS and GLOMSA. J. Mol. Biol. 217, 517-530.
31. Güntert, P., Qian, Y. Q., Otting, G., Müller, M., Gehring, W. J. & Wüthrich, K. (1991b) Structure determination of the Antp(C39S) homeodomain from nuclear magnetic resonance data in solution using a novel trategy for the structure calculation with the programs DIANA, ALIBA, HABAS and GLOMSA, J. Mol. Biol. 217, 531 540.
32. Jeener, J., Meier, B. H., Bachmann, P. & Ernst, R. R. (1979) Investigation of exchange processes by two-dimensional NMR spectroscopy, J. Chem. Phys. 71, 4546-4553.
33. Kissinger, C. R., Liu, B., Martin-Blanco, E., Kornberg, T. B. & Pabo, C. O. (1990) Crystal structure of an engrailed homeodomain-DNA complex at 2.8 Å resolution: a framework for understanding homeodomain-DNA interactions. Cell 63, 579-590.
34. Klemm, J. D., Rould, M. A., Aurora, R., Herr, W. & 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.
35. Leiting, B., De Francesco, R., Tomei, L., Cortese, R., Otting, G. & Wüthrich K. (1993) The three-dimensional NMR-solution structure of the polypeptide fragment 195-286 of the LFB1/HNF1 transcription factor from rat liver comprises a non-classical homeodomain, EMBO J. 12, 1797-1803.
36. Levitt, M. & Perutz, M. F. (1988) Aromatic rings as hydrogen bond acceptors. J. Mol. Biol. 201, 751-754.
37. Marion, D. & Bax, A. (1989) Baseline correction in 2D FT NMR spectra using a simple linear prediction extrapolation of the time-domain data, J. Magn. Reson. 83, 205-211.
38. Marion, D. & Wüthrich, K. (1983) Application of phase sensitive two-dimensional correlated spectroscopy (COSY) for measurements of proton-proton spin-spin coupling constants in proteins, Biochem. Biophys. Res. Commun. 113, 967-974.
39. McGregor, M. J., Islam, S. A. & Sternberg, M. J. E. (1987) Analysis of the relationship between side-chain conformation and secondary structure in globular proteins, J. Mol. Biol. 198, 295-310.
40. Molday, R. S., Englander, S. W. & Kallen, R. G. (1972) Primary structure effects on peptide group hydrogen exchange, Biochemistry II, 150-158.
41. 15N NMR spectroscopy, FEBS Lett. 321, 107-110.
42. Morris, G. A. & Freeman, R. (1978) Selective excitation in Fourier transform nuclear magnetic resonance, J. Magn. Reson. 29, 433 - 462.
43. Müller, M., Affolter, M., Leupin, W., Otting, G., Wüthrich, K. & Gehring, W. J. (1988) Isolation and sequence-specific DNA binding of the Antennapedia homeodomain, EMBO J. 7, 4299-4304.
44. 1H-NMR techniques for the identification of the ami no-acid-proton spin systems in proteins, Eur. J. Biochem. 151, 257-273.
45. Otting, G., Qian, Y. Q., Billeter, M., Müller, M., Affolter, M., Gehring, W. J. & Wüthrich, K. (1988) Secondary structure determination for the Antannapedia homeodomain by nuclear magnetic resonance and evidence for a helix-turn-helix motif, EMBO J. 7, 4305-4309.
46. Otting, G., Qian, Y. Q., Billeter, M., Müller, M., Affolter, M., Gehring, W. J. & Wüthrich, K. (1990) Protein-DNA contacts in the structure of a homeodomain-DNA complex determined by nuclear magnetic resonance spectroscopy in solution, EMBO J. 9, 3085-3092.
47. Pabo, C. O. & Sauer, R. T. (1992) Transcription factors: structural families and principles of DNA recognition, Annu. Rev. Biochem. 61, 1053-1095.
48. Phillips, C. L., Vershon, A. K., Johnson, A. D. & Dahlquist, F. W. (1991) Secondary structure of the homeodomain of yeast α2 repressor determined by NMR spectroscopy. Genes & Dev. 5, 764-772.
49. Piantini, U., Sørensen, O. W. & Ernst, R. R. (1982) Multiple quantum filters for elucidating NMR coupling networks, J. Am. Chem Soc. 104, 6800-6801.
50. Presta, L. G. & Rose, G. D. (1988) Helix signals in proteins, Science 240, 1632-1641.
51. Qian, Y. Q., Billeter, M., Otting, G., Müller, M., Gehring, W. J. & Wüthrich, K. (1989) The structure of the Antennapedia homeodomain determined by NMR spectroscopy in solution: comparison with prokaryotic repressors, Cell 59, 573-580.
52. 13C-labeled Antennapedia homeodomain, J. Mol. Biol. 234, 1070-1083.
53. Qian, Y. Q., Furukubo-Tokunaga, K., Resendez-Perez, D., M., Müller, M., Gehring, W. J. & Wüthrich, K. (1994) Nuclear magnetic resonance solution structure of the fushi tarazu homeodomain from Drosophila and comparison with the Antennapedia homeodomain, J. Mol. Biol. 238, 333-345.
54. Richardson, J. S. (1981) The anatomy and taxonomy of protein structure, Adv. Protein Chem. 34, 167-339.
55. Richardson, J. S. & Richardson, D. C. (1988) Amino acid preferences for specific locations at ends of α helices, Science 240, 1648-1652.
56. Shaka, A. J., Keeler, J. & Freeman, R. (1983) Evaluation of a new broad-band decoupling sequence: WALTZ-16, J. Magn. Reson. 53, 313-340.
57. Sivaraja, M., Botfield, M. C., Mueller, M., Jancso, A. & Weiss, M. A. (1994) Solution structure of a POU-specific homeodoamin: 3D-NMR studies of human B-cell transcription factor oct-2. Biochemistry 33, 9845-9855.
58. Tsao, D. H. H., Gruschus, J. M., Wang, L.-H., Nirenberg, M. & Ferretti, J. A. (1994) Elongation of helix III of the NK-2 homeodomain upon binding to DNA: a secondary structure study by NMR, Biochemistry 33, 15 053-15 060.
59. Viglino, P., Fogolari, F., Formisano, S., Bortolotti, N., Damante, G., Di Lauro, R. & Esposito, G. (1993) Structural study of rat thyroid transcription factor 1 homeodomain (TTF-1 homeodomain) by nuclear magnetic resonance, FEBS Lett. 336, 397-402.
60. Vriend, G. (1990) WHAT IF: a molecular modeling and drug design program, J. Mol. Graphics 8, 52-56.
61. Wagner G., Hyberts, S. G. & Havel, T. F. (1992) NMR structure determination in solution: a critique and comparison with X-ray crystallography, Annu. Rev. Biophys. Biomol. Struct. 21, 167-198.
62. Weiner, S. J., Kollman, P. A., Case, D. A., Singh, U. C., Ghio, C., Alagona, G., Profeta, S. Jr & Weiner, P. (1984) A new force field for molecular mechanical simulation of nucleic acids and proteins, J. Am. Chem. Soc. 106, 765-784.
63. Wolberger, C., Vershon, A. K., Liu, B., Johnson, A. D. & Pabo, C. O. (1991) Crystal structure of MATα2 homeodomain - operator complex suggests a general model for homeodomain-DNA interactions, Cell 67, 517-528.
64. Wüthrich, K. (1986) NMR of proteins and nucleic acids. Wiley, New York.
65. Wüthrich, K., Billeter, M. & Braun, W. (1983) Pseudo-structures for the 20 common amino acids for use in studies of protein conformations by measurements of intramolecular proton-proton distance constraints with nuclear magnetic resonance, J. Mol. Biol. 169, 949-961.
66. Xu, W., Rould, M. A., Jun, S., Desplan, C. & Pabo, C. O. (1995) Crystal structure of a Paired domain - DNA complex at 2. 5 Å resolution reveals structural basis for Pax developmental mutations, Cell 80, 639-650.
67. Zhou, H. X., Pinker, R. J. & Kallenbach, N. R. (1993) Capping interactions in isolated α helices. Position dependent substitution effects and structure of a serine-capped peptide helix, Biochemistry 32, 421-425.
68. Zimmerman, S. S., Pottle, M. S., Nemethy, G. & Scheraga, H. A. (1977) Conformational analysis of the 20 naturally occurring amino acid residues using ECEPP, Macromolecules 10, 1-9.