The solution structure of the homeodomain of the rat insulin-gene enhancer protein Isl-1. Comparison with other homeodomains

Journal of Molecular Biology

Volumn 288, Issue 4, 1999, Pages 689-703

  Ippel, Hans ^a   Larsson, Göran ^a   Behravan, Gity ^a   Zdunek, Janusz ^a   Lundqvist, Martin ^a   Schleucher, Jürgen ^a   Lycksell, Per Olof ^a   Wijmenga, Sybren ^a  

^a UMEÅ UNIVERSITY   (Sweden)

Author keywords

Homeodomain; Isl 1; NMR spectroscopy; Protein structure; Transcription factor

Indexed keywords

DNA; DNA BINDING PROTEIN; HOMEODOMAIN PROTEIN; INSULIN; INSULIN GENE ENHANCER PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DNA BINDING; RAT; SEQUENCE HOMOLOGY; THERMOSTABILITY;

EUKARYOTA; MAMMALIA;

EID: 0032967237     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1999.2718     Document Type: Article

References (64)

1. Ahlgren U., Pfaff S. L., Jessell T. M., Edlund T., Edlund H. Independent requirement for ISL-1 in formation of pancreatic mesenchyme and islet cells. Nature. 385:1997;257-260.
2. Behravan G., Lycksell P.-O., Larsson G. Expression, purification and characterization of the homeodomain of rat Isl-1 protein. Protein Eng. 10:1997;1327-1331.
3. 1H nuclear magnetic resonance spectroscopy. J. Mol. Biol. 214:1990;183-197.
4. Billeter M., Qian Y. Q., Otting G., Muller M., Gehring W., Wüthrich K. Determination of the nuclear magnetic resonance solution structure of an Antennapedia homeodomain-DNA complex. J. Mol. Biol. 234:1993;1084-1094.
5. Borgias B. A., James T. L. Two-dimensional nuclear Overhauser effect-complete relaxation matrix analysis. Methods Enzymol. 176:1989;169-183.
6. Brünger A. T. X-PLOR. A System for X-ray Crystallography and NMR. 1992;Yale University Press, New Haven.
7. Ceska T. A., Lamers M., Monaci P., Nicosia A., Cortese R., Suck D. The X-ray structure of an atypical homeodomain present in the rat-liver transcription factor LFB1 HNF1 and implications for DNA-binding. EMBO J. 12:1993;1805-1810.
8. Clarke N. D., Kissinger C. R., Desjarlais J., Gilliland G. L., Pabo C. O. Structural studies of the engrailed homeodomain. Protein Sci. 3:1994;1779-1787.
9. Cox M., Van Tilborg P. J. A., De Laat W., Boelens R., Van Leeuwen H. C., Van der Vliet P. C., Kaptein R. Solution structure of the Oct-1 POU homeodomain determined by NMR and restrained molecular-dynamics. J. Biomol. NMR. 6:1995;23-32.
10. Damante G., Tell G., Leonardi A., Fogolari F., Bortolotti N., Dilauro R., Formisano S. Analysis of the conformation and stability of rat TTF-1 homeodomain by circular dichroism. FEBS Letters. 354:1994;293-296.
11. Esposito G., Fogolari F., Damante G., Formisano S., Tell G., Leonardi A., DiLauro R., Viglino P. Analysis of the solution structure of the homeodomain of rat thyroid transcription factor 1 by H-1-NMR spectroscopy and restrained molecular mechanics. Eur. J. Biochem. 241:1996;101-113.
12. Fernandez C., Szyperski T., Ono A., Iwai H., Tate S., Kainosho M., Wüthrich K. NMR with C-13, N-15-doubly-labeled DNA: the Antennapedia homeodomain complex with a 14-mer DNA duplex. J. Biomol. NMR. 12:1998;25-37.
13. Fersht A. Forces between molecules, and enzyme-substrate binding energies. Enzyme Structure and Mechanism. 1985;Freeman & Company, New York. p. 298-301, 306.
14. Folmer R. H. A., Hilbers C. W., Konings R. N. H., Nilges M. Floating stereospecific assignment revisited: application to an 18 kDa protein and comparison with J -coupling data. J. Biomol. NMR. 9:1997;245-258.
15. Fraenkel E., Pabo C. Comparison of X-ray and NMR structures for the Antennapedia homeodomain-DNA complex. Nature Struct. Biol. 5:1998;692-696.
16. Frasch M., Warrior R., Tugwood J., Levine M. Molecular analysis of even-skipped mutants in Drosophila development. Genes Dev. 2:1988;1824-1838.
17. Freyd G., Kim S. K., Horvitz H. R. Novel cysteine-rich motif and homeodomain in the product of the Caenorhabditis elegans cell lineage gene lin-11. Nature. 344:1990;876-879.
18. Gehring W. J., Affolter M., Buerglin T. Homeodomain proteins. Annu. Rev. Biochem. 63:1994a;487-526.
19. Gehring W. J., Qian Y. Q., Billeter M., Furukubo-Tokunaga K., Schier A. F., Resendez-Perez D., Affolter M., Otting G., Wüthrich K. Homeodomain-DNA recognition. Cell. 78:1994b;211-223.
20. Gruschus J. M., Tsao D. H. H., Wang L. H., Nirenberg M., Ferretti J. A. Interactions of the Vnd/NK-2 homeodomain with DNA by nuclear magnetic resonance spectroscopy: basis of binding specificity. Biochemistry. 36:1997;5372-5380.
21. Güntert P., Qian Y. Q., Otting G., Mueller M., Gehring W. J., Wüthrich K. Structure determination of the Antp(C39S) homeodomain from nuclear magnetic resonance data in solution using a novel strategy for the structure calculation with the programs DIANA, CALIBA, HABAS and GLOMSA. J. Mol. Biol. 217:1991;531-540.
22. Heberlein U., Penton A., Falsafi S., Hackett D., Rubin G. M. The C-terminus of the homeodomain is required for functional specificity of the Drosophila rough gene. Mech. Dev. 48:1994;35-49.
23. Hirsch J. A., Aggarwal A. K. Structure of the even-skipped homeodomain complexed to AT-rich DNA: new perspectives on homeodomain specificity. EMBO J. 14:1995;6280-6291.
24. 15N assignment of the Isl-1 homeodomain. J. Biomol. NMR. 12:1998;357-359.
25. Karlsson O., Thor S., Norberg T., Ohlsson H., Edlund T. Insulin gene enhancer binding protein Isl-1 is a member of a novel class of proteins containing both a homeo- and a Cys-His domain. Nature. 344:1990;879-882.
26. Kelley L. A., Gardner S. P., Sutcliffe M. J. An automated approach for clustering an ensemble of NMR-derived protein structures into conformationally-related subfamilies. Protein Eng. 9:1996;1063-1065.
27. Kissinger C. R., Liu B., Martin-Blanco E., Kornborg T. B., Pabo C. O. Crystal structure of an engrailed homeodomain-DNA complex at 2.8 Å resolution: a framework for understanding homeodomain-DNA interactions. Cell. 63:1990;579-590.
28. Klemm J. D., Rould M. A., Aurora R., Herr W., Pabo C. O. Crystal-structure of the Oct-1 POU domain bound to an octamer site-DNA recognition with tethered DNA-binding modules. Cell. 77:1994;21-32.
29. Koehl P., Delarue M. Polar and nonpolar environments in the protein core: implications for folding and binding. Proteins: Struct. Funct. Genet. 20:1994;264-278.
30. Koradi R., Billeter M., Wüthrich K. MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graph. 14:1996;51.
31. Kosa J. L., Michelsen J. W., Louis H. A., Olsen J. I., Davis D. R., Beckerle M. C., Winge D. R. Common metal ion coordination in LIM domain proteins. Biochemistry. 33:1994;468-477.
32. Kuszewski J., Gronenborn A. M., Clore G. M. A potential involving multiple proton chemical-shift restraints for nonstereospecifically assigned methyl and methylene protons. J. Magn. Reson. ser. B. 112:1996;79-81.
33. Laskowski R. A., Rullmann J. A. C., MacArthur M. W., Kaptein R., Thornton J. M. AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J. Biomol. NMR. 8:1996;477-486.
34. Lesser G. J., Le R. H., Zehfus M. H., Rose G. D. Hydrophobic interactions in proteins. Oxender D. L., Fox C. F. Protein Engineering. 1987;175-179 Alan R. Liss Inc. New York.
35. Li T., Stark M. R., Johnson A. D., Wolberger C. Crystal-structure of the Mat α1/Mat α2 homeodomain heterodimer bound to DNA. Science. 270:1995;262-269.
36. Lu G. FIT: a program to compare and superimpose two structures using selected atom types and residues. 1996;Karolinska Inst. Stockholm.
37. McGinnis W., Levine M. S., Hafen E., Kuroiwa A., Gehring W. J. A conserved DNA sequence in homeotic genes of the Drosophila Antennapedia and bithorax complexes. Nature. 308:1984a;428-433.
38. McGinnis W., Hart C. P., Gehring W. J., Ruddle F. H. Molecular cloning and chromosome mapping of a mouse DNA sequence homologeous to homeotic genes ofDrosophila. Cell. 38:1984b;675-680.
39. Michelsen J. W., Schmeichel K. L., Beckerle M. C., Winge D. R. The LIM motif defines a specific zinc-binding protein domain. Proc. Natl Acad. Sci. USA. 90:1993;4404-4408.
40. Morita E. H., Shirakawa M., Hayashi F., Imagawa M., Kyogoku Y. Structure of the Oct-3 POU-homeodomain in solution, as determined by triple-resonance heteronuclear multidimensional NMR-spectroscopy. Protein Sci. 4:1995;729-739.
41. Nilges M. A calculation strategy for the structure determination of symmetrical dimers by H-1-NMR. Proteins: Struct. Funct. Genet. 17:1993;297-309.
42. Otting G., Qian Y. Q., Billeter M., Müller M., Affolter M., Gehring W. J., Wüthrich K. Protein-DNA contacts in the structure of a homeodomain-DNA complex determined by nuclear magnetic resonance spectroscopy in solution. EMBO J. 9:1990;3085-3092.
43. Pfaff S. L., Mendelsohn M., Stewart C. L., Edlund T., Jessell T. M. Requirement for LIM homeobox gene Isl-1 in motor neuron generation reveals a motor neuron-dependent step in interneuron differentiation. Cell. 84:1996;309-320.
44. Qian Y. Q., Otting G., Billeter M., Muller M., Gehring W., Wüthrich K. Nuclear magnetic resonance spectroscopy of a DNA complex with the uniformly C-13 labeled Antennapedia homeodomain and structure determination of the DNA-bound homeodomain. J. Mol. Biol. 234:1993;1070-1083.
45. Qian Y. Q., Resendez-Perez D., Gehring W. J., Wüthrich K. The des(1-6) Antennapedia homeodomain - comparison of the NMR solution structure and the DNA-binding affinity with the intact Antennapedia homeodomain. Proc. Natl Acad. Sci. USA. 91:1994a;4091-4095.
46. Qian Y. Q., Furukubo-Tokunaga K., Resendez-Perez D., Mueller M., Gehring W. J., Wüthrich K. Nuclear-magnetic-resonance solution structure of the Fushi-tarazu homeodomain from Drosophila and comparison with the Antennapedia homeodomain. J. Mol. Biol. 238:1994b;333-345.
47. Schott O., Billeter M., Leiting B., Wider G., Wüthrich K. The NMR solution structure of the non-classical homeodomain from the rat liver LFB1/HNF1 transcription factor. J. Mol. Biol. 267:1997;673-683.
48. Scott M. P., Weiner A. J. Structural relationships among genes that control development: sequence homology between the Antennapedia, Ultrabithorax, and Fushi tarazu loci of Drosophila. Proc. Natl Acad. Sci. USA. 81:1984;4115-4119.
49. Sheng H., Zhadanov B. M., Fujii T., Bertuzzi S., Grinberg A., Lee E. J., Huang S.-P., Mahon K. A., Westphal H. Specification of pituitary cell lineages by the LIM homeobox gene Lhx3. Science. 272:1996;1004-1007.
50. Sivaraja M., Botfield M. C., Mueller M., Jancso A., Weiss M. A. Solution structure of a POU-specific homeodomain: 3D-NMR studies of human B-cell transcription factor Oct-2. Biochemistry. 33:1994;9845-9855.
51. Studier F. W., Moffat B. A. Use of bacteriophage T7 polymerase to direct selective high-level expression. J. Mol. Biol. 189:1986;113-130.
52. Tsao D. H. H., Gruschus J. M., Wang L. H., Nirenberg M., Ferretti J. A. Elongation of helix-III of the Nk-2 homeodomain upon binding to DNA - a secondary structure study by NMR. Biochemistry. 33:1994;15053-15060.
53. Tsao D. H. H., Gruschus J. M., Wang L. H., Nirenberg M., Ferretti J. A. The 3-dimensional solution structure of the Nk-2 homeodomain from Drosophila. J. Mol. Biol. 251:1995;297-307.
54. Tucker-Kellogg L., Rould M. A., Chambers K. A., Ades S. E., Sauer R. T., Pabo C. O. Engrailed (Gln50→Lys) homeodomain-DNA complex at 1.9 angstrom resolution: structural basis for enhanced affinity and altered specificity. Structure. 5:1997;1047-1054.
55. 15N-enriched proteins. J. Am. Chem. Soc. 115:1993;7772-7777.
56. Wang A. C., Bax A. Determination of the backbone dihedral angles phi in human ubiquitin from reparametrized empirical Karplus equations. J. Am. Chem. Soc. 118:1996;2483-2494.
57. Wang M., Drucker D. J. The LIM domain homeobox gene Isl-1 is a positive regulator of Islet cell-specific proglucagon gene transcription. J. Biol. Chem. 270:1995;12646-12652.
58. Way J. C., Chalfie M. Mec-3 a homeobox-containing gene that specifies differentiation of the touch receptor of C. elegans. Cell. 54:1988;5-16.
59. Weiler S., Gruschus J. M., Tsao D. H. H., Yu L., Wang L. H., Nirenberg M., Ferretti J. A. Site-directed mutations in the Vnd/NK-2 homeodomain-basis of variations in structure and sequence-specific DNA binding. J. Biol. Chem. 273:1998;10994-11000.
60. Williamson M. P., Kikuchi J., Asakura T. Application of 1H-NMR chemical shifts to measure the quality of protein structures. J. Mol. Biol. 247:1995;541-546.
61. Wilson D. S., Guenther B., Desplan C., Kuriyan J. High-resolution crystal structure of a paired (Pax) class cooperative homeodomain dimer on DNA. Cell. 82:1995;709-719.
62. Wishart D. S., Bigam C. G., Holm A., Hodges R. S., Sykes B. D. H-1, C13 and N15 random coil NMR chemical shifts of the common amino-acids. 1. Investigations of nearest-neighbor effects. J. Biomol. NMR. 5:1995;67-81.
63. Wolberger C. Homeodomain interactions. Curr. Opin. Struct. Biol. 6:1996;62-68.
64. Wolberger C., Vershon A. K., Liu B., Johnson A. D., Pabo C. O. Crystal structure of a MAT alpha2 homeodomain-operator complex suggests a general model for homeodomain-DNA interactions. Cell. 67:1991;517-528.