Conformational stability and DNA binding energetics of the rat thyroid transcription factor 1 homeodomain

Proteins: Structure, Function and Genetics

Volumn 70, Issue 3, 2008, Pages 748-760

  Del Vecchio, Pompea ^a   Carullo, Paola ^a   Barone, Guido ^a   Pagano, Bruno ^b   Graziano, Giuseppe ^c   Iannetti, Alessio ^a   Acquaviva, Renato ^a   Leonardi, Antonio ^a   Formisano, Silvestro ^a  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b UNIVERSITY OF SALERNO   (Italy)

^c UNIVERSITY OF SANNIO   (Italy)

Author keywords

Circular dichroism; Differential scanning calorimetry; DNA binding energetics; Homeodomain; Isothermal titration calorimetry; Molecular dynamics

Indexed keywords

POTASSIUM CHLORIDE; SODIUM CHLORIDE; THYROID TRANSCRIPTION FACTOR 1;

ARTICLE; CIRCULAR DICHROISM; COMPLEX FORMATION; DIFFERENTIAL SCANNING CALORIMETRY; DNA BINDING; DNA SEQUENCE; DNA TRANSCRIPTION; ENERGY TRANSFER; ENTHALPY; MEASUREMENT; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PH; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN STABILITY; PROTEIN STRUCTURE; SIMULATION; TEMPERATURE DEPENDENCE; THERMAL ANALYSIS;

ANIMALS; BINDING SITES; CALORIMETRY; CIRCULAR DICHROISM; DNA; HOMEODOMAIN PROTEINS; MODELS, MOLECULAR; NUCLEAR PROTEINS; PROTEIN CONFORMATION; RATS; THERMODYNAMICS; TRANSCRIPTION FACTORS;

RATTUS;

EID: 38549153850     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.21552     Document Type: Article

References (51)

1. Duboule D (editor). Guidebook to the homeoboxes gene. Oxford, UK: Oxford University Press; 1994.
2. Guazzi S, Price M, De Felice M, Damante G, Mattei MG, Di Lauro R. Thyroid nuclear factor 1 (TTF-1) contains a homeodomain and displays a novel DNA binding specificity. EMBO J 1990;9:3691-3699.
3. Damante G, Fabbro D, Pellizzari L, Civitareale D, Guazzi S, Polycarpou-Schwartz M, Cauci S, Quadrifoglio F, Formisano S, Di Lauro R. Sequence-specific DNA recognition by the thyroid transcription factor-1 homeodomain. Nucleic Acid Res 1994;22:3075-3083.
4. Damante G, Pellizzari L, Esposito G, Fogolari F, Viglino P, Fabbro D, Tell G, Formisano S, Di Lauro R. A molecular code dictates sequence-specific DNA recognition by homeodomains. EMBO J 1996;15:4992-5000.
5. Esposito G, Fogolari F, Damante G, Formisano S, Tell G, Leonardi A, Di Lauro R, Viglino P. Analysis of the solution structure of the homeodomain of rat thyroid transcription factor 1 by 1H-NMR spectroscopy and restrained molecular mechanics. Eur J Biochem 1996;241:101-113.
6. Fogolari F, Esposito G, Viglino P, Damante G, Pastore A. Homology model building of the thyroid transcription factor 1 homeodomain. Prot Eng 1993;6:513-519.
7. Scaloni A, Monti M, Acquaviva R, Tell G, Damante G, Formisano S, Pucci P. Topology of the thyroid transcription factor 1 homeodomain-DNA complex. Biochemistry 1999;38:64-72.
8. Damante G, Tell G, Leonardi A, Fogolari F, Bortolotti N, Di Lauro R, Formisano S. Analysis of the conformation and stability of rat TTF-1 homeodomain by circular dichroism. FEBS Lett 1994;345:293-296.
9. Tell G, Acquaviva R, Formisano S, Fogolari F, Pucillo C, Damante G. Comparative stability analysis of the thyroid transcription factor 1 and Antennapedia homeodomains: evidence for residue 54 in controlling the structural stability of the recognition helix. Int J Biochem Cell Biol 1999;31:1339-1353.
10. Fabbro D, Tell G, Leonardi A, Pellizzari L, Pucillo C, Lonigro R, Formisano S, Damante G. In the TTF-1 homeodomain the contribution of several amino acids to DNA recognition depends on the bound sequence. Nucleic Acid Res 1996;24:3283-3288.
11. Tang Y, Nilsson L. Effect of G40R mutation on the binding of human SRY protein to DNA: a molecular dynamics view. Proteins: Struct Funct Genet 1999;35:101-113.
12. Suenaga A, Yatsu C, Komeiji Y, Uebayasi M, Meguro T, Yamato I. Molecular dynamics simulation of trp-repressor/operator complex: analysis of hydrogen bond patterns of protein-DNA interaction. J Mol Struct 2000;526:209-218.
13. Muller M, Affolter M, Leupin W, Otting G, Wuthrich K, Gehring WJ. Isolation and sequence-specific DNA binding of the Antennapedia homeodomain. EMBO J 1988;7:4299-4304.
14. Pace CN, Vajdos F, Free L, Grimsley G, Gray T. How to measure and predict the molar absorption coefficient of a protein. Protein Sci 1995;4:2411-2423.
15. Cantor CR, Warshaw MM, Shapiro H. Oligonucleotide interactions. III. Circular dichroism studies of the conformation of deoxyoligonucleotides. Biopolymers 1970;9:1059-1077.
16. Freire E, Biltonen RL. Statistical mechanical deconvolution of thermal transitions in macromolecules. I. Theory and application to homogeneous systems. Biopolymers 1978;17:463-479.
17. Catanzano F, Giancola C, Graziano G, Barone G. Temperature-induced denaturation of ribonuclease S: a thermodynamic study. Biochemistry 1996;35:13378-13385.
18. Privalov PL. Stability of proteins: small globular proteins. Adv Protein Chem 1979;33:167-241.
19. Zhou Y, Hall CK, Karplus M. The calorimetric criterion for a two-state process revisited. Protein Sci 1999;5:1064-1074.
20. Venyaminov SY, Yang JT. Determination of protein secondary structure. In: Fasman GD, editor. Circular dichroism and the conformational analysis of biomolecules. New York: Plenum; 1996. pp 69-107.
21. Sreema N, Woody RW. A self-consistent method for the analysis of protein secondary structure from circular dichroism. Anal Biochem 1993;209:32-44.
22. Lobley A, Whitmore AL, Wallace BA. Dichroweb: an interactive website for the analysis of secondary structure from circular dichroism data. Bioinformatics 2002;18:211-212.
23. Del Vecchio P, Graziano G, Granata V, Barone G, Mandrich L, Manco G, Rossi M. Temperature- and denaturant-induced unfolding of two thermophilic esterases. Biochemistry 2002;41:1364-1371.
24. Richardson JM, Makhatadze GI. Temperature dependence of thermodynamics of helix-coil transition. J Mol Biol 2004;335:1029-1037.
25. Gruschus JM, Tsao DH, Wang LH, Nirenberg M, Ferretti JA. Interactions of the vnd/NK-2 homeodomain with DNA by nuclear magnetic resonance spectroscopy: basis of binding specificity. Biochemistry 1997;36:5372-5380.
26. Gruschus JM, Tsao DH, Wang LH, Nirenberg M, Ferretti JA. The three-dimensional structure of the vnd/NK-2 homeodomain-DNA complex by NMR spectroscopy. J Mol Biol 1999;289:529-545.
27. HyperChem 7.5, Hypercube, Inc., Gainesville, Florida, USA.
28. Berendsen HJC, van der Spoel D, van Drunen R. GROMACS: a message-passing parallel molecular dynamics implementation. Comput Phys Commun 1995;91:43-56.
29. Cheatham TE, Cieplak P, Kollman PA. A modified version of the Cornell et al. force field with improved sugar pucker phases and helical repeat. J Biomol Struct Dyn 1999;16:845-862.
30. Jorgensen W, Chandrasekhar J, Madura J, Impey R, Klein M. Comparison of simple potential functions for simulating liquid water. J Chem Phys 1983;79:926-935.
31. Hess B, Bekker H, Berendsen HJC, Fraaije J. LINCS: a linear constraint solver for molecular simulations. J Comput Chem 1997;18:1463-1472.
32. Berendsen HJC, Postma JPM, van Gunsteren WF, Di Nola A, Haak JR. Molecular dynamics with coupling to an external bath. J Chem Phys 1984;81:3684-3690.
33. Darden T, Perera L, Li L, Pedersen L. New tricks for modelers from the crystallography toolkit: the particle mesh Ewald algorithm and its use in nucleic acid simulations. Structure 1999;7:55-60.
34. Carra JH, Privalov PL. Energetics of folding and DNA binding of the MAT α 2 homeodomain. Biochemistry 1997;36:526-535.
35. Dragan AI, Li Z, Makeyeva EN, Milgotina EI, Liu Y, Crane-Robinson C, Privalov PL. Forces driving the binding of homeodomains to DNA. Biochemistry 2006;45:141-151.
36. Lundback T, Hansson H, Knapp S, Ladenstein R, Hard T. Thermodynamic characterization of non-sequence-specific DNA-binding by the Sso7d protein from Sulfolobus solfataricus. J Mol Biol 1998;276:775-786.
37. Dragan AI, Klass J, Read C, Churchill MEA, Crane-Robinson C, Privalov PL. DNA binding of a non-sequence-specific HMG-D protein is entropy driven with a substantial non-electrostatic contribution. J Mol Biol 2003;331:795-813.
38. Manning GS. The molecular theory of polyelectrolyte solutions with applications to the electrostatic properties of polynucleotides. Q Rev Biophys 1978;11:179-246.
39. Record MT, Zhang W, Anderson CF. Analysis of effects of salts and uncharged solutes on protein and nucleic acid equilibria and processes: a practical guide to recognizing and interpreting polyelectrolyte effects. Hohmeister effects, and osmotic effects of salts. Adv Protein Chem 1998;51:281-353.
40. +) to the center of DNA oligomers. Biophys J 1995;68:634-647.
41. Tsao DH, Gruschus JM, Wang LH, Nirenberg M, Ferretti JA. Elongation of helix III of the NK-2 homeodomain upon binding to DNA: a secondary structure study by NMR. Biochemistry 1994;33: 15053-15060.
42. Spolar RS, Record TM. Coupling of local folding to site-specific binding of proteins to DNA. Science 1994;263:777-784.
43. Gonzales M, Weiler S, Ferretti JA, Ginsburg A. The vnd/NK-2 homeodomain: thermodynamics of reversible unfolding and DNA binding for wild-type and with residue replacements H52R and H52R/T56W in helix III. Biochemistry 2001;40:4923-4931.
44. Kleinjung J, Fraternali F. POPSCOMP: an automated interaction analysis of biomolecular complexes. Nucleic Acids Res 2005;33:342-346.
45. Gruschus JM, Ferretti JA. Quantitative measurement of water diffusion lifetimes at a protein/DNA interface by NMR. J Biomol NMR 2001;20:111-26.
46. Gutmanas A, Billeter M. Specific DNA recognition by the Antp homeodomain: MD simulations of specific and nonspecific complexes. Proteins: Struct Funct Bioinfor 2004;57:772-782.
47. Qian YQ, Otting G, Wuthrich K. NMR detection of hydration water in the intermolecular interface of a protein-DNA complex. J Am Chem Soc 1993;115:1189-1190.
48. Makhatadze GI, Privalov PL. Energetics of protein structure. Adv Protein Chem 1995;47:307-425.
49. Rees DC, Robertson AD. Some thermodynamic implications for the thermostability of proteins. Protein Sci 2001;10:1187-1194.
50. Fodor E, Mack JW, Maeng JS, Ju JH, Lee HS, Gruschus JM, Ferretti JA, Ginsburg A. Cardiac-specific Nkx2.5 homeodomain: conformational stability and specific DNA binding of Nkx2.5(C56S). Biochemistry 2005;44:12480-12490.
51. Graziano G, Catanzano F, Barone G. Prediction of the heat capacity change on thermal denaturation of globular proteins. Thermochim Acta 1998;321:23-31.