Deciphering the mechanism of thermodynamic accommodation of telomeric oligonucleotide sequences by the Schizosaccharomyces pombe protection of telomeres 1 (Pot1pN) protein

Biochemistry

Volumn 47, Issue 15, 2008, Pages 4345-4358

  Croy, Johnny E ^a   Fast, Jonas L ^a,b   Grimm, Nicole E ^a   Wuttke, Deborah S ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b University of Colorado at Boulder   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SCHIZOSACCHAROMYCES; SPECIAL CAPPING; THERMODYNAMIC ACCOMMODATION; THERMODYNAMIC ANALYSIS;

CELL PROLIFERATION; CHROMOSOMES; CONFORMATIONS; CRYSTAL STRUCTURE; DNA; ENTROPY; THERMODYNAMICS;

OLIGONUCLEOTIDES;

OLIGONUCLEOTIDE; PROTEIN; SINGLE STRANDED DNA; TELOMERE 1 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CALORIMETRY; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DNA BINDING; DNA SEQUENCE; DNA STRUCTURE; ENTHALPY; ENTROPY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTON NUCLEAR MAGNETIC RESONANCE; SCHIZOSACCHAROMYCES POMBE; STRUCTURE ANALYSIS; TELOMERE; THERMODYNAMICS;

BASE SEQUENCE; CARBOHYDRATES; DNA, SINGLE-STRANDED; MODELS, MOLECULAR; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; NUCLEIC ACID CONFORMATION; OLIGONUCLEOTIDES; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTONS; SCHIZOSACCHAROMYCES POMBE PROTEINS; TELOMERE; TELOMERE-BINDING PROTEINS; THERMODYNAMICS;

SCHIZOSACCHAROMYCES POMBE;

EID: 42049083762     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi701778x     Document Type: Article

References (55)

1. Oda, M., and Nakamura, H. (2000) Thermodynamic and kinetic analyses for understanding sequence-specific DNA recognition. Genes Cells 5, 319-326.
2. Jen-Jacobson, L., Engler, L. E., and Jacobson, L. A. (2000) Structural and thermodynamic strategies for site-specific DNA binding proteins. Struct. Fold Des. 8, 1015-1023.
3. Mandel-Gutfreund, Y., Schueler, O., and Margalit, H. (1995) Comprehensive analysis of hydrogen bonds in regulatory protein DNA-complexes: In search of common principles. J. Mol. Biol. 253, 370-382.
4. O'Brien, R., and Haq, I. (2004) Applications of Biocalorimetry: Binding, Stability and Enzyme Kinetics, Wiley, New York.
5. Milev, S., Gorfe, A. A., Karshikoff, A., Clubb, R. T., Bosshard, H. R., and Jelesarov, I. (2003) Energetics of sequence-specific protein-DNA association: Binding of integrase Tn916 to its target DNA. Biochemistry 42, 3481-3491.
6. Hard, T., and Lundback, T. (1996) Thermodynamics of sequence-specific protein-DNA interactions. Biophys. Chem. 62, 121-139.
7. Privalov, P. L., Dragan, A. I., Crane-Robinson, C., Breslauer, K. J., Remeta, D. P., and Minetti, C. A. S. A. (2007) What drives proteins into the major or minor grooves of DNA? J. Mol. Biol. 365, 1-9.
8. Bochkarev, A., and Bochkareva, E. (2004) From RPA to BRCA2: Lessons from single-stranded DNA binding by the OB-fold. Curr. Opin. Struct. Biol. 14, 36-42.
9. Raghunathan, S., Kozlov, A. G., Lohman, T. M., and Waksman, G. (2000) Structure of the DNA binding domain of E. coli SSB bound to ssDNA. Nat. Struct. Mol. Biol. 7, 648-652.
10. Kozlov, A. G., and Lohman, T. M. (1999) Adenine base unstacking dominates the observed enthalpy and heat capacity changes for the Escherichia coli SSB tetramer binding to single-stranded oligoadenylates. Biochemistry 38, 7388-7397.
11. Kozlov, A. G., and Lohman, T. M. (1998) Calorimetric studies of E. coli SSB protein-single-stranded DNA interactions: Effects of monovalent salts on binding enthalpy. J. Mol. Biol. 278, 999-1014.
12. Larkin, C., Datta, S., Harley, M. J., Anderson, B. J., Ebie, A., Hargreaves, V., and Schildbach, J. F. (2005) Inter- and intramolecular determinants of the specificity of single-stranded DNA binding and cleavage by the F factor relaxase. Structure 13, 1533-1544.
13. Stern, J. C., Anderson, B. J., Owens, T. J., and Schildbach, J. F. (2004) Energetics of the sequence-specific binding of single-stranded DNA by the F factor relaxase domain. J. Biol. Chem. 279, 29155-29159.
14. Stern, J. C., and Schildbach, J. F. (2001) DNA recognition by F factor TraI36: Highly sequence-specific binding of single-stranded DNA. Biochemistry 40, 11586-11595.
15. Tanner, J. J., Komissarov, A. A., and Deutscher, S. L. (2001) Crystal structure of an antigen-binding fragment bound to single-stranded DNA. J. Mol. Biol. 314, 807-822.
16. Komissarov, A. A., and Deutscher, S. L. (1999) Thermodynamics of Fab-ssDNA interactions: Contribution of heavy chain complementarity determining region 3. Biochemistry 38, 14631-14637.
17. Buczek, P., and Horvath, M. P. (2006) Structural reorganization and the cooperative binding of single-stranded telomere DNA in Sterkiella nova. J. Biol. Chem. 281, 40124-40134.
18. Buczek, P., and Horvath, M. P. (2006) Thermodynamic characterization of binding Oxytricha nova single-strand telomere DNA with the α protein N-terminal domain. J. Mol. Biol. 359, 1217-1234.
19. Kerr, I. D., Wadsworth, R. I. M., Cubeddu, L., Blankenfeldt, W., Naismith, J. H., and White, M. F. (2003) Insights into ssDNA recognition by the OB fold from a structural and thermodynamic study of Sulfolobus SSB protein. EMBO J. 22, 2561-2570.
20. Verdun, R. E., and Karlseder, J. (2007) Replication and protection of telomeres. Nature 447, 924-931.
21. Croy, J. E., and Wuttke, D. S. (2006) Themes in ssDNA recognition by telomere-end protection proteins. Trends. Biochem. Sci. 31, 516-525.
22. Peersen, O. B., Ruggles, J. A., and Schultz, S. C. (2002) Dimeric structure of the Oxytricha nova telomere end-binding protein α-subunit bound to ssDNA. Nat. Struct. Mol. Biol. 9, 182-187.
23. Horvath, M. P., and Schultz, S. C. (2001) DNA G-quartets in a 1.86 Å resolution structure of an Oxytricha nova telomeric protein-DNA complex. J. Mol. Biol. 310, 367-377.
24. Classen, S. C., Ruggles, J. A., and Schultz, S. (2001) Crystal structure of the N-terminal domain of Oxytricha nova telomere end-binding protein α subunit both uncomplexed and complexed with telomeric ssDNA. J. Mol. Biol. 314, 1113-1125.
25. Horvath, M. P., Schweiker, V. L., Bevilacqua, J. M., Ruggles, J. A., and Schultz, S. C. (1998) Crystal structure of the Oxytricha nova telomere end binding protein complexed with single strand DNA. Cell 95, 963-974.
26. Mitton-Fry, R. M., Anderson, E. M., Hughes, T. R., Lundblad, V., and Wuttke, D. S. (2002) Conserved structure for single-stranded telomeric DNA recognition. Science 296, 145-147.
27. Lei, M., Podell, E. R., Baumann, P., and Cech, T. R. (2003) DNA self-recognition in the structure of Pot1 bound to telomeric single-stranded DNA. Nature 426, 198-204.
28. Lei, M., Podell, E. R., and Cech, T. R. (2004) Structure of human POT1 bound to telomeric single-stranded DNA provides a model for chromosome end-protection. Nat. Struct. Mol. Biol. 11, 1223-1229.
29. Theobald, D. L., Mitton-Fry, R. M., and Wuttke, D. S. (2003) Nucleic acid recognition by OB-fold proteins. Annu. Rev. Biophys. Biomol. Struct. 32, 115-133.
30. Lei, M., Baumann, P., and Cech, T. R. (2002) Cooperative binding of single-stranded telomeric DNA by the Pot1 protein of Schizosaccharomyces pombe. Biochemistry 41, 14560-14568.
31. Theobald, D. L., and Schultz, S. C. (2003) Nucleotide shuffling and ssDNA recognition in Oxytricha nova telomere end-binding protein complexes. EMBO J. 22, 4314-4324.
32. 1-389. J. Mol. Biol. 361, 80-93.
33. Anderson, E. M., Halsey, W. A., and Wuttke, D. S. (2002) Delineation of the high-affinity single-stranded telomeric DNA-binding domain of Saccharomuces cerevisiae Cdc13. Nucleic Acids Res. 30, 4305-4313.
34. Eldridge, A. M., Halsey, W. A., and Wuttke, D. S. (2006) Identification of the determinants for the specific recognition of single-strand telomeric DNA by Cdc13. Biochemistry 45, 871-879.
35. Pace, C. N., Vajdos, F., Fee, L., Grimsley, G., and Gray, T. (1995) How to measure and predict the molar absorption coefficient of a protein. Protein Sci. 4, 2411-2423.
36. Briggner, L-E., and Wadsö, I. (1991) Test and calibration processes for microcalorimeters, with special reference to heat conduction instruments used with aqueous systems. J. Biochem. Biophys. Methods 22, 101-118.
37. Buschmann, H-J., and Schollmeyer, E. (1999) A test reaction from macrocyclic chemistry for calorimetric titrations. Thermochim. Acta 333, 49-53.
38. Turnbull, W. B., and Daranas, A. H. (2003) On the value of c: Can low affinity systems be studied by isothermal titration calorimetry? J. Am. Chem. Soc. 125, 14859-14866.
39. 15N-labelled nucleic acids by 3D triple resonance NMR. J. Am. Chem. Soc. 115, 11040-11041.
40. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe: A multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6, 277-293.
41. 1H 2D NMR spectra by interactive computer graphics. J. Magn. Reson. 84, 627-633.
42. Vranken, W. F., Boucher, W., Stevens, T. J., Fogh, R. H., Pajon, A., Llinas, M., Ulrich, E. L., Markley, J. L., Ionides, J., and Laue, E. D. (2005) The CCPN data model for NMR spectroscopy: Development of a software pipeline. Proteins 59, 687-696.
43. 1H NMR spectra of isotope labeled proteins, using the X(w1,w2) double half filter. J. NMR Res. 85, 586-594.
44. Ikura, M., and Bax, A. (1992) Isotope-filtered 2D NMR of a protein-peptide complex: Study of a skeletal muscle myosin light chain kinases fragment bound to calmodulin. J. Am. Chem. Soc. 114, 2433-2440.
45. Fraczkiewicz, R., and Werner, B. (1998) Exact and efficient analytical calculation of the accessible surface areas and their gradients for macromolecules. J. Comput. Chem. 19, 319-333.
46. Spolar, R. S., and Record, M. T. Jr. (1994) Coupling of local folding to site-specific binding of proteins to DNA. Science 263, 777-784.
47. Brunger, A. T. (1993) X-PLOR Version 3.1: A System for X-ray Crystallography and NMR, Yale University Press, New Haven, CT.
48. Sharp, K. (2001) Entropy-enthalpy compensation: Fact or artifact? Protein Sci. 10, 661-667.
49. Cooper, A., Johnson, C. M., Lakey, J. H., and Nollmann, M. (2001) Heat does not come in different colours: Entropy-enthalpy compensation, free energy windows, quantum confinement, pressure perturbation calorimetry, solvation and the multiple causes of heat capacity effects in biomolecular interactions. Biophys. Chem. 93, 215-230.
50. 13C chemical-shift data. J. Biomol. NMR 4, 171-180.
51. + binding site on the MurB enzyme by NMR. Nat. Struct. Mol. Biol. 3, 995-997.
52. Spolar, R. S., Livingstone, J. R., and Record, M. T., Jr. (1992) Use of liquid hydrocarbon and amide transfer data to estimate contributions to thermodynamic functions of protein folding from the removal of nonpolar and polar surface from water. Biochemistry 31, 3947-3955.
53. Madan, B., and Sharp, K. A. (2001) Hydration heat capacity of nucleic acid constituents determined from the random network model. Biophys. J. 81, 1881-1887.
54. Kalodimos, C. G., Boelens, R., and Kaptein, R. (2004) Toward an integrated model of protein-DNA recognition as inferred from NMR studies on the Lac-repressor system. Chem. Rev. 104, 3567-3586.
55. DeLano, W. L. (2002) The PyMOL Molecular Graphics System, DeLano Scientific, San Carlos, CA.