Mutational Analysis of the Stability of the H2A and H2B Histone Monomers

Journal of Molecular Biology

Volumn 384, Issue 5, 2008, Pages 1369-1383

  Stump, Matthew R ^a   Gloss, Lisa M ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

circular dichroism; equilibrium stability; fluorescence; kinetic intermediates; symbol values

Indexed keywords

ALANINE; GLYCINE; HISTONE; MONOMER; PROTEIN H2A; PROTEIN H2B; UNCLASSIFIED DRUG;

ARTICLE; CIRCULAR DICHROISM; CRYSTAL STRUCTURE; MUTATIONAL ANALYSIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FOLDING; PROTEIN MOTIF; PROTEIN STABILITY; PROTEIN STRUCTURE;

EUKARYOTA;

EID: 56949105979     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2008.10.040     Document Type: Article

References (71)

1. Milla M.E., and Sauer R.T. P22 Arc repressor: folding kinetics of a single-domain, dimeric protein. Biochemistry 33 (1994) 1125-1133
2. Zitzewitz J.A., Bilsel O., Luo J., Jones B.E., and Matthews C.R. Probing the folding mechanism of a leucine zipper peptide by stopped-flow circular dichroism spectroscopy. Biochemistry 34 (1995) 12812-12819
3. Sosnick T.R., Jackson S., Wilk R.R., Englander S.W., and DeGrado W.F. The role of helix formation in the folding of a fully alpha-helical coiled coil. Proteins 24 (1996) 427-432
4. Durr E., Jelesarov I., and Bosshard H.R. Extremely fast folding of a very stable leucine zipper with a strengthened hydrophobic core and lacking electrostatic interactions between helices. Biochemistry 38 (1999) 870-880
5. Jaenicke R., and Lilie H. Folding and association of oligomeric and multimeric proteins. Adv. Protein Chem. 53 (2000) 329-401
6. Fink A.L. Protein aggregation: folding aggregates, inclusion bodies and amyloid. Folding Des. 3 (1998) R9-R23
7. Matthews C.R. Pathways of protein folding. Annu. Rev. Biochem. 62 (1993) 653-683
8. Shao X., Hensley P., and Matthews C.R. Construction and characterization of monomeric tryptophan repressor: a model for an early intermediate in the folding of a dimeric protein. Biochemistry 36 (1997) 9941-9949
9. Shao X., and Matthews C.R. Single-tryptophan mutants of monomeric tryptophan repressor: optical spectroscopy reveals nonnative structure in a model for an early folding intermediate. Biochemistry 37 (1998) 7850-7858
10. Eliezer D., Chung J., Dyson H.J., and Wright P.E. Native and non-native secondary structure and dynamics in the pH 4 intermediate of apomyoglobin. Biochemistry 39 (2000) 2894-2901
11. Spence G.R., Capaldi A.P., and Radford S.E. Trapping the on-pathway folding intermediate of Im7 at equilibrium. J. Mol. Biol. 341 (2004) 215-226
12. Whittaker S.B., Spence G.R., Gunter Grossmann J., Radford S.E., and Moore G.R. NMR analysis of the conformational properties of the trapped on-pathway folding intermediate of the bacterial immunity protein Im7. J. Mol. Biol. 366 (2007) 1001-1015
13. Gunasekaran K., Eyles S.J., Hagler A.T., and Gierasch L.M. Keeping it in the family: folding studies of related proteins. Curr. Opin. Struct. Biol. 11 (2001) 83-93
14. Zarrine-Afsar A., Larson S.M., and Davidson A.R. The family feud: do proteins with similar structures fold via the same pathway?. Curr. Opin. Struct. Biol. 15 (2005) 42-49
15. Alves C.S., Kuhnert D.C., Sayed Y., and Dirr H.W. The intersubunit lock-and-key motif in human glutathione transferase A1-1: role of the key residues Met51 and Phe52 in function and dimer stability. Biochem. J. 393 (2006) 523-528
16. Thompson L.C., Walters J., Burke J., Parsons J.F., Armstrong R.N., and Dirr H.W. Double mutation at the subunit interface of glutathione transferase rGSTM1-1 results in a stable, folded monomer. Biochemistry 45 (2006) 2267-2273
17. Kim D.H., Jang D.S., Nam G.H., and Choi K.Y. Folding mechanism of ketosteroid isomerase from Comamonas testosteroni. Biochemistry 40 (2001) 5011-5017
18. Kim D.H., Nam G.H., Jang D.S., Yun S., Choi G., Lee H.C., and Choi K.Y. Roles of dimerization in folding and stability of ketosteroid isomerase from Pseudomonas putida biotype B. Protein Sci. 10 (2001) 741-752
19. Nam G.H., Cha S.S., Yun Y.S., Oh Y.H., Hong B.H., Lee H.S., and Choi K.Y. The conserved cis-Pro39 residue plays a crucial role in the proper positioning of the catalytic base Asp38 in ketosteroid isomerase from Comamonas testosteroni. Biochem. J. 375 (2003) 297-305
20. Nam G.H., Kim D.H., Ha N.C., Jang D.S., Yun Y.S., Hong B.H., et al. Contribution of conserved amino acids at the dimeric interface to the conformational stability and the structural integrity of the active site in ketosteroid isomerase from Pseudomonas putida biotype B. J. Biochem. 134 (2003) 101-110
21. Topping T.B., and Gloss L.M. Stability and folding mechanism of mesophilic, thermophilic and hyperthermophilic archaeal histones: the importance of folding intermediates. J. Mol. Biol. 342 (2004) 247-260
22. 2 histone tetramer of the core nucleosome. Protein Sci. 13 (2004) 1304-1316
23. Placek B.J., and Gloss L.M. Three-state kinetic folding mechanism of the H2A/H2B histone heterodimer: the N-terminal tails affect the transition state between a dimeric intermediate and the native dimer. J. Mol. Biol. 345 (2005) 827-836
24. Baxevanis A.D., Arents G., Moudrianakis E.N., and Landsman D. A variety of DNA-binding and multimeric proteins contain the histone fold motif. Nucleic Acids Res. 23 (1995) 2685-2691
25. Xie X., Kokubo T., Cohen S.L., Mirza U., Hoffmann A., Chait B.T., et al. Structural similarity between TAFs and the heterotetrameric core of the histone octamer. Nature 380 (1996) 316-322
26. II18 interact through a histone fold encoded by atypical evolutionary conserved motifs also found in the SPT3 family. Cell 94 (1998) 239-249
27. Selleck W., Howley R., Fang Q., Podolny V., Fried M.G., Buratowski S., and Tan S. A histone fold TAF octamer within the yeast TFIID transcriptional coactivator. Nat. Struct. Biol. 8 (2001) 695-700
28. Davey C.A., Sargent D.F., Luger K., Maeder A.W., and Richmond T.J. Solvent mediated interactions in the structure of the nucleosome core particle at 1.9 Å resolution. J. Mol. Biol. 319 (2002) 1097-1113
29. Luger K., Mader A.W., Richmond R.K., Sargent D.F., and Richmond T.J. Crystal structure of the nucleosome core particle at 2.8 Å resolution. Nature 389 (1997) 251-260
30. Zhu W., Sandman K., Lee G.E., Reeve J.N., and Summers M.F. NMR structure and comparison of the archaeal histone HFoB from the mesophile Methanobacterium formicicum with HMfB from the hyperthermophile Methanothermus fervidus. Biochemistry 37 (1998) 10573-10580
31. Decanniere K., Babu A.M., Sandman K., Reeve J.N., and Heinemann U. Crystal structures of recombinant histones HMfA and HMfB from the hyperthermophilic archaeon Methanothermus fervidus. J. Mol. Biol. 303 (2000) 35-47
32. Stump M.R., and Gloss L.M. Unique fluorophores in the dimeric archaeal histones hMfB and hPyA1 reveal the impact of nonnative structure in a monomeric kinetic intermediate. Protein Sci. 17 (2008) 322-332
33. Isenberg I. Histones. Annu. Rev. Biochem. 48 (1979) 159-191
34. D'Anna J.A., and Isenberg I. A histone cross-complexing pattern. Biochemistry 13 (1974) 4992-4997
35. D'Anna Jr. J.A., and Isenberg I. Fluorescence anisotropy and circular dichroism study of conformational changes in histone IIb2. Biochemistry 11 (1972) 4017-4025
36. D'Anna Jr. J.A., and Isenberg I. Conformational changes of histone LAK (f2a2). Biochemistry 13 (1974) 2093-2098
37. Deleage G., and Geourjon C. An interactive graphic program for calculating the secondary structure content of proteins from circular dichroism spectrum. Comput. Appl. Biosci. 9 (1993) 197-199
38. Placek B.J., and Gloss L.M. The N-terminal tails of the H2A-H2B histones affect dimer structure and stability. Biochemistry 41 (2002) 14960-14968
39. Munoz V., and Serrano L. Development of the multiple sequence approximation within the AGADIR model of alpha-helix formation: comparison with Zimm-Bragg and Lifson-Roig formalisms. Biopolymers 41 (1997) 495-509
40. Gloss L.M., and Placek B.J. The effect of salts on the stability of the H2A-H2B histone dimer. Biochemistry 41 (2002) 14951-14959
41. Wang A., and Bolen D.W. A naturally occurring protective system in urea-rich cells: mechanism of osmolyte protection of proteins against urea denaturation. Biochemistry 36 (1997) 9101-9108
42. Bolen D.W., and Baskakov I.V. The osmophobic effect: natural selection of a thermodynamic force in protein folding. J. Mol. Biol. 310 (2001) 955-963
43. Henkels C.H., Kurz J.C., Fierke C.A., and Oas T.G. Linked folding and anion binding of the Bacillus subtilis ribonuclease P protein. Biochemistry 40 (2001) 2777-2789
44. Banks D.D., and Gloss L.M. Equilibrium folding of the core histones: the H3-H4 tetramer is less stable than the H2A-H2B dimer. Biochemistry 42 (2003) 6827-6839
45. Placek B.J., Harrison L.N., Villers B.M., and Gloss L.M. The H2A.Z/H2B dimer is unstable compared to the dimer containing the major H2A isoform. Protein Sci. 14 (2005) 514-522
46. Beechem J.M. Global analysis of biochemical and biophysical data. Methods Enzymol. 210 (1992) 37-54
47. Myers J.K., Pace C.N., and Scholtz J.M. Denaturant m values and heat capacity changes: relation to changes in accessible surface areas of protein folding. Protein Sci. 4 (1995) 2138-2148
48. Mello C.C., and Barrick D. Measuring the stability of partly folded proteins using TMAO. Protein Sci. 12 (2003) 1522-1529
49. Fersht A.R. Structure and mechanism in protein science: A guide to enzyme catalysis and protein folding (1999), W.H. Freeman & Co, New York
50. Sanchez I.E., and Kiefhaber T. Origin of unusual phi-values in protein folding: evidence against specific nucleation sites. J. Mol. Biol. 334 (2003) 1077-1085
51. Fersht A.R., and Sato S. Phi-value analysis and the nature of protein-folding transition states. Proc. Natl Acad. Sci. USA 101 (2004) 7976-7981
52. Baskakov I., and Bolen D.W. Forcing thermodynamically unfolded proteins to fold. J. Biol. Chem. 273 (1998) 4831-4834
53. Bolen D.W., and Rose G.D. Structure and energetics of the hydrogen-bonded backbone in protein folding. Annu. Rev. Biochem. 77 (2008) 339-362
54. Gursky O. Probing the conformation of a human apolipoprotein C-1 by amino acid substitutions and trimethylamine-N-oxide. Protein Sci. 8 (1999) 2055-2064
55. Suto R.K., Clarkson M.J., Tremethick D.J., and Luger K. Crystal structure of a nucleosome core particle containing the variant histone H2A.Z. Nat. Struct. Biol. 7 (2000) 1121-1124
56. Pace C.N., and Scholtz J.M. A helix propensity scale based on experimental studies of peptides and proteins. Biophys. J. 75 (1998) 422-427
57. Rudolph R., Fuchs I., and Jaenicke R. Reassociation of dimeric cytoplasmic malate dehydrogenase is determined by slow and very slow folding reactions. Biochemistry 25 (1986) 1662-1669
58. Clark A.C., Raso S.W., Sinclair J.F., Ziegler M.M., Chaffotte A.F., and Baldwin T.O. Kinetic mechanism of luciferase subunit folding and assembly. Biochemistry 36 (1997) 1891-1899
59. Apuy J.L., Park Z.Y., Swartz P.D., Dangott L.J., Russell D.H., and Baldwin T.O. Pulsed-alkylation mass spectrometry for the study of protein folding and dynamics: development and application to the study of a folding/unfolding intermediate of bacterial luciferase. Biochemistry 40 (2001) 15153-15163
60. Noland B.W., and Baldwin T.O. Demonstration of two independently folding domains in the alpha subunit of bacterial luciferase by preferential ligand binding-induced stabilization. Biochemistry 42 (2003) 3105-3112
61. Wallace L.A., and Dirr H.W. Folding and assembly of dimeric human glutathione transferase A1-1. Biochemistry 38 (1999) 16686-16694
62. Hornby J.A., Luo J.K., Stevens J.M., Wallace L.A., Kaplan W., Armstrong R.N., and Dirr H.W. Equilibrium folding of dimeric class mu glutathione transferases involves a stable monomeric intermediate. Biochemistry 39 (2000) 12336-12344
63. Mann C.J., and Matthews C.R. Structure and stability of an early folding intermediate of Escherichia coli trp aporepressor measured by far-UV stopped-flow circular dichroism and 8-anilino-1-naphthalene sulfonate binding. Biochemistry 32 (1993) 5282-5290
64. Gloss L.M., Simler B.R., and Matthews C.R. Rough energy landscapes in protein folding: dimeric E. coli Trp repressor folds through three parallel channels. J. Mol. Biol. 312 (2001) 1121-1134
65. Hobart S.A., Meinhold D.W., Osuna R., and Colon W. From two-state to three-state: the effect of the P61A mutation on the dynamics and stability of the factor for inversion stimulation in an altered equilibrium denaturation mechanism. Biochemistry 41 (2002) 13744-13754
66. Topping T.B., Hoch D.A., and Gloss L.M. Folding mechanism of FIS, the intertwined, dimeric factor for inversion stimulation. J. Mol. Biol. 335 (2004) 1065-1081
67. Meinhold D., Boswell S., and Colon W. P61A mutation in the factor for inversion stimulation results in a thermostable dimeric intermediate. Biochemistry 44 (2005) 14715-14724
68. Gloss L.M., and Matthews C.R. Urea and thermal equilibrium denaturation studies on the dimerization domain of Escherichia coli Trp repressor. Biochemistry 36 (1997) 5612-5623
69. Gloss L.M., and Matthews C.R. Mechanism of folding of the dimeric core domain of Escherichia coli Trp repressor: a nearly diffusion-limited reaction leads to the formation of an on-pathway dimeric intermediate. Biochemistry 37 (1998) 15990-15999
70. Gloss L.M., and Matthews C.R. The barriers in the biomolecular and unimolecular folding reaction of the dimeric core domain of Escherichia coli Trp repressor are dominated by enthalpic contributions. Biochemistry 37 (1998) 16000-16010
71. Ho S.N., Hunt H.D., Horton R.M., Pullen J.K., and Pease L.R. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77 (1989) 51-59