Importance of electrostatic interactions in the association of intrinsically disordered histone chaperone Chz1 and histone H2A.Z-H2B

PLoS Computational Biology

Volumn 8, Issue 7, 2012, Pages

  Chu, Xiakun ^a   Wang, Yong ^b   Gan, Linfeng ^b   Bai, Yawen ^c   Han, Wei ^a   Wang, Erkang ^b   Wang, Jin ^a,b,d  

^a JILIN UNIVERSITY   (China)

^b CHANGCHUN INSTITUTE OF APPLIED CHEMISTRY   (China)

^c NATIONAL CANCER INSTITUTE   (United States)

^d STONY BROOK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ASSOCIATION REACTIONS; COULOMB INTERACTIONS; IONIC STRENGTH; PROTEINS;

COARSE-GRAINED MODELING; FOLDINGS; HISTONE VARIANTS; INTRINSICALLY DISORDERED PROTEINS; NUCLEOSOMES; OLD STRUCTURE; RATE LIMITING; STRUCTURE FUNCTIONS; STRUCTURE-BASED; TRANSITION STATE;

COARSE-GRAINED MODELING;

CHAPERONE; HISTONE H2AZ; HISTONE H2B; PROTEIN CHZ1; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONCENTRATION (PARAMETERS); DIELECTRIC CONSTANT; IONIC STRENGTH; MOLECULAR DYNAMICS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; STATIC ELECTRICITY; STRUCTURE ANALYSIS; THERMODYNAMICS; TRANSITION TEMPERATURE; VELOCITY;

EID: 84864578471     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1002608     Document Type: Article

References (61)

1. Kornberg RD, (1974) Chromatin structure- repeating unit of histones and DNA. Science 184: 868-871.
2. Luger K, Mader AW, Richmond RK, Sargent DF, Richmond TJ, (1997) Crystal structure of the nucleosome core particle at 2.8 °A resolution. Nature 389: 251-260.
3. Kornberg RD, Lorch YL, (1999) Twenty-five years of the nucleosome, fundamental particle of the eukaryote chromosome. Cell 98: 285-294.
4. Muthurajan UM, Bao YH, Forsberg LJ, Edayathumangalam RS, Dyer PN, et al. (2004) Crystal structures of histone sin mutant nucleosomes reveal altered protein-DNA interactions. EMBO J 23: 260-271.
5. Laskey RA, Honda BM, Mills AD, Finch JT, (1978) Nucleosomes are assembled by an acidic protein which binds histones and transfers them to DNA. Nature 275: 416-420.
6. Almouzni G, De Koning L, Corpet A, Haber JE, (2007) Histone chaperones: an escort network regulating histone traffic. Nat Struct Mol Biol 14: 997-1007.
7. Horikoshi M, Eitoku M, Sato L, Senda T, (2008) Histone chaperones: 30 years from isolation to elucidation of the mechanisms of nucleosome assembly and disassembly. Cell Mol Life Sci 65: 414-444.
8. Park YJ, Luger K, (2008) Histone chaperones in nucleosome eviction and histone exchange. Curr Opin Struc Biol 18: 282-289.
9. Das C, Tyler JK, Churchill MEA, (2010) The histone shuffle: histone chaperones in an energetic dance. Trends Biochem Sci 35: 476-489.
10. Hondele M, Ladurner AG, (2011) The chaperone-histone partnership: for the greater good of histone traffic and chromatin plasticity. Curr Opin Struct Biol 21: 698-708.
11. Zhou Z, Feng HQ, Zhou BR, Ghirlando R, Hu KF, et al. (2011) Structural basis for recognition of centromere histone variant CenH3 by the chaperone Scm3. Nature 472: 234-237.
12. Korolev N, Vorontsova OV, Nordenskiold L, (2007) Physicochemical analysis of electrostatic foundation for DNA-protein interactions in chromatin transformations. Prog Biophys Mol Bio 95: 23-49.
13. Dunker AK, Radivojac P, Iakoucheva LM, Oldfield CJ, Obradovic Z, et al. (2007) Intrinsic disorder and functional proteomics. Biophys J 92: 1439-1456.
14. Wright PE, Dyson HJ, (2009) Linking folding and binding. Curr Opin Struct Biol 19: 31-38.
15. Luk E, Vu ND, Patteson K, Mizuguchi G, Wu WH, et al. (2007) Chz1, a nuclear chaperone for histone H2AZ. Mol Cell 25: 357-368.
16. Zhou Z, Feng HQ, Hansen DF, Kato H, Luk E, et al. (2008) NMR structure of chaperone Chz1 complexed with histones H2A.Z-H2B. Nat Struct Mol Biol 15: 868-869.
17. Hansen DF, Zhou Z, Fen HQ, Jenkins LMM, Bai YW, et al. (2009) Binding kinetics of histone chaperone Chz1 and variant histone H2A.Z-H2B by relaxation dispersion nmr spectroscopy. J Mol Biol 387: 1-9.
18. Clementi C, Nymeyer H, Onuchic JN, (2000) Topological and energetic factors: What determines the structural details of the transition state ensemble and "en-route" intermediates for protein folding? an investigation for small globular proteins. J Mol Biol 298: 937-953.
19. Levy Y, Cho SS, Onuchic JN, Wolynes PG, (2005) A survey of flexible protein binding mechanisms and their transition states using native topology based energy landscapes. J Mol Biol 346: 1121-1145.
20. Fersht AR, Sato S, (2004) Φ-value analysis and the nature of protein-folding transition states. Proc Natl Acad Sci U S A 101: 7976-7981.
21. Zhou HX, (2005) How do biomolecular systems speed up and regulate rates? Phys Biol 2: R1-R25.
22. Schreiber G, (2002) Kinetic studies of protein-protein interactions. Curr Opin Struc Biol 12: 41-47.
23. Huang Y, Liu Z, (2009) Kinetic advantage of intrinsically disordered proteins in coupled foldingbinding process: A critical assessment of the "fly-casting" mechanism. J Mol Biol 393: 1143-1159.
24. Yang SC, Onuchic J, Levine H, (2005) Protein self-assembly via domain swapping: The effect of intermolecular interactions and protein concentration. Biophys J 88: 198a-198a.
25. Plaxco KW, Kohn JE, Millett IS, Jacob J, Zagrovic B, et al. (2004) Random-coil behavior and the dimensions of chemically unfolded proteins. Proc Natl Acad Sci U S A 101: 12491-12496.
26. Wang J, Wang Y, Chu X, Hagen SJ, Han W, et al. (2011) Multi-scaled explorations of bindinginduced folding of intrinsically disordered protein inhibitor IA3 to its target enzyme. PLoS Comput Biol 7: e1001118.
27. Turjanski AG, Gutkind JS, Best RB, Hummer G, (2008) Binding-induced folding of a natively unstructured transcription factor. PLoS Comput Biol 4: e1000060.
28. Sugase K, Dyson HJ, Wright PE, (2007) Mechanism of coupled folding and binding of an intrinsically disordered protein. Nature 447: 1021-1025.
29. Wang J, Lu Q, Lu HP, (2006) Single-molecule dynamics reveals cooperative binding-folding in protein recognition. PLoS Comput Biol 2: e78.
30. Lu Q, Lu HP, Wang J, (2007) Exploring the mechanism of flexible biomolecular recognition with single molecule dynamics. Phys Rev Lett 98: 128105.
31. Narayanan R, Ganesh OK, Edison AS, Hagen SJ, (2008) Kinetics of folding and binding of an intrinsically disordered protein: The inhibitor of yeast aspartic proteinase YPrA. J Am Chem Soc 130: 11477-11485.
32. Chen JH, (2009) Intrinsically disordered p53 extreme C-Terminus binds to S100B(ββ) through "fly-casting" J Am Chem Soc 131: 2088-2089.
33. Espinoza-Fonseca LM, (2009) Reconciling binding mechanisms of intrinsically disordered proteins. Biochem Bioph Res Co 382: 479-482.
34. Chan HS, Zhang ZQ, Wallin S, Liu ZR, (2011) Cooperativity, local-nonlocal coupling, and nonnative interactions: Principles of protein folding from coarse-grained models. Annu Rev Phys Chem 62: 301-326.
35. Azia A, Levy Y, (2009) Nonnative electrostatic interactions can modulate protein folding: Molecular dynamics with a grain of salt. J Mol Biol 393: 527-542.
36. Clementi C, Plotkin SS, (2004) The effects of nonnative interactions on protein folding rates: Theory and simulation. Protein Sci 13: 1750-1766.
37. Zarrine-Afsar A, Wallin S, Neculai AM, Neudecker P, Howell PL, et al. (2008) Theoretical and experimental demonstration of the importance of specific nonnative interactions in protein folding. Proc Natl Acad Sci U S A 105: 9999-10004.
38. Schreiber G, Fersht AR, (1996) Rapid, electrostatically assisted association of proteins. Nat Struct Biol 3: 427-431.
39. Ganguly D, Chen JH, (2009) Atomistic details of the disordered states of KID and pKID. implications in coupled binding and folding. J Am Chem Soc 131: 5214-5223.
40. Chen HF, (2009) Molecular dynamics simulation of phosphorylated KID post-translational modification. PLoS ONE 4: e6516.
41. Kumar S, Nussinov R, (2002) Close-range electrostatic interactions in proteins. ChemBioChem 3: 604-617.
42. Uversky VN, Gillespie JR, Fink AL, (2000) Why are "natively unfolded" proteins unstructured under physiologic conditions? Proteins 41: 415-427.
43. Weathers EA, Paulaitis ME, Woolf TB, Hoh JH, (2004) Reduced amino acid alphabet is sufficient to accurately recognize intrinsically disordered protein. FEBS Lett 576: 348-352.
44. Sussman JL, Dunker AK, Silman I, Uversky VN, (2008) Function and structure of inherently disordered proteins. Curr Opin Struc Biol 18: 756-764.
45. Weinkam P, Pletneva EV, Gray HB, Winkler JR, Wolynes PG, (2009) Electrostatic effects on funneled landscapes and structural diversity in denatured protein ensembles. Proc Natl Acad Sci U S A 106: 1796-1801.
46. Pappu RV, Mao AH, Crick SL, Vitalis A, Chicoine CL, (2010) Net charge per residue modulates conformational ensembles of intrinsically disordered proteins. Proc Natl Acad Sci U S A 107: 8183-8188.
47. Muller-Spath S, Soranno A, Hirschfeld V, Hofmann H, Ruegger S, et al. (2010) Charge interactions can dominate the dimensions of intrinsically disordered proteins. Proc Natl Acad Sci U S A 107: 14609-14614.
48. Haran G, England JL, (2010) To fold or expand-a charged question. Proc Natl Acad Sci U S A 107: 14519-14520.
49. Sheinerman FB, Norel R, Honig B, (2000) Electrostatic aspects of protein-protein interactions. Curr Opin Struc Biol 10: 153-159.
50. Shoemaker BA, Portman JJ, Wolynes PG, (2000) Speeding molecular recognition by using the folding funnel: The fly-casting mechanism. Proc Natl Acad Sci U S A 97: 8868-8873.
51. Levy Y, Onuchic JN, Wolynes PG, (2007) Fly-casting in protein-DNA binding: Frustration between protein folding and electrostatics facilitates target recognition. J Am Chem Soc 129: 738-739.
52. Onuchic JN, LutheySchulten Z, Wolynes PG, (1997) Theory of protein folding: The energy landscape perspective. Annu Rev Phys Chem 48: 545-600.
53. Tsai CJ, Kumar S, Ma BY, Nussinov R, (1999) Folding funnels, binding funnels, and protein function. Protein Sci 8: 1181-1190.
54. Das P, Matysiak S, Clementi C, (2005) Balancing energy and entropy: A minimalist model for the characterization of protein folding landscapes. Proc Natl Acad Sci U S A 102: 10141-10146.
55. Bryngelson JD, Onuchic JN, Socci ND, Wolynes PG, (1995) Funnels, pathways, and the energy landscape of protein folding: A synthesis. Proteins 21: 167-195.
56. Noel JK, Whitford PC, Sanbonmatsu KY, Onuchic JN, (2010) SMOG@ctbp: simplified deployment of structure-based models in GROMACS. Nucleic Acids Res 38 (Suppl): W657-61.
57. Sobolev V, Sorokine A, Prilusky J, Abola EE, EdelmanM (1999) Automated analysis of interatomic contacts in proteins. Bioinformatics 15: 327-332.
58. Miyazawa S, Jernigan RL, (1996) Residue-residue potentials with a favorable contact pair term and an unfavorable high packing density term, for simulation and threading. J Mol Biol 256: 623-644.
59. Oliveira LC, Schug A, Onuchic JN, (2008) Geometrical features of the protein folding mechanism are a robust property of the energy landscape: A detailed investigation of several reduced models. J Phys Chem B 112: 6131-6136.
60. Whitford PC, Noel JK, Gosavi S, Schug A, Sanbonmatsu KY, et al. (2009) An all-atom structurebased potential for proteins: Bridging minimal models with all-atom empirical forcefields. Proteins: Struct Funct Bioinf 75: 430-441.
61. Cho SS, Levy Y, Wolynes PG, (2009) Quantitative criteria for native energetic heterogeneity influences in the prediction of protein folding kinetics. Proc Natl Acad Sci U S A 106: 434-439.