A Mechanism for Histone Chaperoning Activity of Nucleoplasmin: Thermodynamic and Structural Models

Journal of Molecular Biology

Volumn 393, Issue 2, 2009, Pages 448-463

  Taneva, Stefka G ^a   Bañuelos, Sonia ^a   Falces, Jorge ^a   Arregi, Igor ^a   Muga, Arturo ^a   Konarev, Petr V ^b,c   Svergun, Dmitri I ^b,c   Velázquez Campoy, Adrián ^d   Urbaneja, María A ^a  

^a UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^c SHUBNIKOV INSTITUTE OF CRYSTALLOGRAPHY   (Russian Federation)

^d UNIVERSITY OF ZARAGOZA   (Spain)

Author keywords

histone chaperone; histones; ITC; nucleoplasmin; SAXS

Indexed keywords

CHAPERONE; DNA; HISTONE H2A; HISTONE H2B; HISTONE H5; NUCLEOPLASMIN;

ARTICLE; BINDING AFFINITY; CHROMATIN; CONTROLLED STUDY; DNA BINDING; ISOTHERMAL TITRATION CALORIMETRY; NUCLEOSOME; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; REGULATORY MECHANISM; THERMODYNAMICS; X RAY CRYSTALLOGRAPHY;

XENOPUS LAEVIS;

EID: 70349560000     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2009.08.005     Document Type: Article

References (66)

1. Frehlick L.J., Eirín-López J.M., and Ausió J. New insights into the nucleophosmin/nucleoplasmin family of nuclear chaperones. BioEssays 29 (2007) 49-59
2. Prado A., Ramos I., Frehlick L.J., Muga A., and Ausió J. Nucleoplasmin: a nuclear chaperone. Biochem. Cell Biol. 82 (2004) 437-445
3. Bañuelos S., Omaetxebarria M.J., Ramos I., Larsen M.R., Arregi I., Jensen O.N., et al. Phosphorylation of both nucleoplasmin domains is required for activation of its chromatin decondensation activity. J. Biol. Chem. 282 (2007) 21213-21221
4. Laskey R.A., Honda B.M., Mills A.D., and Finch J.T. Nucleosomes are assembled by an acidic protein which binds histones and transfers them to DNA. Nature 275 (1978) 416-420
5. Philpott A., and Leno G.H. Nucleoplasmin remodels sperm chromatin in Xenopus egg extracts. Cell 69 (1992) 759-767
6. Akey C.W., and Luger K. Histone chaperones and nucleosome assembly. Curr. Opin. Struct. Biol. 13 (2003) 6-14
7. Ramos I., Prado A., Finn R.M., Muga A., and Ausió J. Nucleoplasmin-mediated unfolding of chromatin involves the displacement of linker-associated chromatin proteins. Biochemistry 44 (2005) 8274-8281
8. Cotten M., Sealy L., and Chalkley R. Massive phosphorylation distinguishes Xenopus laevis nucleoplasmin isolated from oocytes or unfertilized eggs. Biochemistry 25 (1986) 5063-5069
9. Dingwall C., Dilworth S.M., Black S.J., Kearsey S.E., Cox L.S., and Laskey R.A. Nucleoplasmin cDNA sequence reveals polyglutamic acid tracts and a cluster of sequences homologous to putative nuclear localization signals. EMBO J. 6 (1987) 69-74
10. Dutta S., Akey I.V., Dingwall C., Hartman K.L., Laue T., Nolte R.T., et al. The crystal structure of nucleoplasmin-core: implications for histone binding and nucleosome assembly. Mol. Cell 8 (2001) 841-853
11. Prieto C., Sapera N., Arnan C., Hills M.H., Wang X., Chiva M., et al. Nucleoplasmin interaction with protamines. Involvement of the polyglutamic tract. Biochemistry 41 (2002) 7802-7810
12. Arnan C., Saperas N., Prieto C., Chiva M., and Ausió J. Interaction of Nucleoplasmin with Core Histones. Biol. Chem. 278 (2003) 31319-31324
13. Salvany L., Chiva M., Arnan C., Ausió J., Subirana J.A., and Saperas N. Mutation of the small acidic tract A1 drastically reduces nucleoplasmin activity. FEBS Lett. 576 (2004) 353-357
14. Arnan C., Prieto C., Chiva M., Salvany L., Ausió J., Subirana J.A., and Saperas N. Analysis of the stability and function of nucleoplasmin through cysteine mutants. Arch. Biochem. Biophys. 437 (2005) 205-214
15. Thoma F., Koller T., and Klug A. Involvement of histone H1 in the organization of the nucleosome and of the salt-dependent superstructures of chromatin. J. Cell Biol. 83 (1979) 403-427
16. Butler P.J., and Thomas J.O. Changes in chromatin folding in solution. J. Mol. Biol. 140 (1980) 505-529
17. Igo-Kemens T., Horz W., and Zachau H.G. Chromatin. Ann. Rev. Biochem. 51 (1982) 89-121
18. Fan L., and Roberts V.A. Complex of linker histone H5 with the nucleosome and its implications for chromatin packing. Proc. Natl. Acad. Sci. USA 103 (2006) 8384-8389
19. Arents G., Burlingame R.W., Wang B.C., Love W.E., and Moudrianakis E.N. The nucleosomal core histone octamer at 3.1 Ǻ resolution: a tripartite protein assembly and a left-handed superhelix. Proc. Natl. Acad. Sci. USA 88 (1991) 10148-10152
20. Arents G., and Moudrianakis E.N. The histone fold: a ubiquitous architectural motif utilized in DNA compaction and protein dimerization. Proc. Natl. Acad. Sci. USA 92 (1995) 11170-11174
21. Zlatanova J. The linker histones and chromatin structure: new twists. Prog. Nucleic Acid Res. Mol. Biol. 52 (1996) 217-259
22. Zlatanova J. Histone H1 zero: a major player in cell differentiation?. FASEB J. 8 (1994) 1260-1268
23. Zlatanova J. Linker histone binding and displacement: versatile mechanism for transcriptional regulation. FASEB J. 14 (2000) 1697-1704
24. Zlatanova J., Seebart C., and Tomschik M. The linker-protein network: control of nucleosomal DNA accessibility. Cell 33 (2008) 247-253
25. Zhou Y.B., Gerchman S.E., Ramakrishnan V., Travers A., and Muyldermans S. Position and orientation of the globular domain of linker histone H5 on the nucleosome. Nature 395 (1998) 402-405
26. Ramakrishnan V., Finch J.T., Graziano V., Lee P.L., and Sweet R.M. Crystal structure of globular domain of histone H5 and its implications for nucleosome binding. Nature 362 (1993) 219-223
27. Luger K., Mäder A.W., Richmond R.K., Sargen D.F., and Richmond T.J. Crystal structure of the nucleosome core particle at 2.8 Ǻ resolution. Nature 389 (1997) 251-260
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 Ǻ resolution. J. Mol. Biol. 319 (2002) 1097-1113
29. English C.M., Adkins M.W., Carson J.J., Churchill M.E.A., and Tyler J.K. Structural basis for the histone chaperone activity of Asf1. Cell 127 (2006) 495-508
30. Zhou Z., Feng H., Hansen D.F., Kato H., Luk E., Freedberg D.I., et al. NMR structure of chaperone Chz1 complexed with histones H2A.Z-H2B. Nat. Struct. Mol. Biol. 15 (2008) 868-869
31. Hierro A., Arizmendi J.M., De las Rivas J., Urbaneja M.A., Prado A., and Muga A. Structural and functional properties of Escherichia coli-derived nucleoplasmin. A comparative study of recombinant and natural proteins. Eur. J. Biochem. 268 (2001) 1739-1748
32. Bañuelos S., Hierro A., Arizmendi J.M., Montoya G., Prado A., and Muga A. Activation mechanism of the nuclear chaperone nucleoplasmin: role of the core domain. J. Mol. Biol. 334 (2003) 585-593
33. Feigin L.A., and Svergun D.I. Structure Analysis by Small-Angle X-ray and Neutron Scattering (1987), Plenum Press, Princeton, NJ
34. Svergun D.I., and Koch M.H.J. Small angle scattering studies of macromolecules in solution. Rep. Prog. Phys. 66 (2003) 1735-1782
35. Svergun D.I. Restoring low resolution structure of biological macromolecules from solution scattering using simulated annealing. Biophys. J. 76 (1999) 2879-2886
36. Petoukhov M.V., and Svergun D.I. Analysis of X-ray and neutron scattering from biomacromolecular solutions. Eur. Biophys. J. 35 (2006) 562-571
37. Petoukhov M.V., and Svergun D.I. Global rigid body modeling of macromolecular complexes against small-angle scattering data. Biophys. J. 89 (2005) 1237-1250
38. Baker B.M., and Murphy K.P.J. Dissecting the energetics of a protein-protein interaction: the binding of ovomucoid third domain to elastas. J. Mol. Biol. 268 (1997) 557-569
39. Gómez J., and Freire E. Thermodynamic mapping of the inhibitor site of the aspartic protease endothiapepsin. J. Mol. Biol 252 (1995) 337-350
40. Petrucci S. Ionic Interactions 1 (1972) 117-177
41. Taneva S.G., Muñoz I., Franco G., Falces J., Arregi I., Muga A., et al. Activation of nucleoplasmin, an oligomeric histone chaperone, challenges its stability. Biochemistry 47 (2008) 13897-13906
42. Namboodiri V.M.H., Akey I.V., Schmidt-Zachmann S., Head J.F., and Akey C.W. The structure and function of Xenopus NO38-core, a histone chaperone in the nucleolus. Structure 12 (2004) 2149-2160
43. Saperas N., Chiva M., Aligué R., Itoh T., Katagiri C., Subirana J.A., and Ausió J. Physicochemical and functional comparison of Xenopus laevis nucleoplasmin obtained from oocytes and from overexpression in bacteria. Arch. Biochem. Biophys. 361 (1999) 135-141
44. Franco G., Bañuelos S., Falces J., Muga A., and Urbaneja M.A. Thermodynamic characterization of nucleoplasmin unfolding: interplay between function and stability. Biochemistry 47 (2008) 7954-7962
45. Sickmeier M., Hamilton J.A., LeGall T., Vacic V., Cortese M.S., Tantos A., et al. DisProt: the database of disordered proteins. Nucleic Acids Res. 35 (2007) D787-D793
46. Koshland Jr. D.E. The structural basis of negative cooperativity: receptors and enzymes. Curr. Opin. Struct. Biol. 6 (1996) 757-761
47. Cabani S., Gianni P., Mollica V., and Lepori L. Group contributions to the thermodynamic properties of non-ionic organic solutes indicate indilute aqueous solution. J. Solution Chem. 10 (1981) 563-595
48. Philpott A., Krude T., and Laskey R.A. Nuclear chaperones. Semin. Cell Dev. 11 (2000) 7-14
49. Woodland H.R., and Adamson E.D. The synthesis and storage of histones during the oogenesis of Xenopus laevis. Dev. Biol. 57 (1977) 118-135
50. Mamoon N.M. Binding of histone H1 to DNA is described by an allosteric model. Biopolymers 77 (2005) 9-17
51. Leno G.H., Mills A.D., Philpott A., and Laskey R.A. Hyperphosphorylation of nucleoplasmin facilitates Xenopus sperm decondensation at fertilization. J. Biol. Chem. 271 (1996) 7253-7256
52. Royer C.A., Ropp T., and Scarlata S.F. Solution studies of the interactions between the histone core proteins and DNA using fluorescence spectroscopy. Biophys. Chem. 43 (1992) 197-211
53. Hierro A., Arizmendi J.M., Bañuelos S., Prado A., and Muga A. Electrostatic interactions at the C-terminal domain of nucleoplasmin modulate its chromatin decondensation activity. Biochemistry 41 (2002) 6408-6413
54. Wang X., Moore S.C., Laszckzak M., and Ausió J. Interaction of Nucleoplasmin with Core Histones. J. Biol. Chem. 275 (2000) 35013-35020
55. Roessle M.W., Klaering R., Ristau U., Robrahn B., Jahn D., Gehrmann T., et al. Upgrade of the small-angle X-ray scattering beamline X33 at the European Molecular Biology Laboratory, Hamburg. J. Appl. Crystallogr. 40 (2007) s190-s194
56. Konarev P.V., Volkov V.V., Sokolova A.V., Koch M.H.J., and Svergun D.I. PRIMUS-a Windows-PC based system for small-angle scattering data analysis. J. Appl. Crystallogr. 36 (2003) 1277-1282
57. Konarev P.V., Petoukhov M.V., Volkov V.V., and Svergun D.I. ATSAS 2.1, a program package for small-angle scattering data analysis. J. Appl. Crystallogr. 39 (2006) 277-286
58. Guinier A. La diffraction des rayous X aux tres petits angles: application a l'etude de phenomenes ultramicroscopiques. Ann. Phys. (Paris) 12 (1939) 161-237
59. Svergun D.I. Determination of the regularization parameter in indirect transform method using perceptual criteria. J. Appl. Crystallogr. 25 (1992) 495-503
60. Porod G. General theory. In: Glatter O., and Kratky O. (Eds). Small-Angle X-ray Scattering (1982), Academic Press, London 17-51
61. Svergun D.I., Barberato C., and Koch M.H.J. CRYSOL-a program to evaluate X-ray solution scattering of biological macromolecules from atomic coordinates. J. Appl. Crystallogr. 28 (1995) 768-773
62. Volkov V.V., and Svergun D.I. Uniqueness of ab initio shape determination in small angle scattering. J. Appl. Crystallogr. 36 (2003) 860-864
63. Kozin M.B., and Svergun D.I. Automated matching of high- and low-resolution structural models. J. Appl. Crystallogr. 34 (2001) 33-41
64. 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
65. Karantza V., Baxevanis A.D., and Moundrianakis N. Thermodynamic studies of the core histones: ionic strength and pH dependence of H2A-H2B dimer stability. Biochemistry 34 (1995) 5988-5996
66. Schön A., and Freire E. Thermodynamics of intersubunit interactions in cholera toxin upon binding to the oligosaccharide portion of its cell surface receptor, ganglioside GM1. Biochemistry 28 (1989) 5019-5024