Activation of nucleoplasms, an oligomeric histone chaperone, challenges its stability

Biochemistry

Volumn 47, Issue 52, 2008, Pages 13897-13906

  Taneva, Stefka G ^a   Muñoz, Inés G ^b   Franco, Guillermo ^a   Falces, Jorge ^a   Arregi, Igor ^a   Muga, Arturo ^a   Montoya, Guillermo ^b   Urbaneja, María A ^a   Bañuelos, Sonia ^a  

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

^b Centro Nacional de Investigaciones Oncológicas   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL FUNCTIONS; CHROMATIN REMODELING; DECONDENSATION; ELECTROSTATIC REPULSION; FULL-LENGTH PROTEINS; HIGH STABILITY; HYDRODYNAMIC PROPERTIES; NEGATIVE CHARGE; NUCLEAR LOCALIZATION SIGNAL; NUCLEOPLASMIN; PENTAMERS; PROTEIN A; QUATERNARY INTERACTIONS; STABLE STRUCTURES; WILD TYPES;

CHEMICAL ACTIVATION; OLIGOMERIZATION; PHOSPHORYLATION; PROTEINS;

CRYSTAL STRUCTURE;

NUCLEOPLASMIN; CHAPERONE; HISTONE; NUCLEAR PROTEIN; PHOSPHOPROTEIN;

ARTICLE; BIOLOGICAL ACTIVITY; CIRCULAR DICHROISM; CRYSTAL STRUCTURE; ENZYME ACTIVATION; GEL FILTRATION CHROMATOGRAPHY; MUTATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; PROTEIN PURIFICATION; PROTEIN QUATERNARY STRUCTURE; PROTEIN STABILITY; PROTEIN STRUCTURE; X RAY CRYSTALLOGRAPHY; CHEMISTRY; HYDROPHOBICITY; NUCLEAR LOCALIZATION SIGNAL; PHOSPHORYLATION; PROTEIN CONFORMATION; STATIC ELECTRICITY;

CRYSTALLOGRAPHY, X-RAY; HISTONES; HYDROPHOBICITY; MOLECULAR CHAPERONES; NUCLEAR LOCALIZATION SIGNALS; NUCLEAR PROTEINS; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN CONFORMATION; PROTEIN STABILITY; PROTEIN STRUCTURE, QUATERNARY; STATIC ELECTRICITY;

EID: 58849107655     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi800975r     Document Type: Article

References (45)

1. Frehlick, L. J., Eirín-López, J. M., and Ausió, J. (2007) New insights into the nucleophosmin/nucleoplasmin family of nuclear chaperones. BioEssays 29, 49-59.
2. Prado, A., Ramos, I., Frehlick, L. J., Muga, A., and Ausió, J. (2004) Nucleoplasmin: a nuclear chaperone. Biochem. Cell Biol. 82, 437-445.
3. Akey, C. W., and Luger, K. (2003) Histone chaperones and nucleosome assembly. Curr. Opin. Struct. Biol. 13, 6-14.
4. Gillespie, P. J., and Blow, J. J. (2000) Nucleoplasmin-mediated chromatin remodelling is required for Xenopus sperm nuclei to become licensed for DNA replication. Nucleic Acids Res. 28, 472-480.
5. Tamada, H., Thuan, N. V., Reed, P., Nelson, D., Katoku-Kikyo, N., Wudel, J., Wakayama, T., and Kikyo, M. (2006) Chromatin decondensation and nuclear reprogramming by nucleoplasmin. Mol. Cell. Biol. 26, 1259-1271.
6. Dutta, S., Akey, I. V., Dingwall, C., Hartman, K. L., Laue, T., Nolte, R. T., Head, J. F., and Akey, C. W. (2001) The crystal structure of nucleoplasmin-core: implications for histone binding and nucleosome assembly. Mol. Cell 8, 841-853.
7. Namboodiri, H. V. M., Dutta, S., Akey, I. V., Head, J. F., and Akey, C. W. (2003) The crystal structure of Drosophila NLP-core provides insight into pentamer formation and histone binding. Structure 11, 175-186.
8. Namboodiri, H. V. M., Akey, I. V., Schmidt-Zachmann, M. S., Head, J. F., and Akey, C. W. (2004) The structure and function of Xenopus N038-core, a histone chaperone in the nucleolus. Structure 12, 2149-2160.
9. Hierro, A., Arizmendi, J. M., Bañuelos, S., Prado, A., and Muga, A. (2002) Electrostatic interactions at the C-terminal domain of nucleoplasmin modulate its chromatin decondensation activity. Biochemistry 41, 6408-6413.
10. Hierro, A., Arizmendi, J. M., De las Rivas, J., Urbaneja, M. A., Prado, A., and Muga, A. (2001) Structural and functional properties of Escherichia coli-derived nucleoplasmin. A comparative study of recombinant and natural proteins. Eur. J. Biochem. 268, 1739-1748.
11. Sickmeier, M., Hamilton, J. A., Le Gall, T., Vacic, V., Cortese, M. S., Tantos, A., Szabo, B., Tompa, P., Chen, J., Uversky, V. N., Obradovic, Z., and Dunker, A. K. (2007) DisProt: the database of disordered proteins. Nucleic Acids Res. 35, D787-D793.
12. Cotten, M., Sealy, L., and Chalkley, R. (1986) Massive phosphorylation distinguishes Xenopus laevis nucleoplasmin isolated from oocytes or unfertilized eggs. Biochemistry 25, 5063-5069.
13. Bañuelos, S., Omaetxebarria, M. J., Ramos, I., Larsen, M. R., Arregi, I., Jensen, O. M., Arizmendi, J. M., Prado, A., and Muga, A. (2007) Phosphorylation of both nucleoplasmin domains is required for activation of its chromatin decondensation activity. J. Biol. Chem. 282, 21213-21221.
14. Bañuelos, S., Hierro, A., Arizmendi, J. M., Montoya, C., Prado, A., and Muga, A. (2003) Activation mechanism of the nuclear chaperone nucleoplasmin: role of the core domain. J. Mol. Biol. 334, 585-593.
15. Franco, C., Bañuelos, S., Falces, J., Muga, A., and Urbaneja, M. A. (2008) Thermodynamic characterization of nucleoplasmin unfolding: interplay between function and stability. Biochemistry 47, 7954-7962.
16. Ben-Bassat, A., Bauer, K., Chang, S. Y., Myambo, K., Boosman, A., and Chang, S. (1987) Processing of the initiation methionine from proteins: properties of the Escherichia coli methionine aminopeptidase and its gene structure. J. Bacteriol. 169, 751-757.
17. Kleywegt, C. J., and Brünger, A. T. (1996) Checking your imagination: applications of the free R value. Structure 4, 897-904.
18. Kissinger, C. R., Gehlhaar, D. K., and Fogel, D. B. (1999) Rapid automated molecular replacement by evolutionary search. Acta Crystallogr., Sect. D: Biol. Crystallogr. 55, 484-491.
19. Thompson, J. D., Higgins, D. C., and Gibson, T. J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673-4680.
20. Murshudov, C. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximumlikelihood method. Acta Crystallogr., Sect. D: Biol. Crystallogr. 53, 240-255.
21. Jones, T. A., Zou, J.-Y., Cowan, S. W., and Kjeldgaard, M. (1991) Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A47, 110-119.
22. Cowtan, K., and Main, P. (1998) Miscellaneous algorithms for density modification. Acta Crystallogr., Sect. D: Biol. Crystallogr. 54, 487-493.
23. Laskowski, R. A., Moss, D. S., and Thornton, J. M. (1993) Mainchain bond lengths and bond angles in protein structures. J. Mol. Biol. 231, 1049-1067.
24. Kholodenko, V., and Freire, E. (1999) A simple method to measure the absolute heat capacity of proteins. Anal. Biochem. 270, 336-338.
25. Arnan, C., Saperas, N., Prieto, C., Chiva, M., and Ausió, J. (2003) Interaction of nucleoplasmin with core histones. J. Biol. Chem. 278, 31319-31324.
26. Sánchez-Ruiz, J. M., López-Lacomba, J. L., Cortijo, M., and Mateo, P. L. (1988) Differential scanning calorimetry of the irreversible thermal denaturation of thermolysin. Biochemistry 27, 1648-1672.
27. Kurganov, B. I., Lyubarev, A. E., Sánchez-Ruiz, J. M., and Shnyrov, V. L. (1997) Analysis of differential scanning calorimetry data for proteins. Criteria of validity of one-step mechanism of irreversible protein denaturation. Biophys. Chem. 69, 125-135.
28. Whitmore, L., and Wallace, B. A. (2008) Protein secondary structure analyses from circular dichroism spectroscopy: methods and reference databases. Biopolymers 89, 392-400.
29. Lees, J. C., Miles, A. J., Wien, F., and Wallace, B. A. (2006) A reference database for circular dichroism spectroscopy covering fold and secondary structure space. Bioinformatics 22, 1955-1962.
30. Salvany, L., Chiva, L., Aman, C., Ausió, J., Subirana, J. A., and Saperas, N. (2004) Mutation of the small acidic tract Al drastically reduces nucleoplasmin activity. FEBS Lett. 576, 353-357.
31. Freire, E., Murphy, K. P., Sánchez-Ruiz, J. M., Galisteo, M. L., and Privalov, P. L. (1992) The molecular basis of cooperativity in protein folding. Thermodynamic dissection of interdomain interactions in phosphoglycerate kinase. Biochemistry 31, 250-256.
32. Sánchez-Ruiz, J. M. (1995) Differential scanning calorimetry of proteins. Subcell. Biochem. 24, 133-176.
33. Georgescu, R. E., García-Mira, M. M., Tasayco, M. L., and Sánchez-Ruiz, J. M. (2001) Heat capacity analysis of oxidized Escherichia coli thioredoxin fragments (1-73, 74-108) and their noncovalent complex. Evidence for the burial of apolar surface in protein unfolded states. Eur. J. Biochem. 268, 1477-1485.
34. Pina, D. C., Gómez, J., Villar, E., Johannes, L., and Shnyrov, V. L. (2003) Thermodynamic analysis of the structural stability of the shiga toxin B-subunit. Biochemistry 42, 9498-9506.
35. Tholey, A., Lindermann, A., Kinzel, V., and Reed, J. (1999) Direct effects of phosphorylation on the preferred backbone conformation of peptides: a nuclear magnetic resonance study. Biophys. J. 76, 76-87.
36. Ramos, I., Prado, A., Finn, R. M., Muga, A., and Ausid, J. (2005) Nucleoplasmin-mediated unfolding of chromatin involves the displacement of linker-associated chromatin proteins. Biochemistry 44, 8274-8281.
37. Johnson, L. N., and Lewis, R. J. (2001) Structural basis for control by phosphorylation. Chem. Rev. 101, 2209-2242.
38. Graves, J. D., and Krebs, E. G. (1999) Protein phosphorylation and signal transduction. Pharmacol. Ther. 82, 111-121.
39. Hierro, A. (2002) Efecto de la fosforilación sobre la estructura y función de la nucleoplasmina, Ph.D. Thesis, University of the Basque Country.
40. Miranda, F. F., Teigen, K., Thórólfsson, M., Svebak, R. M., Knappskog, P. M., Flatmark, T., and Martínez, A. (2002) Phosphorylation and mutations of Ser(16) in human phenylalanine hydroxylase. Kinetic and structural effects. J. Biol. Chem. 277, 40937-40943.
41. Honnappa, S., Jahnke, W., Seelig, J., and Steinmetz, M. O. (2006) Control of intrinsically disordered stathmin by multisite phosphorylation. J. Biol. Chem. 281, 16078-16083.
42. Blanes-Mira, C., Ibáñez, C., Fernández-Ballester, C., PlanellsCases, R., Pérez-Payá, E., and Ferrer-Montiel, A. (2001) Thermal stabilization of the catalytic domain of botulinum neurotoxin E by phosphorylation of a single tyrosine residue. Biochemistry 40, 2234-2242.
43. Nosworthy, N. J., Peterkofsky, A., König, S., Seok, Y. J., Szczepanowski, R. H., and Ginsburg, A. (1998) Phosphorylation destabilizes the amino-terminal domain of enzyme I of the Escherichia coli phosphoenolpyruvate: sugar phosphotransferase system. Biochemistry 37, 6718-6726.
44. Ahmad, M. F., Raman, B., Ramakrishna, T., and Rao, Ch. M. (2008) Effect of phosphorylation on alpha B-crystallin: differences in stability, subunit exchange and chaperone activity of homo and mixed oligomers of alpha B-crystallin and its phosphorylation-mimicking mutant. J. Mol. Biol. 375, 1040-1051.
45. Lu, Z., Zhang, C., and Zhai, Z. (2005) Nucleoplasmin regulates chromatin condensation during apoptosis. Proc. Natl. Acad. Sci. U.S.A. 102, 2778-2783.