Large multimeric assemblies of nucleosome assembly protein and histones revealed by small-angle x-ray scattering and electron microscopy

Journal of Biological Chemistry

Volumn 287, Issue 32, 2012, Pages 26657-26665

  Newman, Emily R ^a,d   Kneale, G Geoff ^a   Ravelli, Raimond B G ^b   Karuppasamy, Manikandan ^b,d   Nejadasl, Fatemeh Karimi ^b   Taylor, Ian A ^c   McGeehan, John E ^a  

^a UNIVERSITY OF PORTSMOUTH   (United Kingdom)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^c NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^d EUROPEAN MOLECULAR BIOLOGY LABORATORY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANALYTICAL ULTRACENTRIFUGATION; CELL VIABILITY; CRYO-ELECTRON MICROSCOPY; MULTIANGLE LASER LIGHT SCATTERING; MULTIMERIC; MULTIMERS; NUCLEOSOME ASSEMBLY PROTEINS; SINGLE-PARTICLE; SMALL ANGLE X-RAY SCATTERING; X-RAY STRUCTURE; XENOPUS LAEVIS;

CENTRIFUGATION; ELECTRON MICROSCOPES; ELECTRON MICROSCOPY; OLIGOMERS; STOICHIOMETRY; X RAY SCATTERING; X RAYS;

PROTEINS;

HISTONE; HISTONE H2A; HISTONE H2B; HISTONE H3; HISTONE H4; NUCLEOSOME ASSEMBLY PROTEIN 1;

ARTICLE; COMPLEX FORMATION; CRYOELECTRON MICROSCOPY; ELECTRON MICROSCOPY; GEL PERMEATION CHROMATOGRAPHY; LIGHT SCATTERING; NONHUMAN; NUCLEOSOME; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN PURIFICATION; STOICHIOMETRY; ULTRACENTRIFUGATION; X RAY CRYSTALLOGRAPHY; XENOPUS LAEVIS;

ANIMALS; CHROMATOGRAPHY, GEL; CRYOELECTRON MICROSCOPY; ELECTROPHORESIS, POLYACRYLAMIDE GEL; HISTONES; NUCLEOSOME ASSEMBLY PROTEIN 1; SCATTERING, SMALL ANGLE; ULTRACENTRIFUGATION; X-RAY DIFFRACTION; XENOPUS LAEVIS;

XENOPUS LAEVIS;

EID: 84864556292     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.340422     Document Type: Article

References (48)

1. Akey, C. W., and Luger, K. (2003) Histone chaperones and nucleosome assembly. Curr. Opin. Struct. Biol. 13, 6-14 (Pubitemid 36170249)
2. Kleinschmidt, J. A., Seiter, A., and Zentgraf, H. (1990) Nucleosome assembly in vitro: separate histone transfer and synergistic interaction of native histone complexes purified from nuclei of Xenopus laevis oocytes. EMBO J. 9, 1309-1318
3. Luger, K., Mäder, A. W., Richmond, R. K., Sargent, D. F., and Richmond, T. J. (1997) Crystal structure of the nucleosome core particle at 2.8 Åresolution. Nature 389, 251-260 (Pubitemid 27406632)
4. Tse, C., Sera, T., Wolffe, A. P., and Hansen, J. C. (1998) Disruption of higher order folding by core histone acetylation dramatically enhances transcription of nucleosomal arrays by RNA polymerase III. Mol. Cell. Biol. 18, 4629-4638 (Pubitemid 28343048)
5. Karantza, V., Freire, E., and Moudrianakis, E. N. (1996) Thermodynamic studies of the core histones: pH and ionic strength effects on the stability of the (H3-H4)/(H3-H4)2 system. Biochemistry 35, 2037-2046 (Pubitemid 26062654)
6. Hondele, M., and Ladurner, A. G. (2011) The chaperone-histone partnership: for the greater good of histone traffic and chromatin plasticity. Curr. Opin. Struct. Biol. 21, 698-708
7. Tyler, J. K. (2002) Chromatin assembly. Cooperation between histone chaperones and ATP-dependent nucleosome remodeling machines. Eur. J. Biochem. 269, 2268-2274
8. Taneva, S. G., Muñoz, I. G., Franco, G., Falces, J., Arregi, I., Muga, A., Montoya, G., Urbaneja, M. A., and Bañuelos, S. (2008) Activation of nucleoplasmin, an oligomeric histone chaperone, challenges its stability. Biochemistry 47, 13897-13906
9. Natsume, R., Eitoku, M., Akai, Y., Sano, N., Horikoshi, M., and Senda, T. (2007) Structure and function of the histone chaperone CIA/ASF1 complexed with histones H3 and H4. Nature 446, 338-341 (Pubitemid 46437114)
10. Zhou, Z., Feng, H., Hansen, D. F., Kato, H., Luk, E., Freedberg, D. I., Kay, L. E., Wu, C., and Bai, Y. (2008) NMR structure of chaperone Chz1 complexed with histones H2A.Z-H2B. Nat. Struct. Mol. Biol. 15, 868-869
11. Kepert, J. F., Mazurkiewicz, J., Heuvelman, G. L., Tóth, K. F., and Rippe, K. (2005) NAP1 modulates binding of linker histone H1 to chromatin and induces an extended chromatin fiber conformation. J. Biol. Chem. 280, 34063-34072 (Pubitemid 41443129)
12. 2 tetramer by NAP1 is mediated by the amino-terminal histone tails. J. Biol. Chem. 278, 44574-44583
13. Park, Y. J., Chodaparambil, J. V., Bao, Y., McBryant, S. J., and Luger, K. (2005) Nucleosome assembly protein 1 exchanges histone H2A-H2B dimers and assists nucleosome sliding. J. Biol. Chem. 280, 1817-1825
14. Ito, T., Bulger, M., Kobayashi, R., and Kadonaga, J. T. (1996) Drosophila NAP1 is a core histone chaperone that functions in ATP-facilitated assembly of regularly spaced nucleosomal arrays. Mol. Cell. Biol. 16, 3112-3124
15. Fyodorov, D. V., and Kadonaga, J. T. (2003) Chromatin assembly in vitro with purified recombinant ACF and NAP1. Methods Enzymol. 371, 499-515 (Pubitemid 37542753)
16. Lorch, Y., Maier-Davis, B., and Kornberg, R. D. (2006) Chromatin remodeling by nucleosome disassembly in vitro. Proc. Natl. Acad. Sci. U.S.A. 103, 3090-3093 (Pubitemid 43346429)
17. Santos, S. F., Zanette, D., Fischer, H., and Itri, R. (2003) A systematic study of bovine serum albumin (BSA) and sodium dodecyl sulfate (SDS) interactions by surface tension and small-angle x-ray scattering. J. Colloid Interface Sci. 262, 400-408 (Pubitemid 36627519)
18. Rattner, B. P., Yusufzai, T., and Kadonaga, J. T. (2009) HMGN proteins act in opposition to ATP-dependent chromatin-remodeling factors to restrict nucleosome mobility. Mol. Cell 34, 620-626
19. Zhang, Y., Moqtaderi, Z., Rattner, B. P., Euskirchen, G., Snyder, M., Kadonaga, J. T., Liu, X. S., and Struhl, K. (2009) Intrinsic histone-DNA interactions are not the major determinant of nucleosome positions in vivo. Nat. Struct. Mol. Biol. 16, 847-852
20. Torigoe, S. E., Urwin, D. L., Ishii, H., Smith, D. E., and Kadonaga, J. T. (2011) Identification of a rapidly formed non-nucleosomal histone-DNA intermediate that is converted into chromatin by ACF. Mol. Cell 43, 638-648
21. Krogan, N. J., and Hughes, T. R. (2006) Signals and systems. Genome Biol. 7, 313
22. Altman, R., and Kellogg, D. (1997) Control of mitotic events by Nap1 and the Gin4 kinase. J. Cell Biol. 138, 119-130 (Pubitemid 27337457)
23. De Koning, L., Corpet, A., Haber, J. E., and Almouzni, G. (2007) Histone chaperones: an escort network regulating histone traffic. Nat. Struct. Mol. Biol. 14, 997-1007 (Pubitemid 350060337)
24. Ishimi, Y., Yasuda, H., Hirosumi, J., Hanaoka, F., and Yamada, M. (1983) A protein which facilitates assembly of nucleosome-like structures in vitro in mammalian cells. J. Biochem. 94, 735-744
25. Tóth, K. F., Mazurkiewicz, J., and Rippe, K. (2005) Association states of nucleosome assembly protein 1 and its complexes with histones. J. Biol. Chem. 280, 15690-15699 (Pubitemid 40616688)
26. Zlatanova, J., Seebart, C., and Tomschik, M. (2007) Nap1: taking a closer look at a juggler protein of extraordinary skills. FASEB J. 21, 1294-1310 (Pubitemid 46684833)
27. Andrews, A. J., Downing, G., Brown, K., Park, Y. J., and Luger, K. (2008) A thermodynamic model for Nap1-histone interactions. J. Biol. Chem. 283, 32412-32418
28. McQuibban, G. A., Commisso-Cappelli, C. N., and Lewis, P. N. (1998) Assembly, remodeling, and histone binding capabilities of yeast nucleosome assembly protein 1. J. Biol. Chem. 273, 6582-6590 (Pubitemid 28144757)
29. Noda, M., Uchiyama, S., McKay, A. R., Morimoto, A., Misawa, S., Yoshida, A., Shimahara, H., Takinowaki, H., Nakamura, S., Kobayashi, Y., Matsunaga, S., Ohkubo, T., Robinson, C. V., and Fukui, K. (2011) Assembly states of the nucleosome assembly protein 1 (NAP1) revealed by sedimentation velocity and nondenaturing MS. Biochem. J. 436, 101-112
30. Bowman, A., Ward, R., Wiechens, N., Singh, V., El-Mkami, H., Norman, D. G., and Owen-Hughes, T. (2011) The histone chaperones Nap1 and Vps75 bind histones H3 and H4 in a tetrameric conformation. Mol. Cell 41, 398-408
31. Park, Y. J., and Luger, K. (2006) The structure of nucleosome assembly protein 1. Proc. Natl. Acad. Sci. U.S.A. 103, 1248-1253
32. Gill, J., Yogavel, M., Kumar, A., Belrhali, H., Jain, S. K., Rug, M., Brown, M., Maier, A. G., and Sharma, A. (2009) Crystal structure of malaria parasite nucleosome assembly protein: distinct modes of protein localization and histone recognition. J. Biol. Chem. 284, 10076-10087
33. Friedeberg, C., Scarlett, G., McGeehan, J., Abu-Daya, A., Guille, M., and Kneale, G. (2006) Identification of a structural and functional domain in xNAP1 involved in protein-protein interactions. Nucleic Acids Res. 34, 4893-4899 (Pubitemid 44605632)
34. Philo, J. S. (2006) Improved methods for fitting sedimentation coefficient distributions derived by time-derivative techniques. Anal. Biochem. 354, 238-246
35. Schuck, P. (2000) Size distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and Lamm equation modeling. Biophys. J. 78, 1606-1619
36. Konarev, P. V., Volkov, V. V., Sokolova, A. V., Koch, M. H., and Svergun, D. I. (2003) PRIMUS: a Windows PC-based system for small-angle scattering data analysis. J. Appl. Crystallogr. 36, 1277-1282
37. Svergun, D. I. (1992) Determination of the regularization parameter in indirect-transform methods using perceptual criteria. J. Appl. Crystallogr. 25, 495-503
38. Franke, D., and Svergun, D. I. (2009) DAMMIF, a program for rapid ab initio shape determination in small-angle scattering. J. Appl. Crystallogr. 42, 342-346
39. Volkov, V. V., and, Svergun, D. I. (2003) Uniqueness of ab initio shape determination in small-angle scattering. J. Appl. Crystallogr. 36, 860-864
40. Karuppasamy, M., Karimi Nejadasl, F., Vulovic, M., Koster, A. J., and Ravelli, R. B. (2011) Radiation damage in single-particle cryo-electron microscopy: effects of dose and dose rate. J. Synchrotron Radiat. 18, 398-412
41. Scheres, S. H., Núñez-Ramírez, R., Sorzano, C. O., Carazo, J. M., and Marabini, R. (2008) Image processing for electron microscopy single-particle analysis using XMIPP. Nat. Protoc. 3, 977-990 (Pubitemid 351818686)
42. Tang, G., Peng, L., Baldwin, P. R., Mann, D. S., Jiang, W., Rees, I., and Ludtke, S. J. (2007) EMAN2: an extensible image processing suite for electron microscopy. J. Struct. Biol. 157, 38-46 (Pubitemid 44880785)
43. Kastner, B., Fischer, N., Golas, M. M., Sander, B., Dube, P., Boehringer, D., Hartmuth, K., Deckert, J., Hauer, F., Wolf, E., Uchtenhagen, H., Urlaub, H., Herzog, F., Peters, J. M., Poerschke, D., Lührmann, R., and Stark, H. (2008) GraFix: sample preparation for single-particle electron cryomicroscopy. Nat. Methods 5, 53-55
44. Stark, H. (2010) GraFix: stabilization of fragile macromolecular complexes for single-particle cryo-EM. Methods Enzymol. 481, 109-126
45. De Carlo, S., and Stark, H. (2010) Cryonegative staining of macromolecular assemblies. Methods Enzymol. 481, 127-145
46. Friedeberg, C. (2005) Structural and Functional Characterization of the Nucleosome Assembly Protein, xNAP1. Ph.D. thesis, The University of Portsmouth
47. Park, Y. J., McBryant, S. J., and Luger, K. (2008) A β-hairpin comprising the nuclear localization sequence sustains the self-associated states of nucleosome assembly protein 1. J. Mol. Biol. 375, 1076-1085 (Pubitemid 50010799)
48. McBryant, S. J., and Peersen, O. B. (2004) Self-association of the yeast nucleosome assembly protein 1. Biochemistry 43, 10592-10599 (Pubitemid 39079329)