A quantitative investigation of linker histone interactions with nucleosomes and chromatin

Scientific Reports

Volumn 6, Issue , 2016, Pages

  White, Alison E ^a,b   Hieb, Aaron R ^a,c   Luger, Karolin ^a,b  

^a UNIVERSITY OF COLORADO   (United States)

^b Department of Environmental and Radiological Health Sciences   (United States)

^c GENENTECH INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHROMATIN; DNA; HISTONE; NUCLEOSOME; PROTEIN BINDING;

ANIMAL; CHEMISTRY; CHROMATIN; GENETICS; METABOLISM; MOUSE; NUCLEOSOME; PROTEIN DOMAIN;

ANIMALS; CHROMATIN; DNA; HISTONES; MICE; NUCLEOSOMES; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS;

EID: 84954112596     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep19122     Document Type: Article

References (46)

1. Izzo, A., Kamieniarz, K. & Schneider, R. The histone H1 family: specific members, specific functions ? Biological chemistry 389, 333-343, doi: 10.1515/BC.2008.037 (2008).
2. Woodcock, C. L., Skoultchi, A. I. & Fan, Y. Role of linker histone in chromatin structure and function: H1 stoichiometry and nucleosome repeat length. Chromosome Res 14, 17-25, doi: 10.1007/s10577-005-1024-3 (2006).
3. Kalashnikova, A. A. et al. Linker histone H1.0 interacts with an extensive network of proteins found in the nucleolus. Nucleic Acids Res 41, 4026-4035, doi: 10.1093/nar/gkt104 (2013).
4. Varga-Weisz, P., van Holde, K. & Zlatanova, J. Preferential binding of histone H1 to four-way helical junction DNA. J Biol Chem 268, 20699-20700 (1993).
5. Nightingale, K. P. & Becker, P. B. Structural and functional analysis of chromatin assembled from defined histones [In Process Citation]. Methods 15, 343-353 (1998).
6. Ura, K., Nightingale, K. & Wolffe, A. P. Differential association of HMG1 and linker histones B4 and H1 with dinucleosomal DNA: structural transitions and transcriptional repression. EMBO J 15, 4959-4969 (1996).
7. Luger, K., Mader, A. W., Richmond, R. K., Sargent, D. F. & Richmond, T. J. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389, 251-260, doi: 10.1038/38444 (1997).
8. Ramakrishnan, V., Finch, J. T., Graziano, V., Lee, P. L. & Sweet, R. M. Crystal structure of globular domain of histone H5 and its implications for nucleosome binding. Nature 362, 219-223 (1993).
9. Zhou, B. R. et al. Structural insights into the histone H1-nucleosome complex. PNAS 110, 19390-19395, doi: 10.1073/pnas.1314905110 (2013).
10. Vogler, C. et al. Histone H2A C-terminus regulates chromatin dynamics, remodeling, and histone H1 binding. PLoS Genet 6, e1001234, doi: 10.1371/journal.pgen.1001234 (2010).
11. Song, F. et al. Cryo-EM study of the chromatin fiber reveals a double helix twisted by tetranucleosomal units. Science 344, 376-380, doi: 10.1126/science.1251413 (2014).
12. Syed, S. H. et al. Single-base resolution mapping of H1-nucleosome interactions and 3D organization of the nucleosome. PNAS 107, 9620-9625, doi: 1000309107 (2010).
13. Cutter, A. R. & Hayes, J. J. A brief review of nucleosome structure. FEBS Lett, doi: 10.1016/j.febslet.2015.05.016 (2015).
14. Simpson, R. T. Structure of the chromatosome, a chromatin particle containing 160 base pairs of DNA and all the histones. Biochemistry 17, 5524-5531. (1978).
15. Hayes, J. J., Pruss, D. & Wolffe, A. P. Contacts of the globular domain of histone H5 and core histones with DNA in a "chromatosome". PNAS 91, 7817-7821 (1994).
16. Duggan, M. M. & Thomas, J. O. Two DNA-binding sites on the globular domain of histone H5 are required for binding to both bulk and 5 S reconstituted nucleosomes. J Mol Biol 304, 21-33, doi: 10.1006/jmbi.2000.4205 (2000).
17. Brown, D. T., Izard, T. & Misteli, T. Mapping the interaction surface of linker histone H1(0) with the nucleosome of native chromatin in vivo. Nat Struct Mol Biol 13, 250-255, doi: 10.1038/nsmb1050 (2006).
18. An, W., Leuba, S. H., van Holde, K. & Zlatanova, J. Linker histone protects linker DNA on only one side of the core particle and in a sequence-dependent manner. Proc Natl Acad Sci USA m 95, 3396-3401 (1998).
19. Pruss, D. et al. An asymmetric model for the nucleosome: a binding site for linker histones inside the DNA gyres. Science 274, 614-617 (1996).
20. Lowary, P. T. & Widom, J. New DNA sequence rules for high affinity binding to histone octamer and sequence-directed nucleosome positioning. J Mol Biol 276, 19-42. (1998).
21. Caterino, T. L., Fang, H. & Hayes, J. J. Nucleosome linker DNA contacts and induces specific folding of the intrinsically disordered H1 carboxyl-terminal domain. Mol Cell Biol 31, 2341-2348, doi: 10.1128/MCB.05145-11 (2011).
22. Nightingale, K. P., Pruss, D. & Wolffe, A. P. A single high affinity binding site for histone H1 in a nucleosome containing the Xenopus borealis 5 S ribosomal RNA gene. J Biol Chem 271, 7090-7094. (1996).
23. Hieb, A. R., D'Arcy, S., Kramer, M. A., White, A. E. & Luger, K. Fluorescence strategies for high-throughput quantification of protein interactions. Nucleic Acids Res 40, e33, doi: gkr1045 (2012).
24. Stasevich, T. J., Mueller, F., Brown, D. T. & McNally, J. G. Dissecting the binding mechanism of the linker histone in live cells: an integrated FRAP analysis. EMBO J 29, 1225-1234, doi: 10.1038/emboj.2010.24 (2010).
25. Hendzel, M. J., Lever, M. A., Crawford, E. & Th'ng, J. P. The C-terminal domain is the primary determinant of histone H1 binding to chromatin in vivo. J Biol Chem 279, 20028-20034 (2004).
26. Vyas, P. & Brown, D. T. N- and C-terminal domains determine differential nucleosomal binding geometry and affinity of linker histone isotypes H1(0) and H1c. J Biol Chem 287, 11778-11787, doi: 10.1074/jbc.M111.312819 (2012).
27. Caterino, T. L. & Hayes, J. J. Structure of the H1 C-terminal domain and function in chromatin condensation. Biochem Cell Biol 89, 35-44, doi: o10-024 (2011).
28. Lu, X., Hamkalo, B., Parseghian, M. H. & Hansen, J. C. Chromatin condensing functions of the linker histone C-terminal domain are mediated by specific amino acid composition and intrinsic protein disorder. Biochemistry 48, 164-172, doi: 10.1021/ bi801636y10.1021/bi801636y (2009).
29. Clark, D. J., Hill, C. S., Martin, S. R. & Thomas, J. O. Alpha-helix in the carboxy-terminal domains of histones H1 and H5. EMBO J 7, 69-75 (1988).
30. Roque, A., Ponte, I. & Suau, P. Role of charge neutralization in the folding of the carboxy-terminal domain of histone H1. J Phys Chem B 113, 12061-12066, doi: 10.1021/jp9022579 (2009).
31. Assenberg, R. et al. A critical role in structure-specific DNA binding for the acetylatable lysine residues in HMGB1. Biochem J 411, 553-561, doi: 10.1042/BJ20071613 (2008).
32. Muthurajan, U. M. et al. Automodification switches PARP-1 function from chromatin architectural protein to histone chaperone. PNAS 111, 12752-12757, doi: 10.1073/pnas.1405005111 (2014).
33. Lu, X. & Hansen, J. C. Identification of specific functional subdomains within the linker histone H10 C-terminal domain. J Biol Chem 279, 8701-8707 (2004).
34. Ura, K., Wolffe, A. P. & Hayes, J. J. Core histone acetylation does not block linker histone binding to a nucleosome including a Xenopus borealis 5 S rRNA gene. J Biol Chem 269, 27171-27174 (1994).
35. Fang, H., Clark, D. J. & Hayes, J. J. DNA and nucleosomes direct distinct folding of a linker histone H1 C-terminal domain. Nucleic Acids Res 40, 1475-1484, doi: 10.1093/nar/gkr866 (2012).
36. Clark, D. J. & Thomas, J. O. Salt-dependent co-operative interaction of histone H1 with linear DNA. J Mol Biol 187, 569-580 (1986).
37. Hayes, J. J. & Wolffe, A. P. Preferential and asymmetric interaction of linker histones with 5 S DNA in the nucleosome. PNAS 90, 6415-6419 (1993).
38. Zhou, B. R. et al. Structural Mechanisms of Nucleosome Recognition by Linker Histones. Mol Cell 59, 628-638, doi: 10.1016/j.molcel.2015.06.025 (2015).
39. Bussiek, M., Toth, K., Schwarz, N. & Langowski, J. Trinucleosome compaction studied by fluorescence energy transfer and scanning force microscopy. Biochemistry 45, 10838-10846, doi: 10.1021/bi060807p (2006).
40. Lu, X. & Hansen, J. C. Revisiting the structure and functions of the linker histone C-terminal tail domain. Biochem Cell Biol 81, 173-176 (2003).
41. Thastrom, A., Bingham, L. M. & Widom, J. Nucleosomal locations of dominant DNA sequence motifs for histone-DNA interactions and nucleosome positioning. J Mol Biol 338, 695-709 (2004).
42. Dyer, P. N. et al. Reconstitution of nucleosome core particles from recombinant histones and DNA. Methods Enzymol 375, 23-44 (2004).
43. Webb, M. & Thomas, J. O. Structure-specific binding of the two tandem HMG boxes of HMG1 to four-way junction DNA is mediated by the A domain. J Mol Biol 294, 373-387, doi: 10.1006/jmbi.1999.3150 (1999).
44. Muthurajan, U. M., McBryant, S. J., Lu, X., Hansen, J. C. & Luger, K. The linker region of macroH2A promotes self-association of nucleosomal arrays. J Biol Chem 286, 23852-23864, doi: M111.244871 (2011).
45. Winkler, D. D., Muthurajan, U. M., Hieb, A. R. & Luger, K. Histone chaperone FACT coordinates nucleosome interaction through multiple synergistic binding events. J Biol Chem 286, 41883-41892, doi: 10.1074/jbc.M111.301465 (2011).
46. Rogge, R. A. et al. Assembly of nucleosomal arrays from recombinant core histones and nucleosome positioning DNA. Journal of visualized experiments: JoVE, doi: 10.3791/50354 (2013).