Dynamic condensation of linker histone C-terminal domain regulates chromatin structure

Nucleic Acids Research

Volumn 42, Issue 12, 2014, Pages 7553-7560

  Luque, Antoni ^a   Collepardo Guevara, Rosana ^b   Grigoryev, Sergei ^c   Schlick, Tamar ^a,d  

^a NEW YORK UNIVERSITY   (United States)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c PENN STATE COLLEGE OF MEDICINE   (United States)

^d NEW YORK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; HISTONE;

ARTICLE; CARBOXY TERMINAL DOMAIN; CARBOXY TERMINAL SEQUENCE; CHROMATIN STRUCTURE; COMPUTER MODEL; EPIGENETICS; GENE STRUCTURE; IN VITRO STUDY; IN VIVO STUDY; NUCLEOSOME; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM;

CHROMATIN; HISTONES; MAGNESIUM; MODELS, MOLECULAR; NUCLEOSOMES; PROTEIN STRUCTURE, TERTIARY;

EID: 84903979437     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku491     Document Type: Article

References (58)

1. Felsenfeld, G., Groudine, M. (2003) Controlling the double helix. Nature, 421, 448-453.
2. Szerlong, H., Hansen, J. (2011) Nucleosome distribution and linker DNA: connecting nuclear function to dynamic chromatin structure. Biochem. Cell Biol., 89, 24-34.
3. Grigoryev, S., Woodcock, C. (2012) Chromatin organization - the 30 nm fiber. Exp. Cell Res., 318, 1448-1455.
4. Quenet, D., McNally, J., Dalai, Y. (2012) Through thick and thin: the conundrum of chromatin fibre folding in vivo. EMBO Rep., 13, 943-944.
5. Schlick, T., Hayes, J., Grigoryev, S. (2012) Towards convergence of experimental studies and theoretical modeling of the chromatin fiber. J. Biol. Chem., 287, 5183-5191.
6. Caterino, T., Hayes, J. (2011) Structure of the H1 C-terminal domain and function in chromatin condensation. Biochem. Cell Biol., 89, 35-44.
7. Misteli, T., Gunjan, A., Hock, R., Bustin, M., Brown, D. (2000) Dynamic binding of histone H1 to chromatin in living cells. Nature, 408, 877-881.
8. Fan, Y., Nikitina, T., Zhao, J., Fleury, T., Bhattacharyya, R., Bouhassira, E., Stein, A., Woodcock, C., Skoultchi, A. (2005) Depletion of histone H1 in mammals alters global chromatin structure but causes specific changes in gene regulation. Cell, 123, 1119-1212.
9. Popova, E., Grigoryev, S., Fan, Y., Skoultchi, A., Zhang, S., Barnstable, C. (2013) Developmentally regulated linker histone h1c promotes heterochromatin condensation and mediates structural integrity of rod photoreceptors in mouse retina. J. Biol. Chem., 288, 17895-17907.
10. Routh, A., Sandin, S., Rhodes, D. (2008) Nucleosome repeat length and linker histone stoichiometry determine chromatin fiber structure. Proc. Natl. Acad. Sci. U.S.A., 105, 8872-8877.
11. Grigoryev, S., Arya, G., Correll, S., Woodcock, C., Schlick, T. (2009) Evidence for heteromorphic chromatin fibers from analysis of nucleosome interactions. Proc. Natl. Acad. Sci. U.S.A., 106, 13317-13322.
12. Meyer, S., Becker, N., Syed, S., Goutte-Gattat, D., Shukla, M., Hayes, J., Angelov, D., Bednar, J., Dimitrov, S., Everaers, R. (2011) From crystal and NMR structures, footprints and cryo-electron-micrographs to large and soft structures: nanoscale modeling of the nucleosomal stem. Nucleic Acids Res., 39, 9139-9154.
13. Bussiek, M., Toth, K., Schwarz, N., Langowski, J. (2006) Trinucleosome compaction studied by fluorescence energy transfer and scanning force microscopy. Biochemistry, 45, 10838-10846.
14. Bednar, J., Horowitz, R., Grigoryev, S., Carruthers, L., Hansen, J., Koster, A., Woodcock, C. (1998) Nucleosomes, linker DNA, and linker histone form a unique structural motif that directs the higher-order folding and compaction of chromatin. Proc. Natl. Acad. Sci. U.S.A., 95, 14173-14178.
15. Perisic, O., Collepardo-Guevara, R., Schlick, T. (2010) Modeling studies of chromatin fiber structure as a function of DNA linker length. J. Mol. Biol., 403, 777-802.
16. Jerzmanowski, A. (2004) The linker histones. In: Zlatanova, J., Leuba, S.H., (eds.), Chromatin Structure and Dynamics: State-of-the-Art, Elsevier B.V. 75-102.
17. Ramakrishnan, V., Finch, J., Graziano, V., Lee, P., Sweet, R. (1993) Crystal structure of globular domain of histone H5 and its implications for nucleosome binding. Nature, 362, 219-223.
18. Ali, T., Coles, P., Stevens, T., Stott, K., Thomas, J. (2004) Two homologous domains of similar structure but different stability in the yeast linker histone, Hho1p. J. Mol. Biol., 338, 139-48.
19. Cerf, C., Lippens, G., Ramakrishnan, V., Muyldermans, S., Segers, A., Wyns, L., Wodak, S., Hallenga, K. (1994) Homo- and heteronuclear two-dimensional NMR studies of the globular domain of histone H1: full assignment, tertiary structure, and comparison with the globular domain of histone H5. Biochemistry, 33, 11079-11086.
20. Allan, J., Hartman, P., Crane-Robinson, C. (1980) The structure of histone H1 and its location in chromatin. Nature, 288, 675-679.
21. Bharath, M., Chandra, N., Rao, M. (2003) Molecular modeling of the chromatosome particle. Nucleic Acids Res., 31, 4264-4274.
22. Fan, L., Roberts, V. (2006) Complex of linker histone H5 with the nucleosome and its implications for chromatin packing. Proc. Natl. Acad. Sci. U.S.A., 103, 8384-8389.
23. Zhou, B.-R., Feng, H., Kato, H., Dai, L., Yang, Y., Zhou, Y., Bai, Y. (2013) Structural insights into the histone H1-nucleosome complex. Proc. Natl. Acad. Sci. U.S.A., 110, 19390-19395.
24. Allan, J., Mitchell, T., Harborne, N., Bohm, L., Crane-Robin-son, C. (1986) Roles of H1 domains in determining higher order chromatin structure and H1 location. J. Mol. Biol., 187, 591-601.
25. Hansen, J., Lu, X., Ross, E., Woody, R. (2006) Intrinsic protein disorder, amino acid composition, and histone terminal domains. J. Biol. Chem., 281, 1853-1856.
26. Ponte, I., Vila, R., Suau, P. (2003) Sequence complexity of histone H1 subtypes. Mol. Biol. Evol., 20, 371-380.
27. Hendzel, M., Lever, M., Crawford, E., Th'ng, J. (2004) The C-terminal domain is the primary determinant of histone H1 binding to chromatin in vivo. J. Biol. Chem., 279, 20028-20034.
28. Fang, H., Clark, D., Hayes, J. (2012) DNA and nucleosomes direct distinct folding of a linker histone H1 C-terminal domain. Nucleic Acids Res., 40, 1475-1484.
29. Bharath, M., Chandra, N., Rao, M. (2002) Prediction of an HMG-box fold in the C-terminal domain of histone H1: insights into its role in DNA condensation. Proteins, 49, 71-81.
30. Schlick, T., Collepardo-Guevara, R., Halvorsen, L., Jung, S., Xiao, X. (2011) Biomolecular modeling and simulation: a field coming of age. Q. Rev. Biophys., 44, 191-228.
31. Schlick, T. (2013) The 2013 Nobel Prize in chemistry celebrates computations in chemistry and biology. SIAM News, 46, 10.
32. Pachov, G., Gabdoulline, R., Wade, R. (2011) On the structure and dynamics of the complex of the nucleosome and the linker histone. Nucleic Acids Res., 39, 5255-5263.
33. Arya, G., Schlick, T. (2009) A tale of tails: how histone tails mediate chromatin compaction in different salt and linker histone environments. J. Phys. Chem. A, 113, 4045-4059.
34. Collepardo-Guevara, R., Schlick, T. (2014) Chromatin fiber polymorphism triggered by variations of DNA linker lengths. Proceedings of the National Academy of Sciences of the United States of America.
35. Collepardo-Guevara, R., Schlick, T. (2012) Crucial role of dynamic linker histone binding and divalent ions for DNA accessibility and gene regulation revealed by mesoscale modeling of oligonucleosomes. Nucleic Acids Res., 40, 8803-8817.
36. Collepardo-Guevara, R., Schlick, T. (2011) The effect of linker histone's nucleosome binding affinity on chromatin unfolding mechanisms. Biophysical journal 101, 1670-1680.
37. Schlick, T., Perisic, O. (2009) Mesoscale simulations of two nucleosome-repeat length oligonucleosomes. Phys. Chem. Chem. Phys., 11, 10729-10737.
38. Song, F., Chen, P., Sun, D., Wang, M., Dong, L., Liang, D., Xu, R.-M., Zhu, P., Li, G. (2014) Cryo-EM study of the chromatin fiber reveals a double helix twisted by tetranucleosomal units. Science, 344, 376-380.
39. Zhang, Q., Beard, D., Schlick, T. (2003) Constructing irregular surfaces to enclose macromolecular complexes for mesoscale modeling using the discrete surface charge optimization (DiSCO) algorithm. J. Comput. Chem., 24, 2063-2074.
40. Stigter, D. (1977) Interactions of highly charged colloidal cylinders with applications to double-stranded. Biopolymers, 16, 1435-1448.
41. Schlick, T., Li, B., Olson, W.K. (1994) The influence of salt on the structure and energetics of supercoiled DNA. Biophys. J., 67, 2146-2166.
42. Xiao, B., Freedman, B.S., Miller, K.E., Heald, R., Marko, J.F. (2012) Histone H1 compacts DNA under force and during chromatin assembly. Mol. Biol. Cell, 67, 2146-2166.
43. Yin, Y., Arkhipov, A., Schulten, K. (2009) Simulations of membrane tubulation by lattices of amphiphysin N-BAR domains. Structure, 17, 882-892.
44. Humphrey, W., Dalke, A., Schulten, K. (1996) VMD-visual molecular dynamics. J. Mol. Graph., 14, 33-38.
45. Woodcock, C.L., Skoultchi, A.I., Fan, Y. (2006) Role of linker histone in chromatin structure and function: H1 stoichiometry and nucleosome repeat length. Chromosome Res., 14, 17-25.
46. Scheffer, M., Eltsov, M., Bednar, J., Frangakis, A. (2012) Nucleosomes stacked with aligned dyad axes are found in native compact chromatin in vitro. J. Struct. Biol., 178, 207-214.
47. Artimo, P., Jonnalagedda, M., Arnold, K., Baratin, D., Csardi, E.A. (2012) ExPASy: SIB bioinformatics resource portal. Nucleic Acids Res., 40, W597-W603.
48. Nikitina, T., Wang, D., Gomberg, M., Grigoryev, S., Zhurkin, V. (2013) Combined micrococcal nuclease and exonuclease III digestion reveals precise positions of the nucleosome core/linker junctions: implications for high-resolution nucleosome mapping. J. Mol. Biol., 425, 1946-1960.
49. Carruthers, L., Bednar, J., Woodcock, C.L., Hansen, J.C. (1998) Linker histones stabilize the intrinsic salt-dependent folding of nucleosomal arrays: mechanistic ramifications for higher-order chromatin folding. Biochemistry, 37, 14776-14787.
50. Butler, P., Thomas, J. (1980) Changes in chromatin folding in solution. J. Mol. Biol., 140, 505-529.
51. Scheffer, M., Eltsov, M., Frangakis, A. (2011) Evidence for short-range helical order in the 30-nm chromatin fibers of erythrocyte nuclei. Proc. Natl. Acad. Sci. U.S.A., 108, 16992-16997.
52. Bergman, M., Wawra, E., Winge, M. (1988) Chicken histone H5 inhibits transcription and replication when introduced into proliferating cells by microinjection. J. Cell Sci., 91, 201-209.
53. Eltsov, M., Maclellan, K., Maeshima, K., Frangakis, A., Dubochet, J. (2008) Analysis of cryo-electron microscopy images does not support the existence of 30-nm chromatin fibers in mitotic chromosomes in situ. Proc. Natl. Acad. Sci. U.S.A., 105, 19732-19737.
54. Brown, D., Izard, T., Misteli, T. (2006) Mapping the interaction surface of linker histone H1(0) with the nucleosome of native chromatin in vivo. Nat. Struct. Mol. Biol., 13, 250-255.
55. Wisniewski, J., Zougman, A., Krüger, S., Mann, M. (2007) Mass spectrometric mapping of linker histone H1 variants reveals multiple acetylations, methylations, and phosphorylation as well as differences between cell culture and tissue. Mol. Cell. Proteomics, 6, 72-87.
56. Dou, Y., Gorovsky, M. (2002) Regulation of transcription by H1 phosphorylation in Tetrahymena is position independent and requires clustered sites. Proc. Natl. Acad. Sci. U.S.A., 99, 6142-6146.
57. Maria, A. Christophorou, Castelo-Branco, Goncalo, Richard, P. Halley-Stott, Slade Oliveira, Clara, Loos, Remco, Radzisheuskaya, Aliaksandra, Kerri, A. Mowen, Bertone, Paul, C R Silva, Jose, Zernicka-Goetz, Magdalena, L Nielsen, Michael, B Gurdon, John and Kouzarides, Tony (2014) Citrullination regulates pluripotency and histone H1 binding to chromatin. Nature 507, 104-108.
58. Roth, S.Y., Allis, C.D. (1992) Chromatin condensation: does histone H1 dephosphorylation play a role? Trends Biochem. Sci., 17, 93-98.