Regulation of ISW2 by Concerted Action of Histone H4 Tail and Extranucleosomal DNA

Overview

Journal Mol Cell Biol

Specialty Cell Biology

Date 2006 Oct 4

PMID 17015471

Citations 53

Authors

Weiwei Dang

Mohamedi N Kagalwala

Blaine Bartholomew

Affiliations

Soon will be listed here.

Abstract

The stable contact of ISW2 with nucleosomal DNA approximately 20 bp from the dyad was shown by DNA footprinting and photoaffinity labeling using recombinant histone octamers to require the histone H4 N-terminal tail. Efficient ISW2 remodeling also required the H4 N-terminal tail, although the lack of the H4 tail can be mostly compensated for by increasing the incubation time or concentration of ISW2. Similarly, the length of extranucleosomal DNA affected the stable contact of ISW2 with this same internal nucleosomal site, with the optimal length being 70 to 85 bp. These data indicate the histone H4 tail, in concert with a favorable length of extranucleosomal DNA, recruits and properly orients ISW2 onto the nucleosome for efficient nucleosome remodeling. One consequence of this property of ISW2 is likely its previously observed nucleosome spacing activity.

Citing Articles

The role of auxiliary domains in modulating CHD4 activity suggests mechanistic commonality between enzyme families.

Zhong Y, Sani H, Paudel B, Low J, Silva A, Mueller S Nat Commun. 2022; 13(1):7524.

PMID: 36473839 PMC: 9726900. DOI: 10.1038/s41467-022-35002-0.

Sophisticated Conversations between Chromatin and Chromatin Remodelers, and Dissonances in Cancer.

Clapier C Int J Mol Sci. 2021; 22(11).

PMID: 34070411 PMC: 8197500. DOI: 10.3390/ijms22115578.

The yeast ISW1b ATP-dependent chromatin remodeler is critical for nucleosome spacing and dinucleosome resolution.

Eriksson P, Clark D Sci Rep. 2021; 11(1):4195.

PMID: 33602956 PMC: 7892562. DOI: 10.1038/s41598-021-82842-9.

Basis of specificity for a conserved and promiscuous chromatin remodeling protein.

Donovan D, Crandall J, Truong V, Vaaler A, Bailey T, Dinwiddie D Elife. 2021; 10.

PMID: 33576335 PMC: 7968928. DOI: 10.7554/eLife.64061.

Remodeler Catalyzed Nucleosome Repositioning: Influence of Structure and Stability.

Morgan A, LeGresley S, Fischer C Int J Mol Sci. 2020; 22(1).

PMID: 33374740 PMC: 7793527. DOI: 10.3390/ijms22010076.

References

Schwanbeck R, Xiao H, Wu C . Spatial contacts and nucleosome step movements induced by the NURF chromatin remodeling complex. J Biol Chem. 2004; 279(38):39933-41. DOI: 10.1074/jbc.M406060200. View

Eberharter A, Becker P . ATP-dependent nucleosome remodelling: factors and functions. J Cell Sci. 2004; 117(Pt 17):3707-11. DOI: 10.1242/jcs.01175. View

Lorch Y, LaPointe J, Kornberg R . Nucleosomes inhibit the initiation of transcription but allow chain elongation with the displacement of histones. Cell. 1987; 49(2):203-10. DOI: 10.1016/0092-8674(87)90561-7. View

Tullius T, Dombroski B, Churchill M, Kam L . Hydroxyl radical footprinting: a high-resolution method for mapping protein-DNA contacts. Methods Enzymol. 1987; 155:537-58. DOI: 10.1016/0076-6879(87)55035-2. View

Ebralidse K, Grachev S, Mirzabekov A . A highly basic histone H4 domain bound to the sharply bent region of nucleosomal DNA. Nature. 1988; 331(6154):365-7. DOI: 10.1038/331365a0. View

Stefanovsky VYu , Dimitrov S, Russanova V, Angelov D, Pashev I . Laser-induced crosslinking of histones to DNA in chromatin and core particles: implications in studying histone-DNA interactions. Nucleic Acids Res. 1989; 17(23):10069-81. PMC: 335231. DOI: 10.1093/nar/17.23.10069. View

DIXON W, HAYES J, Levin J, Weidner M, Dombroski B, Tullius T . Hydroxyl radical footprinting. Methods Enzymol. 1991; 208:380-413. DOI: 10.1016/0076-6879(91)08021-9. View

Usachenko S, Bavykin S, Gavin I, Bradbury E . Rearrangement of the histone H2A C-terminal domain in the nucleosome. Proc Natl Acad Sci U S A. 1994; 91(15):6845-9. PMC: 44294. DOI: 10.1073/pnas.91.15.6845. View

Tsukiyama T, Daniel C, Tamkun J, Wu C . ISWI, a member of the SWI2/SNF2 ATPase family, encodes the 140 kDa subunit of the nucleosome remodeling factor. Cell. 1995; 83(6):1021-6. DOI: 10.1016/0092-8674(95)90217-1. View

10.

Ito T, Bulger M, Pazin M, Kobayashi R, Kadonaga J . ACF, an ISWI-containing and ATP-utilizing chromatin assembly and remodeling factor. Cell. 1997; 90(1):145-55. DOI: 10.1016/s0092-8674(00)80321-9. View

11.

Wilm M, Bonte E, Dumas K, Mann M, Becker P . Chromatin-remodelling factor CHRAC contains the ATPases ISWI and topoisomerase II. Nature. 1997; 388(6642):598-602. DOI: 10.1038/41587. View

12.

Luger K, Mader A, Richmond R, Sargent D, Richmond T . Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature. 1997; 389(6648):251-60. DOI: 10.1038/38444. View

13.

Baneres J, Martin A, Parello J . The N tails of histones H3 and H4 adopt a highly structured conformation in the nucleosome. J Mol Biol. 1997; 273(3):503-8. DOI: 10.1006/jmbi.1997.1297. View

14.

Lowary P, Widom J . New DNA sequence rules for high affinity binding to histone octamer and sequence-directed nucleosome positioning. J Mol Biol. 1998; 276(1):19-42. DOI: 10.1006/jmbi.1997.1494. View

15.

Lee K, HAYES J . Linker DNA and H1-dependent reorganization of histone-DNA interactions within the nucleosome. Biochemistry. 1998; 37(24):8622-8. DOI: 10.1021/bi980499y. View

16.

Hansen J, Tse C, Wolffe A . Structure and function of the core histone N-termini: more than meets the eye. Biochemistry. 1999; 37(51):17637-41. DOI: 10.1021/bi982409v. View

17.

Tsukiyama T, Palmer J, Landel C, Shiloach J, Wu C . Characterization of the imitation switch subfamily of ATP-dependent chromatin-remodeling factors in Saccharomyces cerevisiae. Genes Dev. 1999; 13(6):686-97. PMC: 316555. DOI: 10.1101/gad.13.6.686. View

18.

Langst G, Bonte E, CORONA D, Becker P . Nucleosome movement by CHRAC and ISWI without disruption or trans-displacement of the histone octamer. Cell. 1999; 97(7):843-52. DOI: 10.1016/s0092-8674(00)80797-7. View

19.

Saha A, Wittmeyer J, Cairns B . Chromatin remodeling through directional DNA translocation from an internal nucleosomal site. Nat Struct Mol Biol. 2005; 12(9):747-55. DOI: 10.1038/nsmb973. View

20.

Zheng C, Lu X, Hansen J, Hayes J . Salt-dependent intra- and internucleosomal interactions of the H3 tail domain in a model oligonucleosomal array. J Biol Chem. 2005; 280(39):33552-7. DOI: 10.1074/jbc.M507241200. View