Abstract
The mechanisms responsible for organizing linear arrays of nucleosomes into the three-dimensional structure of chromatin are still largely unknown. In a companion paper (Leuba, S. H., et al. 1998. Biophys. J. 74:2823-2829), we study the contributions of linker histone domains and the N-terminal tail of core histone H3 to extended chromatin fiber structure by scanning force microscopy imaging of mildly trypsinized fibers. Here we complement and extend these studies by scanning force microscopy imaging of selectively reconstituted chromatin fibers, which differ in subtle but distinctive ways in their histone composition. We demonstrate an absolute requirement for the globular domain of the linker histones and a structural redundancy of the tails of linker histones and of histone H3 in determining conformational stability.
Full Text
The Full Text of this article is available as a PDF (392.8 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Allan J., Harborne N., Rau D. C., Gould H. Participation of core histone "tails" in the stabilization of the chromatin solenoid. J Cell Biol. 1982 May;93(2):285–297. doi: 10.1083/jcb.93.2.285. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Allan J., Hartman P. G., Crane-Robinson C., Aviles F. X. The structure of histone H1 and its location in chromatin. Nature. 1980 Dec 25;288(5792):675–679. doi: 10.1038/288675a0. [DOI] [PubMed] [Google Scholar]
- Allan J., Mitchell T., Harborne N., Bohm L., Crane-Robinson C. Roles of H1 domains in determining higher order chromatin structure and H1 location. J Mol Biol. 1986 Feb 20;187(4):591–601. doi: 10.1016/0022-2836(86)90337-2. [DOI] [PubMed] [Google Scholar]
- 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 U S A. 1998 Mar 31;95(7):3396–3401. doi: 10.1073/pnas.95.7.3396. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Arents G., Burlingame R. W., Wang B. C., Love W. E., Moudrianakis E. N. The nucleosomal core histone octamer at 3.1 A resolution: a tripartite protein assembly and a left-handed superhelix. Proc Natl Acad Sci U S A. 1991 Nov 15;88(22):10148–10152. doi: 10.1073/pnas.88.22.10148. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Arents G., Moudrianakis E. N. Topography of the histone octamer surface: repeating structural motifs utilized in the docking of nucleosomal DNA. Proc Natl Acad Sci U S A. 1993 Nov 15;90(22):10489–10493. doi: 10.1073/pnas.90.22.10489. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bates D. L., Thomas J. O. Histones H1 and H5: one or two molecules per nucleosome? Nucleic Acids Res. 1981 Nov 25;9(22):5883–5894. doi: 10.1093/nar/9.22.5883. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bavykin S. G., Usachenko S. I., Zalensky A. O., Mirzabekov A. D. Structure of nucleosomes and organization of internucleosomal DNA in chromatin. J Mol Biol. 1990 Apr 5;212(3):495–511. doi: 10.1016/0022-2836(90)90328-J. [DOI] [PubMed] [Google Scholar]
- Belyavsky A. V., Bavykin S. G., Goguadze E. G., Mirzabekov A. D. Primary organization of nucleosomes containing all five histones and DNA 175 and 165 base-pairs long. J Mol Biol. 1980 May 25;139(3):519–536. doi: 10.1016/0022-2836(80)90144-8. [DOI] [PubMed] [Google Scholar]
- Böhm L., Briand G., Sautière P., Crane-Robinson C. Proteolytic digestion studies of chromatin core-histone structure. Identification of the limit peptides of histones H3 and H4. Eur J Biochem. 1981 Sep;119(1):67–74. doi: 10.1111/j.1432-1033.1981.tb05577.x. [DOI] [PubMed] [Google Scholar]
- Böhm L., Crane-Robinson C. Proteases as structural probes for chromatin: the domain structure of histones. Biosci Rep. 1984 May;4(5):365–386. doi: 10.1007/BF01122502. [DOI] [PubMed] [Google Scholar]
- Clark D. J., Kimura T. Electrostatic mechanism of chromatin folding. J Mol Biol. 1990 Feb 20;211(4):883–896. doi: 10.1016/0022-2836(90)90081-V. [DOI] [PubMed] [Google Scholar]
- Furrer P., Bednar J., Dubochet J., Hamiche A., Prunell A. DNA at the entry-exit of the nucleosome observed by cryoelectron microscopy. J Struct Biol. 1995 May-Jun;114(3):177–183. doi: 10.1006/jsbi.1995.1017. [DOI] [PubMed] [Google Scholar]
- Garcia-Ramirez M., Leuba S. H., Ausio J. One-step fractionation method for isolating H1 histones from chromatin under nondenaturing conditions. Protein Expr Purif. 1990 Sep;1(1):40–44. doi: 10.1016/1046-5928(90)90043-x. [DOI] [PubMed] [Google Scholar]
- Hamiche A., Schultz P., Ramakrishnan V., Oudet P., Prunell A. Linker histone-dependent DNA structure in linear mononucleosomes. J Mol Biol. 1996 Mar 22;257(1):30–42. doi: 10.1006/jmbi.1996.0144. [DOI] [PubMed] [Google Scholar]
- Hill C. S., Thomas J. O. Core histone-DNA interactions in sea urchin sperm chromatin. The N-terminal tail of H2B interacts with linker DNA. Eur J Biochem. 1990 Jan 12;187(1):145–153. doi: 10.1111/j.1432-1033.1990.tb15288.x. [DOI] [PubMed] [Google Scholar]
- Karpov V. L., Bavykin S. G., Preobrazhenskaya O. V., Belyavsky A. V., Mirzabekov A. D. Alignment of nucleosomes along DNA and organization of spacer DNA in Drosophila chromatin. Nucleic Acids Res. 1982 Jul 24;10(14):4321–4337. doi: 10.1093/nar/10.14.4321. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Krylov D., Leuba S., van Holde K., Zlatanova J. Histones H1 and H5 interact preferentially with crossovers of double-helical DNA. Proc Natl Acad Sci U S A. 1993 Jun 1;90(11):5052–5056. doi: 10.1073/pnas.90.11.5052. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
- Leuba S. H., Bustamante C., Zlatanova J., van Holde K. Contributions of linker histones and histone H3 to chromatin structure: scanning force microscopy studies on trypsinized fibers. Biophys J. 1998 Jun;74(6):2823–2829. doi: 10.1016/S0006-3495(98)77989-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Leuba S. H., Yang G., Robert C., Samori B., van Holde K., Zlatanova J., Bustamante C. Three-dimensional structure of extended chromatin fibers as revealed by tapping-mode scanning force microscopy. Proc Natl Acad Sci U S A. 1994 Nov 22;91(24):11621–11625. doi: 10.1073/pnas.91.24.11621. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Leuba S. H., Zlatanova J., van Holde K. On the location of histones H1 and H5 in the chromatin fiber. Studies with immobilized trypsin and chymotrypsin. J Mol Biol. 1993 Feb 20;229(4):917–929. doi: 10.1006/jmbi.1993.1096. [DOI] [PubMed] [Google Scholar]
- Libertini L. J., Small E. W. Salt induced transitions of chromatin core particles studied by tyrosine fluorescence anisotropy. Nucleic Acids Res. 1980 Aug 25;8(16):3517–3534. doi: 10.1093/nar/8.16.3517. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Luger K., Mäder A. W., Richmond R. K., Sargent D. F., Richmond T. J. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature. 1997 Sep 18;389(6648):251–260. doi: 10.1038/38444. [DOI] [PubMed] [Google Scholar]
- Renz M., Day L. A. Transition from noncooperative to cooperative and selective binding of histone H1 to DNA. Biochemistry. 1976 Jul 27;15(15):3220–3228. doi: 10.1021/bi00660a010. [DOI] [PubMed] [Google Scholar]
- Thoma F., Koller T. Unravelled nucleosomes, nucleosome beads and higher order structures of chromatin: influence of non-histone components and histone H1. J Mol Biol. 1981 Jul 15;149(4):709–733. doi: 10.1016/0022-2836(81)90354-5. [DOI] [PubMed] [Google Scholar]
- Travers A. A., Muyldermans S. V. A DNA sequence for positioning chromatosomes. J Mol Biol. 1996 Apr 5;257(3):486–491. doi: 10.1006/jmbi.1996.0178. [DOI] [PubMed] [Google Scholar]
- Yang G., Leuba S. H., Bustamante C., Zlatanova J., van Holde K. Role of linker histones in extended chromatin fibre structure. Nat Struct Biol. 1994 Nov;1(11):761–763. doi: 10.1038/nsb1194-761. [DOI] [PubMed] [Google Scholar]
- Zlatanova J., van Holde K. The linker histones and chromatin structure: new twists. Prog Nucleic Acid Res Mol Biol. 1996;52:217–259. doi: 10.1016/s0079-6603(08)60968-x. [DOI] [PubMed] [Google Scholar]
- van Holde K., Zlatanova J. What determines the folding of the chromatin fiber? Proc Natl Acad Sci U S A. 1996 Oct 1;93(20):10548–10555. doi: 10.1073/pnas.93.20.10548. [DOI] [PMC free article] [PubMed] [Google Scholar]