DNA-mediated association of two histone-bound complexes of yeast Chromatin Assembly Factor-1 (CAF-1) drives tetrasome assembly in the wake of DNA replication
Nucleosome assembly in the wake of DNA replication is a key process that regulates cell identity and survival. Chromatin assembly factor 1 (CAF-1) is a H3-H4 histone chaperone that associates with the replisome and orchestrates chromatin assembly following DNA synthesis. Little is known about the me...
| Main Authors: | , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2017-03-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/22799 |
| _version_ | 1818025006058176512 |
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| author | Francesca Mattiroli Yajie Gu Tejas Yadav Jeremy L Balsbaugh Michael R Harris Eileen S Findlay Yang Liu Catherine A Radebaugh Laurie A Stargell Natalie G Ahn Iestyn Whitehouse Karolin Luger |
| author_facet | Francesca Mattiroli Yajie Gu Tejas Yadav Jeremy L Balsbaugh Michael R Harris Eileen S Findlay Yang Liu Catherine A Radebaugh Laurie A Stargell Natalie G Ahn Iestyn Whitehouse Karolin Luger |
| author_sort | Francesca Mattiroli |
| collection | DOAJ |
| description | Nucleosome assembly in the wake of DNA replication is a key process that regulates cell identity and survival. Chromatin assembly factor 1 (CAF-1) is a H3-H4 histone chaperone that associates with the replisome and orchestrates chromatin assembly following DNA synthesis. Little is known about the mechanism and structure of this key complex. Here we investigate the CAF-1•H3-H4 binding mode and the mechanism of nucleosome assembly. We show that yeast CAF-1 binding to a H3-H4 dimer activates the Cac1 winged helix domain interaction with DNA. This drives the formation of a transient CAF-1•histone•DNA intermediate containing two CAF-1 complexes, each associated with one H3-H4 dimer. Here, the (H3-H4)2 tetramer is formed and deposited onto DNA. Our work elucidates the molecular mechanism for histone deposition by CAF-1, a reaction that has remained elusive for other histone chaperones, and it advances our understanding of how nucleosomes and their epigenetic information are maintained through DNA replication. |
| first_indexed | 2024-12-10T04:09:14Z |
| format | Article |
| id | doaj.art-410e9faf371748e7b2e4751d43090423 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-12-10T04:09:14Z |
| publishDate | 2017-03-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-410e9faf371748e7b2e4751d430904232022-12-22T02:02:46ZengeLife Sciences Publications LtdeLife2050-084X2017-03-01610.7554/eLife.22799DNA-mediated association of two histone-bound complexes of yeast Chromatin Assembly Factor-1 (CAF-1) drives tetrasome assembly in the wake of DNA replicationFrancesca Mattiroli0https://orcid.org/0000-0002-1574-7217Yajie Gu1https://orcid.org/0000-0002-1514-1477Tejas Yadav2Jeremy L Balsbaugh3Michael R Harris4Eileen S Findlay5Yang Liu6Catherine A Radebaugh7Laurie A Stargell8Natalie G Ahn9Iestyn Whitehouse10https://orcid.org/0000-0003-0385-3116Karolin Luger11https://orcid.org/0000-0001-5136-5331Department of Chemistry and Biochemistry, Howard Hughes Medical Institute, University of Colorado Boulder, Boulder, United StatesDepartment of Chemistry and Biochemistry, Howard Hughes Medical Institute, University of Colorado Boulder, Boulder, United States; Department of Biochemistry and Molecular Biology, Colorado State University, Fort Collins, United StatesWeill Cornell Graduate School of Medical Sciences, New York, United States; Molecular Biology Program, Memorial Sloan Kettering Cancer Center, New York, United StatesDepartment of Chemistry and Biochemistry, University of Colorado Boulder, Boulder, United StatesMolecular Biology Program, Memorial Sloan Kettering Cancer Center, New York, United StatesDepartment of Chemistry and Biochemistry, Howard Hughes Medical Institute, University of Colorado Boulder, Boulder, United StatesDepartment of Chemistry and Biochemistry, Howard Hughes Medical Institute, University of Colorado Boulder, Boulder, United StatesDepartment of Biochemistry and Molecular Biology, Colorado State University, Fort Collins, United StatesDepartment of Biochemistry and Molecular Biology, Colorado State University, Fort Collins, United States; Institute for Genome Architecture and Function, Colorado State University, Fort Collins, United StatesBiofrontiers Institute, University of Colorado Boulder, Boulder, United StatesMolecular Biology Program, Memorial Sloan Kettering Cancer Center, New York, United StatesDepartment of Chemistry and Biochemistry, Howard Hughes Medical Institute, University of Colorado Boulder, Boulder, United States; Institute for Genome Architecture and Function, Colorado State University, Fort Collins, United StatesNucleosome assembly in the wake of DNA replication is a key process that regulates cell identity and survival. Chromatin assembly factor 1 (CAF-1) is a H3-H4 histone chaperone that associates with the replisome and orchestrates chromatin assembly following DNA synthesis. Little is known about the mechanism and structure of this key complex. Here we investigate the CAF-1•H3-H4 binding mode and the mechanism of nucleosome assembly. We show that yeast CAF-1 binding to a H3-H4 dimer activates the Cac1 winged helix domain interaction with DNA. This drives the formation of a transient CAF-1•histone•DNA intermediate containing two CAF-1 complexes, each associated with one H3-H4 dimer. Here, the (H3-H4)2 tetramer is formed and deposited onto DNA. Our work elucidates the molecular mechanism for histone deposition by CAF-1, a reaction that has remained elusive for other histone chaperones, and it advances our understanding of how nucleosomes and their epigenetic information are maintained through DNA replication.https://elifesciences.org/articles/22799chromatin assemblyDNA replicationhistone chaperones |
| spellingShingle | Francesca Mattiroli Yajie Gu Tejas Yadav Jeremy L Balsbaugh Michael R Harris Eileen S Findlay Yang Liu Catherine A Radebaugh Laurie A Stargell Natalie G Ahn Iestyn Whitehouse Karolin Luger DNA-mediated association of two histone-bound complexes of yeast Chromatin Assembly Factor-1 (CAF-1) drives tetrasome assembly in the wake of DNA replication eLife chromatin assembly DNA replication histone chaperones |
| title | DNA-mediated association of two histone-bound complexes of yeast Chromatin Assembly Factor-1 (CAF-1) drives tetrasome assembly in the wake of DNA replication |
| title_full | DNA-mediated association of two histone-bound complexes of yeast Chromatin Assembly Factor-1 (CAF-1) drives tetrasome assembly in the wake of DNA replication |
| title_fullStr | DNA-mediated association of two histone-bound complexes of yeast Chromatin Assembly Factor-1 (CAF-1) drives tetrasome assembly in the wake of DNA replication |
| title_full_unstemmed | DNA-mediated association of two histone-bound complexes of yeast Chromatin Assembly Factor-1 (CAF-1) drives tetrasome assembly in the wake of DNA replication |
| title_short | DNA-mediated association of two histone-bound complexes of yeast Chromatin Assembly Factor-1 (CAF-1) drives tetrasome assembly in the wake of DNA replication |
| title_sort | dna mediated association of two histone bound complexes of yeast chromatin assembly factor 1 caf 1 drives tetrasome assembly in the wake of dna replication |
| topic | chromatin assembly DNA replication histone chaperones |
| url | https://elifesciences.org/articles/22799 |
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