Insights into the molecular architecture and histone H3-H4 deposition mechanism of yeast Chromatin assembly factor 1
How the very first step in nucleosome assembly, deposition of histone H3-H4 as tetramers or dimers on DNA, is accomplished remains largely unclear. Here, we report that yeast chromatin assembly factor 1 (CAF1), a conserved histone chaperone complex that deposits H3-H4 during DNA replication, binds a...
| 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/23474 |
| _version_ | 1818018550032367616 |
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| author | Paul Victor Sauer Jennifer Timm Danni Liu David Sitbon Elisabetta Boeri-Erba Christophe Velours Norbert Mücke Jörg Langowski Françoise Ochsenbein Geneviève Almouzni Daniel Panne |
| author_facet | Paul Victor Sauer Jennifer Timm Danni Liu David Sitbon Elisabetta Boeri-Erba Christophe Velours Norbert Mücke Jörg Langowski Françoise Ochsenbein Geneviève Almouzni Daniel Panne |
| author_sort | Paul Victor Sauer |
| collection | DOAJ |
| description | How the very first step in nucleosome assembly, deposition of histone H3-H4 as tetramers or dimers on DNA, is accomplished remains largely unclear. Here, we report that yeast chromatin assembly factor 1 (CAF1), a conserved histone chaperone complex that deposits H3-H4 during DNA replication, binds a single H3-H4 heterodimer in solution. We identify a new DNA-binding domain in the large Cac1 subunit of CAF1, which is required for high-affinity DNA binding by the CAF1 three-subunit complex, and which is distinct from the previously described C-terminal winged-helix domain. CAF1 binds preferentially to DNA molecules longer than 40 bp, and two CAF1-H3-H4 complexes concertedly associate with DNA molecules of this size, resulting in deposition of H3-H4 tetramers. While DNA binding is not essential for H3–H4 tetrasome deposition in vitro, it is required for efficient DNA synthesis-coupled nucleosome assembly. Mutant histones with impaired H3-H4 tetramerization interactions fail to release from CAF1, indicating that DNA deposition of H3-H4 tetramers by CAF1 requires a hierarchical cooperation between DNA binding, H3-H4 deposition and histone tetramerization. |
| first_indexed | 2024-04-14T07:41:05Z |
| format | Article |
| id | doaj.art-13159998535b4ce984485d81f26c20d9 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-14T07:41:05Z |
| publishDate | 2017-03-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-13159998535b4ce984485d81f26c20d92022-12-22T02:05:29ZengeLife Sciences Publications LtdeLife2050-084X2017-03-01610.7554/eLife.23474Insights into the molecular architecture and histone H3-H4 deposition mechanism of yeast Chromatin assembly factor 1Paul Victor Sauer0https://orcid.org/0000-0001-7204-5863Jennifer Timm1Danni Liu2David Sitbon3Elisabetta Boeri-Erba4Christophe Velours5Norbert Mücke6Jörg Langowski7Françoise Ochsenbein8Geneviève Almouzni9Daniel Panne10https://orcid.org/0000-0001-9158-5507European Molecular Biology Laboratory, Grenoble, FranceEuropean Molecular Biology Laboratory, Grenoble, FranceCEA, DRF, SB2SM, Laboratoire de Biologie Structurale et Radiobiologie, Gif-sur-Yvette, France; Institute for Integrative Biology of the Cell (I2BC), CEA, CNRS, Université Paris-Sud, Gif-sur-Yvette, FranceInstitut Curie, PSL Research University, CNRS, UMR3664, Equipe Labellisée Ligue contre le Cancer, Paris, France; Sorbonne Universités, UPMC Univ Paris 06, CNRS, UMR3664, Paris, FranceUniversité Grenoble Alpes, Institut de Biologie Structurale (IBS), Grenoble, France; Commissariat à l'Energie Atomique et aux Energies Alternatives (CEA), Grenoble, FranceInstitute for Integrative Biology of the Cell (I2BC), CEA, CNRS, Université Paris-Sud, Gif-sur-Yvette, FranceAbteilung Biophysik der Makromoleküle, Deutsches Krebsforschungszentrum, Heidelberg, GermanyAbteilung Biophysik der Makromoleküle, Deutsches Krebsforschungszentrum, Heidelberg, GermanyCEA, DRF, SB2SM, Laboratoire de Biologie Structurale et Radiobiologie, Gif-sur-Yvette, France; Institute for Integrative Biology of the Cell (I2BC), CEA, CNRS, Université Paris-Sud, Gif-sur-Yvette, FranceInstitut Curie, PSL Research University, CNRS, UMR3664, Equipe Labellisée Ligue contre le Cancer, Paris, France; Sorbonne Universités, UPMC Univ Paris 06, CNRS, UMR3664, Paris, FranceEuropean Molecular Biology Laboratory, Grenoble, FranceHow the very first step in nucleosome assembly, deposition of histone H3-H4 as tetramers or dimers on DNA, is accomplished remains largely unclear. Here, we report that yeast chromatin assembly factor 1 (CAF1), a conserved histone chaperone complex that deposits H3-H4 during DNA replication, binds a single H3-H4 heterodimer in solution. We identify a new DNA-binding domain in the large Cac1 subunit of CAF1, which is required for high-affinity DNA binding by the CAF1 three-subunit complex, and which is distinct from the previously described C-terminal winged-helix domain. CAF1 binds preferentially to DNA molecules longer than 40 bp, and two CAF1-H3-H4 complexes concertedly associate with DNA molecules of this size, resulting in deposition of H3-H4 tetramers. While DNA binding is not essential for H3–H4 tetrasome deposition in vitro, it is required for efficient DNA synthesis-coupled nucleosome assembly. Mutant histones with impaired H3-H4 tetramerization interactions fail to release from CAF1, indicating that DNA deposition of H3-H4 tetramers by CAF1 requires a hierarchical cooperation between DNA binding, H3-H4 deposition and histone tetramerization.https://elifesciences.org/articles/23474chromatinhistonesDNA replicationchromatin assembly factor 1histone chaperone |
| spellingShingle | Paul Victor Sauer Jennifer Timm Danni Liu David Sitbon Elisabetta Boeri-Erba Christophe Velours Norbert Mücke Jörg Langowski Françoise Ochsenbein Geneviève Almouzni Daniel Panne Insights into the molecular architecture and histone H3-H4 deposition mechanism of yeast Chromatin assembly factor 1 eLife chromatin histones DNA replication chromatin assembly factor 1 histone chaperone |
| title | Insights into the molecular architecture and histone H3-H4 deposition mechanism of yeast Chromatin assembly factor 1 |
| title_full | Insights into the molecular architecture and histone H3-H4 deposition mechanism of yeast Chromatin assembly factor 1 |
| title_fullStr | Insights into the molecular architecture and histone H3-H4 deposition mechanism of yeast Chromatin assembly factor 1 |
| title_full_unstemmed | Insights into the molecular architecture and histone H3-H4 deposition mechanism of yeast Chromatin assembly factor 1 |
| title_short | Insights into the molecular architecture and histone H3-H4 deposition mechanism of yeast Chromatin assembly factor 1 |
| title_sort | insights into the molecular architecture and histone h3 h4 deposition mechanism of yeast chromatin assembly factor 1 |
| topic | chromatin histones DNA replication chromatin assembly factor 1 histone chaperone |
| url | https://elifesciences.org/articles/23474 |
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