Stage-specific dynamic reorganization of genome topology shapes transcriptional neighborhoods in developing human retinal organoids
We have generated a high-resolution Hi-C map of developing human retinal organoids to elucidate spatiotemporal dynamics of genomic architecture and its relationship with gene expression patterns. We demonstrate progressive stage-specific alterations in DNA topology and correlate these changes with t...
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| Published in | Cell reports (Cambridge) Vol. 42; no. 12; p. 113543 |
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| Main Authors | , , , , |
| Format | Journal Article |
| Language | English |
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Elsevier Inc
26.12.2023
Elsevier |
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| Abstract | We have generated a high-resolution Hi-C map of developing human retinal organoids to elucidate spatiotemporal dynamics of genomic architecture and its relationship with gene expression patterns. We demonstrate progressive stage-specific alterations in DNA topology and correlate these changes with transcription of cell-type-restricted gene markers during retinal differentiation. Temporal Hi-C reveals a shift toward A compartment for protein-coding genes and B compartment for non-coding RNAs, displaying high and low expression, respectively. Notably, retina-enriched genes are clustered near lost boundaries of topologically associated domains (TADs), and higher-order assemblages (i.e., TAD cliques) localize in active chromatin regions with binding sites for eye-field transcription factors. These genes gain chromatin contacts at their transcription start site as organoid differentiation proceeds. Our study provides a global view of chromatin architecture dynamics associated with diversification of cell types during retinal development and serves as a foundational resource for in-depth functional investigations of retinal developmental traits.
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•Major change in 3D genome correlates with emergence of late-born retinal cell types•TAD boundaries and inter/intra-TAD interactions are dynamic and stage specific•Enhanced chromatin looping forms growing networks with retinal marker and TF genes•Genome topology of organoids progressively resembles that of the adult human retina
Qu et al. use retinal organoids to measure the interplay between 3D genome organization and gene expression during the differentiation of a complex human neural tissue, showing topology changes at all levels in key retinal genes. |
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| AbstractList | We have generated a high-resolution Hi-C map of developing human retinal organoids to elucidate spatiotemporal dynamics of genomic architecture and its relationship with gene expression patterns. We demonstrate progressive stage-specific alterations in DNA topology and correlate these changes with transcription of cell-type-restricted gene markers during retinal differentiation. Temporal Hi-C reveals a shift toward A compartment for protein-coding genes and B compartment for non-coding RNAs, displaying high and low expression, respectively. Notably, retina-enriched genes are clustered near lost boundaries of topologically associated domains (TADs), and higher-order assemblages (i.e., TAD cliques) localize in active chromatin regions with binding sites for eye-field transcription factors. These genes gain chromatin contacts at their transcription start site as organoid differentiation proceeds. Our study provides a global view of chromatin architecture dynamics associated with diversification of cell types during retinal development and serves as a foundational resource for in-depth functional investigations of retinal developmental traits. We have generated a high-resolution Hi-C map of developing human retinal organoids to elucidate spatiotemporal dynamics of genomic architecture and its relationship with gene expression patterns. We demonstrate progressive stage-specific alterations in DNA topology and correlate these changes with transcription of cell-type-restricted gene markers during retinal differentiation. Temporal Hi-C reveals a shift toward A compartment for protein-coding genes and B compartment for non-coding RNAs, displaying high and low expression, respectively. Notably, retina-enriched genes are clustered near lost boundaries of topologically associated domains (TADs), and higher-order assemblages (i.e., TAD cliques) localize in active chromatin regions with binding sites for eye-field transcription factors. These genes gain chromatin contacts at their transcription start site as organoid differentiation proceeds. Our study provides a global view of chromatin architecture dynamics associated with diversification of cell types during retinal development and serves as a foundational resource for in-depth functional investigations of retinal developmental traits.We have generated a high-resolution Hi-C map of developing human retinal organoids to elucidate spatiotemporal dynamics of genomic architecture and its relationship with gene expression patterns. We demonstrate progressive stage-specific alterations in DNA topology and correlate these changes with transcription of cell-type-restricted gene markers during retinal differentiation. Temporal Hi-C reveals a shift toward A compartment for protein-coding genes and B compartment for non-coding RNAs, displaying high and low expression, respectively. Notably, retina-enriched genes are clustered near lost boundaries of topologically associated domains (TADs), and higher-order assemblages (i.e., TAD cliques) localize in active chromatin regions with binding sites for eye-field transcription factors. These genes gain chromatin contacts at their transcription start site as organoid differentiation proceeds. Our study provides a global view of chromatin architecture dynamics associated with diversification of cell types during retinal development and serves as a foundational resource for in-depth functional investigations of retinal developmental traits. We have generated a high-resolution Hi-C map of developing human retinal organoids to elucidate spatiotemporal dynamics of genomic architecture and its relationship with gene expression patterns. We demonstrate progressive stage-specific alterations in DNA topology and correlate these changes with transcription of cell-type-restricted gene markers during retinal differentiation. Temporal Hi-C reveals a shift toward A compartment for protein-coding genes and B compartment for non-coding RNAs, displaying high and low expression, respectively. Notably, retina-enriched genes are clustered near lost boundaries of topologically associated domains (TADs), and higher-order assemblages (i.e., TAD cliques) localize in active chromatin regions with binding sites for eye-field transcription factors. These genes gain chromatin contacts at their transcription start site as organoid differentiation proceeds. Our study provides a global view of chromatin architecture dynamics associated with diversification of cell types during retinal development and serves as a foundational resource for in-depth functional investigations of retinal developmental traits. Qu et al. use retinal organoids to measure the interplay between 3D genome organization and gene expression during the differentiation of a complex human neural tissue, showing topology changes at all levels in key retinal genes. We have generated a high-resolution Hi-C map of developing human retinal organoids to elucidate spatiotemporal dynamics of genomic architecture and its relationship with gene expression patterns. We demonstrate progressive stage-specific alterations in DNA topology and correlate these changes with transcription of cell-type-restricted gene markers during retinal differentiation. Temporal Hi-C reveals a shift toward A compartment for protein-coding genes and B compartment for non-coding RNAs, displaying high and low expression, respectively. Notably, retina-enriched genes are clustered near lost boundaries of topologically associated domains (TADs), and higher-order assemblages (i.e., TAD cliques) localize in active chromatin regions with binding sites for eye-field transcription factors. These genes gain chromatin contacts at their transcription start site as organoid differentiation proceeds. Our study provides a global view of chromatin architecture dynamics associated with diversification of cell types during retinal development and serves as a foundational resource for in-depth functional investigations of retinal developmental traits. [Display omitted] •Major change in 3D genome correlates with emergence of late-born retinal cell types•TAD boundaries and inter/intra-TAD interactions are dynamic and stage specific•Enhanced chromatin looping forms growing networks with retinal marker and TF genes•Genome topology of organoids progressively resembles that of the adult human retina Qu et al. use retinal organoids to measure the interplay between 3D genome organization and gene expression during the differentiation of a complex human neural tissue, showing topology changes at all levels in key retinal genes. |
| ArticleNumber | 113543 |
| Author | Batz, Zachary Marchal, Claire Singh, Nivedita Qu, Zepeng Swaroop, Anand |
| AuthorAffiliation | 4 Lead contact 2 In silichrom Ltd, 15 Digby Road, Newbury RG14 1TS, UK 1 Neurobiology, Neurodegeneration, and Repair Laboratory, National Eye Institute, National Institutes of Health, MSC0610, 6 Center Drive, Bethesda, MD 20892, USA 3 These authors contributed equally |
| AuthorAffiliation_xml | – name: 4 Lead contact – name: 2 In silichrom Ltd, 15 Digby Road, Newbury RG14 1TS, UK – name: 1 Neurobiology, Neurodegeneration, and Repair Laboratory, National Eye Institute, National Institutes of Health, MSC0610, 6 Center Drive, Bethesda, MD 20892, USA – name: 3 These authors contributed equally |
| Author_xml | – sequence: 1 givenname: Zepeng surname: Qu fullname: Qu, Zepeng organization: Neurobiology, Neurodegeneration, and Repair Laboratory, National Eye Institute, National Institutes of Health, MSC0610, 6 Center Drive, Bethesda, MD 20892, USA – sequence: 2 givenname: Zachary surname: Batz fullname: Batz, Zachary organization: Neurobiology, Neurodegeneration, and Repair Laboratory, National Eye Institute, National Institutes of Health, MSC0610, 6 Center Drive, Bethesda, MD 20892, USA – sequence: 3 givenname: Nivedita surname: Singh fullname: Singh, Nivedita organization: Neurobiology, Neurodegeneration, and Repair Laboratory, National Eye Institute, National Institutes of Health, MSC0610, 6 Center Drive, Bethesda, MD 20892, USA – sequence: 4 givenname: Claire surname: Marchal fullname: Marchal, Claire organization: Neurobiology, Neurodegeneration, and Repair Laboratory, National Eye Institute, National Institutes of Health, MSC0610, 6 Center Drive, Bethesda, MD 20892, USA – sequence: 5 givenname: Anand orcidid: 0000-0002-1975-1141 surname: Swaroop fullname: Swaroop, Anand email: swaroopa@nei.nih.gov organization: Neurobiology, Neurodegeneration, and Repair Laboratory, National Eye Institute, National Institutes of Health, MSC0610, 6 Center Drive, Bethesda, MD 20892, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/38048222$$D View this record in MEDLINE/PubMed |
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| Keywords | stem cells transcription factor CP: Stem cell research chromatin looping Hi-C gene regulation CP: Neuroscience 3D chromatin structure retinal development organogenesis organoid topologically associated domains |
| Language | English |
| License | This is an open access article under the CC BY license. Copyright © 2023. Published by Elsevier Inc. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/). |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Conceptualization, Z.Q. and A.S.; methodology and investigation, Z.Q. and N.S.; bioinformatic analysis and visualization, Z.B., C.M., and Z.Q.; data submission, Z.B.; writing - original draft, all authors; writing - review & editing, all authors; supervision, project administration, and funding acquisition, A.S. AUTHOR CONTRIBUTIONS |
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| SubjectTerms | 3D chromatin structure Cell Differentiation - genetics Chromatin chromatin looping CP: Neuroscience CP: Stem cell research gene regulation Genome Hi-C Humans organogenesis organoid Organoids Retina retinal development stem cells topologically associated domains transcription factor |
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| Title | Stage-specific dynamic reorganization of genome topology shapes transcriptional neighborhoods in developing human retinal organoids |
| URI | https://dx.doi.org/10.1016/j.celrep.2023.113543 https://www.ncbi.nlm.nih.gov/pubmed/38048222 https://www.proquest.com/docview/2898312560 https://pubmed.ncbi.nlm.nih.gov/PMC10790351 https://doaj.org/article/5e01e1ec43cd464b9283111e41a31196 |
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