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Article ; Online: Global mapping of RNA-chromatin contacts reveals a proximity-dominated connectivity model for ncRNA-gene interactions.

Limouse, Charles / Smith, Owen K / Jukam, David / Fryer, Kelsey A / Greenleaf, William J / Straight, Aaron F

2023 Volume 14, Issue 1, Page(s) 6073

Abstract: Non-coding RNAs (ncRNAs) are transcribed throughout the genome and provide regulatory inputs to gene expression through their interaction with chromatin. Yet, the genomic targets and functions of most ncRNAs are unknown. Here we use chromatin-associated ... ...

Abstract	Non-coding RNAs (ncRNAs) are transcribed throughout the genome and provide regulatory inputs to gene expression through their interaction with chromatin. Yet, the genomic targets and functions of most ncRNAs are unknown. Here we use chromatin-associated RNA sequencing (ChAR-seq) to map the global network of ncRNA interactions with chromatin in human embryonic stem cells and the dynamic changes in interactions during differentiation into definitive endoderm. We uncover general principles governing the organization of the RNA-chromatin interactome, demonstrating that nearly all ncRNAs exclusively interact with genes in close three-dimensional proximity to their locus and provide a model predicting the interactome. We uncover RNAs that interact with many loci across the genome and unveil thousands of unannotated RNAs that dynamically interact with chromatin. By relating the dynamics of the interactome to changes in gene expression, we demonstrate that activation or repression of individual genes is unlikely to be controlled by a single ncRNA.
MeSH term(s)	Humans ; Chromatin/genetics ; RNA/metabolism ; RNA, Untranslated/genetics ; RNA, Untranslated/metabolism ; Genome
Chemical Substances	Chromatin ; RNA (63231-63-0) ; RNA, Untranslated
Language	English
Publishing date	2023-09-28
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2553671-0
ISSN	2041-1723 ; 2041-1723
ISSN (online)	2041-1723
ISSN	2041-1723
DOI	10.1038/s41467-023-41848-9
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: The DNA-to-cytoplasm ratio broadly activates zygotic gene expression in Xenopus.

Jukam, David / Kapoor, Rishabh R / Straight, Aaron F / Skotheim, Jan M

Current biology : CB

2021 Volume 31, Issue 19, Page(s) 4269–4281.e8

Abstract: In multicellular animals, the first major event after fertilization is the switch from maternal to zygotic control of development. During this transition, zygotic gene transcription is broadly activated in an otherwise quiescent genome in a process known ...

Abstract	In multicellular animals, the first major event after fertilization is the switch from maternal to zygotic control of development. During this transition, zygotic gene transcription is broadly activated in an otherwise quiescent genome in a process known as zygotic genome activation (ZGA). In fast-developing embryos, ZGA often overlaps with the slowing of initially synchronous cell divisions at the mid-blastula transition (MBT). Initial studies of the MBT led to the nuclear-to-cytoplasmic ratio model where MBT timing is regulated by the exponentially increasing amounts of some nuclear component "N" titrated against a fixed cytoplasmic component "C." However, more recent experiments have been interpreted to suggest that ZGA is independent of the N/C ratio. To determine the role of the N/C ratio in ZGA, we generated Xenopus frog embryos with ∼3-fold differences in genomic DNA (i.e., N) by using X. tropicalis sperm to fertilize X. laevis eggs with or without their maternal genome. Resulting embryos have otherwise identical X. tropicalis genome template amounts, embryo sizes, and X. laevis maternal environments. We generated transcriptomic time series across the MBT in both conditions and used X. tropicalis paternally derived mRNA to identify a high-confidence set of exclusively zygotic transcripts. Both ZGA and the increase in cell-cycle duration are delayed in embryos with ∼3-fold less DNA per cell. Thus, DNA is an important component of the N/C ratio, which is a critical regulator of zygotic genome activation in Xenopus embryos.
MeSH term(s)	Animals ; Blastula/metabolism ; Cytoplasm ; DNA/metabolism ; Gene Expression ; Gene Expression Regulation, Developmental ; Xenopus laevis ; Zygote/metabolism
Chemical Substances	DNA (9007-49-2)
Language	English
Publishing date	2021-08-12
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	1071731-6
ISSN	1879-0445 ; 0960-9822
ISSN (online)	1879-0445
ISSN	0960-9822
DOI	10.1016/j.cub.2021.07.035
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Article ; Online: Mapping Transcriptome-Wide and Genome-Wide RNA-DNA Contacts with Chromatin-Associated RNA Sequencing (ChAR-seq).

Limouse, Charles / Jukam, David / Smith, Owen K / Fryer, Kelsey A / Straight, Aaron F

Methods in molecular biology (Clifton, N.J.)

2020 Volume 2161, Page(s) 115–142

Abstract: RNAs play key roles in the cell as molecular intermediates for protein synthesis and as regulators of nuclear processes such as splicing, posttranscriptional regulation, or chromatin remodeling. Various classes of non-coding RNAs, including long non- ... ...

Abstract	RNAs play key roles in the cell as molecular intermediates for protein synthesis and as regulators of nuclear processes such as splicing, posttranscriptional regulation, or chromatin remodeling. Various classes of non-coding RNAs, including long non-coding RNAs (lncRNAs), can bind chromatin either directly or via interaction with chromatin binding proteins. It has been proposed that lncRNAs regulate cell-state-specific genes by coordinating the locus-dependent activity of chromatin-modifying complexes. Yet, the vast majority of lncRNAs have unknown functions, and we know little about the specific loci they regulate. A key step toward understanding chromatin regulation by RNAs is to map the genomic loci with which every nuclear RNA interacts and, reciprocally, to identify all RNAs that target a given locus. Our ability to generate such data has been limited, until recently, by the lack of methods to probe the genomic localization of more than a few RNAs at a time. Here, we describe a protocol for ChAR-seq, an RNA-DNA proximity ligation method that maps the binding loci for thousands of RNAs at once and without the need for specific RNA or DNA probe sequences. The ChAR-seq approach generates chimeric RNA-DNA molecules in situ and then converts those chimeras to DNA for next-generation sequencing. Using ChAR-seq we detect many types of chromatin-associated RNA, both coding and non-coding. Understanding the RNA-DNA interactome and its changes during differentiation or disease with ChAR-seq will likely provide key insights into chromatin and RNA biology.
MeSH term(s)	Animals ; Cell Line ; Cells, Cultured ; Chromatin/chemistry ; Chromatin/metabolism ; Chromatin Immunoprecipitation Sequencing/methods ; DNA/chemistry ; DNA/metabolism ; Humans ; RNA, Long Noncoding/chemistry ; RNA, Long Noncoding/metabolism ; Transcriptome ; Whole Genome Sequencing/methods
Chemical Substances	Chromatin ; RNA, Long Noncoding ; DNA (9007-49-2)
Language	English
Publishing date	2020-07-17
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, U.S. Gov't, Non-P.H.S.
ISSN	1940-6029
ISSN (online)	1940-6029
DOI	10.1007/978-1-0716-0680-3_10
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Article ; Online: Zygotic Genome Activation in Vertebrates.

Jukam, David / Shariati, S Ali M / Skotheim, Jan M

Developmental cell

2017 Volume 42, Issue 4, Page(s) 316–332

Abstract: The first major developmental transition in vertebrate embryos is the maternal-to-zygotic transition (MZT) when maternal mRNAs are degraded and zygotic transcription begins. During the MZT, the embryo takes charge of gene expression to control cell ... ...

Abstract	The first major developmental transition in vertebrate embryos is the maternal-to-zygotic transition (MZT) when maternal mRNAs are degraded and zygotic transcription begins. During the MZT, the embryo takes charge of gene expression to control cell differentiation and further development. This spectacular organismal transition requires nuclear reprogramming and the initiation of RNAPII at thousands of promoters. Zygotic genome activation (ZGA) is mechanistically coordinated with other embryonic events, including changes in the cell cycle, chromatin state, and nuclear-to-cytoplasmic component ratios. Here, we review progress in understanding vertebrate ZGA dynamics in frogs, fish, mice, and humans to explore differences and emphasize common features.
MeSH term(s)	Animals ; Cellular Reprogramming ; Embryo, Mammalian/embryology ; Embryo, Mammalian/metabolism ; Embryo, Nonmammalian/embryology ; Embryo, Nonmammalian/metabolism ; Gene Expression Regulation, Developmental ; Genome ; Vertebrates/embryology ; Vertebrates/genetics ; Zygote/metabolism
Language	English
Publishing date	2017-08-02
Publishing country	United States
Document type	Journal Article ; Review ; Research Support, Non-U.S. Gov't ; Research Support, N.I.H., Extramural
ZDB-ID	2054967-2
ISSN	1878-1551 ; 1534-5807
ISSN (online)	1878-1551
ISSN	1534-5807
DOI	10.1016/j.devcel.2017.07.026
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Zs.A 5742: Show issues			Location: Je nach Verfügbarkeit (siehe Angabe bei Bestand) bis Jg. 1994: Bestellungen von Artikeln über das Online-Bestellformular Jg. 1995 - 2021: Lesesall (2.OG) ab Jg. 2022: Lesesaal (EG)
Zs.MG 76: Show issues

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Article ; Online: Chromatin-Associated RNA Sequencing (ChAR-seq).

Jukam, David / Limouse, Charles / Smith, Owen K / Risca, Viviana I / Bell, Jason C / Straight, Aaron F

Current protocols in molecular biology

2019 Volume 126, Issue 1, Page(s) e87

Abstract: RNA is a fundamental component of chromatin. Noncoding RNAs (ncRNAs) can associate with chromatin to influence gene expression and chromatin state; many also act at long distances from their transcriptional origin. Yet we know almost nothing about the ... ...

Abstract	RNA is a fundamental component of chromatin. Noncoding RNAs (ncRNAs) can associate with chromatin to influence gene expression and chromatin state; many also act at long distances from their transcriptional origin. Yet we know almost nothing about the functions or sites of action for most ncRNAs. Current methods to identify sites of RNA interaction with the genome are limited to the study of a single RNA at a time. Here we describe a protocol for ChAR-seq, a strategy to identify all chromatin-associated RNAs and map their DNA contacts genome-wide. In ChAR-seq, proximity ligation of RNA and DNA to a linker molecule is used to construct a chimeric RNA-DNA molecule that is converted to DNA for sequencing. In a single assay, ChAR-seq can discover de novo chromatin interactions of distinct RNAs, including nascent transcripts, splicing RNAs, and long noncoding RNAs (lncRNAs). Resulting "maps" of genome-bound RNAs should provide new insights into RNA biology. © 2019 by John Wiley & Sons, Inc.
MeSH term(s)	RNA, Small Nuclear/analysis ; RNA, Small Nuclear/genetics ; Sequence Analysis, RNA/methods
Chemical Substances	RNA, Small Nuclear
Language	English
Publishing date	2019-02-20
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
ISSN	1934-3647
ISSN (online)	1934-3647
DOI	10.1002/cpmb.87
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Article ; Online: Binary regulation of Hippo pathway by Merlin/NF2, Kibra, Lgl, and Melted specifies and maintains postmitotic neuronal fate.

Jukam, David / Desplan, Claude

Developmental cell

2011 Volume 21, Issue 5, Page(s) 874–887

Abstract: Patterning the Drosophila retina for color vision relies on postmitotic specification of photoreceptor subtypes. R8 photoreceptors express one of two light-sensing Rhodopsins, Rh5 or Rh6. This fate decision involves a bistable feedback loop between ... ...

Abstract	Patterning the Drosophila retina for color vision relies on postmitotic specification of photoreceptor subtypes. R8 photoreceptors express one of two light-sensing Rhodopsins, Rh5 or Rh6. This fate decision involves a bistable feedback loop between Melted, a PH-domain protein, and Warts, a kinase in the Hippo growth pathway. Here, we show that a subset of the Hippo pathway-Merlin, Kibra, and Lethal(2)giant larvae (Lgl), but not Expanded or Fat-is required for Warts expression and activity in R8 to specify Rh6 fate. Melted represses warts transcription to disrupt Hippo pathway activity and specify Rh5 fate. Therefore, R8 Hippo signaling exhibits ON-or-OFF regulation, promoting mutually exclusive fates. Furthermore, Merlin and Lgl are continuously required to maintain R8 neuronal subtypes. These results reveal roles for Merlin, Kibra, and Lgl in neuronal specification and maintenance and show that the Hippo pathway is reimplemented for sensory neuron fate by combining canonical and noncanonical regulatory steps.
MeSH term(s)	Animals ; Cell Differentiation ; Drosophila ; Drosophila Proteins/metabolism ; Intracellular Signaling Peptides and Proteins/metabolism ; Mitosis ; Neurofibromin 2/metabolism ; Neurons/cytology ; Neurons/metabolism ; Protein-Serine-Threonine Kinases/metabolism ; Tumor Suppressor Proteins/metabolism
Chemical Substances	Drosophila Proteins ; Intracellular Signaling Peptides and Proteins ; Neurofibromin 2 ; Tumor Suppressor Proteins ; kibra protein, Drosophila ; l(2)gl protein, Drosophila ; merlin, Drosophila ; Protein-Serine-Threonine Kinases (EC 2.7.11.1) ; hpo protein, Drosophila (EC 2.7.11.1)
Language	English
Publishing date	2011-11-03
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2054967-2
ISSN	1878-1551 ; 1534-5807
ISSN (online)	1878-1551
ISSN	1534-5807
DOI	10.1016/j.devcel.2011.10.004
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Zs.A 5742: Show issues			Location: Je nach Verfügbarkeit (siehe Angabe bei Bestand) bis Jg. 1994: Bestellungen von Artikeln über das Online-Bestellformular Jg. 1995 - 2021: Lesesall (2.OG) ab Jg. 2022: Lesesaal (EG)
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Article: Binary Regulation of Hippo Pathway by Merlin/NF2, Kibra, Lgl, and Melted Specifies and Maintains Postmitotic Neuronal Fate

Jukam, David / Desplan, Claude

Developmental cell. 2011 Nov. 15, v. 21, no. 5

2011

Abstract	Patterning the Drosophila retina for color vision relies on postmitotic specification of photoreceptor subtypes. R8 photoreceptors express one of two light-sensing Rhodopsins, Rh5 or Rh6. This fate decision involves a bistable feedback loop between Melted, a PH-domain protein, and Warts, a kinase in the Hippo growth pathway. Here, we show that a subset of the Hippo pathway—Merlin, Kibra, and Lethal(2)giant larvae (Lgl), but not Expanded or Fat—is required for Warts expression and activity in R8 to specify Rh6 fate. Melted represses warts transcription to disrupt Hippo pathway activity and specify Rh5 fate. Therefore, R8 Hippo signaling exhibits ON-or-OFF regulation, promoting mutually exclusive fates. Furthermore, Merlin and Lgl are continuously required to maintain R8 neuronal subtypes. These results reveal roles for Merlin, Kibra, and Lgl in neuronal specification and maintenance and show that the Hippo pathway is reimplemented for sensory neuron fate by combining canonical and noncanonical regulatory steps.
Keywords	Drosophila ; color vision ; larvae ; melting ; photoreceptors ; retina ; rhodopsin ; sensory neurons ; warts
Language	English
Dates of publication	2011-1115
Size	p. 874-887.
Publishing place	Elsevier Inc.
Document type	Article
ZDB-ID	2054967-2
ISSN	1878-1551 ; 1534-5807
ISSN (online)	1878-1551
ISSN	1534-5807
DOI	10.1016/j.devcel.2011.10.004
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Article ; Online: Histone titration against the genome sets the DNA-to-cytoplasm threshold for the Xenopus midblastula transition.

Amodeo, Amanda A / Jukam, David / Straight, Aaron F / Skotheim, Jan M

Proceedings of the National Academy of Sciences of the United States of America

2015 Volume 112, Issue 10, Page(s) E1086–95

Abstract: During early development, animal embryos depend on maternally deposited RNA until zygotic genes become transcriptionally active. Before this maternal-to-zygotic transition, many species execute rapid and synchronous cell divisions without growth phases ... ...

Abstract	During early development, animal embryos depend on maternally deposited RNA until zygotic genes become transcriptionally active. Before this maternal-to-zygotic transition, many species execute rapid and synchronous cell divisions without growth phases or cell cycle checkpoints. The coordinated onset of transcription, cell cycle lengthening, and cell cycle checkpoints comprise the midblastula transition (MBT). A long-standing model in the frog, Xenopus laevis, posits that MBT timing is controlled by a maternally loaded inhibitory factor that is titrated against the exponentially increasing amount of DNA. To identify MBT regulators, we developed an assay using Xenopus egg extract that recapitulates the activation of transcription only above the DNA-to-cytoplasm ratio found in embryos at the MBT. We used this system to biochemically purify factors responsible for inhibiting transcription below the threshold DNA-to-cytoplasm ratio. This unbiased approach identified histones H3 and H4 as concentration-dependent inhibitory factors. Addition or depletion of H3/H4 from the extract quantitatively shifted the amount of DNA required for transcriptional activation in vitro. Moreover, reduction of H3 protein in embryos induced premature transcriptional activation and cell cycle lengthening, and the addition of H3/H4 shortened post-MBT cell cycles. Our observations support a model for MBT regulation by DNA-based titration and suggest that depletion of free histones regulates the MBT. More broadly, our work shows how a constant concentration DNA binding molecule can effectively measure the amount of cytoplasm per genome to coordinate division, growth, and development.
MeSH term(s)	Animals ; Blastula/embryology ; Cytoplasm/metabolism ; DNA/metabolism ; Genome ; Histones/metabolism ; Transcription, Genetic ; Xenopus/embryology ; Xenopus/metabolism
Chemical Substances	Histones ; DNA (9007-49-2)
Language	English
Publishing date	2015-02-23
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	209104-5
ISSN	1091-6490 ; 0027-8424
ISSN (online)	1091-6490
ISSN	0027-8424
DOI	10.1073/pnas.1413990112
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Zs.A 1148: Show issues

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Article ; Online: Binary fate decisions in differentiating neurons.

Jukam, David / Desplan, Claude

Current opinion in neurobiology

2009 Volume 20, Issue 1, Page(s) 6–13

Abstract: Neural cell fate programs must generate an enormous number of neurons with distinct adult functions. The decision to choose one neuronal subtype from two alternatives--a binary fate decision--is one way to diversify neuronal subtypes during nervous ... ...

Abstract	Neural cell fate programs must generate an enormous number of neurons with distinct adult functions. The decision to choose one neuronal subtype from two alternatives--a binary fate decision--is one way to diversify neuronal subtypes during nervous system development. Recent progress has been made in describing the genetic programs that define late-stage neuronal identity. Here, we review mechanisms that control how such fate decisions generate two different postmitotic, terminally differentiated neuronal subtypes. We survey examples from Caenorhabditis elegans and Drosophila that demonstrate different modes of binary neuronal fate specification that depend on cell division, lineage, stochastic gene expression, or extracellular signals. Comparison of these strategies reveals that, although organisms use diverse approaches to generate neural diversity, some common themes do exist.
MeSH term(s)	Animals ; Caenorhabditis elegans/genetics ; Cell Lineage/genetics ; Cell Proliferation ; Drosophila/genetics ; Gene Expression/genetics ; Gene Expression Regulation, Developmental/genetics ; Neurogenesis/genetics ; Neurons/physiology
Language	English
Publishing date	2009-12-10
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Review
ZDB-ID	1078046-4
ISSN	1873-6882 ; 0959-4388
ISSN (online)	1873-6882
ISSN	0959-4388
DOI	10.1016/j.conb.2009.11.002
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Article ; Online: The neuronal transcription factor erect wing regulates specification and maintenance of Drosophila R8 photoreceptor subtypes.

Hsiao, Hui-Yi / Jukam, David / Johnston, Robert / Desplan, Claude

Developmental biology

2013 Volume 381, Issue 2, Page(s) 482–490

Abstract: Signaling pathways are often re-used during development in surprisingly different ways. The Hippo tumor suppressor pathway is best understood for its role in the control of growth. The pathway is also used in a very different context, in the Drosophila ... ...

Abstract	Signaling pathways are often re-used during development in surprisingly different ways. The Hippo tumor suppressor pathway is best understood for its role in the control of growth. The pathway is also used in a very different context, in the Drosophila eye for the robust specification of R8 photoreceptor neuron subtypes, which complete their terminal differentiation by expressing light-sensing Rhodopsin (Rh) proteins. A double negative feedback loop between the Warts kinase of the Hippo pathway and the PH-domain growth regulator Melted regulates the choice between 'pale' R8 (pR8) fate defined by Rh5 expression and 'yellow' R8 (yR8) fate characterized by Rh6 expression. Here, we show that the gene encoding the homolog of human Nuclear respiratory factor 1, erect wing (ewg), is autonomously required to inhibit warts expression and to promote melted expression to specify pR8 subtype fate and induce Rh5. ewg mutants express Rh6 in most R8s due to ectopic warts expression. Further, ewg is continuously required to maintain repression of Rh6 in pR8s in aging flies. Our work shows that Ewg is a critical factor for the stable down-regulation of Hippo pathway activity to determine neuronal subtype fates. Neural-enriched factors, such as Ewg, may generally contribute to the contextual re-use of signaling pathways in post-mitotic neurons.
MeSH term(s)	Animals ; Cell Differentiation ; Drosophila/cytology ; Drosophila/metabolism ; Drosophila Proteins/genetics ; Drosophila Proteins/metabolism ; Feedback, Physiological ; Female ; Gene Expression Regulation, Developmental ; Intracellular Signaling Peptides and Proteins/genetics ; Intracellular Signaling Peptides and Proteins/metabolism ; Male ; Neuropeptides/genetics ; Neuropeptides/metabolism ; Organ Specificity ; Photoreceptor Cells, Invertebrate/cytology ; Photoreceptor Cells, Invertebrate/metabolism ; Protein Isoforms/genetics ; Protein Isoforms/metabolism ; Protein-Serine-Threonine Kinases/genetics ; Protein-Serine-Threonine Kinases/metabolism ; Retina/cytology ; Retina/metabolism ; Rhodopsin/genetics ; Rhodopsin/metabolism ; Signal Transduction ; Transcription Factors/genetics ; Transcription Factors/metabolism
Chemical Substances	Drosophila Proteins ; EWG protein, Drosophila ; Intracellular Signaling Peptides and Proteins ; Neuropeptides ; Protein Isoforms ; Rh5 protein, Drosophila ; Transcription Factors ; melt protein, Drosophila ; Rhodopsin (9009-81-8) ; Protein-Serine-Threonine Kinases (EC 2.7.11.1) ; hpo protein, Drosophila (EC 2.7.11.1)
Language	English
Publishing date	2013-07-11
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	1114-9
ISSN	1095-564X ; 0012-1606
ISSN (online)	1095-564X
ISSN	0012-1606
DOI	10.1016/j.ydbio.2013.07.001
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