Diversity and Emerging Roles of Enhancer RNA in Regulation of Gene Expression and Cell Fate

Adolescent alcohol exposure epigenetically suppresses amygdala Arc enhancer RNA expression to confer adult anxiety susceptibility

(2019) Evan J. Kyzar et al.   BIOLOGICAL PSYCHIATRY

Aberrant enhancer hypomethylation contributes to hepatic carcinogenesis through global transcriptional reprogramming

(2019) Lei Xiong et al.   Nature Communications

C1 CAGE detects transcription start sites and enhancer activity at single-cell resolution

(2019) Tsukasa Kouno et al.   Nature Communications

AP001056.1, A Prognosis-Related Enhancer RNA in Squamous Cell Carcinoma of the Head and Neck

(2019) Xiaolian Gu et al.   Cancers

Phase separation of ligand-activated enhancers licenses cooperative chromosomal enhancer assembly

(2019) Sreejith J. Nair et al.   NATURE STRUCTURAL & MOLECULAR BIOLOGY

Inhibition of the HIF1α-Induced Cardiospecific HERNA1 eRNA Protects from Heart Disease

(2019) Peter Mirtschink et al.   CIRCULATION

The enhancer RNA ARIEL activates the oncogenic transcriptional program in T-cell acute lymphoblastic leukemia

(2019) Shi Hao Tan et al.   BLOOD

The RNA N6-methyladenosine modification landscape of human fetal tissues

(2019) Shan Xiao et al.   NATURE CELL BIOLOGY

Spontaneous driving forces give rise to protein−RNA condensates with coexisting phases and complex material properties

(2019) Steven Boeynaems et al.   PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA

m6A enhances the phase separation potential of mRNA

(2019) Ryan J. Ries et al.   NATURE

Pol II phosphorylation regulates a switch between transcriptional and splicing condensates

(2019) Yang Eric Guo et al.   NATURE

A Molecular Grammar Governing the Driving Forces for Phase Separation of Prion-like RNA Binding Proteins

(2018) Jie Wang et al.   CELL

Diminished nuclear RNA decay upon Salmonella infection upregulates antibacterial noncoding RNAs

(2018) Katsutoshi Imamura et al.   EMBO JOURNAL

Widespread transcriptional pausing and elongation control at enhancers

(2018) Telmo Henriques et al.   GENES & DEVELOPMENT

The degree of enhancer or promoter activity is reflected by the levels and directionality of eRNA transcription

(2018) Olga Mikhaylichenko et al.   GENES & DEVELOPMENT

Guidance of super-enhancers in regulation of IL-9 induction and airway inflammation

(2018) Xiang Xiao et al.   JOURNAL OF EXPERIMENTAL MEDICINE

MUNC, an eRNA upstream from the MYOD gene, induces a subgroup of myogenic transcripts in trans, independently of MyoD

(2018) Magdalena A. Cichewicz et al.   MOLECULAR AND CELLULAR BIOLOGY

A Muscle-Specific Enhancer RNA Mediates Cohesin Recruitment and Regulates Transcription In trans

(2018) Pei-Fang Tsai et al.   MOLECULAR CELL

Targeted Enhancer Activation by a Subunit of the Integrator Complex

(2018) Elisa Barbieri et al.   MOLECULAR CELL

Differential activity of transcribed enhancers in the prefrontal cortex of 537 cases with schizophrenia and controls

(2018) Mads E. Hauberg et al.   MOLECULAR PSYCHIATRY

Different Neuronal Activity Patterns Induce Different Gene Expression Programs

(2018) Kelsey M. Tyssowski et al.   NEURON

Transcription start site analysis reveals widespread divergent transcription in D. melanogaster and core promoter-encoded enhancer activities

(2018) Sarah Rennie et al.   NUCLEIC ACIDS RESEARCH

HPSE enhancer RNA promotes cancer progression through driving chromatin looping and regulating hnRNPU/p300/EGR1/HPSE axis

(2018) Wanju Jiao et al.   ONCOGENE

RNA buffers the phase separation behavior of prion-like RNA binding proteins

(2018) Shovamayee Maharana et al.   SCIENCE

mRNA structure determines specificity of a polyQ-driven phase separation

(2018) Erin M. Langdon et al.   SCIENCE

Coactivator condensation at super-enhancers links phase separation and gene control

(2018) Benjamin R. Sabari et al.   SCIENCE

Mediator and RNA polymerase II clusters associate in transcription-dependent condensates

(2018) Won-Ki Cho et al.   SCIENCE

Paraspeckles: Where Long Noncoding RNA Meets Phase Separation

(2018) Archa H. Fox et al.   TRENDS IN BIOCHEMICAL SCIENCES

Dissecting super-enhancer hierarchy based on chromatin interactions

(2018) Jialiang Huang et al.   Nature Communications

Dismissal of RNA Polymerase II Underlies a Large Ligand-Induced Enhancer Decommissioning Program

(2018) Yuliang Tan et al.   MOLECULAR CELL

The Evf2 Ultraconserved Enhancer lncRNA Functionally and Spatially Organizes Megabase Distant Genes in the Developing Forebrain

(2018) Ivelisse Cajigas et al.   MOLECULAR CELL

RNAs interact with BRD4 to promote enhanced chromatin engagement and transcription activation

(2018) Homa Rahnamoun et al.   NATURE STRUCTURAL & MOLECULAR BIOLOGY

Enhancer Activity Requires CBP/P300 Bromodomain-Dependent Histone H3K27 Acetylation

(2018) Ryan Raisner et al.   Cell Reports

Transcription Factors Activate Genes through the Phase-Separation Capacity of Their Activation Domains

(2018) Ann Boija et al.   CELL

Transcription factor dimerization activates the p300 acetyltransferase

(2018) Esther Ortega et al.   NATURE

The enhancer RNA lnc-SLC4A1-1 epigenetically regulates unexplained recurrent pregnancy loss (URPL) by activating CXCL8 and NF-kB pathway

(2018) Zhenyao Huang et al.   EBioMedicine

Demethylase Kdm6a epigenetically promotes IL-6 and IFN-β production in macrophages

(2017) Xia Li et al.   JOURNAL OF AUTOIMMUNITY

Expression of long non-coding RNAs in autoimmunity and linkage to enhancer function and autoimmune disease risk genetic variants

(2017) T.M. Aune et al.   JOURNAL OF AUTOIMMUNITY

Profiles of Long Noncoding RNAs in Human Naive and Memory T Cells

(2017) Charles F. Spurlock et al.   JOURNAL OF IMMUNOLOGY

Targeting of Polycomb Repressive Complex 2 to RNA by Short Repeats of Consecutive Guanines

(2017) Xueyin Wang et al.   MOLECULAR CELL

Mll3 and Mll4 Facilitate Enhancer RNA Synthesis and Transcription from Promoters Independently of H3K4 Monomethylation

(2017) Kristel M. Dorighi et al.   MOLECULAR CELL

Intragenic Enhancers Attenuate Host Gene Expression

(2017) Senthilkumar Cinghu et al.   MOLECULAR CELL

SERPINB2 is regulated by dynamic interactions with pause-release proteins and enhancer RNAs

(2017) Lihua Shii et al.   MOLECULAR IMMUNOLOGY

Biomolecular condensates: organizers of cellular biochemistry

(2017) Salman F. Banani et al.   NATURE REVIEWS MOLECULAR CELL BIOLOGY

Functional anatomy of the immunoglobulin heavy chain 3΄ super-enhancer needs not only core enhancer elements but also their unique DNA context

(2017) Sandrine Le Noir et al.   NUCLEIC ACIDS RESEARCH

Genome-wide profiling of transcribed enhancers during macrophage activation

(2017) Elena Denisenko et al.   Epigenetics & Chromatin

The Super-Enhancer-Derived alncRNA-EC7/Bloodlinc Potentiates Red Blood Cell Development in  trans

(2017) Juan R. Alvarez-Dominguez et al.   Cell Reports

Analysis of the human monocyte-derived macrophage transcriptome and response to lipopolysaccharide provides new insights into genetic aetiology of inflammatory bowel disease

(2017) J. Kenneth Baillie et al.   PLoS Genetics

Altered enhancer transcription underlies Huntington’s disease striatal transcriptional signature

(2017) Stéphanie Le Gras et al.   Scientific Reports

Functional annotation of structural ncRNAs within enhancer RNAs in the human genome: implications for human disease

(2017) Chao Ren et al.   Scientific Reports

Polar Positioning of Phase-Separated Liquid Compartments in Cells Regulated by an mRNA Competition Mechanism

(2016) Shambaditya Saha et al.   CELL

Compositional Control of Phase-Separated Cellular Bodies

(2016) Salman F. Banani et al.   CELL

Chromatin remodeling effects on enhancer activity

(2016) Estela García-González et al.   CELLULAR AND MOLECULAR LIFE SCIENCES

The interaction of PRC2 with RNA or chromatin is mutually antagonistic

(2016) Manuel Beltran et al.   GENOME RESEARCH

Unlinking an lncRNA from Its Associated cis Element

(2016) Vikram R. Paralkar et al.   MOLECULAR CELL

Hierarchy within the mammary STAT5-driven Wap super-enhancer

(2016) Ha Youn Shin et al.   NATURE GENETICS

Enhancers as non-coding RNA transcription units: recent insights and future perspectives

(2016) Wenbo Li et al.   NATURE REVIEWS GENETICS

Single-cell profiling reveals that eRNA accumulation at enhancer–promoter loops is not required to sustain transcription

(2016) Samir Rahman et al.   NUCLEIC ACIDS RESEARCH

Epstein–Barr virus super-enhancer eRNAs are essential for MYC oncogene expression and lymphoblast proliferation

(2016) Jun Liang et al.   PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA

Deposition of 5-Methylcytosine on Enhancer RNAs Enables the Coactivator Function of PGC-1α

(2016) Francesca Aguilo et al.   Cell Reports

Enhancer RNA-driven looping enhances the transcription of the long noncoding RNA DHRS4-AS1, a controller of the DHRS4 gene cluster

(2016) Yingying Yang et al.   Scientific Reports

Chromatin looping and eRNA transcription precede the transcriptional activation of gene in the β-globin locus

(2015) Yea Woon Kim et al.   BIOSCIENCE REPORTS

High-density P300 enhancers control cell state transitions

(2015) Steven Witte et al.   BMC GENOMICS

Phase Separation by Low Complexity Domains Promotes Stress Granule Assembly and Drives Pathological Fibrillization

(2015) Amandine Molliex et al.   CELL

RNA Exosome-Regulated Long Non-Coding RNA Transcription Controls Super-Enhancer Activity

(2015) Evangelos Pefanis et al.   CELL

The Integrator complex controls the termination of transcription at diverse classes of gene targets

(2015) Jeffrey R Skaar et al.   CELL RESEARCH

Acute TNF-induced repression of cell identity genes is mediated by NFκB-directed redistribution of cofactors from super-enhancers

(2015) Søren Fisker Schmidt et al.   GENOME RESEARCH

Mediator complex cooperatively regulates transcription of retinoic acid target genes with Polycomb Repressive Complex 2 during neuronal differentiation

(2015) Rikiya Fukasawa et al.   JOURNAL OF BIOCHEMISTRY

CARMEN, a human super enhancer-associated long noncoding RNA controlling cardiac specification, differentiation and homeostasis

(2015) Samir Ounzain et al.   JOURNAL OF MOLECULAR AND CELLULAR CARDIOLOGY

Transcription of Mammalian cis-Regulatory Elements Is Restrained by Actively Enforced Early Termination

(2015) Liv M.I. Austenaa et al.   MOLECULAR CELL

RNA Controls PolyQ Protein Phase Transitions

(2015) Huaiying Zhang et al.   MOLECULAR CELL

Formation and Maturation of Phase-Separated Liquid Droplets by RNA-Binding Proteins

(2015) Yuan Lin et al.   MOLECULAR CELL

Phase Transition of a Disordered Nuage Protein Generates Environmentally Responsive Membraneless Organelles

(2015) Timothy J. Nott et al.   MOLECULAR CELL

Pioneer factors govern super-enhancer dynamics in stem cell plasticity and lineage choice

(2015) Rene C. Adam et al.   NATURE

Integrator mediates the biogenesis of enhancer RNAs

(2015) Fan Lai et al.   NATURE

The histone variant H2A.Z is an important regulator of enhancer activity

(2015) Mylène Brunelle et al.   NUCLEIC ACIDS RESEARCH

Dynamic recruitment of Ets1 to both nucleosome-occupied and -depleted enhancer regions mediates a transcriptional program switch during early T-cell differentiation

(2015) Pierre Cauchy et al.   NUCLEIC ACIDS RESEARCH

New roles for DNA cytosine modification, eRNA, anchors, and superanchors in developing B cell progenitors

(2015) Christopher Benner et al.   PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA

RNA transcribed from a distal enhancer is required for activating the chromatin at the promoter of the gonadotropin α-subunit gene

(2015) Lilach Pnueli et al.   PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA

Inflammation-sensitive super enhancers form domains of coordinately regulated enhancer RNAs

(2015) Nasun Hah et al.   PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA

Transcription factor trapping by RNA in gene regulatory elements

(2015) A. A. Sigova et al.   SCIENCE

Transcribed enhancers lead waves of coordinated transcription in transitioning mammalian cells

(2015) Erik Arner et al.   SCIENCE

Genome-wide analysis of enhancer RNA in gene regulation across 12 mouse tissues

(2015) Jen-Hao Cheng et al.   Scientific Reports

Convergent Transcription at Intragenic Super-Enhancers Targets AID-Initiated Genomic Instability

(2014) Fei-Long Meng et al.   CELL

Environment Drives Selection and Function of Enhancers Controlling Tissue-Specific Macrophage Identities

(2014) David Gosselin et al.   CELL

Enhancer Activation Requires trans-Recruitment of a Mega Transcription Factor Complex

(2014) Zhijie Liu et al.   CELL

Divergent signalling pathways regulate lipopolysaccharide-induced eRNA expression in human monocytic THP1 cells

(2014) James A. Heward et al.   FEBS LETTERS

Regulatory Interactions between RNA and Polycomb Repressive Complex 2

(2014) Catherine Cifuentes-Rojas et al.   MOLECULAR CELL

Integrator Regulates Transcriptional Initiation and Pause Release following Activation

(2014) Alessandro Gardini et al.   MOLECULAR CELL

Enhancer RNA Facilitates NELF Release from Immediate Early Genes

(2014) Katie Schaukowitch et al.   MOLECULAR CELL

An atlas of active enhancers across human cell types and tissues

(2014) Robin Andersson et al.   NATURE

Genetic and epigenetic fine mapping of causal autoimmune disease variants

(2014) Kyle Kai-How Farh et al.   NATURE

BRD4 assists elongation of both coding and enhancer RNAs by interacting with acetylated histones

(2014) Tomohiko Kanno et al.   NATURE STRUCTURAL & MOLECULAR BIOLOGY

Non-coding RNA derived from the region adjacent to the human HO-1 E2 enhancer selectively regulates HO-1 gene induction by modulating Pol II binding

(2014) Atsushi Maruyama et al.   NUCLEIC ACIDS RESEARCH

Enhancer RNAs participate in androgen receptor-driven looping that selectively enhances gene activation

(2014) C.-L. Hsieh et al.   PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA

In search of the determinants of enhancer–promoter interaction specificity

(2014) Joris van Arensbergen et al.   TRENDS IN CELL BIOLOGY

Nuclear stability and transcriptional directionality separate functionally distinct RNA species

(2014) Robin Andersson et al.   Nature Communications

Tissue-Specific RNA Expression Marks Distant-Acting Developmental Enhancers

(2014) Han Wu et al.   PLoS Genetics

Tyrosine phosphorylation of RNA polymerase II CTD is associated with antisense promoter transcription and active enhancers in mammalian cells

(2014) Nicolas Descostes et al.   eLife

Master Transcription Factors and Mediator Establish Super-Enhancers at Key Cell Identity Genes

(2013) Warren A. Whyte et al.   CELL

Super-Enhancers in the Control of Cell Identity and Disease

(2013) Denes Hnisz et al.   CELL

Enhancer transcribed RNAs arise from hypomethylated, Tet-occupied genomic regions

(2013) Kirthi Pulakanti et al.   Epigenetics

Enhancer transcripts mark active estrogen receptor binding sites

(2013) N. Hah et al.   GENOME RESEARCH

eRNAs Promote Transcription by Establishing Chromatin Accessibility at Defined Genomic Loci

(2013) Kambiz Mousavi et al.   MOLECULAR CELL

Remodeling of the Enhancer Landscape during Macrophage Activation Is Coupled to Enhancer Transcription

(2013) Minna U. Kaikkonen et al.   MOLECULAR CELL

Functional roles of enhancer RNAs for oestrogen-dependent transcriptional activation

(2013) Wenbo Li et al.   NATURE

Rev-Erbs repress macrophage gene expression by inhibiting enhancer-directed transcription

(2013) Michael T. Y. Lam et al.   NATURE

Activating RNAs associate with Mediator to enhance chromatin architecture and transcription

(2013) Fan Lai et al.   NATURE

PRC2 binds active promoters and contacts nascent RNAs in embryonic stem cells

(2013) Syuzo Kaneko et al.   NATURE STRUCTURAL & MOLECULAR BIOLOGY

Polyadenylation site–induced decay of upstream transcripts enforces promoter directionality

(2013) Evgenia Ntini et al.   NATURE STRUCTURAL & MOLECULAR BIOLOGY

eRNAs Are Required for p53-Dependent Enhancer Activity and Gene Transcription

(2012) Carlos A. Melo et al.   MOLECULAR CELL

The long-range interaction landscape of gene promoters

(2012) Amartya Sanyal et al.   NATURE

Landscape of transcription in human cells

(2012) Sarah Djebali et al.   NATURE

DNA-binding factors shape the mouse methylome at distal regulatory regions

(2011) Michael B. Stadler et al.   NATURE

Reprogramming transcription by distinct classes of enhancers functionally defined by eRNA

(2011) Dong Wang et al.   NATURE

Transcription initiation platforms and GTF recruitment at tissue-specific enhancers and promoters

(2011) Frederic Koch et al.   NATURE STRUCTURAL & MOLECULAR BIOLOGY

Widespread transcription at neuronal activity-regulated enhancers

(2010) Tae-Kyung Kim et al.   NATURE

A Large Fraction of Extragenic RNA Pol II Transcription Sites Overlap Enhancers

(2010) Francesca De Santa et al.   PLOS BIOLOGY