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Mono-ADP-ribosylation, a MARylationmultifaced modification of protein, DNA and RNA: characterizations, functions and mechanisms
Facts
MARTs catalyze MARylation, the hydrolases reverse MARylation and ADP-ribose binding domains recognize MARylation.
The newly identified MARylated substrates includes protein, DNA and RNA, and possess physiological and pathological roles in mammal via diverse mechanisms.
Targeting MARylation and MARylation-associated enzymes are promising therapeutic perspectives in human diseases.
Open questions
What are the biofunctions of nucleic acids MARylation, especially RNA MARylation.
Is there any undiscovered enzymes regulating MARylation reactions.
What is the potential connection between MARylation and PARylation.
Introduction
ADP-ribosylation is a dynamic covalent modification that highly conserved throughout almost all domains of life [1]. The processes of this modification include transferring the ADP-ribose from nicotinamide adenine dinucleotide (NAD) to its specific substrate meanwhile releasing nicotinamide. ADP-ribosylation was firstly defined as a post transcriptional modification (PTM) of protein in the sixties [2], followed by described crucial roles in the DNA damage responses [3]. In the following decades, major cellular processes involving cell growth and differentiation, transcription, stress responses, metabolisms and immunity were sequentially proved to be modulated by ADP-ribosylation as a PTM [4]. Of note, recent studies demonstrated ADP-ribosylation of nucleotides, besides protein targets [5]. In this enzymatic reaction, according to their roles, the enzymes can be categorized as ADP-ribosyl transferases (ARTs) which add ADP-ribose and ADP-ribosyl hydrolases which remove the ADP-ribose (Fig. 1). ADP-ribosylation is grouped into two patterns that MARylation identified by a single ADP-ribose unit linked to targets while PARylation containing polymers of ADP-ribose unit modification. Published in final edited form as: Cell Rep. 2022 Jun 14;39(11):110944. doi: 10.1016/j.celrep.2022.110944 To better understand the functions of non-coding enhancer RNAs (eRNAs), we annotated the estrogen-regulated eRNA transcriptome in estrogen receptor α (ERα)-positive breast cancer cells using PRO-cap and RNA sequencing. We then cloned a subset of the eRNAs identified, fused them to single guide RNAs, and targeted them to their ERα enhancers of origin using CRISPR/dCas9. Some of the eRNAs tested modulated the expression of cognate, but not heterologous, target genes after estrogen treatment by increasing ERα recruitment and stimulating p300-catalyzed H3K27 acetylation at the enhancer. We identified a ~40 nucleotide functional eRNA regulatory motif (FERM) present in many eRNAs that was necessary and sufficient to modulate gene expression, but not the specificity of activation, after estrogen treatment. The FERM interacted with BCAS2, an RNA-binding protein amplified in breast cancers. The ectopic expression of a targeted eRNA controlling the expression of an oncogene resulted in increased cell proliferation, demonstrating the regulatory potential of eRNAs in breast cancer. Hou and Kraus show that some eRNAs fused to sgRNAs can be targeted back to their ERα enhancers to stimulate ERα recruitment, p300-catalyzed H3K27 acetylation, and estrogen-dependent target gene expression. They discovered a conserved functional eRNA regulatory motif (FERM) in some eRNAs that mediates the effects of the functional eRNAs. Enhancers are genomic regulatory elements that act as nucleation sites for the binding of sequence-specific transcription factors and the formation of transcription regulatory complexes (Catarino and Stark, 2018). Enhancers are characterized by common molecular features such as (1) an open or accessible chromatin environment (Boyle et al., 2008; Buen .SUMMARY
Graphical Abstract
In brief
INTRODUCTION