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The multifaceted role of PARP1 in RNA biogenesis

Advanced Review

Rebekah Eleazer, Yvonne N. Fondufe‐Mittendorf

Published Online: Jul 12 2020

DOI: 10.1002/wrna.1617

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Abstract Poly(ADP‐ribose) polymerases (PARPs) are abundant nuclear proteins that synthesize ADP ribose polymers (pADPr) and catalyze the addition of (p)ADPr to target biomolecules. PARP1, the most abundant and well‐studied PARP, is a multifunctional enzyme that participates in numerous critical cellular processes. A considerable amount of PARP research has focused on PARP1's role in DNA damage. However, an increasing body of evidence outlines more routine roles for PARP and PARylation in nearly every step of RNA biogenesis and metabolism. PARP1's involvement in these RNA processes is pleiotropic and has been ascribed to PARP1's unique flexible domain structures. PARP1 domains are modular self‐arranged enabling it to recognize structurally diverse substrates and to act simultaneously through multiple discrete mechanisms. These mechanisms include direct PARP1‐protein binding, PARP1‐nucleic acid binding, covalent PARylation of target molecules, covalent autoPARylation, and induction of noncovalent interactions with PAR molecules. A combination of these mechanisms has been implicated in PARP1's context‐specific regulation of RNA biogenesis and metabolism. We examine the mechanisms of PARP1 regulation in transcription initiation, elongation and termination, co‐transcriptional splicing, RNA export, and post‐transcriptional RNA processing. Finally, we consider promising new investigative avenues for PARP1 involvement in these processes with an emphasis on PARP1 regulation of subcellular condensates. This article is categorized under: RNA Processing > Splicing Regulation/Alternative Splicing

PARP1 domain structure. (a) PARP1 is composed of three main regions, consisting of six independently folded domains connected by flexible linker regions. The N‐terminal nucleic acid‐binding region contains three zinc finger domains (Zn1, Zn2, Zn3). The BRCA C‐terminus (BRCT)‐containing automodification domain lies in the PARP1 interior. The C‐terminal region contains an additional nucleic acid‐binding motif tryptophan‐glycine–arginine‐rich (WGR) as well as the catalytic domain, which is made up of an alpha helical subdomain and the highly conserved PAR signature subdomain. (b) PARP1 adopts a collapsed conformation for variable substrate recognition during activation (Langelier, Zandarashvili, Aguiar, Black, & Pascal, 2018; Rudolph, Mahadevan, Dyer, & Luger, 2018)

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PARP‐1 regulation of subcellular condensates. (a) PARP1 influences condensate composition through protein shuttling. (b) PAR levels can regulate spatiotemporal dynamics of condensates. (c) PARP1 recruitment of METTL3 may enhance phase separation through hypermethylation of constituent RNA

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PARylation and modes of PARP1 interactions. Upon activation, PARP1 can influence protein functions through either covalent PARylation of target proteins or through non‐covalent interactions after autoPARylation. PAR associates with RNA binding domains where it competes for binding with target RNA. PARG then degrades PAR to mono ADP‐ribose, which can then be further digested by ADP‐ribosyl hydrolase 3 or TARG (not shown)

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PARP1 and co‐transcriptional alternative splicing. PARP1 associates with chromatin at intron/exon boundaries. PARP1 can influence splicing decisions by (1) controlling RNAPII elongation kinetics and (2) once RNAPII passes, PARP1‐chromatin reassembles and can bind to the nascent mRNA, where it controls the recruitment and RNA‐binding capacities of splicing factors at splice sites. Splicing condensate is shown as the yellowish structure

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PARP1's role in transcription elongation. During RNAPII pausing, a chromatin associated PARP1 assists NELF by binding to the nascent pre‐mRNA. Partial phosphorylation of RNAPII carboxy‐terminal domain (CTD) recruits the low complexity region of P‐TEFb, activating CDK9 (reviewed in Thomas et al. (2019)). To release RNAPII, CDK9 then hyperphosphorylates RNAPII's CTD and also phosphorylates NELF‐E. Phosphorylation of NELF‐E then instigates PARylation of NELF‐E by PARP1, which is also autoPARylated. PARylation of NELF‐E and PARP1 inhibit their RNA‐binding, releasing both proteins from the nascent pre‐mRNA, and allowing the RNAPII complex to enter productive elongation. Splicing condensate is shown as the reddish structure

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Poly(ADP‐ribose) polymerase (PARP) in transcription initiation. PARP regulates transcription initiation by (a) promoting local chromatin loosening at active genes; (b) acting as a canonical transcription factor through direct binding of promoter sequences; (c) acting as a co‐factor for other transcription factors; (d) influencing long range chromatin structure; and (e) altering the DNA‐binding capabilities of transcription factors

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