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Identification of RNAs containing TOP3B cleavage complexes

ABSTRACT: Human TOP3B is unique as it can act as RNA topoisomerase. For identification of RNAs with TOP3B cleavage sites, we engineered a “self-trapping” mutant of TOP3B (R338W TOP3B) and performed performed native RNA Immunoprecipitation and sequencing without crosslinking (Native RIP seq). 2,856 RNAs (Supplementary Figure 7F) were enriched in R338W TOP3B immunoprecipitated samples and found that TOP3B regulates key cellular RNA-related pathways.

ORGANISM(S): Homo sapiens

PROVIDER: GSE155996 | GEO | 2022/06/24

REPOSITORIES: GEO

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Identification of RNAs containing TOP3B cleavage complexes

Project description:Identification of RNAs containing TOP3B cleavage complexes

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A dual-activity topoisomerase complex regulates mRNA translation and turnover

Project description:Topoisomerase 3β (TOP3B) and TDRD3 form a dual-activity topoisomerase complex that interacts with FMRP and can change the topology of both DNA and RNA. Here, we investigated the post-transcriptional influence of TOP3B and associated proteins on mRNA translation and turnover. First, we discovered that in human HCT116 colon cancer cells, knock-out (KO) of TOP3B had similar effects on mRNA turnover and translation as did TDRD3-KO, while FMRP-KO resulted in rather distinct effects, indicating that TOP3B had stronger coordination with TDRD3 than FMRP in mRNA regulation. Second, we identified TOP3B-bound mRNAs in HCT116 cells; we found that while TOP3B did not directly influence the stability or translation of most TOP3B target mRNAs, it stabilized a subset of target mRNAs but had a more complex effect on translation--enhancing for some mRNAs whereas reducing for others. Interestingly, a point mutation that specifically disrupted TOP3B catalytic activity only partially recapitulated the effects of TOP3B-KO on mRNA stability and translation, suggesting that the impact of TOP3B on target mRNAs is only in part linked to its ability to change topology of mRNAs. Collectively, our data suggest that TOP3B-TDRD3 can regulate mRNA translation and turnover by mechanisms that are dependent and independent of topoisomerase activity.

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Project description:Topoisomerases are required to release topological stress generated by RNA polymerase II (RNAPII) during transcription. Here we show that in response to starvation, the complex of topoisomerase 3b (TOP3B) and TDRD3 can promote transcriptional activation or repression. Human HCT116 cells individually inactivated for TOP3B, TDRD3, or TOP3B topoisomerase activity, exhibit similarly disrupted transcription for both starvation-activated genes (SAGs) and starvation-repressed genes (SRGs). Responding to starvation, both TOP3B-TDRD3 and the elongating form of RNAPII exhibit concomitantly increased binding to TOP3B-dependent SAGs, at binding sites that overlap. Strikingly, TOP3B inactivation decreases the binding of elongating RNAPII to TOP3B-dependent SAGs while increased it to SRGs. Furthermore, TOP3B-ablated cells display reduced transcription of several autophagy-associated genes and autophagy per se. Our data suggest that TOP3B-TDRD3 can promote both transcriptional activation and repression by regulating RNAPII distribution. In addition, the findings that it can facilitate autophagy may account for the shortened lifespan of Top3b-KO mice.

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Topoisomerase 3B Interacts with RNAi Machinery to Promote Heterochromatin Formation and Transcriptional Silencing

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Project description:Topoisomerases solve topological problems during DNA metabolism, but whether they participate in RNA metabolism remains unclear. Top3b represents a family of topoisomerases carrying activities for both DNA and RNA. Here we show that in Drosophila, Top3b interacts biochemically and genetically with the RNAi-induced silencing complex (RISC) containing AGO2, p68 RNA helicase, and FMRP. Top3b and RISC mutants are similarly defective in heterochromatin formation and transcriptional silencing by position-effect variegation assay. Moreover, both Top3b and AGO2 mutants exhibit reduced levels of heterochromatin protein HP1 in pericentric heterochromatin. Furthermore, expression of several genes and transposable elements in heterochromatin is increased in the Top3b mutant. Notably, Top3b mutants defective in either RNA binding or catalytic activity are deficient in promoting HP1 recruitment and silencing of transposable elements. Our data suggest that Top3b may act as an RNA topoisomerase in siRNA-guided heterochromatin formation and transcriptional silencing.

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