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Direct RNA-RNA Interaction Between Neat1 And Direct RNA-RNA interaction between Neat1 and RNA targets, as a mechanism for RNAs paraspeckle retention Audrey Jacq, Denis Becquet, Séverine Guillen, Bénédicte Boyer, Maria-Montserrat Bello-Goutierrez, Jean-Louis Franc, Anne-Marie François-Bellan To cite this version: Audrey Jacq, Denis Becquet, Séverine Guillen, Bénédicte Boyer, Maria-Montserrat Bello-Goutierrez, et al.. Direct RNA-RNA interaction between Neat1 and RNA targets, as a mechanism for RNAs paraspeckle retention. 2020. hal-03007506 HAL Id: hal-03007506 https://hal.archives-ouvertes.fr/hal-03007506 Preprint submitted on 8 Dec 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. bioRxiv preprint doi: https://doi.org/10.1101/2020.10.26.354712; this version posted October 26, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. Direct RNA-RNA interaction between Neat1 and RNA targets, as a mechanism for RNAs paraspeckle retention Audrey Jacq1, Denis Becquet1, Séverine Guillen1, Bénédicte Boyer1, Maria-Montserrat Bello-Goutierrez1, Jean-Louis Franc1†* and Anne-Marie François-Bellan1†* 1 INP, AMU-CNRS UMR 7051, Faculté des Sciences Médicales et Paramédicales, Campus Timone, 27 Bd Jean Moulin, 13385 Marseille cedex 05 † These authors contributed equally to this work. * To whom correspondence should be addressed. Tel: 33 491 698 807; Fax: 33 491 698 920 Email: [email protected]; [email protected] ORCIDs: Denis Becquet: 0000-0001-8232-7418 Jean-Louis Franc: 0000-0002-2900-5468 Anne-Marie François-Bellan: 0000-0002-3278-4642 bioRxiv preprint doi: https://doi.org/10.1101/2020.10.26.354712; this version posted October 26, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. ABSTRACT Paraspeckles are nuclear ribonucleic complex formed of a long non-coding RNA, nuclear- enriched abundant transcript one (Neat1) and associated RNA-binding proteins (RBP) whose cellular known functions are to sequester in the nucleus both proteins and RNAs. However, how RNAs are bound to paraspeckles is largely unknown. It is highly likely that binding of RNAs may occur via interactions with RBPs and accordingly, two structures present in the 3’UTR of some RNAs have been shown to allow their association to paraspeckles via protein binding. However, Neat1 could also be involved in the targeting of RNAs through direct RNA-RNA interactions. Using a RNA pull-down procedure adapted to select only RNAs engaged in direct RNA-RNA interactions and followed by RNA-seq we showed that in a rat pituitary cell line, GH4C1 cells, 1791 RNAs were associated with paraspeckles by direct interaction with Neat1. Neat1 was actually found able to bind more than 30% of the total transcripts targeted by the paraspeckles, we have identified in this cell line in a previous study. Furthermore, given the biological processes in which direct RNAs targets of Neat1 were involved as determined by gene ontology analysis, it was proposed that Neat1 played a major role in paraspeckle functions such as circadian rhythms, mRNA processing, RNA splicing and regulation of cell cycle. Finally, we provided evidence that direct RNA targets of Neat1 were preferentially bound to the 5’ end of Neat1 demonstrating that they are located in the shell region of paraspeckles. KEYWORDS Paraspeckles, Neat1, RNA-RNA interaction, RNA targets, Psoralen bioRxiv preprint doi: https://doi.org/10.1101/2020.10.26.354712; this version posted October 26, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. INTRODUCTION Paraspeckles are nuclear ribonucleoprotein complexes found in almost all cell lines and tissues from mammals, except for embryonic stem cells (for review see 1, 2). These nuclear bodies are usually detected as a variable number of discrete dots found in close proximity to nuclear speckles (3, 4). The structural element of paraspeckles is a long non- coding RNA, nuclear-enriched abundant transcript one (Neat1). The locus of Neat1 generates two major isoforms, the short one Neat1-1 (previously named MENε) and the long one Neat1- 2 (MENβ) which are transcribed from the same promoter (5, 6). It is known that paraspeckle proteins (PSPs) accumulate on Neat1-2 isoform to form the paraspeckles (7) and that not less than 60 proteins have been identified so far in these nuclear bodies (8). Among them two RNA-binding proteins (RBP), HNRNPK and RBM14, as well as two proteins of the Drosophila Behavior Human Splicing (DBHS) family, NONO and SFPQ, have been shown to be essential for the formation and maintain of paraspeckles (9). These well organized structures can be subdivided into two zones, the core and the shell, the later containing both the 5’ end of Neat1-1 and the 5' and 3' ends of Neat1-2 (10, 11). In addition to proteins, paraspeckles have been shown to retain RNAs in the nucleus. In a rat pituitary cell line, GH4C1 cells, we have previously shown that the expression of both Neat1 and four major PSPs followed a circadian pattern that leads to rhythmic variations in paraspeckle number within the cells (12). As a consequence, paraspeckles rhythmically retain target RNAs in the nucleus of the cells, leading to the rhythmic expression of the correspond- ing genes (13). However, how target mRNAs are bound to paraspeckles is largely unknown. The presence of duplex structures in the target RNAs (14) is a feature that can lead to paraspeckle retention, as it was shown to be the case for the mouse cationic amino acid trans- porter 2 transcribed nuclear-RNA (Ctn-RNA) and the human RNAs Nicolin 1 (NICN1) and Lin28 (15, 16). Indeed these later RNAs contain a dsRNA structure resulting from inverted repeated short interspersed nuclear elements (IRSINEs) in their 3’-UTR (15). In human cells, hundreds of genes contain inverted repeated IRSINEs (mainly IRAlu elements) in their 3’- UTRs (16). However, unexpectedly we didn’t find IRSINEs in 3’-UTR of the 4268 RNAs, we previously identified as paraspeckle RNAs targets using a Neat1 RNA pull-down procedure (17) followed by RNA-sequencing in GH4C1 cells (12). By contrast, a sequence motive of 15 nucleotides identified in the 3’UTR of more than 30% of the 4268 RNAs that are paraspeckle targets may be involved in the nuclear retention of RNAs by paraspeckles through its binding bioRxiv preprint doi: https://doi.org/10.1101/2020.10.26.354712; this version posted October 26, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. by PSP component HNRNPK (18). However, whereas PSPs probably play a crucial role in binding RNA targets, it is also possible that the lncRNA Neat1, in addition to its structural role, may also be directly involved in the binding by base pairing of RNAs and consequently in their retention in paraspeckles. To test this hypothesis, we adapted the Neat1 RNA pull-down procedure we previously described (17) by treating GH4C1 cells with psoralen, which only fix the RNA- RNA interactions by crosslinking the uracil-uracil bounds (19). We found 1791 RNAs directly bound by Neat1, which represent more than 30% of the total paraspeckle targets previously identified (12). By gene ontology analysis, the direct RNAs targets of Neat1 were further shown involved in major paraspeckle functions such as circadian rhythms, mRNA processing, RNA splicing and regulation of cell cycle, underlying the crucial role Neat1 played in these functions by means of RNA-RNA interactions. Since direct RNA targets of Neat1 were shown preferentially bound to the 5' end of Neat1, it is proposed that these direct RNA targets were mainly localized in the shell region of paraspeckles. MATERIALS AND METHODS Cell line culture GH4C1 cells, a rat pituitary somatolactotroph line, were obtained from ATCC (CCL-82.2, lot number: 58945448) with certificate analysis and were confirmed to be free of mycoplasma (MycoAlert). They were grown in 10 cm cell dishes, in an incubator at 37°C, saturated with H2O and with 5% CO2. The HamF10 cell medium was supplemented with 15% horse serum, 2% fetal calf serum, 0.5% streptomycin and 0.5% penicillin. To synchronize cells between themselves and to be able to select the time of maximum Neat1 expression (12), GH4C1 cells were transferred to fresh medium 24 to 30 h before crosslinking. Neat1 pull down LncRNA pull-down (17) is a hybridization-based strategy that uses complementary oligonucleotides to purify lncRNA together with its targets from reversibly cross-linked extracts. In cross-linked extracts, it is expected that some regions of the RNA will be more accessible for hybridization than others due in particular to secondary structure.
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