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      The long noncoding RNA Six3OS acts in trans to regulate retinal development by modulating Six3 activity

      research-article
      Author(s): 1 , 2 , 1 , 3 , 1 ,
      Publication date (Electronic):
      Journal: Neural Development
      Publisher: BioMed Central

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          Abstract

          Background

          Thousands of different long non-coding RNAs are expressed during embryonic development, but the function of these molecules remains largely unexplored.

          Results

          Here we characterize the expression and function of Six3OS, a long non-coding RNA that is transcribed from the distal promoter region of the gene encoding the homeodomain transcription factor Six3. Overexpression and knockdown analysis of Six3OS reveals that it plays an essential role in regulating retinal cell specification. We further observe that Six3OS regulates Six3 activity in developing retina, but does not do so by modulating Six3 expression. Finally, we show that Six3OS binds directly to Ezh2 and Eya family members, indicating that Six3OS can act as a molecular scaffold to recruit histone modification enzymes to Six3 target genes.

          Conclusions

          Our findings demonstrate a novel mechanism by which promoter-associated long non-coding RNAs can modulate the activity of their associated protein coding genes, and highlight the importance of this diverse class of molecules in the control of neural development.

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          Most cited references28

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          Long noncoding RNA as modular scaffold of histone modification complexes.

          Miao-Chih Tsai, Ohad Manor, Yue Wan … (2010)
          Long intergenic noncoding RNAs (lincRNAs) regulate chromatin states and epigenetic inheritance. Here, we show that the lincRNA HOTAIR serves as a scaffold for at least two distinct histone modification complexes. A 5' domain of HOTAIR binds polycomb repressive complex 2 (PRC2), whereas a 3' domain of HOTAIR binds the LSD1/CoREST/REST complex. The ability to tether two distinct complexes enables RNA-mediated assembly of PRC2 and LSD1 and coordinates targeting of PRC2 and LSD1 to chromatin for coupled histone H3 lysine 27 methylation and lysine 4 demethylation. Our results suggest that lincRNAs may serve as scaffolds by providing binding surfaces to assemble select histone modification enzymes, thereby specifying the pattern of histone modifications on target genes.
          Article 0 comments Cited 1316 times – based on 0 reviews     Review now
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            Kcnq1ot1 antisense noncoding RNA mediates lineage-specific transcriptional silencing through chromatin-level regulation.

            Radha Raman Pandey, Tanmoy Mondal, Faizaan Mohammad … (2008)
            Recent investigations have implicated long antisense noncoding RNAs in the epigenetic regulation of chromosomal domains. Here we show that Kcnq1ot1 is an RNA polymerase II-encoded, 91 kb-long, moderately stable nuclear transcript and that its stability is important for bidirectional silencing of genes in the Kcnq1 domain. Kcnq1ot1 interacts with chromatin and with the H3K9- and H3K27-specific histone methyltransferases G9a and the PRC2 complex in a lineage-specific manner. This interaction correlates with the presence of extended regions of chromatin enriched with H3K9me3 and H3K27me3 in the Kcnq1 domain in placenta, whereas fetal liver lacks both chromatin interactions and heterochromatin structures. In addition, the Kcnq1 domain is more often found in contact with the nucleolar compartment in placenta than in liver. Taken together, our data describe a mechanism whereby Kcnq1ot1 establishes lineage-specific transcriptional silencing patterns through recruitment of chromatin remodeling complexes and maintenance of these patterns through subsequent cell divisions occurs via targeting the associated regions to the perinucleolar compartment.
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              Electroporation and RNA interference in the rodent retina in vivo and in vitro.

              Takahiko Matsuda, Constance L Cepko (2004)
              The large number of candidate genes made available by comprehensive genome analysis requires that relatively rapid techniques for the study of function be developed. Here, we report a rapid and convenient electroporation method for both gain- and loss-of-function studies in vivo and in vitro in the rodent retina. Plasmid DNA directly injected into the subretinal space of neonatal rodent pups was taken up by a significant fraction of exposed cells after several pulses of high voltage. With this technique, GFP expression vectors were efficiently transfected into retinal cells with little damage to the operated pups. Transfected GFP allowed clear visualization of cell morphologies, and the expression persisted for at least 50 days. DNA-based RNA interference vectors directed against two transcription factors important in photoreceptor development led to photoreceptor phenotypes similar to those of the corresponding knockout mice. Reporter constructs carrying retinal cell type-specific promoters were readily introduced into the retina in vivo, where they exhibited the appropriate expression patterns. Plasmid DNA was also efficiently transfected into retinal explants in vitro by high-voltage pulses.
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                Author and article information

                Journal
                Journal ID (nlm-ta): Neural Dev
                Title: Neural Development
                Publisher: BioMed Central
                ISSN (Electronic): 1749-8104
                Publication date Collection: 2011
                Publication date (Electronic): 21 September 2011
                Volume: 6
                Page: 32
                Affiliations
                [1 ]Department of Neuroscience, Neurology and Ophthalmology, Center for High-Throughput Biology and Institute for Cell Engineering, Johns Hopkins University School of Medicine, 733 N. Broadway Avenue, Baltimore, MD 21287, USA
                [2 ]Howard Hughes Medical Institute and Program in Epithelial Biology, Department of Dermatology, Stanford University School of Medicine, Stanford, CA 94305, USA
                [3 ]Department of Pharmacology and Center for High-Throughput Biology, Johns Hopkins University School of Medicine, 733 N. Broadway Avenue, Baltimore, MD 21287, USA
                Article
                Publisher ID: 1749-8104-6-32
                DOI: 10.1186/1749-8104-6-32
                PMC ID: 3191369
                PubMed ID: 21936910
                SO-VID: 4b2abcf9-7873-4919-a0a7-6d98b7a5d72a
                Copyright © Copyright ©2011 Rapicavoli et al; licensee BioMed Central Ltd.
                License:

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                Date received : 28 May 2011
                Date accepted : 21 September 2011
                Categories
                Subject: Research Article

                ScienceOpen disciplines: Neurosciences
                Data availability:
                ScienceOpen disciplines: Neurosciences

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