PUMILIO hyperactivity drives premature aging of Norad-deficient mice
Posted on: 9 October 2018
Preprint posted on 1 October 2018
Article now published in eLife at http://dx.doi.org/10.7554/elife.42650
An (un)expected surprise? NORAD lncRNA regulates tissue homeostasis, genome integrity and mitochrondrial function in vivo.
Selected by Carmen Adriaens
Introduction/background
After the realization that a substantial amount of the transcribed genome does not code for proteins, long non-coding RNAs have been an intense subject of study in the past couple of decades. However, still few have been shown to be essential in vivo, and even less are really functionally and mechanistically understood. One of the more recently studied lncRNAs is Noncoding RNA activated by DNA damage, NORAD, named after its induction upon doxorubicin treatment. NORAD has been initially shown to interact with Pumilio proteins involved in post-transcriptional regulation of RNA targets in the cytoplasm. With its 15+ conserved Pumilio Response Elements (PREs), NORAD was shown to be the preferential binding partner of these proteins, thus serving as a decoy (much like lncRNA can serve as a decoy for microRNAs), so that other PUMILIO targets are not downregulated when they are needed in the cell1,2. An important subset of these targets are mRNAs involved in processes such as chromosomal segregation in cell division and DNA replication1,2. When NORAD is lost, Pumilio proteins become hyperactive and excessively inhibit these targets thus causing aberrant mitosis and aneuploidy. Another recent study has identified NORAD as a central scaffold of a novel nuclear complex, NARC1 (NORAD Activated Ribonucleoprotein Complex 1), which is built on the RNA binding protein RBMX3. Upon DNA damage, NARC1 is formed by shuttling NORAD from the cytoplasm back to the nucleus, where it tethers Topoisomerase I and other factors important for genomic stability together with RBMX.
Although a variety of functions and binding partners of NORAD have been investigated by different groups using cultured mammalian cells1–5, its functions have so far not been explored in vivo. In a recent preprint, the group of Prof. J.T. Mendell tackled the question of whether Norad was also, and similarly, functional in living tissues by making a mouse model constitutively deleted for the mouse Norad ortholog, and comparing the phenotypes in these mice with those overexpressing PUM2.
What are the main findings?
First, the authors found that although Norad KO mice were viable and developed initially in a similar fashion as their WT littermates, soon after they reached adulthood they showed signs of premature aging. For instance, they observed increased baldness, greying hairs, spine deformations, weight loss and muscle and neuronal malfunction in Norad KO mice, and noted they had shorter lifespans as compared to wild types. When looking at the molecular cause for these phenotypes, they initially focused their attention to the well-studied interaction of Norad with Pumilio proteins, which had previously been implicated in aging. The authors could indeed identify a conserved interaction between Norad and Pum2, and found that the published canonical Pumilio targets were largely the same in vivo as they were in cultured cells. Furthermore, Pumilio occupancy on its targets was significantly increased in Norad KO mice, which led to a decrease in their expression in this model.
Next, the authors assessed if the aging phenotypes were due to aberrant mitosis previously reported in vitro. For this, they assessed the highly proliferative blood lineage and could indeed establish that both lymphocytes and splenocytes displayed increased aneuploidy.
Because muscle cells were heavily affected by Norad loss and the observed phenotypes pointed to aging-related diseases, the authors assessed if mitochondrial function was affected (for instance, it is known that mitochondrial defects can lead to premature aging6). They noted that Norad KO mice displayed severe mitochondrial abnormalities, including in their morphology and function, which led to a pathological accumulation of reactive oxygen species and oxidative damage, as well as faulty cellular metabolism and decreased mitochondrial respiration rates. Upon further investigation, they found that Norad-depleted tissues and cell lines showed significantly decreased levels of mitochondria-related genes, a subset of which were shown in PUM2 CLIP experiments to be direct targets of this protein.
As Norad was known to tether away Pum2 to prevent unwanted downregulation of its mRNA targets, the authors hypothesized that Norad KO phenotypes could be phenocopied upon Pum2 overexpression if it functioned in the same way in tissues as it does in vitro. Thus, to definitively establish the link between the Norad KO observed phenotypes and Pum2 hyperactivity, they created a mouse model in which doxycycline (dox) administration ubiquitously induced Flag-PUM2 expression. In this model, dox induction did not cause a significant increase in the levels of PUM2 protein, but rather seemed to replace endogenous protein with the tagged version, an observation potentially explained by the known tight regulation of PUM proteins via negative and positive feedback loops. When PUM2 was forcibly expressed, the mice neatly phenocopied, but with an even faster onset, the absence of Norad, both on the gross physiological level and on the cell biological level including the mitochondrial dysfunction.
Overall, the data in this preprint make a compelling case for Norad lncRNA function in adult tissue physiology through interactions with a tightly regulated RNA binding protein.
What do I think about the work?
In short: I really, really like it. It’s a well-controlled study with a beautiful design and compelling results in living animals. I think it is eye-opening that this abundant lncRNA can have such late-onset phenotypes, and I believe it urges the research community to look further than just the binary “viable or not” question. As this study shows, very highly conserved proteins can undergo lineage-specific fine tuning by less conserved RNAs (eg. here, in the mammalian lineage). Furthermore, I am always captivated by the idea that the biology of adult tissues can differ so significantly from these same tissues during development (why do the phenotypes only occur upon reaching adulthood? What changes are made, for instance in the chromatin, that cells become more sensitive to replication stress, and how are developing tissues protected from it when they need to quickly proliferate?).
Some more topical questions, of course, always remain. For instance, in light of the recent study by Munschauer et al., is the NARC1 conserved in mouse tissues, and if so, are any of the observed phenotypes related to NARC1 and the DNA damage regulating factors bound within it? The authors also mention that not all Norad KO mice show the same degree of phenotype. It would be interesting to determine what drives the penetrance of such phenotype, and if in tissues or individuals in which it is less severe, compensatory mechanisms can be identified. Finally, and this maybe just out of curiosity, are Norad KO mice more cancer prone as well? For instance, are blood cancers more prevalent due to the increased aneuploidy, and could this be an important cause of early death?
Ps. I initially named this paper when I saved its PDF “Norad KO pumilio gone mad”. Maybe not appropriate, but since I still like it as a title, I’ll make it my bottomline! :- ).
References
- Lee, S. et al. Noncoding RNA NORAD Regulates Genomic Stability by Sequestering PUMILIO Proteins. Cell (2016). doi:10.1016/j.cell.2015.12.017
- Tichon, A. et al. A conserved abundant cytoplasmic long noncoding RNA modulates repression by Pumilio proteins in human cells. Nat. Commun. (2016). doi:10.1038/ncomms12209
- Munschauer, M. et al. The NORAD lncRNA assembles a topoisomerase complex critical for genome stability. Nature 561, 132–136 (2018).
- Spiniello, M. et al. HyPR-MS for multiplexed discovery of MALAT1, NEAT1, and NORAD lncRNA protein interactomes. J. Proteome Res. 17, 3022–3038 (2018).
- Tichon, A., Perry, R. B. T., Stojic, L. & Ulitsky, I. SAM68 is required for regulation of pumilio by the NORAD long noncoding RNA. Genes Dev. (2018). doi:10.1101/gad.309138.117
- Trifunovic, A. et al. Premature ageing in mice expressing defective mitochondrial DNA polymerase. Nature (2004). doi:10.1038/nature02517
doi: https://doi.org/10.1242/prelights.5136
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This preList contains preprints discussed during the 9th International Symposium on the Biology of Vertebrate Sex Determination. This conference was held in Kona, Hawaii from April 17th to 21st 2023.
| List by | Martin Estermann |
Alumni picks – preLights 5th Birthday
This preList contains preprints that were picked and highlighted by preLights Alumni - an initiative that was set up to mark preLights 5th birthday. More entries will follow throughout February and March 2023.
| List by | Sergio Menchero et al. |
Semmelweis Symposium 2022: 40th anniversary of international medical education at Semmelweis University
This preList contains preprints discussed during the 'Semmelweis Symposium 2022' (7-9 November), organised around the 40th anniversary of international medical education at Semmelweis University covering a wide range of topics.
| List by | Nándor Lipták |
20th “Genetics Workshops in Hungary”, Szeged (25th, September)
In this annual conference, Hungarian geneticists, biochemists and biotechnologists presented their works. Link: http://group.szbk.u-szeged.hu/minikonf/archive/prg2021.pdf
| List by | Nándor Lipták |
2nd Conference of the Visegrád Group Society for Developmental Biology
Preprints from the 2nd Conference of the Visegrád Group Society for Developmental Biology (2-5 September, 2021, Szeged, Hungary)
| List by | Nándor Lipták |
EMBL Conference: From functional genomics to systems biology
Preprints presented at the virtual EMBL conference "from functional genomics and systems biology", 16-19 November 2020
| List by | Jesus Victorino |
TAGC 2020
Preprints recently presented at the virtual Allied Genetics Conference, April 22-26, 2020. #TAGC20
| List by | Maiko Kitaoka et al. |
ECFG15 – Fungal biology
Preprints presented at 15th European Conference on Fungal Genetics 17-20 February 2020 Rome
| List by | Hiral Shah |
Autophagy
Preprints on autophagy and lysosomal degradation and its role in neurodegeneration and disease. Includes molecular mechanisms, upstream signalling and regulation as well as studies on pharmaceutical interventions to upregulate the process.
| List by | Sandra Malmgren Hill |
Zebrafish immunology
A compilation of cutting-edge research that uses the zebrafish as a model system to elucidate novel immunological mechanisms in health and disease.
| List by | Shikha Nayar |
Also in the genomics category:
End-of-year preprints – the genetics & genomics edition
In this community-driven preList, a group of preLighters, with expertise in different areas of genetics and genomics have worked together to create this preprint reading list. Categories include: 1) genomics 2) bioinformatics 3) gene regulation 4) epigenetics
| List by | Chee Kiang Ewe et al. |
BSCB-Biochemical Society 2024 Cell Migration meeting
This preList features preprints that were discussed and presented during the BSCB-Biochemical Society 2024 Cell Migration meeting in Birmingham, UK in April 2024. Kindly put together by Sara Morais da Silva, Reviews Editor at Journal of Cell Science.
| List by | Reinier Prosee |
9th International Symposium on the Biology of Vertebrate Sex Determination
This preList contains preprints discussed during the 9th International Symposium on the Biology of Vertebrate Sex Determination. This conference was held in Kona, Hawaii from April 17th to 21st 2023.
| List by | Martin Estermann |
Semmelweis Symposium 2022: 40th anniversary of international medical education at Semmelweis University
This preList contains preprints discussed during the 'Semmelweis Symposium 2022' (7-9 November), organised around the 40th anniversary of international medical education at Semmelweis University covering a wide range of topics.
| List by | Nándor Lipták |
20th “Genetics Workshops in Hungary”, Szeged (25th, September)
In this annual conference, Hungarian geneticists, biochemists and biotechnologists presented their works. Link: http://group.szbk.u-szeged.hu/minikonf/archive/prg2021.pdf
| List by | Nándor Lipták |
EMBL Conference: From functional genomics to systems biology
Preprints presented at the virtual EMBL conference "from functional genomics and systems biology", 16-19 November 2020
| List by | Jesus Victorino |
TAGC 2020
Preprints recently presented at the virtual Allied Genetics Conference, April 22-26, 2020. #TAGC20
| List by | Maiko Kitaoka et al. |
Also in the molecular biology category:
2024 Hypothalamus GRC
This 2024 Hypothalamus GRC (Gordon Research Conference) preList offers an overview of cutting-edge research focused on the hypothalamus, a critical brain region involved in regulating homeostasis, behavior, and neuroendocrine functions. The studies included cover a range of topics, including neural circuits, molecular mechanisms, and the role of the hypothalamus in health and disease. This collection highlights some of the latest advances in understanding hypothalamic function, with potential implications for treating disorders such as obesity, stress, and metabolic diseases.
| List by | Nathalie Krauth |
BSCB-Biochemical Society 2024 Cell Migration meeting
This preList features preprints that were discussed and presented during the BSCB-Biochemical Society 2024 Cell Migration meeting in Birmingham, UK in April 2024. Kindly put together by Sara Morais da Silva, Reviews Editor at Journal of Cell Science.
| List by | Reinier Prosee |
‘In preprints’ from Development 2022-2023
A list of the preprints featured in Development's 'In preprints' articles between 2022-2023
| List by | Alex Eve, Katherine Brown |
CSHL 87th Symposium: Stem Cells
Preprints mentioned by speakers at the #CSHLsymp23
| List by | Alex Eve |
9th International Symposium on the Biology of Vertebrate Sex Determination
This preList contains preprints discussed during the 9th International Symposium on the Biology of Vertebrate Sex Determination. This conference was held in Kona, Hawaii from April 17th to 21st 2023.
| List by | Martin Estermann |
Alumni picks – preLights 5th Birthday
This preList contains preprints that were picked and highlighted by preLights Alumni - an initiative that was set up to mark preLights 5th birthday. More entries will follow throughout February and March 2023.
| List by | Sergio Menchero et al. |
CellBio 2022 – An ASCB/EMBO Meeting
This preLists features preprints that were discussed and presented during the CellBio 2022 meeting in Washington, DC in December 2022.
| List by | Nadja Hümpfer et al. |
EMBL Synthetic Morphogenesis: From Gene Circuits to Tissue Architecture (2021)
A list of preprints mentioned at the #EESmorphoG virtual meeting in 2021.
| List by | Alex Eve |
FENS 2020
A collection of preprints presented during the virtual meeting of the Federation of European Neuroscience Societies (FENS) in 2020
| List by | Ana Dorrego-Rivas |
ECFG15 – Fungal biology
Preprints presented at 15th European Conference on Fungal Genetics 17-20 February 2020 Rome
| List by | Hiral Shah |
ASCB EMBO Annual Meeting 2019
A collection of preprints presented at the 2019 ASCB EMBO Meeting in Washington, DC (December 7-11)
| List by | Madhuja Samaddar et al. |
Lung Disease and Regeneration
This preprint list compiles highlights from the field of lung biology.
| List by | Rob Hynds |
MitoList
This list of preprints is focused on work expanding our knowledge on mitochondria in any organism, tissue or cell type, from the normal biology to the pathology.
| List by | Sandra Franco Iborra |