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The long non-coding RNA nuclear-enriched abundant transcript 1_2 induces paraspeckle formation in the motor neuron during the early phase of amyotrophic lateral sclerosis
Open accessAbstract
BACKGROUND: A long non-coding RNA (lncRNA), nuclear-enriched abundant transcript 1_2 (NEAT1_2), constitutes nuclear bodies known as "paraspeckles". Mutations of RNA binding proteins, including TAR DNA-binding protein-43 (TDP-43) and fused in sarcoma/translocated in liposarcoma (FUS/TLS), have been described in amyotrophic lateral sclerosis (ALS). ALS is a devastating motor neuron disease, which progresses rapidly to a total loss of upper and lower motor neurons, with consciousness sustained. The aim of this study was to clarify the interaction of paraspeckles with ALS-associated RNA-binding proteins, and to identify increased occurrence of paraspeckles in the nucleus of ALS spinal motor neurons. RESULTS: In situ hybridization (ISH) and ultraviolet cross-linking and immunoprecipitation were carried out to investigate interactions of NEAT1_2 lncRNA with ALS-associated RNA-binding proteins, and to test if paraspeckles form in ALS spinal motor neurons. As the results, TDP-43 and FUS/TLS were enriched in paraspeckles and bound to NEAT1_2 lncRNA directly. The paraspeckles were localized apart from the Cajal bodies, which were also known to be related to RNA metabolism. Analyses of 633 human spinal motor neurons in six ALS cases showed NEAT1_2 lncRNA was upregulated during the early stage of ALS pathogenesis. In addition, localization of NEAT1_2 lncRNA was identified in detail by electron microscopic analysis combined with ISH for NEAT1_2 lncRNA. The observation indicating specific assembly of NEAT1_2 lncRNA around the interchromatin granule-associated zone in the nucleus of ALS spinal motor neurons verified characteristic paraspeckle formation. CONCLUSIONS: NEAT1_2 lncRNA may act as a scaffold of RNAs and RNA binding proteins in the nuclei of ALS motor neurons, thereby modulating the functions of ALS-associated RNA-binding proteins during the early phase of ALS. These findings provide the first evidence of a direct association between paraspeckle formation and a neurodegenerative disease, and may shed light on the development of novel therapeutic targets for the treatment of ALS.
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Cites
Ubiquitinated TDP-43 in Frontotemporal Lobar Degeneration and Amyotrophic Lateral Sclerosis
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TDP-43 Mutations in Familial and Sporadic Amyotrophic Lateral Sclerosis
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Mutations in FUS, an RNA Processing Protein, Cause Familial Amyotrophic Lateral Sclerosis Type 6
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Mutations in the FUS/TLS Gene on Chromosome 16 Cause Familial Amyotrophic Lateral Sclerosis
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TARDBP mutations in individuals with sporadic and familial amyotrophic lateral sclerosis
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Self-citationCharacterizing the RNA targets and position-dependent splicing regulation by TDP-43
Tollervey, J. R., Curk, T., Rogelj, B., Briese, M., Cereda, M., Kayikci, M., König, J., Hortobágyi, T., Nishimura, A. L., Župunski, V., et al. (2011) · Nature Neuroscience · doi:10.1038/nn.2778 · Cited by 1,165
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Paraspeckles: Where Long Noncoding RNA Meets Phase Separation
Fox, A. H., Nakagawa, S., Hirose, T., & Bond, C. S. (2018) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2017.12.001 · Cited by 441
Self-citationThe Long Non-Coding RNAs in Neurodegenerative Diseases: Novel Mechanisms of Pathogenesis
Riva, P., Ratti, A., & Venturin, M. (2016) · Current Alzheimer Research · doi:10.2174/1567205013666160622112234 · Cited by 312
Lekka, E., & Hall, J. (2018) · FEBS Letters · doi:10.1002/1873-3468.13182 · Cited by 251
Functional roles and networks of non-coding RNAs in the pathogenesis of neurodegenerative diseases
Wu, Y.-Y., & Kuo, H.-C. (2020) · Journal of Biomedical Science · doi:10.1186/s12929-020-00636-z · Cited by 213
Mutant FUS and ELAVL4 (HuD) Aberrant Crosstalk in Amyotrophic Lateral Sclerosis
De Santis, R., Alfano, V., de Turris, V., Colantoni, A., Santini, L., Garone, M. G., Antonacci, G., Peruzzi, G., Sudria-Lopez, E., Wyler, E., et al. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.05.085 · Cited by 70
Metadata
- Authors
- Nishimoto, Y., Nakagawa, S., Hirose, T., Okano, H., Takao, M., Shibata, S., Suyama, S., Kuwako, K.-I., Imai, T., Murayama, S., Suzuki, N., & Okano, H.
- Venue
- Molecular Brain
- Published
- 2013
- Volume
- 6
- Issue
- 1
- Pages
- 31
- ISSN
- 1756-6606 (ISSN-L)
- OpenAlex
- W2024715297
- Cited by
- 272
- References
- 50
- FWCI
- 6.65
- Type
- journal article
- Language
- en
- Open access
- gold
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- Nishimoto, Y., Nakagawa, S., Hirose, T., Okano, H., Takao, M., Shibata, S., Suyama, S., Kuwako, K.-I., Imai, T., Murayama, S., Suzuki, N., & Okano, H. (2013). The long non-coding RNA nuclear-enriched abundant transcript 1_2 induces paraspeckle formation in the motor neuron during the early phase of amyotrophic lateral sclerosis. Molecular Brain. https://doi.org/10.1186/1756-6606-6-31
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