LncRNA NEAT1 induces autophagy through epigenetic regulation of autophagy-related gene expression in neuroglial cells

doi:10.1002/jcp.30556

. 2022 Jan;237(1):824-832.

doi: 10.1002/jcp.30556. Epub 2021 Aug 16.

LncRNA NEAT1 induces autophagy through epigenetic regulation of autophagy-related gene expression in neuroglial cells

Ziqiang Wang^{1

2}, Shikuan Zhang^{3

4

5}, Kun Li¹

Affiliations

¹ Department of Nuclear Medicine, The First Affiliated Hospital of Shandong First Medical University & Shandong Provincial Qianfoshan Hospital, Jinan, China.
² Biomedical Sciences College & Shandong Medicinal Biotechnology Centre, Shandong First Medical University & Shandong Academy of Medical Sciences, Jinan, China.
³ School of Life Sciences, Tsinghua University, Beijing, China.
⁴ China State Key Laboratory of Chemical Oncogenomics, Tsinghua Shenzhen International Graduate School, Shenzhen, China.
⁵ Key Lab in Healthy Science and Technology of Shenzhen, Tsinghua Shenzhen International Graduate School, Shenzhen, China.

PMID: 34402054
DOI: 10.1002/jcp.30556

LncRNA NEAT1 induces autophagy through epigenetic regulation of autophagy-related gene expression in neuroglial cells

Ziqiang Wang et al. J Cell Physiol. 2022 Jan.

. 2022 Jan;237(1):824-832.

doi: 10.1002/jcp.30556. Epub 2021 Aug 16.

Authors

Ziqiang Wang^{1

2}, Shikuan Zhang^{3

4

5}, Kun Li¹

Affiliations

¹ Department of Nuclear Medicine, The First Affiliated Hospital of Shandong First Medical University & Shandong Provincial Qianfoshan Hospital, Jinan, China.
² Biomedical Sciences College & Shandong Medicinal Biotechnology Centre, Shandong First Medical University & Shandong Academy of Medical Sciences, Jinan, China.
³ School of Life Sciences, Tsinghua University, Beijing, China.
⁴ China State Key Laboratory of Chemical Oncogenomics, Tsinghua Shenzhen International Graduate School, Shenzhen, China.
⁵ Key Lab in Healthy Science and Technology of Shenzhen, Tsinghua Shenzhen International Graduate School, Shenzhen, China.

PMID: 34402054
DOI: 10.1002/jcp.30556

Abstract

Endocytosis and autophagy are two important pathways for amyloid-β (Aβ) clearance in neuroglial cells. Our previous study demonstrated that nuclear paraspeckle assembly transcript 1 (NEAT1) long noncoding RNA modulates Aβ clearance mediated by neuroglial cells via the epigenetic regulation of endocytosis-related genes. Herein, we demonstrate that NEAT1 functions as an autophagy inducer by modulating the expression of multiple autophagy-related genes, including autophagy-related 5 (atg5), autophagy-related 3 (atg3), and beclin1. NEAT1 can promote transcription of these genes by altering histone modification near these transcriptional start sites of the genes and thereby influencing the recruitment of signal transducer and activator of transcription 3 to these gene promoters. Our findings demonstrate a new cellular function of NEAT1 in neuroglial cells and suggest a potential therapeutic target for the treatment of autophagy-related diseases.

Keywords: NEAT1; autophagy; epigenetic; gene regulation; lncRNA.

PubMed Disclaimer

Cited by

Knockdown of NEAT1 prevents post-stroke lipid droplet agglomeration in microglia by regulating autophagy.
Pan Y, Xin W, Wei W, Tatenhorst L, Graf I, Popa-Wagner A, Gerner ST, Huber SE, Kilic E, Hermann DM, Bähr M, Huttner HB, Doeppner TR. Pan Y, et al. Cell Mol Life Sci. 2024 Jan 12;81(1):30. doi: 10.1007/s00018-023-05045-7. Cell Mol Life Sci. 2024. PMID: 38212456 Free PMC article.
LncRNA H19: a novel player in the regulation of diabetic kidney disease.
Wu Q, Huang F. Wu Q, et al. Front Endocrinol (Lausanne). 2023 Oct 27;14:1238981. doi: 10.3389/fendo.2023.1238981. eCollection 2023. Front Endocrinol (Lausanne). 2023. PMID: 37964955 Free PMC article. Review.
Neat1 lncRNA organizes the inflammatory gene expressions in the dorsal root ganglion in neuropathic pain caused by nerve injury.
Maruyama M, Sakai A, Fukunaga T, Miyagawa Y, Okada T, Hamada M, Suzuki H. Maruyama M, et al. Front Immunol. 2023 Aug 8;14:1185322. doi: 10.3389/fimmu.2023.1185322. eCollection 2023. Front Immunol. 2023. PMID: 37614230 Free PMC article.
Non-coding RNAs: Key players in T cell exhaustion.
Li K, Wang Z. Li K, et al. Front Immunol. 2022 Oct 4;13:959729. doi: 10.3389/fimmu.2022.959729. eCollection 2022. Front Immunol. 2022. PMID: 36268018 Free PMC article. Review.
Keeping up with the condensates: The retention, gain, and loss of nuclear membrane-less organelles.
Lacroix E, Audas TE. Lacroix E, et al. Front Mol Biosci. 2022 Sep 20;9:998363. doi: 10.3389/fmolb.2022.998363. eCollection 2022. Front Mol Biosci. 2022. PMID: 36203874 Free PMC article. Review.

See all "Cited by" articles

References

REFERENCES

1. Bravo-San Pedro, J. M., Kroemer, G., & Galluzzi, L. (2017). Autophagy and mitophagy in cardiovascular disease. Circulation Research, 120(11), 1812-1824.
1. Chakravarty, D., Sboner, A., Nair, S. S., Giannopoulou, E., Li, R., Hennig, S., Mosquera, J. M., Pauwels, J., Park, K., Kossai, M., MacDonald, T. Y., Fontugne, J., Erho, N., Vergara, I. A., Ghadessi, M., Davicioni, E., Jenkins, R. B., Palanisamy, N., Chen, Z., … Rubin, M. A. (2014). The oestrogen receptor alpha-regulated lncRNA NEAT1 is a critical modulator of prostate cancer. Nature Communications, 5, 5383.
1. Chen, L. L., & Carmichael, G. G. (2009). Altered nuclear retention of mRNAs containing inverted repeats in human embryonic stem cells: Functional role of a nuclear noncoding RNA. Molecular Cell, 35(4), 467-478.
1. Cho, M. H., Cho, K., Kang, H. J., Jeon, E. Y., Kim, H. S., Kwon, H. J., Kim, H. M., Kim, D. H., & Yoon, S. Y. (2014). Autophagy in microglia degrades extracellular β-amyloid fibrils and regulates the NLRP3 inflammasome. Autophagy, 10(10), 1761-1775.
1. Clemson, C. M., Hutchinson, J. N., Sara, S. A., Ensminger, A. W., Fox, A. H., Chess, A., & Lawrence, J. B. (2009). An architectural role for a nuclear noncoding RNA: NEAT1 RNA is essential for the structure of paraspeckles. Molecular Cell, 33(6), 717-726.

Publication types

Actions

MeSH terms

Actions
Actions
Actions
Actions
Actions
Actions

Substances

Actions

LinkOut - more resources

Full Text Sources
- Wiley

[1] Bravo-San Pedro, J. M., Kroemer, G., & Galluzzi, L. (2017). Autophagy and mitophagy in cardiovascular disease. Circulation Research, 120(11), 1812-1824.

[2] Bravo-San Pedro, J. M., Kroemer, G., & Galluzzi, L. (2017). Autophagy and mitophagy in cardiovascular disease. Circulation Research, 120(11), 1812-1824.

[3] Chakravarty, D., Sboner, A., Nair, S. S., Giannopoulou, E., Li, R., Hennig, S., Mosquera, J. M., Pauwels, J., Park, K., Kossai, M., MacDonald, T. Y., Fontugne, J., Erho, N., Vergara, I. A., Ghadessi, M., Davicioni, E., Jenkins, R. B., Palanisamy, N., Chen, Z., … Rubin, M. A. (2014). The oestrogen receptor alpha-regulated lncRNA NEAT1 is a critical modulator of prostate cancer. Nature Communications, 5, 5383.

[4] Chakravarty, D., Sboner, A., Nair, S. S., Giannopoulou, E., Li, R., Hennig, S., Mosquera, J. M., Pauwels, J., Park, K., Kossai, M., MacDonald, T. Y., Fontugne, J., Erho, N., Vergara, I. A., Ghadessi, M., Davicioni, E., Jenkins, R. B., Palanisamy, N., Chen, Z., … Rubin, M. A. (2014). The oestrogen receptor alpha-regulated lncRNA NEAT1 is a critical modulator of prostate cancer. Nature Communications, 5, 5383.

[5] Chen, L. L., & Carmichael, G. G. (2009). Altered nuclear retention of mRNAs containing inverted repeats in human embryonic stem cells: Functional role of a nuclear noncoding RNA. Molecular Cell, 35(4), 467-478.

[6] Chen, L. L., & Carmichael, G. G. (2009). Altered nuclear retention of mRNAs containing inverted repeats in human embryonic stem cells: Functional role of a nuclear noncoding RNA. Molecular Cell, 35(4), 467-478.

[7] Cho, M. H., Cho, K., Kang, H. J., Jeon, E. Y., Kim, H. S., Kwon, H. J., Kim, H. M., Kim, D. H., & Yoon, S. Y. (2014). Autophagy in microglia degrades extracellular β-amyloid fibrils and regulates the NLRP3 inflammasome. Autophagy, 10(10), 1761-1775.

[8] Cho, M. H., Cho, K., Kang, H. J., Jeon, E. Y., Kim, H. S., Kwon, H. J., Kim, H. M., Kim, D. H., & Yoon, S. Y. (2014). Autophagy in microglia degrades extracellular β-amyloid fibrils and regulates the NLRP3 inflammasome. Autophagy, 10(10), 1761-1775.

[9] Clemson, C. M., Hutchinson, J. N., Sara, S. A., Ensminger, A. W., Fox, A. H., Chess, A., & Lawrence, J. B. (2009). An architectural role for a nuclear noncoding RNA: NEAT1 RNA is essential for the structure of paraspeckles. Molecular Cell, 33(6), 717-726.

[10] Clemson, C. M., Hutchinson, J. N., Sara, S. A., Ensminger, A. W., Fox, A. H., Chess, A., & Lawrence, J. B. (2009). An architectural role for a nuclear noncoding RNA: NEAT1 RNA is essential for the structure of paraspeckles. Molecular Cell, 33(6), 717-726.

Save citation to file

Email citation

Add to Collections

Add to My Bibliography

Your saved search

Create a file for external citation management software

Your RSS Feed

LncRNA NEAT1 induces autophagy through epigenetic regulation of autophagy-related gene expression in neuroglial cells

Affiliations

LncRNA NEAT1 induces autophagy through epigenetic regulation of autophagy-related gene expression in neuroglial cells

Authors

Affiliations

Abstract

Similar articles

Cited by

References

REFERENCES

Publication types

MeSH terms

Substances

LinkOut - more resources

Full Text Sources

Abstract

Similar articles

Cited by

References

REFERENCES

Publication types

MeSH terms

Substances

Related information

LinkOut - more resources

Full Text Sources