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Absence of RNase H2 triggers generation of immunogenic micronuclei removed by autophagy
Open accessAbstract
Hypomorphic mutations in the DNA repair enzyme RNase H2 cause the neuroinflammatory autoimmune disorder Aicardi-Goutières syndrome (AGS). Endogenous nucleic acids are believed to accumulate in patient cells and instigate pathogenic type I interferon expression. However, the underlying nucleic acid species amassing in the absence of RNase H2 has not been established yet. Here, we report that murine RNase H2 knockout cells accumulated cytosolic DNA aggregates virtually indistinguishable from micronuclei. RNase H2-dependent micronuclei were surrounded by nuclear lamina and most of them contained damaged DNA. Importantly, they induced expression of interferon-stimulated genes (ISGs) and co-localized with the nucleic acid sensor cGAS. Moreover, micronuclei associated with RNase H2 deficiency were cleared by autophagy. Consequently, induction of autophagy by pharmacological mTOR inhibition resulted in a significant reduction of cytosolic DNA and the accompanied interferon signature. Autophagy induction might therefore represent a viable therapeutic option for RNase H2-dependent disease. Endogenous retroelements have previously been proposed as a source of self-nucleic acids triggering inappropriate activation of the immune system in AGS. We used human RNase H2-knockout cells generated by CRISPR/Cas9 to investigate the impact of RNase H2 on retroelement propagation. Surprisingly, replication of LINE-1 and Alu elements was blunted in cells lacking RNase H2, establishing RNase H2 as essential host factor for the mobilisation of endogenous retrotransposons.
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“Similarly, cGAS activation due to rupture of the MN nuclear envelope is thought to be the major trigger of an interferon-based inflammatory response (Bartsch et al., 2017; Gekara, 2017; Harding et al., 2017; Mackenzie et al., 2017).”
From Cytoplasmic DNA: sources, sensing, and role in aging and disease (2021) · cites this paper as Bartsch et al., 2017
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“For example, the loss of nuclear membrane integrity in senescent cells (Shimi et al., 2011) and laminopathies, such as HGPS, parallels loss of membrane integrity in MN (Bartsch et al., 2017; Gekara, 2017; Harding et al., 2017; Mackenzie et al., 2017).”
From Cytoplasmic DNA: sources, sensing, and role in aging and disease (2021) · cites this paper as Bartsch et al., 2017
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Kandabashi, M., Yano, H., Hara, H., Ogawa, S., Kamoda, K., Ishibashi, S., Himeda, K., Baba, M., Takita, T., & Yasukawa, K. (2022) · The Journal of Biochemistry · doi:10.1093/jb/mvac056 · Cited by 1
ESCRT-III accumulates in micronuclei with ruptured nuclear envelopesPreprint
Willan, J., Cleasby, A. J., Rodriguez, N. F., Stefani, F., Rinaldo, C., Pisciottani, A., Grant, E. K., Woodman, P. G., Bryant, H. E., & Ciani, B. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/476630
Gene Polymorphism of XRCC1 in Systemic Lupus Erythematous
Zaki, M. E. S., Abdelsalam, M., Bassiouni, S. A. R. A. K., & Osman, A. O. B. (2021) · The Open Rheumatology Journal · doi:10.2174/1874312902115010024
Imler, J. (2021) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.739487836.793585723
Abskopale Reaktion – ein unterschätzter Effekt mit großem Potenzial
Exner, S., Behrens, F., & Fehlauer, F. (2022) · Deutsche Zeitschrift für Onkologie · doi:10.1055/a-1731-6050
Mergny, J. (2019) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.734702236.793565038
Validation of an RNase H2 activity assay suitable for clinical screeningPreprint
Schulz, M., Günther, C., Behrendt, R., & Roers, A. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.06.09.494809
Dressel, N., Natusch, L., Munz, C. M., Ramon, S. C., Morcos, M. N. F., Loff, A., Hiller, B., Lesche, M., Dahl, A., Luksch, H., et al. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.06.24.497496 · Cited by 1
RNA-mediated double-strand break repair in human cellsPreprint
Jeon, Y., Ferrari, M. M., Channagiri, T., Xu, P., Balachander, S., Park, V. S., Marsili, S., Pursell, Z. F., Jonoska, N., & Storici, F. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.11.01.514688
Construction and characterization of ribonuclease H2 C subunit-knockout NIH3T3 cells
Hara, H., Yano, H., Akazawa, K., Kamoda, K., Kandabashi, M., Baba, M., Takita, T., & Yasukawa, K. (2023) · Bioscience Biotechnology and Biochemistry · doi:10.1093/bbb/zbad077
Pajić, J., & Milovanović, A. P. S. (2023) · International Journal of Radiation Biology · doi:10.1080/09553002.2023.2241901
“…of both chromosome breakage and chromosome loss (Fenech 2007, 2020); moreover, recent studies by Mackenzie et al. (2017), Harding et al. (2017), and Bartsch et al. (2017) proposed MN as a substantial source of immunostimulatory DNA during genotoxic stress suggesting the possibility that fragmented…”
BackgroundAutophagy-targeted drug delivery system in the management of cancer
Gupta, S., Bisht, P., Babu, R., Sharma, Y., & Garabadu, D. (2024) · Elsevier eBooks · doi:10.1016/b978-0-323-95303-0.00002-2
The Pathogenesis and Research Progress of Immunogenic Micronuclei in Tumors
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The role of micronuclei in chromatin elimination
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The Role of Micronuclei in Chromatin Elimination
Akhmadullina, Y. R., & Khomenko, P. O. (2025) · Biology Bulletin Reviews · doi:10.1134/s2079086425700021
“…breaks can be associated with the replication process, which is confirmed by the studies that showed that various disturbances in the DNA replication and reparation factors lead to formation of micronuclei with acentric fragments (Bartsch et al., 2017; Bailey et al., 2019; Leimbacher et al., 2019).”
Repurposing Drugs Modulating Autophagy: Toward a New Era for the Treatment of Cancer
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Paul, S., Tomsick, P. L., Milner, J. P., Biswas, S. R., Brindley, S., DeFoor, N., Zavar, L., Wright, G., Soto, Y., & Pickrell, A. M. (2026) · Autophagy · doi:10.1080/15548627.2026.2617844
“Also, the upregulation of autophagy processes pharmacologically by MTOR inhibitors do reduce the levels of micronucleation [41].”
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Self-citationClinical and molecular characterisation of the type I interferonopathies and approaches to therapy
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Autophagy inhibition in pancreatic cancer: hope or hype?
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“…of anti-phagocytic signals [13], limit the cytosolic availability of nuclear and mitochondrial nucleic acids promoting interferon responses [14,15], and counter-act the cytotoxic effects of immune effector molecules including GZMB (granzyme B) [16], globally endowing PDAC cells with…”
Chromosomal instability in cancer: sources, consequences and new therapeutic opportunities
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“267,268 269 – 271 Moreover, inaccurate replication/repair mechanisms and membrane abnormalities can lead to ampli fi cation of oncogenes or loss of tumor suppressor genes as well as altered epigenetic control of shattered chromosomal fragments within MN. 265,272 In addition, chromosomal fragments…”
TREX1 limits anti-tumor immunity by degrading short cytosolic DNA molecules
Yang, C. Y., Chami, B., Ursino, C., Johnson, S. M., Faget, J., Mettling, C., Gros, L., Pasero, P., & Lin, Y. (2026) · EMBO Reports · doi:10.1038/s44319-026-00961-8
Metadata
- Authors
- Bartsch, K., Knittler, K., Borowski, C., Rudnik, S., Damme, M., Aden, K., Spehlmann, M. E., Frey, N., Saftig, P., Chalaris, A., & Rabe, B.
- Affiliations
- Christian-Albrechts-Universität zu Kiel (DE)
- University Hospital Schleswig-Holstein (DE)
- Corresponding author
- Rabe, Björn
- Venue
- Human Molecular Genetics
- Publisher
- Oxford University Press (OUP)
- Published
- 2017-07-17
- Volume
- 26
- Issue
- 20
- Pages
- 3960-3972
- ISSN
- 0964-6906 (ISSN-L)
- 1460-2083
- OpenAlex
- W2735349030
- Cited by
- 196
- References
- 52
- Citations by year
- 2026: 10 · 2025: 12 · 2024: 18 · 2023: 23 · 2022: 20 · 2021: 27 · 2020: 25 · 2019: 28 · 2018: 31 · 2017: 2
- FWCI
- 10.67
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Human Molecular Genetics (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Deutsche Forschungsgemeinschaft (RA 2404/1-1)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › interferon and immune responses
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA Repair Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Autophagy in Disease and Therapy
- Keywords
- RNase H2, Aicardi-Goutières syndrome, autophagy, micronuclei, cytosolic DNA, type I interferon, cGAS, interferon-stimulated genes, endogenous retrotransposons, LINE-1, Alu elements, mTOR inhibition, DNA repair, neuroinflammation
- MeSH terms
- Animals, Autophagy, DNA, DNA Damage, DNA Replication, Mutation, Nervous System Malformations, Ribonuclease H, Mice, Knockout, Autoimmune Diseases of the Nervous System, Micronucleus, Germline, Mice
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