Effects of the cross-talk between PARP12/PARP13 and nonsense mediated RNA decay pathway on RNA stability and replication of SARS-CoV-2

Nandadeva Lokugamage; Subhadip Choudhuri; Kempaiah Rayavara; Chien-Te Tseng; Shinji Makino; Nisha Jain Garg

Nandadeva Lokugamage, Subhadip Choudhuri, Kempaiah Rayavara, Chien-Te Tseng, Shinji Makino, Nisha Jain Garg

Frontiers in Virology, doi:10.3389/fviro.2025.1691166

Background: Nonsense-mediated mRNA decay (NMD) pathway recognizes the mRNAs of host and cytoplasmic pathogens harboring aberrant features and targets them for degradation. Poly(ADP-ribose) polymerases (PARPs) superfamily consists of 17 members, among which macrodomain and zinc finger PARPs function as regulators of RNA metabolism and transcription. In this study, we investigated whether crosstalk between NMD and PARPs regulates SARS-CoV-2 RNA stability and viral infection. Methods: Transgenic mice (hACE2 tg ) expressing human angiotensin-converting enzyme 2, and human alveolar epithelial cells (Calu-3 ACE2+ , A549 ACE2+ ), in which the expression of NMD factors and PARPs was modulated by molecular approaches were used for various studies. Results: We found that NMD pathway targets endogenous and exogenous aberrant transcripts in human lung epithelial cells. Upon SARS-CoV-2 infection, the expression of NMD factors, up-framshift 1 and 2 (UPF1/UPF2) was decreased while PARP12 and PARP13 were significantly increased in Calu-3 ACE2+ and A549 ACE2+ cells and lung tissues of hACE2 tg mice. Depletion of PARP12/PARP13 using target-specific (vs. scrambled) siRNAs significantly enhanced the stability of NMD targeted endogenous and exogenous aberrant transcripts and SARS-CoV-2 subgenomic S, E, M, and N mRNAs in A549 ACE2+ cells, like what was noted in siUPF1/ siUPF2-transfected lung epithelial cells. Conversely, overexpression of PARP12/ PARP13 enhanced the NMD-dependent degradation of aberrant transcripts and SARS-CoV-2 subgenomic and genomic RNAs. Further, overexpression of PARP12/ PARP13 had a dose-dependent effect in enhancing the anti-viral NMD activity and suppression of SARS-CoV-2 replication in infected cells. Conclusion: We conclude that PARP12/PARP13 synergize with NMD pathway to regulate the viral mRNA stability and replication of SARS-CoV-2.

Ethics statement The animal study was approved by Institutional Animal Care and Use Committee. The study was conducted in accordance with the local legislation and institutional requirements. Author contributions Conflict of interest The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. The author(s) declared that they were an editorial board member of Frontiers, at the time of submission. This had no impact on the peer review process and the final decision. Generative AI statement The author(s) declare that no Generative AI was used in the creation of this manuscript. Any alternative text (alt text) provided alongside figures in this article has been generated by Frontiers with the support of artificial intelligence and reasonable efforts have been made to ensure accuracy, including review by the authors wherever possible. If you identify any issues, please contact us. Publisher's note All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

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DOI record: { "DOI": "10.3389/fviro.2025.1691166", "ISSN": [ "2673-818X" ], "URL": "http://dx.doi.org/10.3389/fviro.2025.1691166", "abstract": "\n Background\n Nonsense-mediated mRNA decay (NMD) pathway recognizes the mRNAs of host and cytoplasmic pathogens harboring aberrant features and targets them for degradation. Poly(ADP-ribose) polymerases (PARPs) superfamily consists of 17 members, among which macrodomain and zinc finger PARPs function as regulators of RNA metabolism and transcription. In this study, we investigated whether crosstalk between NMD and PARPs regulates SARS-CoV-2 RNA stability and viral infection.\n \n \n Methods\n \n Transgenic mice (hACE2\n tg\n ) expressing human angiotensin-converting enzyme 2, and human alveolar epithelial cells (Calu-3\n ACE2+\n , A549\n ACE2+\n ), in which the expression of NMD factors and PARPs was modulated by molecular approaches were used for various studies.\n \n \n \n Results\n \n We found that NMD pathway targets endogenous and exogenous aberrant transcripts in human lung epithelial cells. Upon SARS-CoV-2 infection, the expression of NMD factors, up-framshift 1 and 2 (UPF1/UPF2) was decreased while PARP12 and PARP13 were significantly increased in Calu-3\n ACE2+\n and A549\n ACE2+\n cells and lung tissues of hACE2\n tg\n mice. Depletion of PARP12/PARP13 using target-specific (vs. scrambled) siRNAs significantly enhanced the stability of NMD targeted endogenous and exogenous aberrant transcripts and SARS-CoV-2 subgenomic S, E, M, and N mRNAs in A549\n ACE2+\n cells, like what was noted in siUPF1/siUPF2-transfected lung epithelial cells. Conversely, overexpression of PARP12/PARP13 enhanced the NMD-dependent degradation of aberrant transcripts and SARS-CoV-2 subgenomic and genomic RNAs. Further, overexpression of PARP12/PARP13 had a dose-dependent effect in enhancing the anti-viral NMD activity and suppression of SARS-CoV-2 replication in infected cells.\n \n \n \n Conclusion\n We conclude that PARP12/PARP13 synergize with NMD pathway to regulate the viral mRNA stability and replication of SARS-CoV-2.\n ", "alternative-id": [ "10.3389/fviro.2025.1691166" ], "article-number": "1691166", "author": [ { "affiliation": [], "family": "Lokugamage", "given": "Nandadeva", "sequence": "first" }, { "affiliation": [], "family": "Choudhuri", "given": "Subhadip", "sequence": "additional" }, { "affiliation": [], "family": "Rayavara", "given": "Kempaiah", "sequence": "additional" }, { "affiliation": [], "family": "Tseng", "given": "Chien-Te", "sequence": "additional" }, { "affiliation": [], "family": "Makino", "given": "Shinji", "sequence": "additional" }, { "affiliation": [], "family": "Garg", "given": "Nisha Jain", "sequence": "additional" } ], "container-title": "Frontiers in Virology", "container-title-short": "Front. 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