The DNA glycosylase NEIL2 is protective during SARS-CoV-2 infection

Tapryal, Nisha; Chakraborty, Anirban; Saha, Kaushik; Islam, Azharul; Pan, Lang; Hosoki, Koa; Sayed, Ibrahim M.; Duran, Jason M.; Alcantara, Joshua; Castillo, Vanessa; Tindle, Courtney; Sarker, Altaf H.; Wakamiya, Maki; Cardenas, Victor J.; Sharma, Gulshan; Crotty Alexander, Laura E.; Sur, Sanjiv; Sahoo, Debashis; Ghosh, Gourisankar; Das, Soumita; Ghosh, Pradipta; Boldogh, Istvan; Hazra, Tapas K.

doi:10.1038/s41467-023-43938-0

The DNA glycosylase NEIL2 is protective during SARS-CoV-2 infection

Journal Article · Fri Dec 08 23:00:00 EST 2023 · Nature Communications

DOI:https://doi.org/10.1038/s41467-023-43938-0· OSTI ID:2470867

Tapryal, Nisha ^[1]; Chakraborty, Anirban ^[1]; ^[2]; Islam, Azharul ^[1]; Pan, Lang ^[1]; Hosoki, Koa ^[3]; Sayed, Ibrahim M. ^[4]; Duran, Jason M. ^[5]; ^[6]; Castillo, Vanessa ^[6]; Tindle, Courtney ^[6]; ^[7]; Wakamiya, Maki ^[1]; Cardenas, Victor J. ^[1]; Sharma, Gulshan ^[1]; ^[8]; Sur, Sanjiv ^[3]; ^[6]; ^[9]; Das, Soumita ^[4] more »

University of Texas Medical Branch, Galveston, TX (United States)
SRM University-AP, Andhra Pradesh (India); University of California, San Diego, La Jolla, CA (United States)
Baylor College of Medicine, Houston, TX (United States)
University of Massachusetts-Lowell, MA (United States); University of California, San Diego, CA (United States)
UC San Diego Medical Center, La Jolla, CA (United States)
University of California San Diego, La Jolla, CA (United States)
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
University of California, San Diego, CA (United States)
University of California, San Diego, La Jolla, CA (United States)
University of California San Diego, La Jolla, CA (United States); University of California, San Diego, CA (United States)

SARS-CoV-2 infection-induced aggravation of host innate immune response not only causes tissue damage and multiorgan failure in COVID-19 patients but also induces host genome damage and activates DNA damage response pathways. To test whether the compromised DNA repair capacity of individuals modulates the severity of COVID-19 infection, we analyze DNA repair gene expression in publicly available patient datasets and observe a lower level of the DNA glycosylase NEIL2 in the lungs of severely infected COVID-19 patients. This observation of lower NEIL2 levels is further validated in infected patients, hamsters and ACE2 receptor-expressing human A549 (A549-ACE2) cells. Furthermore, delivery of recombinant NEIL2 in A549-ACE2 cells shows decreased expression of proinflammatory genes and viral E-gene, as well as lowers the yield of viral progeny compared to mock-treated cells. Mechanistically, NEIL2 cooperatively binds to the 5’-UTR of SARS-CoV-2 genomic RNA to block viral protein synthesis. Collectively, these data strongly suggest that the maintenance of basal NEIL2 levels is critical for the protective response of hosts to viral infection and disease.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE; National Institutes for Health; US National Institute of Allergic and Infectious Diseases; US Department of Defense

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 2470867

Journal Information:: Nature Communications, Journal Name: Nature Communications Journal Issue: 1 Vol. 14; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (86)

Interaction properties of human TRAMP‐like proteins and their role in pre‐rRNA 5′ETS turnover Sudo, Haruka; Nozaki, Aya; Uno, Hideaki FEBS Letters, Vol. 590, Issue 17 https://doi.org/10.1002/1873-3468.12314	journal	August 2016
Complexities of the DNA base excision repair pathway for repair of oxidative DNA damage Mitra, Sankar; Boldogh, Istvan; Izumi, Tadahide Environmental and Molecular Mutagenesis, Vol. 38, Issue 2-3 https://doi.org/10.1002/em.1070	journal	January 2001
Can Colchicine as an Old Anti‐Inflammatory Agent Be Effective in COVID‐19? Nasiripour, Somayyeh; Zamani, Farhad; Farasatinasab, Maryam The Journal of Clinical Pharmacology, Vol. 60, Issue 7 https://doi.org/10.1002/jcph.1645	journal	May 2020
Quantitative Analysis of Protein-RNA Interactions by Gel Mobility Shift Ryder, Sean P.; Recht, Michael I.; Williamson, James R. RNA-Protein Interaction Protocols https://doi.org/10.1007/978-1-60327-475-3_7	book	January 2008
The Role and Therapeutic Potential of NF-kappa-B Pathway in Severe COVID-19 Patients Hariharan, Apurva; Hakeem, Abdul Rahman; Radhakrishnan, Subathra Inflammopharmacology, Vol. 29, Issue 1 https://doi.org/10.1007/s10787-020-00773-9	journal	November 2020
Clinical progression and viral load in a community outbreak of coronavirus-associated SARS pneumonia: a prospective study Peiris, Jsm; Chu, Cm; Cheng, Vcc The Lancet, Vol. 361, Issue 9371 https://doi.org/10.1016/S0140-6736(03)13412-5	journal	May 2003
Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China Huang, Chaolin; Wang, Yeming; Li, Xingwang The Lancet, Vol. 395, Issue 10223 https://doi.org/10.1016/S0140-6736(20)30183-5	journal	February 2020
Epidemiological, demographic, and clinical characteristics of 47 cases of Middle East respiratory syndrome coronavirus disease from Saudi Arabia: a descriptive study Assiri, Abdullah; Al-Tawfiq, Jaffar A.; Al-Rabeeah, Abdullah A. The Lancet Infectious Diseases, Vol. 13, Issue 9 https://doi.org/10.1016/S1473-3099(13)70204-4	journal	September 2013
Pathological findings of COVID-19 associated with acute respiratory distress syndrome Xu, Zhe; Shi, Lei; Wang, Yijin The Lancet Respiratory Medicine, Vol. 8, Issue 4 https://doi.org/10.1016/S2213-2600(20)30076-X	journal	April 2020
The immunology of COVID-19: is immune modulation an option for treatment? Zhong, Jixin; Tang, Jungen; Ye, Cong The Lancet Rheumatology, Vol. 2, Issue 7 https://doi.org/10.1016/S2665-9913(20)30120-X	journal	July 2020
Oxidative Stress as Key Player in Severe Acute Respiratory Syndrome Coronavirus (SARS-CoV) Infection Delgado-Roche, Livan; Mesta, Fernando Archives of Medical Research, Vol. 51, Issue 5 https://doi.org/10.1016/j.arcmed.2020.04.019	journal	July 2020
Defective Anti-oxidant System: An Aggravating Factor for COVID-19 Patients Outcome? Kassi, Eva N.; Papavassiliou, Kostas A.; Papavassiliou, Athanasios G. Archives of Medical Research, Vol. 51, Issue 7 https://doi.org/10.1016/j.arcmed.2020.05.017	journal	October 2020
Activation of innate immunity system during aging: NF-kB signaling is the molecular culprit of inflamm-aging Salminen, Antero; Huuskonen, Jari; Ojala, Johanna Ageing Research Reviews, Vol. 7, Issue 2 https://doi.org/10.1016/j.arr.2007.09.002	journal	April 2008
Comprehensive Integration of Single-Cell Data Stuart, Tim; Butler, Andrew; Hoffman, Paul Cell, Vol. 177, Issue 7 https://doi.org/10.1016/j.cell.2019.05.031	journal	June 2019
SARS-CoV-2 Cell Entry Depends on ACE2 and TMPRSS2 and Is Blocked by a Clinically Proven Protease Inhibitor Hoffmann, Markus; Kleine-Weber, Hannah; Schroeder, Simon Cell, Vol. 181, Issue 2 https://doi.org/10.1016/j.cell.2020.02.052	journal	April 2020
Molecular Mechanism of RNA Recognition by Zinc-Finger Antiviral Protein Luo, Xiu; Wang, Xinlu; Gao, Yina Cell Reports, Vol. 30, Issue 1 https://doi.org/10.1016/j.celrep.2019.11.116	journal	January 2020
Increased risk of lung cancer associated with a functionally impaired polymorphic variant of the human DNA glycosylase NEIL2 Dey, Sanjib; Maiti, Amit K.; Hegde, Muralidhar L. DNA Repair, Vol. 11, Issue 6 https://doi.org/10.1016/j.dnarep.2012.03.005	journal	June 2012
Base excision repair: A critical player in many games Wallace, Susan S. DNA Repair, Vol. 19 https://doi.org/10.1016/j.dnarep.2014.03.030	journal	July 2014
AI-guided discovery of the invariant host response to viral pandemics Sahoo, Debashis; Katkar, Gajanan D.; Khandelwal, Soni EBioMedicine, Vol. 68 https://doi.org/10.1016/j.ebiom.2021.103390	journal	June 2021
Early administration of interleukin-6 inhibitors for patients with severe COVID-19 disease is associated with decreased intubation, reduced mortality, and increased discharge Sinha, Pranay; Mostaghim, Anahita; Bielick, Catherine G. International Journal of Infectious Diseases, Vol. 99 https://doi.org/10.1016/j.ijid.2020.07.023	journal	October 2020
COVID-19: A New Virus, but a Familiar Receptor and Cytokine Release Syndrome Hirano, Toshio; Murakami, Masaaki Immunity, Vol. 52, Issue 5 https://doi.org/10.1016/j.immuni.2020.04.003	journal	May 2020
Intrapulmonary administration of purified NEIL2 abrogates NF-κB–mediated inflammation Tapryal, Nisha; Shahabi, Shandy; Chakraborty, Anirban Journal of Biological Chemistry, Vol. 296 https://doi.org/10.1016/j.jbc.2021.100723	journal	January 2021
Nei-like DNA glycosylase 2 selectively antagonizes interferon-β expression upon respiratory syncytial virus infection Pan, Lang; Xue, Yaoyao; Wang, Ke Journal of Biological Chemistry, Vol. 299, Issue 8 https://doi.org/10.1016/j.jbc.2023.105028	journal	August 2023
Old and new antirheumatic drugs for the treatment of COVID-19 Benucci, Maurizio; Damiani, Arianna; Infantino, Maria Joint Bone Spine, Vol. 87, Issue 3 https://doi.org/10.1016/j.jbspin.2020.03.013	journal	May 2020
Sex Hormones and Novel Corona Virus Infectious Disease (COVID-19) Al-Lami, Rasha A.; Urban, Randall J.; Volpi, Elena Mayo Clinic Proceedings, Vol. 95, Issue 8 https://doi.org/10.1016/j.mayocp.2020.05.013	journal	August 2020
AP Endonuclease-Independent DNA Base Excision Repair in Human Cells Wiederhold, Lee; Leppard, John B.; Kedar, Padmini Molecular Cell, Vol. 15, Issue 2 https://doi.org/10.1016/j.molcel.2004.06.003	journal	July 2004
Tackle the free radicals damage in COVID-19 Wu, Jun Nitric Oxide, Vol. 102 https://doi.org/10.1016/j.niox.2020.06.002	journal	September 2020
8-Oxoguanine DNA glycosylase 1: Beyond repair of the oxidatively modified base lesions Ba, Xueqing; Boldogh, Istvan Redox Biology, Vol. 14 https://doi.org/10.1016/j.redox.2017.11.008	journal	April 2018
Reactive oxygen species as an initiator of toxic innate immune responses in retort to SARS-CoV-2 in an ageing population, consider N-acetylcysteine as early therapeutic intervention Nasi, Aikaterini; McArdle, Stephanie; Gaudernack, Gustav Toxicology Reports, Vol. 7 https://doi.org/10.1016/j.toxrep.2020.06.003	journal	January 2020
The structure and functions of coronavirus genomic 3′ and 5′ ends Yang, Dong; Leibowitz, Julian L. Virus Research, Vol. 206 https://doi.org/10.1016/j.virusres.2015.02.025	journal	August 2015
A Clinical-Stage Cysteine Protease Inhibitor blocks SARS-CoV-2 Infection of Human and Monkey Cells Mellott, Drake M.; Tseng, Chien-Te; Drelich, Aleksandra ACS Chemical Biology, Vol. 16, Issue 4 https://doi.org/10.1021/acschembio.0c00875	journal	March 2021
Endogenous Deficiency of Glutathione as the Most Likely Cause of Serious Manifestations and Death in COVID-19 Patients Polonikov, Alexey ACS Infectious Diseases, Vol. 6, Issue 7 https://doi.org/10.1021/acsinfecdis.0c00288	journal	May 2020
Translational repression precedes and is required for ZAP-mediated mRNA decay Zhu, Yiping; Wang, Xinlu; Goff, Stephen P. The EMBO Journal, Vol. 31, Issue 21 https://doi.org/10.1038/emboj.2012.271	journal	September 2012
Base-excision repair of oxidative DNA damage David, Sheila S.; O'Shea, Valerie L.; Kundu, Sucharita Nature, Vol. 447, Issue 7147 https://doi.org/10.1038/nature05978	journal	June 2007
Single-cell dissection of transcriptional heterogeneity in human colon tumors Dalerba, Piero; Kalisky, Tomer; Sahoo, Debashis Nature Biotechnology, Vol. 29, Issue 12 https://doi.org/10.1038/nbt.2038	journal	November 2011
Near-optimal probabilistic RNA-seq quantification Bray, Nicolas L.; Pimentel, Harold; Melsted, Páll Nature Biotechnology, Vol. 34, Issue 5 https://doi.org/10.1038/nbt.3519	journal	April 2016
Classical non-homologous end-joining pathway utilizes nascent RNA for error-free double-strand break repair of transcribed genes Chakraborty, Anirban; Tapryal, Nisha; Venkova, Tatiana Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms13049	journal	October 2016
RNA-binding proteins in immune regulation: a focus on CCCH zinc finger proteins Fu, Mingui; Blackshear, Perry J. Nature Reviews Immunology, Vol. 17, Issue 2 https://doi.org/10.1038/nri.2016.129	journal	December 2016
Structure of N-terminal domain of ZAP indicates how a zinc-finger protein recognizes complex RNA Chen, Shoudeng; Xu, Yihui; Zhang, Kuo Nature Structural & Molecular Biology, Vol. 19, Issue 4 https://doi.org/10.1038/nsmb.2243	journal	March 2012
The architecture of the SARS-CoV-2 RNA genome inside virion Cao, Changchang; Cai, Zhaokui; Xiao, Xia Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-021-22785-x	journal	June 2021
RIG-I-like receptors: their regulation and roles in RNA sensing Rehwinkel, Jan; Gack, Michaela U. Nature Reviews Immunology, Vol. 20, Issue 9 https://doi.org/10.1038/s41577-020-0288-3	journal	March 2020
COVID-19: risk for cytokine targeting in chronic inflammatory diseases? Schett, Georg; Sticherling, Michael; Neurath, Markus F. Nature Reviews Immunology, Vol. 20, Issue 5 https://doi.org/10.1038/s41577-020-0312-7	journal	April 2020
Coronavirus biology and replication: implications for SARS-CoV-2 V’kovski, Philip; Kratzel, Annika; Steiner, Silvio Nature Reviews Microbiology, Vol. 19, Issue 3 https://doi.org/10.1038/s41579-020-00468-6	journal	October 2020
Regulation of cGAS- and RLR-mediated immunity to nucleic acids Ablasser, Andrea; Hur, Sun Nature Immunology, Vol. 21, Issue 1 https://doi.org/10.1038/s41590-019-0556-1	journal	December 2019
Human SARS-CoV-2 has evolved to reduce CG dinucleotide in its open reading frames Wang, Yong; Mao, Jun-Ming; Wang, Guang-Dong Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-69342-y	journal	July 2020
Glucocorticoid (dexamethasone)-induced metabolome changes in healthy males suggest prediction of response and side effects Bordag, Natalie; Klie, Sebastian; Jürchott, Kathrin Scientific Reports, Vol. 5, Issue 1 https://doi.org/10.1038/srep15954	journal	November 2015
CDX2 as a Prognostic Biomarker in Stage II and Stage III Colon Cancer Dalerba, Piero; Sahoo, Debashis; Paik, Soonmyung New England Journal of Medicine, Vol. 374, Issue 3 https://doi.org/10.1056/NEJMoa1506597	journal	January 2016
Identification and characterization of a human DNA glycosylase for repair of modified bases in oxidatively damaged DNA Hazra, Tapas K.; Izumi, Tadahide; Boldogh, Istvan Proceedings of the National Academy of Sciences, Vol. 99, Issue 6 https://doi.org/10.1073/pnas.062053799	journal	March 2002
Three differentiation states risk-stratify bladder cancer into distinct subtypes Volkmer, Jens-Peter; Sahoo, Debashis; Chin, Robert K. Proceedings of the National Academy of Sciences, Vol. 109, Issue 6 https://doi.org/10.1073/pnas.1120605109	journal	January 2012
Effective treatment of severe COVID-19 patients with tocilizumab Xu, Xiaoling; Han, Mingfeng; Li, Tiantian Proceedings of the National Academy of Sciences, Vol. 117, Issue 20 https://doi.org/10.1073/pnas.2005615117	journal	April 2020
Activation of Ras Signaling Pathway by 8-Oxoguanine DNA Glycosylase Bound to Its Excision Product, 8-Oxoguanine Boldogh, Istvan; Hajas, Gyorgy; Aguilera-Aguirre, Leopoldo Journal of Biological Chemistry, Vol. 287, Issue 25 https://doi.org/10.1074/jbc.C112.364620	journal	June 2012
Catecholamine Stress Hormones Regulate Cellular Iron Homeostasis by a Posttranscriptional Mechanism Mediated by Iron Regulatory Protein Tapryal, Nisha; Vivek G., Vishnu; Mukhopadhyay, Chinmay K. Journal of Biological Chemistry, Vol. 290, Issue 12 https://doi.org/10.1074/jbc.M114.592519	journal	March 2015
Neil2 -null Mice Accumulate Oxidized DNA Bases in the Transcriptionally Active Sequences of the Genome and Are Susceptible to Innate Inflammation Chakraborty, Anirban; Wakamiya, Maki; Venkova-Canova, Tatiana Journal of Biological Chemistry, Vol. 290, Issue 41 https://doi.org/10.1074/jbc.M115.658146	journal	August 2015
Oxidized Guanine Base Lesions Function in 8-Oxoguanine DNA Glycosylase-1-mediated Epigenetic Regulation of Nuclear Factor κB-driven Gene Expression Pan, Lang; Zhu, Bing; Hao, Wenjing Journal of Biological Chemistry, Vol. 291, Issue 49 https://doi.org/10.1074/jbc.M116.751453	journal	October 2016
Identification of a Zinc Finger Domain in the Human NEIL2 (Nei-like-2) Protein Das, Aditi; Rajagopalan, Lavanya; Mathura, Venkatarajan S. Journal of Biological Chemistry, Vol. 279, Issue 45 https://doi.org/10.1074/jbc.M406224200	journal	November 2004
Helicobacter pylori infection downregulates the DNA glycosylase NEIL2, resulting in increased genome damage and inflammation in gastric epithelial cells Sayed, Ibrahim M.; Sahan, Ayse Z.; Venkova, Tatiana Journal of Biological Chemistry, Vol. 295, Issue 32 https://doi.org/10.1074/jbc.RA119.009981	journal	August 2020
Remdesivir is a direct-acting antiviral that inhibits RNA-dependent RNA polymerase from severe acute respiratory syndrome coronavirus 2 with high potency Gordon, Calvin J.; Tchesnokov, Egor P.; Woolner, Emma Journal of Biological Chemistry, Vol. 295, Issue 20 https://doi.org/10.1074/jbc.RA120.013679	journal	May 2020
Secondary structure of the SARS-CoV-2 5’-UTR Miao, Zhichao; Tidu, Antonin; Eriani, Gilbert RNA Biology, Vol. 18, Issue 4 https://doi.org/10.1080/15476286.2020.1814556	journal	September 2020
Exploration, normalization, and summaries of high density oligonucleotide array probe level data Irizarry, Rafael A.; Hobbs, Bridget; Collin, Francois Biostatistics, Vol. 4, Issue 2, p. 249-264 https://doi.org/10.1093/biostatistics/4.2.249	journal	April 2003
Dysregulation of Immune Response in Patients With Coronavirus 2019 (COVID-19) in Wuhan, China Qin, Chuan; Zhou, Luoqi; Hu, Ziwei Clinical Infectious Diseases, Vol. 71, Issue 15 https://doi.org/10.1093/cid/ciaa248	journal	March 2020
Zinc finger proteins in the host-virus interplay: multifaceted functions based on their nucleic acid-binding property Wang, Guanming; Zheng, Chunfu FEMS Microbiology Reviews, Vol. 45, Issue 3 https://doi.org/10.1093/femsre/fuaa059	journal	November 2020
Gene Expression Omnibus: NCBI gene expression and hybridization array data repository Edgar, R. Nucleic Acids Research, Vol. 30, Issue 1 https://doi.org/10.1093/nar/30.1.207	journal	January 2002
Cooperative engagement and subsequent selective displacement of SR proteins define the pre-mRNA 3D structural scaffold for early spliceosome assembly Saha, Kaushik; Ghosh, Gourisankar Nucleic Acids Research, Vol. 50, Issue 14 https://doi.org/10.1093/nar/gkac636	journal	July 2022
NCBI GEO: mining millions of expression profiles--database and tools Barrett, T. Nucleic Acids Research, Vol. 33, Issue Database issue https://doi.org/10.1093/nar/gki022	journal	December 2004
NCBI GEO: archive for functional genomics data sets—update Barrett, Tanya; Wilhite, Stephen E.; Ledoux, Pierre Nucleic Acids Research, Vol. 41, Issue D1 https://doi.org/10.1093/nar/gks1193	journal	November 2012
Summaries of Affymetrix GeneChip probe level data Irizarry, R. A. Nucleic Acids Research, Vol. 31, Issue 4 https://doi.org/10.1093/nar/gng015	journal	February 2003
A conserved virus-induced cytoplasmic TRAMP-like complex recruits the exosome to target viral RNA for degradation Molleston, Jerome M.; Sabin, Leah R.; Moy, Ryan H. Genes & Development, Vol. 30, Issue 14 https://doi.org/10.1101/gad.284604.116	journal	July 2016
Repositioning PARP inhibitors for SARS‐CoV‐2 infection(COVID‐19); a new multi‐pronged therapy for acute respiratory distress syndrome? Curtin, Nicola; Bányai, Krisztián; Thaventhiran, James British Journal of Pharmacology, Vol. 177, Issue 16 https://doi.org/10.1111/bph.15137	journal	July 2020
Link to MERS Virus Underscores Bats' Puzzling Threat Kupferschmidt, Kai Science, Vol. 341, Issue 6149 https://doi.org/10.1126/science.341.6149.948	journal	August 2013
Isolation of potent SARS-CoV-2 neutralizing antibodies and protection from disease in a small animal model Rogers, Thomas F.; Zhao, Fangzhu; Huang, Deli Science, Vol. 369, Issue 6506 https://doi.org/10.1126/science.abc7520	journal	June 2020
Zinc Finger-Containing Cellular Transcription Corepressor ZBTB25 Promotes Influenza Virus RNA Transcription and Is a Target for Zinc Ejector Drugs Chen, Shu-Chuan; Jeng, King-Song; Lai, Michael M. C. Journal of Virology, Vol. 91, Issue 20 https://doi.org/10.1128/JVI.00842-17	journal	October 2017
Virus DNA Replication and the Host DNA Damage Response Weitzman, Matthew D.; Fradet-Turcotte, Amélie Annual Review of Virology, Vol. 5, Issue 1 https://doi.org/10.1146/annurev-virology-092917-043534	journal	September 2018
Clinical and immunological features of severe and moderate coronavirus disease 2019 Chen, Guang; Wu, Di; Guo, Wei Journal of Clinical Investigation, Vol. 130, Issue 5 https://doi.org/10.1172/JCI137244	journal	April 2020
RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome Li, Bo; Dewey, Colin N. BMC Bioinformatics, Vol. 12, Issue 1 https://doi.org/10.1186/1471-2105-12-323	journal	August 2011
Age and sex differences in soluble ACE2 may give insights for COVID-19 Swärd, Per; Edsfeldt, Andreas; Reepalu, Anton Critical Care, Vol. 24, Issue 1 https://doi.org/10.1186/s13054-020-02942-2	journal	May 2020
SARS-CoV-2: from its discovery to genome structure, transcription, and replication Brant, Ayslan Castro; Tian, Wei; Majerciak, Vladimir Cell & Bioscience, Vol. 11, Issue 1 https://doi.org/10.1186/s13578-021-00643-z	journal	July 2021
siRNA Screening of a Targeted Library of DNA Repair Factors in HIV Infection Reveals a Role for Base Excision Repair in HIV Integration Espeseth, Amy S.; Fishel, Rick; Hazuda, Daria PLoS ONE, Vol. 6, Issue 3 https://doi.org/10.1371/journal.pone.0017612	journal	March 2011
The Base Excision Repair Pathway Is Required for Efficient Lentivirus Integration Yoder, Kristine E.; Espeseth, Amy; Wang, Xiao-hong PLoS ONE, Vol. 6, Issue 3 https://doi.org/10.1371/journal.pone.0017862	journal	March 2011
IHC Profiler: An Open Source Plugin for the Quantitative Evaluation and Automated Scoring of Immunohistochemistry Images of Human Tissue Samples Varghese, Frency; Bukhari, Amirali B.; Malhotra, Renu PLoS ONE, Vol. 9, Issue 5 https://doi.org/10.1371/journal.pone.0096801	journal	May 2014
Efficacy and safety of corticosteroids in COVID-19 based on evidence for COVID-19, other coronavirus infections, influenza, community-acquired pneumonia and acute respiratory distress syndrome: a systematic review and meta-analysis Ye, Zhikang; Wang, Ying; Colunga-Lozano, Luis Enrique Canadian Medical Association Journal, Vol. 192, Issue 27 https://doi.org/10.1503/cmaj.200645	journal	May 2020
Why does COVID-19 disproportionately affect older people? Mueller, Amber L.; McNamara, Maeve S.; Sinclair, David A. Aging, Vol. 12, Issue 10 https://doi.org/10.18632/aging.103344	journal	May 2020
Activation of the DNA Damage Response by RNA Viruses Ryan, Ellis; Hollingworth, Robert; Grand, Roger Biomolecules, Vol. 6, Issue 1 https://doi.org/10.3390/biom6010002	journal	January 2016
Endothelial Dysfunction through Oxidatively Generated Epigenetic Mark in Respiratory Viral Infections Vlahopoulos, Spiros; Wang, Ke; Xue, Yaoyao Cells, Vol. 10, Issue 11 https://doi.org/10.3390/cells10113067	journal	November 2021
The DNA Glycosylase NEIL2 Suppresses Fusobacterium-Infection-Induced Inflammation and DNA Damage in Colonic Epithelial Cells Sayed, Ibrahim M.; Chakraborty, Anirban; Abd El-Hafeez, Amer Ali Cells, Vol. 9, Issue 9 https://doi.org/10.3390/cells9091980	journal	August 2020
Factors Influencing the Response to Infectious Diseases: Focusing on the Case of SARS and MERS in South Korea Lee, Kyu-Myoung; Jung, Kyujin International Journal of Environmental Research and Public Health, Vol. 16, Issue 8 https://doi.org/10.3390/ijerph16081432	journal	April 2019
Adult stem cell-derived complete lung organoid models emulate lung disease in COVID-19 Tindle, Courtney; Fuller, MacKenzie; Fonseca, Ayden eLife, Vol. 10 https://doi.org/10.7554/eLife.66417	journal	August 2021

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60 APPLIED LIFE SCIENCES
SARS-CoV-2
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Virus–host interactions

The DNA glycosylase NEIL2 is protective during SARS-CoV-2 infection

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