Pulmonary infection by SARS-CoV-2 induces senescence accompanied by an inflammatory phenotype in severe COVID-19: possible implications for viral mutagenesis
Open accessAbstract
Background: Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection of the respiratory system can progress to a multisystemic disease with aberrant inflammatory response. Cellular senescence promotes chronic inflammation, named senescence-associated secretory phenotype (SASP). We investigated whether coronavirus disease 2019 (COVID-19) is associated with cellular senescence and SASP. Methods: Autopsy lung tissue samples from 11 COVID-19 patients and 43 age-matched non-COVID-19 controls with similar comorbidities were analysed by immunohistochemistry for SARS-CoV-2, markers of senescence and key SASP cytokines. Virally induced senescence was functionally recapitulated in vitro , by infecting epithelial Vero-E6 cells and a three-dimensional alveosphere system of alveolar type 2 (AT2) cells with SARS-CoV-2 strains isolated from COVID-19 patients. Results: SARS-CoV-2 was detected by immunocytochemistry and electron microscopy predominantly in AT2 cells. Infected AT2 cells expressed angiotensin-converting enzyme 2 and exhibited increased senescence (p16 INK4A and SenTraGor positivity) and interleukin (IL)-1β and IL-6 expression. In vitro , infection of Vero-E6 cells with SARS-CoV-2 induced senescence (SenTraGor), DNA damage (γ-H2AX) and increased cytokine (IL-1β, IL-6, CXCL8) and apolipoprotein B mRNA-editing (APOBEC) enzyme expression. Next-generation sequencing analysis of progenies obtained from infected/senescent Vero-E6 cells demonstrated APOBEC-mediated SARS-CoV-2 mutations. Dissemination of the SARS-CoV-2-infection and senescence was confirmed in extrapulmonary sites (kidney and liver) of a COVID-19 patient. Conclusions: We demonstrate that in severe COVID-19, AT2 cells infected by SARS-CoV-2 exhibit senescence and a proinflammatory phenotype. In vitro , SARS-CoV-2 infection induces senescence and inflammation. Importantly, infected senescent cells may act as a source of SARS-CoV-2 mutagenesis mediated by APOBEC enzymes. Therefore, SARS-CoV-2-induced senescence may be an important molecular mechanism of severe COVID-19, disease persistence and mutagenesis.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
SARS-CoV-2 directly induces senescence in vitro in Vero kidney cells, shown by increased lipofuscin, SASP factors, γH2A.X, and loss of Ki67.
“The direct induction of senescence through infection with SARS-CoV-2 was demonstrated in vitro with a SARS-CoV-2-susceptible kidney cell line (Vero) as detected by an increase in lipofuscin (Box 1), the secretion of SASP factors, including IL-1β, IL-6 and IL-8, and the DNA damage mark γH2A.X, as well as a loss of Ki67 expression44”
From COVID-19 and cellular senescence (2023) · cites this paper as [44]
Lung specimens from COVID-19 patients show much stronger signs of senescence than SARS-CoV-2 negative controls.
“Similar analyses of lung specimens from patients with COVID-19, consistent with multiple independent patient datasets29,44,52, also showed much stronger signs of senescence compared to SARS-CoV-2 negative controls28.”
From COVID-19 and cellular senescence (2023) · cites this paper as [44]
A panel of senescence markers distinguishes nasopharyngeal mucosa from COVID-19 patients versus pre-pandemic controls, with higher reactivity in COVID-19 samples.
“when comparing samples of nasopharyngeal mucosa from patients with COVID-19 to pre-pandemic biopsy samples from individuals without a manifest respiratory tract infection, a panel of senescence markers was shown to robustly discriminate these two groups, with significantly higher reactivity in samples from patients with COVID-19 (refs.28,29,44,52).”
From COVID-19 and cellular senescence (2023) · cites this paper as [44]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Characteristics of SARS-CoV-2 and COVID-19
Hu, B., Guo, H., Zhou, P., & Shi, Z.-L. (2021) · Nature Reviews Microbiology · doi:10.1038/s41579-020-00459-7 · Cited by 5,291 · see citing works
Nalbandian, A., Sehgal, K., Gupta, A., Madhavan, M. V., McGroder, C., Stevens, J. S., Cook, J. R., Nordvig, A. S., Shalev, D., Sehrawat, T. S., et al. (2021) · Nature Medicine · doi:10.1038/s41591-021-01283-z · Cited by 4,862 · see citing works
Cellular Senescence: Defining a Path Forward
Gorgoulis, V., Adams, P. D., Alimonti, A., Bennett, D. C., Bischof, O., Bishop, C., Campisi, J., Collado, M., Evangelou, K., Ferbeyre, G., et al. (2019) · Cell · doi:10.1016/j.cell.2019.10.005 · Cited by 3,225 · see citing works
Self-citationGISAID: Global initiative on sharing all influenza data – from vision to reality
Shu, Y., & McCauley, J. (2017) · Eurosurveillance · doi:10.2807/1560-7917.es.2017.22.13.30494 · Cited by 3,039 · see citing works
Structural and Functional Basis of SARS-CoV-2 Entry by Using Human ACE2
Wang, Q., Zhang, Y., Wu, L., Niu, S., Song, C., Zhang, Z., Lu, G., Qiao, C., Hu, Y., Yuen, K.-Y., et al. (2020) · Cell · doi:10.1016/j.cell.2020.03.045 · Cited by 2,892 · see citing works
An inflammatory cytokine signature predicts COVID-19 severity and survival
Del Valle, D. M., Kim-Schulze, S., Huang, H.-H., Beckmann, N. D., Nirenberg, S., Wang, B., Lavin, Y., Swartz, T. H., Madduri, D., Stock, A., et al. (2020) · Nature Medicine · doi:10.1038/s41591-020-1051-9 · Cited by 2,605 · see citing works
Activation of the DNA damage checkpoint and genomic instability in human precancerous lesions
Gorgoulis, V. G., Vassiliou, L.-V. F., Karakaidos, P., Zacharatos, P., Kotsinas, A., Liloglou, T., Venere, M., DiTullio, R. A., Kastrinakis, N. G., Levy, B., et al. (2005) · Nature · doi:10.1038/nature03485 · Cited by 2,009 · see citing works
Self-citationOncogene-induced senescence is part of the tumorigenesis barrier imposed by DNA damage checkpoints
Bartkova, J., Rezaei, N., Liontos, M., Karakaidos, P., Kletsas, D., Issaeva, N., Vassiliou, L.-V. F., Kolettas, E., Niforou, K., Zoumpourlis, V. C., et al. (2006) · Nature · doi:10.1038/nature05268 · Cited by 1,986 · see citing works
Self-citationData, disease and diplomacy: GISAID's innovative contribution to global health
Elbe, S., & Buckland‐Merrett, G. (2017) · Global Challenges · doi:10.1002/gch2.1018 · Cited by 1,928 · see citing works
A proteomic atlas of senescence-associated secretomes for aging biomarker development
Basisty, N., Kale, A., Jeon, O. H., Kuehnemann, C., Payne, T., Rao, C., Holtz, A., Shah, S., Sharma, V., Ferrucci, L., et al. (2020) · PLOS Biology · doi:10.1371/journal.pbio.3000599 · Cited by 1,348 · see citing works
Cytokine Storm in COVID-19: The Current Evidence and Treatment Strategies
Tang, Y., Liu, J., Zhang, D., Xu, Z., Ji, J., & Wen, C. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.01708 · Cited by 1,094 · see citing works
Senescence and apoptosis: dueling or complementary cell fates?
Childs, B. G., Baker, D. J., Kirkland, J. L., Campisi, J., & van Deursen, J. M. (2014) · The EMBO Reports · doi:10.15252/embr.201439245 · Cited by 915 · see citing works
Unmasking senescence: context-dependent effects of SASP in cancer
Faget, D. V., Ren, Q., & Stewart, S. A. (2019) · Nature Reviews Cancer · doi:10.1038/s41568-019-0156-2 · Cited by 863 · see citing works
Structural Basis for RNA Replication by the SARS-CoV-2 Polymerase
Wang, Q., Wu, J., Wang, H., Gao, Y., Liu, Q., Mu, A., Ji, W., Yan, L., Zhu, Y., Zhu, C., et al. (2020) · Cell · doi:10.1016/j.cell.2020.05.034 · Cited by 779 · see citing works
Chu, H., Chan, J. F., Yuen, T. T., Shuai, H., Yuan, S., Wang, Y., Hu, B., Yip, C. C., Tsang, J. O., Huang, X., et al. (2020) · The Lancet Microbe · doi:10.1016/s2666-5247(20)30004-5 · Cited by 754 · see citing works
Immunity and immunopathology to viruses: what decides the outcome?
Rouse, B. T., & Sehrawat, S. (2010) · Nature reviews. Immunology · doi:10.1038/nri2802 · Cited by 621 · see citing works
Cellular Senescence as a Mechanism and Target in Chronic Lung Diseases
Barnes, P. J., Baker, J. R., & Donnelly, L. (2019) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.201810-1975tr · Cited by 559 · see citing works
Self-citationSARS-CoV-2 immunity: review and applications to phase 3 vaccine candidates
Poland, G., Ovsyannikova, I., & Kennedy, R. (2020) · The Lancet · doi:10.1016/s0140-6736(20)32137-1 · Cited by 540 · see citing works
The aging lung: Physiology, disease, and immunity
Schneider, J. L., Rowe, J. H., Garcia-de-Alba, C., Kim, C. F., Sharpe, A. H., & Haigis, M. C. (2021) · Cell · doi:10.1016/j.cell.2021.03.005 · Cited by 500 · see citing works
Modelling Cryptosporidium infection in human small intestinal and lung organoids
Heo, I., Dutta, D., Schaefer, D. A., Iakobachvili, N., Artegiani, B., Sachs, N., Boonekamp, K. E., Bowden, G. D., Hendrickx, A. P. A., Willems, R. J. L., et al. (2018) · Nature Microbiology · doi:10.1038/s41564-018-0177-8 · Cited by 386 · see citing works
SARS-CoV-2 triggers inflammatory responses and cell death through caspase-8 activation
Li, S., Zhang, Y., Guan, Z., Li, H., Ye, M., Chen, X., Shen, J., Zhou, Y., Shi, Z.-L., Zhou, P., et al. (2020) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-020-00334-0 · Cited by 365 · see citing works
Regulating the adaptive immune response to respiratory virus infection
Braciale, T. J., Sun, J., & Kim, T. S. (2012) · Nature reviews. Immunology · doi:10.1038/nri3166 · Cited by 362 · see citing works
The spatial landscape of lung pathology during COVID-19 progression
Rendeiro, A. F., Ravichandran, H., Bram, Y., Chandar, V., Kim, J., Meydan, C., Park, J., Foox, J., HETHER, T. D., Warren, S. E., et al. (2021) · Nature · doi:10.1038/s41586-021-03475-6 · Cited by 353 · see citing works
Virus-induced senescence is a driver and therapeutic target in COVID-19
Lee, S., Yu, Y., Trimpert, J., Benthani, F., Mairhofer, M., Richter-Pechanska, P., Wyler, E., Belenki, D., Kaltenbrunner, S., Pammer, M., et al. (2021) · Nature · doi:10.1038/s41586-021-03995-1 · Cited by 350 · see citing works
Senolytics reduce coronavirus-related mortality in old mice
Camell, C. D., Yousefzadeh, M. J., Zhu, Y., Prata, L. G. P. L., Huggins, M. A., Pierson, M., Zhang, L., O’Kelly, R. D., Pirtskhalava, T., Xun, P., et al. (2021) · Science · doi:10.1126/science.abe4832 · Cited by 320 · see citing works
Protease-mediated enhancement of severe acute respiratory syndrome coronavirus infection
Matsuyama, S., Ujike, M., Morikawa, S., Tashiro, M., & Taguchi, F. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0503203102 · Cited by 314 · see citing works
Viral infection and the evolution of caspase 8-regulated apoptotic and necrotic death pathways
Mocarski, E. S., Upton, J. W., & Kaiser, W. J. (2011) · Nature reviews. Immunology · doi:10.1038/nri3131 · Cited by 300 · see citing works
Özcan, S., Alessio, N., Acar, M. B., Mert, E., Omerli, F., Peluso, G., & Galderisi, U. (2016) · Aging · doi:10.18632/aging.100971 · Cited by 295 · see citing works
Cell fusion induced by ERVWE1 or measles virus causes cellular senescence
Chuprin, A., Gal, H., Biron-Shental, T., Biran, A., Amiel, A., Rozenblatt, S., & Krizhanovsky, V. (2013) · Genes & Development · doi:10.1101/gad.227512.113 · Cited by 262 · see citing works
Robust, universal biomarker assay to detect senescent cells in biological specimens
Evangelou, K., Lougiakis, N., Rizou, S. V., Kotsinas, A., Kletsas, D., Muñoz‐Espín, D., Kastrinakis, N. G., Pouli, N., Marakos, P., Townsend, P., et al. (2017) · Aging Cell · doi:10.1111/acel.12545 · Cited by 259 · cited 2× · see citing works
“At the cellular level, intrinsic defence mechanisms are activated and outcomes range from complete recovery to cell death [7-11].”
BackgroundMethodSelf-citationSARS-CoV-2 infection of primary human lung epithelium for COVID-19 modeling and drug discovery
Mulay, A., Konda, B. M., Garcia, G., Yao, C., Beil, S., Villalba, J. M., Koziol, C., Sen, C., Purkayastha, A., Kolls, J. K., et al. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.109055 · Cited by 256 · see citing works
Self-citationThe Genome Landscape of the African Green Monkey Kidney-Derived Vero Cell Line
Osada, N., Kohara, A., Yamaji, T., Hirayama, N., Kasai, F., Sekizuka, T., Kuroda, M., & Hanada, K. (2014) · DNA Research · doi:10.1093/dnares/dsu029 · Cited by 250 · see citing works
Algorithmic assessment of cellular senescence in experimental and clinical specimens
Kohli, J., Wang, B., Brandenburg, S. M., Basisty, N., Evangelou, K., Varela-Eirin, M., Campisi, J., Schilling, B., Gorgoulis, V., & Demaria, M. (2021) · Nature Protocols · doi:10.1038/s41596-021-00505-5 · Cited by 196 · see citing works
Self-citationDistinct phenotypes require distinct respiratory management strategies in severe COVID-19
Robba, C., Battaglini, D., Ball, L., Patroniti, N. A., Loconte, M., Brunetti, I., Vena, A., Giacobbe, D. R., Bassetti, M., Rocco, P. R. M., et al. (2020) · Respiratory Physiology & Neurobiology · doi:10.1016/j.resp.2020.103455 · Cited by 185 · see citing works
Di Pierro, F., Derosa, G., Maffioli, P., Bertuccioli, A., Togni, S., Riva, A., Allegrini, P., Khan, A., Khan, S., Khan, B. A., et al. (2021) · International Journal of General Medicine · doi:10.2147/ijgm.s318720 · Cited by 182 · see citing works
Di Pierro, F., Iqtadar, S., Khan, A., Ullah Mumtaz, S., Masud Chaudhry, M., Bertuccioli, A., Derosa, G., Maffioli, P., Togni, S., Riva, A., et al. (2021) · International Journal of General Medicine · doi:10.2147/ijgm.s318949 · Cited by 180 · see citing works
Adaptive immune responses to SARS-CoV-2 infection in severe versus mild individuals
Zhang, F., Gan, R., Zhen, Z., Hu, X., Li, X., Zhou, F., Liu, Y., Chen, C., Xie, S., Zhang, B., et al. (2020) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-020-00263-y · Cited by 163 · see citing works
Senescence and senotherapeutics: a new field in cancer therapy
Myrianthopoulos, V., Evangelou, K., Vasileiou, P. V. S., Cooks, T., Vassilakopoulos, T. P., Pangalis, G. A., Kouloukoussa, M., Kittas, C., Georgakilas, A. G., & Gorgoulis, V. G. (2019) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2018.08.006 · Cited by 160 · see citing works
Self-citationBreaking Bad: How Viruses Subvert the Cell Cycle
Fan, Y., Sanyal, S., & Bruzzone, R. (2018) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2018.00396 · Cited by 147 · see citing works
Venkatesan, S., Angelova, M., Puttick, C., Zhai, H.-R., Caswell, D. R., Lu, W.-T., Dietzen, M., Galanos, P., Evangelou, K., Bellelli, R., et al. (2021) · Cancer Discovery · doi:10.1158/2159-8290.cd-20-0725 · Cited by 134 · see citing works
Self-citationZhao, J., Zhang, L., Lu, A., Han, Y., Colangelo, D., Bukata, C., Scibetta, A., Yousefzadeh, M. J., Li, X., Gurkar, A. U., et al. (2020) · Aging · doi:10.18632/aging.102863 · Cited by 122 · see citing works
Actionable Cytopathogenic Host Responses of Human Alveolar Type 2 Cells to SARS-CoV-2
Hekman, R. M., Hume, A. J., Goel, R. K., Abo, K. M., Huang, J., Blum, B. C., Werder, R. B., Suder, E. L., Paul, I., Phanse, S., et al. (2020) · Molecular Cell · doi:10.1016/j.molcel.2020.11.028 · Cited by 114 · see citing works
Integrating the DNA damage and protein stress responses during cancer development and treatment
Gorgoulis, V. G., Pefani, D., Pateras, I. S., & Trougakos, I. P. (2018) · The Journal of Pathology · doi:10.1002/path.5097 · Cited by 108 · see citing works
Self-citationWurtz, N., Penant, G., Jardot, P., Duclos, N., & Scola, B. L. (2021) · European Journal of Clinical Microbiology & Infectious Diseases · doi:10.1007/s10096-020-04106-0 · Cited by 106 · see citing works
Cell senescence is an antiviral defense mechanism
Baz-Martínez, M., Da Silva-Álvarez, S., Rodríguez, E., Guerra, J., El Motiam, A., Vidal, A., García-Caballero, T., González-Barcia, M., Sánchez, L., Muñoz-Fontela, C., et al. (2016) · Scientific Reports · doi:10.1038/srep37007 · Cited by 103 · see citing works
Ratcliff, J., & Peter Simmonds, K. (2021) · Virology · doi:10.1016/j.virol.2020.12.018 · Cited by 98 · see citing works
Cellular senescence as a potential mediator of COVID‐19 severity in the elderly
Nehme, J., Borghesan, M., Mackedenski, S., Bird, T. G., & Demaria, M. (2020) · Aging Cell · doi:10.1111/acel.13237 · Cited by 94 · see citing works
Type I interferons and related pathways in cell senescence
Frisch, S. M., & MacFawn, I. (2020) · Aging Cell · doi:10.1111/acel.13234 · Cited by 85 · see citing works
SARS-CoV-2 Spike Protein Induces Paracrine Senescence and Leukocyte Adhesion in Endothelial Cells
Meyer, K., Patra, T., Vijayamahantesh, & Ray, R. (2021) · Journal of Virology · doi:10.1128/jvi.00794-21 · Cited by 71 · see citing works
Recent Advances: Molecular Mechanism of RNA Oxidation and Its Role in Various Diseases
Li, Z., Chen, X., Liu, Z., Ye, W., Li, L., Qian, L., Ding, H., Li, P., & Aung, L. H. H. (2020) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2020.00184 · Cited by 67 · see citing works
Deubiquitinating Enzymes in Coronaviruses and Possible Therapeutic Opportunities for COVID-19
Clemente, V., D’Arcy, P., & Bazzaro, M. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21103492 · Cited by 62 · see citing works
SARS-CoV-2 triggers DNA damage response in Vero E6 cells
Victor, J., Deutsch, J., Whitaker, A., Lamkin, E. N., March, A., Zhou, P., Botten, J., & Chatterjee, N. (2021) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2021.09.024 · Cited by 55 · see citing works
The struggle of a good friend getting old: cellular senescence in viral responses and therapy
Kohli, J., Veenstra, I., & Demaria, M. (2021) · The EMBO Reports · doi:10.15252/embr.202052243 · Cited by 52 · see citing works
Komseli, E.-S., Pateras, I. S., Krejsgaard, T., Stawiski, K., Rizou, S. V., Polyzos, A., Roumelioti, F., Chiourea, M., Mourkioti, I., Paparouna, E., et al. (2018) · BMC Genomics · doi:10.1186/s12864-017-4375-1 · Cited by 49 · see citing works
Self-citationThe Interaction of Viruses with the Cellular Senescence Response
Seoane, R., Vidal, S., Bouzaher, Y. H., El Motiam, A., & Rivas, C. (2020) · Biology · doi:10.3390/biology9120455 · Cited by 49 · see citing works
Cellular senescence: friend or foe to respiratory viral infections?
Kelley, W. J., Zemans, R. L., & Goldstein, D. R. (2020) · European Respiratory Journal · doi:10.1183/13993003.02708-2020 · Cited by 44 · see citing works
Sample pooling strategies for SARS-CoV-2 detection
Lаgopati, N., Tsioli, P., Mourkioti, I., Polyzou, A., Papaspyropoulos, A., Zafiropoulos, A., Evangelou, K., Sourvinos, G., & Gorgoulis, V. G. (2020) · Journal of Virological Methods · doi:10.1016/j.jviromet.2020.114044 · Cited by 40 · see citing works
Self-citationViral Infections: Negative Regulators of Apoptosis and Oncogenic Factors
Zamaraev, A. V., Zhivotovsky, B., & Kopeina, G. S. (2020) · Biochemistry (Moscow) · doi:10.1134/s0006297920100077 · Cited by 21 · see citing works
SARS-CoV-2 Antigenemia as a Confounding Factor in Immunodiagnostic Assays: A Case Study
Belogiannis, K., Florou, V. A., Fragkou, P. C., Ferous, S., Chatzis, L. G., Polyzou, A., Lаgopati, N., Touliatou, A., Vassilakos, D., Κίττας, Χ., et al. (2021) · Viruses · doi:10.3390/v13061143 · Cited by 20 · see citing works
Self-citationActionable Cytopathogenic Host Responses of Human Alveolar Type 2 Cells to SARS-CoV-2
Hekman, R. M., Hume, A. J., Goel, R. K., Abo, K. M., Huang, J., Blum, B. C., Werder, R. B., Suder, E. L., Paul, I., Phanse, S., et al. (2021) · Molecular Cell · doi:10.1016/j.molcel.2020.12.028 · Cited by 19 · see citing works
Wang, Y., Wu, S., Zheng, S., Wang, S., Wali, A., Ezhilarasan, R., Sulman, E. P., Koul, D., & Yung, W. K. A. (2017) · Oncotarget · doi:10.18632/oncotarget.17348 · Cited by 19 · see citing works
Cellular senescence as a source of SARS‐CoV‐2 quasispecies
Karakasiliοtis, I., Lаgopati, N., Evangelou, K., & Gorgoulis, V. G. (2021) · FEBS Journal · doi:10.1111/febs.16230 · Cited by 15 · see citing works
Self-citationFlintoft, L. (2011) · Nature Reviews Genetics · doi:10.1038/nrg2945 · Cited by 14 · see citing works
APOBEC3G rescues cells from the deleterious effects of DNA damage
Botvinnik, A., Shivam, P., Smith, Y., Sharma, G., Olshevsky, U., Moshel, O., Manevitch, Z., Climent, N., Oliva, H., Britan‐Rosich, E., et al. (2021) · FEBS Journal · doi:10.1111/febs.16025 · Cited by 12 · see citing works
Inhibition of APOBEC 3G activity impedes double‐stranded DNA repair
Prabhu, P., Shandilya, S. M. D., Britan‐Rosich, E., Nagler, A., Schiffer, C. A., & Kotler, M. (2015) · FEBS Journal · doi:10.1111/febs.13556 · Cited by 12 · see citing works
Evangelou, K., Veroutis, D., Foukas, P. G., Paschalaki, K. E., Lаgopati, N., Dimitriou, M., Papaspyropoulos, A., Hazapis, O. G., Polyzou, A., Havaki, S., et al. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.01.02.424917 · Cited by 7 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
FXR inhibition may protect from SARS-CoV-2 infection by reducing ACE2
Brevini, T., Maes, M., Webb, G. J., John, B. V., Fuchs, C. D., Buescher, G., Wang, L., Griffiths, C., Brown, M. L., Scott, W. E., et al. (2022) · Nature · doi:10.1038/s41586-022-05594-0 · Cited by 296 · see citing works
Self-citationCOVID-19 and cellular senescence
Schmitt, C. A., Tchkonia, T., Niedernhofer, L. J., Robbins, P. D., Kirkland, J. L., & Lee, S. (2023) · Nature Reviews Immunology · doi:10.1038/s41577-022-00785-2 · Cited by 153 · see citing works
Cellular senescence and cardiovascular diseases: moving to the “heart” of the problem
Evangelou, K., Vasileiou, P. V. S., Papaspyropoulos, A., Hazapis, O. G., Petty, R., Demaria, M., & Gorgoulis, V. G. (2022) · Physiological Reviews · doi:10.1152/physrev.00007.2022 · Cited by 124 · see citing works
Self-citationCellular senescence: Neither irreversible nor reversible
Reimann, M., Lee, S., & Schmitt, C. A. (2024) · The Journal of Experimental Medicine · doi:10.1084/jem.20232136 · Cited by 120 · see citing works
Gioia, U., Tavella, S., Martínez-Orellana, P., Cicio, G., Colliva, A., Ceccon, M., Cabrini, M., Henriques, A. C., Fumagalli, V., Paldino, A., et al. (2023) · Nature Cell Biology · doi:10.1038/s41556-023-01096-x · Cited by 116 · see citing works
Challenges in developing Geroscience trials
Rolland, Y., Sierra, F., Ferrucci, L., Barzilai, N., de Cabo, R., Mannick, J. B., Oliva, A. A., Evans, W. J., Angioni, D., Barreto, P. D. S., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-39786-7 · Cited by 94 · see citing works
Senescence of alveolar epithelial progenitor cells: a critical driver of lung fibrosis
Parimon, T., Chen, P., Stripp, B. R., Liang, J., Jiang, D., Noble, P. W., Parks, W. C., & Yao, C. (2023) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00239.2023 · Cited by 89 · see citing works
Self-citationSARS-CoV-2 and innate immunity: the good, the bad, and the “goldilocks”
Sievers, B. L., Cheng, M., Csiba, K., Meng, B., & Gupta, R. K. (2023) · Cellular & Molecular Immunology · doi:10.1038/s41423-023-01104-y · Cited by 78 · see citing works
Liu, B., Peng, Z., Zhang, H., Zhang, N., Liu, Z., Xia, Z., Huang, S., Luo, P., & Cheng, Q. (2025) · Molecular Cancer · doi:10.1186/s12943-025-02284-z · Cited by 82 · see citing works
Cellular senescence and kidney aging
Rex, N., Melk, A., & Schmitt, R. (2023) · Clinical Science · doi:10.1042/cs20230140 · Cited by 83 · see citing works
Magkouta, S., Veroutis, D., Pousias, A., Papaspyropoulos, A., Pippa, N., Lougiakis, N., Kambas, K., Lagopati, N., Polyzou, A., Georgiou, M., et al. (2023) · Molecular Cell · doi:10.1016/j.molcel.2023.09.006 · Cited by 59 · see citing works
Self-citationHönzke, K., Obermayer, B., Mache, C., Fatykhova, D., Kessler, M., Dökel, S., Wyler, E., Baumgardt, M., Löwa, A., Hoffmann, K., et al. (2022) · European Respiratory Journal · doi:10.1183/13993003.02725-2021 · Cited by 60 · see citing works
Alveolar type 2 epithelial cell senescence and radiation-induced pulmonary fibrosis
Zhou, S., Zhu, J., Zhou, P., & Gu, Y. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.999600 · Cited by 57 · see citing works
Delval, L., Hantute-Ghesquier, A., Sencio, V., Flaman, J., Robil, C., Angulo, F. S., Lipskaia, L., Çobanoglu, Ö., Lacoste, A., Machelart, A., et al. (2023) · Nature Aging · doi:10.1038/s43587-023-00442-w · Cited by 55 · see citing works
Escape from senescence: molecular basis and therapeutic ramifications
Evangelou, K., Belogiannis, K., Papaspyropoulos, A., Petty, R., & Gorgoulis, V. G. (2023) · The Journal of Pathology · doi:10.1002/path.6164 · Cited by 55 · see citing works
Self-citationPantelis, P., Theocharous, G., Lаgopati, N., Veroutis, D., Thanos, D.-F., Lampoglou, G.-P., Pippa, Ν., Gatou, Μ.-A., Tremi, I., Papaspyropoulos, A., et al. (2023) · Antioxidants · doi:10.3390/antiox12010169 · Cited by 43 · see citing works
Self-citationRidgway, H. F., Moore, G. J., Mavromoustakos, T., Tsiodras, S., Ligielli, I., Kelaidonis, K., Chasapis, C. T., Gadanec, L. K., Zulli, A., Apostolopoulos, V., et al. (2022) · Computational and Structural Biotechnology Journal · doi:10.1016/j.csbj.2022.04.010 · Cited by 43 · see citing works
Self-citationCOVID-19 lung disease shares driver AT2 cytopathic features with Idiopathic pulmonary fibrosis
Sinha, S., Castillo, V., Espinoza, C. R., Tindle, C., Fonseca, A. G., Dan, J., Katkar, G. D., Das, S., Sahoo, D., & Ghosh, P. (2022) · EBioMedicine · doi:10.1016/j.ebiom.2022.104185 · Cited by 9 · see citing works
Neutrophil extracellular traps and long COVID
Shafqat, A., Omer, M. H., Albalkhi, I., Razzak, G. A., Abdulkader, H. S., Rab, S. A., Sabbah, B. N., AlKattan, K. M., & Yaqinuddin, A. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1254310 · Cited by 46 · see citing works
Veroutis, D., Argyropoulou, O. D., Goules, A. V., Kambas, K., Palamidas, D. A., Evangelou, K., Havaki, S., Polyzou, A., Valakos, D., Xingi, E., et al. (2023) · Annals of the Rheumatic Diseases · doi:10.1136/ard-2023-224467 · Cited by 39 · see citing works
Self-citationRidgway, H. F., Chasapis, C. T., Kelaidonis, K., Ligielli, I., Moore, G. J., Gadanec, L. K., Zulli, A., Apostolopoulos, V., Mavromoustakos, T., & Matsoukas, J. (2022) · Viruses · doi:10.3390/v14051029 · Cited by 35 · see citing works
Contribution of viral and bacterial infections to senescence and immunosenescence
Reyes, A., Ortiz, G., Duarte, L. F., Fernández, C., Hernández‐Armengol, R., Palacios, P. A., Prado, Y., Andrade, C. A., Rodríguez‐Guilarte, L., Kalergis, A. M., et al. (2023) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2023.1229098 · Cited by 36 · see citing works
Gorman, E. A., Rynne, J., Gardiner, H. J., Rostron, A., Bannard‐Smith, J., Bentley, A. M., Brealey, D. A., Campbell, C., Curley, G. F., Clarke, M. J., et al. (2023) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.202302-0297oc · Cited by 29 · see citing works
Treatment with the senolytics dasatinib/quercetin reduces SARS‐CoV ‐2‐related mortality in mice
Pastor‐Fernández, A., Bertos, A. R., Sierra‐Ramírez, A., del Moral‐Salmoral, J., Merino, J., de Ávila, A. I., Olagüe, C., Villares, R., González‐Aseguinolaza, G., Rodríguez, M. Á., et al. (2023) · Aging Cell · doi:10.1111/acel.13771 · Cited by 28 · see citing works
Wang, J., Zhou, X., Yu, P., Yao, J., Guo, P., Xu, Q., Zhao, Y., Wang, G., Li, Q., Zhu, X., et al. (2025) · Nature Aging · doi:10.1038/s43587-025-00886-2 · Cited by 28 · see citing works
Ozdemir, S. A., Faizan, M. I., Kaur, G., Shaikh, S. B., Islam, K. U., & Rahman, I. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26199687 · Cited by 26 · see citing works
SARS-CoV-2 and the DNA damage response
Grand, R. J. A. (2023) · Journal of General Virology · doi:10.1099/jgv.0.001918 · Cited by 23 · see citing works
A GATA2-CDC6 axis modulates androgen receptor blockade-induced senescence in prostate cancer
Mourkioti, I., Polyzou, A., Veroutis, D., Theocharous, G., Lаgopati, N., Gentile, E., Stravokefalou, V., Thanos, D.-F., Havaki, S., Kletsas, D., et al. (2023) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-023-02769-z · Cited by 20 · see citing works
Self-citationWang, X., Xu, Y., Zhang, S., Zhu, X., Zhang, H., & Liu, Y. (2023) · Acta Physiologica · doi:10.1111/apha.14059 · Cited by 19 · see citing works
Immunological and regenerative properties of lung stem cells
Hao, D., Liu, Y., Li, L., Stripp, B. R., & Chen, H. (2025) · Physiological Reviews · doi:10.1152/physrev.00056.2024 · Cited by 18 · see citing works
Self-citationGonzález‐Gualda, E., Reinius, M., Macías, D., Morsli, S., Ge, J., Olan, I., Martín, J. E., Ou, H., Hartono, M., Puerto-Camacho, M. P., et al. (2026) · Nature Aging · doi:10.1038/s43587-025-01054-2 · Cited by 18 · see citing works
Self-citationDetsika, M. G., Nikitopoulou, I., Veroutis, D., Vassiliou, A. G., Jahaj, E., Tsipilis, S., Athanassiou, N., Gakiopoulou, H., Gorgoulis, V. G., Dimopoulou, I., et al. (2022) · Antioxidants · doi:10.3390/antiox11071300 · Cited by 17 · see citing works
Self-citationCellular and molecular features of COVID-19 associated ARDS: therapeutic relevance
Scaramuzzo, G., Nucera, F., Asmundo, A., Messina, R., Mari, M., Montanaro, F., Johansen, M. D., Monaco, F. L., Fadda, G., Tuccari, G., et al. (2023) · Journal of Inflammation · doi:10.1186/s12950-023-00333-2 · Cited by 17 · see citing works
Ridgway, H. F., Moore, G. J., Gadanec, L. K., Zulli, A., Apostolopoulos, V., Hoffmann, W., Wegrzyn, K. E., Vassilaki, N., Mpekoulis, G., Zouridakis, M., et al. (2024) · Expert Opinion on Therapeutic Targets · doi:10.1080/14728222.2024.2362675 · Cited by 17 · see citing works
Self-citationDecoding T cell senescence in cancer: Is revisiting required?
Magkouta, S., Markaki, E., Evangelou, K., Petty, R., Verginis, P., & Gorgoulis, V. G. (2024) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2024.11.003 · Cited by 17 · see citing works
Self-citationKontoghiorghes, G. J. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23126735 · Cited by 16 · see citing works
Senotherapy for chronic lung disease
Barnes, P. J. (2025) · Pharmacological Reviews · doi:10.1016/j.pharmr.2025.100069 · Cited by 17 · see citing works
Self-citationde Gonzalo‐Calvo, D., Molinero, M., Benitez, I. D., Perez‐Pons, M., García‐Mateo, N., Ortega, A., Postigo, T., García‐Hidalgo, M. C., Belmonte, T., Rodríguez‐Muñoz, C., et al. (2023) · Respiratory Research · doi:10.1186/s12931-023-02462-x · Cited by 15 · see citing works
Shafqat, A., Masters, M. C., Tripathi, U., Tchkonia, T., Kirkland, J. L., & Hashmi, S. K. (2024) · Ageing Research Reviews · doi:10.1016/j.arr.2024.102400 · Cited by 15 · see citing works
Ito, K., Daly, L., & Coates, M. S. (2023) · Frontiers in Medicine · doi:10.3389/fmed.2023.1144050 · Cited by 14 · see citing works
Lee, J. D., Menasché, B. L., Mavrikaki, M., Uyemura, M. M., Hong, S. M., Kozlova, N. V., Wei, J., Alfajaro, M. M., Filler, R. B., Müller, A. M., et al. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.113478 · Cited by 15 · see citing works
Immune cell senescence drives responsiveness to immunotherapy in melanoma
Pantelis, P., Tremoulis, D. C., Evangelou, K., Bakouros, P., Magkouta, S., Ntintas, O. A., Veroutis, D., Theocharous, G., Kostopoulos, I. V., Thanos, D.-F., et al. (2025) · Molecular Cancer · doi:10.1186/s12943-025-02517-1 · Cited by 13 · see citing works
Self-citationSenotherapeutics: An emerging approach to the treatment of viral infectious diseases in the elderly
Li, Z., Tian, M., Wang, G., Cui, X., Ma, J., Liu, S., Shen, B., Liu, F., Wu, K., Xiao, X., et al. (2023) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2023.1098712 · Cited by 13 · see citing works
Radiotherapy for non-cancer diseases: benefits and long-term risks
Thariat, J., Little, M. P., Zablotska, L. B., Samson, P. P., O’Banion, M. K., Leuraud, K., Bergom, C. R., Girault, G., Azimzadeh, O., Bouffler, S. D., et al. (2024) · International Journal of Radiation Biology · doi:10.1080/09553002.2023.2295966 · Cited by 13 · see citing works
Blockade of endothelin receptors mitigates SARS-CoV-2-induced osteoarthritis
Au, M. T., Ni, J., Tang, K., Wang, W., Zhang, L., Wang, H., Zhao, F., Li, Z., Luo, P., Lau, L. C.-M., et al. (2024) · Nature Microbiology · doi:10.1038/s41564-024-01802-x · Cited by 11 · see citing works
Persistent alveolar type 2 dysfunction and lung structural derangement in post-acute COVID-19Preprint
Rendeiro, A. F., Ravichandran, H., Kim, J., Borczuk, A., Elemento, O., & Schwartz, R. E. (2022) · medRxiv · doi:10.1101/2022.11.28.22282811 · Cited by 9 · see citing works
Sfera, A., Osorio, C. P., Hazan, S., Kozlakidis, Z., Maldonado, J. C., del Campo, C. M. Z.-M., Anton, J. J., Rahman, L., Andronescu, C. V., & Nicolson, G. L. (2022) · Endocrines · doi:10.3390/endocrines3040058 · Cited by 9 · see citing works
Virus‐Induced Cellular Senescence Causes Pulmonary Sequelae Post‐Influenza Infection
Lipskaia, L., Delval, L., Sencio, V., Born, E., Heumel, S., Houssaini, A., Valentin, C., Raviola, S., Deruyter, L., Angulo, F. S., et al. (2025) · Aging Cell · doi:10.1111/acel.70140 · Cited by 10 · see citing works
Palamidas, D. A., Chatzis, L. G., Papadaki, M. E., Gissis, I., Kambas, K., Andreakos, E., Goules, A. V., & Tzioufas, A. G. (2024) · Cells · doi:10.3390/cells13050430 · Cited by 9 · see citing works
Self-citationShould We Expect an Increase in the Number of Cancer Cases in People with Long COVID?
Amiama-Roig, A., Pérez‐Martínez, L., Ledo, P. R., Verdugo‐Sivianes, E. M., & Blanco, J. R. (2023) · Microorganisms · doi:10.3390/microorganisms11030713 · Cited by 9 · see citing works
Kalisperati, P., Spanou, E., Pateras, I. S., Evangelou, K., Thymara, I., Korkolopoulou, P. A., Kotsinas, A., Vlachoyiannopoulos, P. G., Tzioufas, A. G., Kanellopoulos, C., et al. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25073888 · Cited by 8 · see citing works
Self-citationBulk and Single-Cell RNA Sequencing Elucidate the Etiology of Severe COVID-19
Huminiecki, Ł. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25063280 · Cited by 7 · see citing works
Imaging Techniques: Essential Tools for the Study of SARS-CoV-2 Infection
Deroubaix, A., & Kramvis, A. (2022) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2022.794264 · Cited by 7 · see citing works
Overview of molecular signatures of senescence and associated resources: pros and cons
Ntintas, O. A., Vagena, S., Pantelis, P., Theocharous, G., Petty, R., Evangelou, K., & Gorgoulis, V. G. (2026) · FEBS Open Bio · doi:10.1002/2211-5463.70134 · Cited by 6 · see citing works
Self-citationCellular senescence in acute human infectious disease: a systematic review
Miller, W., Wallace, S., Kamm, W., Reardon, E. E., Theis-Mahon, N. R., Yousefzadeh, M. J., Schmidt, E. L., Niedernhofer, L. J., & Puskarich, M. A. (2024) · Frontiers in Aging · doi:10.3389/fragi.2024.1500741 · Cited by 6 · see citing works
Respiratory viral infections in the elderly: From the perspective of the aging immune system
Zhang, X., Xu, J., Wang, Y., Li, H., Yu, J., Shang, L., Shang, L., Hou, B., Zhang, X., & Cao, B. (2023) · The Innovation Medicine · doi:10.59717/j.xinn-med.2023.100022 · Cited by 6 · see citing works
Heil, M. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1259879 · Cited by 6 · see citing works
Madruga, M. P., Grün, L. K., Santos, L. S. M. D., Friedrich, F., Antunes, D. B., Rocha, M. E. F., Silva, P. L., Dorneles, G. P., Teixeira, P. C., de Oliveira, T. F., et al. (2024) · Immunity & Ageing · doi:10.1186/s12979-024-00423-6 · Cited by 6 · see citing works
Epigenetics of SARS-CoV2 (COVID-19)
Rawat, S., Gilhotra, R. M., Singh, S. K., Bhat, A. A., Ojha, A., Dhaundhiyal, K., Dhramshaktu, I. S., & Gupta, G. (2023) · Springer eBooks · doi:10.1007/978-981-99-4780-5_12 · Cited by 5 · see citing works
Alveolar epithelial cells of lung fibrosis patients are susceptible to severe virus-induced injury
Read, J. M., Reid, A. T., Thomson, C., Plit, M., Mejia, R., Knight, D. A., Lizé, M., Kasmi, K. E., Grainge, C., Stahl, H. F., et al. (2024) · Clinical Science · doi:10.1042/cs20240220 · Cited by 5 · see citing works
Han, Y., Leng, D., Zhang, T., Ge, J., Fang, Y., Lu, T., Dong, X., Nair, M. S., de Silva, N., Han, Z., et al. (2025) · Advanced Science · doi:10.1002/advs.202503932 · Cited by 4 · see citing works
Loss of CFTR Reverses Senescence Hallmarks in SARS-CoV-2 Infected Bronchial Epithelial Cells
Merigo, F., Lagni, A., Boschi, F., Bernardi, P., Conti, A., Plebani, R., Romano, M., Sorio, C., Lotti, V., & Sbarbati, A. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25116185 · Cited by 4 · see citing works
Chentoufi, A. A., Khan, A. A., Srivastava, R., Karan, S., Lekbach, Y., Vahed, H., & BenMohamed, L. (2025) · Viruses · doi:10.3390/v17050606 · Cited by 4 · see citing works
Respiratory infections and cancer
Pollock, J. S., Hughes, C., & Chalmers, J. D. (2022) · European Respiratory Society eBooks · doi:10.1183/2312508x.10018121 · Cited by 4 · see citing works
Losartan and enalapril maleate differently influence SARS-CoV-2-infected vero cells
Majolo, J. H., Gonçalves, J. I. B., de Souza, R. P., González, L. C., Sperotto, N. D. D. M., Silveira, M. D., de Oliveira, S. D., Bizarro, C. V., Machado, P., Basso, L. A., et al. (2024) · Scientific Reports · doi:10.1038/s41598-024-76657-7 · Cited by 4 · see citing works
SARS-CoV-2-induced senescence as a potential therapeutic target
Denholm, M., Rintoul, R. C., & Muñoz‐Espín, D. (2022) · European Respiratory Journal · doi:10.1183/13993003.01101-2022 · Cited by 4 · see citing works
Distinct Molecular Mechanisms Characterizing Pathogenesis of SARS-CoV-2
Lee, S. J., Kim, Y., & Ahn, D. (2022) · Journal of Microbiology and Biotechnology · doi:10.4014/jmb.2206.06064 · Cited by 4 · see citing works
Unlocking Alveolar Regeneration: AT2 Stem Cells, Signaling Networks, and Therapeutic Frontiers
Zhang, Y., Zhou, Y., Wang, J., & Wang, Q. (2026) · Stem Cell Reviews and Reports · doi:10.1007/s12015-026-11086-9 · Cited by 2 · see citing works
Martínez-Orellana, P., Manzati, M., Pozzi, D., Xiao, Y., Clemente, A. D., Mearelli, M., Kalebić, C., Perrera, V., Ferrarini, D., Carletti, T., et al. (2025) · Journal of NeuroVirology · doi:10.1007/s13365-025-01283-6 · Cited by 3 · see citing works
Silva-Neto, P. V. D., de Carvalho, J. C. S., Toro, D. M., Oliveira, B., Cominal, J. G., Castro, R. C., Almeida, M., Prado, C. M., Arruda, E., Frantz, F. G., et al. (2025) · Viruses · doi:10.3390/v17050610 · Cited by 2 · see citing works
Putrescine functions as a metabolic checkpoint in replication stress-induced senescence
Vasilogiannakopoulou, T., Begou, O., Karali, C. S., Efthymiou, G., Roubelakis, M. G., Gorgoulis, V. G., Gkouskou, K. K., Gika, H., & Eliopoulos, A. G. (2025) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-025-05962-9 · Cited by 2 · see citing works
Self-citationLinks between COVID-19, long COVID, and neurodegeneration: The role of glycosphingolipids
Spedding, M., Aerts, J. M. F. G., Alexander, S. P. H., Woestelandt, A.-G. B., Chiricozzi, E., Henriques, A., Lledo, P., Loeffler, J., Perera, R. M., Platt, F. M., et al. (2026) · Pharmacological Reviews · doi:10.1016/j.pharmr.2026.100113 · Cited by 2 · see citing works
Molecular mechanisms and recent advances in cellular senescence
Hussain, A., Tatar, M., & Gong, R. (2026) · Cell & Bioscience · doi:10.1186/s13578-026-01596-x · Cited by 2 · see citing works
Gupta, S., Mohindra, R., Ramola, M., Kanta, P., Singla, M., Malhotra, M., Mehta, N., Goyal, A., & Singh, M. P. (2024) · Journal of Indian Society of Periodontology · doi:10.4103/jisp.jisp_508_23 · Cited by 2 · see citing works
Havaki, S., Evangelou, K., Paschalaki, K. E., Petty, R., Barnes, P. J., & Gorgoulis, V. G. (2022) · European Respiratory Journal · doi:10.1183/13993003.00754-2022 · Cited by 2 · see citing works
Self-citationGonzález‐Gualda, E., Macías, D., Morsli, S., Martín, J., Ou, H., Denholm, M., Olan, I., Hoffmann, R. J., Dane, M. A., Veroutis, D., et al. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.08.01.502019 · Cited by 2 · see citing works
Self-citationSenescence Signatures Predict Hospitalization Risk and Severity in COVID-19 Patients
Singh, T., Lynch, S. M., McLarnon, T., Cooper, E., McDaid, D., Guo, G., McLaughlin, J. K., McGilligan, V., Watterson, S., Shukla, P., et al. (2024) · doi:10.59368/agingbio.20240035 · Cited by 1 · see citing works
Acute lung injury in the context of aging: Pathogenetic mechanisms and therapeutic strategies
Huang, J., Feng, Z., Fu, J., He, J., Ren, Q., Yu, Y., Li, L., & Yu, R. (2026) · Ageing Research Reviews · doi:10.1016/j.arr.2026.103289 · Cited by 1 · see citing works
Ni, J., Au, M. T., Tang, K., Zhao, F., Wang, W., Zhang, L., Zhou, B., Zhu, L., Lau, L., Wang, X., et al. (2026) · Cell Reports · doi:10.1016/j.celrep.2026.117841 · Cited by 1 · see citing works
Lira, R., Luna-Rivero, C., Bolaños-Morales, F. V., Sandoval‐Gutiérrez, J. L., Moreno‐Verduzco, E. R., Maldonado-Rodríguez, A., Torres-Flores, J. M., Yocupicio‐Monroy, M., & Sevilla-Reyes, E. E. (2023) · Heliyon · doi:10.1016/j.heliyon.2023.e23485 · Cited by 1 · see citing works
Dittmayer, C., & Laue, M. M. (2022) · European Respiratory Journal · doi:10.1183/13993003.00266-2022 · Cited by 1 · see citing works
Ishibashi, N., Maebayashi, T., Aizawa, T., Sakaguchi, M., & Okada, M. (2022) · Thoracic Cancer · doi:10.1111/1759-7714.14677
Veroutis, D., Argyropoulou, O., Goules, A. V., Kambas, K., Palamidas, D., Evangelou, K., Havaki, S., Polyzou, A., Xingi, E., Karatza, E., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.05.19.541093
Self-citationGaggero, G., Drommi, M., Bedocchi, D., Barranco, R., & Ventura, F. (2023) · Minerva Forensic Medicine · doi:10.23736/s2784-8922.23.01843-5
Mourkioti, I., Polyzou, A., Veroutis, D., Theocharous, G., Lаgopati, N., Gentile, E., Stravokefalou, V., Thanos, D.-F., Havaki, S., Kletsas, D., et al. (2023) · Figshare · doi:10.6084/m9.figshare.23803087
Self-citationMourkioti, I., Polyzou, A., Veroutis, D., Theocharous, G., Lаgopati, N., Gentile, E., Stravokefalou, V., Thanos, D.-F., Havaki, S., Kletsas, D., et al. (2023) · Discovery Research Portal (University of Dundee) · doi:10.6084/m9.figshare.23803090
Self-citationMechanism and significance of cell senescence induced by viral infection
Chang, Y., Wu, X., Deng, L., Wang, S., & Mao, G. (2025) · Journal of Zhejiang University (Medical Sciences) · doi:10.3724/zdxbyxb-2024-0213
Love in the Time of COVID: Psychiatric Outcomes Related to Oxytocin and the “Endocrine Organ”
Sfera, A., Hazan, S., Anton, J., Ciuperca, I., Klein, C. A., & Thomas, K. G. (2025) · OBM Neurobiology · doi:10.21926/obm.neurobiol.2502287
Aldahhan, R. A., & El-Sheikh, A. A. (2025) · Translational Research in Anatomy · doi:10.1016/j.tria.2025.100411
Therapeutic effects and molecular mechanisms of isorhamnetin against pulmonary diseases
Jing, S., Meng, H., Dong, C., & Li, B. (2025) · Inflammopharmacology · doi:10.1007/s10787-025-02056-7
Mourkioti, I., Polyzou, A., Veroutis, D., Theocharous, G., Lagopati, N., Gentile, E., Stravokefalou, V., Thanos, D.-F., Havaki, S., Kletsas, D., et al. (2023) · Figshare · doi:10.6084/m9.figshare.23803084
Self-citationMadruga, M. P., Grün, L. K., Santos, L. S. M. D., Friedrich, F. O., Antunes, D. B., Rocha, M. E. F., Silva, P. L., Dorneles, G. P., Teixeira, P. C., Oliveira, T. F., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26690677
Madruga, M. P., Grün, L. K., Santos, L. S. M. D., Friedrich, F. O., Antunes, D. B., Rocha, M. E. F., Silva, P. L., Dorneles, G. P., Teixeira, P. C., Oliveira, T. F., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26690680
Madruga, M. P., Grün, L. K., Santos, L. S. M. D., Friedrich, F. O., Antunes, D. B., Rocha, M. E. F., Silva, P. L., Dorneles, G. P., Teixeira, P. C., Oliveira, T. F., et al. (2024) · Figshare · doi:10.6084/m9.figshare.25367524
de Gonzalo-Calvo, D., Molinero, M., Benitez, I. D., Perez‐Pons, M., García‐Mateo, N., Ortega, A., Postigo, T., García‐Hidalgo, M. C., Belmonte, T., Rodríguez‐Muñoz, C., et al. (2023) · Figshare · doi:10.6084/m9.figshare.23536167
de Gonzalo-Calvo, D., Molinero, M., Benitez, I. D., Perez‐Pons, M., García‐Mateo, N., Ortega, A., Postigo, T., García‐Hidalgo, M. C., Belmonte, T., Rodríguez‐Muñoz, C., et al. (2023) · Figshare · doi:10.6084/m9.figshare.23536164
Madruga, M. P., Grün, L. K., Santos, L. S. M. D., Friedrich, F. O., Antunes, D. B., Rocha, M. E. F., Silva, P. L., Dorneles, G. P., Teixeira, P. C., Oliveira, T. F., et al. (2024) · Figshare · doi:10.6084/m9.figshare.25367332
Madruga, M. P., Grün, L. K., Santos, L. S. M. D., Friedrich, F. O., Antunes, D. B., Rocha, M. E. F., Silva, P. L., Dorneles, G. P., Teixeira, P. C., Oliveira, T. F., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26690674
Cellular sensor DAP5 decodes Betacoronaviral NSP5 to drive virus-induced senescence
Lu, Y. P., Xiao, J., Wang, J., Meng, Z. S., Fan, G., Zheng, J. H., Yu, Z., Wang, X., & Li, L. (2026) · Frontiers in Immunology · doi:10.3389/fimmu.2026.1768183
Kyryk, V. M., Ustymenko, A., Tsupykov, O., Skarzhevskyi, O. A., & Parkhomenko, A. N. (2026) · BioMed Research International · doi:10.1155/bmri/5553698
- Authors
- Evangelou, K., Veroutis, D., Paschalaki, K., Foukas, P. G., Lagopati, N., Dimitriou, M., Papaspyropoulos, A., Konda, B., Hazapis, O., Polyzou, A., Havaki, S., Kotsinas, A., Kittas, C., Tzioufas, A. G., de Leval, L., Vassilakos, D., Tsiodras, S., Stripp, B. R., Papantonis, A., Blandino, G., Karakasiliotis, I., Barnes, P. J., & Gorgoulis, V. G.
- Affiliations
- National and Kapodistrian University of Athens (GR)
- Imperial College London (GB)
- Democritus University of Thrace (GR)
- Cedars-Sinai Medical Center (US)
- University of Cologne (DE)
- Instituto Nazionale Tumori Regina Elena (IT)
- Corresponding author
- Gorgoulis, Vassilis G.
- ORCID
- Evangelou, Konstantinos
- Veroutis, Dimitris
- Paschalaki, Koralia
- Foukas, Periklis G.
- Dimitriou, Marios
- Papaspyropoulos, Angelos
- Konda, Bindu
- Havaki, Sophia
- Kotsinas, Athanassios
- Kittas, Christos
- Tzioufas, Athanasios G.
- Tsiodras, Sotirios
- Stripp, Barry R.
- Papantonis, Argyris
- Blandino, Giovanni
- Barnes, Peter J.
- Gorgoulis, Vassilis G.
- Venue
- European Respiratory Journal
- Publisher
- European Respiratory Society (ERS)
- Published
- 2022-01-27
- Volume
- 60
- Issue
- 2
- Pages
- 2102951
- ISSN
- 0903-1936 (ISSN-L)
- 1399-3003
- PMC
- PMC8796696
- OpenAlex
- W4210558603
- Cited by
- 98
- References
- 66
- Citations by year
- 2026: 9 · 2025: 17 · 2024: 21 · 2023: 31 · 2022: 20
- FWCI
- 11.23
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- European Respiratory Journal (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Kölner Universitäts PublikationsServer (Universität zu Köln) (publishedVersion)
- SERVAL (Université de Lausanne) (publishedVersion, cc-by)
- IRIS (submittedVersion, cc-by)
- Funders
- National Public Investment Program of the Ministry of Development and Investment / General Secretariat for Research and Technology, in the framework of the Flagship Initiative to address SARS-CoV-2 (2020ΣΕ01300001)
- H2020 Marie Skłodowska-Curie Actions (722729 (SYNTRAIN))
- Welfare Foundation for Social & Cultural Sciences, Athens, Greece
- Hellenic Foundation for Research and Innovation (3782, 70/3/8916, 775, NKUA-SARG grant)
- H. Pappas
- Topics
- Health Sciences › Medicine › Infectious Diseases › COVID-19 Clinical Research Studies
- Health Sciences › Medicine › Physiology › Telomeres, Telomerase, and Senescence
- Health Sciences › Medicine › Infectious Diseases › SARS-CoV-2 and COVID-19 Research
- Keywords
- SARS-CoV-2, COVID-19 pandemic, cellular senescence, senescence-associated secretory phenotype, alveolar type II cells, APOBEC mutagenesis, viral mutagenesis, APOBEC3G, APOBEC3F, interleukin-6, IL-1β, interleukin-8, p16INK4a, ACE2, lung tissue, extrapulmonary dissemination, chronic inflammation
- MeSH terms
- COVID-19, SARS-CoV-2, Humans, Inflammation, Lung, Phenotype, Interleukin-6, Cytokines, Mutagenesis, Cellular Senescence
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
