Deconstructing replicative senescence heterogeneity of human mesenchymal stem cells at single cell resolution reveals therapeutically targetable senescent cell sub-populations
Open accessAbstract
Cellular senescence is characterised by a state of permanent cell cycle arrest. It is accompanied by often variable release of the so-called senescence-associated secretory phenotype (SASP) factors, and occurs in response to a variety of triggers such as persistent DNA damage, telomere dysfunction, or oncogene activation. While cellular senescence is a recognised driver of organismal ageing, the extent of heterogeneity within and between different senescent cell populations remains largely unclear. Elucidating the drivers and extent of variability in cellular senescence states is important for discovering novel targeted seno-therapeutics and for overcoming cell expansion constraints in the cell therapy industry. Here we combine cell biological and single cell RNA-sequencing approaches to investigate heterogeneity of replicative senescence in human ESC-derived mesenchymal stem cells (esMSCs) as MSCs are the cell type of choice for the majority of current stem cell therapies and senescence of MSC is a recognized driver of organismal ageing. Our data identify three senescent subpopulations in the senescing esMSC population that differ in SASP, oncogene expression, and escape from senescence. Uncovering and defining this heterogeneity of senescence states in cultured human esMSCs allowed us to identify potential drug targets that may delay the emergence of senescent MSCs in vitro and perhaps in vivo in the future.
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Single-cell RNA-sequencing has revealed high levels of heterogeneity in cellular senescence in culture.
“Recently, single-cell RNA-sequencing (scRNA-Seq) has been used to analyze the diversity within senescent cell populations in culture revealing high levels of heterogeneity in cellular senescence [13–15].”
From Senescent cell heterogeneity and responses to senolytic treatment are related to cell cycle status during senescence induction (2025) · cites this paper as [14]
Significant heterogeneity was observed in different senescent cell clusters with different transcriptomic profiles, suggesting existence of senescent cell subpopulations with different cell states that likely exhibit distinct function and biology.
“Despite the carefully controlled uniform experimental conditions, significant heterogeneity was observed in different senescent cell clusters with different transcriptomic profiles, suggesting the existence of senescent cell subpopulations with different cell states that likely would exhibit distinct function and biology.”
From Senescent cell heterogeneity and responses to senolytic treatment are related to cell cycle status during senescence induction (2025) · cites this paper as [14]
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clusterProfiler: an R Package for Comparing Biological Themes Among Gene Clusters
Yu, G., Wang, L.-G., Han, Y., & He, Q.-Y. (2012) · OMICS: A Journal of Integrative Biology · doi:10.1089/omi.2011.0118 · Cited by 36,259 · see citing works
Molecular signatures database (MSigDB) 3.0
Liberzon, A., Subramanian, A., Pinchback, R., Thorvaldsdóttir, H., Tamayo, P., & Mesirov, J. P. (2011) · Bioinformatics · doi:10.1093/bioinformatics/btr260 · Cited by 7,111 · see citing works
An automated method for finding molecular complexes in large protein interaction networks
Bader, G. D., & Hogue, C. W. V. (2003) · BMC Bioinformatics · doi:10.1186/1471-2105-4-2 · Cited by 6,112 · see citing works
CellProfiler: image analysis software for identifying and quantifying cell phenotypes
Carpenter, A. E., Jones, T. R., Lamprecht, M. R., Clarke, C., Kang, I. H., Friman, O., Guertin, D. A., Chang, J. H., Lindquist, R. A., Moffat, J., et al. (2006) · Genome biology · doi:10.1186/gb-2006-7-10-r100 · Cited by 5,172 · see citing works
COSMIC: the Catalogue Of Somatic Mutations In Cancer
Tate, J. G., Bamford, S., Jubb, H. C., Sondka, Z., Beare, D. M., Bindal, N., Boutselakis, H., Cole, C. G., Creatore, C., Dawson, E., et al. (2019) · Nucleic Acids Research · doi:10.1093/nar/gky1015 · Cited by 4,867 · see citing works
Hafemeister, C., & Satija, R. (2019) · Genome Biology · doi:10.1186/s13059-019-1874-1 · Cited by 4,479 · see citing works
Slingshot: cell lineage and pseudotime inference for single-cell transcriptomics
Street, K., Risso, D., Fletcher, R. B., Das, D., Ngai, J., Yosef, N., Purdom, E., & Dudoit, S. (2018) · BMC Genomics · doi:10.1186/s12864-018-4772-0 · Cited by 3,159 · see citing works
mclust 5: Clustering, Classification and Density Estimation Using Gaussian Finite Mixture Models
Scrucca, L., Fop, M., Murphy, T. B., & Adrian, E. R. (2016) · The R Journal · doi:10.32614/rj-2016-021 · Cited by 2,914 · see citing works
A DNA damage checkpoint response in telomere-initiated senescence
Fagagna, F. D. D., Reaper, P. M., Clay-Farrace, L., Fiegler, H., Carr, P., von Zglinicki, T., Saretzki, G., Carter, N. P., & Jackson, S. P. (2003) · Nature · doi:10.1038/nature02118 · Cited by 2,855 · cited 1× · see citing works
“Quantification of the number of γH2AX stained cells and telomere damage induced foci (TIFs), both hallmarks of senescence [50], indicated that esMSCs accumulate DNA damage in the form of double strand breaks over time in culture, although this did not translate into significant changes in TIF levels (one-way ANOVA, p-…”
BackgroundCellular senescence in aging and age-related disease: from mechanisms to therapy
Childs, B. G., Durik, M., Baker, D. J., & van Deursen, J. M. (2015) · Nature Medicine · doi:10.1038/nm.4000 · Cited by 2,363 · see citing works
Stochastic mRNA Synthesis in Mammalian Cells
Raj, A., Peskin, C. S., Tranchina, D., Vargas, D. Y., & Tyagi, S. (2006) · PLoS Biology · doi:10.1371/journal.pbio.0040309 · Cited by 1,737 · see citing works
UHRF1 Plays a Role in Maintaining DNA Methylation in Mammalian Cells
Bostick, M. L., Kim, J. K., Estève, P., Clark, A. T., Pradhan, S., & Jacobsen, S. E. (2007) · Science · doi:10.1126/science.1147939 · Cited by 1,459 · see citing works
Inflammatory networks during cellular senescence: causes and consequences.
Freund, A., Orjalo, A. V., Desprez, P.-Y., & Campisi, J. (2010) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2010.03.003 · Cited by 1,354 · 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
Senescence and aging: Causes, consequences, and therapeutic avenues
McHugh, D., & Gil, J. (2018) · Journal of Cell Biology · doi:10.1083/jcb.201708092 · Cited by 1,233 · see citing works
Pathway Commons, a web resource for biological pathway data
Cerami, E. G., Gross, B. E., Demir, E., Rodchenkov, I., Babur, O., Anwar, N., Schultz, N., Bader, G. D., & Sander, C. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkq1039 · Cited by 1,101 · see citing works
Mitochondrial dysfunction accounts for the stochastic heterogeneity in telomere-dependent senescence
Passos, J. F., Saretzki, G., Ahmed, S., Nelson, G., Richter, T., Peters, H., Wappler, I., Birket, M. J., Harold, G., Schaeuble, K., et al. (2007) · PLoS Biology · doi:10.1371/journal.pbio.0050110 · Cited by 796 · see citing works
Senescence-associated inflammatory responses: aging and cancer perspectives
Lasry, A., & Ben-Neriah, Y. (2015) · Trends in Immunology · doi:10.1016/j.it.2015.02.009 · Cited by 408 · see citing works
A multidimensional systems biology analysis of cellular senescence in aging and disease
Avelar, R. A., Ortega, J. G., Tacutu, R., Tyler, E. J., Bennett, D., Binetti, P., Budovsky, A., Chatsirisupachai, K., Johnson, E., Murray, A., et al. (2020) · Genome Biology · doi:10.1186/s13059-020-01990-9 · Cited by 399 · see citing works
TGF-β Signaling in Cellular Senescence and Aging-Related Pathology
Tominaga, K., & Suzuki, H. I. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20205002 · Cited by 393 · see citing works
Transcriptome signature of cellular senescence
Casella, G., Munk, R., Kim, K. M., Piao, Y., De, S., Abdelmohsen, K., & Gorospe, M. (2019) · Nucleic Acids Research · doi:10.1093/nar/gkz555 · Cited by 359 · see citing works
Long-term In vitro Expansion Alters the Biology of Adult Mesenchymal Stem Cells
Izadpanah, R., Kaushal, D., Kriedt, C. L., Tsien, F., Patel, B. G., Dufour, J., & Bunnell, B. A. (2008) · Cancer Research · doi:10.1158/0008-5472.can-07-5272 · Cited by 352 · see citing works
Cytoplasmic intermediate filaments revealed as dynamic and multipurpose scaffolds
Coulombe, P. A., & Wong, P. (2004) · Nature Cell Biology · doi:10.1038/ncb0804-699 · Cited by 352 · see citing works
Single-cell entropy for accurate estimation of differentiation potency from a cell’s transcriptome
Teschendorff, A. E., & Enver, T. (2017) · Nature Communications · doi:10.1038/ncomms15599 · Cited by 346 · see citing works
Comparison of Gene Expression of Umbilical Cord Vein and Bone Marrow–Derived Mesenchymal Stem Cells
Panepucci, R. A., Siufi, J. L. C., Silva, W. A., Proto‐Siquiera, R., Neder, L., Orellana, M. D., Rocha, V., Covas, D. T., & Zago, M. A. (2004) · Stem Cells · doi:10.1634/stemcells.2004-0024 · Cited by 330 · see citing works
TSGene: a web resource for tumor suppressor genes
Zhao, M., Sun, J., & Zhao, Z. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks937 · Cited by 325 · see citing works
Watanabe, S., Kawamoto, S., Ohtani, N., & Hara, E. (2017) · Cancer Science · doi:10.1111/cas.13184 · Cited by 321 · cited 2× · see citing works
“Depending on the cell type and cellular context, senescent cells will secrete a variety of pro-inflammatory cytokines, chemokines, growth modulators, proteases and other soluble signalling factors, collectively termed senescence-associated secretory-phenotype (SASP) factors [3].”
BackgroundLiu, J., Ding, Y., Liu, Z., & Liang, X. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.00258 · Cited by 272 · see citing works
Heterogeneity of mesenchymal stromal cell preparations
Ho, A. D., Wagner, W., & Franke, W. W. (2008) · Cytotherapy · doi:10.1080/14653240802217011 · Cited by 265 · see citing works
Crystal structure of human CDK4 in complex with a D-type cyclin
Day, P. J., Cleasby, A., Tickle, I. J., O’Reilly, M., Coyle, J. E., Holding, F. P., McMenamin, R. L., Yon, J. R., Chopra, R., Christoph Lengauer, C., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0809645106 · Cited by 241 · see citing works
The Influence of Aging on the Regenerative Potential of Human Adipose Derived Mesenchymal Stem Cells
Marędziak, M., Marycz, K., Tomaszewski, K. A., Kornicka, K., & Henry, B. M. (2016) · Stem Cells International · doi:10.1155/2016/2152435 · Cited by 225 · see citing works
Age‐related impairment of mesenchymal progenitor cell function
Stolzing, A., & Scutt, A. M. (2006) · Aging Cell · doi:10.1111/j.1474-9726.2006.00213.x · Cited by 219 · see citing works
Tsai, M., Hwang, S., Chen, K.-D., Lee, Y.-S., Hsu, L., Chang, Y.-J., Wang, C., Peng, H.-H., Chang, Y., Chao, A.-S., et al. (2007) · Stem Cells · doi:10.1634/stemcells.2007-0023 · Cited by 209 · see citing works
Gardner, J., & Ghorpade, A. (2003) · Journal of Neuroscience Research · doi:10.1002/jnr.10835 · Cited by 199 · see citing works
Kornicka, K., Houston, J. M. I., & Marycz, K. (2018) · Stem Cell Reviews and Reports · doi:10.1007/s12015-018-9809-x · Cited by 184 · see citing works
Mesenchymal Stem Cell Senescence and Rejuvenation: Current Status and Challenges
Xueke, Z., Hong, Y., Zhang, H., & Li, X. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.00364 · Cited by 166 · see citing works
A continuum model of transcriptional bursting
Corrigan, A. M., Tunnacliffe, E., Cannon, D., & Chubb, J. R. (2016) · eLife · doi:10.7554/elife.13051 · Cited by 165 · see citing works
Roobrouck, V. D., Clavel, C., Jacobs, S. A., Ulloa‐Montoya, F., Crippa, S., Sohni, A., Roberts, S. J., Luyten, F. P., Gool, S. W. V., Sampaolesi, M., et al. (2011) · Stem Cells · doi:10.1002/stem.633 · Cited by 160 · see citing works
Mitochondria: Are they causal players in cellular senescence?
Correia-Melo, C., & Passos, J. F. (2015) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2015.05.017 · Cited by 160 · see citing works
Cell Senescence, DNA Damage, and Metabolism
Shmulevich, R., & Krizhanovsky, V. (2021) · Antioxidants & Redox Signaling · doi:10.1089/ars.2020.8043 · Cited by 157 · see citing works
Functional Interaction Network Construction and Analysis for Disease Discovery
Wu, G., & Haw, R. (2017) · Methods in molecular biology · doi:10.1007/978-1-4939-6783-4_11 · Cited by 156 · see citing works
Nishimura, K., Kumazawa, T., Kuroda, T., Katagiri, N., Tsuchiya, M., Goto, N., Furumai, R., Murayama, A., Yanagisawa, J., & Kimura, K. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.01.055 · Cited by 155 · see citing works
Inflammatory signaling and cellular senescence
Ren, J., Pan, J., Lu, Y.-P., Sun, P., & Han, J. (2008) · Cellular Signalling · doi:10.1016/j.cellsig.2008.10.011 · Cited by 149 · see citing works
Arima, Y., Hirota, T., Bronner, C., Mousli, M., Fujiwara, T., Niwa, S., Ishikawa, H. T., & Saya, H. (2004) · Genes to Cells · doi:10.1111/j.1356-9597.2004.00710.x · Cited by 142 · see citing works
Wang, J., Wen, S., Symmans, W. F., Pusztai, L., & Coombes, K. R. (2009) · Cancer Informatics · doi:10.4137/cin.s2846 · Cited by 142 · see citing works
Jansen, B. J. H., Gilissen, C., Roelofs, H., Schaap-Oziemlak, A., Veltman, J. A., Raymakers, R. A. P., Jansen, J. H., Kögler, G., Figdor, C. G., Torensma, R., et al. (2010) · Stem Cells and Development · doi:10.1089/scd.2009.0288 · Cited by 139 · see citing works
Guo, Y., Ayers, J. L., Carter, K. T., Wang, T., Maden, S. K., Edmond, D., Newcomb P, P., Li, C., Ulrich, C., Yu, M., et al. (2019) · Aging Cell · doi:10.1111/acel.13013 · Cited by 139 · see citing works
Mitochondrial peptides modulate mitochondrial function during cellular senescence
Kim, S., Mehta, H. H., Wan, J., Kuehnemann, C., Chen, J., Hu, J., Hoffman, A. R., & Cohen, P. (2018) · Aging · doi:10.18632/aging.101463 · Cited by 135 · see citing works
Aguado, J., Sola-Carvajal, A., Cancila, V., Revêchon, G., Ong, P. F., Jones-Weinert, C. W., Wallén Arzt, E., Lattanzi, G., Dreesen, O., Tripodo, C., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-13018-3 · Cited by 133 · see citing works
UHRF1 depletion causes a G2/M arrest, activation of DNA damage response and apoptosis
Tien, A. L., SenBanerjee, S., Kulkarni, A., Mudbhary, R., Goudreau, B. J., Ganesan, S., Sadler, K. C., & Ukomadu, C. (2011) · Biochemical Journal · doi:10.1042/bj20100840 · Cited by 117 · see citing works
Therapy-induced lipid uptake and remodeling underpin ferroptosis hypersensitivity in prostate cancer
Tousignant, K. D., Rockstroh, A., Poad, B. L. J., Talebi, A., Young, R. S. E., Fard, A. T., Gupta, R., Zang, T., Wang, C., Lehman, M., et al. (2020) · Cancer & Metabolism · doi:10.1186/s40170-020-00217-6 · Cited by 111 · see citing works
Self-citationLncRNAs Regulatory Networks in Cellular Senescence
Pavan Kumar, P. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20112615 · Cited by 107 · see citing works
Menßen, A., Häupl, T., Sittinger, M., Delorme, B., Charbord, P., & Ringe, J. (2011) · BMC Genomics · doi:10.1186/1471-2164-12-461 · Cited by 103 · see citing works
Secco, M., Moreira, Y. B., Zucconi, E., Vieira, N. M., Jazedje, T., Muotri, A. R., Okamoto, O. K., Verjovski‐Almeida, S., & Zatz, M. (2009) · Stem Cell Reviews and Reports · doi:10.1007/s12015-009-9098-5 · Cited by 93 · see citing works
Park, H., Kim, C.-H., Jeong, J.-H., Park, M., & Kim, K. S. (2016) · Oncotarget · doi:10.18632/oncotarget.7457 · Cited by 92 · see citing works
Senescence-Associated Metabolomic Phenotype in Primary and iPSC-Derived Mesenchymal Stromal Cells
Fernández‐Rebollo, E., Franzen, J., Goetzke, R., Hollmann, J., Ostrowska, A., Oliverio, M., Sieben, T., Rath, B., Kornfeld, J., & Wagner, W. (2020) · Stem Cell Reports · doi:10.1016/j.stemcr.2019.12.012 · Cited by 91 · see citing works
Regulation of senescence escape by TSP1 and CD47 following chemotherapy treatment
Guillon, J., Petit, C., Moreau, M., Toutain, B., Henry, C., Roché, H., Bonichon-Lamichhane, N., Salmon, J. P., Lemonnier, J., Campone, M., et al. (2019) · Cell Death & Disease · doi:10.1038/s41419-019-1406-7 · Cited by 90 · see citing works
Dasgupta, J., Kar, S., Liu, R., Joseph, J., Kalyanaraman, B., Remington, S. J., Chen, C., & Melendez, J. A. (2010) · Journal of Cellular Physiology · doi:10.1002/jcp.22193 · Cited by 90 · see citing works
Wnt Antagonist SFRP1 Functions as a Secreted Mediator of Senescence
Elzi, D. J., Song, M., Hakala, K. W., Weintraub, S. T., & Shiio, Y. (2012) · Molecular and Cellular Biology · doi:10.1128/mcb.06023-11 · Cited by 88 · see citing works
Aging of bone marrow– and umbilical cord–derived mesenchymal stromal cells during expansion
de Witte, S. F. H., Lambert, E. E., Merino, A. M., Strini, T., Douben, H., O’Flynn, L., Elliman, S. J., de Klein, A., Newsome, P. N., Baan, C. C., et al. (2017) · Cytotherapy · doi:10.1016/j.jcyt.2017.03.071 · Cited by 81 · see citing works
Zheng, D., Cho, Y., Lau, A. T. Y., Zhang, J., Ma, W.-Y., Bode, A. M., & Dong, Z. (2008) · Cancer Research · doi:10.1158/0008-5472.can-08-1137 · Cited by 68 · see citing works
Accelerated aging syndromes, are they relevant to normal human aging?
Dreesen, O., & Stewart, C. L. (2011) · Aging · doi:10.18632/aging.100383 · Cited by 66 · see citing works
Ren, J., Stroncek, D. F., Zhao, Y., Jin, P., Castiello, L., Civini, S., Wang, H., Feng, J., Tran, K., Kuznetsov, S. A., et al. (2013) · Stem Cell Research · doi:10.1016/j.scr.2013.07.005 · Cited by 63 · see citing works
Regenerative Potential of Mesenchymal Stromal Cells: Age‐Related Changes
Bruna, F., Contador, D., Conget, P. A., Erranz, B., Sossa, C., & Arango-Rodríguez, M. L. (2016) · Stem Cells International · doi:10.1155/2016/1461648 · Cited by 62 · see citing works
Temporal changes in the gene expression heterogeneity during brain development and aging
Işıldak, U., Somel, M., Thornton, J. M., & Dönertaş, H. M. (2020) · Scientific Reports · doi:10.1038/s41598-020-60998-0 · Cited by 53 · see citing works
Gene expression profile in mesenchymal stem cells derived from dental tissues and bone marrow
Kim, S., Kim, Y., Lee, S., Kim, K.-H., Lee, Y., Kim, W., & Lee, Y.-K. (2011) · Journal of Periodontal & Implant Science · doi:10.5051/jpis.2011.41.4.192 · Cited by 52 · see citing works
G0S2 Suppresses Oncogenic Transformation by Repressing a MYC-Regulated Transcriptional Program
Yim, C. Y., Sekula, D., Hever-Jardine, M. P., Liu, X., Warzecha, J. M., Tam, J. K. V., Freemantle, S. J., Dmitrovsky, E., & Spinella, M. J. (2016) · Cancer Research · doi:10.1158/0008-5472.can-15-2265 · Cited by 51 · see citing works
Tang, H., Geng, A., Zhang, T., Wang, C., Jiang, Y., & Mao, Z. (2019) · Protein & Cell · doi:10.1007/s13238-018-0591-y · Cited by 50 · see citing works
Reactive Oxygen Species Detection in Senescent Cells
Victorelli, S. G., & Passos, J. F. (2018) · Methods in molecular biology · doi:10.1007/978-1-4939-8931-7_3 · Cited by 50 · see citing works
Role of lncRNAs in Cellular Aging
Degirmenci, U., & Sun, L. (2016) · Frontiers in Endocrinology · doi:10.3389/fendo.2016.00151 · Cited by 49 · see citing works
A molecular classification of human mesenchymal stromal cells
Rohart, F., Mason, E. A., Matigian, N., Mosbergen, R., Korn, O., Chen, T., Butcher, S., Patel, J., Atkinson, K., Khosrotehrani, K., et al. (2016) · PeerJ · doi:10.7717/peerj.1845 · Cited by 47 · see citing works
Al‐Mudares, F., Reddick, S. J., Ren, J. L., Venkatesh, A., Zhao, C., & Lingappan, K. (2020) · Frontiers in Medicine · doi:10.3389/fmed.2020.594137 · Cited by 44 · see citing works
Ran-dependent TPX2 activation promotes acentrosomal microtubule nucleation in neurons
Chen, W., Chen, Y., Huang, Y., Hsieh, B.-Y., Chiu, H.-C., Kao, P.-Y., Chao, C.-Y., & Hwang, E. (2017) · Scientific Reports · doi:10.1038/srep42297 · Cited by 43 · see citing works
Hsu, C., Chen, Y., Su, H., Huang, G.-J., Shu, C., Wu, T. T.-L., & Pan, H. (2017) · Journal of Cancer · doi:10.7150/jca.17478 · Cited by 41 · see citing works
Su, Y., Xu, C., Sun, Z., Liang, Y., Li, G., Tong, T., & Chen, J. (2019) · Aging · doi:10.18632/aging.101760 · Cited by 36 · see citing works
Lafferty‐Whyte, K., Bilsland, A. E., Hoare, S. F., Burns, S., Zaffaroni, N., Cairney, C. J., & Keith, W. N. (2010) · Neoplasia · doi:10.1593/neo.10180 · Cited by 34 · see citing works
Identification of senescence-associated genes in human bone marrow mesenchymal stem cells
Ryu, E., Hong, S. H., Kang, J., Woo, J., Park, J., Lee, J., & Seo, J. (2008) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2008.04.111 · Cited by 34 · see citing works
Miranda, H. C., Herai, R. H., Thomé, C. H., Gomes, G. G., Panepucci, R. A., Orellana, M. D., Covas, D. T., Muotri, A. R., Greene, L. J., & Faça, V. M. (2012) · PROTEOMICS · doi:10.1002/pmic.201200111 · Cited by 34 · see citing works
Pivotal Role of the Chromatin Protein Nupr1 in Kras-Induced Senescence and Transformation
Grasso, D., Bintz, J., Lomberk, G. A., Molejon, M. I., Loncle, C., Garcia, M. N., López‐Millán, B., Urrutia, R. A., & Iovanna, J. (2015) · Scientific Reports · doi:10.1038/srep17549 · Cited by 34 · see citing works
Marques, J. C. M. T., Cornélio, D. A., Silbiger, V. N., Luchessi, A. D., de Souza, S., & de Medeiros, S. R. B. (2017) · Scientific Reports · doi:10.1038/s41598-017-16224-5 · Cited by 33 · see citing works
Yoo, H. J., Yoon, S. S., Park, S. Y., Lee, E. Y., Lee, E. B., Kim, J. H., & Song, Y. W. (2011) · Journal of Korean Medical Science · doi:10.3346/jkms.2011.26.7.851 · Cited by 31 · see citing works
The role of recombination in telomere length maintenance
Royle, N. J., Méndez-Bermúdez, A., Gravani, A., Novo, C. L., Foxon, J. L., Williams, J. P., Cotton, V. E., & Hidalgo, A. (2009) · Biochemical Society Transactions · doi:10.1042/bst0370589 · Cited by 26 · see citing works
Yoo, J. K., Choi, S., & Kim, J. K. (2013) · Experimental Gerontology · doi:10.1016/j.exger.2013.02.022 · Cited by 23 · see citing works
Survivin knockdown induces senescence in TTF‑1-expressing, KRAS-mutant lung adenocarcinomas
Sumi, T., Hirai, S., Yamaguchi, M., Tanaka, Y., Tada, M., Yamada, G., Hasegawa, T., Miyagi, Y., Niki, T., Watanabe, A., et al. (2018) · International Journal of Oncology · doi:10.3892/ijo.2018.4365 · Cited by 20 · see citing works
Kandhaya‐Pillai, R., Hou, D., Zhang, J., Yang, X., Compoginis, G., Mori, T., Tchkonia, T., Martin, G. M., Hisama, F. M., Kirkland, J. L., et al. (2021) · GeroScience · doi:10.1007/s11357-020-00318-6 · Cited by 19 · see citing works
Kadota, Y., Yanagawa, M., Nakaya, T., Kawakami, T., Sato, M., & Suzuki, S. S. (2012) · The Journal of Physiological Sciences · doi:10.1007/s12576-012-0217-8 · Cited by 16 · see citing works
Wang, T., Lee, Y., & Hwang, S.-M. (2011) · Methods in molecular biology · doi:10.1007/978-1-60761-999-4_29 · Cited by 16 · see citing works
Progeria accelerates adult stem cell aging
Brunauer, R., & Kennedy, B. K. (2015) · Science · doi:10.1126/science.aac4214 · Cited by 15 · see citing works
Lyu, G., Guan, Y., Zhang, C., Zong, L., Sun, L., Huang, X., Huang, L., Zhang, L., Tian, X., Zhou, Z., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-06710-3 · Cited by 13 · see citing works
Therapy-induced lipid uptake and remodeling underpin ferroptosis hypersensitivity in prostate cancerPreprint
Tousignant, K. D., Rockstroh, A., Poad, B. L. J., Talebi, A., Young, R. S. E., Fard, A. T., Gupta, R., Zang, T., Wang, C., Lehman, M., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.01.08.899609 · Cited by 10 · see citing works
Self-citationDharmaratne, M., Kulkarni, A. S., Fard, A. T., & Mar, J. C. (2022) · GigaScience · doi:10.1093/gigascience/giac126 · Cited by 8 · see citing works
Self-citationDerivation of human embryonic stem cell line Genea022
Dumevska, B., Bosman, A., McKernan, R., Schmidt, U., & Peura, T. T. (2016) · Stem Cell Research · doi:10.1016/j.scr.2016.02.011 · Cited by 6 · see citing works
Xue, N., Li, D., Wang, D.-K., Fu, J., & Ju, X. (2012) · PubMed · Cited by 6 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Neri, F., Zheng, S., Watson, M. A., Desprez, P. Y., Gerencser, A. A., Campisi, J., Wirtz, D., Wu, P.-H., & Schilling, B. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.06.22.600200 · Cited by 7 · see citing works
Neri, F., Zheng, S., Watson, M. A., Desprez, P.-Y., Gerencser, A. A., Campisi, J., Wirtz, D., Wu, P.-H., & Schilling, B. (2025) · Aging · doi:10.18632/aging.206299 · Cited by 6 · see citing works
Pietrogrande, G., Shaker, M. R., Stednitz, S. J., Soheilmoghaddam, M., Aguado, J., Morrison, S. D., Zambrano, S., Tabassum, T., Javed, I., Cooper-White, J. J., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.08.29.555421
Self-citation
- Authors
- Fard, A. T., Leeson, H., Perez, J. A., Pietrogrande, G., Power, D., Inclan, C. L. G., Zheng, H., Nelson, C., Soheilmoghaddam, F., Glass, N., Dharmaratne, M., Watson, E. R., Lu, J., Martin, S., Pickett, H., Cooper-White, J., Wolvetang, E., & Mar, J. C.
- Affiliations
- The University of Queensland (AU)
- The University of Sydney (AU)
- Corresponding author
- Wolvetang, Ernst
- Mar, Jessica C.
- ORCID
- Venue
- bioRxiv (Cold Spring Harbor Laboratory)
- Publisher
- openRxiv
- Published
- 2022-01-27
- OpenAlex
- W4225077734
- Cited by
- 3
- References
- 92
- Citations by year
- 2025: 1 · 2024: 1 · 2023: 1
- Type
- posted content
- Language
- en
- Open access
- green
- doi.org
- Locations
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
- Topics
- Health Sciences › Medicine › Physiology › Telomeres, Telomerase, and Senescence
- Health Sciences › Medicine › Genetics › Mesenchymal stem cell research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
- Keywords
- replicative senescence, mesenchymal stem cells, senescence-associated secretory phenotype, senescence escape, oncogene expression, aging
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 ›
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