Cellular senescence: the good, the bad and the unknown

The limited in vitro lifetime of human diploid cell strains

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DNA damage response as a candidate anti-cancer barrier in early human tumorigenesis

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Hallmarks of Cellular Senescence

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Senolytics improve physical function and increase lifespan in old age

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Cellular senescence in ageing: from mechanisms to therapeutic opportunities

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An Essential Role for Senescent Cells in Optimal Wound Healing through Secretion of PDGF-AA

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Clearance of senescent cells by ABT263 rejuvenates aged hematopoietic stem cells in mice

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Protocols to detect senescence-associated beta-galactosidase (SA-βgal) activity, a biomarker of senescent cells in culture and in vivo

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Mechanisms of Cellular Senescence: Cell Cycle Arrest and Senescence Associated Secretory Phenotype

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Senescence surveillance of pre-malignant hepatocytes limits liver cancer development

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Targeted Apoptosis of Senescent Cells Restores Tissue Homeostasis in Response to Chemotoxicity and Aging

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Programmed cell senescence during mammalian embryonic development

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Senolytics decrease senescent cells in humans: Preliminary report from a clinical trial of Dasatinib plus Quercetin in individuals with diabetic kidney disease

Hickson, L. J., Langhi Prata, L. G. P., Bobart, S. A., Evans, T. K., Giorgadze, N., Hashmi, S. K., Herrmann, S. M., Jensen, M. D., Jia, Q., Jordan, K. L., et al. (2019) · EBioMedicine · doi:10.1016/j.ebiom.2019.08.069 · Cited by 1,383 · 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

DNA damage triggers a prolonged p53-dependent G1 arrest and long-term induction of Cip1 in normal human fibroblasts.

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Senescence is a developmental mechanism that contributes to embryonic growth and patterning

Storer, M., Mas, A., Robert-Moreno, A., Pecoraro, M., Ortells, M. C., Di Giacomo, V., Yosef, R., Pilpel, N., Krizhanovsky, V., Sharpe, J., et al. (2013) · Cell · doi:10.1016/j.cell.2013.10.041 · Cited by 1,186 · see citing works

Identification of a novel senolytic agent, navitoclax, targeting the Bcl‐2 family of anti‐apoptotic factors

Zhu, Y., Tchkonia, T., Fuhrmann‐Stroissnigg, H., Dai, H. M., Ling, Y. Y., Stout, M. B., Pirtskhalava, T., Giorgadze, N., Johnson, K. O., Giles, C. B., et al. (2016) · Aging Cell · doi:10.1111/acel.12445 · Cited by 1,148 · see citing works

Senolytic CAR T cells reverse senescence-associated pathologies

Amor, C., Feucht, J., Leibold, J., Ho, Y.-J., Zhu, C., Alonso-Curbelo, D., Mansilla-Soto, J., Boyer, J. A., Li, X., Giavridis, T., et al. (2020) · Nature · doi:10.1038/s41586-020-2403-9 · Cited by 1,098 · see citing works

ROS, Cell Senescence, and Novel Molecular Mechanisms in Aging and Age‐Related Diseases

Davalli, P., Mitic, T., Caporali, A., Lauriola, A., & D’Arca, D. (2016) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2016/3565127 · Cited by 1,059 · see citing works

Lamin B1 loss is a senescence-associated biomarker

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Fisetin is a senotherapeutic that extends health and lifespan

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The matricellular protein CCN1 induces fibroblast senescence and restricts fibrosis in cutaneous wound healing

Jun, J.-I., & Lau, L. F. (2010) · Nature Cell Biology · doi:10.1038/ncb2070 · Cited by 998 · see citing works

JAK inhibition alleviates the cellular senescence-associated secretory phenotype and frailty in old age

Xu, M., Tchkonia, T., Ding, H., Ogrodnik, M., Lubbers, E. R., Pirtskhalava, T., White, T. A., Johnson, K. O., Stout, M. B., Mezera, V., et al. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1515386112 · Cited by 915 · see citing works

Mitochondria are required for pro-ageing features of the senescent phenotype

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New agents that target senescent cells: the flavone, fisetin, and the BCL-XL inhibitors, A1331852 and A1155463

Zhu, Y., Doornebal, E. J., Pirtskhalava, T., Giorgadze, N., Wentworth, M., Fuhrmann-Stroissnigg, H., Niedernhofer, L. J., Robbins, P. D., Tchkonia, T., & Kirkland, J. L. (2017) · Aging · doi:10.18632/aging.101202 · Cited by 757 · see citing works

Identification of HSP90 inhibitors as a novel class of senolytics

Fuhrmann-Stroissnigg, H., Ling, Y. Y., Zhao, J., McGowan, S. J., Zhu, Y., Brooks, R. W., Grassi, D., Gregg, S. Q., Stripay, J. L., Dorronsoro, A., et al. (2017) · Nature Communications · doi:10.1038/s41467-017-00314-z · Cited by 701 · see citing works

Metformin inhibits the senescence‐associated secretory phenotype by interfering with <scp>IKK</scp>/<scp>NF</scp>‐κ<scp>B</scp> activation

Moiseeva, O., Deschênes‐Simard, X., St‐Germain, E., Igelmann, S., Huot, G., Cadar, A. E., Bourdeau, V., Pollak, M. N., & Ferbeyre, G. (2013) · Aging Cell · doi:10.1111/acel.12075 · Cited by 654 · see citing works

The BCL-2 arbiters of apoptosis and their growing role as cancer targets

Adams, J. M., & Cory, S. (2018) · Cell Death &amp; Differentiation · doi:10.1038/cdd.2017.161 · Cited by 530 · see citing works

Chronic Oxidative Stress Compromises Telomere Integrity and Accelerates the Onset of Senescence in Human Endothelial Cells

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Senescent Human Fibroblasts Increase the Early Growth of Xenograft Tumors via Matrix Metalloproteinase Secretion

Liu, D., & Hornsby, P. J. (2007) · Cancer Research · doi:10.1158/0008-5472.can-06-3452 · Cited by 499 · see citing works

Stromal senescence establishes an immunosuppressive microenvironment that drives tumorigenesis

Ruhland, M. K., Loza, A. J., Capietto, A.-H., Luo, X., Knolhoff, B. L., Flanagan, K. C., Belt, B. A., Alspach, E., Leahy, K., Luo, J., et al. (2016) · Nature Communications · doi:10.1038/ncomms11762 · Cited by 496 · see citing works

Dose-dependent oncogene-induced senescence in vivo and its evasion during mammary tumorigenesis

Sarkisian, C. J., Keister, B. A., Stairs, D. B., Boxer, R. B., Moody, S. E., & Chodosh, L. A. (2007) · Nature Cell Biology · doi:10.1038/ncb1567 · Cited by 490 · see citing works

Markers of cellular senescence. Telomere shortening as a marker of cellular senescence

Bernadotte, A., Mikhelson, V. M., & Spivak, I. M. (2016) · Aging · doi:10.18632/aging.100871 · Cited by 466 · see citing works

p53-dependent chemokine production by senescent tumor cells supports NKG2D-dependent tumor elimination by natural killer cells

Iannello, A., Thompson, T. W., Ardolino, M., Lowe, S. W., & Raulet, D. H. (2013) · Journal of Experimental Medicine · doi:10.1084/jem.20130783 · Cited by 414 · see citing works

p16(Ink4a) and senescence-associated β-galactosidase can be induced in macrophages as part of a reversible response to physiological stimuli

Hall, B. M., Balan, V., Gleiberman, A. S., Strom, E., Krasnov, P., Virtuoso, L. P., Rydkina, E., Vujcic, S., Balan, K., Gitlin, I. I., et al. (2017) · Aging · doi:10.18632/aging.101268 · Cited by 407 · see citing works

Whole‐body senescent cell clearance alleviates age‐related brain inflammation and cognitive impairment in mice

Ogrodnik, M., Evans, S. A., Fielder, E., Victorelli, S., Kruger, P., Salmonowicz, H., Weigand, B. M., Patel, A. D., Pirtskhalava, T., Inman, C. L., et al. (2021) · Aging Cell · doi:10.1111/acel.13296 · Cited by 405 · see citing works

Biomarkers of cellular senescence and skin aging

Wang, A. S., & Dreesen, O. (2018) · Frontiers in Genetics · doi:10.3389/fgene.2018.00247 · Cited by 404 · see citing works

A novel type of cellular senescence that can be enhanced in mouse models and human tumor xenografts to suppress prostate tumorigenesis

Alimonti, A., Nardella, C., Chen, Z., Clohessy, J. G., Carracedo, A., Trotman, L. C., Cheng, K., Varmeh, S., Kozma, S. C., Thomas, G., et al. (2010) · Journal of Clinical Investigation · doi:10.1172/jci40535 · Cited by 374 · see citing works

Loss of Klotho Contributes to Kidney Injury by Derepression of Wnt/β-Catenin Signaling

Zhou, L., Li, Y., Zhou, D. F., Tan, R. J., & Liu, Y. (2013) · Journal of the American Society of Nephrology · doi:10.1681/asn.2012080865 · Cited by 374 · see citing works

Multiple facets of histone variant H2AX: a DNA double-strand-break marker with several biological functions

Turinetto, V., & Giachino, C. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv061 · Cited by 373 · see citing works

Is β-Galactosidase Staining a Marker of Senescence in Vitro and in Vivo?

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Rapamycin inhibits the secretory phenotype of senescent cells by a Nrf2-independent mechanism

Wang, R., Yu, Z., Sunchu, B., Shoaf, J., Dang, I., Zhao, S., Caples, K., Bradley, L., Beaver, L. M., Ho, E., et al. (2017) · Aging Cell · doi:10.1111/acel.12587 · Cited by 360 · see citing works

Downregulation of cytoplasmic DNases is implicated in cytoplasmic DNA accumulation and SASP in senescent cells

Takahashi, A., Loo, T. M., Okada, R., Kamachi, F., Watanabe, Y., Wakita, M., Watanabe, S., Kawamoto, S., Miyata, K., Barber, G. N., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-03555-8 · Cited by 350 · see citing works

The chemokine growth-regulated oncogene 1 (Gro-1) links RAS signaling to the senescence of stromal fibroblasts and ovarian tumorigenesis

Yang, G., Rosen, D. G., Zhang, Z., Bast, R. C., Mills, G. B., Colacino, J. A., Mercado-Uribe, I., & Liu, J. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0605752103 · Cited by 341 · see citing works

The flavonoid procyanidin C1 has senotherapeutic activity and increases lifespan in mice

Xu, Q., Fu, Q., Li, Z., Liu, H., Wang, Y., Lin, X., He, R., Zhang, X., Ju, Z., Campisi, J., et al. (2021) · Nature Metabolism · doi:10.1038/s42255-021-00491-8 · Cited by 341 · see citing works

Sarcopenia, obesity, and natural killer cell immune senescence in aging: Altered cytokine levels as a common mechanism

Lutz, C. T., & Quinn, L. S. (2012) · Aging · doi:10.18632/aging.100482 · Cited by 338 · see citing works

Senescence from G2 arrest, revisited

Gire, V., & Dulić, V. (2015) · Cell Cycle · doi:10.1080/15384101.2014.1000134 · Cited by 300 · see citing works

Unbiased analysis of senescence associated secretory phenotype (SASP) to identify common components following different genotoxic stresses

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

Mesenchymal stem cell-derived small extracellular vesicles mitigate oxidative stress-induced senescence in endothelial cells via regulation of miR-146a/Src

Xiao, X., Xu, M., Yu, H., Wang, L., Li, X., Rak, J. W., Wang, S., & Zhao, R. C. (2021) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-021-00765-3 · Cited by 294 · see citing works

Accelerated senescence: An emerging role in tumor cell response to chemotherapy and radiation

Gewirtz, D. A., Holt, S. E., & Elmore, L. W. (2008) · Biochemical Pharmacology · doi:10.1016/j.bcp.2008.06.024 · Cited by 281 · see citing works

Wnt9a Promotes Renal Fibrosis by Accelerating Cellular Senescence in Tubular Epithelial Cells

Luo, C., Zhou, S., Zhou, Z., Liu, Y., Yang, L., Liu, J., Zhang, Y., Li, H., Liu, Y., Hou, F. F., et al. (2018) · Journal of the American Society of Nephrology · doi:10.1681/asn.2017050574 · Cited by 277 · see citing works

Modelling the impact of decidual senescence on embryo implantation in human endometrial assembloids

Rawlings, T. M., Makwana, K., Taylor, D. M., Molè, M. A., Fishwick, K. J., Tryfonos, M., Odendaal, J., Hawkes, A., Zernicka‐Goetz, M., Hartshorne, G. M., et al. (2021) · eLife · doi:10.7554/elife.69603 · Cited by 274 · see citing works

Metformin as Anti-Aging Therapy: Is It for Everyone?

Soukas, A. A., Hao, H., & Wu, L. (2019) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2019.07.015 · Cited by 260 · see citing works

TAp63 induces senescence and suppresses tumorigenesis in vivo

Guo, X., Keyes, W. M., Papazoglu, C., Zuber, J. A., Li, W., Lowe, S. W., Vogel, H. S., & Mills, A. A. (2009) · Nature Cell Biology · doi:10.1038/ncb1988 · Cited by 251 · see citing works

Small extracellular vesicles and their miRNA cargo are anti-apoptotic members of the senescence-associated secretory phenotype

Terlecki‐Ζaniewicz, L., Lämmermann, I., Latreille, J., Bobbili, M. R., Pils, V., Schosserer, M., Weinmüllner, R., Dellago, H., Skalicky, S., Pum, D., et al. (2018) · Aging · doi:10.18632/aging.101452 · Cited by 246 · see citing works

Small molecule compounds that induce cellular senescence.

Petrova, N. V., Velichko, A. K., Razin, S. V., & Kantidze, O. L. (2016) · Aging Cell · doi:10.1111/acel.12518 · Cited by 240 · see citing works

Food as medicine: targeting the uraemic phenotype in chronic kidney disease

Mafra, D., Borges, N. A., Lindholm, B., Shiels, P. G., Evenepoel, P., & Stenvinkel, P. (2021) · Nature Reviews Nephrology · doi:10.1038/s41581-020-00345-8 · Cited by 238 · see citing works

PTBP1-Mediated Alternative Splicing Regulates the Inflammatory Secretome and the Pro-tumorigenic Effects of Senescent Cells

Georgilis, A., Klotz, S., Hanley, C. J., Herranz, N., Weirich, B., Morancho, B., Leote, A. C., D'Artista, L., Gallage, S., Seehawer, M., et al. (2018) · Cancer Cell · doi:10.1016/j.ccell.2018.06.007 · Cited by 237 · see citing works

Immunosenescence Study of T Cells: A Systematic Review

Rodríguez, I. J., Lalinde-Ruiz, N., León, M. L., Martínez-Enriquez, L. C., Velásquez, M. D. P. M., Aguirre, J. P. O., Bohórquez, O. M. R., Vargas, E. A. V., Hernández-Álvarez, E. D., & Parra-López, C. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2020.604591 · Cited by 224 · see citing works

Senolytic agent Quercetin ameliorates intervertebral disc degeneration via the Nrf2/NF-κB axis

Shao, Z., Wang, B., Shi, Y., Xie, C., Huang, C., Chen, B., Zhang, H.-S., Zeng, G., Liang, H., Wu, Y., et al. (2020) · Osteoarthritis and Cartilage · doi:10.1016/j.joca.2020.11.006 · Cited by 216 · see citing works

Cellular senescence inhibits renal regeneration after injury in mice, with senolytic treatment promoting repair

Mylonas, K. J., O'Sullivan, E. D., Humphries, D. C., Baird, D., Docherty, M.-H., Neely, S. A., Krimpenfort, P., Melk, A., Schmitt, R., Ferreira-González, S., et al. (2021) · Science Translational Medicine · doi:10.1126/scitranslmed.abb0203 · Cited by 216 · see citing works

Oxidative Stress Induces Premature Senescence by Stimulating Caveolin-1 Gene Transcription through p38 Mitogen-Activated Protein Kinase/Sp1–Mediated Activation of Two GC-Rich Promoter Elements

Dasari, A., Bartholomew, J. N., Volonté, D., & Galbiati, F. (2006) · Cancer Research · doi:10.1158/0008-5472.can-06-1236 · Cited by 215 · see citing works

MiR-146a as marker of senescence-associated pro-inflammatory status in cells involved in vascular remodelling

Olivieri, F., Lazzarini, R., Recchioni, R., Marcheselli, F., Rippo, M. R., Nuzzo, S., Albertini, M. C., Graciotti, L., Babini, L., Mariotti, S., et al. (2012) · AGE · doi:10.1007/s11357-012-9440-8 · Cited by 206 · see citing works

Cellular senescence in cancer: from mechanisms to detection

Ou, H., Hoffmann, R. J., González‐López, C., Doherty, G. J., Korkola, J. E., & Muñoz‐Espín, D. (2020) · Molecular Oncology · doi:10.1002/1878-0261.12807 · Cited by 198 · see citing works

Chromatin Remodeling Underlies the Senescence-Associated Secretory Phenotype of Tumor Stromal Fibroblasts That Supports Cancer Progression

Pazolli, E., Alspach, E., Milczarek, A., Prior, J., Piwnica-Worms, D., & Stewart, S. A. (2012) · Cancer Research · doi:10.1158/0008-5472.can-11-3386 · Cited by 192 · see citing works

KLRG1—more than a marker for T cell senescence

Henson, S. M., & Akbar, A. N. (2009) · AGE · doi:10.1007/s11357-009-9100-9 · Cited by 191 · see citing works

Senescence Reprogramming by TIMP1 Deficiency Promotes Prostate Cancer Metastasis

Guccini, I., Revandkar, A., D'Ambrosio, M., Colucci, M., Pasquini, E., Mosole, S., Troiani, M., Brina, D., Sheibani-Tezerji, R., Elia, A. R., et al. (2021) · Cancer Cell · doi:10.1016/j.ccell.2020.10.012 · Cited by 185 · see citing works

In senescence, age‐associated B cells secrete TNF α and inhibit survival of B‐cell precursors*

Ratliff, M., Alter, S., Frasca, D., Blomberg, B. B., & Riley, R. L. (2013) · Aging Cell · doi:10.1111/acel.12055 · Cited by 183 · see citing works

Senescence promotes in vivo reprogramming through p16<scp>^INK</scp>^4a and <scp>IL</scp>‐6

Mosteiro, L., Pantoja, C., de Martino, A., & Serrano, M. (2018) · Aging Cell · doi:10.1111/acel.12711 · Cited by 182 · see citing works

p38MAPK plays a crucial role in stromal-mediated tumorigenesis

Alspach, E., Flanagan, K. C., Luo, X., Ruhland, M. K., Huang, H., Pazolli, E., Donlin, M. J., Marsh, T., Piwnica-Worms, D., Monahan, J., et al. (2014) · Cancer Discovery · doi:10.1158/2159-8290.cd-13-0743 · Cited by 167 · see citing works

Suppression of the senescence-associated secretory phenotype (SASP) in human fibroblasts using small molecule inhibitors of p38 MAP kinase and MK2

Alimbetov, D., Davis, T., Brook, A. J. C., Cox, L. S., Faragher, R. G. A., Nurgozhin, T., Zhumadilov, Z., & Kipling, D. (2016) · Biogerontology · doi:10.1007/s10522-015-9610-z · Cited by 162 · see citing works

Human Obesity Induces Dysfunction and Early Senescence in Adipose Tissue-Derived Mesenchymal Stromal/Stem Cells

Conley, S. M., Hickson, L. J., Kellogg, T. A., McKenzie, T. J., Heimbach, J. K., Taner, T., Tang, H. J., Jordan, K. L., Saadiq, I. M., Woollard, J. R., et al. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.00197 · Cited by 160 · see citing works

Accelerated expression of senescence associated cell cycle inhibitor p16INK4A in kidneys with glomerular disease

Sis, B., Tasanarong, A., Khoshjou, F., Dadras, F., Solez, K., & Halloran, P. F. (2007) · Kidney International · doi:10.1038/sj.ki.5002039 · Cited by 159 · see citing works

PAI-1 Regulation of TGF-β1–induced Alveolar Type II Cell Senescence, SASP Secretion, and SASP-mediated Activation of Alveolar Macrophages

Rana, T., Jiang, C., Liu, G., Miyata, T., Antony, V. B., Thannickal, V. J., & Liu, R.-M. (2019) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2019-0071oc · Cited by 159 · see citing works

Quercetin alleviates kidney fibrosis by reducing renal tubular epithelial cell senescence through the SIRT1/PINK1/mitophagy axis

Liu, T., Yang, Q., Zhang, X., Qin, R., Shan, W., Zhang, H., & Chen, X. (2020) · Life Sciences · doi:10.1016/j.lfs.2020.118116 · Cited by 158 · see citing works

Similarities and interplay between senescent cells and macrophages

Behmoaras, J., & Gil, J. (2021) · Journal of Cell Biology · doi:10.1083/jcb.202010162 · Cited by 158 · see citing works

Irreparable telomeric DNA damage and persistent DDR signalling as a shared causative mechanism of cellular senescence and ageing

Rossiello, F., Herbig, U., Longhese, M. P., Fumagalli, M., & di Fagagna, F. D. (2014) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2014.06.009 · Cited by 156 · see citing works

Cell-cycle arrest and senescence in TP53-wild type renal carcinoma by enhancer RNA-P53-bound enhancer regions 2 (p53BER2) in a p53-dependent pathway

Xie, H., Ma, K., Zhang, K., Zhou, J., Li, L., Yang, W., Gong, Y., Cai, L., & Gong, K. (2021) · Cell Death &amp; Disease · doi:10.1038/s41419-020-03229-8 · Cited by 155 · see citing works

Uncoupling between Phenotypic Senescence and Cell Cycle Arrest in Aging p21-Deficient Fibroblasts

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A Study of Serum Immunoglobulin Levels in Elderly Persons That Provides New Insights into B Cell Immunosenescence

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