Biology of premature ageing in survivors of cancer
Open accessAbstract
Over 30 million cancer survivors exist worldwide. Survivors have an earlier onset and higher incidence of chronic comorbidities, including endocrinopathies, cardiac dysfunction, osteoporosis, pulmonary fibrosis, secondary cancers and frailty than the general population; however, the fundamental basis of these changes at the cellular level is unknown. An electronic search was performed on Embase, Medline In-Process & Other Non-Indexed Citations, and the Cochrane Central Register of Controlled Trials. Original articles addressing the cellular biology of ageing and/or the mechanisms of cancer therapies similar to ageing mechanisms were included, and references of these articles were reviewed for further search. We found multiple biological process of ageing at the cellular level and their association with cancer therapies, as well as with clinical effects. The direct effects of various chemotherapies and radiation on telomere length, senescent cells, epigenetic modifications and microRNA were found. We review the effects of cancer therapies on recognised hallmarks of ageing. Long-term comorbidities seen in cancer survivors mimic the phenotypes of ageing and likely result from the interaction between therapeutic exposures and the underlying biology of ageing. Long-term follow-up of cancer survivors and research on prevention strategies should be pursued to increase the length and quality of life among the growing population of cancer survivors.
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Senotherapeutic drugs could potentially treat a variety of conditions primarily or secondarily mediated by senescent cell accumulation.
“The use of senotherapeutic drugs could potentially be effective in treating a variety of conditions primarily or secondarily mediated by accumulation of senescent cells [6, 33, 67–87].”
From Reducing Senescent Cell Burden in Aging and Disease (2020) · cites this paper as [67]
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1 retracted
Akiyama, M., Hideshima, T., Hayashi, T., Tai, Y., Mitsiades, C. S., Mitsiades, N., Chauhan, D., Richardson, P. G. G., Munshi, N. C., & Anderson, K. C. (2003) · PubMed · Cited by 212 · see citing works
RetractedCancer incidence and mortality worldwide: Sources, methods and major patterns in GLOBOCAN 2012
Ferlay, J., Soerjomataram, I., Dikshit, R., Eser, S., Mathers, C., Rebelo, M., Parkin, D. M., Forman, D., & Bray, F. (2015) · International Journal of Cancer · doi:10.1002/ijc.29210 · Cited by 28,766 · see citing works
López-Otín, C., Blasco, M. A., Partridge, L., Serrano, M., & Kroemer, G. (2013) · Cell · doi:10.1016/j.cell.2013.05.039 · Cited by 14,982 · see citing works
Jemal, A., Siegel, R., Ward, E., Hao, Y., Xu, J., & Thun, M. J. (2009) · CA: A Cancer Journal for Clinicians · doi:10.3322/caac.20006 · Cited by 9,709 · see citing works
The serial cultivation of human diploid cell strains
Hayflick, L., & Moorhead, P. S. (1961) · Experimental Cell Research · doi:10.1016/0014-4827(61)90192-6 · Cited by 8,508 · see citing works
A biomarker that identifies senescent human cells in culture and in aging skin in vivo.
Dimri, G. P., Lee, X., Basile, G., Acosta, M., Scott, G., Roskelley, C., Medrano, E. E., Linskens, M., Rubelj, I., & Pereira-Smith, O. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.20.9363 · Cited by 7,477 · see citing works
Specific Association of Human Telomerase Activity with Immortal Cells and Cancer
Kim, N. W., Piatyszek, M. A., Prowse, K. R., Harley, C. B., West, M. D., Ho, P. L. C., Coviello, G. M., Wright, W. E., Weinrich, S. L., & Shay, J. W. (1994) · Science · doi:10.1126/science.7605428 · Cited by 7,091 · cited 1× · see citing works
“47 48 Due to the numerous replicative cycles they undergo, cancer cells have shorter telomeres than cells in normal tissue.(49) They can survive high numbers of replications by maintaining telomeres with telomerase, an enzyme expressed in over 90% of immortal cell lines and cancers but undetectable in most normal tiss…”
BackgroundEpigenetic differences arise during the lifetime of monozygotic twins
Fraga, M. F., Ballestar, E., Paz, M. F., Ropero, S., Setien, F., Ballestar, M. L., Heine-Suñer, D., Cigudosa, J. C., Urioste, M., Benitez, J., et al. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0500398102 · Cited by 3,602 · see citing works
Chronic Health Conditions in Adult Survivors of Childhood Cancer
Oeffinger, K. C., Mertens, A. C., Sklar, C. A., Kawashima, T. I., Hudson, M. M., Meadows, A. T., Friedman, D. L., Marina, N. M., Hobbie, W. L., Kadan‐Lottick, N. S., et al. (2006) · New England Journal of Medicine · doi:10.1056/nejmsa060185 · Cited by 3,597 · see citing works
Prevalence of frailty in community-dwelling older persons: a systematic review
Collard, R. M., Boter, H., Schoevers, R. A., & Oude Voshaar, R. C. (2012) · Journal of the American Geriatrics Society · doi:10.1111/j.1532-5415.2012.04054.x · Cited by 3,073 · see citing works
From Cancer Patient to Cancer Survivor: Lost in Transition
(2005) · PsycEXTRA Dataset · doi:10.1037/e720092007-001 · Cited by 2,364 · see citing works
Farber, S., Diamond, L. K., Mercer, R. D., Sylvester, R. F., & Wolff, J. A. (1948) · New England Journal of Medicine · doi:10.1056/nejm194806032382301 · Cited by 1,806 · see citing works
Kirkwood, T. B. L., & Austad, S. N. (2000) · Nature · doi:10.1038/35041682 · Cited by 1,774 · see citing works
Cellular senescence and the senescent secretory phenotype: therapeutic opportunities
Tchkonia, T., Zhu, Y., van Deursen, J., Campisi, J., & Kirkland, J. L. (2013) · Journal of Clinical Investigation · doi:10.1172/jci64098 · Cited by 1,774 · see citing works
Self-citationFabbri, M., Garzon, R., Cimmino, A., Liu, Z., Zanesi, N. A. O., Callegari, E., Liu, S., Alder, H., Costinean, S., Fernandez-Cymering, C., et al. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0707628104 · Cited by 1,676 · see citing works
Walston, J., Hadley, E. C., Ferrucci, L., Guralnik, J. M., Newman, A. B., Studenski, S. A., Ershler, W. B., Harris, T., & Fried, L. P. (2006) · Journal of the American Geriatrics Society · doi:10.1111/j.1532-5415.2006.00745.x · Cited by 1,605 · see citing works
Schröder, F. H., Hugosson, J., Roobol, M. J., Tammela, T. L. J., Zappa, M., Nelen, V., KWIATKOWSKI, M. K., Lujan, M., Määttänen, L., Lilja, H. G., et al. (2014) · The Lancet · doi:10.1016/s0140-6736(14)60525-0 · Cited by 1,566 · see citing works
Inhibition of telomerase limits the growth of human cancer cells
Hahn, W. C., Stewart, S. A., Brooks, M. W., York, S. G., Eaton, E. N., Kurachi, A. L., Beijersbergen, R. L., Knoll, J. H. M., Meyerson, M. M., & Weinberg, R. A. (1999) · Nature Medicine · doi:10.1038/13495 · Cited by 1,032 · see citing works
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
Self-citationStructure and variability of human chromosome ends.
de Lange, T., Shiue, L., Myers, R. M., Cox, D. R., Naylor, S. L., Killery, A. M., & Varmus, H. E. (1990) · Molecular and Cellular Biology · doi:10.1128/mcb.10.2.518 · Cited by 848 · see citing works
Buta, B. J., Walston, J. D., Godino, J., Park, M., Kalyani, R. R., Xue, Q., Bandeen‐Roche, K., & Varadhan, R. (2015) · Ageing Research Reviews · doi:10.1016/j.arr.2015.12.003 · Cited by 847 · see citing works
Hudson, M. M. (2003) · JAMA · doi:10.1001/jama.290.12.1583 · Cited by 809 · see citing works
Armstrong, G. T., Liu, Q., Yasui, Y., Neglia, J. P., Leisenring, W., Robison, L. L., & Mertens, A. C. (2009) · Journal of Clinical Oncology · doi:10.1200/jco.2008.21.1425 · Cited by 776 · see citing works
Self-citationFrailty, fitness and late-life mortality in relation to chronological and biological age
Mitnitski, A. B., Graham, J., Mogilner, A. J., & Rockwood, K. J. (2002) · BMC Geriatrics · doi:10.1186/1471-2318-2-1 · Cited by 711 · see citing works
The Identification of Frailty: A Systematic Literature Review
Sternberg, S. A., Schwartz, A. W., Karunananthan, S., Bergman, H., & Mark Clarfield, A. (2011) · Journal of the American Geriatrics Society · doi:10.1111/j.1532-5415.2011.03597.x · Cited by 703 · see citing works
Subsequent Neoplasms in 5-Year Survivors of Childhood Cancer: The Childhood Cancer Survivor Study
Friedman, D. L., Whitton, J. A., Leisenring, W. M., Mertens, A. C., Hammond, S., Stovall, M., Donaldson, S. S., Meadows, A. T., Robison, L. L., & Neglia, J. P. (2010) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/djq238 · Cited by 700 · see citing works
(2002) · PubMed · Cited by 640 · see citing works
Conditioning regimens for hematopoietic cell transplantation: one size does not fit all
Gyurkocza, B., & Sandmaier, B. M. (2014) · Blood · doi:10.1182/blood-2014-02-514778 · Cited by 616 · see citing works
(2003) · PubMed · Cited by 608 · see citing works
Targeting senescent cells enhances adipogenesis and metabolic function in old age
Xu, M., Palmer, A. K., Ding, H., Weivoda, M. M., Pirtskhalava, T., White, T. A., Sepe, A., Johnson, K. O., Stout, M. B., Giorgadze, N., et al. (2015) · eLife · doi:10.7554/elife.12997 · Cited by 604 · see citing works
Self-citationArmstrong, G. T., Kawashima, T. I., Leisenring, W. M., Stratton, K. L., Stovall, M., Hudson, M. M., Sklar, C. A., Robison, L. L., & Oeffinger, K. C. (2014) · Journal of Clinical Oncology · doi:10.1200/jco.2013.51.1055 · Cited by 584 · see citing works
Self-citationReduction in Late Mortality among 5-Year Survivors of Childhood Cancer
Armstrong, G. T., Chen, Y., Yasui, Y., Leisenring, W. M., Gibson, T. M., Mertens, A. C., Stovall, M., Oeffinger, K. C., Bhatia, S., Krull, K. R., et al. (2016) · New England Journal of Medicine · doi:10.1056/nejmoa1510795 · Cited by 570 · see citing works
Self-citationSurvivors of Childhood Cancer in the United States: Prevalence and Burden of Morbidity
Phillips, S. M., Padgett, L. S., Leisenring, W. M., Stratton, K. K., Bishop, K., Krull, K. R., Alfano, C. M., Gibson, T. M., de Moor, J. S., Blanch‐Hartigan, D., et al. (2015) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.epi-14-1418 · Cited by 558 · see citing works
Self-citationProlonged bed rest decreases skeletal muscle and whole body protein synthesis
Ferrando, A. A., Lane, H. W., Stuart, C. A., Davis-Street, J. E., & Wolfe, R. R. (1996) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1996.270.4.e627 · Cited by 498 · see citing works
The association of telomere length and cancer: a meta-analysis
Wentzensen, I. M., Mirabello, L., Pfeiffer, R. M., & Savage, S. A. (2011) · Cancer Epidemiology, Biomarkers & Prevention · doi:10.1158/1055-9965.epi-11-0005 · Cited by 458 · see citing works
Danazol Treatment for Telomere Diseases
Townsley, D. M., Dumitriu, B., Liu, D., Biancotto, A., Weinstein, B., Chen, C., Hardy, N., Mihalek, A. D., Lingala, S., Kim, Y. J., et al. (2016) · New England Journal of Medicine · doi:10.1056/nejmoa1515319 · Cited by 415 · see citing works
Wang, M. L., Blum, K. A., Martin, P., Goy, A. H., Auer, R. L., Kahl, B. S., Jurczak, W. J., Advani, R. H., Romaguera, J. E., Williams, M. E., et al. (2015) · Blood · doi:10.1182/blood-2015-03-635326 · Cited by 412 · see citing works
The Role of DNA Methylation in Aging, Rejuvenation, and Age-Related Disease
Johnson, A. A., Akman, K., Calimport, S., Wuttke, D., Stolzing, A., & de Magalhães, J. P. (2012) · Rejuvenation Research · doi:10.1089/rej.2012.1324 · Cited by 386 · see citing works
Calado, R. T., Yewdell, W. T., Wilkerson, K. L., Regal, J. A., Kajigaya, S., Stratakis, C. A., & Young, N. S. (2009) · Blood · doi:10.1182/blood-2008-09-178871 · Cited by 362 · see citing works
A Comprehensive Review of the Adverse Effects of Systemic Corticosteroids
Poetker, D. M., & Reh, D. D. (2010) · Otolaryngologic Clinics of North America · doi:10.1016/j.otc.2010.04.003 · Cited by 340 · see citing works
Long-term Risks of Subsequent Primary Neoplasms Among Survivors of Childhood Cancer
Reulen, R. C. (2011) · JAMA · doi:10.1001/jama.2011.747 · Cited by 334 · see citing works
Ness, K. K., Krull, K. R., Jones, K., Mulrooney, D. A., Armstrong, G. T., Green, D. M., Chemaitilly, W., Smith, W. A., Wilson, C. L., Sklar, C. A., et al. (2013) · Journal of Clinical Oncology · doi:10.1200/jco.2013.52.2268 · Cited by 334 · see citing works
Self-citationNovel anticancer therapeutics targeting telomerase
Ruden, M., & Puri, N. (2012) · Cancer Treatment Reviews · doi:10.1016/j.ctrv.2012.06.007 · Cited by 309 · see citing works
Short Telomeres, even in the Presence of Telomerase, Limit Tissue Renewal Capacity
Hao, L.-Y., Armanios, M., Strong, M. A., Karim, B., Feldser, D. M., Huso, D., & Greider, C. W. (2005) · Cell · doi:10.1016/j.cell.2005.11.020 · Cited by 302 · see citing works
Leukemias and myelodysplastic syndromes secondary to drug, radiation, and environmental exposure.
Levine, E. G., & Bloomfield, C. D. (1992) · PubMed · Cited by 301 · see citing works
Cellular senescence and the senescent secretory phenotype in age-related chronic diseases
Zhu, Y., Armstrong, J. L., Tchkonia, T., & Kirkland, J. L. (2014) · Current Opinion in Clinical Nutrition and Metabolic Care · doi:10.1097/mco.0000000000000065 · Cited by 273 · see citing works
Self-citationPersistent γH2AX: A promising molecular marker of DNA damage and aging
Siddiqui, M. S., François, M., Fenech, M. F., & Leifert, W. R. (2015) · Mutation Research/Reviews in Mutation Research · doi:10.1016/j.mrrev.2015.07.001 · Cited by 266 · see citing works
Syrjala, K. L., Langer, S. L., Abrams, J. R., Storer, B. E., & Martin, P. J. (2005) · Journal of Clinical Oncology · doi:10.1200/jco.2005.12.674 · Cited by 259 · see citing works
Structure and Variability of Human Chromosome Ends
de Lange, T., Shiue, L., Myers, R., et al. (1990) · Molecular and Cellular Biology · doi:10.1128/mcb.10.2.518-527.1990 · Cited by 257 · see citing works
Cross‐Talk between Aging and Cancer: The Epigenetic Language
FRAGA, M. F., AGRELO, R., & ESTELLER, M. (2007) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1395.005 · Cited by 251 · see citing works
Muscle dysfunction in cancer patients
Christensen, J. F., Jones, L. W., Andersen, J. L., Daugaard, G., Rørth, M. R., & Højman, P. (2014) · Annals of Oncology · doi:10.1093/annonc/mdt551 · Cited by 244 · see citing works
Accelerated telomere shortening in young recipients of allogeneic bone-marrow transplants
Wynn, R. F., Cross, M. A., Hatton, C. E., Will, A., Lashford, L. S., Dexter, T. M., & Testa, N. G. (1998) · The Lancet · doi:10.1016/s0140-6736(97)08256-1 · Cited by 228 · see citing works
Alterations in microRNA expression in stress-induced cellular senescence
Li, G., Luna, C., Qiu, J., Epstein, D. L., & González, P. (2009) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2009.09.002 · Cited by 220 · see citing works
Telomere length behaves as biomarker of somatic redundancy rather than biological age
Boonekamp, J. J., Simons, M. J. P., Hemerik, L., & Verhulst, S. (2013) · Aging Cell · doi:10.1111/acel.12050 · Cited by 209 · see citing works
Armenian, S. H., Sun, C., Kawashima, T. I., Arora, M., Leisenring, W. M., Sklar, C. A., Baker, K. S., Francisco, L., Teh, J. B., Mills, G., et al. (2011) · Blood · doi:10.1182/blood-2011-01-331835 · Cited by 205 · see citing works
Self-citationLifelong Cancer Incidence in 47 697 Patients Treated for Childhood Cancer in the Nordic Countries
Olsen, J. H., Möller, T., Anderson, H., et al. (2009) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/djp104 · Cited by 196 · see citing works
Mohty, B., & Mohty, M. (2011) · Blood Cancer Journal · doi:10.1038/bcj.2011.14 · Cited by 195 · see citing works
Bhakta, N. H., Liu, Q., Yeo, F., et al. (2016) · The Lancet Oncology · doi:10.1016/s1470-2045(16)30215-7 · Cited by 180 · see citing works
The Clinical Pharmacology of Antineoplastic Agents
Chabner, B. A., Myers, C. E., Coleman, C. N., & Johns, D. G. (1975) · New England Journal of Medicine · doi:10.1056/nejm197505292922206 · Cited by 175 · see citing works
Clinical strategies and animal models for developing senolytic agents
Kirkland, J. L., & Tchkonia, T. (2015) · Experimental Gerontology · doi:10.1016/j.exger.2014.10.012 · Cited by 168 · see citing works
Self-citationDoxorubicin induces senescence and impairs function of human cardiac progenitor cells
Piegari, E., Angelis, A. D., Cappetta, D., Russo, R., Esposito, G., Costantino, S., Graiani, G., Frati, C., Prezioso, L., Berrino, L., et al. (2013) · Basic Research in Cardiology · doi:10.1007/s00395-013-0334-4 · Cited by 166 · see citing works
Cellular Senescence and the Biology of Aging, Disease, and Frailty
LeBrasseur, N. K., Tchkonia, T., & Kirkland, J. L. (2015) · Nestlé Nutrition Institute Workshop Series · doi:10.1159/000382054 · Cited by 147 · see citing works
Self-citationPossible acceleration of aging by adjuvant chemotherapy: A cause of early onset frailty?
MacCormick, R. (2006) · Medical Hypotheses · doi:10.1016/j.mehy.2006.01.045 · Cited by 146 · see citing works
Is telomerase a viable target in cancer?
Buseman, C. M., Wright, W. E., & Shay, J. W. (2011) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/j.mrfmmm.2011.07.006 · Cited by 145 · see citing works
The roles of telomeres and telomerase in cell life span
Counter, C. M. (1996) · Mutation Research/Reviews in Genetic Toxicology · doi:10.1016/s0165-1110(96)90006-8 · Cited by 140 · see citing works
The Clinical Pharmacology of Antineoplastic Agents
Chabner, B. A., Myers, C. E., Coleman, C. N., & Johns, D. G. (1975) · New England Journal of Medicine · doi:10.1056/nejm197505222922107 · Cited by 123 · see citing works
Sun, C., Kersey, J. H., Francisco, L., Armenian, S. H., Baker, K. S., Weisdorf, D. J., Forman, S. J., & Bhatia, R. (2013) · Transplantation and Cellular Therapy · doi:10.1016/j.bbmt.2013.04.002 · Cited by 121 · see citing works
Self-citationDrug-induced DNA hypermethylation and drug resistance in human tumors.
Nyce, J. W. (1989) · PubMed · Cited by 119 · see citing works
Physiologic Frailty in Nonelderly Hematopoietic Cell Transplantation Patients
Arora, M., Sun, C., Ness, K. K., Teh, J. B., Wu, J., Francisco, L., Armenian, S. H., Schad, A., Namdar, G., Bosworth, A., et al. (2016) · JAMA Oncology · doi:10.1001/jamaoncol.2016.0855 · Cited by 115 · see citing works
Self-citationAge-Dependent Changes in Health Status in the Childhood Cancer Survivor Cohort
Hudson, M. M., Oeffinger, K. C., Jones, K., Brinkman, T. M., Krull, K. R., Mulrooney, D. A., Mertens, A., Castellino, S. M., Casillas, J., Gurney, J. G., et al. (2015) · Journal of Clinical Oncology · doi:10.1200/jco.2014.57.4863 · Cited by 113 · see citing works
Self-citationHashmi, S. K., Carpenter, P. A., Khera, N., Tichelli, A., & Savani, B. N. (2014) · Transplantation and Cellular Therapy · doi:10.1016/j.bbmt.2014.06.035 · Cited by 97 · see citing works
Self-citationJustice, J., Miller, J. D., Newman, J. C., Hashmi, S. K., Halter, J., Austad, S. N., Barzilai, N., & Kirkland, J. L. (2016) · The Journals of Gerontology Series A: Biological Sciences and Medical Sciences · doi:10.1093/gerona/glw126 · Cited by 96 · see citing works
Self-citationArmstrong, G. T., Reddick, W. E., Petersen, R. C., et al. (2013) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/djt089 · Cited by 95 · see citing works
Self-citationMicroRNA Regulation of Ionizing Radiation-Induced Premature Senescence
Wang, Y., Scheiber, M. N., Neumann, C. A., Călin, G. A., & Zhou, D. (2010) · International Journal of Radiation Oncology*Biology*Physics · doi:10.1016/j.ijrobp.2010.09.048 · Cited by 89 · see citing works
Bone Marrow-Derived Cells: The Influence of Aging and Cellular Senescence
Beausejour, C. M. (2007) · Springer eBooks · doi:10.1007/978-3-540-68976-8_4 · Cited by 79 · see citing works
Telomere length shortening in non-Hodgkin's lymphoma patients undergoing chemotherapy
Lee, J.-J., Nam, C.-E., Cho, S.-H., Park, K.-S., Chung, I.-J., & Kim, H.-J. (2003) · Annals of Hematology · doi:10.1007/s00277-003-0691-4 · Cited by 69 · see citing works
Mertens, A. C., Yong, J., Dietz, A. C., et al. (2014) · Cancer · doi:10.1002/cncr.29170 · Cited by 65 · see citing works
Proliferative capacity of erythropoietic stem cell lines and aging: An overview
Harrison, D. E. (1979) · Mechanisms of Ageing and Development · doi:10.1016/0047-6374(79)90082-4 · Cited by 55 · see citing works
Organ variation in the mutagenicity of MeIQ in Big Blue® lacI transgenic mice
Suzuki, T., Hayashi, M., Ochiai, M., Wakabayashi, K., Ushijima, T., Sügimura, T., Nagao, M., & Sofuni, T. (1996) · Mutation Research/Genetic Toxicology · doi:10.1016/s0165-1218(96)90046-4 · Cited by 53 · see citing works
Telomere dynamics in childhood leukemia and solid tumors: a follow-up study
Franco, S., Ozkaynak, M. F., Sandoval, C., Tugal, O., Jayabose, S., Engelhardt, M. M., & Moore, M. A. S. (2003) · Leukemia · doi:10.1038/sj.leu.2402815 · Cited by 43 · see citing works
Effects of cisplatin on telomerase activity and telomere length in BEL-7404 human hepatoma cells
ZHANG, R. G., ZHANG, R. P., Wang, X. W., & Xie, H. J. (2002) · Cell Research · doi:10.1038/sj.cr.7290110 · Cited by 43 · see citing works
Childhood to adult transition and long-term follow-up after blood and marrow transplantation
Cupit-Link, M., Duncan, C. N., Savani, B. N., & Hashmi, S. K. (2015) · Bone Marrow Transplantation · doi:10.1038/bmt.2015.228 · Cited by 39 · see citing works
Self-citationLOSS OF TELOMERIC DNA DURING AGING MAY PREDISPOSE CELLS TO CANCER (REVIEW)
Shay, J., Wright, W. E., & Werbin, H. (1993) · International Journal of Oncology · doi:10.3892/ijo.3.4.559 · Cited by 37 · see citing works
Lahav, M., Uziel, O., Kestenbaum, M., Fraser, A., Shapiro, H., Radnay, J., Szyper‐Kravitz, M., Shimoni, A., Hardan, I., Shem‐Tov, N., et al. (2005) · Transplantation · doi:10.1097/01.tp.0000173649.99261.df · Cited by 31 · see citing works
Bone Marrow-Derived Progenitors
Kauser, K. Z., & Zeiher, A.-M. (2007) · Handbook of experimental pharmacology · doi:10.1007/978-3-540-68976-8 · Cited by 10 · see citing works
Dose Intensity of Chemotherapy for Childhood Cancers
Smith, M. A., Abrams, J. S., Trimble, E. L., et al. (1996) · The Oncologist · doi:10.1634/theoncologist.1-5-293 · Cited by 10 · see citing works
Lobetti‐Bodoni, C., Ferrero, D., Genuardi, E., Passera, R., Bernocco, E., Sia, D., Grignani, G., Crisà, E., Monitillo, L., Rocci, A., et al. (2012) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2012.05.007 · Cited by 9 · see citing works
Arora, M., Sun, C., Ness, K. K., et al. (2015) · Blood · doi:10.1182/blood.v126.23.739.739 · Cited by 1 · see citing works
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Senolytic drugs: from discovery to translation
Kirkland, J. L., & Tchkonia, T. (2020) · Journal of Internal Medicine · doi:10.1111/joim.13141 · Cited by 1,227 · see citing works
Self-citationCellular senescence and senolytics: the path to the clinic
Chaib, S., Tchkonia, T., & Kirkland, J. L. (2022) · Nature Medicine · doi:10.1038/s41591-022-01923-y · Cited by 1,105 · see citing works
Self-citationSenescent cell clearance by the immune system: Emerging therapeutic opportunities
Prata, L. G. P. L., Ovsyannikova, I. G., Tchkonia, T., & Kirkland, J. L. (2018) · Seminars in Immunology · doi:10.1016/j.smim.2019.04.003 · Cited by 497 · see citing works
Self-citationSalminen, A., Kaarniranta, K., & Kauppinen, A. (2022) · Inflammation Research · doi:10.1007/s00011-022-01598-8 · Cited by 432 · see citing works
Reducing Senescent Cell Burden in Aging and Disease
Pignolo, R. J., Passos, J. F., Khosla, S., Tchkonia, T., & Kirkland, J. L. (2020) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2020.03.005 · Cited by 177 · see citing works
Self-citationSpontaneous DNA damage to the nuclear genome promotes senescence, redox imbalance and aging
Robinson, A. R., Yousefzadeh, M. J., Rozgaja, T. A., Wang, J., Li, X., Tilstra, J. S., Feldman, C. H., Gregg, S. Q., Johnson, C. H., Skoda, E. M., et al. (2018) · Redox Biology · doi:10.1016/j.redox.2018.04.007 · Cited by 155 · see citing works
Discovery, development, and future application of senolytics: theories and predictions
Wissler Gerdes, E. O., Zhu, Y., Tchkonia, T., & Kirkland, J. L. (2020) · The FEBS Journal · doi:10.1111/febs.15264 · Cited by 160 · see citing works
Self-citationTchkonia, T., Palmer, A. K., & Kirkland, J. L. (2021) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/clinem/dgaa728 · Cited by 129 · see citing works
Self-citationTripathi, U., Misra, A., Tchkonia, T., & Kirkland, J. L. (2021) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2021.111548 · Cited by 104 · see citing works
Self-citationClinical perspectives on the age-related increase of immunosuppressive activity
Salminen, A. (2022) · Journal of Molecular Medicine · doi:10.1007/s00109-022-02193-4 · Cited by 57 · see citing works
Neurocognitive and behavioral outcomes of Chinese survivors of childhood lymphoblastic leukemia
Peng, L., Yang, L. S., Yam, P., Lam, C. S., Chan, A. S.-Y., Li, C. K., & Cheung, Y. T. (2021) · Frontiers in Oncology · doi:10.3389/fonc.2021.655669 · Cited by 29 · see citing works
- Authors
- Cupit-Link, M. C., Kirkland, J. L., Ness, K. K., Armstrong, G. T., Tchkonia, T., LeBrasseur, N. K., Armenian, S. H., Ruddy, K. J., & Hashmi, S. K.
- Affiliations
- Mayo Clinic (US)
- St. Jude Children's Research Hospital (US)
- City Of Hope National Medical Center (US)
- Corresponding author
- Hashmi, Shahrukh K.
- ORCID
- Venue
- ESMO Open
- Publisher
- Elsevier BV
- Published
- 2017
- Volume
- 2
- Issue
- 5
- Pages
- e000250
- ISSN
- 2059-7029 (ISSN-L)
- PMC
- PMC5757468
- OpenAlex
- W2777353230
- Cited by
- 214
- References
- 88
- Citations by year
- 2026: 14 · 2025: 17 · 2024: 24 · 2023: 34 · 2022: 33 · 2021: 33 · 2020: 31 · 2019: 16 · 2018: 12
- FWCI
- 1.98
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- ESMO Open (publishedVersion, cc-by-nc)
- Europe PMC (PubMed Central) (publishedVersion, cc-by-nc)
- PubMed Central (publishedVersion, cc-by-nc)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Physiology › Telomeres, Telomerase, and Senescence
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
- Health Sciences › Medicine › Oncology › Cancer survivorship and care
- Keywords
- premature aging, cancer survivors, cellular aging, hallmarks of aging, chemotherapy, radiotherapy, telomere length, cellular senescence, epigenetic modifications, microRNA, comorbidities, frailty, secondary malignancies, quality of life
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.
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