Extracellular superoxide dismutase is a major antioxidant in human fibroblasts and slows telomere shortening
Open accessAbstract
There is good evidence that telomere shortening acts as a biological clock in human fibroblasts, limiting the number of population doublings a culture can achieve. Oxidative stress also limits the growth potential of human cells, and recent data show that the effect of mild oxidative stress is mediated by a stress-related increased rate of telomere shortening. Thus, fibroblast strains have donor-specific antioxidant defense, telomere shortening rate, and growth potential. We used low-density gene expression array analysis of fibroblast strains with different antioxidant potentials and telomere shortening rates to identify gene products responsible for these differences. Extracellular superoxide dismutase was identified as the strongest candidate, a correlation that was confirmed by Northern blotting. Over-expression of this gene in human fibroblasts with low antioxidant capacity increased total cellular superoxide dismutase activity, decreased the intracellular peroxide content, slowed the telomere shortening rate, and elongated the life span of these cells under normoxia and hyperoxia. These results identify extracellular superoxide dismutase as an important antioxidant gene product in human fibroblasts, confirm the causal role of oxidative stress for telomere shortening, and strongly suggest that the senescence-like arrest under mild oxidative stress is telomere-driven.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
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?
Overexpressing SOD3 or reducing intracellular peroxide reduces the rate of telomere shortening and extends replicative lifespan of human fibroblasts.
“overexpressing the antioxidant enzyme superoxide dismutase (SOD3) in human fibroblasts, or reducing the levels of intracellular peroxide using antioxidants, are effective in reducing the rate of telomere shortening and extending replicative lifespan of these cells (von Zglinicki et al., 2000, Serra et al., 2003).”
From Telomeres and cell senescence—size matters not (2017) · cites this paper as Serra et al., 2003
Cites
Telomeres shorten during ageing of human fibroblasts
Harley, C. B., Futcher, A. B., & Greider, C. W. (1990) · Nature · doi:10.1038/345458a0 · Cited by 5,750 · see citing works
Extension of Life-Span by Introduction of Telomerase into Normal Human Cells
Bodnar, A. G., Ouellette, M., Frolkis, M., Holt, S. E., Chiu, C.-P., Morin, G. B., Harley, C. B., Shay, J. W., Lichtsteiner, S., & Wright, W. E. (1998) · Science · doi:10.1126/science.279.5349.349 · Cited by 4,975 · see citing works
Oxidative stress shortens telomeres
von Zglinicki, T. (2002) · Trends in Biochemical Sciences · doi:10.1016/s0968-0004(02)02110-2 · Cited by 2,524 · see citing works
Olovnikov (1973) · doi:10.1016/0022-5193(73)90198-7 · Cited by 1,847 · see citing works
Kirkwood, T. B. L., & Austad, S. N. (2000) · Nature · doi:10.1038/35041682 · Cited by 1,774 · see citing works
Extension of Life-Span with Superoxide Dismutase/Catalase Mimetics
Melov, S., Ravenscroft, J., Malik, S., Gill, M. S., Walker, D. W., Clayton, P., Wallace, D. C., Malfroy, B., Doctrow, S. R., & Lithgow, G. J. (2000) · Science · doi:10.1126/science.289.5484.1567 · Cited by 913 · see citing works
Mild hyperoxia shortens telomeres and inhibits proliferation of fibroblasts: a model for senescence?
von Zglinicki, T., Saretzki, G., Döcke, W., & Lotze, C. (1995) · Experimental Cell Research · doi:10.1006/excr.1995.1305 · Cited by 856 · see citing works
Self-citationOxidative DNA damage and senescence of human diploid fibroblast cells.
Chen, Q., Fischer, A., Reagan, J. D., Yan, L. J., & Ames, B. N. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.10.4337 · Cited by 720 · see citing works
Toussaint, O., Medrano, E. E., & von Zglinicki, T. (2000) · Experimental Gerontology · doi:10.1016/s0531-5565(00)00180-7 · Cited by 713 · see citing works
Genetic analysis of ageing: role of oxidative damage and environmental stresses
Martin, G. M., Austad, S. N., & Johnson, T. E. (1996) · Nature Genetics · doi:10.1038/ng0596-25 · Cited by 641 · see citing works
Senescence-like growth arrest induced by hydrogen peroxide in human diploid fibroblast F65 cells.
Chen, Q., & Ames, B. N. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.10.4130 · Cited by 641 · see citing works
Accumulation of single-strand breaks is the major cause of telomere shortening in human fibroblasts
von Zglinicki, T., Pilger, R., & Sitte, N. (2000) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(99)00207-5 · Cited by 546 · see citing works
Mice lacking extracellular superoxide dismutase are more sensitive to hyperoxia.
Carlsson, L. M. S., Jonsson, J., Edlund, H., & Marklund, S. L. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.14.6264 · Cited by 487 · see citing works
Role of Oxidative Stress in Telomere Length Regulation and Replicative Senescence
von Zglinicki, T. (2000) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2000.tb06639.x · Cited by 445 · see citing works
Preferential Accumulation of Single-Stranded Regions in Telomeres of Human Fibroblasts
Petersen, S., Saretzki, G., & Zglinicki, T. V. (1998) · Experimental Cell Research · doi:10.1006/excr.1997.3893 · Cited by 427 · see citing works
Self-citationLow oxygen concentration extends the lifespan of cultured human diploid cells
Packer, L., & FUEHR, K. (1977) · Nature · doi:10.1038/267423a0 · Cited by 393 · see citing works
von Zglinicki, T., Serra, V., Lorenz, M., Saretzki, G. C., Lenzen-Großimlinghaus, R., Gessner, R. V., Risch, A., & Steinhagen‐Thiessen, E. (2000) · Laboratory Investigation · doi:10.1038/labinvest.3780184 · Cited by 305 · see citing works
Self-citationAntunes, F., Cadenas, E., & Brunk, U. T. (2001) · Biochemical Journal · doi:10.1042/0264-6021:3560549 · Cited by 286 · see citing works
Isolation and sequence of complementary DNA encoding human extracellular superoxide dismutase.
Hjalmarsson, K., Marklund, S. L., Engström, Å., & Edlund, H. (1987) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.84.18.6340 · Cited by 241 · see citing works
Mitochondrial dysfunction leads to telomere attrition and genomic instability
Liu, L., Trimarchi, J. R., Smith, P. J. S., & Keefe, D. L. (2002) · Aging Cell · doi:10.1046/j.1474-9728.2002.00004.x · Cited by 237 · see citing works
Thiels, E., Urban, N. N., González‐Burgos, G., Kanterewicz, B. I., Barrionuevo, G., Chu, C. T., Oury, T. D., & Klann, E. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-20-07631.2000 · Cited by 214 · see citing works
Sitte, N., Merker, K., von Zglinicki, T., Grune, T., & Davies, K. J. A. (2000) · The FASEB Journal · doi:10.1096/fj.00-0209com · Cited by 213 · see citing works
Antunes, F., Cadenas, E., & Brunk, U. T. (2001) · Biochemical Journal · doi:10.1042/bj3560549 · Cited by 181 · see citing works
Accelerated Telomere Shortening in Fibroblasts After Extended Periods of Confluency
Sitte, N. (1998) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(97)00363-8 · Cited by 162 · see citing works
Expression of extracellular superoxide dismutase by human cell lines
Marklund, S. L. (1990) · Biochemical Journal · doi:10.1042/bj2660213 · Cited by 132 · see citing works
Lipofuscin accumulation in proliferating fibroblasts in vitro: an indicator of oxidative stress
Sitte, N., Merker, K., Grune, T., & von Zglinicki, T. (2001) · Experimental Gerontology · doi:10.1016/s0531-5565(00)00253-9 · Cited by 127 · see citing works
Ludwig, A., Saretzki, G. C., Holm, P. S., Tiemann, F., Lorenz, M., Emrich, T., Harley, C. B., & von Zglinicki, T. (2001) · PubMed · doi:10.25405/ncl.34663959 · Cited by 117 · see citing works
Self-citationStrålin, P., & Marklund, S. L. (1994) · Biochemical Journal · doi:10.1042/bj2980347 · Cited by 107 · see citing works
Telomere Length As a Marker of Oxidative Stress in Primary Human Fibroblast Cultures
Serra, V., Grune, T., Sitte, N., Saretzki, G. C., & von Zglinicki, T. (2000) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2000.tb06666.x · Cited by 99 · see citing works
Self-citationThe Reductive Hotspot Hypothesis: An Update
de Grey, A. D. N. J. (2000) · Archives of Biochemistry and Biophysics · doi:10.1006/abbi.1999.1509 · Cited by 97 · see citing works
Sohal, R. S., Marzabadi, M. R., Galaris, D., & Brunk, U. T. (1989) · Free Radical Biology and Medicine · doi:10.1016/0891-5849(89)90155-x · Cited by 91 · see citing works
The effect of oxygen and vitamin E on the lifespan of human diploid cells in vitro.
Balin, A. K., Goodman, D. B. P., Rasmussen, H., & Cristofalo, V. J. (1977) · The Journal of Cell Biology · doi:10.1083/jcb.74.1.58 · Cited by 87 · see citing works
Lorenz, M., Saretzki, G. C., Sitte, N., Metzkow, S., & von Zglinicki, T. (2001) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(01)00664-5 · Cited by 85 · see citing works
Self-citationWhen helicase and topoisomerase meet!
Duguet, M. (1997) · Journal of Cell Science · doi:10.1242/jcs.110.12.1345 · Cited by 81 · see citing works
Similar Gene Expression Pattern in Senescent and Hyperoxic-Treated Fibroblasts
Saretzki, G. C., Feng, J., von Zglinicki, T., & Villeponteau, B. (1998) · The Journals of Gerontology Series A · doi:10.1093/gerona/53a.6.b438 · Cited by 76 · see citing works
Self-citationMolecular Manipulations of Extracellular Superoxide Dismutase: Functional Importance for Learning
Levin, E. D., Brady, T. C., Hochrein, E. C., Oury, T. D., Jonsson, L. M., Marklund, S. L., & Crapo, J. D. (1998) · Behavior Genetics · doi:10.1023/a:1021673703129 · Cited by 68 · see citing works
Sheng, H., Kudo, M., Mackensen, G. B., Pearlstein, R. D., Crapo, J. D., & Warner, D. S. (2000) · Experimental Neurology · doi:10.1006/exnr.2000.7363 · Cited by 67 · see citing works
Effects of yeast DNA topoisomerase III on telomere structure.
Kim, R. A., Caron, P. R., & Wang, J. C. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.7.2667 · Cited by 39 · see citing works
DNA topoisomerase II cleavage of telomeres in vitro and in vivo
Yoon, H. J., Choi, I. Y., Kang, M. R., Kim, S. S., Muller, M. T., Spitzner, J. R., & Chung, I. K. (1998) · Biochimica et Biophysica Acta (BBA) - Gene Structure and Expression · doi:10.1016/s0167-4781(97)00139-5 · Cited by 36 · see citing works
Levin, E. D., Christopher, N. C., Lateef, S., Elamir, B. M., Patel, M., Liang, L., & Crapo, J. D. (2002) · Behavior Genetics · doi:10.1023/a:1015201823417 · Cited by 33 · see citing works
Human fibroblasts in vitro senesce with a donor‐specific telomere length
Serra, V., & von Zglinicki, T. (2002) · FEBS Letters · doi:10.1016/s0014-5793(02)02504-8 · Cited by 31 · see citing works
Self-citationEC-SOD and the response to inflammatory reactions and aging in mouse lung
Sentman, M.-L., Brännström, T., & Marklund, S. L. (2002) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(02)00790-6 · Cited by 16 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Mitochondria, Oxidants, and Aging
Balaban, R. S., Nemoto, S., & Finkel, T. (2005) · Cell · doi:10.1016/j.cell.2005.02.001 · Cited by 4,388 · see citing works
Trends in oxidative aging theories
Muller, F. L., Lustgarten, M. S., Jang, Y., Richardson, A., & Van Remmen, H. (2007) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2007.03.034 · Cited by 1,053 · see citing works
Oxidative Stress, Mitochondrial Dysfunction, and Aging
Cui, H., Kong, Y., & Zhang, H. (2011) · Journal of Signal Transduction · doi:10.1155/2012/646354 · Cited by 1,036 · 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
“negative human somatic cells can be significantly modulated by either increasing oxidative stress [10] or by antioxidant protection [34,37].”
BackgroundMethodInfluentialSelf-citationA New Description of Cellular Quiescence
Coller, H. A., Sang, L., & Roberts, J. M. (2006) · PLoS Biology · doi:10.1371/journal.pbio.0040083 · Cited by 548 · see citing works
Demissie, S., Levy, D., Benjamin, E. J., Cupples, L. A., Gardner, J. P., Herbert, A., Kimura, M., Larson, M. G., Meigs, J. B., Keaney, J. F., et al. (2006) · Aging Cell · doi:10.1111/j.1474-9726.2006.00224.x · Cited by 508 · see citing works
DNA damage, cellular senescence and organismal ageing: causal or correlative?
Chen, J.-H., Hales, C. N., & Ozanne, S. E. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkm681 · Cited by 481 · see citing works
Telomeres and cell senescence—size matters not
Victorelli, S., & Passos, J. F. (2017) · EBioMedicine · doi:10.1016/j.ebiom.2017.03.027 · Cited by 413 · see citing works
Psychological and metabolic stress: A recipe for accelerated cellular aging?
Epel, E. S. (2009) · HORMONES · doi:10.14310/horm.2002.1217 · Cited by 422 · see citing works
Human cell senescence as a DNA damage response
Zglinicki, T. V., Saretzki, G., Ladhoff, J., Fagagna, F. D. D., & Jackson, S. P. (2005) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2004.09.034 · Cited by 419 · see citing works
Self-citationRedox Control of the Cell Cycle in Health and Disease
Sarsour, E. H., Kumar, M. G., Chaudhuri, L., Kalen, A. L., & Goswami, P. C. (2009) · Antioxidants and Redox Signaling · doi:10.1089/ars.2009.2513 · Cited by 379 · see citing works
Changes in aqueous humor dynamics with age and glaucoma
Gabelt, B. T., & Kaufman, P. L. (2005) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2004.10.003 · Cited by 380 · see citing works
Rise in Insulin Resistance Is Associated With Escalated Telomere Attrition
Gardner, J. P., Li, S., Srinivasan, S. R., Chen, W., Kimura, M., Lu, X., Berenson, G. S., & Aviv, A. (2005) · Circulation · doi:10.1161/01.cir.0000163550.70487.0b · Cited by 361 · see citing works
The evolutionary ecology of senescence
Monaghan, P., Charmantier, A., Nussey, D. H., & Ricklefs, R. E. (2008) · Functional Ecology · doi:10.1111/j.1365-2435.2008.01418.x · Cited by 355 · see citing works
DNA damage in telomeres and mitochondria during cellular senescence: is there a connection?
Passos, J. F., Saretzki, G., & von Zglinicki, T. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkm893 · Cited by 344 · see citing works
Self-citationThe Cambridge handbook of age and ageing
Johnson, M. L., Bengtson, V., Coleman, P., & Kirkwood, T. (2005) · Cambridge University Press eBooks · doi:10.1017/cbo9780511610714 · Cited by 392 · see citing works
Lu, T., & Finkel, T. (2008) · Experimental Cell Research · doi:10.1016/j.yexcr.2008.01.011 · Cited by 327 · see citing works
A continuous correlation between oxidative stress and telomere shortening in fibroblasts
Richter, T., & Zglinicki, T. V. (2007) · Experimental Gerontology · doi:10.1016/j.exger.2007.08.005 · Cited by 321 · see citing works
Short Telomeres Are Associated With Increased Carotid Atherosclerosis in Hypertensive Subjects
Benetos, A., Gardner, J. P., Zureik, M., Labat, C., Xiaobin, L., Adamopoulos, C., Temmar, M., Bean, K. E., Thomas, F., & Aviv, A. (2004) · Hypertension · doi:10.1161/01.hyp.0000113081.42868.f4 · Cited by 313 · see citing works
Associations between diet, lifestyle factors, and telomere length in women
Cassidy, A., Vivo, I. D., Liu, Y., Han, J., Prescott, J., Hunter, D. J., & Rimm, E. B. (2010) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.2009.28947 · Cited by 308 · see citing works
Accelerated senescence in the kidneys of patients with type 2 diabetic nephropathy
Verzola, D., Gandolfo, M. T., Gaetani, G., Ferraris, A., Mangerini, R., Ferrario, F., Villaggio, B., Gianiorio, F., Tosetti, F., Weiss, U., et al. (2008) · American Journal of Physiology-Renal Physiology · doi:10.1152/ajprenal.90302.2008 · Cited by 302 · see citing works
Oxidative damage in telomeric DNA disrupts recognition by TRF1 and TRF2
Opresko, P. L. (2005) · Nucleic Acids Research · doi:10.1093/nar/gki273 · Cited by 289 · see citing works
Cellular Senescence in Neurodegenerative Diseases
Martínez‐Cué, C., & Rueda, N. (2020) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2020.00016 · Cited by 285 · see citing works
Factors contributing to the outcome of oxidative damage to nucleic acids
Evans, M. D., & Cooke, M. S. (2004) · BioEssays · doi:10.1002/bies.20027 · Cited by 280 · see citing works
Mesquita, A., Weinberger, M., Silva, A., Sampaio‐Marques, B., Almeida, B., Leão, C., Costa, V., Rodrigues, F. J. S., Burhans, W. C., & Ludovico, P. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1004432107 · Cited by 268 · see citing works
Telomere length predicts poststroke mortality, dementia, and cognitive decline
Martin-Ruiz, C. M., Dickinson, H. O., Keys, B., Rowan, E. N., Kenny, R. A., & von Zglinicki, T. (2006) · Annals of Neurology · doi:10.1002/ana.20869 · Cited by 257 · see citing works
Speakman, J. R., & Selman, C. (2011) · BioEssays · doi:10.1002/bies.201000132 · Cited by 259 · see citing works
Transcriptional responses to oxidative stress: Pathological and toxicological implications
Ma, Q. (2009) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2009.11.004 · Cited by 248 · see citing works
Telomere loss in relation to age and early environment in long-lived birds
Hall, M. E., Nasir, L., Daunt, F., Gault, E. A., Croxall, J. P., Wanless, S., & Monaghan, P. (2004) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2004.2768 · Cited by 247 · see citing works
A Life‐History Perspective on Short‐ and Long‐Term Consequences of Compensatory Growth
Mangel, M., & Munch, S. B. (2005) · The American Naturalist · doi:10.1086/444439 · Cited by 245 · see citing works
Cellular Senescence: Molecular Mechanisms, In Vivo Significance, and Redox Considerations
Müller, M. K. (2008) · Antioxidants and Redox Signaling · doi:10.1089/ars.2008.2104 · Cited by 237 · see citing works
Brain Endothelial Cells Are Exquisite Sensors of Age-Related Circulatory Cues
Chen, M. B., Yang, A. C., Yousef, H., Lee, D., Chen, W., Schaum, N., Lehallier, B., Quake, S. R., & Wyss-Coray, T. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.03.012 · Cited by 233 · see citing works
“Interestingly, transcript levels of superoxide dismutase (Sod1)–an antioxidant shown to increase lifespan, decrease the rate of telomere shortening (Serra et al., 2003), protect AD model mice (Murakami et al.”
The association between stressors and telomeres in non‐human vertebrates: a meta‐analysis
Chatelain, M., Drobniak, S. M., & Szulkin, M. (2019) · Ecology Letters · doi:10.1111/ele.13426 · Cited by 222 · see citing works
Telomere Length Variations in Aging and Age-Related Diseases
Rizvi, S., Raza, S. T., & Mahdi, F. (2015) · Current Aging Science · doi:10.2174/1874609808666150122153151 · Cited by 209 · see citing works
Saretzki, G., Murphy, M. P., & Von Zglinicki, T. (2003) · Aging Cell · doi:10.1046/j.1474-9728.2003.00040.x · Cited by 203 · see citing works
Self-citationTelomeres and human aging: facts and fibs
Aviv, A. (2004) · Science of Aging Knowledge Environment · doi:10.1126/sageke.2004.51.pe43 · Cited by 198 · see citing works
Carrero, J. J., Stenvinkel, P., Fellström, B., Qureshi, A. R., Lamb, K. J., Heimbürger, O., Barany, P. F., Radhakrishnan, K., Lindholm, B., Soveri, I., et al. (2007) · Journal of Internal Medicine · doi:10.1111/j.1365-2796.2007.01890.x · Cited by 185 · see citing works
Telomere shortening occurs in Asian Indian Type 2 diabetic patients
Adaikalakoteswari, A., Balasubramanyam, M., & Mohan, V. (2005) · Diabetic Medicine · doi:10.1111/j.1464-5491.2005.01574.x · Cited by 179 · see citing works
The evolution of senescence from a comparative perspective
Ricklefs, R. E. (2008) · Functional Ecology · doi:10.1111/j.1365-2435.2008.01420.x · Cited by 165 · see citing works
Collerton, J. C., Barrass, K., Bond, J., Eccles, M., Jagger, C., James, O., Martin-Ruiz, C. M., Robinson, L. A., von Zglinicki, T., & Kirkwood, T. B. L. (2007) · BMC Geriatrics · doi:10.1186/1471-2318-7-14 · Cited by 163 · see citing works
Telomere Length in Prospective and Retrospective Cancer Case-Control Studies
Pooley, K. A., Sandhu, M. S., Tyrer, J. P., Shah, M., Driver, K. E., Luben, R., Bingham, S. A., Ponder, B. A. J., Pharoah, P. D. P., Khaw, K., et al. (2010) · Cancer Research · doi:10.1158/0008-5472.can-09-4595 · Cited by 161 · 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
Telomere attrition as ageing biomarker.
Bekaert, S., Meyer, T. D., & Oostveldt, P. V. (2005) · PubMed · Cited by 158 · see citing works
Hoxha, M., Dioni, L., Bonzini, M., Pesatori, A. C., Fustinoni, S., Cavallo, D. M., Carugno, M., Albetti, B., Marinelli, B., Schwartz, J. D., et al. (2009) · Environmental Health · doi:10.1186/1476-069x-8-41 · Cited by 156 · see citing works
Developmental differences in the immortalization of lung fibroblasts by telomerase
Forsyth, N. R., Evans, A., Shay, J. W., & Wright, W. E. (2003) · Aging Cell · doi:10.1046/j.1474-9728.2003.00057.x · Cited by 156 · see citing works
Redox Regulation in the Extracellular Environment
Ottaviano, F. G., Handy, D. E., & Loscalzo, J. (2007) · Circulation Journal · doi:10.1253/circj.72.1 · Cited by 155 · see citing works
Mitochondrial function as a determinant of life span
Lanza, I. R., & Nair, K. S. (2009) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-009-0724-5 · Cited by 151 · see citing works
Telomerase, mitochondria and oxidative stress
Saretzki, G. C. (2009) · Experimental Gerontology · doi:10.1016/j.exger.2009.05.004 · Cited by 149 · see citing works
Self-citationA new generation of proto-oncogenes: Cold-inducible RNA binding proteins
LLeonart, M. E. (2009) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2009.11.001 · Cited by 145 · see citing works
Kondoh, H., LLeonart, M. E., Bernard, D., & Gil, J. (2007) · PubMed · doi:10.14670/hh-22.85 · Cited by 142 · see citing works
Accelerated Telomere Shortening in Leukocyte Subpopulations of Patients With Coronary Heart Disease
Spyridopoulos, I., Hoffmann, J., Aicher, A., Brümmendorf, T. H., Doerr, H. W., Zeiher, A. M., & Dimmeler, S. (2009) · Circulation · doi:10.1161/circulationaha.109.854299 · Cited by 147 · see citing works
Telomere shortening in chronic obstructive pulmonary disease
Houben, J. M. J., Mercken, E. M., Ketelslegers, H. B., Bast, A., Wouters, E. F., Hageman, G. J., & Schols, A. M. W. J. (2009) · Respiratory Medicine · doi:10.1016/j.rmed.2008.09.003 · Cited by 141 · see citing works
Telomere dysfunction, genome instability and cancer
Annie, L. M. C. (2007) · Frontiers in bioscience · doi:10.2741/2825 · Cited by 134 · see citing works
Rai, P., Young, J. J., Burton, D. G. A., Giribaldi, M. G., Önder, T. T., & Weinberg, R. A. (2010) · Oncogene · doi:10.1038/onc.2010.520 · Cited by 136 · see citing works
Martin-Ruiz, C. M., Saretzki, G. C., Petrie, J., Ladhoff, J., Jeyapalan, J. C., Wei, W., Sedivy, J. M., & von Zglinicki, T. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m311980200 · Cited by 135 · see citing works
Self-citationMitochondria, telomeres and cell senescence
Passos, J. F., & von Zglinicki, T. (2005) · Experimental Gerontology · doi:10.1016/j.exger.2005.04.006 · Cited by 133 · see citing works
Oxygen free radicals in cell senescence: Are they signal transducers?
Passos, J. F., & Von Zglinicki, T. (2006) · Free Radical Research · doi:10.1080/10715760600917151 · Cited by 122 · see citing works
Chronic oxidative stress induces a tissue-specific reduction in telomere length in CAST/Ei mice
Cattan, V., Mercier, N., Gardner, J. P., Regnault, V., Labat, C., Mäki-Jouppila, J. H., Nzietchueng, R., Bénétos, A., Kimura, M., Aviv, A., et al. (2008) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2008.01.007 · Cited by 120 · see citing works
The role of cold‐inducible RNA binding protein in cell stress response
Liao, Y., Tong, L., Tang, L., & Wu, S. (2017) · International Journal of Cancer · doi:10.1002/ijc.30833 · Cited by 116 · see citing works
Gorowiec, M. R., Borthwick, L. A., Parker, S., Kirby, J. A., Saretzki, G. C., & Fisher, A. J. (2012) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2011.12.020 · Cited by 117 · see citing works
Self-citationCardiomyocyte‐Specific Telomere Shortening is a Distinct Signature of Heart Failure in Humans
Sharifi‐Sanjani, M., Oyster, N. M., Tichy, E. D., Bedi, K. C., Harel, O., Margulies, K. B., & Mourkioti, F. (2017) · Journal of the American Heart Association · doi:10.1161/jaha.116.005086 · Cited by 112 · see citing works
Redox Control of Signal Transduction, Gene Expression and Cellular Senescence
Esposito, F., Ammendola, R., Faraonio, R., Russo, T., & Cimino, F. (2004) · Neurochemical Research · doi:10.1023/b:nere.0000014832.78725.1a · Cited by 113 · see citing works
Effect of Long-Term Hormone Therapy on Telomere Length in Postmenopausal Women
Lee, D., Im, J., Kim, J., Lee, H.-R., & Shim, J. (2005) · Yonsei Medical Journal · doi:10.3349/ymj.2005.46.4.471 · Cited by 114 · see citing works
Oxidative Stress, Mitochondrial Dysfunction and the Mitochondria Theory of Aging
Kong, Y., Trabucco, S. E., & Zhang, H. (2014) · Interdisciplinary topics in gerontology and geriatrics · doi:10.1159/000358901 · Cited by 112 · see citing works
Mitochondria, Telomeres and Telomerase Subunits
Zheng, Q., Huang, J., & Wang, G. (2019) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2019.00274 · Cited by 110 · see citing works
Free Radical Theory of Aging: Implications in Male Infertility
Desai, N. R., Sabanegh, E., Kim, T. S., & Agarwal, A. K. (2009) · Urology · doi:10.1016/j.urology.2009.05.025 · Cited by 109 · see citing works
Nicotinamide extends replicative lifespan of human cells
Kang, H. T., Lee, H. I., & Hwang, E. S. (2006) · Aging Cell · doi:10.1111/j.1474-9726.2006.00234.x · Cited by 105 · see citing works
Telomere length and cardiovascular aging
Fyhrquist, F., & Saijonmaa, O. J. (2012) · Annals of Medicine · doi:10.3109/07853890.2012.660497 · Cited by 102 · see citing works
Tsitsimpikou, C., Tzatzarakis, M. N., Fragkiadaki, P., Kovatsi, L., Stivaktakis, P. D., Kalogeraki, A. M., Kouretas, D., & Tsatsakis, A. M. (2012) · Toxicology · doi:10.1016/j.tox.2012.11.002 · Cited by 101 · see citing works
Theurey, P., & Pizzo, P. (2018) · Genes · doi:10.3390/genes9010022 · Cited by 103 · see citing works
Involvement of the INK4a/Arf gene locus in senescence
Collins, C. J., & Sedivy, J. M. (2003) · Aging Cell · doi:10.1046/j.1474-9728.2003.00048.x · Cited by 113 · see citing works
Cellular life span and the Warburg effect
Kondoh, H. (2008) · Experimental Cell Research · doi:10.1016/j.yexcr.2008.03.007 · Cited by 98 · see citing works
Short telomeres in short‐lived males: what are the molecular and evolutionary causes?
Jemielity, S., Kimura, M., Parker, K. M., Parker, J. D., Cao, X., Aviv, A., & Keller, L. (2007) · Aging Cell · doi:10.1111/j.1474-9726.2007.00279.x · Cited by 94 · see citing works
Starr, J. M., Shiels, P. G., Harris, S. E., Pattie, A., Pearce, M. S., Relton, C. L., & Deary, I. J. (2008) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2008.09.020 · Cited by 95 · see citing works
Mitochondrial longevity pathways
Vendelbo, M. H., & Nair, K. S. (2011) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2011.01.029 · Cited by 90 · see citing works
Epigenetic Mechanisms Impacting Aging: A Focus on Histone Levels and Telomeres
Song, S., & Johnson, F. B. (2018) · Genes · doi:10.3390/genes9040201 · Cited by 91 · see citing works
Bull, C. F., & Fenech, M. F. (2008) · Proceedings of The Nutrition Society · doi:10.1017/s0029665108006988 · Cited by 91 · see citing works
Proteasome inhibition induces a senescence-like phenotype in primary human fibroblasts cultures
Chondrogianni, N., & Gonos, E. S. (2004) · Biogerontology · doi:10.1023/b:bgen.0000017687.55667.42 · Cited by 86 · see citing works
Stress-induced Premature Senescence in hTERT-expressing Ataxia Telangiectasia Fibroblasts
Naka, K., Tachibana, A., Ikeda, K., & Motoyama, N. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m309457200 · Cited by 86 · see citing works
Cardiotoxicity in rabbits after a low-level exposure to diazinon, propoxur, and chlorpyrifos
Zafiropoulos, A., Tsarouhas, K., Tsitsimpikou, C., Fragkiadaki, P., Germanakis, I. E., Tsardi, M., Maravgakis, G., Goutzourelas, N., Vasilaki, F., Kouretas, D., et al. (2014) · Human & Experimental Toxicology · doi:10.1177/0960327114532384 · Cited by 83 · see citing works
Grahame, T. J., & Schlesinger, R. B. (2012) · Particle and Fibre Toxicology · doi:10.1186/1743-8977-9-21 · Cited by 80 · see citing works
Integrated Multi-Omics for Novel Aging Biomarkers and Antiaging Targets
Wu, L., Xie, X., Liang, T., Ma, J., Yang, L., Yang, J., Li, L., Xi, Y., Li, H., Zhang, J., et al. (2021) · Biomolecules · doi:10.3390/biom12010039 · Cited by 82 · see citing works
Physical Activity and Telomere Biology: Exploring the Link with Aging-Related Disease Prevention
Ludlow, A. T., & Roth, S. M. (2011) · Journal of Aging Research · doi:10.4061/2011/790378 · Cited by 79 · see citing works
Reactive oxygen species, ageing and the hormesis police
Ludovico, P., & Burhans, W. C. (2013) · FEMS Yeast Research · doi:10.1111/1567-1364.12070 · Cited by 78 · see citing works
Leukocyte telomere length is associated with HDL cholesterol levels: The Bogalusa heart study
Chen, W., Gardner, J. P., Kimura, M., Brimacombe, M. B., Cao, X., Srinivasan, S. R., Berenson, G. S., & Aviv, A. (2009) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2009.01.021 · Cited by 77 · see citing works
Franco, S., Blasco, M. A., Siedlak, S. L., Harris, P. L. R., Moreira, P. I., Perry, G. L., & Smith, M. A. (2006) · Alzheimer s & Dementia · doi:10.1016/j.jalz.2006.03.001 · Cited by 74 · see citing works
Diet-related telomere shortening and chromosome stability
Marcon, F., Siniscalchi, E., Crebelli, R., Saieva, C., Sera, F., Fortini, P., Simonelli, V., & Palli, D. (2011) · Mutagenesis · doi:10.1093/mutage/ger056 · Cited by 71 · see citing works
The intrinsic stiffness of human trabecular meshwork cells increases with senescence
Morgan, J. T., Raghunathan, V. K., Chang, Y.-R., Murphy, C. J., & Russell, P. (2015) · Oncotarget · doi:10.18632/oncotarget.3798 · Cited by 69 · see citing works
Zhao, F., Yang, Q., Shi, S., Luo, X., & Sun, Y. (2016) · Scientific Reports · doi:10.1038/srep39051 · Cited by 66 · see citing works
Replicative senescence and the art of counting
von Zglinicki, T. (2003) · Experimental Gerontology · doi:10.1016/j.exger.2003.09.015 · Cited by 68 · see citing works
Telomeric aging: mitotic clock or stress indicator?
Koliada, A. K., Krasnienkov, D. S., & Vaiserman, A. M. (2015) · Frontiers in Genetics · doi:10.3389/fgene.2015.00082 · Cited by 67 · see citing works
Growth, telomere dynamics and successful and unsuccessful human aging
Aviv, A., Levy, D. A., & Mangel, M. (2003) · Mechanisms of Ageing and Development · doi:10.1016/s0047-6374(03)00143-x · Cited by 67 · see citing works
Caruso, C. (2009) · Frontiers in Bioscience-Scholar · doi:10.2741/s72 · Cited by 68 · see citing works
Short telomeres in aggressive non-Hodgkin's lymphoma as a risk factor in lymphomagenesis
Widmann, T., Herrmann, M., Taha, N., König, J., & Pfreundschuh, M. G. (2007) · Experimental Hematology · doi:10.1016/j.exphem.2007.03.009 · Cited by 64 · see citing works
Cardiotoxicity in rabbits after long-term nandrolone decanoate administration
Vasilaki, F., Tsitsimpikou, C., Tsarouhas, K., Germanakis, I. E., Tzardi, M., Kavvalakis, M. P., Özçağlı, E., Kouretas, D., & Tsatsakis, A. M. (2015) · Toxicology Letters · doi:10.1016/j.toxlet.2015.10.026 · Cited by 64 · see citing works
Shim, G., Ricoul, M., Hempel, W. M., Azzam, E. I., & Sabatier, L. (2014) · Mutation Research/Reviews in Mutation Research · doi:10.1016/j.mrrev.2014.01.001 · Cited by 64 · see citing works
Lin, S., Huo, X., Zhang, Q., Fan, X., Du, L., Xu, X., Qiu, S., Zhang, Y., Wang, Y., & Gu, J. (2013) · PLoS ONE · doi:10.1371/journal.pone.0060815 · Cited by 63 · see citing works
Lawless, C., Jurk, D., Gillespie, C. S., Shanley, D., Saretzki, G., von Zglinicki, T., & Passos, J. F. (2012) · PLoS ONE · doi:10.1371/journal.pone.0032117 · Cited by 62 · see citing works
Self-citationCellular senescence: unravelling complexity
Passos, J. F., Simillion, C., Hallinan, J. S., Wipat, A., & von Zglinicki, T. (2009) · AGE · doi:10.1007/s11357-009-9108-1 · Cited by 61 · see citing works
Richter, T., Saretzki, G. C., Nelson, G., Melcher, M., Olijslagers, S., & von Zglinicki, T. (2007) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2007.02.003 · Cited by 61 · see citing works
Self-citation
- Authors
- Serra, V., von Zglinicki, T., Lorenz, M., & Saretzki, G.
- Affiliations
- Stiftung Charité (DE)
- Newcastle University (GB)
- Venue
- Journal of Biological Chemistry
- Publisher
- Elsevier BV
- Published
- 2003-02
- Volume
- 278
- Issue
- 9
- Pages
- 6824-6830
- ISSN
- 0021-9258 (ISSN-L)
- OpenAlex
- W2128014750
- Cited by
- 278
- References
- 41
- Citations by year
- 2026: 2 · 2025: 3 · 2024: 6 · 2023: 7 · 2022: 10 · 2021: 18 · 2020: 6 · 2019: 11 · 2018: 8 · 2017: 7 · 2016: 7 · 2015: 14 · 2014: 13 · 2013: 13 · 2012: 14
- FWCI
- 10.68
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Biological Chemistry (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Newcastle University ePrints (Newcastle Univesity)
- Topics
- Health Sciences › Medicine › Physiology › Telomeres, Telomerase, and Senescence
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Redox biology and oxidative stress
- Keywords
- extracellular superoxide dismutase, telomere shortening, human fibroblasts, oxidative stress, antioxidant defense, cellular aging, replicative lifespan, hyperoxia, hydrogen peroxide, gene expression profiling, senescence
- MeSH terms
- Actins, Aging, Hypoxia, Antioxidants, Cells, Cultured, Cytoplasm, Fibroblasts, Humans, Superoxide Dismutase, Blotting, Northern, Gene Expression, Telomere, Oxidative Stress, Reverse Transcriptase Polymerase Chain Reaction
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