Stochastic and genetic factors influence tissue-specific decline in ageing C. elegans
Abstract
The nematode Caenorhabditis elegans is an important model for studying the genetics of ageing, with over 50 life-extension mutations known so far. However, little is known about the pathobiology of ageing in this species, limiting attempts to connect genotype with senescent phenotype. Using ultrastructural analysis and visualization of specific cell types with green fluorescent protein, we examined cell integrity in different tissues as the animal ages. We report remarkable preservation of the nervous system, even in advanced old age, in contrast to a gradual, progressive deterioration of muscle, resembling human sarcopenia. The age-1(hx546) mutation, which extends lifespan by 60-100%, delayed some, but not all, cellular biomarkers of ageing. Strikingly, we found strong evidence that stochastic as well as genetic factors are significant in C. elegans ageing, with extensive variability both among same-age animals and between cells of the same type within individuals.
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?
Ultrastructural studies in C. elegans showed vastly different rates of aging of tissues and cells in individual worms, ascribed largely to stochastic events, and the onset of degenerative changes was neither linear nor synchronized.
“Ultrastructural studies in C. elegans almost two decades ago hinted that it might not.30 The authors noted not only vastly different rates of aging of tissues and cells in individual worms, which they ascribed largely to stochastic events, but the onset of degenerative changes was neither linear nor synchronized.”
From Asynchronous, contagious and digital aging (2021) · cites this paper as [30]
In C. elegans, muscles undergo an aging-related ultrastructural deterioration (sarcopenia), whereas nervous system ultrastructure remains largely intact.
“In the model organism C. elegans the muscles undergo an aging-related ultrastructural deterioration (also referred to as sarcopenia), whereas nervous system ultrastructure remains largely intact(Herndon et al., 2002).”
From Programmed cell death in aging (2015) · cites this paper as Herndon et al., 2002
Cites
The structure of the nervous system of the nematode <i>Caenorhabditis elegans</i>
White, J. G., Southgate, E., Thomson, J. N., & Brenner, S. (1986) · Philosophical Transactions of the Royal Society of London. B, Biological Sciences · doi:10.1098/rstb.1986.0056 · Cited by 5,589 · see citing works
Post-embryonic cell lineages of the nematode, Caenorhabditis elegans
Sulston, J. E., & Horvitz, H. R. (1977) · Developmental Biology · doi:10.1016/0012-1606(77)90158-0 · Cited by 3,479 · see citing works
The Nematode Caenorhabditis elegans
Wood, W. B. (1988) · Cold Spring Harbor Laboratory eBooks · Cited by 2,821 · see citing works
Kimura, K. D., Tissenbaum, H. A., Liu, Y., & Ruvkun, G. (1997) · Science · doi:10.1126/science.277.5328.942 · Cited by 2,250 · see citing works
Kirkwood, T. B. L. (1977) · Nature · doi:10.1038/270301a0 · Cited by 2,007 · see citing works
Life and Death of Neurons in the Aging Brain
Morrison, J. H., & Hof, P. R. (1997) · Science · doi:10.1126/science.278.5337.412 · Cited by 1,344 · see citing works
Signals from the reproductive system regulate the lifespan of C. elegans
Hsin, H., & Kenyon, C. J. (1999) · Nature · doi:10.1038/20694 · Cited by 1,015 · see citing works
Friedman, D. B., & Johnson, T. E. (1988) · Genetics · doi:10.1093/genetics/118.1.75 · Cited by 1,011 · see citing works
Campagnola, P. J., Millard, A. C., Terasaki, M., Hoppe, P. E., Malone, C. J., & Mohler, W. A. (2002) · Biophysical Journal · doi:10.1016/s0006-3495(02)75414-3 · Cited by 922 · see citing works
Mutant sensory cilia in the nematode Caenorhabditis elegans
Perkins, L. A., Hedgecock, E. M., Thomson, J. N., & Culotti, J. G. (1986) · Developmental Biology · doi:10.1016/0012-1606(86)90314-3 · Cited by 907 · see citing works
Garigan, D., Hsu, A.-L., Fraser, A. G., Kamath, R. S., Ahringer, J., & Kenyon, C. (2002) · Genetics · doi:10.1093/genetics/161.3.1101 · Cited by 803 · see citing works
Kirkwood, T. B. L. (2002) · Mechanisms of Ageing and Development · doi:10.1016/s0047-6374(01)00419-5 · Cited by 801 · see citing works
Klass, M. R. (1977) · Mechanisms of Ageing and Development · doi:10.1016/0047-6374(77)90043-4 · Cited by 793 · see citing works
Caenorhabditis elegans : modern biological analysis of an organism
Epstein, H. F., & Diane, C. S. (1995) · Cited by 685 · see citing works
Regulation of C. elegans Life-Span by Insulinlike Signaling in the Nervous System
Wolkow, C. A., Kimura, K. D., Lee, M. S., & Ruvkun, G. (2000) · Science · doi:10.1126/science.290.5489.147 · Cited by 681 · see citing works
Regulation of lifespan by sensory perception in Caenorhabditis elegans
Apfeld, J., & Kenyon, C. (1999) · Nature · doi:10.1038/45544 · Cited by 573 · see citing works
Regulation of Life-Span by Germ-Line Stem Cells in Caenorhabditis elegans
Arantes-Oliveira, N., Apfeld, J., Dillin, A. G., & Kenyon, C. J. (2002) · Science · doi:10.1126/science.1065768 · Cited by 530 · see citing works
Maduro, M., & Pilgrim, D. B. (1995) · Genetics · doi:10.1093/genetics/141.3.977 · Cited by 449 · see citing works
Hedgecock, E. M., Culotti, J. G., Thomson, J. N., & Perkins, L. A. (1985) · Developmental Biology · doi:10.1016/0012-1606(85)90443-9 · Cited by 435 · see citing works
Hall, D. H., Winfrey, V. P., Blaeuer, G. L., Hoffman, L. H., Furuta, T., Rose, K. L., Hobert, O., & Greenstein, D. (1999) · Developmental Biology · doi:10.1006/dbio.1999.9356 · Cited by 325 · see citing works
Self-citationTranscriptional Profile of Aging in C. elegans
Lund, J., Tedesco, P. M., Duke, K., Wang, J., Kim, S. K., & Johnson, T. E. (2002) · Current Biology · doi:10.1016/s0960-9822(02)01146-6 · Cited by 304 · see citing works
Chance, development, and aging
de Grey, A. D. N. J. (2001) · Experimental Gerontology · doi:10.1016/s0531-5565(01)00123-1 · Cited by 281 · see citing works
Chance, development, and aging
Finch, C. E., & Kirkwood, T. (2000) · Cited by 256 · see citing works
Pioneer Axon Guidance by UNC-129, a C. elegans TGF-β
Colavita, A., Krishna, S., Zheng, H., Padgett, R. W., & Culotti, J. G. (1998) · Science · doi:10.1126/science.281.5377.706 · Cited by 222 · see citing works
Stress resistance as a determinate of C. elegans lifespan
Lithgow, G. J., & Walker, G. A. (2002) · Mechanisms of Ageing and Development · doi:10.1016/s0047-6374(01)00422-5 · Cited by 212 · see citing works
Mechanisms of life span determination in Caenorhabditis elegans☆
Vanfleteren, J. R., & Braeckman, B. P. (1999) · Neurobiology of Aging · doi:10.1016/s0197-4580(99)00087-1 · Cited by 181 · see citing works
Johnson, T. E. (1987) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.84.11.3777 · Cited by 175 · see citing works
Chapter 17 Electron Microscopy and Three-Dimensional Image Reconstruction
Hall, D. H. (1995) · Methods in cell biology · doi:10.1016/s0091-679x(08)61397-7 · Cited by 166 · see citing works
Self-citationNeuropathology of Degenerative Cell Death inCaenorhabditis elegans
Hall, D. H., Gong, G., Garcı́a-Añoveros, J., Gong, L., Chalfie, M., & Driscoll, M. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-03-01033.1997 · Cited by 163 · see citing works
Self-citationJohnson, T. E., de Castro, E., de Castro, S. H., Cypser, J. R., Henderson, S., & Tedesco, P. (2001) · Experimental Gerontology · doi:10.1016/s0531-5565(01)00144-9 · Cited by 153 · see citing works
Bolanowski, M. A., Russell, R. L., & Jacobson, L. A. (1981) · Mechanisms of Ageing and Development · doi:10.1016/0047-6374(81)90136-6 · Cited by 141 · see citing works
Combinatorial control of touch receptor neuron expression in Caenorhabditis elegans
Mitani, S., Du, H., Hall, D. H., Driscoll, M., & Chalfie, M. (1993) · Development · doi:10.1242/dev.119.3.773 · Cited by 137 · see citing works
Self-citationSozou, P. D., & Kirkwood, T. B. L. (2001) · Journal of Theoretical Biology · doi:10.1006/jtbi.2001.2432 · Cited by 115 · see citing works
Insulin-like signaling, metabolism, stress resistance and aging in Caenorhabditis elegans
Braeckman, B. P. (2001) · Mechanisms of Ageing and Development · doi:10.1016/s0047-6374(01)00222-6 · Cited by 110 · see citing works
Degeneration of photoreceptors in rhodopsin mutants of Drosophila
Leonard, D. S., Bowman, V. D., Ready, D. F., et al. (1992) · Journal of Neurobiology · doi:10.1002/neu.480230602 · Cited by 98 · see citing works
Kirkwood, T. B. L. (1996) · BioEssays · doi:10.1002/bies.950181211 · Cited by 89 · see citing works
Studies on ageing in nematodes III. Electronmicroscopical studies on age-associated cellular damage
Epstein, J., Himmelhoch, S., & Gershon, D. (1972) · Mechanisms of Ageing and Development · doi:10.1016/0047-6374(72)90070-x · Cited by 85 · see citing works
Movement as an Index of Vitality:Comparing Wild Type and the age-1 Mutant of Caenorhabditis elegans
Duhon, S. A., & Johnson, T. (1995) · The Journals of Gerontology Series A · doi:10.1093/gerona/50a.5.b254 · Cited by 73 · see citing works
Some observations on the skeletal musculature of aged rats
Fujisawa, K. (1975) · Journal of the Neurological Sciences · doi:10.1016/0022-510x(75)90170-7 · Cited by 71 · see citing works
Johnson, T. E., & McCaffrey, G. (1985) · Mechanisms of Ageing and Development · doi:10.1016/0047-6374(85)90118-6 · Cited by 67 · see citing works
Electron Microscope Studies on Aging Drosophila melanogaster III. Flight Muscle
Takahashi, A., Philpott, D. E., & Miquel, J. (1970) · Journal of Gerontology · doi:10.1093/geronj/25.3.222 · Cited by 55 · see citing works
Control of muscle fibre size: a crucial factor in ageing.
Hughes, S. M., & Schiaffino, S. (1999) · PubMed · doi:10.1046/j.1365-201x.1999.00622.x · Cited by 50 · see citing works
Control of muscle fibre size: a crucial factor in ageing
Hughes, S. M., & Schiaffino, S. (1999) · Acta Physiologica Scandinavica · doi:10.1046/j.1365-201x.1999.00619.x · Cited by 50 · see citing works
Cell Death in C. elegans: Molecular insights into Mechanisms Conserved Between Nematodes and Mammals
Driscoll, M. (1996) · Brain Pathology · doi:10.1111/j.1750-3639.1996.tb00873.x · Cited by 46 · see citing works
Self-citationImmuno-EM Localization of GFP-tagged Yolk Proteins in C. Elegans Using Microwave Fixation
Paupard, M., Miller, A. E., Grant, B. D., et al. (2001) · Journal of Histochemistry & Cytochemistry · doi:10.1177/002215540104900803 · Cited by 43 · see citing works
Self-citationRegulation of gene expression is preserved in aging Drosophila melanogaster
Rogina, B., Vaupel, J. W., Partridge, L., & Helfand, S. L. (1998) · Current Biology · doi:10.1016/s0960-9822(98)70184-8 · Cited by 34 · see citing works
Bolanowski, M. A., Jacobson, L. A., & Russell, R. L. (1983) · Mechanisms of Ageing and Development · doi:10.1016/0047-6374(83)90048-9 · Cited by 26 · see citing works
Structural brain aging in inbred mice: potential for genetic linkage
Jucker, M., Bondolfi, L., Calhoun, M. E., et al. (2000) · Experimental Gerontology · doi:10.1016/s0531-5565(00)00190-x · Cited by 26 · see citing works
Rattan, S. I. S. (2000) · Biogerontology · doi:10.1023/a:1026536128119 · Cited by 20 · see citing works
Electron microscope studies on aging Drosophila melanogaster. I
Miquel, J., Philpott, D. E., & Takahashi, A. (1970) · NASA Technical Reports Server (NASA) · Cited by 18 · see citing works
Helfand, S. L., & Naprta, B. (1996) · Mechanisms of Development · doi:10.1016/0925-4773(95)00489-0 · Cited by 18 · see citing works
Changing complexity in aging: a metric not an hypothesis
Kirkwood, T. B. L. (2002) · Neurobiology of Aging · doi:10.1016/s0197-4580(01)00260-3 · Cited by 7 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Kenyon, C. J. (2010) · Nature · doi:10.1038/nature08980 · Cited by 2,739 · see citing works
Insights into the ageing mind: a view from cognitive neuroscience
Hedden, T., & Gabrieli, J. D. E. (2004) · Nature Reviews Neuroscience · doi:10.1038/nrn1323 · Cited by 2,223 · see citing works
Understanding the odd science of aging
Kirkwood, T. B. L. (2005) · Cell · doi:10.1016/j.cell.2005.01.027 · Cited by 1,984 · see citing works
The plasticity of aging: insights from long-lived mutants
Kenyon, C. (2005) · Cell · doi:10.1016/j.cell.2005.02.002 · Cited by 1,338 · see citing works
Sarcopenia: its assessment, etiology, pathogenesis, consequences and future perspectives
Rolland, Y., Czerwinski, S., van Kan, G. A., Morley, J. E., Cesari, M., Onder, G., Woo, J., Baumgartner, R., Pillard, F., Boirie, Y., et al. (2008) · The Journal of nutrition, health and aging · doi:10.1007/bf02982704 · Cited by 1,071 · see citing works
The Cell Non-Autonomous Nature of Electron Transport Chain-Mediated Longevity
Durieux, J., Wolff, S., & Dillin, A. (2011) · Cell · doi:10.1016/j.cell.2010.12.016 · Cited by 1,059 · see citing works
Tissue-Specific Activities of C. elegans DAF-16 in the Regulation of Lifespan
Libina, N., Berman, J. R., & Kenyon, C. (2003) · Cell · doi:10.1016/s0092-8674(03)00889-4 · Cited by 820 · 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
Telomere length in early life predicts lifespan
Heidinger, B. J., Blount, J. D., Boner, W., Griffiths, K., Metcalfe, N. B., & Monaghan, P. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1113306109 · Cited by 713 · see citing works
FOXO/4E-BP Signaling in Drosophila Muscles Regulates Organism-wide Proteostasis during Aging
Demontis, F., & Perrimon, N. (2010) · Cell · doi:10.1016/j.cell.2010.10.007 · Cited by 656 · see citing works
Onken, B., & Driscoll, M. (2010) · PLoS ONE · doi:10.1371/journal.pone.0008758 · Cited by 671 · see citing works
Self-citationWidespread protein aggregation as an inherent part of aging in C. elegans
David, D. C., Ollikainen, N., Trinidad, J. C., Cary, M. P., Burlingame, A. L., & Kenyon, C. (2010) · PLoS Biology · doi:10.1371/journal.pbio.1000450 · Cited by 627 · see citing works
Apfeld, J., O'Connor, G., McDonagh, T., DiStefano, P. S., & Curtis, R. (2004) · Genes & Development · doi:10.1101/gad.1255404 · Cited by 643 · see citing works
Kell, D. B. (2009) · BMC Medical Genomics · doi:10.1186/1755-8794-2-2 · Cited by 554 · see citing works
Mitochondrial DNA mutations in human colonic crypt stem cells
Taylor, R. W., Barron, M. J., Borthwick, G. M., Gospel, A., Chinnery, P. F., Samuels, D. C., Taylor, G. A., Plusa, S. M., Needham, S. J., Greaves, L. C., et al. (2003) · Journal of Clinical Investigation · doi:10.1172/jci19435 · Cited by 530 · see citing works
The probabilistic model of Alzheimer disease: the amyloid hypothesis revised
Frisoni, G. B., Altomare, D., Thal, D. R., Ribaldi, F., van der Kant, R., Ossenkoppele, R., Blennow, K., Cummings, J., van Duijn, C., Nilsson, P. M., et al. (2022) · Nature Reviews Neuroscience · doi:10.1038/s41583-021-00533-w · Cited by 513 · see citing works
Prasanth, M. I., Sivamaruthi, B. S., Chaiyasut, C., & Tencomnao, T. (2019) · Nutrients · doi:10.3390/nu11020474 · Cited by 457 · see citing works
Genetics and the Specificity of the Aging Process
Hekimi, S., & Guarente, L. (2003) · Science · doi:10.1126/science.1082358 · Cited by 434 · see citing works
Programmed cell death in aging
Tower, J. (2015) · Ageing Research Reviews · doi:10.1016/j.arr.2015.04.002 · Cited by 426 · see citing works
Ryanodine receptor oxidation causes intracellular calcium leak and muscle weakness in aging
Andersson, D. C., Betzenhauser, M. J., Reiken, S., Meli, A. C., Umanskaya, A., Xie, W., Shiomi, T., Zalk, R., Lacampagne, A., & Marks, A. R. (2011) · Cell Metabolism · doi:10.1016/j.cmet.2011.05.014 · Cited by 424 · see citing works
Puzzles, promises and a cure for ageing
Vijg, J., & Campisi, J. (2008) · Nature · doi:10.1038/nature07216 · Cited by 407 · see citing works
Uncoupling lifespan and healthspan in <i>Caenorhabditis elegans</i> longevity mutants
Bansal, A., Zhu, L. J., Yen, K., & Tissenbaum, H. A. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1412192112 · Cited by 367 · see citing works
Metformin promotes lifespan through mitohormesis via the peroxiredoxin PRDX-2
De Haes, W., Frooninckx, L., Van Assche, R., Smolders, A., Depuydt, G., Billen, J., Braeckman, B. P., Schoofs, L., & Temmerman, L. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1321776111 · Cited by 355 · see citing works
Skeletal muscle and mortality results from the InCHIANTI study
Cesari, M., Pahor, M., Lauretani, F., Zamboni, V., Bandinelli, S., Bernabei, R., Guralnik, J. M., & Ferrucci, L. (2009) · The Journals of Gerontology Series A: Biological Sciences and Medical Sciences · doi:10.1093/gerona/gln031 · Cited by 346 · see citing works
Dietary deprivation extends lifespan in <i>Caenorhabditis elegans</i>
Lee, G. D., Wilson, M. A., Zhu, M., Wolkow, C. A., De Cabo, R., Ingram, D. K., & Zou, S. (2006) · Aging Cell · doi:10.1111/j.1474-9726.2006.00241.x · Cited by 307 · see citing works
Heterochromatin formation promotes longevity and represses ribosomal RNA synthesis
Larson, K., Yan, S.-J., Tsurumi, A., Liu, J., Zhou, J., Gaur, K., Guo, D., Eickbush, T. H., & Li, W. X. (2012) · PLoS Genetics · doi:10.1371/journal.pgen.1002473 · Cited by 284 · see citing works
Gerstbrein, B., Stamatas, G., Kollias, N., & Driscoll, M. (2005) · Aging Cell · doi:10.1111/j.1474-9726.2005.00153.x · Cited by 286 · see citing works
Self-citationAn elt-3/elt-5/elt-6 GATA transcription circuit guides aging in C. elegans
Budovskaya, Y. V., Wu, K., Southworth, L. K., Jiang, M., Tedesco, P., Johnson, T. E., & Kim, S. K. (2008) · Cell · doi:10.1016/j.cell.2008.05.044 · Cited by 253 · see citing works
HIF-1 Modulates Dietary Restriction-Mediated Lifespan Extension via IRE-1 in Caenorhabditis elegans
Chen, D., Thomas, E. L., & Kapahi, P. (2009) · PLoS Genetics · doi:10.1371/journal.pgen.1000486 · Cited by 250 · see citing works
The influence of skeletal muscle on systemic aging and lifespan
Demontis, F., Piccirillo, R., Goldberg, A. L., & Perrimon, N. (2013) · Aging Cell · doi:10.1111/acel.12126 · Cited by 238 · see citing works
Insulin/IGF-like signalling, the central nervous system and aging
Broughton, S., & Partridge, L. (2009) · Biochemical Journal · doi:10.1042/bj20082102 · Cited by 228 · see citing works
Skeletal muscle aging and the mitochondrion
Johnson, M. L., Robinson, M. M., & Nair, K. S. (2013) · Trends in Endocrinology & Metabolism · doi:10.1016/j.tem.2012.12.003 · Cited by 233 · see citing works
Neurite Sprouting and Synapse Deterioration in the Aging Caenorhabditis elegans Nervous System
Toth, M. L., Melentijevic, I., Shah, L., Bhatia, A., Lu, K., Talwar, A., Naji, H., Ibanez-Ventoso, C., Ghose, P., Jevince, A., et al. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.1494-11.2012 · Cited by 205 · see citing works
Self-citationIndoles from commensal bacteria extend healthspan
Sonowal, R., Swimm, A., Sahoo, A., Luo, L., Matsunaga, Y., Wu, Z., Bhingarde, J. A., Ejzak, E. A., Ranawade, A., Qadota, H., et al. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1706464114 · Cited by 197 · see citing works
Pharmacogenetic analysis of lithium-induced delayed aging in Caenorhabditis elegans
McColl, G., Killilea, D. W., Hubbard, A. E., Vantipalli, M. C., Melov, S., & Lithgow, G. J. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m705028200 · Cited by 202 · see citing works
Males Shorten the Life Span of <i>C. elegans</i> Hermaphrodites via Secreted Compounds
Maures, T. J., Booth, L. N., Benayoun, B. A., Izrayelit, Y., Schroeder, F. C., & Brunet, A. (2014) · Science · doi:10.1126/science.1244160 · Cited by 165 · see citing works
Rowland, A. M., Richmond, J. E., Olsen, J. G., Hall, D. H., & Bamber, B. A. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.2279-05.2006 · Cited by 159 · see citing works
Self-citationLiu, J., Zhang, B., Lei, H., Feng, Z., Liu, J., Hsu, A.-L., & Xu, X. Z. S. (2013) · Cell Metabolism · doi:10.1016/j.cmet.2013.08.007 · Cited by 154 · see citing works
Membrez, M., Migliavacca, E., Christen, S., Yaku, K., Trieu, J., Lee, A. K., Morandini, F., Giner, M. P., Stiner, J., Makarov, M. V., et al. (2024) · Nature Metabolism · doi:10.1038/s42255-024-00997-x · Cited by 148 · see citing works
Brunetti, G., Di Rosa, G., Scuto, M., Leri, M., Stefani, M., Schmitz-Linneweber, C., Calabrese, V., & Saul, N. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21072588 · Cited by 138 · see citing works
Garinis, G. A., Uittenboogaard, L. M., Stachelscheid, H., Fousteri, M., van Ijcken, W., Breit, T. M., van Steeg, H., Mullenders, L. H. F., van der Horst, G. T. J., Brüning, J. C., et al. (2009) · Nature Cell Biology · doi:10.1038/ncb1866 · Cited by 138 · see citing works
Hormone Replacement Therapy and Physical Function in Healthy Older Men. Time to Talk Hormones?
Giannoulis, M. G., Martin, F. C., Nair, K. S., Umpleby, A. M., & Sonksen, P. (2012) · Endocrine Reviews · doi:10.1210/er.2012-1002 · Cited by 132 · see citing works
Deep proteome analysis identifies age-related processes in C. elegans
Narayan, V., Ly, T., Pourkarimi, E., Murillo, A. B., Gartner, A., Lamond, A. I., & Kenyon, C. (2016) · Cell Systems · doi:10.1016/j.cels.2016.06.011 · Cited by 127 · see citing works
Sex-specific regulation of aging and apoptosis
Tower, J. (2006) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2006.05.001 · Cited by 125 · see citing works
Christian, C. J., & Benian, G. M. (2020) · Aging Cell · doi:10.1111/acel.13223 · Cited by 113 · see citing works
Asynchronous, contagious and digital aging
Rando, T. A., & Wyss-Coray, T. (2021) · Nature Aging · doi:10.1038/s43587-020-00015-1 · Cited by 121 · see citing works
Proteostasis and longevity: when does aging really begin?
Labbadia, J., & Morimoto, R. I. (2014) · F1000Prime Reports · doi:10.12703/p6-07 · Cited by 100 · see citing works
Differential patterns of apoptosis in response to aging in <i>Drosophila</i>
Zheng, J., Edelman, S. W., Tharmarajah, G., Walker, D. W., Pletcher, S. D., & Seroude, L. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0503374102 · Cited by 100 · see citing works
Telomerase and telomeres in aging theory and chronographic aging theory (Review)
Razgonova, M., Zakharenko, A., Golokhvast, K., Thanasoula, M., Sarandi, E., Nikolouzakis, K., Fragkiadaki, P., Tsoukalas, D., Spandidos, D., & Tsatsakis, A. (2020) · Molecular Medicine Reports · doi:10.3892/mmr.2020.11274 · Cited by 89 · see citing works
Proteasome activation delays aging in vitro and in vivo
Chondrogianni, N., Sakellari, M., Lefaki, M., Papaevgeniou, N., & Gonos, E. S. (2014) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2014.03.031 · Cited by 94 · see citing works
Histone methylation and aging: Lessons learned from model systems
McCauley, B. S., & Dang, W. (2014) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2014.05.008 · Cited by 93 · see citing works
Morsci, N. S., Hall, D. H., Driscoll, M., & Sheng, Z.-H. (2016) · The Journal of Neuroscience · doi:10.1523/jneurosci.2799-15.2016 · Cited by 92 · see citing works
Self-citationFisher, A. L. (2005) · Journal of the American Geriatrics Society · doi:10.1111/j.1532-5415.2005.00510.x · Cited by 87 · see citing works
Regulation of skeletal muscle mitochondrial function: genes to proteins
Lanza, I. R., & Sreekumaran Nair, K. (2010) · Acta Physiologica · doi:10.1111/j.1748-1716.2010.02124.x · Cited by 83 · see citing works
Alzheimer's disease: An acquired neurodegenerative laminopathy
Frost, B. (2016) · Nucleus · doi:10.1080/19491034.2016.1183859 · Cited by 74 · 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
A genome-scale database and reconstruction of Caenorhabditis elegans metabolism
Gebauer, J., Gentsch, C., Mansfeld, J., Schmeißer, K., Waschina, S., Brandes, S., Klimmasch, L., Zamboni, N., Zarse, K., Schuster, S., et al. (2016) · Cell Systems · doi:10.1016/j.cels.2016.04.017 · Cited by 33 · see citing works
Effect of Creatine Supplementation Dosing Strategies on Aging Muscle Performance
Chami, J., & Candow, D. G. (2019) · The Journal of nutrition, health and aging · doi:10.1007/s12603-018-1148-8 · Cited by 27 · see citing works
Recent advances in understanding the mechanisms determining longevity
Bayersdorf, R., & Schumacher, B. (2019) · F1000Research · doi:10.12688/f1000research.19610.1 · Cited by 14 · see citing works
- Authors
- Herndon, L. A., Schmeissner, P. J., Dudaronek, J. M., Brown, P. A., Listner, K. M., Sakano, Y., Paupard, M. C., Hall, D. H., & Driscoll, M.
- Affiliations
- Rutgers, The State University of New Jersey (US)
- Albert Einstein College of Medicine (US)
- Corresponding author
- Hall, David H.
- Driscoll, Monica
- Venue
- Nature
- Published
- 2002-10
- Volume
- 419
- Issue
- 6909
- Pages
- 808-814
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W2034734284
- Cited by
- 1,214
- References
- 52
- Citations by year
- 2026: 40 · 2025: 49 · 2024: 65 · 2023: 39 · 2022: 63 · 2021: 65 · 2020: 68 · 2019: 61 · 2018: 60 · 2017: 57 · 2016: 69 · 2015: 51 · 2014: 54 · 2013: 77 · 2012: 48
- FWCI
- 9.31
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- National Institutes of Health (R24OD010943)
- National Center for Research Resources (R24RR012596)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
- Health Sciences › Medicine › Physiology › Telomeres, Telomerase, and Senescence
- Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
- Keywords
- Caenorhabditis elegans, aging, lifespan extension, sarcopenia, muscle degeneration, ultrastructure, interindividual variability, cell-to-cell variability
- MeSH terms
- Aging, Animals, Gene Expression Regulation, Humans, Locomotion, Longevity, Muscles, Mutation, Nervous System Physiological Phenomena, Neurons, Organ Specificity, Phenotype, Reproduction, Stochastic Processes, Time Factors, Biomarkers, Cellular Senescence, Caenorhabditis elegans, Genes, Helminth, Phosphatidylinositol 3-Kinases, Caenorhabditis elegans Proteins
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