DAF-16/FOXO and EGL-27/GATA promote developmental growth in response to persistent somatic DNA damage
Open accessAbstract
Genome maintenance defects cause complex disease phenotypes characterized by developmental failure, cancer susceptibility and premature ageing. It remains poorly understood how DNA damage responses function during organismal development and maintain tissue functionality when DNA damage accumulates with ageing. Here we show that the FOXO transcription factor DAF-16 is activated in response to DNA damage during development, whereas the DNA damage responsiveness of DAF-16 declines with ageing. We find that in contrast to its established role in mediating starvation arrest, DAF-16 alleviates DNA-damage-induced developmental arrest and even in the absence of DNA repair promotes developmental growth and enhances somatic tissue functionality. We demonstrate that the GATA transcription factor EGL-27 co-regulates DAF-16 target genes in response to DNA damage and together with DAF-16 promotes developmental growth. We propose that EGL-27/GATA activity specifies DAF-16-mediated DNA damage responses to enable developmental progression and to prolong tissue functioning when DNA damage persists.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
In C. elegans, attenuation of insulin-like signaling enhances tissue maintenance amid DNA damage accumulation through activation of the FOXO transcription factor DAF-16.
“In C. elegans IIS attenuation enhanced tissue maintenance amid DNA damage accumulation through the activation of the FOXO transcription factor DAF-1695.”
From The central role of DNA damage in the ageing process (2021) · cites this paper as [95]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
A new mathematical model for relative quantification in real-time RT-PCR
Pfaffl, M. W. (2001) · Nucleic Acids Research · doi:10.1093/nar/29.9.e45 · Cited by 34,610 · see citing works
THE GENETICS OF CAENORHABDITIS ELEGANS
Brenner, S. (1974) · Genetics · doi:10.1093/genetics/77.1.71 · Cited by 14,984 · see citing works
Systematic functional analysis of the Caenorhabditis elegans genome using RNAi
Kamath, R. S., Fraser, A. G., Yan, D., Poulin, G. B., Durbin, R. M., Gotta, M., Kanapin, A. A., Bot, N. L., Moreno, S., Sohrmann, M., et al. (2003) · Nature · doi:10.1038/nature01278 · Cited by 3,542 · 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
A C. elegans mutant that lives twice as long as wild type
Kenyon, C., Chang, J., Gensch, E., Rudner, A., & Tabtiang, R. (1993) · Nature · doi:10.1038/366461a0 · Cited by 3,387 · see citing works
Genes that act downstream of DAF-16 to influence the lifespan of Caenorhabditis elegans
Murphy, C. T., McCarroll, S. A., Bargmann, C. I., Fraser, A., Kamath, R. S., Ahringer, J., Li, H., & Kenyon, C. (2003) · Nature · doi:10.1038/nature01789 · Cited by 2,280 · see citing works
Quantifying similarity between motifs
Gupta, S., Stamatoyannopoulos, J. A., Bailey, T. L., & Noble, W. S. (2007) · Genome Biology · doi:10.1186/gb-2007-8-2-r24 · Cited by 2,058 · 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
Ogg, S., Paradis, S., Gottlieb, S., Patterson, G. I., Lee, L., Tissenbaum, H. A., & Ruvkun, G. (1997) · Nature · doi:10.1038/40194 · Cited by 1,935 · see citing works
Genomic Instability and Aging-like Phenotype in the Absence of Mammalian SIRT6
Mostoslavsky, R., Chua, K. F., Lombard, D. B., Pang, W. W., Fischer, M. R., Gellon, L., Liu, P., Mostoslavsky, G., Franco, S., Murphy, M. M., et al. (2006) · Cell · doi:10.1016/j.cell.2005.11.044 · Cited by 1,637 · see citing works
Regulation of aging and age-related disease by DAF-16 and heat-shock factor
Hsu, A.-L., Murphy, C. T., & Kenyon, C. (2003) · Science · doi:10.1126/science.1083701 · Cited by 1,513 · see citing works
Genetic pathways that regulate ageing in model organisms
Guarente, L., & Kenyon, C. J. (2000) · Nature · doi:10.1038/35041700 · Cited by 1,337 · see citing works
Henderson, S. T., & Johnson, T. E. (2001) · Current Biology · doi:10.1016/s0960-9822(01)00594-2 · Cited by 949 · see citing works
Direct inhibition of the longevity-promoting factor SKN-1 by insulin-like signaling in C. elegans
Tullet, J. M. A., Hertweck, M., An, J. H., Baker, J., Hwang, J. Y., Liu, S., Oliveira, R. P., Baumeister, R., & Blackwell, T. K. (2008) · Cell · doi:10.1016/j.cell.2008.01.030 · Cited by 923 · see citing works
Morris, J. Z., Tissenbaum, H. A., & Ruvkun, G. (1996) · Nature · doi:10.1038/382536a0 · Cited by 891 · 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
DNA damage checkpoints: from initiation to recovery or adaptation
Bartek, J., & Lukas, J. (2007) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2007.02.009 · Cited by 784 · see citing works
SKN-1 links C. elegans mesendodermal specification to a conserved oxidative stress responsePreprint
An, J. H., & Blackwell, T. K. (2003) · Genes & Development · doi:10.1101/gad.1107803 · Cited by 722 · see citing works
Furuyama, T., Nakazawa, T., Nakano, I., & Mori, N. (2000) · Biochemical Journal · doi:10.1042/0264-6021:3490629 · Cited by 672 · see citing works
A new progeroid syndrome reveals that genotoxic stress suppresses the somatotroph axis
Niedernhofer, L. J., Garinis, G. A., Raams, A., Lalai, A. S., Robinson, A. R., Appeldoorn, E., Odijk, H., Oostendorp, R., Ahmad, A., van Leeuwen, W., et al. (2006) · Nature · doi:10.1038/nature05456 · Cited by 669 · see citing works
Gartner, A., Milstein, S., Ahmed, S. C., Hodgkin, J., & Hengartner, M. O. (2000) · Molecular Cell · doi:10.1016/s1097-2765(00)80438-4 · Cited by 513 · see citing works
Disorders of nucleotide excision repair: the genetic and molecular basis of heterogeneity
Cleaver, J. E., Lam, E. T., & Revet, I. (2009) · Nature Reviews Genetics · doi:10.1038/nrg2663 · Cited by 428 · cited 1× · see citing works
“We also included mutants of age-1, the PI(3) kinase acting downstream of DAF-2 (ref.”
A Genetic Pathway Conferring Life Extension and Resistance to UV Stress in Caenorhabditis elegans
Murakami, S., & Johnson, T. E. (1996) · Genetics · doi:10.1093/genetics/143.3.1207 · Cited by 394 · see citing works
Gottlieb, S., & Ruvkun, G. (1994) · Genetics · doi:10.1093/genetics/137.1.107 · Cited by 387 · see citing works
Reboul, J., Vaglio, P., Rual, J.-F. M., Lamesch, P., Martinez, M., Armstrong, C. M., Li, S., Jacotot, L., Bertin, N., Janky, R., et al. (2003) · Nature Genetics · doi:10.1038/ng1140 · Cited by 379 · see citing works
Advances in Chemical Carcinogenesis: A Historical Review and Prospective
Loeb, L. A., & Harris, C. C. (2008) · Cancer Research · doi:10.1158/0008-5472.can-08-2852 · Cited by 314 · see citing works
AKT/FOXO Signaling Enforces Reversible Differentiation Blockade in Myeloid Leukemias
Sykes, S., Lane, S. W., Bullinger, L., Kalaitzidis, D., Yusuf, R., Saez, B., Ferraro, F., Mercier, F., Singh, H., Brumme, K., et al. (2011) · Cell · doi:10.1016/j.cell.2011.07.032 · Cited by 281 · see citing works
RSAT: regulatory sequence analysis tools
Thomas‐Chollier, M., Sand, O., Turatsinze, J., Janky, R., Defrance, M., Vervisch, E., Brohée, S., & van Helden, J. (2008) · Nucleic Acids Research · doi:10.1093/nar/gkn304 · Cited by 278 · see citing works
Age to survive: DNA damage and aging
Schumacher, B., Garinis, G. A., & Hoeijmakers, J. H. J. (2008) · Trends in Genetics · doi:10.1016/j.tig.2007.11.004 · Cited by 255 · 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
Baugh, L. R., & Sternberg, P. W. (2006) · Current Biology · doi:10.1016/j.cub.2006.03.021 · Cited by 249 · see citing works
van der Pluijm, I., Garinis, G. A., Brandt, R. M. C., Gorgels, T. G. M. F., Wijnhoven, S., Diderich, K. E. M., de Wit, J., Mitchell, J. R., van Oostrom, C., Beems, R. B., et al. (2006) · PLoS Biology · doi:10.1371/journal.pbio.0050002 · Cited by 237 · see citing works
WormBase: a comprehensive data resource for Caenorhabditis biology and genomics
Chen, N. (2004) · Nucleic Acids Research · doi:10.1093/nar/gki066 · Cited by 190 · see citing works
RNA polymerase II bypass of oxidative DNA damage is regulated by transcription elongation factors
Charlet‐Berguerand, N., Feuerhahn, S., Kong, S. E., Ziserman, H., Conaway, J. W., Conaway, R. C., & Egly, J. (2006) · The EMBO Journal · doi:10.1038/sj.emboj.7601403 · Cited by 189 · see citing works
Mitochondrial SKN-1/Nrf Mediates a Conserved Starvation Response
Paek, J., Lo, J. Y., Narasimhan, S. D., Nguyen, T. N., Glover-Cutter, K. M., Robida-Stubbs, S., Suzuki, T., Yamamoto, M. P., Blackwell, T. K., & Curran, S. P. (2012) · Cell Metabolism · doi:10.1016/j.cmet.2012.09.007 · Cited by 178 · see citing works
Emerging roles of MTA family members in human cancers
Kumar, R. A. (2003) · Seminars in Oncology · doi:10.1053/j.seminoncol.2003.08.005 · Cited by 177 · see citing works
Johnson, T. E., Henderson, S. T., Murakami, S., de Castro, E., de Castro, S. H., Cypser, J. R., Rikke, B. A., Tedesco, P., & Link, C. D. (2002) · Journal of Inherited Metabolic Disease · doi:10.1023/a:1015677828407 · Cited by 174 · see citing works
Zhang, P., Judy, M. E., Lee, S., & Kenyon, C. J. (2013) · Cell Metabolism · doi:10.1016/j.cmet.2012.12.013 · Cited by 170 · see citing works
RNA Pol II Accumulates at Promoters of Growth Genes During Developmental Arrest
Baugh, L. R., DeModena, J. A., & Sternberg, P. W. (2009) · Science · doi:10.1126/science.1169628 · Cited by 165 · see citing works
NPHP4, a cilia-associated protein, negatively regulates the Hippo pathway
Habbig, S., Bartram, M. P., Müller, R., Schwarz, R., Andriopoulos, N., Chen, S., Sägmüller, J. G., Hoehne, M., Burst, V. R., Liebau, M. C., et al. (2011) · The Journal of Cell Biology · doi:10.1083/jcb.201009069 · Cited by 162 · see citing works
Self-citationTemporal Dynamics and Linkage Disequilibrium in NaturalCaenorhabditis elegansPopulations
Barrière, A., & Félix, M. (2007) · Genetics · doi:10.1534/genetics.106.067223 · Cited by 162 · see citing works
Nicolson, G. L., Nawa, A., Toh, Y., Taniguchi, S., Nishimori, K., & Moustafa, A. S. (2003) · Clinical & Experimental Metastasis · doi:10.1023/a:1022534217769 · Cited by 154 · see citing works
Genomes Optimize Reproduction: Aging as a Consequence of the Developmental Program
de Magalhães, J. P., & Church, G. M. (2005) · Physiology · doi:10.1152/physiol.00010.2005 · Cited by 152 · 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
Self-citationLans, H., Marteijn, J. A. F., Schumacher, B., Hoeijmakers, J. H. J., Jansen, G., & Vermeulen, W. (2010) · PLoS Genetics · doi:10.1371/journal.pgen.1000941 · Cited by 131 · see citing works
Self-citationNovel aspects of heat shock factors: DNA recognition, chromatin modulation and gene expression
Sakurai, H., & Enoki, Y. (2010) · FEBS Journal · doi:10.1111/j.1742-4658.2010.07829.x · Cited by 129 · see citing works
Luijsterburg, M. S., von Bornstaedt, G., Gourdin, A. M., Politi, A. Z., Moné, M. J., Warmerdam, D. O., Goedhart, J., Vermeulen, W., van Driel, R., & Höfer, T. (2010) · Journal of Cell Biology · doi:10.1083/jcb.200909175 · Cited by 121 · see citing works
A soma-to-germline transformation in long-lived Caenorhabditis elegans mutants
Curran, S. P., Wu, X., Riedel, C. G., & Ruvkun, G. (2009) · Nature · doi:10.1038/nature08106 · Cited by 120 · see citing works
Solari, F., Bateman, A. G., & Ahringer, J. (1999) · Development · doi:10.1242/dev.126.11.2483 · Cited by 112 · see citing works
Stergiou, L., Doukoumetzidis, K., Sendoel, A., & Hengartner, M. O. (2007) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4402115 · Cited by 110 · see citing works
Herman, M. A., Ch'ng, Q.-L., Hettenbach, S. M., Ratliff, T. M., Kenyon, C. J., & Herman, R. K. (1999) · Development · doi:10.1242/dev.126.5.1055 · Cited by 70 · see citing works
Genome maintenance and transcription integrity in aging and disease
Wolters, S., & Schumacher, B. (2013) · Frontiers in Genetics · doi:10.3389/fgene.2013.00019 · Cited by 69 · see citing works
Self-citationBoyd, W. A., Crocker, T. L., Rodriguez, A. M., Leung, M. C. K., Lehmann, D. W., Freedman, J. H., Houten, B. V., & Meyer, J. N. (2009) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/j.mrfmmm.2009.10.008 · Cited by 54 · see citing works
Ch'ng, Q.-L., & Kenyon, C. J. (1999) · Development · doi:10.1242/dev.126.15.3303 · Cited by 51 · see citing works
Differential repair of the two major UV-induced photolesions in trichothiodystrophy fibroblasts
Riou, L., Eveno, E., van Hoffen, A., van Zeeland, A. A., Sarasin, A., & Mullenders, L. H. F. (2004) · Cancer Research · doi:10.1158/0008-5472.can-03-2070 · Cited by 46 · see citing works
Environmental UV Radiation: Impact on Ecosystems and Human Health and Predictive Models
Ghetti, F., Bornman, J. F., & Checcucci, G. (2006) · NATO science series. Series IV, Earth and environmental sciences · doi:10.1007/1-4020-3697-3 · Cited by 45 · see citing works
Requirement of MTA1 in ATR-mediated DNA Damage Checkpoint Function
Li, D., Ohshiro, K., Khan, M. N., & Kumar, R. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.085258 · Cited by 43 · see citing works
Xu, X., & Kim, S. K. (2012) · PLoS Genetics · doi:10.1371/journal.pgen.1003108 · Cited by 29 · see citing works
A Novel Heme-responsive Element Mediates Transcriptional Regulation in Caenorhabditis elegans
Sinclair, J. W., & Hamza, I. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.167619 · Cited by 25 · see citing works
Eldonet — European Light Dosimeter Network
Häder, D. P., & Lebert, M. (2006) · NATO science series. Series IV, Earth and environmental sciences · doi:10.1007/1-4020-3697-3_8 · Cited by 16 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
The central role of DNA damage in the ageing process
Schumacher, B., Pothof, J., Vijg, J., & Hoeijmakers, J. H. J. (2021) · Nature · doi:10.1038/s41586-021-03307-7 · Cited by 907 · see citing works
Self-citationDNA damage responses and p53 in the aging process
Ou, H.-L., & Schumacher, B. (2018) · Blood · doi:10.1182/blood-2017-07-746396 · Cited by 377 · see citing works
Self-citationFoxO integration of insulin signaling with glucose and lipid metabolism
Lee, S., & Dong, H. H. (2017) · Journal of Endocrinology · doi:10.1530/joe-17-0002 · Cited by 361 · see citing works
Altıntaş, Ö., Park, S., & Lee, S. (2016) · BMB Reports · doi:10.5483/bmbrep.2016.49.2.261 · Cited by 205 · see citing works
Lin, X.-X., Sen, I., Janssens, G. E., Zhou, X., Fonslow, B. R., Edgar, D., Stroustrup, N., Swoboda, P., Yates, J. R., Ruvkun, G., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-06624-0 · Cited by 170 · see citing works
BiT age: A transcriptome‐based aging clock near the theoretical limit of accuracy
Meyer, D. H., & Schumacher, B. (2021) · Aging Cell · doi:10.1111/acel.13320 · Cited by 165 · see citing works
Self-citationSystemic DNA damage responses in aging and diseases
Ribezzo, F., Shiloh, Y., & Schumacher, B. (2016) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2015.12.005 · Cited by 116 · see citing works
Self-citationIakovou, E., & Kourti, M. (2022) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2022.827900 · Cited by 113 · see citing works
Principles of the Molecular and Cellular Mechanisms of Aging
da Silva, P. F. L., & Schumacher, B. (2021) · Journal of Investigative Dermatology · doi:10.1016/j.jid.2020.11.018 · Cited by 99 · see citing works
Self-citationSon, H. G., Seo, M., Ham, S., Hwang, W., Lee, D.-Y., An, S. W. A., Artan, M., Seo, K., Kaletsky, R. L., Arey, R. N., et al. (2017) · Nature Communications · doi:10.1038/ncomms14749 · Cited by 91 · see citing works
FOXOs: masters of the equilibrium
Gui, T., & Burgering, B. M. T. (2021) · FEBS Journal · doi:10.1111/febs.16221 · Cited by 83 · see citing works
Culberson, J. W., Kopel, J. J., Sehar, U., & Reddy, P. H. (2023) · Ageing Research Reviews · doi:10.1016/j.arr.2023.102001 · Cited by 88 · see citing works
The DREAM complex functions as conserved master regulator of somatic DNA-repair capacities
Bujarrabal-Dueso, A., Sendtner, G., Meyer, D. H., Chatzinikolaou, G., Stratigi, K., Garinis, G. A., & Schumacher, B. (2023) · Nature Structural & Molecular Biology · doi:10.1038/s41594-023-00942-8 · Cited by 78 · see citing works
Self-citationCaenorhabditis elegans as a Model System to Study Human Neurodegenerative Disorders
Roussos, A., Kitopoulou, K., Borbolis, F., & Palikaras, K. (2023) · Biomolecules · doi:10.3390/biom13030478 · Cited by 76 · see citing works
DNA repair, recombination, and damage signaling
Gartner, A., & Engebrecht, J. (2021) · Genetics · doi:10.1093/genetics/iyab178 · Cited by 73 · see citing works
Tissue specific response to DNA damage: C. elegans as role model
Lans, H., & Vermeulen, W. (2015) · DNA repair · doi:10.1016/j.dnarep.2015.04.025 · Cited by 58 · see citing works
DNA damage responses in ageing
da Silva, P. F. L., & Schumacher, B. (2019) · Open Biology · doi:10.1098/rsob.190168 · Cited by 55 · see citing works
Self-citationDNA Damage Response and Metabolic Reprogramming in Health and Disease
Chatzidoukaki, O., Goulielmaki, E., Schumacher, B., & Garinis, G. A. (2020) · Trends in Genetics · doi:10.1016/j.tig.2020.06.018 · Cited by 54 · see citing works
Self-citationH3K4me2 regulates the recovery of protein biosynthesis and homeostasis following DNA damage
Wang, S., Meyer, D. H., & Schumacher, B. (2020) · Nature Structural & Molecular Biology · doi:10.1038/s41594-020-00513-1 · Cited by 49 · see citing works
Self-citationLocal and long-range activation of innate immunity by infection and damage in C. elegans
Ewbank, J. J., & Pujol, N. (2015) · Current Opinion in Immunology · doi:10.1016/j.coi.2015.09.005 · Cited by 53 · see citing works
Mitochondrial function in skeletal myofibers is controlled by a TRF2‐SIRT3 axis over lifetime
Robin, J. D., Burbano, M. S. J., Peng, H., Croce, O., Thomas, J. L., Laberthonnìère, C., Renault, V. M., Lototska, L., Pousse, M., Tessier, F., et al. (2020) · Aging Cell · doi:10.1111/acel.13097 · Cited by 51 · see citing works
Miles, J., Scherz‐Shouval, R., & van Oosten‐Hawle, P. (2019) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2019.06.009 · Cited by 51 · see citing works
Molecular pathology of rare progeroid diseases
Rieckher, M., Garinis, G. A., & Schumacher, B. (2021) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2021.06.011 · Cited by 48 · see citing works
Self-citationMultilayered Reprogramming in Response to Persistent DNA Damage in C. elegans
Edifizi, D., Nolte, H., Babu, V. V. S., Castells‐Roca, L., Mueller, M. M., Brodesser, S., Krüger, M., & Schumacher, B. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.08.028 · Cited by 50 · see citing works
Self-citationEffector and regulator: Diverse functions of C. elegans C-type lectin-like domain proteins
Pees, B., Yang, W., Kloock, A., Petersen, C., Peters, L., Li, F., Friedrichsen, M., Butze, S., Zárate-Potes, A., Hinrich Schulenburg, Y., et al. (2021) · PLoS Pathogens · doi:10.1371/journal.ppat.1009454 · Cited by 49 · see citing works
Rieckher, M., Markaki, M., Princz, A., Schumacher, B., & Tavernarakis, N. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.09.009 · Cited by 46 · see citing works
Self-citationGraphene, other carbon nanomaterials and the immune system: toward nanoimmunity-by-design
Gazzi, A., Fusco, L., Orecchioni, M., Ferrari, S., Franzoni, G., Yan, J. S., Rieckher, M., Peng, G., Lucherelli, M. A., Vacchi, I. A., et al. (2020) · Journal of Physics Materials · doi:10.1088/2515-7639/ab9317 · Cited by 46 · see citing works
Self-citationGATA3 recruits UTX for gene transcriptional activation to suppress metastasis of breast cancer
Yu, W., Huang, W., Yang, Y., Qiu, R., Zeng, Y., Hou, Y., Sun, G., Shi, H., Leng, S., Feng, D., et al. (2019) · Cell Death and Disease · doi:10.1038/s41419-019-2062-7 · Cited by 46 · see citing works
Gurkar, A. U., Robinson, A. R., Cui, Y., Li, X., Allani, S. K., Webster, A., Muravia, M., Fallahi, M., Weissbach, H., Robbins, P. D., et al. (2018) · Redox Biology · doi:10.1016/j.redox.2018.06.005 · Cited by 43 · see citing works
A C. elegans model for neurodegeneration in Cockayne syndrome
Lopes, A. F. C., Bożek, K., Herholz, M., Trifunović, A., Rieckher, M., & Schumacher, B. (2020) · Nucleic Acids Research · doi:10.1093/nar/gkaa795 · Cited by 43 · see citing works
Self-citationEdifizi, D., & Schumacher, B. (2015) · Biomolecules · doi:10.3390/biom5031855 · Cited by 42 · see citing works
Self-citationStem Cell DNA Damage and Genome Mutation in the Context of Aging and Cancer InitiationPreprint
Zouabi, L. A., & Bardin, A. J. (2020) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a036210 · Cited by 37 · see citing works
Somatic Niche Cells Regulate the CEP-1/p53-Mediated DNA Damage Response in Primordial Germ Cells.
Ou, H., Kim, C. S., Uszkoreit, S., Wickström, S. A., & Schumacher, B. (2019) · Developmental Cell · doi:10.1016/j.devcel.2019.06.012 · Cited by 33 · see citing works
Self-citationTissue-Specific DNA Repair Activity of ERCC-1/XPF-1
Sabatella, M., Thijssen, K. L., Davó-Martínez, C., Vermeulen, W., & Lans, H. (2021) · Cell Reports · doi:10.1016/j.celrep.2020.108608 · Cited by 36 · see citing works
Yang, W., Petersen, C., Pees, B., Zimmermann, J., Waschina, S., Dirksen, P., Rosenstiel, P. C., Tholey, A., Leippe, M., Dierking, K., et al. (2019) · Frontiers in Microbiology · doi:10.3389/fmicb.2019.01793 · Cited by 32 · see citing works
Rieckher, M., Bujarrabal-Dueso, A., Doll, M. A., Soltanmohammadi, N., & Schumacher, B. (2017) · Journal of Cellular Physiology · doi:10.1002/jcp.25979 · Cited by 32 · see citing works
Self-citationHamsanathan, S., Anthonymuthu, T., Han, S., Shinglot, H., Siefken, E., Sims, A., Sen, P., Pepper, H. L., Snyder, N. W., Bayir, H., et al. (2022) · Science Advances · doi:10.1126/sciadv.abl6083 · Cited by 30 · see citing works
RNA interference may result in unexpected phenotypes in Caenorhabditis elegans
De‐Souza, E. A., Camara, H., Salgueiro, W. G., Moro, R. D. P., Knittel, T. L., Tonon-da-Silva, G., Pinto, S., Pinca, A. P. F., Antebi, A., Pasquinelli, A. E., et al. (2019) · Nucleic Acids Research · doi:10.1093/nar/gkz154 · Cited by 28 · see citing works
DAF-16 and SMK-1 Contribute to Innate Immunity During Adulthood in Caenorhabditis elegans
McHugh, D. R., Koumis, E., Jacob, P., Goldfarb, J. A., Schlaubitz-Garcia, M., Bennani, S., Regan, P., Patel, P., & Youngman, M. J. (2020) · G3 Genes Genomes Genetics · doi:10.1534/g3.120.401166 · Cited by 28 · see citing works
Wilson, D. M., Rieckher, M., Williams, A. B., & Schumacher, B. (2017) · Nucleic Acids Research · doi:10.1093/nar/gkx660 · Cited by 26 · see citing works
Self-citationMPK-1/ERK pathway regulates DNA damage response during development through DAF-16/FOXO
Bianco, J. N., & Schumacher, B. (2018) · Nucleic Acids Research · doi:10.1093/nar/gky404 · Cited by 26 · see citing works
Self-citationFan, X., Zeng, Y. Y., Fan, Z., Cui, L., Song, W., Wu, Q., Gao, Y., Yang, D., Mao, X., Zeng, B., et al. (2020) · Aging · doi:10.18632/aging.202156 · Cited by 26 · see citing works
Deng, J., Bai, X., Tang, H., & Pang, S. (2020) · Journal of Biological Chemistry · doi:10.1074/jbc.ra120.016083 · Cited by 24 · see citing works
Rieckher, M., Gallrein, C., Alquézar-Artieda, N., Bourached-Silva, N., Vaddavalli, P. L., Mares, D., Backhaus, M., Blindauer, T., Greger, K., Wiesner, E., et al. (2024) · Nucleic Acids Research · doi:10.1093/nar/gkae519 · Cited by 25 · see citing works
Self-citationCaenorhabditis elegansfor research on cancer hallmarks
Cerón, J. (2023) · Disease Models & Mechanisms · doi:10.1242/dmm.050079 · Cited by 22 · see citing works
Quality control mechanisms in cellular and systemic DNA damage responses
Ermolaeva, M., Dakhovnik, A., & Schumacher, B. (2015) · Ageing Research Reviews · doi:10.1016/j.arr.2014.12.009 · Cited by 22 · see citing works
Self-citationDNA repair deficiencies and neurodegeneration
Ropert, B., Gallrein, C., & Schumacher, B. (2024) · DNA repair · doi:10.1016/j.dnarep.2024.103679 · Cited by 21 · see citing works
Self-citationGuédon, R., Maremonti, E., Armant, O., Galas, S., Brede, D. A., & Lecomte-Pradines, C. (2021) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2021.112793 · Cited by 21 · see citing works
Genome instability: Linking ageing and brain degeneration
Barzilai, A., Schumacher, B., & Shiloh, Y. (2016) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2016.03.011 · Cited by 20 · see citing works
Self-citationAnge, J. S., Weng, Y., Kaletsky, R. L., Stevenson, M. E., Moore, R. S., Zhou, S., & Murphy, C. T. (2024) · Cell Genomics · doi:10.1016/j.xgen.2024.100720 · Cited by 20 · see citing works
DNA damage responses and stress resistance: Concepts from bacterial SOS to metazoan immunity
Williams, A. B., & Schumacher, B. (2016) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2016.09.007 · Cited by 20 · see citing works
Self-citationFOXOs Maintaining the Equilibrium for Better or for Worse
van Doeselaar, S., & Burgering, B. M. T. (2018) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2017.10.003 · Cited by 17 · see citing works
Servello, F. A., Fernandes, R., Eder, M., Harris, N., Martin, O. M. F., Oswal, N., Lindberg, A., Derosiers, N., Sengupta, P., Stroustrup, N., et al. (2022) · eLife · doi:10.7554/elife.78941 · Cited by 17 · see citing works
Regulation and functions of membrane lipids: Insights from Caenorhabditis elegans
Koyiloth, M., & Gummadi, S. N. (2022) · BBA Advances · doi:10.1016/j.bbadva.2022.100043 · Cited by 16 · see citing works
Zhao, Q., Rangan, R., Weng, S., Özdemir, C., & Cenik, E. S. (2023) · PLoS Biology · doi:10.1371/journal.pbio.3002276 · Cited by 13 · see citing works
Du, L., Tracy, S., & Rifkin, S. A. (2016) · Developmental Biology · doi:10.1016/j.ydbio.2016.02.013 · Cited by 15 · 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
Scope of 2D materials for immune response-a review
Hossain, N., Chowdhury, M. A., Sultana, S., & Nandee, R. (2022) · Results in Engineering · doi:10.1016/j.rineng.2022.100413 · Cited by 14 · see citing works
A C. elegans homolog for the UV-hypersensitivity syndrome disease gene UVSSA
Babu, V. V. S., & Schumacher, B. (2016) · DNA repair · doi:10.1016/j.dnarep.2016.03.008 · Cited by 14 · see citing works
Self-citationMony, V. K., Drangowska-Way, A., Albert, R., Harrison, E., Ghaddar, A., Horak, M. K., Ke, W., & O’Rourke, E. J. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2104832118 · Cited by 13 · see citing works
Yan, J., Bhanshali, F., Shuzenji, C., Mendenhall, T. T., Taylor, S. K. B., Ermakova, G., Cheng, X., Bai, P., Diwan, G., Seraj, D., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-56766-1 · Cited by 11 · see citing works
Zhang, X., Li, W., Feng, K., Xiao, J., Du, J., Cao, Y., & Chen, Y. (2021) · Experimental Gerontology · doi:10.1016/j.exger.2021.111388 · Cited by 11 · see citing works
Identification of polymorphisms in cancer patients that differentially affect survival with age
Doherty, A., Kernogitski, Y., Kulminski, A. M., & de Magalhães, J. P. (2017) · Aging · doi:10.18632/aging.101305 · Cited by 11 · see citing works
Light Sheet Microscopy to Measure Protein Dynamics
Rieckher, M. (2016) · Journal of Cellular Physiology · doi:10.1002/jcp.25451 · Cited by 10 · see citing works
Longevity Regulation by Insulin/IGF-1 Signalling
An, S. W. A., Artan, M., Park, S., Altıntaş, Ö., & Lee, S. (2016) · Healthy ageing and longevity · doi:10.1007/978-3-319-44703-2_4 · Cited by 8 · see citing works
DNA damage signals from somatic uterine tissue arrest oogenesis through activated DAF-16
Sarkar, G. C., Rautela, U., Goyala, A., Datta, S., Anand, N., Singh, A., Singh, P., Chamoli, M., & Mukhopadhyay, A. (2023) · Development · doi:10.1242/dev.201472 · Cited by 9 · see citing works
Lohmann, G., Vasyutina, E. L., Bloehdorn, J., Reinart, N., Schneider, J. I., Babu, V. V. S., Knittel, G., Crispatzu, G., Mayer, P., Prinz, C., et al. (2016) · Leukemia · doi:10.1038/leu.2016.294 · Cited by 9 · see citing works
Self-citationNontranscriptional Function of FOXO1/DAF-16 Contributes to Translesion DNA Synthesis
Daitoku, H., Kaneko, Y., Yoshimochi, K., Matsumoto, K., Araoi, S., Sakamaki, J.-I., Takahashi, Y., & Fukamizu, A. (2016) · Molecular and Cellular Biology · doi:10.1128/mcb.00265-16 · Cited by 9 · see citing works
Development of a next-generation endogenous OCT4 inducer and its anti-aging effect in vivo
Kang, H. C., Hasselbeck, S., Taškova, K., Wang, N., van Oosten, L. N., Mrowka, R., Utikal, J. S., Andrade-Navarro, M. A., Wang, J., Wölfl, S., et al. (2023) · European Journal of Medicinal Chemistry · doi:10.1016/j.ejmech.2023.115513 · Cited by 7 · see citing works
Proximity labeling of DAF-16 FOXO highlights aging regulatory proteins
Artan, M., Schoen, H., & de Bono, M. (2025) · Nature Communications · doi:10.1038/s41467-025-66409-0 · Cited by 6 · see citing works
Khanna, A., Sellegounder, D., Kumar, J., Chamoli, M., Vargas, M., Chinta, S. J., Rane, A., Nelson, C. S., Peiris, T. H., Brem, R. B., et al. (2021) · Aging Cell · doi:10.1111/acel.13351 · Cited by 6 · see citing works
Omics Approaches for Identifying Physiological Adaptations to Genome Instability in Aging
Edifizi, D., & Schumacher, B. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18112329 · Cited by 6 · see citing works
Self-citationLongevity through DNA damage tolerance
Castells‐Roca, L., Mueller, M. M., & Schumacher, B. (2015) · Cell Cycle · doi:10.1080/15384101.2015.1006543 · Cited by 5 · see citing works
Self-citationFreeman, T. F., Zhao, Q., Surya, A., Rothe, R., & Cenik, E. S. (2023) · BMC Genomics · doi:10.1186/s12864-023-09576-y · Cited by 5 · see citing works
Lin, X., Shao, C., Elsherbiny, S. M., & Huang, Q. (2024) · Photochemistry and Photobiology · doi:10.1111/php.13958 · Cited by 5 · see citing works
Rochester, J. D., Tanner, P. C., Sharp, C. S., Andralojc, K. M., & Updike, D. L. (2017) · Biology Open · doi:10.1242/bio.027987 · Cited by 5 · see citing works
Sharika, R., Verma, K., Tencomnao, T., & Chuchawankul, S. (2024) · Nutrition and Healthy Aging · doi:10.3233/nha-220200 · Cited by 4 · see citing works
Age Deceleration and Reversal Gene Patterns in Dauer Diapause
Totska, K., Barata, J. C. V. V., Sandt, W., Meyer, D. H., & Schumacher, B. (2025) · Aging Cell · doi:10.1111/acel.70253 · Cited by 3 · see citing works
Self-citationFoxO1: A Conductor of Insulin Signaling to Glucose and Lipid Metabolism
Zhang, T., & Dong, H. H. (2015) · Springer eBooks · doi:10.1007/978-3-319-25065-6_4 · Cited by 3 · see citing works
Marchal, L., Hamsanathan, S., Karthikappallil, R., Han, S., Shinglot, H., & Gurkar, A. U. (2021) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2021.111573 · Cited by 3 · see citing works
In memoriam Olivier Toussaint – Stress-induced premature senescence and the role of DNA damage
Bürkle, A. (2017) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2017.06.003 · Cited by 4 · see citing works
Genome Stability in Caenorhabditis elegans
Rieckher, M., Lopes, A. F. C., & Schumacher, B. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-803309-8.00011-2 · Cited by 2 · see citing works
Self-citationGurkar, A. U., Gill, M. S., & Niedernhofer, L. J. (2016) · Healthy ageing and longevity · doi:10.1007/978-3-319-44703-2_11 · Cited by 2 · see citing works
Zhao, Q., Rangan, R., Weng, S., Özdemir, C., & Cenik, E. S. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.09.28.509886 · Cited by 2 · see citing works
Inactivation of the DREAM complex mimics the molecular benefits of sleepPreprint
Valentim, I. S., Romero-Expósito, F. J., Schwab, K., Bayar, M., Tauassarova, A., Riege, K., Lange, L., Engmann, O., Fischer, M., Olmedo, M., et al. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.06.26.600859 · Cited by 2 · see citing works
Self-citationvan der Woude, M., Thijssen, K. L., Sabatella, M., Marteijn, J. A. F., Vermeulen, W., & Lans, H. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.03.21.644538 · Cited by 2 · see citing works
Genome stability in Caenorhabditis elegans
Kovalchuk, I. (2021) · Elsevier eBooks · doi:10.1016/b978-0-323-85679-9.00011-8 · Cited by 1 · see citing works
Nunes, I. J. G., Feltes, B. C., David, M. Z., & Dorn, M. (2022) · Journal of Biomedical Informatics · doi:10.1016/j.jbi.2022.104053 · Cited by 1 · see citing works
Wan, C., & Barton, C. (2024) · ACM Symposium on Applied Computing · doi:10.1145/3605098.3635943 · Cited by 1 · see citing works
Uszkoreit, S., Meyer, D. H., Rechavi, O., & Schumacher, B. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.07.19.500657 · Cited by 1 · see citing works
Self-citationDAF-16/FOXO maintains genome integrity following genotoxic stressPreprint
Rautela, U., Devendran, O., Sarkar, G. C., Ranjisha, K. R., Mittal, R., Goyala, A., & Mukhopadhyay, A. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.10.27.684284 · Cited by 1 · see citing works
Wormpath: searching for molecular interaction networks in Caenorhabditis elegans
Frommolt, P., & Schumacher, B. (2015) · Source Code for Biology and Medicine · doi:10.1186/s13029-015-0034-6
Self-citationClosing the Circle: Stem Cell Rejuvenation and Longevity
Florian, M. C., & Geiger, H. (2015) · Springer eBooks · doi:10.1007/978-3-7091-1232-8_16
Functional Consequences of Embryonic Stem Cell- Specific Alternative Splicing
Nachman, E. N. (2015) · TSpace (University of Toronto)
Genes, Aging, and Parkinson’s Disease
Milanese, C., & Mastroberardino, P. G. (2017) · Royal Society of Chemistry eBooks · doi:10.1039/9781782622888-00389
Studies on Molecular Basis for FOXO1-DNA Damage Responses
悠太, 金. (2016) · Terrestrial Environment Research Center (University of Tsukuba)
Schumacher, B. (2019) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.733897159.793563342
Self-citationLee, S., & Park, H. H. (2019) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.734291273.793555709
Schumacher, B. (2019) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.734291273.793563332
Self-citation
- Authors
- Mueller, M. M., Castells-Roca, L., Babu, V., Ermolaeva, M. A., Müller, R.-U., Frommolt, P., Williams, A. B., Greiss, S., Schneider, J. I., Benzing, T., Schermer, B., & Schumacher, B.
- Affiliations
- University of Cologne (DE)
- Corresponding author
- Schumacher, Björn
- ORCID
- Venue
- Nature Cell Biology
- Published
- 2014-11-24
- Volume
- 16
- Issue
- 12
- Pages
- 1168-1179
- ISSN
- 1465-7392 (ISSN-L)
- 1476-4679
- PMC
- PMC4250074
- OpenAlex
- W2094033379
- Cited by
- 108
- References
- 60
- Citations by year
- 2026: 4 · 2025: 6 · 2024: 7 · 2023: 9 · 2022: 9 · 2021: 15 · 2020: 10 · 2019: 10 · 2018: 5 · 2017: 11 · 2016: 13 · 2015: 9
- FWCI
- 4.51
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Cell Biology (publishedVersion)
- PubMed (publishedVersion)
- Kölner Universitäts PublikationsServer (Universität zu Köln) (publishedVersion)
- PubMed Central (acceptedVersion)
- Edinburgh Research Explorer (University of Edinburgh) (submittedVersion, other-oa)
- Funders
- Deutsche Forschungsgemeinschaft (SFB 832, SFB829, KFO286, SFB 670, P40 OD010440)
- Bundesministerium für Bildung und Forschung (SFB 670)
- Deutsche Krebshilfe (SFB832, 109453)
- National Institutes of Health (OD010440, P40OD010440)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › FOXO transcription factor regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA Repair Mechanisms
- Keywords
- DAF-16/FOXO, developmental growth, DNA damage response, aging, developmental arrest, transcriptional co-regulation, DNA repair, Caenorhabditis elegans
- MeSH terms
- Aging, Animals, DNA Damage, DNA Repair, DNA-Binding Proteins, Herbicides, Paraquat, Transcription Factors, Signal Transduction, Caenorhabditis elegans, Gene Expression Regulation, Developmental, Caenorhabditis elegans Proteins, Animals, Genetically Modified, Forkhead Transcription Factors
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