Differential patterns of apoptosis in response to aging in Drosophila
Open accessAbstract
Several lines of evidence suggest that programmed cell death may play a role in the aging process and the age-related functional declines of multicellular organisms. To pave the way for the use of Drosophila to rigorously test this hypothesis in a genetic model organism, this work examines the pattern of apoptosis in the adult fly during aging. The analysis across the lifespan of caspase activity and DNA fragmentation shows that apoptosis occurs in adult flies at all ages and that it is linked to physiological age. The results establish that under normal conditions, fly aging is coupled with a lifelong gradual increase of apoptosis within muscle cells and an activation of apoptosis in fat cells of old flies. The nervous system does not show signs of apoptosis. These time- and tissue-specific changes indicate that aging influences the levels and the nature of the cells that commit to apoptosis. The comparison with the apoptotic response to starvation and oxidative stresses strongly suggests that the lifelong increase in flight and leg muscles results from the accumulation of oxidative damage associated with aging. This finding presents an attractive mechanism to account for the decline of locomotor functions and muscle loss in the elderly and opens the way for the genetic analysis of sarcopenia in Drosophila.
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In Drosophila, increased PCD-like events were observed during aging in muscle tissue and in fat tissue, as indicated by DNA fragmentation and caspase activity.
“Increased PCD-like events were observed during aging in muscle tissue and in fat tissue, as indicated by DNA fragmentation and caspase activity (Zheng et al., 2005).”
From Programmed cell death in aging (2015) · cites this paper as Zheng et al., 2005
Cites
Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation.
Gavrieli, Y., Sherman, Y., & Ben-Sasson, S. A. (1992) · The Journal of cell biology · doi:10.1083/jcb.119.3.493 · Cited by 9,444 · see citing works
Invited Review: Aging and sarcopenia
Doherty, T. J. (2003) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00347.2003 · Cited by 1,764 · see citing works
Gene expression profile of aging and its retardation by caloric restriction
Lee, C.-K., Klopp, R. G., Weindruch, R., & Prolla, T. A. (1999) · Science · doi:10.1126/science.285.5432.1390 · Cited by 1,473 · see citing works
Strasser, A., O’Connor, L., & Dixit, V. M. (2000) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.69.1.217 · Cited by 1,369 · see citing works
Oxidative stress and apoptosis
Kannan, K., & Jain, S. K. (2000) · Pathophysiology · doi:10.1016/s0928-4680(00)00053-5 · Cited by 1,291 · see citing works
Stochastic and genetic factors influence tissue-specific decline in ageing C. elegans
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. (2002) · Nature · doi:10.1038/nature01135 · Cited by 1,214 · see citing works
Gene-expression profile of the ageing brain in mice
Lee, C.-K., Weindruch, R., & Prolla, T. A. (2000) · Nature Genetics · doi:10.1038/77046 · Cited by 1,055 · see citing works
Calcium and oxidative stress: from cell signaling to cell death
Ermak, G., & Davies, K. J. A. (2002) · Molecular Immunology · doi:10.1016/s0161-5890(01)00108-0 · Cited by 874 · 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
A Yeast Mutant Showing Diagnostic Markers of Early and Late Apoptosis
Madeo, F., Fröhlich, E., & Fröhlich, K. (1997) · The Journal of Cell Biology · doi:10.1083/jcb.139.3.729 · Cited by 794 · see citing works
Ways of dying: multiple pathways to apoptosisPreprint
Adams, J. M. (2003) · Genes & Development · doi:10.1101/gad.1126903 · Cited by 779 · see citing works
Norbury, C. J., & Zhivotovsky, B. (2004) · Oncogene · doi:10.1038/sj.onc.1207532 · Cited by 701 · see citing works
Genome-Wide Transcript Profiles in Aging and Calorically Restricted Drosophila melanogaster
Pletcher, S. D., Macdonald, S. J., Marguerie, R., Certa, U., Stearns, S. C., Goldstein, D. B., & Partridge, L. (2002) · Current Biology · doi:10.1016/s0960-9822(02)00808-4 · Cited by 568 · see citing works
Self-citationDemerec, M. (1950) · Medical Entomology and Zoology · Cited by 556 · see citing works
Wang, S. L., Hawkins, C. J., Yoo, S. J., Müller, H. ‐. J., & Hay, B. A. (1999) · Cell · doi:10.1016/s0092-8674(00)81974-1 · Cited by 505 · see citing works
Caspase Activity and a Specific Cytochrome C Are Required for Sperm Differentiation in Drosophila
Arama, E., Agapite, J., & Steller, H. (2003) · Developmental Cell · doi:10.1016/s1534-5807(03)00120-5 · Cited by 417 · see citing works
Apoptosis in skeletal muscle with aging
Dirks, A., & Leeuwenburgh, C. (2002) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00458.2001 · Cited by 377 · see citing works
Lee, C.-K., Allison, D. B., Brand, J., Weindruch, R., & Prolla, T. A. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.232308999 · Cited by 314 · see citing works
The Role of Apoptosis in the Normal Aging Brain, Skeletal Muscle, and Heart
POLLACK, M., Phaneuf, S., Dirks, A. J., & Leeuwenburgh, C. (2002) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2002.tb02086.x · Cited by 285 · see citing works
Phillips, T., & Leeuwenburgh, C. (2005) · The FASEB Journal · doi:10.1096/fj.04-2870fje · Cited by 283 · see citing works
The Swiss Cheese Mutant Causes Glial Hyperwrapping and Brain Degeneration in Drosophila
Kretzschmar, D., Hasan, G., Sharma, S., Heisenberg, M., & Benzer, S. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-19-07425.1997 · Cited by 251 · see citing works
Cellular senescence and apoptosis: how cellular responses might influence aging phenotypes
Campisi, J. (2003) · Experimental Gerontology · doi:10.1016/s0531-5565(02)00152-3 · Cited by 218 · see citing works
Robinow, S., Talbot, W. S., Hogness, D. S., & Truman, J. W. (1993) · Development · doi:10.1242/dev.119.4.1251 · Cited by 216 · see citing works
Apoptosis in the aging process
Higami, Y., & Shimokawa, I. (2000) · Cell and Tissue Research · doi:10.1007/s004419900156 · Cited by 213 · see citing works
Eggs over easy: cell death in the Drosophila ovary
McCall, K. (2004) · Developmental Biology · doi:10.1016/j.ydbio.2004.07.017 · Cited by 201 · see citing works
Huh, J. R., Vernooy, S. Y., Yu, H., Yan, N., Shi, Y., Guo, M., & Hay, B. A. (2003) · PLoS Biology · doi:10.1371/journal.pbio.0020015 · Cited by 181 · see citing works
Muscle-specific expression of Drosophila hsp70 in response to aging and oxidative stress.
Wheeler, J. C., Bieschke, E., & Tower, J. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.22.10408 · Cited by 171 · see citing works
AGE DEPENDENT APOPTOSIS AND LOSS OF RHABDOSPHINCTER CELLS
Strasser, H., Tiefenthaler, M., Steinlechner, M., Eder, I. E., Bartsch, G. H., & Konwalinka, G. (2000) · The Journal of Urology · doi:10.1016/s0022-5347(05)67106-6 · Cited by 148 · see citing works
Role of Apoptosis in Sarcopenia
Leeuwenburgh, C. (2003) · The Journals of Gerontology Series A · doi:10.1093/gerona/58.11.m999 · Cited by 147 · see citing works
Spatio‐temporal analysis of gene expression during aging in Drosophila melanogaster
Seroude, L., Brummel, T., Kapahi, P., & Benzer, S. (2002) · Aging Cell · doi:10.1046/j.1474-9728.2002.00007.x · Cited by 128 · see citing works
Self-citationAging alters the apoptotic response to genotoxic stress
Suh, Y., Lee, K.-A., Kim, W. H., Han, B. G., Vijg, J., & Park, S. C. (2002) · Nature Medicine · doi:10.1038/nm0102-3 · Cited by 114 · see citing works
blue cheeseMutations Define a Novel, Conserved Gene Involved in Progressive Neural Degeneration
Finley, K. D., Edeen, P. T., Cumming, R. C., Mardahl‐Dumesnil, M., Taylor, B. J., Rodriguez, M. H., Hwang, C. E., Benedetti, M., & McKeown, M. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-04-01254.2003 · Cited by 113 · see citing works
Cell Death Regulation in Drosophila
Vernooy, S. Y., Copeland, J. M., Ghaboosi, N., Griffin, E. E., Yoo, S. J., & Hay, B. A. (2000) · The Journal of Cell Biology · doi:10.1083/jcb.150.2.f69 · Cited by 110 · see citing works
Stage-specific regulation of caspase activity in drosophila oogenesis
Peterson, J. S., Barkett, M., & McCall, K. (2003) · Developmental Biology · doi:10.1016/s0012-1606(03)00240-9 · Cited by 110 · see citing works
Mitochondrial “swirls” induced by oxygen stress and in the Drosophila mutant hyperswirl
Walker, D. W., & Benzer, S. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0403767101 · Cited by 108 · see citing works
Self-citationGhosh, S., & Feany, M. Β. (2004) · Human Molecular Genetics · doi:10.1093/hmg/ddh214 · Cited by 106 · see citing works
Robinow, S., Draizen, T. A., & Truman, J. W. (1997) · Developmental Biology · doi:10.1006/dbio.1997.8696 · Cited by 89 · see citing works
Dissociation between functional senescence and oxidative stress resistance in Drosophila
Cook-Wiens, E., & Grotewiel, M. S. (2002) · Experimental Gerontology · doi:10.1016/s0531-5565(02)00096-7 · Cited by 83 · see citing works
Tornusciolo, D. R. Z., Schmidt, R. L., & Roth, K. A. (1995) · PubMed · Cited by 73 · see citing works
Genetic alteration of normal aging processes is responsible for extended longevity in Drosophila
Arking, R., & Wells, R. A. (1990) · Developmental Genetics · doi:10.1002/dvg.1020110204 · Cited by 67 · see citing works
Role of the Nuclei in Eyeblink Conditioning
Lavond, D. G. (2002) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2002.tb07558.x · Cited by 66 · 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
Insect brain as a model for the study of aging
Herman, M. M., Miquel, J., & Johnson, M. (1971) · Acta Neuropathologica · doi:10.1007/bf00684595 · Cited by 54 · see citing works
Functional domains in plant shoot meristems
Brand, U., Hobe, M., & Simon, R. G. (2001) · BioEssays · doi:10.1002/1521-1878(200102)23:2 · Cited by 49 · see citing works
Miquel, J. (1971) · PubMed · Cited by 48 · see citing works
Motorneurons, reactive oxygen, and life span in Drosophila.
Parkes, T. L., Hilliker, A., & Phillips, J. (1999) · Neurobiology of Aging · doi:10.1016/s0197-4580(99)00086-x · Cited by 39 · see citing works
Han, T. M., & Vries, G. J. D. (1999) · Journal of Neurobiology · doi:10.1002/(sici)1097-4695(199903)38:4 · Cited by 35 · see citing works
The Strange Case of the Armored Scale Insect and Its Bacteriome
Normark, B. B. (2004) · PLoS Biology · doi:10.1371/journal.pbio.0020043 · Cited by 31 · see citing works
Robinow, S., Talbot, W. S., Hogness, D. S., & Truman, J. W. (1994) · Trends in Genetics · doi:10.1016/0168-9525(94)90226-7 · Cited by 24 · see citing works
GAL4 drivers expression in the whole adult fly
Seroude, L. (2002) · genesis · doi:10.1002/gene.10128 · Cited by 21 · see citing works
Self-citationFine-structural changes in the midgut of old Drosophila melanogaster
Anton‐Erxleben, F., Miquel, J., & Philpott, D. E. (1983) · Mechanisms of Ageing and Development · doi:10.1016/0047-6374(83)90027-1 · Cited by 20 · see citing works
Glutamic acid participation in the process of collagen biosynthesis.
Brzuszkiewicz-Zarnowska, H. (1971) · PubMed · Cited by 5 · see citing works
Flagged first, then by citations
1 of the 53 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
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
Sarcopenia – Molecular mechanisms and open questions
Wiedmer, P., Jung, T., Castro, J. P., Pomatto, L. C. D., Sun, P. Y., Davies, K. J. A., & Grune, T. (2020) · Ageing Research Reviews · doi:10.1016/j.arr.2020.101200 · Cited by 476 · 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
AMPK Modulates Tissue and Organismal Aging in a Non-Cell-Autonomous Manner
Ulgherait, M., Rana, A., Rera, M., Graniel, J. V., & Walker, D. W. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.08.006 · Cited by 307 · see citing works
Self-citationThe 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
Flatt, T., & Heyland, A. (2011) · Cited by 256 · see citing works
Mechanisms of skeletal muscle aging: insights from <i>Drosophila</i> and mammalian models
Demontis, F., Piccirillo, R., Goldberg, A. L., & Perrimon, N. (2013) · Disease Models & Mechanisms · doi:10.1242/dmm.012559 · Cited by 238 · see citing works
van der Goot, A. T., Zhu, W., Vázquez‐Manrique, R. P., Seinstra, R. I., Dettmer, K., Michels, H., Farina, F., Krijnen, J., Melki, R., Buijsman, R. C., et al. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1203083109 · Cited by 192 · see citing works
Mechanisms of muscle growth and atrophy in mammals and Drosophila
Piccirillo, R., Demontis, F., Perrimon, N., & Goldberg, A. L. (2013) · Developmental Dynamics · doi:10.1002/dvdy.24036 · Cited by 145 · see citing works
Sanchez, D., López-Arias, B., Torroja, L., Canal, I., Wang, X., Bastiani, M. J., & Ganfornina, M. D. (2006) · Current Biology · doi:10.1016/j.cub.2006.03.024 · Cited by 141 · see citing works
Thermal stress depletes energy reserves in Drosophila
Klepsatel, P., Gáliková, M., Xu, Y., & Kühnlein, R. P. (2016) · Scientific Reports · doi:10.1038/srep33667 · Cited by 139 · 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
Bauer, J. H., Poon, P. C., Glatt-Deeley, H. R., Abrams, J., & Helfand, S. L. (2005) · Current Biology · doi:10.1016/j.cub.2005.10.051 · Cited by 121 · see citing works
Specific age related signatures in Drosophila body parts transcriptome
Girardot, F., Lasbleiz, C., Monnier, V., & Tricoire, H. (2006) · BMC Genomics · doi:10.1186/1471-2164-7-69 · Cited by 113 · see citing works
Radyuk, S. N., Michalak, K., Klichko, V. I., Benes, J. J., Rebrin, I., Sohal, R. S., & Orr, W. C. (2009) · Biochemical Journal · doi:10.1042/bj20082003 · Cited by 102 · see citing works
Tower, J. (2009) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2008.12.005 · Cited by 99 · see citing works
Temporal and spatial transcriptional profiles of aging in Drosophila melanogasterPreprint
Zhan, M., Yamaza, H., Sun, Y., Sinclair, J. W., Li, H., & Zou, S. (2007) · Genome Research · doi:10.1101/gr.6216607 · Cited by 95 · see citing works
New tricks of an old molecule: lifespan regulation by p53
Bauer, J. H., & Helfand, S. L. (2006) · Aging Cell · doi:10.1111/j.1474-9726.2006.00228.x · Cited by 95 · see citing works
Targeting Efferocytosis in Inflammaging
Poon, I. K. H., & Ravichandran, K. S. (2023) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev-pharmtox-032723-110507 · Cited by 92 · see citing works
Modelling the Role of the Hsp70/Hsp90 System in the Maintenance of Protein Homeostasis
Proctor, C. J., & Lorimer, I. A. J. (2011) · PLoS ONE · doi:10.1371/journal.pone.0022038 · Cited by 87 · see citing works
Senescence of the cellular immune response in Drosophila melanogaster
Mackenzie, D. K., Bussière, L. F., & Tinsley, M. C. (2011) · Experimental Gerontology · doi:10.1016/j.exger.2011.07.004 · Cited by 83 · see citing works
Varland, S., Silva, R. D., Kjosås, I., Faustino, A., Bogaert, A., Billmann, M., Boukhatmi, H., Kellen, B., Costanzo, M., Drazic, A., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-42342-y · Cited by 84 · see citing works
Mitochondrial maintenance failure in aging and role of sexual dimorphism
Tower, J. (2014) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2014.10.008 · Cited by 67 · see citing works
Invertebrate models of age-related muscle degeneration
Augustin, H., & Partridge, L. (2009) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2009.06.011 · Cited by 66 · see citing works
Increased Rheb-TOR signaling enhances sensitivity of the whole organism to oxidative stress
Patel, P. H., & Tamanoi, F. (2006) · Journal of Cell Science · doi:10.1242/jcs.03199 · Cited by 60 · see citing works
Involvement of Redox State in the Aging of <i>Drosophila melanogaster</i>
Orr, W. C., Radyuk, S. N., & Sohal, R. S. (2013) · Antioxidants & Redox Signaling · doi:10.1089/ars.2012.5002 · Cited by 55 · see citing works
Skeletal Muscle Degeneration and Regeneration in Mice and Flies
Rai, M., Nongthomba, U., & Grounds, M. D. (2014) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/b978-0-12-391498-9.00007-3 · Cited by 55 · see citing works
Radyuk, S. N., Rebrin, I., Klichko, V. I., Sohal, B. H., Michalak, K., Benes, J. J., Sohal, R. S., & Orr, W. C. (2010) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2010.09.014 · Cited by 52 · see citing works
Shen, J., Curtis, C. N., Tavaré, S., & Tower, J. (2009) · Aging · doi:10.18632/aging.100018 · Cited by 51 · see citing works
Sod2 knockdown in the musculature has whole-organism consequences in Drosophila
Martin, I., Jones, M. A., Rhodenizer, D., Zheng, J., Warrick, J. M., Seroude, L., & Grotewiel, M. (2009) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2009.06.021 · Cited by 46 · see citing works
Self-citationBaker, D. J., & Hepple, R. T. (2006) · Experimental Gerontology · doi:10.1016/j.exger.2006.08.007 · Cited by 42 · see citing works
Radyuk, S. N., Klichko, V. I., Michalak, K., & Orr, W. C. (2012) · The FASEB Journal · doi:10.1096/fj.12-214106 · Cited by 41 · see citing works
JNK Signaling in Drosophila Aging and Longevity
Gan, T., Fan, L., Zhao, L., Misra, M., Liu, M., Zhang, M., & Su, Y. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22179649 · Cited by 36 · see citing works
Li, X., Gao, J., Yu, Z., Jiang, W., Sun, W., Yu, C., Sun, J., Wang, C., Chen, J., Jing, S., et al. (2020) · Clinical Interventions in Aging · doi:10.2147/cia.s237601 · Cited by 36 · see citing works
Patterns and processes of human life history evolution
Muehlenbein, M. P., & Flinn, M. V. (2011) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199568765.003.0012 · Cited by 36 · see citing works
Cell death during preoviposition period in Boophilus microplus tick
de Freitas, D. R. J., Rosa, R. M., Moura, D. J., Seitz, A. L., Colodel, É. M., Driemeier, D., Vaz, I. D. S., & Masuda, A. (2006) · Veterinary Parasitology · doi:10.1016/j.vetpar.2006.10.017 · Cited by 33 · see citing works
Regulating the UAS/GAL4 system in adult Drosophila with Tet-off GAL80 transgenes
Barwell, T., DeVeale, B., Poirier, L., Zheng, J., Seroude, F., & Seroude, L. (2017) · PeerJ · doi:10.7717/peerj.4167 · Cited by 32 · see citing works
Self-citationBednářová, A., Kropf, M., & Krishnan, N. (2019) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2019.109883 · Cited by 32 · see citing works
The role of peroxiredoxin 4 in inflammatory response and aging
Klichko, V. I., Orr, W. C., & Radyuk, S. N. (2015) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2015.12.008 · Cited by 31 · see citing works
Carlson, K. A., Gardner, K., Pashaj, A., Carlson, D. J., Yu, F., Eudy, J. D., Zhang, C., & Harshman, L. G. (2015) · Genetics Research International · doi:10.1155/2015/835624 · Cited by 30 · see citing works
Zhao, Y. G., Xie, Y., & Liu, Y. (2022) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2022.949074 · Cited by 29 · see citing works
Ginkgo biloba Extract EGb 761 and Wisconsin Ginseng Delay Sarcopenia in Caenorhabditis elegans
Cao, Z., Wu, Y., Curry, K., Wu, Z., Christen, Y., & Luo, Y. (2007) · The Journals of Gerontology Series A · doi:10.1093/gerona/62.12.1337 · Cited by 29 · see citing works
UNC5B Promotes Vascular Endothelial Cell Senescence via the ROS‐Mediated P53 Pathway
Yang, Z. L., Li, H., Luo, P., Yan, D., Yang, N., Zhang, Y., Huang, Y., Liu, Y., Zhang, L., Yan, J., et al. (2021) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2021/5546711 · Cited by 27 · see citing works
Drosophila as a lipotoxicity model organism — more than a promise?
Kühnlein, R. P. (2009) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2009.09.006 · Cited by 26 · see citing works
Martínez‐Azorín, F., Calleja, M., Hernández‐Sierra, R., Farr, C. L., Kaguni, L. S., & Garesse, R. (2007) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2007.05122.x · Cited by 25 · see citing works
Age-Related Changes of Gene Expression Profiles in Drosophila
Bordet, G., Lodhi, N., Kossenkov, A. V., & Tulin, A. V. (2021) · Genes · doi:10.3390/genes12121982 · Cited by 23 · see citing works
Cells with Impaired Mitochondrial H 2 O 2 Sensing Generate Less • OH Radicals and Live Longer
Martins, D., Titorenko, V. I., & English, A. M. (2014) · Antioxidants and Redox Signaling · doi:10.1089/ars.2013.5575 · Cited by 23 · see citing works
The unfulfilled gene is required for the development of mushroom body neuropil in Drosophila
Bates, K. E., Sung, C. S., & Robinow, S. (2010) · Neural Development · doi:10.1186/1749-8104-5-4 · Cited by 23 · see citing works
Age-related Cardiac Deterioration: insights from Drosophila
Wessells, R. J. (2006) · Frontiers in bioscience · doi:10.2741/2047 · Cited by 22 · see citing works
Alway, S. E., Morissette, M. R., & Siu, P. M. (2010) · Elsevier eBooks · doi:10.1016/b978-0-12-378638-8.00004-x · Cited by 21 · see citing works
Golubovsky, M. D., Weisman, N. Y., Arbeev, K. G., Ukraintseva, S. V., & YASHIN, A. I. (2006) · Experimental Gerontology · doi:10.1016/j.exger.2006.06.035 · Cited by 20 · see citing works
Righi, V., Apidianakis, Y., Psychogios, N., Rahme, L. G., Tompkins, R. G., & Tzika, A. A. (2014) · International Journal of Molecular Medicine · doi:10.3892/ijmm.2014.1757 · Cited by 19 · see citing works
Odnokoz, O., Nakatsuka, K., Klichko, V. I., Nguyen, J., Solis, L. C., Ostling, K., Badinloo, M., Orr, W. C., & Radyuk, S. N. (2016) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2016.10.017 · Cited by 17 · see citing works
Mitochondrial Redox Signaling Is Critical to the Normal Functioning of the Neuronal System
Odnokoz, O., Nakatsuka, K., Wright, C., Castellanos, J., Klichko, V. I., Kretzschmar, D., Orr, W. C., & Radyuk, S. N. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.613036 · Cited by 15 · see citing works
Neuroendocrinal and molecular basis of flight performance in locusts
Hou, L., Guo, S., Ding, D., Du, B., & Wang, X. (2022) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-022-04344-9 · Cited by 15 · see citing works
Modification of the alkaline comet assay with human mesenchymal stem cells
Fuchs, R., Stelzer, I., Drees, C., Rehnolt, C., Schraml, E., Sadjak, A., & Schwinger, W. (2011) · Cell Biology International · doi:10.1042/cbi20110251 · Cited by 15 · see citing works
Expression of Heat Shock Protein 70 Is Insufficient To Extend Drosophila melanogaster Longevity
Xiao, C., Hull, D., Qiu, S., Yeung, J., Zheng, J., Barwell, T., Robertson, R. M., & Seroude, L. (2019) · G3 Genes Genomes Genetics · doi:10.1534/g3.119.400782 · Cited by 14 · see citing works
Self-citationMarkers and mechanisms of death in Drosophila
Tower, J. (2023) · Frontiers in Aging · doi:10.3389/fragi.2023.1292040 · Cited by 13 · see citing works
Lim, J. J., & Hyun, S. (2022) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2022.112803 · Cited by 13 · see citing works
Muscle degeneration in aging Drosophila flies: the role of mechanical stress
Chechenova, M. B., McLendon, L., Dallas, B., Stratton, H., Kiani, K., Gerberich, E., Alekseyenko, A., Tamba, N., An, S., Castillo, L., et al. (2024) · Skeletal Muscle · doi:10.1186/s13395-024-00352-4 · Cited by 12 · see citing works
Aging features of the migratory locust at physiological and transcriptional levels
Guo, S., Yang, P., Liang, B., Zhou, F., Hou, L., Kang, L., & Wang, X. (2021) · BMC Genomics · doi:10.1186/s12864-021-07585-3 · Cited by 12 · see citing works
Memantine – neuroprotective drug in aging brain
Karolczak, D., Sawicka, E., Dorszewska, J., Radel, A., Bodnar, M., Błaszczyk, A., Jagielska, J., & Marszałek, A. (2013) · Polish Journal of Pathology · doi:10.5114/pjp.2013.38139 · Cited by 12 · see citing works
Lim, J. J., Noh, S., Kang, W., Hyun, B., Lee, B., & Hyun, S. (2024) · Autophagy · doi:10.1080/15548627.2024.2389607 · Cited by 11 · see citing works
Rybina, O. Y., Schelkunov, M. I., Veselkina, E. R., Sarantseva, S. V., Krementsova, A. V., Vysokikh, M. Y., Melentev, P. A., Volodina, M. A., & PASYUKOVA, E. G. (2019) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2019.111121 · Cited by 11 · see citing works
Jeon, H.-J., Kim, Y.-S., Park, J., Pyo, J.-H., Na, H.-J., Kim, I.-J., Kim, C.-M., Chung, H. Y., Kim, N. D., Arking, R., et al. (2015) · Biogerontology · doi:10.1007/s10522-015-9573-0 · Cited by 11 · see citing works
Responses of Drosophila melanogaster to atypical oxygen atmospheres
Skandalis, D. A., Stuart, J. A., & Tattersall, G. J. (2011) · Journal of Insect Physiology · doi:10.1016/j.jinsphys.2011.01.005 · Cited by 12 · see citing works
Chang, Y. C., Tu, H., Huang, T.-W., Xu, B., & Pi, H. (2020) · Scientific Reports · doi:10.1038/s41598-020-68313-7 · Cited by 10 · see citing works
Giraldo, Y. M., Muscedere, M. L., & Traniello, J. F. A. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.673172 · Cited by 9 · see citing works
Yang, L. C., Lu, S., Lu, Y., Chen, M., & Cui, S. (2025) · Insects · doi:10.3390/insects16070678 · Cited by 8 · see citing works
Apoptosis inhibition mitigates aging effects in Drosophila melanogaster
Kidera, H., Hatabu, T., & Takahashi, K. H. (2020) · Genetica · doi:10.1007/s10709-020-00088-1 · Cited by 8 · see citing works
Decoding Cell Death: From a Veritable Library of Babel toVade Mecum?
Hughes, L. D., Wang, Y., Meli, A. P., Rothlin, C. V., & Ghosh, S. (2021) · Annual Review of Immunology · doi:10.1146/annurev-immunol-102819-072601 · Cited by 7 · see citing works
Effects of unpaired 1 gene overexpression on the lifespan of Drosophila melanogaster
Moskalev, A., Николаевна, П. Е., Zhavoronkov, A. A., & Shaposhnikov, M. V. (2019) · BMC Systems Biology · doi:10.1186/s12918-019-0687-x · Cited by 7 · see citing works
Abaquita, T. A. L., Damulewicz, M., Tylko, G., & Pyza, E. (2023) · Frontiers in Physiology · doi:10.3389/fphys.2023.1060175 · Cited by 6 · see citing works
Peroxiredoxins Play an Important Role in the Regulation of Immunity and Aging in Drosophila
Odnokoz, O., Earland, N. J., Badinloo, M., Klichko, V. I., Benes, J. J., Orr, W. C., & Radyuk, S. N. (2023) · Antioxidants · doi:10.3390/antiox12081616 · Cited by 5 · see citing works
Nerve‐racking – apoptotic and non‐apoptotic roles of caspases in the nervous system of Drosophila
Melzer, J., & Broemer, M. (2016) · European Journal of Neuroscience · doi:10.1111/ejn.13213 · Cited by 5 · see citing works
Applying deductive reasoning and the principles of particle physics to aging research
Moldakozhayev, A., Tskhay, A., & Gladyshev, V. N. (2021) · Aging · doi:10.18632/aging.203555 · Cited by 5 · see citing works
NUCB1 is required for proper insulin signaling to control longevity in Drosophila
Yoon, J., Baek, S., Yang, J., & Yeom, E. (2024) · Geriatrics and gerontology international/Geriatrics & gerontology international · doi:10.1111/ggi.14858 · Cited by 5 · see citing works
Martínez‐Azorín, F., Calleja, M., Hernández‐Sierra, R., Farr, C. L., Kaguni, L. S., & Garesse, R. (2013) · Archives of Insect Biochemistry and Physiology · doi:10.1002/arch.21101 · Cited by 4 · see citing works
Wolkow, C. A., Zou, S., & Mattson, M. P. (2009) · Springer eBooks · doi:10.1007/978-90-481-3465-6_14 · Cited by 3 · see citing works
Comparative Skeletal Muscle Aging
Marcinek, D. J., Wanagat, J., & Villarin, J. J. (2009) · Springer eBooks · doi:10.1007/978-90-481-3465-6_13 · Cited by 3 · see citing works
PARG Protein Regulation Roles in Drosophila Longevity Control
Bordet, G., & Tulin, A. V. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25116189 · Cited by 2 · see citing works
On the origins and evolution of apoptosis: the predator–mitochondrial prey hypothesis
Zielenkiewicz, U., Kaushal, V., & Kaczanowski, S. (2025) · Journal of Evolutionary Biology · doi:10.1093/jeb/voaf039 · Cited by 2 · see citing works
Daud, A. I., Zin, W. M. K. W. M., Isa, M. I. N., & Wahid, K. A. A. (2018) · Makara Journal of Technology · doi:10.7454/mst.v21i3.3377 · Cited by 2 · see citing works
Rutin Attenuates Oxidative Stress Associated with Aging: Molecular Docking Study
El‐Far, A. H., Saafan, S. M., Mohamed, S., Tedawy, F. E., & Alsenosy, A. A. (2023) · Damanhour Journal of Veterinary Sciences · doi:10.21608/djvs.2022.165692.1096 · Cited by 1 · see citing works
Bedoukian, M. A., Rodriguez, S. M., Cohen, M. B., Smith, S. V. D., & Park, J. (2009) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2009.01.002 · Cited by 1 · see citing works
Nuclear Apoptosis and Sarcopenia
Alway, S. E., & Siu, P. M. (2010) · Springer eBooks · doi:10.1007/978-90-481-9713-2_9 · Cited by 1 · see citing works
van der Goot, A. T., Zhu, W., Seinstra, R. I., Krijnen, J., Silva, M. R., Thijssen, K. L., Oefner, P. J., Kema, I. P., & Nollen, E. (2012) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp-2012-303524.33
Sex-specific effects of drosophila p53 on adult life span
Shen, J. (2015) · University of Southern California Digital Library · doi:10.25549/usctheses-m2329
GENETIC EVIDENCE FOR DIFFERENTIAL ACTIVITIES OF Goα ISOFORMS IN DROSOPHILA MELANOGASTER
Gioacchino, V. D. (2014)
Sousa‐Neves, R., & Mizutani, C. M. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-811353-0.00035-x
Effect of Age on Histological Changes of Urogenital Tract in Albino Rats
AL-HAYYALI, F. Q. M. (2020) · Al-Anbar Journal of Veterinary Sciences · doi:10.37940/ajvs.2020.13.1.10
Ageing and the cellular immune response in adult Drosophila melanogaster
Mackenzie, D. K. (2014) · Stirling Online Research Repository (University of Stirling)
Dietary Restriction and Aging in Drosophila Melanogaster
Poirier, L., de Cabo, R., & Zou, S. (2010) · Springer eBooks · doi:10.1007/978-90-481-8556-6_5
(2007) · Elsevier eBooks · doi:10.1016/b978-012373657-4/50008-8
(2005) · Science of Aging Knowledge Environment · doi:10.1126/sageke.2005.33.nw31
Guo, S., Yang, P., Liang, B., Zhou, F., Hou, L., Kang, L., & Wang, X. (2021) · Figshare · doi:10.6084/m9.figshare.14398372
Guo, S., Yang, P., Liang, B., Zhou, F., Hou, L., Kang, L., & Wang, X. (2021) · Figshare · doi:10.6084/m9.figshare.14398369
Guo, S., Yang, P., Liang, B., Zhou, F., Hou, L., Kang, L., & Wang, X. (2021) · Figshare · doi:10.6084/m9.figshare.14398375
Guo, S., Yang, P., Liang, B., Zhou, F., Hou, L., Kang, L., & Wang, X. (2021) · Figshare · doi:10.6084/m9.figshare.14398357
Guo, S., Yang, P., Liang, B., Zhou, F., Hou, L., Kang, L., & Wang, X. (2021) · Figshare · doi:10.6084/m9.figshare.14398360
- Authors
- Zheng, J., Edelman, S. W., Tharmarajah, G., Walker, D. W., Pletcher, S. D., & Seroude, L.
- Affiliations
- California Institute of Technology (US)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2005-08-12
- Volume
- 102
- Issue
- 34
- Pages
- 12083-12088
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC1189317
- OpenAlex
- W2137068591
- Cited by
- 100
- References
- 53
- Citations by year
- 2026: 1 · 2025: 2 · 2024: 4 · 2023: 6 · 2022: 3 · 2021: 9 · 2020: 5 · 2019: 4 · 2018: 3 · 2017: 1 · 2016: 3 · 2015: 5 · 2014: 8 · 2013: 7 · 2012: 3
- FWCI
- 1.57
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- CaltechAUTHORS (California Institute of Technology) (submittedVersion)
- Funders
- Queen's University
- Canadian Institutes of Health Research
- Natural Sciences and Engineering Research Council of Canada
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
- Keywords
- apoptosis, aging, Drosophila, caspase activity, DNA fragmentation, muscle cells, adipocytes, nervous system, oxidative stress, starvation, sarcopenia, tissue-specific aging
- MeSH terms
- Adipose Tissue, Age Factors, Aging, Animals, Drosophila, Muscles, Apoptosis, DNA Primers, Oxidative Stress, Reverse Transcriptase Polymerase Chain Reaction, Caspases, In Situ Nick-End Labeling, DNA Fragmentation
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