Regulation of lifespan by sensory perception in Caenorhabditis elegans

Apfeld, Javier; Kenyon, Cynthia

doi:10.1038/45544

Cited by 573Genetics, Aging, and Longevity in Model OrganismsNeurobiology and Insect Physiology ResearchGenetic and Kidney Cyst Diseases

Regulation of lifespan by sensory perception in Caenorhabditis elegans

Apfeld, Javier, Kenyon, Cynthia·1999·Nature

DOI 10.1038/45544

Open this paper in CoChat — free account

Abstract

Caenorhabditis elegans senses environmental signals through ciliated sensory neurons located primarily in sensory organs in the head and tail. Cilia function as sensory receptors, and mutants with defective sensory cilia have impaired sensory perception. Cilia are membrane-bound microtubule-based structures and in C. elegans are only found at the dendritic endings of sensory neurons. Here we show that mutations that cause defects in sensory cilia or their support cells, or in sensory signal transduction, extend lifespan. Our findings imply that sensory perception regulates the lifespan of this animal, and suggest that in nature, its lifespan may be regulated by environmental cues.

Integrity signals

Registry

Crossref · 10.1038/45544

Cites

26 of 26 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

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 worms, various mutations that disrupt sensory neuron function extend lifespan.
“In worms, a number of different mutations that disrupt the function of sensory neurons extend lifespan (90).”
From Neural mechanisms of ageing and cognitive decline (2010) · cites this paper as [90]

The structure of the nervous system of the nematode Caenorhabditis elegans
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
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
Self-citation
daf-2 , an Insulin Receptor-Like Gene That Regulates Longevity and Diapause in Caenorhabditis elegans
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
The Fork head transcription factor DAF-16 transduces insulin-like metabolic and longevity signals in C. elegans
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
daf-16 : An HNF-3/forkhead Family Member That Can Function to Double the Life-Span of Caenorhabditis elegans
Lin, K., Dorman, J. B., Rodan, A. R., & Kenyon, C. J. (1997) · Science · doi:10.1126/science.278.5341.1319 · Cited by 1,496 · see citing works
Self-citation
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
Self-citation
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
Chlamydomonas Kinesin-II–dependent Intraflagellar Transport (IFT): IFT Particles Contain Proteins Required for Ciliary Assembly in Caenorhabditis elegans Sensory Neurons
Cole, D. G., Diener, D. R., Himelblau, A. L., Beech, P. L., Fuster, J. C., & Rosenbaum, J. L. (1998) · The Journal of Cell Biology · doi:10.1083/jcb.141.4.993 · Cited by 898 · see citing works
The Caenorhabditis elegans dauer larva: Developmental effects of pheromone, food, and temperature
Golden, J. W., & Riddle, D. L. (1984) · Developmental Biology · doi:10.1016/0012-1606(84)90201-x · Cited by 602 · see citing works
Genes that regulate both development and longevity in Caenorhabditis elegans.
Larsen, P. L., Albert, P. S., & Riddle, D. L. (1995) · Genetics · doi:10.1093/genetics/139.4.1567 · Cited by 584 · see citing works
Interacting genes in nematode dauer larva formation
Riddle, D. L., Swanson, M. M., & Albert, P. S. (1981) · Nature · doi:10.1038/290668a0 · Cited by 518 · see citing works
Structure and Function of Cyclic Nucleotide-Gated Channels
Zagotta, W. N., & Siegelbaum, S. A. (1996) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.19.030196.001315 · Cited by 501 · see citing works
The age-1 and daf-2 genes function in a common pathway to control the lifespan of Caenorhabditis elegans.
Dorman, J. B., Albinder, B., Shroyer, T., & Kenyon, C. J. (1995) · Genetics · doi:10.1093/genetics/141.4.1399 · Cited by 449 · see citing works
Self-citation
Mutations in a Cyclic Nucleotide–Gated Channel Lead to Abnormal Thermosensation and Chemosensation in C. elegans
Komatsu, H., Mori, I., Rhee, J.-S., Akaike, N., & Ohshima, Y. (1996) · Neuron · doi:10.1016/s0896-6273(00)80202-0 · Cited by 446 · see citing works
A Putative Cyclic Nucleotide–Gated Channel Is Required for Sensory Development and Function in C. elegans
Coburn, C. M., & Bargmann, C. I. (1996) · Neuron · doi:10.1016/s0896-6273(00)80201-9 · Cited by 441 · see citing works
A PDK1 homolog is necessary and sufficient to transduce AGE-1 PI3 kinase signals that regulate diapause in Caenorhabditis elegansPreprint
Paradis, S., Ailion, M., Toker, A., Thomas, J. H., & Ruvkun, G. (1999) · Genes & Development · doi:10.1101/gad.13.11.1438 · Cited by 428 · see citing works
Cell Nonautonomy of C. elegans daf-2 Function in the Regulation of Diapause and Life Span
Apfeld, J., & Kenyon, C. J. (1998) · Cell · doi:10.1016/s0092-8674(00)81751-1 · Cited by 380 · see citing works
Self-citation
Genetic analysis of chemosensory control of dauer formation in Caenorhabditis elegans.
Vowels, J. J., & Thomas, J. H. (1992) · Genetics · doi:10.1093/genetics/130.1.105 · Cited by 350 · see citing works
Pharyngeal pumping continues after laser killing of the pharyngeal nervous system of C. elegans
Avery, L., & Horvitz, H. R. (1989) · Neuron · doi:10.1016/0896-6273(89)90206-7 · Cited by 349 · see citing works
Analysis of osm-6, a Gene That Affects Sensory Cilium Structure and Sensory Neuron Function in Caenorhabditis elegans
Collet, J., Spike, C. A., Lundquist, E. A., Shaw, J. E., & Herman, R. K. (1998) · Genetics · doi:10.1093/genetics/148.1.187 · Cited by 241 · see citing works
Sensory control of dauer larva formation in Caenorhabditis elegans
Albert, P. S., Brown, S. J., & Riddle, D. L. (1981) · The Journal of Comparative Neurology · doi:10.1002/cne.901980305 · Cited by 202 · see citing works
Neurosecretory control of aging in Caenorhabditis elegans
Ailion, M., Inoue, T., Weaver, C. I., Holdcraft, R. W., & Thomas, J. H. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.13.7394 · Cited by 121 · see citing works
Exclusive Expression of Kinesin Gene in Chemosnsory Neurons Open to the External Environment
Tabish, M., Siddiqui, Z. K., Nishikawa, K., & Siddiqui, S. S. (1995) · Journal of Molecular Biology · doi:10.1006/jmbi.1994.0146 · Cited by 120 · see citing works
Functional reconstitution of a heteromeric cyclic nucleotide-gated channel of Caenorhabditis elegans in cultured cells
Komatsu, H., Jin, Y., L’Étoile, N. D., Mori, I., Bargmann, C. I., Akaike, N., & Ohshima, Y. (1999) · Brain Research · doi:10.1016/s0006-8993(99)01111-7 · Cited by 115 · see citing works
A cyclic nucleotide-gated channel inhibits sensory axon outgrowth in larval and adult Caenorhabditis elegans: a distinct pathway for maintenance of sensory axon structure
Coburn, C. M., Mori, I., Ohshima, Y., & Bargmann, C. I. (1998) · Development · doi:10.1242/dev.125.2.249 · Cited by 108 · see citing works
Sensory activity affects sensory axon development in C. elegans
Peckol, E. L., Zallen, J. A., Yarrow, J. C., & Bargmann, C. I. (1999) · Development · doi:10.1242/dev.126.9.1891 · Cited by 89 · see citing works

Flagged first, then by citations

Sorted by citations

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
Self-citation
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
Self-citation
Neural mechanisms of ageing and cognitive decline
Bishop, N. A., Lu, T., & Yankner, B. A. (2010) · Nature · doi:10.1038/nature08983 · Cited by 1,323 · see citing works
Promoting Health and Longevity through Diet: From Model Organisms to Humans
Fontana, L., & Partridge, L. (2015) · Cell · doi:10.1016/j.cell.2015.02.020 · Cited by 1,245 · 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
Regulation of the Caenorhabditis elegans longevity protein DAF-16 by insulin/IGF-1 and germline signaling
Lin, K., Hsin, H., Libina, N., & Kenyon, C. J. (2001) · Nature Genetics · doi:10.1038/88850 · Cited by 1,027 · see citing works
Self-citation
Genome-wide RNAi analysis of Caenorhabditis elegans fat regulatory genes
Ashrafi, K., Chang, F., Watts, J. L., Fraser, A. G., Kamath, R. S., Ahringer, J., & Ruvkun, G. (2003) · Nature · doi:10.1038/nature01279 · Cited by 972 · see citing works
Genetic Analysis of Tissue Aging in Caenorhabditis elegans : A Role for Heat-Shock Factor and Bacterial Proliferation
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
Self-citation
Chemosensation in C. elegans
Bargmann, C. I. (2006) · WormBook · doi:10.1895/wormbook.1.123.1 · Cited by 787 · see citing works
Resveratrol Prolongs Lifespan and Retards the Onset of Age-Related Markers in a Short-Lived Vertebrate
Valenzano, D. R., Tozzini, E. T., Genade, T., Cattaneo, A., Domenici, L., & Cellerino, A. (2006) · Current Biology · doi:10.1016/j.cub.2005.12.038 · Cited by 786 · see citing works
Two neurons mediate diet-restriction-induced longevity in C. elegans
Bishop, N. A., & Guarente, L. (2007) · Nature · doi:10.1038/nature05904 · Cited by 643 · see citing works
The AMP-activated protein kinase AAK-2 links energy levels and insulin-like signals to lifespan in C. elegans
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
Self-citation
Widespread 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
Self-citation
Absence of effects of Sir2 overexpression on lifespan in C. elegans and Drosophila
Burnett, C., Valentini, S., Cabreiro, F., Goss, M., Somogyvári, M., Piper, M. D., Hoddinott, M., Sutphin, G. L., Leko, V., McElwee, J. J., et al. (2011) · Nature · doi:10.1038/nature10296 · Cited by 624 · see citing works
Aging and Survival: The Genetics of Life Span Extension by Dietary Restriction
Mair, W. B., & Dillin, A. G. (2008) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.77.061206.171059 · Cited by 600 · see citing works
XBP-1 Is a Cell-Nonautonomous Regulator of Stress Resistance and Longevity
Taylor, R. C., & Dillin, A. G. (2013) · Cell · doi:10.1016/j.cell.2013.05.042 · Cited by 570 · see citing works
C. elegans dauer formation and the molecular basis of plasticityPreprint
Fielenbach, N., & Antebi, A. (2008) · Genes & Development · doi:10.1101/gad.1701508 · Cited by 556 · see citing works
PHA-4/Foxa mediates diet-restriction-induced longevity of C. elegans
Panowski, S. H., Wolff, S., Aguilaniu, H., Durieux, J., & Dillin, A. G. (2007) · Nature · doi:10.1038/nature05837 · Cited by 538 · see citing works
New Genes Tied to Endocrine, Metabolic, and Dietary Regulation of Lifespan from a Caenorhabditis elegans Genomic RNAi Screen
Hansen, M., Hsu, A., Dillin, A. G., & Kenyon, C. J. (2005) · PLoS Genetics · doi:10.1371/journal.pgen.0010017 · Cited by 533 · see citing works
Self-citation
A systematic RNAi screen for longevity genes in C. elegansPreprint
Hamilton, B., Dong, Y., Shindo, M., Liu, W., Odell, I., Ruvkun, G., & Lee, S. S. (2005) · Genes & Development · doi:10.1101/gad.1308205 · Cited by 513 · see citing works
Mechanisms of aging: public or private?
Partridge, L., & Gems, D. (2002) · Nature Reviews Genetics · doi:10.1038/nrg753 · Cited by 510 · see citing works
The Insulin-Like Growth Factor System and Its Pleiotropic Functions in Brain
Russo, V. C., Gluckman, P. D., Feldman, E. L., & Werther, G. A. (2005) · Endocrine Reviews · doi:10.1210/er.2004-0024 · Cited by 488 · see citing works
The Genetics of Aging
Finch, C. E., & Ruvkun, G. (2001) · Annual Review of Genomics and Human Genetics · doi:10.1146/annurev.genom.2.1.435 · Cited by 446 · see citing works
Neuronal Regulation of Energy Homeostasis: Beyond the Hypothalamus and Feeding
Waterson, M. J., & Horváth, T. L. (2015) · Cell Metabolism · doi:10.1016/j.cmet.2015.09.026 · Cited by 439 · see citing works
Genetic links between diet and lifespan: shared mechanisms from yeast to humans
Bishop, N. A., & Guarente, L. (2007) · Nature Reviews Genetics · doi:10.1038/nrg2188 · Cited by 421 · see citing works
daf-12encodes a nuclear receptor that regulates the dauer diapause and developmental age inC. elegansPreprint
Antebi, A., Yeh, W.-H., Tait, D. S., Hedgecock, E. M., & Riddle, D. L. (2000) · Genes & Development · doi:10.1101/gad.14.12.1512 · Cited by 418 · see citing works
Regulation of Drosophila Life Span by Olfaction and Food-Derived Odors
Libert, S., Zwiener, J., Chu, X., VanVoorhies, W., Roman, G., & Pletcher, S. D. (2007) · Science · doi:10.1126/science.1136610 · Cited by 410 · see citing works
Glucose Shortens the Life Span of C. elegans by Downregulating DAF-16/FOXO Activity and Aquaporin Gene Expression
Lee, S., Murphy, C. T., & Kenyon, C. J. (2009) · Cell Metabolism · doi:10.1016/j.cmet.2009.10.003 · Cited by 391 · see citing works
Self-citation
Regulation of C. elegans Longevity by Specific Gustatory and Olfactory Neurons
Alcedo, J., & Kenyon, C. (2004) · Neuron · doi:10.1016/s0896-6273(03)00816-x · Cited by 388 · see citing works
Self-citation
Dietary restriction in Drosophila
Partridge, L., Piper, M. D. W., & Mair, W. B. (2005) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2005.03.023 · Cited by 388 · see citing works
Intraflagellar Transport
Scholey, J. M. (2003) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.19.111401.091318 · Cited by 378 · see citing works
daf-28 encodes a C. elegans insulin superfamily member that is regulated by environmental cues and acts in the DAF-2 signaling pathwayPreprint
Li, W., Kennedy, S. G., & Ruvkun, G. (2003) · Genes & Development · doi:10.1101/gad.1066503 · Cited by 368 · see citing works
Chemical structure and biological activity of the Caenorhabditis elegans dauer-inducing pheromone
Jeong, P.-Y., Jung, M., Yim, Y., Kim, H., Park, M., Hong, E., Lee, W., Kim, Y. H., Kim, K. H., & Paik, Y. (2005) · Nature · doi:10.1038/nature03201 · Cited by 356 · see citing works
Regulation of Body Size and Behavioral State of C. elegans by Sensory Perception and the EGL-4 cGMP-Dependent Protein Kinase
Fujiwara, M., Sengupta, P., & McIntire, S. L. (2002) · Neuron · doi:10.1016/s0896-6273(02)01093-0 · Cited by 344 · see citing works
EVOLUTIONARY AND MECHANISTIC THEORIES OF AGING
Hughes, K. A., & Reynolds, R. M. (2004) · Annual Review of Entomology · doi:10.1146/annurev.ento.50.071803.130409 · Cited by 328 · see citing works
Insulin regulation of heart function in aging fruit flies
Wessells, R. J., Fitzgerald, E., Cypser, J. R., Tatar, M., & Bodmer, R. (2004) · Nature Genetics · doi:10.1038/ng1476 · Cited by 319 · see citing works
Dauer
Hu, P. J. (2007) · WormBook · doi:10.1895/wormbook.1.144.1 · Cited by 318 · see citing works
A PHYSIOLOGICAL VIEW OF THE PRIMARY CILIUM
Prætorius, H. A., & Spring, K. R. (2004) · Annual Review of Physiology · doi:10.1146/annurev.physiol.67.040403.101353 · Cited by 293 · see citing works
Brain IGF-1 Receptors Control Mammalian Growth and Lifespan through a Neuroendocrine Mechanism
Kappeler, L., Filho, C. D. D. M., Dupont, J., Leneuve, P., Cervera, P., Périn, L., Loudes, C., Blaise, A., Klein, R., Epelbaum, J., et al. (2008) · PLoS Biology · doi:10.1371/journal.pbio.0060254 · Cited by 289 · see citing works
Overlapping and distinct functions for a Caenorhabditis elegans SIR2 and DAF-16/FOXO
Wang, Y., & Tissenbaum, H. A. (2005) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2005.09.005 · Cited by 263 · see citing works
Insulin-Like Growth Factor 1: At the Crossroads of Brain Development and Aging
Wrigley, S., Arafa, D., & Tropea, D. (2017) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2017.00014 · Cited by 263 · see citing works
An 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
A Genetic Program Promotes C. elegans Longevity at Cold Temperatures via a Thermosensitive TRP Channel
Xiao, R., Zhang, B., Dong, Y., Gong, J., Xu, T., Liu, J., & Xu, X. Z. S. (2013) · Cell · doi:10.1016/j.cell.2013.01.020 · Cited by 253 · see citing works
Life extension via dietary restriction is independent of the Ins/IGF-1 signalling pathway in Caenorhabditis elegans
Houthoofd, K. (2003) · Experimental Gerontology · doi:10.1016/s0531-5565(03)00161-x · Cited by 245 · see citing works
Insulin/IGF-1 signaling mutants reprogram ER stress response regulators to promote longevity
Henis‐Korenblit, S., Zhang, P., Hansen, M., McCormick, M. A., Lee, S., Cary, M. P., & Kenyon, C. J. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1002575107 · Cited by 236 · see citing works
Self-citation
TheC. eleganshomolog of the murine cystic kidney disease geneTg737functions in a ciliogenic pathway and is disrupted inosm-5mutant worms
Haycraft, C. J., Swoboda, P., Taulman, P. D., Thomas, J. H., & Yoder, B. K. (2001) · Development · doi:10.1242/dev.128.9.1493 · Cited by 234 · see citing works
Regulation of lifespan by neural excitation and REST
Zullo, J., Drake, D., Aron, L., O’Hern, P., Dhamne, S. C., Davidsohn, N., Mao, C., Klein, W. H., Rotenberg, A., Bennett, D. A., et al. (2019) · Nature · doi:10.1038/s41586-019-1647-8 · Cited by 232 · see citing works
Genetic control of epithelial cell polarity: Lessons fromDrosophila
M�ller, H.-W. (2000) · Developmental Dynamics · doi:10.1002/(sici)1097-0177(200005)218:1 · Cited by 110 · see citing works
Evolution of the innate immune system: the worm perspective
Schulenburg, H., Kurz, C. L., & Ewbank, J. J. (2004) · Immunological Reviews · doi:10.1111/j.0105-2896.2004.0125.x · Cited by 229 · see citing works
The C. elegans adult neuronal IIS/FOXO transcriptome reveals adult phenotype regulators
Kaletsky, R. L., Lakhina, V., Arey, R. N., Williams, A. E., Landis, J. N., Ashraf, J. M., & Murphy, C. T. (2015) · Nature · doi:10.1038/nature16483 · Cited by 226 · see citing works
TRPV1 Pain Receptors Regulate Longevity and Metabolism by Neuropeptide Signaling
Riera, C. E., Huising, M. O., Follett, P., Leblanc, M., Halloran, J. J., Andel, R. V., Filho, C. D. D. M., Merkwirth, C., & Dillin, A. G. (2014) · Cell · doi:10.1016/j.cell.2014.03.051 · Cited by 218 · see citing works
Pseudomonas aeruginosa Suppresses Host Immunity by Activating the DAF-2 Insulin-Like Signaling Pathway in Caenorhabditis elegans
Evans, E., Kawli, T., & Tan, M. (2008) · PLoS Pathogens · doi:10.1371/journal.ppat.1000175 · Cited by 217 · see citing works
Primates and the Evolution of Long, Slow Life Histories
Jones, J. H. (2011) · Current Biology · doi:10.1016/j.cub.2011.08.025 · Cited by 216 · see citing works
Aging networks in Caenorhabditis elegans : AMP‐activated protein kinase ( aak‐2 ) links multiple aging and metabolism pathways
Curtis, R., O'Connor, G., & DiStefano, P. S. (2006) · Aging Cell · doi:10.1111/j.1474-9726.2006.00205.x · Cited by 215 · see citing works
The sensory cilia of Caenorhabditis elegans_Revised
Scholey, J. M. (2007) · WormBook · doi:10.1895/wormbook.1.126.2 · Cited by 209 · 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
Aging: The Reality: Biomarkers of Aging: From Primitive Organisms to Humans
Butler, R. N., Sprott, R., Warner, H. R., Bland, J. S., Feuers, R. J., Forster, M. J., Fillit, H. M., Harman, S. M., Hewitt, M., Hyman, M., et al. (2004) · The Journals of Gerontology Series A · doi:10.1093/gerona/59.6.b560 · Cited by 201 · see citing works
Obesity and vulnerability of the CNS
Bruce-Keller, A. J., Keller, J. N., & Morrison, C. D. (2009) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2008.10.004 · Cited by 200 · see citing works
“For example, studies in both Drosophila melanogaster and Caenorhabditis elegans have shown that genetic mutations that cause defects in sensory cilia or their support cells, or in sensory signal transduction, significantly extend lifespan [116,117].”
Bacterial Nitric Oxide Extends the Lifespan of C. elegans
Gusarov, I., Gautier, L., Смоленцева, О. А., Shamovsky, I., Eremina, S. Y., Mironov, A. S., & Nudler, E. (2013) · Cell · doi:10.1016/j.cell.2012.12.043 · Cited by 194 · see citing works
The role of stem cells in aging
Zant, G. E. V., & Liang, Y. (2003) · Experimental Hematology · doi:10.1016/s0301-472x(03)00088-2 · Cited by 194 · see citing works
Polygenic control of Caenorhabditis elegans fat storage
Mak, H. Y., Nelson, L. S., Basson, M., Johnson, C. D., & Ruvkun, G. (2006) · Nature Genetics · doi:10.1038/ng1739 · Cited by 194 · see citing works
Anticonvulsant Medications Extend Worm Life-Span
Evason, K. J., Huang, C., Yamben, I. F., Covey, D. F., & Kornfeld, K. (2005) · Science · doi:10.1126/science.1105299 · Cited by 192 · see citing works
Lifespan-regulating genes in C. elegans
Uno, M., & Nishida, E. (2016) · npj Aging and Mechanisms of Disease · doi:10.1038/npjamd.2016.10 · Cited by 192 · see citing works
Endocrine signaling in Caenorhabditis elegans controls stress response and longevity
Baumeister, R., Schaffitzel, E., & Hertweck, M. (2006) · Journal of Endocrinology · doi:10.1677/joe.1.06856 · Cited by 192 · see citing works
Regulation of Caenorhabditis elegans lifespan by sir-2.1 transgenes
Viswanathan, M., & Guarente, L. (2011) · Nature · doi:10.1038/nature10440 · Cited by 191 · see citing works
Worming pathways to and from DAF-16/FOXO
Mukhopadhyay, A., Oh, S. W., & Tissenbaum, H. A. (2006) · Experimental Gerontology · doi:10.1016/j.exger.2006.05.020 · Cited by 190 · see citing works
Genetics of Aging in Caenorhabditis elegans
Antebi, A. (2007) · PLoS Genetics · doi:10.1371/journal.pgen.0030129 · Cited by 188 · see citing works
Reactive Oxygen Species and Aging in Caenorhabditis elegans : Causal or Casual Relationship?
Raamsdonk, J. M. V., & Hekimi, S. (2010) · Antioxidants and Redox Signaling · doi:10.1089/ars.2010.3215 · Cited by 184 · see citing works
Tissue entrainment by feedback regulation of insulin gene expression in the endoderm of Caenorhabditis elegans
Murphy, C. T., Lee, S., & Kenyon, C. J. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0709613104 · Cited by 179 · see citing works
Self-citation
Regulation of the Longevity Response to Temperature by Thermosensory Neurons in Caenorhabditis elegans
Lee, S., & Kenyon, C. J. (2009) · Current Biology · doi:10.1016/j.cub.2009.03.041 · Cited by 178 · see citing works
Self-citation
Longevity genes in the nematode Caenorhabditis elegans also mediate increased resistance to stress and prevent disease
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
Insulin/IGF signalling and ageing: seeing the bigger picture
Gems, D. (2001) · Current Opinion in Genetics & Development · doi:10.1016/s0959-437x(00)00192-1 · Cited by 173 · see citing works
Suppression of brain aging and neurodegenerative disorders by dietary restriction and environmental enrichment: molecular mechanisms
Mattson, M. P. (2001) · Mechanisms of Ageing and Development · doi:10.1016/s0047-6374(01)00226-3 · Cited by 171 · see citing works
Dauer Formation Induced by High Temperatures in Caenorhabditis elegans
Ailion, M., & Thomas, J. H. (2000) · Genetics · doi:10.1093/genetics/156.3.1047 · Cited by 169 · see citing works
Dietary restriction in C. elegans: From rate-of-living effects to nutrient sensing pathways
Walker, G. A., Houthoofd, K., Vanfleteren, J. R., & Gems, D. (2005) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2005.03.014 · Cited by 167 · see citing works
Control of intestinal bacterial proliferation in regulation of lifespan in Caenorhabditis elegans
Portal‐Celhay, C., Bradley, E., & Blaser, M. J. (2012) · BMC Microbiology · doi:10.1186/1471-2180-12-49 · Cited by 166 · see citing works
Males Shorten the Life Span of C. elegans 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
Converging Pathways in Lifespan Regulation
Narasimhan, S. D., Yen, K., & Tissenbaum, H. A. (2009) · Current Biology · doi:10.1016/j.cub.2009.06.013 · Cited by 165 · see citing works
Longitudinal imaging of Caenorhabditis elegans in a microfabricated device reveals variation in behavioral decline during aging
Churgin, M. A., Jung, S., Yu, C.-C., Chen, X., Raizen, D. M., & Fang-Yen, C. M. (2017) · eLife · doi:10.7554/elife.26652 · Cited by 164 · see citing works
Compensatory ingestion upon dietary restriction in Drosophila melanogaster
Carvalho, G. B., Kapahi, P., & Benzer, S. (2005) · Nature Methods · doi:10.1038/nmeth798 · Cited by 164 · see citing works
Positive Selection of Caenorhabditis elegans Mutants With Increased Stress Resistance and Longevity
Muñoz, M. J., & Riddle, D. L. (2003) · Genetics · doi:10.1093/genetics/163.1.171 · Cited by 164 · see citing works
A redox-sensitive peroxiredoxin that is important for longevity has tissue- and stress-specific roles in stress resistance
Oláhová, M., Taylor, S. R., Khazaipoul, S., Wang, J., Morgan, B. A., Matsumoto, K., Blackwell, T. K., & Veal, E. A. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0805507105 · Cited by 163 · see citing works
Signaling networks determining life span
Riera, C. E., Merkwirth, C., De Magalhaes Filho, C. D., & Dillin, A. (2016) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-060815-014451 · Cited by 161 · see citing works
Molecular mechanisms of brain aging and neurodegenerative disorders: Lessons from dietary restriction
Prolla, T. A., & Mattson, M. P. (2001) · Trends in Neurosciences · doi:10.1016/s0166-2236(00)01957-3 · Cited by 159 · see citing works
Insulin/IGF1 Signaling Inhibits Age-Dependent Axon Regeneration
Byrne, A. B., Walradt, T. J., Gardner, K. E., Hubbert, A., Reinke, V., & Hammarlund, M. (2014) · Neuron · doi:10.1016/j.neuron.2013.11.019 · Cited by 158 · see citing works
daf-16 Protects the Nematode Caenorhabditis elegans During Food Deprivation
Henderson, S. T., Bonafè, M., & Johnson, T. E. (2006) · The Journals of Gerontology Series A · doi:10.1093/gerona/61.5.444 · Cited by 154 · see citing works
The sensory cilia of Caenorhabditis elegans
Inglis, P. N. (2006) · WormBook · doi:10.1895/wormbook.1.126.1 · Cited by 151 · see citing works
Drosophila Life Span and Physiology Are Modulated by Sexual Perception and Reward
Gendron, C. M., Kuo, T.-H., Harvanek, Z. M., Chung, B. Y., Yew, J. Y., Dierick, H. A., & Pletcher, S. D. (2013) · Science · doi:10.1126/science.1243339 · Cited by 144 · see citing works
Specific insulin-like peptides encode sensory information to regulate distinct developmental processes
Cornils, A., Gloeck, M., Chen, Z., Zhang, Y., & Alcedo, J. (2011) · Development · doi:10.1242/dev.060905 · Cited by 144 · see citing works
Regulation of aging and innate immunity in C. elegans
Kurz, C. L., & Tan, M. (2004) · Aging Cell · doi:10.1111/j.1474-9728.2004.00108.x · Cited by 142 · see citing works
Glycogen controls Caenorhabditis elegans lifespan and resistance to oxidative stress
Gusarov, I., Pani, B., Gautier, L., Смоленцева, О. А., Eremina, S. Y., Shamovsky, I., Katkova-Zhukotskaya, O. A., Mironov, A. S., & Nudler, E. (2017) · Nature Communications · doi:10.1038/ncomms15868 · Cited by 137 · see citing works
Transcriptional profiling of MnSOD-mediated lifespan extension in Drosophilareveals a species-general network of aging and metabolic genes
Curtis, C. N., Landis, G. N., Folk, D. G., Wehr, N. B., Hoe, N., Waskar, M., Abdueva, D. A., Skvortsov, D., Ford, D., Luu, A., et al. (2007) · Genome biology · doi:10.1186/gb-2007-8-12-r262 · Cited by 135 · see citing works
Age- and calorie-independent life span extension from dietary restriction by bacterial deprivation in Caenorhabditis elegans
Smith, E. D., Kaeberlein, T. L., Lydum, B. T., Sager, J. E., Welton, K. L., Kennedy, B. K., & Kaeberlein, M. R. (2008) · BMC Developmental Biology · doi:10.1186/1471-213x-8-49 · Cited by 133 · see citing works
A conserved ubiquitination pathway determines longevity in response to diet restriction
Carrano, A. C., Liu, Z., Dillin, A. G., & Hunter, T. R. (2009) · Nature · doi:10.1038/nature08130 · Cited by 131 · see citing works
Bacillus subtilis biofilm extends Caenorhabditis elegans longevity through downregulation of the insulin-like signalling pathway
Donato, V., Ayala, F. R., Cogliati, S., Bauman, C., Costa, J. G., Leñini, C., & Grau, R. R. (2017) · Nature Communications · doi:10.1038/ncomms14332 · Cited by 129 · see citing works
Model Organisms as a Guide to Mammalian Aging
Tissenbaum, H. A., & Guarente, L. (2002) · Developmental Cell · doi:10.1016/s1534-5807(01)00098-3 · Cited by 128 · see citing works
Costing reproduction
Barnes, A. I., & Partridge, L. (2003) · Animal Behaviour · doi:10.1006/anbe.2003.2122 · Cited by 126 · see citing works
Neuroendocrine signals modulate the innate immunity of Caenorhabditis elegans through insulin signaling
Kawli, T., & Tan, M. (2008) · Nature Immunology · doi:10.1038/ni.1672 · Cited by 124 · see citing works
Insulin, Aging, and the Brain: Mechanisms and Implications
Akintola, A. A., & van Heemst, D. (2015) · Frontiers in Endocrinology · doi:10.3389/fendo.2015.00013 · Cited by 123 · see citing works
C. elegans tubby regulates life span and fat storage by two independent mechanisms
Mukhopadhyay, A., Deplancke, B., Walhout, A. J. M., & Tissenbaum, H. A. (2005) · Cell Metabolism · doi:10.1016/j.cmet.2005.06.004 · Cited by 123 · see citing works

Smelling your way to longevity
van Oosten‐Hawle, P. (2023) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-023-00664-1
Regulation of C. elegans Longevity by Specific Gustatory and Olfactory Neurons
Alcedo, J., & Kenyon, C. (2004) · Neuron · doi:10.1016/s0896-6273(03)00816-x · Cited by 388 · see citing works
Self-citation
Longer Life Through Sensory Deprivation
(1999) · Science Signaling · doi:10.1126/stke.1999.13.tw3
Modulation of lifespan by sensory neurons in C. elegans
Lee, S. (2013) · Open Access System for Information Sharing (Pohang University of Science and Technology)
Sensory neuronal regulation of lifespan via endocrine signaling in C. elegans
Lee, S., MuratArtan, Jeong, D., Lee, D., 김영일, & (231670), J. A. (2013) · Open Access System for Information Sharing (Pohang University of Science and Technology)

Authors: Apfeld, J., & Kenyon, C.
Affiliations: University of California, San Francisco (US)
Corresponding author: Kenyon, Cynthia
ORCID: Apfeld, Javier
Kenyon, Cynthia
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 1999-12
Volume: 402
Issue: 6763
Pages: 804-809
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/45544
OpenAlex: W1587592813
Cited by: 573
References: 26
Citations by year: 2026: 17 · 2025: 17 · 2024: 27 · 2023: 14 · 2022: 20 · 2021: 27 · 2020: 15 · 2019: 30 · 2018: 13 · 2017: 25 · 2016: 21 · 2015: 24 · 2014: 15 · 2013: 22 · 2012: 23
FWCI: 5.50
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: Howard Hughes Medical Institute
National Institute on Aging
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic and Kidney Cyst Diseases
Keywords: lifespan regulation, sensory perception, sensory cilia, sensory neurons, sensory transduction, ciliary defects, Caenorhabditis elegans, environmental cues, aging
MeSH terms: Animals, Cilia, Germ Cells, Larva, Longevity, Mutation, Neurons, Afferent, Receptor, Insulin, Sensory Deprivation, Transcription Factors, Helminth Proteins, Caenorhabditis elegans, Genes, Helminth, Caenorhabditis elegans Proteins, 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

Regulation of lifespan by sensory perception in Caenorhabditis elegans

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Cites

Cited by

Related

Record

About these checks