Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Regulation of lifespan by sensory perception in Caenorhabditis elegans

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 perception1,2. Cilia are membrane-bound microtubule-based structures and in C. elegans are only found at the dendritic endings of sensory neurons3. 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.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Animals with defects in sensory cilia and sensory transduction live longer than wild type.
Figure 2: Survival curves of germline- and gonad-ablated animals, and double mutants.

Similar content being viewed by others

References

  1. Perkins,L. A., Hedgecock,E. M., Thomson,J. N. & Culotti,J. G. Mutant sensory cilia in the nematode Caenorhabditis elegans. Dev. Biol. 117, 456–487 (1986).

    Article  CAS  PubMed  Google Scholar 

  2. Peckol,E. L., Zallen,J. A., Yarrow,J. C. & Bargmann,C. I. Sensory activity affects sensory axon development in C. elegans. Development 126, 1891–1902 (1999).

    CAS  PubMed  Google Scholar 

  3. White,J. G., Southgate,E., Thomson,J. N. & Brenner,S. The structure of the nervous system of the nematode C. elegans. Phil. Trans R. Soc. Lond. B 314, 1–340 (1986).

    Article  ADS  CAS  Google Scholar 

  4. Collet,J., Spike,C. A., Lundquist,E. A., Shaw,J. E. & Herman,R. K. Analysis of osm-6, a gene that affects sensory cilium structure and sensory neuron function in Caenorhabditis elegans. Genetics 148, 187–200 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  5. Cole,D. G. et al. Chlamydomonas kinesin-II-dependent intraflagellar transport (IFT): IFT particles contain proteins required for ciliary assembly in Caenorhabditis elegans sensory neurons. J. Cell Biol. 141, 993–1008 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Albert,P., Brown,S. & Riddle,D. Sensory control of dauer larva formation in Caenorhabditis elegans. J. Comp. Neurol. 198, 435–451 (1981).

    Article  CAS  PubMed  Google Scholar 

  7. Tabish,M., Siddiqui,Z. K., Nishikawa,K. & Siddiqui,S. S. Exclusive expression of C. elegans osm-3 kinesin gene in chemosensory neurons open to the external environment. J. Mol. Biol. 247, 377–389 (1995).

    Article  CAS  PubMed  Google Scholar 

  8. Zagotta,W. N. & Siegelbaum,S. A. Structure and function of cyclic nucleotide-gated channels. Annu. Rev. Neurosci. 19, 235–263 (1996).

    Article  CAS  PubMed  Google Scholar 

  9. Komatsu,H., Mori,I., Rhee,J. S., Akaike,N. & Ohshima,Y. Mutations in a cyclic nucleotide-gated channel lead to abnormal thermosensation and chemosensation in C. elegans. Neuron 17, 707–718 (1996).

    Article  CAS  PubMed  Google Scholar 

  10. Coburn,C. M. & Bargmann,C. I. A putative cyclic nucleotide-gated channel is required for sensory development and function in C. elegans. Neuron 17, 695–706 (1996).

    Article  CAS  PubMed  Google Scholar 

  11. Komatsu,H. et al. Functional reconstitution of a heteromeric cyclic nucleotide-gated channel of Caenorhabditis elegans in cultured cells. Brain Res. 821, 160–168 (1999).

    Article  CAS  PubMed  Google Scholar 

  12. Avery,L. & Horvitz,H. R. Pharyngeal pumping continues after laser killing of the pharyngeal nervous system of C. elegans. Neuron 3, 473–485 (1989).

    Article  CAS  PubMed  Google Scholar 

  13. Hsin,H. & Kenyon,C. Signals from the reproductive system regulate the lifespan of C. elegans. Nature 399, 362–366 (1999).

    Article  ADS  CAS  PubMed  Google Scholar 

  14. Kenyon,C., Chang,J., Gensch,E., Rudner,A. & Tabtiang,R. A C. elegans mutant that lives twice as long as wild type. Nature 366, 461–464 (1993).

    Article  ADS  CAS  PubMed  Google Scholar 

  15. Kimura,K. D., Tissenbaum,H. A., Liu,Y. & Ruvkun,G. daf-2, an insulin receptor-like gene that regulates longevity and diapause in Caenorhabditis elegans. Science 277, 942–946 (1997).

    Article  CAS  PubMed  Google Scholar 

  16. Paradis,S., Ailion,M., Toker,A., Thomas,J. H. & Ruvkun,G. A PDK1 homolog is necessary and sufficient to transduce AGE-1 PI3 kinase signals that regulate diapause in Caenorhabditis elegans. Genes Dev. 13, 1438–1452 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Larsen,P. L., Albert,P. S. & Riddle,D. L. Genes that regulate both development and longevity in Caenorhabditis elegans. Genetics 139, 1567–1583 (1995).

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Dorman,J. B., Albinder,B., Shroyer,T. & Kenyon,C. The age-1 and daf-2 genes function in a common pathway to control the lifespan of Caenorhabditis elegans. Genetics 141, 1399–1406 (1995).

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Ogg,S. et al. The fork head transcription factor DAF-16 transduces insulin-like metabolic and longevity signals in C. elegans. Nature 389, 994–999 (1997).

    Article  ADS  CAS  PubMed  Google Scholar 

  20. Lin,K., Dorman,J. B., Rodan,A. & Kenyon,C. daf-16: an HNF-3-forkhead family member that can function to double the life-span of Caenorhabditis elegans. Science 278, 1319–1322 (1997).

    Article  ADS  CAS  PubMed  Google Scholar 

  21. Riddle,D., Swanson,M. & Albert,P. Interacting genes in nematode dauer larva formation. Nature 290, 668–671 (1981).

    Article  ADS  CAS  PubMed  Google Scholar 

  22. Golden,J. & Riddle,D. The Caenorhabditis elegans dauer larva: developmental effects of pheromone, food, and temperature. Dev. Biol. 102, 368–378 (1984).

    Article  CAS  PubMed  Google Scholar 

  23. Vowels,J. & Thomas,J. Genetic analysis of chemosensory control of dauer formation in Caenorhabditis elegans. Genetics 130, 105–123 (1992).

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Coburn,C. M., Mori,I., Ohshima,Y. & Bargmann,C. I. A cyclic nucleotide-gated channel inhibits sensory axon outgrowth in larval and adult Caenorhabditis elegans: a distinct pathway for maintenance of sensory axon structure. Development 125, 249–258 (1998).

    CAS  PubMed  Google Scholar 

  25. Ailion,M., Inoue,T., Weaver,C. I., Holdcraft,R. W. & Thomas,J. H. Neurosecretory control of aging in Caenorhabditis elegans. Proc. Natl Acad. Sci. USA 96, 7394–7397 (1999).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  26. Apfeld,J. & Kenyon,C. Cell nonautonomy of C. elegans daf-2 function in the regulation of diapause and life span. Cell 95, 199–210 (1998).

    Article  CAS  PubMed  Google Scholar 

  27. Lawless,J. F. Models and Methods for Lifetime Data (Wiley, New York, 1982).

    MATH  Google Scholar 

Download references

Acknowledgements

We thank J. Whangbo, S. Alper, J. Alcedo, H. Hsin, K. Lin, L. Yang, Q. Ch'ng, A. Dillin, D. Garigan and other members of the Kenyon Lab, as well as members of Cori Bargmann's lab, for stimulating discussions. Some nematode strains were provided by the Caenorhabditis Genetics Center, which is funded by the NIH. J.A. was supported by an HHMI Predoctoral Fellowship. This work was supported by a grant from the NIA to C.K.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Cynthia Kenyon.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Apfeld, J., Kenyon, C. Regulation of lifespan by sensory perception in Caenorhabditis elegans. Nature 402, 804–809 (1999). https://doi.org/10.1038/45544

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/45544

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing