The first long-lived mutants: Discovery of the insulin/IGF-1 pathway for ageing

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 366, Issue 1561, 2011, Pages 9-16

  Kenyon, Cynthia ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Daf 16; Daf 2; Foxo; History; Ifg 1; Insulin

Indexed keywords

ENZYME ACTIVITY; INHIBITION; MOLECULAR ANALYSIS; MUTATION; NEMATODE;

ANIMALIA; CAENORHABDITIS ELEGANS; NEMATODA;

EID: 79251470797     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2010.0276     Document Type: Review

References (52)

1. Klass, M. R. 1977 Aging in the nematode Caenorhabditis elegans: Major biological and environmental factors influencing life span. Mech. Ageing Dev. 6, 413-429. (doi:10.1016/0047-6374(77)90043-4)
2. Klass, M. R. 1983 A method for the isolation of longevity mutants in the nematode Caenorhabditis elegans and initial results. Mech Ageing Dev. 22, 279-286. (doi:10. 1016/0047-6374(83)90082-9)
3. Johnson, T. E. & Wood, W. B. 1982 Genetic analysis of life-span in Caenorhabditis elegans. Proc. Natl Acad. Sci. USA 79, 6603-6607. (doi:10.1073/pnas.79.21.6603) (Pubitemid 13220223)
4. Johnson, T. E. 1987 Aging can be genetically dissected into component processes using long-lived lines of Caenorhabditis elegans. Proc. Natl Acad. Sci. USA 84, 3777-3781. (doi:10.1073/pnas.84.11.3777)
5. Friedman, D. B. & Johnson, T. E. 1988 A mutation in the age-1 gene in Caenorhabditis elegans lengthens life and reduces hermaphrodite fertility. Genetics 118, 75-86.
6. Johnson, T. E. 1990 Increased life-span of age-1 mutants in Caenorhabditis elegans and lower Gompertz rate of aging. Science 249, 908-912. (doi:10.1126/science.2392681)
7. Johnson, T. E., Tedesco, P. M. & Lithgow, G. J. 1993 Comparing mutants, selective breeding, and transgenics in the dissection of aging processes of Caenorhabditis elegans. Genetica 91, 65-77. (doi:10. 1007/BF01435988)
8. Hayflick, L. 1965 The limited in vitro lifetime of human diploid cell strains. Exp. Cell Res. 37, 614-636. (doi:10. 1016/0014-4827(65)90211-9)
9. Hayflick, L. 1989 Antecedents of cell aging research. Exp. Gerontol. 24, 355-365. (doi:10.1016/0531-5565(89)90043-0) (Pubitemid 20004763)
10. Thomson, J. & Forfar, J. O. 1950 Progeria (Hutchinson- Gilford syndrome). Report of a case and review of the literature. Arch. Dis. Child. 25, 224-234. (doi:10.1136/ adc.25.123.224)
11. Brown, W. T. 1979 Human mutations affecting aging-a review. Mech. Ageing Dev. 9, 325-336. (doi:10.1016/ 0047-6374(79)90109-X)
12. Costa, M., Weir, M., Coulson, A., Sulston, J. & Kenyon, C. 1988 Posterior pattern formation in C. elegans involves position-specific expression of a gene containing a homeobox. Cell 55, 747-756. (doi:10.1016/0092- 8674(88)90131-6)
13. Kenyon, C. 1996 Ponce d'elegans: Genetic quest for the fountain of youth. Cell 84, 501-504. (doi:10.1016/ S0092-8674(00)81024-7)
14. Kenyon, C. 1997 Environmental factors and gene activities that influence the lifespan of C. elegans. In The nematode Caenorhabditis elegans II (eds D. Riddle, B. Meyer & J. Priess), pp. 791-813. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
15. Bagg, A., Kenyon, C. J. & Walker, G. C. 1981 Inducibility of a gene product required for UV and chemical mutagenesis in Escherichia coli. Proc. Natl Acad. Sci. USA 78, 5749-5753. (doi:10.1073/pnas.78.9.5749)
16. Riddle, D. L., Swanson, M. M. & Albert, P. S. 1981 Interacting genes in nematode dauer larva formation. Nature 290, 668-671. (doi:10.1038/290668a0) (Pubitemid 11068954)
17. Vowels, J. J. & Thomas, J. H. 1992 Genetic analysis of chemosensory control of dauer formation in Caenorhabditis elegans. Genetics 130, 105-123.
18. Kenyon, C., Chang, J., Gensch, E., Rudner, A. & Tabtiang, R. 1993 A C. elegans mutant that lives twice as long as wild type. Nature 366, 461-464. (doi:10. 1038/366461a0)
19. Garigan, D., Hsu, A. L., Fraser, A. G., Kamath, R. S., Ahringer, J. & Kenyon, C. 2002 Genetic analysis of tissue aging in Caenorhabditis elegans: A role for heat-shock factor and bacterial proliferation. Genetics 161, 1101-1112.
20. Hansen, M., Hsu, A. L., Dillin, A. & Kenyon, C. 2005 New genes tied to endocrine, metabolic, and dietary regulation of lifespan from a Caenorhabditis elegans genomic RNAi screen. PLoS Genet. 1, 119-128. (doi:10.1371/journal.pgen.0010017)
21. Larsen, P. L., Albert, P. S. & Riddle, D. L. 1995 Genes that regulate both development and longevity in Caenorhabditis elegans. Genetics 139, 1567-1583.
22. Gems, D., Sutton, A. J., Sundermeyer, M. L., Albert, P. S., King, K. V., Edgley,M. L., Larsen, P. L. & Riddle, M. L. 1998 Two pleiotropic classes of daf-2 mutation affect larval arrest, adult behavior, reproduction and longevity in Caenorhabditis elegans. Genetics. 150, 129-155.
23. Dillin, A., Crawford, D. K. & Kenyon, C. 2002 Timing requirements for insulin/IGF-1 signaling in C. elegans. Science 298, 830-834. (doi:10.1126/science.1074240) (Pubitemid 35231536)
24. Tissenbaum, H. A. & Ruvkun, G. 1998 An insulin-like signaling pathway affects both longevity and reproduction in Caenorhabditis elegans. Genetics 148, 703-717.
25. Riddle, D. L. & Albert, P. S. 1997 Genetic and environmental regulation of dauer larvae development. In The nematode Caenorhabditis elegans II (eds D. Riddle, B. Meyer & J. Priess), pp. 739-768. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
26. Shaw, W. M., Luo, S., Landis, J., Ashraf, J. & Murphy, C. T. 2007 The C. elegans TGF-b dauer pathway regulates longevity via insulin signaling. Curr. Biol. 17, 1635-1645. (doi:10.1016/j.cub.2007.08.058) (Pubitemid 47503810)
27. Honjoh, S., Yamamoto, T., Uno, M. & Nishida, E. 2009 Signalling through RHEB-1 mediates intermittent fasting-induced longevity in C. elegans. Nature 457, 726-730. (doi:10.1038/nature07583)
28. Greer, E. L., Dowlatshahi, D., Banko, M. R., Villen, J., Hoang, K., Blanchard, D., Gygi, S. P. & Brunet, A. 2007 An AMPK-FOXO pathway mediates longevity induced by a novel method of dietary restriction in C. elegans. Curr. Biol. 17, 1646-1656. (doi:10.1016/j. cub.2007.08.047)
29. Lakowski, B. & Hekimi, S. 1998 The genetics of caloric restriction in Caenorhabditis elegans. Proc. Natl Acad. Sci. USA 95, 13091-13096. (doi:10.1073/pnas.95.22.13091) (Pubitemid 28509529)
30. Dorman, J. B., Albinder, B., Shroyer, T. & Kenyon, C. 1995 The age-1 and daf-2 genes function in a common pathway to control the lifespan of Caenorhabditis elegans. Genetics 141, 1399-1406.
31. Murakami, S. & Johnson, T. E. 1996 A genetic pathway conferring life extension and resistance to UV stress in Caenorhabditis elegans. Genetics 143, 1207-1218.
32. Gottlieb, S. & Ruvkun, G. 1994 daf-2, daf-16 and daf-23: Genetically interacting genes controlling dauer formation in Caenorhabditis elegans. Genetics 137, 107-120.
33. Malone, E. A., Inoue, T. & Thomas, J. H. 1996 Genetic analysis of the roles of daf-28 and age-1 in regulating Caenorhabditis elegans dauer formation. Genetics 143, 1193-1205.
34. Morris, J. Z., Tissenbaum, H. A. & Ruvkun, G. 1996 A phosphatidylinositol-3-OH kinase family member regulating longevity and diapause in Caenorhabditis elegans. Nature 382, 536-539. (doi:10.1038/382536a0) (Pubitemid 26260694)
35. Auger, K. R., Serunian, L. A., Soltoff, S. P., Libby, P. & Cantley, L. C. 1989 PDGF-dependent tyrosine phosphorylation stimulates production of novel polyphosphoinositides in intact cells. Cell 57, 167-175. (doi:10. 1016/0092-8674(89)90182-7)
36. Varticovski, L., Druker, B., Morrison, D., Cantley, L. & Roberts, T. 1989 The colony stimulating factor-1 receptor associates with and activates phosphatidylinositol-3 kinase. Nature 342, 699-702. (doi:10.1038/342699a0) (Pubitemid 20001589)
37. Bjorge, J. D., Chan, T. O., Antczak, M., Kung, H. J. & Fujita, D. J. 1990 Activated type I phosphatidylinositol kinase is associated with the epidermal growth factor (EGF) receptor following EGF stimulation. Proc. Natl Acad. Sci. USA 87, 3816-3820. (doi:10.1073/pnas.87. 10.3816) (Pubitemid 20182550)
38. Herman, P. K. & Emr, S. D. 1990 Characterization of VPS34, a gene required for vacuolar protein sorting and vacuole segregation in Saccharomyces cerevisiae. Mol. Cell Biol. 10, 6742-6754.
39. Sjolander, A., Yamamoto, K., Huber, B. E. & Lapetina, E. G. 1991 Association of p21ras with phosphatidylinositol 3-kinase. Proc. Natl Acad. Sci. USA 88, 7908-7912. (doi:10.1073/pnas.88.18.7908)
40. Calabretta, B. & Skorski, T. 1996 BCR/ABL regulation of PI-3 kinase activity. Leuk. Lymphoma 23, 473-476. (doi:10.3109/10428199609054856)
41. Comoglio, P. M. & Boccaccio, C. 1996 The HGF receptor family: Unconventional signal transducers for invasive cell growth. Genes Cells 1, 347-354. (doi:10.1046/j. 1365-2443.1996.37037.x)
42. Shimizu, Y. & Hunt III, S. W. 1996 Regulating integrinmediated adhesion: One more function for PI 3-kinase? Immunol. Today 17, 565-573. (doi:10.1016/S0167- 5699(96)10061-X)
43. Ward, S. G. 1996 CD28: A signalling perspective. Biochem. J. 318, 361-377.
44. Weiss, R. H. & Yabes, A. P. 1996 Mitogenic inhibition by phorbol esters is associated with decreased phosphatidylinositol- 3 kinase activation. Am. J. Physiol. 270, C619-C627.
45. Johnson, T. E. 1997 Genetic influences on aging. Exp. Gerontol. 32, 11-22. (doi:10.1016/S0531- 5565(96)00079-4)
46. Kimura, K. D., Tissenbaum, H. A., Liu, Y. & Ruvkun, G. 1997 daf-2, an insulin receptor-like gene that regulates longevity and diapause in Caenorhabditis elegans. Science 277, 942-946. (doi:10.1126/science.277.5328.942) (Pubitemid 27366677)
47. Taguchi, A., Wartschow, L. M. & White, M. F. 2007 Brain IRS2 signaling coordinates life span and nutrient homeostasis. Science 317, 369-372. (doi:10.1126/ science.1142179)
48. Lin,K., Dorman, J. B., Rodan, A. &Kenyon, C. 1997 daf- 16: AnHNF-3/forkhead family member that can function to double the life-span of Caenorhabditis elegans. Science 278, 1319-1322. (doi:10.1126/science.278.5341. 1319) (Pubitemid 27495748)
49. Ogg, S., Paradis, S., Gottlieb, S., Patterson, G. I., Lee, L., Tissenbaum, H. A. & Ruvkun, G. 1997 The Fork head transcription factor DAF-16 transduces insulinlike metabolic and longevity signals in C. elegans. Nature 389, 994-999. (doi:10.1038/40194) (Pubitemid 27485694)
50. Kenyon, C. 2005 The plasticity of aging: Insights from long-lived mutants. Cell 120, 449-460. (doi:10.1016/j. cell.2005.02.002)
51. Kenyon, C. J. 2010 The genetics of ageing. Nature 464, 504-512. (doi:10.1038/nature08980)
52. Kaeberlein, M., McVey, M. & Guarente, L. 1999 The SIR2/3/4 complex and SIR2 alone promote longevity in Saccharomyces cerevisiae by two different mechanisms. Genes Dev. 13, 2570-2580. (doi:10.1101/gad.13.19. 2570) (Pubitemid 29489648)