Separating cause from effect: How does insulin/IGF signalling control lifespan in worms, flies and mice?

Journal of Internal Medicine

Volumn 263, Issue 2, 2008, Pages 179-191

  Piper, M D W ^a   Selman, C ^b   McElwee, J J ^c   Partridge, L ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF ABERDEEN   (United Kingdom)

^c UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Ageing; Caenorhabditis elegans; Drosophila; Insulin IGF signalling; Lifespan; Mice

Indexed keywords

CYTOCHROME P450; FORKHEAD TRANSCRIPTION FACTOR; GLUCURONOSYLTRANSFERASE; INSULIN; INSULIN RECEPTOR; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; SOMATOMEDIN; SOMATOMEDIN C; SUPEROXIDE DISMUTASE; TRANSCRIPTION FACTOR FOXO;

AGING; CAENORHABDITIS ELEGANS; CONFERENCE PAPER; DROSOPHILA MELANOGASTER; FLY; GENE MUTATION; GENETIC CONSERVATION; LIFESPAN; MOLECULAR EVOLUTION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; WORM;

AGING; ANIMALS; CAENORHABDITIS ELEGANS; DROSOPHILA MELANOGASTER; INSULIN; INSULIN-LIKE GROWTH FACTOR I; LONGEVITY; MICE; MODELS, ANIMAL;

EID: 38349103636     PISSN: 09546820     EISSN: 13652796     Source Type: Journal    
DOI: 10.1111/j.1365-2796.2007.01906.x     Document Type: Conference Paper

References (118)

1. Hafen E. Cancer, type 2 diabetes, and ageing: news from flies and worms. Swiss Med Wkly 2004 134 : 711 9.
2. Saltiel AR, Kahn CR. Insulin signalling and the regulation of glucose and lipid metabolism. Nature 2001 414 : 799 806.
3. Simpson L, Parsons R. PTEN: life as a tumor suppressor. Exp Cell Res 2001 264 : 29 41.
4. Partridge L, Gems D, Withers DJ. Sex and death: what is the connection? Cell 2005 120 : 461 72.
5. Braeckman BP, Vanfleteren JR. Genetic control of longevity in C. elegans. Exp Gerontol 2007 42 : 90 8.
6. Giannakou ME, Partridge L. Role of insulin-like signalling in Drosophila lifespan. Trends Biochem Sci 2007 32 : 180 8.
7. Klass MR. A method for the isolation of longevity mutants in the nematode Caenorhabditis elegans and initial results. Mech Ageing Dev 1983 22 : 279 86.
8. Friedman DB, Johnson TE. A mutation in the age-1 gene in Caenorhabditis elegans lengthens life and reduces hermaphrodite fertility. Genetics 1988 118 : 75 86.
9. Morris JZ, Tissenbaum HA, Ruvkun G. A phosphatidylinositol-3-OH kinase family member regulating longevity and diapause in Caenorhabditis elegans. Nature 1996 382 : 536 9.
10. Kenyon C, Chang J, Gensch E, Rudner A, Tabtiang R. A C. elegans mutant that lives twice as long as wild type. Nature 1993 366 : 461 4.
11. Kimura KD, Tissenbaum HA, Liu Y, Ruvkun G. daf-2, an insulin receptor-like gene that regulates longevity and diapause in Caenorhabditis elegans. Science 1997 277 : 942 6.
12. Lin K, Dorman JB, Rodan A, Kenyon C. daf-16: an HNF-3/forkhead family member that can function to double the life-span of Caenorhabditis elegans. Science 1997 278 : 1319 22.
13. Ogg S, Paradis S, Gottlieb S et al. The Fork head transcription factor DAF-16 transduces insulin-like metabolic and longevity signals in C. elegans. Nature 1997 389 : 994 9.
14. Tatar M, Kopelman A, Epstein D, Tu MP, Yin CM, Garofalo RS. A mutant Drosophila insulin receptor homolog that extends life-span and impairs neuroendocrine function. Science 2001 292 : 107 10.
15. Clancy DJ, Gems D, Harshman LG et al. Extension of life-span by loss of CHICO, a Drosophila insulin receptor substrate protein. Science 2001 292 : 104 6.
16. Bluher M, Kahn BB, Kahn CR. Extended longevity in mice lacking the insulin receptor in adipose tissue. Science 2003 299 : 572 4.
17. Holzenberger M, Dupont J, Ducos B et al. IGF-1 receptor regulates lifespan and resistance to oxidative stress in mice. Nature 2003 421 : 182 7.
18. Selman C, Lingard S, Choudhury AI et al. Evidence for lifespan extension and delayed age-related biomarkers in insulin receptor substrate 1 null mice. FASEB J 2007 in press.
19. Taguchi A, Wartschow LM, White MF. Brain IRS2 signaling coordinates life span and nutrient homeostasis. Science 2007 317 : 369 72.
20. Arantes-Oliveira N, Berman JR, Kenyon C. Healthy animals with extreme longevity. Science 2003 302 : 611.
21. Pinkston JM, Garigan D, Hansen M, Kenyon C. Mutations that increase the life span of C. elegans inhibit tumor growth. Science 2006 313 : 971 5.
22. Pinkston-Gosse J, Kenyon C. DAF-16/FOXO targets genes that regulate tumor growth in Caenorhabditis elegans. Nat Genet 2007 39 : 1403 9.
23. Cohen E, Bieschke J, Perciavalle RM, Kelly JW, Dillin A. Opposing activities protect against age-onset proteotoxicity. Science 2006 313 : 1604 10.
24. Wessells RJ, Fitzgerald E, Cypser JR, Tatar M, Bodmer R. Insulin regulation of heart function in aging fruit flies. Nat Genet 2004 36 : 1275 81.
25. Link CD. Invertebrate models of Alzheimer's disease. Genes Brain Behav 2005 4 : 147 56.
26. Ocorr K, Perrin L, Lim HY, Qian L, Wu X, Bodmer R. Genetic control of heart function and aging in Drosophila. Trends Cardiovasc Med 2007 17 : 177 82.
27. Zerofsky M, Harel E, Silverman N, Tatar M. Aging of the innate immune response in Drosophila melanogaster. Aging Cell 2005 4 : 103 8.
28. Kurz CL, Tan MW. Regulation of aging and innate immunity in C. elegans. Aging Cell 2004 3 : 185 93.
29. Partridge L. Some highlights of research on aging with invertebrates, 2006-2007. Aging Cell 2007 6 : 595 8.
30. Kawano T, Ito Y, Ishiguro M, Takuwa K, Nakajima T, Kimura Y. Molecular cloning and characterization of a new insulin/IGF-like peptide of the nematode Caenorhabditis elegans. Biochem Biophys Res Commun 2000 273 : 431 6.
31. Murphy CT, McCarroll SA, Bargmann CI et al. Genes that act downstream of DAF-16 to influence the lifespan of Caenorhabditis elegans. Nature 2003 424 : 277 83.
32. Pierce SB, Costa M, Wisotzkey R et al. Regulation of DAF-2 receptor signaling by human insulin and ins-1, a member of the unusually large and diverse C. elegans insulin gene family. Genes Dev 2001 15 : 672 86.
33. Ikeya T, Galic M, Belawat P, Nairz K, Hafen E. Nutrient-dependent expression of insulin-like peptides from neuroendocrine cells in the CNS contributes to growth regulation in Drosophila. Curr Biol 2002 12 : 1293 300.
34. Rulifson EJ, Kim SK, Nusse R. Ablation of insulin-producing neurons in flies: growth and diabetic phenotypes. Science 2002 296 : 1118 20.
35. Broughton SJ, Piper MD, Ikeya T et al. Longer lifespan, altered metabolism, and stress resistance in Drosophila from ablation of cells making insulin-like ligands. Proc Natl Acad Sci U S A 2005 102 : 3105 10.
36. Rhodes CJ, White MF. Molecular insights into insulin action and secretion. Eur J Clin Invest 2002 32 (Suppl. 3 3 13.
37. Dillin A, Crawford DK, Kenyon C. Timing requirements for insulin/IGF-1 signaling in C. elegans. Science 2002 298 : 830 4.
38. Hwangbo DS, Gersham B, Tu MP, Palmer M, Tatar M. Drosophila dFOXO controls lifespan and regulates insulin signalling in brain and fat body. Nature 2004 429 : 562 6.
39. Giannakou ME, Goss M, Junger MA, Hafen E, Leevers SJ, Partridge L. Long-lived Drosophila with overexpressed dFOXO in adult fat body. Science 2004 305 : 361.
40. Giannakou ME, Goss M, Jacobson J, Vinti G, Leevers SJ, Partridge L. Dynamics of the action of dFOXO on adult mortality in Drosophila. Aging Cell 2007 6 : 429 38.
41. Wolkow CA, Kimura KD, Lee MS, Ruvkun G. Regulation of C. elegans life-span by insulinlike signaling in the nervous system. Science 2000 290 : 147 50.
42. Libina N, Berman JR, Kenyon C. Tissue-specific activities of C. elegans DAF-16 in the regulation of lifespan. Cell 2003 115 : 489 502.
43. de la Monte SM, Wands JR. Review of insulin and insulin-like growth factor expression, signaling, and malfunction in the central nervous system: relevance to Alzheimer's disease. J Alzheimers Dis 2005 7 : 45 61.
44. Weindruch R, Walford RL. The Retardation of Aging and Disease by Dietary Restriction. Springfield, IL : Thomas, 1988.
45. Flurkey K, Papaconstantinou J, Miller RA, Harrison DE. Lifespan extension and delayed immune and collagen aging in mutant mice with defects in growth hormone production. Proc Natl Acad Sci U S A 2001 98 : 6736 41.
46. Coschigano KT, Clemmons D, Bellush LL, Kopchick JJ. Assessment of growth parameters and life span of GHR/BP gene-disrupted mice. Endocrinology 2000 141 : 2608 13.
47. Brown-Borg HM, Borg KE, Meliska CJ, Bartke A. Dwarf mice and the ageing process. Nature 1996 384 : 33.
48. Arantes-Oliveira N, Apfeld J, Dillin A, Kenyon C. Regulation of life-span by germ-line stem cells in Caenorhabditis elegans. Science 2002 295 : 502 5.
49. Hsin H, Kenyon C. Signals from the reproductive system regulate the lifespan of C. elegans. Nature 1999 399 : 362 6.
50. Barnes AI, Boone JM, Jacobson J, Partridge L, Chapman T. No extension of lifespan by ablation of germ line in Drosophila. Proc Biol Sci 2006 273 : 939 47.
51. Cargill SL, Carey JR, Muller HG, Anderson G. Age of ovary determines remaining life expectancy in old ovariectomized mice. Aging Cell 2003 2 : 185 90.
52. Gems D, Sutton AJ, Sundermeyer ML et al. Two pleiotropic classes of daf-2 mutation affect larval arrest, adult behavior, reproduction and longevity in Caenorhabditis elegans. Genetics 1998 150 : 129 55.
53. Partridge L, Gems D. A lethal side-effect. Nature 2002 418 : 921.
54. Larsen PL. Aging and resistance to oxidative damage in Caenorhabditis elegans. Proc Natl Acad Sci U S A 1993 90 : 8905 9.
55. Harman D. Aging: a theory based on free radical and radiation chemistry. J Gerontol 1956 11 : 298 300.
56. Sohal RS, Weindruch R. Oxidative stress, caloric restriction, and aging. Science 1996 273 : 59 63.
57. Melov S, Ravenscroft J, Malik S et al. Extension of life-span with superoxide dismutase/catalase mimetics. Science 2000 289 : 1567 9.
58. Keaney M, Gems D. No increase in lifespan in Caenorhabditis elegans upon treatment with the superoxide dismutase mimetic EUK-8. Free Radic Biol Med 2003 34 : 277 82.
59. Keaney M, Matthijssens F, Sharpe M, Vanfleteren J, Gems D. Superoxide dismutase mimetics elevate superoxide dismutase activity in vivo but do not retard aging in the nematode Caenorhabditis elegans. Free Radic Biol Med 2004 37 : 239 50.
60. Orr WC, Mockett RJ, Benes JJ, Sohal RS. Effects of overexpression of copper-zinc and manganese superoxide dismutases, catalase, and thioredoxin reductase genes on longevity in Drosophila melanogaster. J Biol Chem 2003 278 : 26418 22.
61. Sohal RS, Mockett RJ, Orr WC. Mechanisms of aging: an appraisal of the oxidative stress hypothesis. Free Radic Biol Med 2002 33 : 575 86.
62. Parkes TL, Elia AJ, Dickinson D, Hilliker AJ, Phillips JP, Boulianne GL. Extension of Drosophila lifespan by overexpression of human SOD1 in motorneurons. Nat Genet 1998 19 : 171 4.
63. Sun J, Folk D, Bradley TJ, Tower J. Induced overexpression of mitochondrial Mn-superoxide dismutase extends the life span of adult Drosophila melanogaster. Genetics 2002 161 : 661 72.
64. Sun J, Tower J. FLP recombinase-mediated induction of Cu/Zn-superoxide dismutase transgene expression can extend the life span of adult Drosophila melanogaster flies. Mol Cell Biol 1999 19 : 216 28.
65. Schriner SE, Linford NJ, Martin GM et al. Extension of murine life span by overexpression of catalase targeted to mitochondria. Science 2005 308 : 1909 11.
66. Huang TT, Carlson EJ, Gillespie AM, Shi Y, Epstein CJ. Ubiquitous overexpression of CuZn superoxide dismutase does not extend life span in mice. J Gerontol A Biol Sci Med Sci 2000 55 : B5 9.
67. McElwee J, Bubb K, Thomas JH. Transcriptional outputs of the Caenorhabditis elegans forkhead protein DAF-16. Aging Cell 2003 2 : 111 21.
68. McElwee JJ, Schuster E, Blanc E, Thomas JH, Gems D. Shared transcriptional signature in Caenorhabditis elegans Dauer larvae and long-lived daf-2 mutants implicates detoxification system in longevity assurance. J Biol Chem 2004 279 : 44533 43.
69. Gems D, McElwee JJ. Broad spectrum detoxification: the major longevity assurance process regulated by insulin/IGF-1 signaling? Mech Ageing Dev 2005 126 : 381 7.
70. McElwee JJ, Schuster E, Blanc E et al. Evolutionary conservation of regulated longevity assurance mechanisms. Genome Biol 2007 8 : R132.
71. Amador-Noguez D, Dean A, Huang W, Setchell K, Moore D, Darlington G. Alterations in xenobiotic metabolism in the long-lived little mice. Aging Cell 2007 6 : 453 70.
72. Henderson ST, Bonafe M, Johnson TE. daf-16 protects the nematode Caenorhabditis elegans during food deprivation. J Gerontol A Biol Sci Med Sci 2006 61 : 444 60.
73. Hansen M, Taubert S, Crawford D, Libina N, Lee SJ, Kenyon C. Lifespan extension by conditions that inhibit translation in Caenorhabditis elegans. Aging Cell 2007 6 : 95 110.
74. Pan KZ, Palter JE, Rogers AN et al. Inhibition of mRNA translation extends lifespan in Caenorhabditis elegans. Aging Cell 2007 6 : 111 9.
75. Hsu AL, Murphy CT, Kenyon C. Regulation of aging and age-related disease by DAF-16 and heat-shock factor. Science 2003 300 : 1142 5.
76. Walker GA, Lithgow GJ. Lifespan extension in C. elegans by a molecular chaperone dependent upon insulin-like signals. Aging Cell 2003 2 : 131 9.
77. Morrow G, Samson M, Michaud S, Tanguay RM. Overexpression of the small mitochondrial Hsp22 extends Drosophila life span and increases resistance to oxidative stress. FASEB J 2004 18 : 598 9. doi:.
78. Wang MC, Bohmann D, Jasper H. JNK signaling confers tolerance to oxidative stress and extends lifespan in Drosophila. Dev Cell 2003 5 : 811 6.
79. Melendez A, Talloczy Z, Seaman M, Eskelinen EL, Hall DH, Levine B. Autophagy genes are essential for dauer development and life-span extension in C. elegans. Science 2003 301 : 1387 91.
80. Cuervo AM, Bergamini E, Brunk UT, Droge W, Ffrench M, Terman A. Autophagy and aging: the importance of maintaining "clean" cells. Autophagy 2005 1 : 131 40.
81. Libert S, Chao Y, Zwiener J, Pletcher SD. Realized immune response is enhanced in long-lived puc and chico mutants but is unaffected by dietary restriction. Mol Immunol 2007 45 : 810 17.
82. Garsin DA, Villanueva JM, Begun J et al. Long-lived C. elegans daf-2 mutants are resistant to bacterial pathogens. Science 2003 300 : 1921.
83. Libert S, Chao Y, Chu X, Pletcher SD. Trade-offs between longevity and pathogen resistance in Drosophila melanogaster are mediated by NFkappaB signaling. Aging Cell 2006 5 : 533 43.
84. Ren C, Webster P, Finkel SE, Tower J. Increased internal and external bacterial load during Drosophila aging without life-span trade-off. Cell Metab 2007 6 : 144 52.
85. Patient RK, McGhee JD. The GATA family (vertebrates and invertebrates). Curr Opin Genet Dev 2002 12 : 416 22.
86. Maduro MF, Rothman JH. Making worm guts: the gene regulatory network of the Caenorhabditis elegans endoderm. Dev Biol 2002 246 : 68 85.
87. Kerry S, Tekippe M, Gaddis NC, Aballay A. GATA transcription factor required for immunity to bacterial and fungal pathogens. PLoS ONE 2006 1 : e77.
88. Brennan CA, Anderson KV. Drosophila: the genetics of innate immune recognition and response. Annu Rev Immunol 2004 22 : 457 83.
89. Lossky M, Wensink PC. Regulation of Drosophila yolk protein genes by an ovary-specific GATA factor. Mol Cell Biol 1995 15 : 6943 52.
90. Cooper TG. Transmitting the signal of excess nitrogen in Saccharomyces cerevisiae from the Tor proteins to the GATA factors: connecting the dots. FEMS Microbiol Rev 2002 26 : 223 38.
91. Park JH, Attardo GM, Hansen IA, Raikhel AS. GATA factor translation is the final downstream step in the amino acid/target-of-rapamycin-mediated vitellogenin gene expression in the anautogenous mosquito Aedes aegypti. J Biol Chem 2006 281 : 11167 76.
92. Kaeberlein M, Powers RW III., Steffen KK et al. Regulation of yeast replicative life span by TOR and Sch9 in response to nutrients. Science 2005 310 : 1193 6.
93. Powers RW III., Kaeberlein M, Caldwell SD, Kennedy BK, Fields S. Extension of chronological life span in yeast by decreased TOR pathway signaling. Genes Dev 2006 20 : 174 84.
94. Vellai T, Takacs-Vellai K, Zhang Y, Kovacs AL, Orosz L, Müller F. Influence of TOR kinase on lifespan in C. elegans. Nature 2003 426 : 620.
95. Kapahi P, Zid BM, Harper T, Koslover D, Sapin V, Benzer S. Regulation of lifespan in Drosophila by modulation of genes in the TOR signaling pathway. Curr Biol 2004 14 : 885 90.
96. Girardot F, Lasbleiz C, Monnier V, Tricoire H. Specific age-related signatures in Drosophila body parts transcriptome. BMC Genomics 2006 7 : 69.
97. Chintapalli VR, Wang J, Dow JA. Using FlyAtlas to identify better Drosophila melanogaster models of human disease. Nat Genet 2007 39 : 715 20.
98. Zhan M, Yamaza H, Sun Y, Sinclair J, Li H, Zou S. Temporal and spatial transcriptional profiles of aging in Drosophila melanogaster. Genome Res 2007 17 : 1236 43.
99. Schmidt E, Seifert M, Baumeister R. Caenorhabditis elegans as a model system for Parkinson's disease. Neurodegener Dis 2007 4 : 199 217.
100. Cauchi RJ, van den HM. The fly as a model for neurodegenerative diseases: is it worth the jump? Neurodegener Dis 2006 3 : 338 56.
101. Crowther DC, Page R, Chandraratna D, Lomas DA. A Drosophila model of Alzheimer's disease. Methods Enzymol 2006 412 : 234 55.
102. Bilen J, Bonini NM. Drosophila as a model for human neurodegenerative disease. Annu Rev Genet 2005 39 : 153 71.
103. Hsiao K, Chapman P, Nilsen S et al. Correlative memory deficits, Abeta elevation, and amyloid plaques in transgenic mice. Science 1996 274 : 99 102.
104. Gotz J, Deters N, Doldissen A et al. A decade of tau transgenic animal models and beyond. Brain Pathol 2007 17 : 91 103.
105. Morley JF, Brignull HR, Weyers JJ, Morimoto RI. The threshold for polyglutamine-expansion protein aggregation and cellular toxicity is dynamic and influenced by aging in Caenorhabditis elegans. Proc Natl Acad Sci U S A 2002 99 : 10417 22.
106. Ravikumar B, Vacher C, Berger Z et al. Inhibition of mTOR induces autophagy and reduces toxicity of polyglutamine expansions in fly and mouse models of Huntington disease. Nat Genet 2004 36 : 585 95.
107. Wolfgang WJ, Miller TW, Webster JM et al. Suppression of Huntington's disease pathology in Drosophila by human single-chain Fv antibodies. Proc Natl Acad Sci U S A 2005 102 : 11563 8.
108. Zhang X, Smith DL, Meriin AB et al. A potent small molecule inhibits polyglutamine aggregation in Huntington's disease neurons and suppresses neurodegeneration in vivo. Proc Natl Acad Sci U S A 2005 102 : 892 7.
109. Marsh JL, Thompson LM. Drosophila in the study of neurodegenerative disease. Neuron 2006 52 : 169 78.
110. Kuwahara T, Koyama A, Gengyo-Ando K et al. Familial Parkinson mutant alpha-synuclein causes dopamine neuron dysfunction in transgenic Caenorhabditis elegans. J Biol Chem 2006 281 : 334 40.
111. Lakso M, Vartiainen S, Moilanen AM et al. Dopaminergic neuronal loss and motor deficits in Caenorhabditis elegans overexpressing human alpha-synuclein. J Neurochem 2003 86 : 165 72.
112. Nass R, Hall DH, Miller DM III., Blakely RD. Neurotoxin-induced degeneration of dopamine neurons in Caenorhabditis elegans. Proc Natl Acad Sci U S A 2002 99 : 3264 9.
113. Cooper AA, Gitler AD, Cashikar A et al. Alpha-synuclein blocks ER-Golgi traffic and Rab1 rescues neuron loss in Parkinson's models. Science 2006 313 : 324 8.
114. Whitworth AJ, Wes PD, Pallanck LJ. Drosophila models pioneer a new approach to drug discovery for Parkinson's disease. Drug Discov Today 2006 11 : 119 26.
115. Herndon LA, Schmeissner PJ, Dudaronek JM et al. Stochastic and genetic factors influence tissue-specific decline in ageing C. elegans. Nature 2002 419 : 808 14.
116. Martin I, Grotewiel MS. Distinct genetic influences on locomotor senescence in Drosophila revealed by a series of metrical analyses. Exp Gerontol 2006 41 : 877 81.
117. Larsen PL, Albert PS, Riddle DL. Genes that regulate both development and longevity in Caenorhabditis elegans. Genetics 1995 139 : 1567 83.
118. Suzuki Y, Han M. Genetic redundancy masks diverse functions of the tumor suppressor gene PTEN during C. elegans development. Genes Dev 2006 20 : 423 8.