TOR signaling and rapamycin influence longevity by regulating SKN-1/Nrf and DAF-16/FoxO

Cell Metabolism

Volumn 15, Issue 5, 2012, Pages 713-724

  Robida Stubbs, Stacey ^a   Glover Cutter, Kira ^a   Lamming, Dudley W ^b,c,d   Mizunuma, Masaki ^a,e   Narasimhan, Sri Devi ^a   Neumann Haefelin, Elke ^a,f   Sabatini, David M ^b,c,d   Blackwell, T Keith ^a  

^a HARVARD STEM CELL INSTITUTE   (United States)

^b WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^d MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^e HIROSHIMA UNIVERSITY   (Japan)

^f UNIVERSITY OF FREIBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN SKN 1; RAPAMYCIN; TARGET OF RAPAMYCIN KINASE; TORC1 ENZYME; TORC2 ENZYME; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR DAF 16; TRANSCRIPTION FACTOR FOXO; UNCLASSIFIED DRUG;

ARTICLE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; DNA-BINDING PROTEINS; INSULIN-LIKE GROWTH FACTOR I; LONGEVITY; MALE; MICE; SIGNAL TRANSDUCTION; SIROLIMUS; TOR SERINE-THREONINE KINASES; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

CAENORHABDITIS ELEGANS; MUS;

EID: 84860461929     PISSN: 15504131     EISSN: 19327420     Source Type: Journal    
DOI: 10.1016/j.cmet.2012.04.007     Document Type: Article

References (55)

1. J.H. An, and T.K. Blackwell SKN-1 links C. elegans mesendodermal specification to a conserved oxidative stress response Genes Dev. 17 2003 1882 1893 (Pubitemid 36944565)
2. D.L. Bentley Rules of engagement: co-transcriptional recruitment of pre-mRNA processing factors Curr. Opin. Cell Biol. 17 2005 251 256 (Pubitemid 40719913)
3. N.A. Bishop, and L. Guarente Two neurons mediate diet-restriction-induced longevity in C. elegans Nature 447 2007 545 549 (Pubitemid 46868049)
4. I. Bjedov, J.M. Toivonen, F. Kerr, C. Slack, J. Jacobson, A. Foley, and L. Partridge Mechanisms of life span extension by rapamycin in the fruit fly Drosophila melanogaster Cell Metab. 11 2010 35 46
5. A.V. Budanov, J.H. Lee, and M. Karin Stressin' Sestrins take an aging fight EMBO Mol Med 2 2010 388 400
6. J. Durieux, S. Wolff, and A. Dillin The cell-non-autonomous nature of electron transport chain-mediated longevity Cell 144 2011 79 91
7. K. Glover-Cutter, S. Kim, J. Espinosa, and D.L. Bentley RNA polymerase II pauses and associates with pre-mRNA processing factors at both ends of genes Nat. Struct. Mol. Biol. 15 2008 71 78
8. M. Hansen, S. Taubert, D. Crawford, N. Libina, S.J. Lee, and C. Kenyon Lifespan extension by conditions that inhibit translation in Caenorhabditis elegans Aging Cell 6 2007 95 110 (Pubitemid 46140143)
9. D.E. Harrison, R. Strong, Z.D. Sharp, J.F. Nelson, C.M. Astle, K. Flurkey, N.L. Nadon, J.E. Wilkinson, K. Frenkel, and C.S. Carter Rapamycin fed late in life extends lifespan in genetically heterogeneous mice Nature 460 2009 392 395
10. N. Hay Interplay between FOXO, TOR, and Akt Biochim. Biophys. Acta 1813 2011 1965 1970
11. S.T. Henderson, M. Bonafè, and T.E. Johnson daf-16 protects the nematode Caenorhabditis elegans during food deprivation J. Gerontol. A Biol. Sci. Med. Sci. 61 2006 444 460 (Pubitemid 43794702)
12. S. Honjoh, T. Yamamoto, M. Uno, and E. Nishida Signalling through RHEB-1 mediates intermittent fasting-induced longevity in C. elegans Nature 457 2009 726 730
13. P.P. Hsu, S.A. Kang, J. Rameseder, Y. Zhang, K.A. Ottina, D. Lim, T.R. Peterson, Y. Choi, N.S. Gray, and M.B. Yaffe The mTOR-regulated phosphoproteome reveals a mechanism of mTORC1-mediated inhibition of growth factor signaling Science 332 2011 1317 1322
14. C. Huang, C. Xiong, and K. Kornfeld Measurements of age-related changes of physiological processes that predict lifespan of Caenorhabditis elegans Proc. Natl. Acad. Sci. USA 101 2004 8084 8089 (Pubitemid 38698058)
15. K. Jia, D. Chen, and D.L. Riddle The TOR pathway interacts with the insulin signaling pathway to regulate C. elegans larval development, metabolism and life span Development 131 2004 3897 3906 (Pubitemid 39232150)
16. P. Kapahi, D. Chen, A.N. Rogers, S.D. Katewa, P.W. Li, E.L. Thomas, and L. Kockel With TOR, less is more: a key role for the conserved nutrient-sensing TOR pathway in aging Cell Metab. 11 2010 453 465
17. C.J. Kenyon The genetics of ageing Nature 464 2010 504 512
18. D. Kokel, Y. Li, J. Qin, and D. Xue The nongenotoxic carcinogens naphthalene and para-dichlorobenzene suppress apoptosis in Caenorhabditis elegans Nat. Chem. Biol. 2 2006 338 345 (Pubitemid 43787216)
19. E.S. Kwon, S.D. Narasimhan, K. Yen, and H.A. Tissenbaum A new DAF-16 isoform regulates longevity Nature 466 2010 498 502
20. D.W. Lamming, L. Ye, P. Katajisto, M.D. Goncalves, M. Saitoh, D.M. Stevens, J.G. Davis, A.B. Salmon, A. Richardson, and R.S. Ahima Rapamycin-induced insulin resistance is mediated by mTORC2 loss and uncoupled from longevity Science 335 2012 1638 1643
21. S.S. Lee, S. Kennedy, A.C. Tolonen, and G. Ruvkun DAF-16 target genes that control C. elegans life-span and metabolism Science 300 2003 644 647 (Pubitemid 36520589)
22. X. Li, O. Matilainen, C. Jin, K.M. Glover-Cutter, C.I. Holmberg, and T.K. Blackwell Specific SKN-1/Nrf stress responses to perturbations in translation elongation and proteasome activity PLoS Genet. 7 2011 e1002119
23. K. Loh, H. Deng, A. Fukushima, X. Cai, B. Boivin, S. Galic, C. Bruce, B.J. Shields, B. Skiba, and L.M. Ooms Reactive oxygen species enhance insulin sensitivity Cell Metab. 10 2009 260 272
24. X.M. Ma, and J. Blenis Molecular mechanisms of mTOR-mediated translational control Nat. Rev. Mol. Cell Biol. 10 2009 307 318
25. D. Malhotra, E. Portales-Casamar, A. Singh, S. Srivastava, D. Arenillas, C. Happel, C. Shyr, N. Wakabayashi, T.W. Kensler, W.W. Wasserman, and S. Biswal Global mapping of binding sites for Nrf2 identifies novel targets in cell survival response through ChIP-Seq profiling and network analysis Nucleic Acids Res. 38 2010 5718 5734
26. J.J. McElwee, E. Schuster, E. Blanc, M.D. Piper, J.H. Thomas, D.S. Patel, C. Selman, D.J. Withers, J.M. Thornton, L. Partridge, and D. Gems Evolutionary conservation of regulated longevity assurance mechanisms Genome Biol. 8 2007 R132
27. A. Meléndez, Z. Tallóczy, M. Seaman, E.L. Eskelinen, D.H. Hall, and B. Levine Autophagy genes are essential for dauer development and life-span extension in C. elegans Science 301 2003 1387 1391 (Pubitemid 37075816)
28. M.M. Mihaylova, D.S. Vasquez, K. Ravnskjaer, P.D. Denechaud, R.T. Yu, J.G. Alvarez, M. Downes, R.M. Evans, M. Montminy, and R.J. Shaw Class IIa histone deacetylases are hormone-activated regulators of FOXO and mammalian glucose homeostasis Cell 145 2011 607 621
29. C.T. Murphy, S.A. McCarroll, C.I. Bargmann, A. Fraser, R.S. Kamath, J. Ahringer, H. Li, and C. Kenyon Genes that act downstream of DAF-16 to influence the lifespan of Caenorhabditis elegans Nature 424 2003 277 283
30. W. Niu, Z.J. Lu, M. Zhong, M. Sarov, J.I. Murray, C.M. Brdlik, J. Janette, C. Chen, P. Alves, and E. Preston Diverse transcription factor binding features revealed by genome-wide ChIP-seq in C. elegans Genome Res. 21 2010 245 254
31. W.J. Oh, C.C. Wu, S.J. Kim, V. Facchinetti, L.A. Julien, M. Finlan, P.P. Roux, B. Su, and E. Jacinto mTORC2 can associate with ribosomes to promote cotranslational phosphorylation and stability of nascent Akt polypeptide EMBO J. 29 2010 3939 3951
32. M. Ohtsuji, F. Katsuoka, A. Kobayashi, H. Aburatani, J.D. Hayes, and M. Yamamoto Nrf1 and Nrf2 play distinct roles in activation of antioxidant response element-dependent genes J. Biol. Chem. 283 2008 33554 33562
33. R.P. Oliveira, J. Porter Abate, K. Dilks, J. Landis, J. Ashraf, C.T. Murphy, and T.K. Blackwell Condition-adapted stress and longevity gene regulation by Caenorhabditis elegans SKN-1/Nrf Aging Cell 8 2009 524 541
34. K.Z. Pan, J.E. Palter, A.N. Rogers, A. Olsen, D. Chen, G.J. Lithgow, and P. Kapahi Inhibition of mRNA translation extends lifespan in Caenorhabditis elegans Aging Cell 6 2007 111 119 (Pubitemid 46140144)
35. S.H. Panowski, S. Wolff, H. Aguilaniu, J. Durieux, and A. Dillin PHA-4/Foxa mediates diet-restriction-induced longevity of C. elegans Nature 447 2007 550 555 (Pubitemid 46868041)
36. H. Qadota, M. Inoue, T. Hikita, M. Köppen, J.D. Hardin, M. Amano, D.G. Moerman, and K. Kaibuchi Establishment of a tissue-specific RNAi system in C. elegans Gene 400 2007 166 173 (Pubitemid 47284742)
37. A.N. Rogers, D. Chen, G. McColl, G. Czerwieniec, K. Felkey, B.W. Gibson, A. Hubbard, S. Melov, G.J. Lithgow, and P. Kapahi Life span extension via eIF4G inhibition is mediated by posttranscriptional remodeling of stress response gene expression in C. elegans Cell Metab. 14 2011 55 66
38. M.A. Schreiber, J.T. Pierce-Shimomura, S. Chan, D. Parry, and S.L. McIntire Manipulation of behavioral decline in Caenorhabditis elegans with the Rag GTPase raga-1 PLoS Genet. 6 2010 e1000972
39. R.C. Scott, O. Schuldiner, and T.P. Neufeld Role and regulation of starvation-induced autophagy in the Drosophila fat body Dev. Cell 7 2004 167 178 (Pubitemid 39145023)
40. C. Selman, J.M. Tullet, D. Wieser, E. Irvine, S.J. Lingard, A.I. Choudhury, M. Claret, H. Al-Qassab, D. Carmignac, and F. Ramadani Ribosomal protein S6 kinase 1 signaling regulates mammalian life span Science 326 2009 140 144
41. K.L. Sheaffer, D.L. Updike, and S.E. Mango The Target of Rapamycin pathway antagonizes pha-4/FoxA to control development and aging Curr. Biol. 18 2008 1355 1364
42. A.A. Soukas, E.A. Kane, C.E. Carr, J.A. Melo, and G. Ruvkun Rictor/TORC2 regulates fat metabolism, feeding, growth, and life span in Caenorhabditis elegans Genes Dev. 23 2009 496 511
43. M.N. Stanfel, L.S. Shamieh, M. Kaeberlein, and B.K. Kennedy The TOR pathway comes of age Biochim. Biophys. Acta 1790 2009 1067 1074
44. G.P. Sykiotis, and D. Bohmann Stress-activated cap'n'collar transcription factors in aging and human disease Sci. Signal. 3 2010 re3
45. D. Tohyama, A. Yamaguchi, and T. Yamashita Inhibition of a eukaryotic initiation factor (eIF2Bdelta/F11A3.2) during adulthood extends lifespan in Caenorhabditis elegans FASEB J. 22 2008 4327 4337
46. J.M. Tullet, M. Hertweck, J.H. An, J. Baker, J.Y. Hwang, S. Liu, R.P. Oliveira, R. Baumeister, and T.K. Blackwell Direct inhibition of the longevity-promoting factor SKN-1 by insulin-like signaling in C. elegans Cell 132 2008 1025 1038 (Pubitemid 351391953)
47. T. Vellai, K. Takacs-Vellai, Y. Zhang, A.L. Kovacs, L. Orosz, and F. Müller Genetics: influence of TOR kinase on lifespan in C. elegans Nature 426 2003 620 (Pubitemid 38009359)
48. J. Wang, S. Robida-Stubbs, J.M. Tullet, J.F. Rual, M. Vidal, and T.K. Blackwell RNAi screening implicates a SKN-1-dependent transcriptional response in stress resistance and longevity deriving from translation inhibition PLoS Genet. 6 2010 e1001048
49. K.C. Wu, J.Y. Cui, and C.D. Klaassen Beneficial role of Nrf2 in regulating NADPH generation and consumption Toxicol. Sci. 123 2011 590 600
50. S. Wullschleger, R. Loewith, and M.N. Hall TOR signaling in growth and metabolism Cell 124 2006 471 484 (Pubitemid 43199434)
51. L. Yu, C.K. McPhee, L. Zheng, G.A. Mardones, Y. Rong, J. Peng, N. Mi, Y. Zhao, Z. Liu, and F. Wan Termination of autophagy and reformation of lysosomes regulated by mTOR Nature 465 2010 942 946
52. Y. Yu, S.O. Yoon, G. Poulogiannis, Q. Yang, X.M. Ma, J. Villén, N. Kubica, G.R. Hoffman, L.C. Cantley, S.P. Gygi, and J. Blenis Phosphoproteomic analysis identifies Grb10 as an mTORC1 substrate that negatively regulates insulin signaling Science 332 2011 1322 1326
53. B.M. Zid, A.N. Rogers, S.D. Katewa, M.A. Vargas, M.C. Kolipinski, T.A. Lu, S. Benzer, and P. Kapahi 4E-BP extends lifespan upon dietary restriction by enhancing mitochondrial activity in Drosophila Cell 139 2009 149 160
54. V. Zinzalla, D. Stracka, W. Oppliger, and M.N. Hall Activation of mTORC2 by association with the ribosome Cell 144 2011 757 768
55. R. Zoncu, A. Efeyan, and D.M. Sabatini mTOR: from growth signal integration to cancer, diabetes and ageing Nat. Rev. Mol. Cell Biol. 12 2011 21 35