mTORC2-SGK-1 acts in two environmentally responsive pathways with opposing effects on longevity

Aging Cell

Volumn 13, Issue 5, 2014, Pages 869-878

  Mizunuma, Masaki ^a,b   Neumann Haefelin, Elke ^a,c   Moroz, Natalie ^a,d   Li, Yujie ^c   Blackwell, T Keith ^a  

^a HARVARD STEM CELL INSTITUTE   (United States)

^b HIROSHIMA UNIVERSITY   (Japan)

^c UNIVERSITY OF FREIBURG   (Germany)

^d HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

Aging; Microbiome; MTORC2; Rictor; Serum and glucocorticoid regulated kinase; SKN 1 Nrf

Indexed keywords

MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 2; SERUM AND GLUCOCORTICOID REGULATED KINASE 1; IMMEDIATE EARLY PROTEIN; MULTIPROTEIN COMPLEX; PROTEIN SERINE THREONINE KINASE; SERUM-GLUCOCORTICOID REGULATED KINASE; TARGET OF RAPAMYCIN KINASE; TOR COMPLEX 2; TRANSCRIPTION FACTOR;

AGING; ARTICLE; AUTOPHAGY; BIOLOGICAL FUNCTIONS; CAENORHABDITIS ELEGANS; DETOXIFICATION; GERMLINE STEM CELL; LIFE EXTENSION; LIFESPAN; LIPID METABOLISM; LONGEVITY; LOSS OF FUNCTION MUTATION; MICROENVIRONMENT; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; REGULATORY MECHANISM; SENESCENCE; SIGNAL TRANSDUCTION; STRESS; ANIMAL; GENETICS; METABOLISM; MICROFLORA; PHOSPHORYLATION;

BACTERIA (MICROORGANISMS); CAENORHABDITIS ELEGANS; EUKARYOTA;

ANIMALS; CAENORHABDITIS ELEGANS; IMMEDIATE-EARLY PROTEINS; LONGEVITY; MICROBIOTA; MULTIPROTEIN COMPLEXES; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES; TRANSCRIPTION FACTORS;

EID: 84925271824     PISSN: 14749718     EISSN: 14749726     Source Type: Journal    
DOI: 10.1111/acel.12248     Document Type: Article

References (38)

1. Alam H, Williams TW, Dumas KJ, Guo C, Yoshina S, Mitani S, Hu PJ (2010) EAK-7 controls development and life span by regulating nuclear DAF-16/FoxO activity. Cell Metab. 12, 30-41.
2. An JH, Blackwell TK (2003) SKN-1 links C. elegans mesendodermal specification to a conserved oxidative stress response. Genes Dev. 17, 1882-1893.
3. Avery L, Shtonda BB (2003) Food transport in the C. elegans pharynx. J. Exp. Biol. 206, 2441-2457.
4. Bjedov I, Toivonen JM, Kerr F, Slack C, Jacobson J, Foley A, Partridge L (2010) Mechanisms of life span extension by rapamycin in the fruit fly Drosophila melanogaster. Cell Metab. 11, 35-46.
5. Bowerman B, Eaton BA, Priess JR (1992) skn-1, a maternally expressed gene required to specify the fate of ventral blastomeres in the early C. elegans embryo. Cell 68, 1061-1075.
6. Bruhn MA, Pearson RB, Hannan RD, Sheppard KE (2013) AKT-independent PI3-K signaling in cancer - emerging role for SGK3. Cancer Manag. Res. 5, 281-292.
7. Calixto A, Chelur D, Topalidou I, Chen X, Chalfie M (2010) Enhanced neuronal RNAi in C. elegans using SID-1. Nat. Methods 7, 554-559.
8. Chen AT, Guo C, Dumas KJ, Ashrafi K, Hu PJ (2013) Effects of Caenorhabditis elegans sgk-1 mutations on lifespan, stress resistance, and DAF-16/FoxO regulation. Aging Cell 12, 932-940.
9. Fang Y, Westbrook R, Hill C, Boparai RK, Arum O, Spong A, Wang F, Javors MA, Chen J, Sun LY, Bartke A (2013) Duration of rapamycin treatment has differential effects on metabolism in mice. Cell Metab. 17, 456-462.
10. Glover-Cutter KM, Lin S, Blackwell TK (2013) Integration of the unfolded protein and oxidative stress responses through SKN-1/Nrf. PLoS Genet. 9, e1003701.
11. Gracida X, Eckmann CR (2013) Fertility and germline stem cell maintenance under different diets requires nhr-114/HNF4 in C. elegans. Curr. Biol. 23, 607-613.
12. Harrison DE, Strong R, Sharp ZD, Nelson JF, Astle CM, Flurkey K, Nadon NL, Wilkinson JE, Frenkel K, Carter CS, Pahor M, Javors MA, Fernandez E, Miller RA (2009) Rapamycin fed late in life extends lifespan in genetically heterogeneous mice. Nature 460, 392-395.
13. Hertweck M, Göbel C, Baumeister R (2004) C. elegans SGK-1 is the critical component in the Akt/PKB kinase complex to control stress response and life span. Dev. Cell 6, 577-588.
14. Johnson SC, Rabinovitch PS, Kaeberlein M (2013) mTOR is a key modulator of ageing and age-related disease. Nature 493, 338-345.
15. Jones KT, Greer ER, Pearce D, Ashrafi K (2009) Rictor/TORC2 regulates Caenorhabditis elegans fat storage, body size, and development through sgk-1. PLoS Biol. 7, e60.
16. Kapahi P, Chen D, Rogers AN, Katewa SD, Li PW, Thomas EL, Kockel L (2010) With TOR, less is more: a key role for the conserved nutrient-sensing TOR pathway in aging. Cell Metab. 11, 453-465.
17. Kenyon CJ (2010) The genetics of ageing. Nature 464, 504-512.
18. Lamming DW, Ye L, Katajisto P, Goncalves MD, Saitoh M, Stevens DM, Davis JG, Salmon AB, Richardson A, Ahima RS, Guertin DA, Sabatini DM, Baur JA (2012) Rapamycin-induced insulin resistance is mediated by mTORC2 loss and uncoupled from longevity. Science 335, 1638-1643.
19. Lang F, Shumilina E (2013) Regulation of ion channels by the serum- and glucocorticoid-inducible kinase SGK1. FASEB J. 27, 3-12.
20. Laplante M, Sabatini DM (2012) mTOR signaling in growth control and disease. Cell 149, 274-293.
21. Lee SJ, Kenyon C (2009) Regulation of the longevity response to temperature by thermosensory neurons in Caenorhabditis elegans. Curr. Biol. 19, 715-722.
22. MacNeil LT, Watson E, Arda HE, Zhu LJ, Walhout AJ (2013) Diet-induced developmental acceleration independent of TOR and insulin in C. elegans. Cell 153, 240-252.
23. Maier W, Adilov B, Regenass M, Alcedo J (2010) A neuromedin U receptor acts with the sensory system to modulate food type-dependent effects on C. elegans lifespan. PLoS Biol. 8, e1000376.
24. Melo JA, Ruvkun G (2012) Inactivation of conserved C. elegans genes engages pathogen- and xenobiotic-associated defenses. Cell 149, 452-466.
25. Oliveira RP, Porter Abate J, Dilks K, Landis J, Ashraf J, Murphy CT, Blackwell TK (2009) Condition-adapted stress and longevity gene regulation by Caenorhabditis elegans SKN-1/Nrf. Aging Cell 8, 524-541.
26. Pang S, Curran SP (2014) Adaptive capacity to bacterial diet modulates aging in C. elegans. Cell Metab. 9, 221-231.
27. Robida-Stubbs S, Glover-Cutter K, Lamming DW, Mizunuma M, Narasimhan SD, Neumann-Haefelin E, Sabatini DM, Blackwell TK (2012) TOR signaling and rapamycin influence longevity by regulating SKN-1/Nrf and DAF-16/FoxO. Cell Metab. 15, 713-724.
28. Ruf V, Holzem C, Peyman T, Walz G, Blackwell TK, Neumann-Haefelin E (2013) TORC2 signaling antagonizes SKN-1 to induce C. elegans mesendodermal embryonic development. Dev. Biol. 383, 214-227.
29. Shtonda BB, Avery L (2006) Dietary choice behavior in Caenorhabditis elegans. J. Exp. Biol. 209, 89-102.
30. Soukas AA, Kane EA, Carr CE, Melo JA, Ruvkun G (2009) Rictor/TORC2 regulates fat metabolism, feeding, growth, and life span in Caenorhabditis elegans. Genes Dev. 23, 496-511.
31. Sykiotis GP, Bohmann D (2010) Stress-activated cap'n'collar transcription factors in aging and human disease. Sci. Signal. 3, re3.
32. Timmons L, Court DL, Fire A (2001) Ingestion of bacterially expressed dsRNAs can produce specific and potent genetic interference in Caenorhabditis elegans. Gene 263, 103-112.
33. Tremaroli V, Bäckhed F (2012) Functional interactions between the gut microbiota and host metabolism. Nature 489, 242-249.
34. Tullet JM, Hertweck M, An JH, Baker J, Hwang JY, Liu S, Oliveira RP, Baumeister R, Blackwell TK (2008) Direct inhibition of the longevity-promoting factor SKN-1 by insulin-like signaling in C. elegans. Cell 132, 1025-1038.
35. Wang T, Blumhagen R, Lao U, Kuo Y, Edgar BA (2012) LST8 regulates cell growth via target-of-rapamycin complex 2 (TORC2). Mol. Cell. Biol. 32, 2203-2213.
36. Wullschleger S, Loewith R, Hall MN (2006) TOR signaling in growth and metabolism. Cell 124, 471-484.
37. Xiao R, Zhang B, Dong Y, Gong J, Xu T, Liu J, Xu XZ (2013) A genetic program promotes C. elegans longevity at cold temperatures via a thermosensitive TRP channel. Cell 152, 806-817.
38. Zinzalla V, Stracka D, Oppliger W, Hall MN (2011) Activation of mTORC2 by association with the ribosome. Cell 144, 757-768.