Target of rapamycin activation predicts lifespan in fruit flies

Cell Cycle

Volumn 14, Issue 18, 2015, Pages 2949-2958

  Scialò, Filippo ^a   Sriram, Ashwin ^a   Naudí, Alba ^b   Ayala, Victoria ^b   Jové, Mariona ^b   Pamplona, Reinald ^b   Sanz, Alberto ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF LLEIDA   (Spain)

Author keywords

Aging; Damage theories; Hyperfunction; Mitochondria; Target of rapamycin

Indexed keywords

INSULIN; MITOCHONDRIAL PROTEIN; MITOCHONDRIAL REACTIVE OXYGEN SPECIES; PHOSPHATIDYLINOSITOL 3 KINASE; REACTIVE OXYGEN METABOLITE; TARGET OF RAPAMYCIN KINASE; UNCLASSIFIED DRUG; RAPAMYCIN;

AGING; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; LIFESPAN; LONGEVITY; METABOLIC RATE; MITOCHONDRION; NONHUMAN; NUTRIENT; OXIDATIVE STRESS; PARAMETERS; SIGNAL TRANSDUCTION; TEMPERATURE; WILD TYPE; ANIMAL; DRUG EFFECTS; ENERGY METABOLISM; METABOLISM; PHYSIOLOGY;

AGING; ANIMALS; DROSOPHILA MELANOGASTER; ENERGY METABOLISM; LONGEVITY; MITOCHONDRIA; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; SIROLIMUS;

EID: 84953889068     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.1080/15384101.2015.1071745     Document Type: Article

References (55)

1. Merker K, Stolzing A, Grune T. Proteolysis, caloric restriction and aging. Mech Ageing Dev 2001; 122:595-615; PMID:11322989; http://dx.doi.org/10.1016/S0047-6374(01)00219-6
2. Harman D. The biologic clock: the mitochondria? J Am Geriatr Soc 1972; 20:145-7; PMID:5016631; http://dx.doi.org/10.1111/j.1532-5415.1972.tb00787.x
3. Barja G. Updating the mitochondrial free radical the ory of aging: an integrated view, key aspects, and confounding concepts. Antioxid Redox Signal 2013; 19:1420-45; PMID:23642158; http://dx.doi.org/10.1089/ars.2012.5148
4. Bratic A, Larsson NG. The role of mitochondria in aging. J Clin Invest 2013; 123:951-7; PMID:23454757; http://dx.doi.org/10.1172/JCI64125
5. Scialo F, Mallikarjun V, Stefanatos R, Sanz A. Regulation of lifespan by the mitochondrial electron transport chain: reactive oxygen species-dependent and reactive oxygen species-independent mechanisms. Antioxid Redox Signal 2013; 19:1953-69; PMID:22938137; http://dx.doi.org/10.1089/ars.2012.4900
6. Hulbert AJ, Pamplona R, Buffenstein R, Buttemer WA. Life and death: metabolic rate, membrane composition, and life span of animals. Physiol Rev 2007; 87:1175-213; PMID:17928583; http://dx.doi.org/10.1152/physrev.00047.2006
7. Pamplona R. Membrane phospholipids, lipoxidative damage and molecular integrity: a causal role in aging and longevity. Biochim Biophys Acta 2008; 1777:1249-62; PMID:18721793; http://dx.doi.org/10.1016/j.bbabio.2008.07.003
8. Shmookler Reis RJ, Xu L, Lee H, Chae M, Thaden JJ, Bharill P, Tazearslan C, Siegel E, Alla R, Zimniak P, et al. Modulation of lipid biosynthesis contributes to stress resistance and longevity of C. elegans mutants. Aging (Albany NY) 2011; 3:125-47; PMID:21386131
9. Van Raamsdonk JM, Hekimi S. Superoxide dismutase is dispensable for normal animal lifespan. Proc Natl Acad Sci USA 2012; 109:5785-90; PMID:22451939; http://dx.doi.org/10.1073/pnas.1116158109
10. Van Remmen H, Ikeno Y, Hamilton M, Pahlavani M, Wolf N, Thorpe SR, Alderson NL, Baynes JW, Epstein CJ, Huang TT, et al. Life-long reduction in MnSOD activity results in increased DNA damage and higher incidence of cancer but does not accelerate aging. Physiol Genomics 2003; 16:29-37; PMID:14679299; http://dx.doi.org/10.1152/physiolgenomics.00122.2003
11. Gems D, Partridge L. Genetics of Longevity in Model Organisms: Debates and Paradigm Shifts. Annu Rev Physiol 2012; PMID:23190075
12. Blagosklonny MV. Aging and immortality: quasi-programmed senescence and its pharmacologic inhibition. Cell Cycle 2006; 5:2087-102; PMID:17012837; http://dx.doi.org/10.4161/cc.5.18.3288
13. Gems D, de la Guardia Y. Alternative Perspectives on Aging in Caenorhabditis elegans: Reactive Oxygen Species or Hyperfunction? Antioxid Redox Signal 2013; 19:321-9; PMID:22870907; http://dx.doi.org/10.1089/ars.2012.4840
14. Pan Y, Schroeder EA, Ocampo A, Barrientos A, Shadel GS. Regulation of yeast chronological life span by TORC1 via adaptive mitochondrial ROS signaling. Cell Metab 2011; 13:668-78; PMID:21641548; http://dx.doi.org/10.1016/jxmet.2011.03.018
15. Spindler SR, Mote PL, Flegal JM. Dietary supplementation with Lovaza and krill oil shortens the life span of long-lived F1 mice. Age (Dordr) 2014; 36:9659; PMID:24816553; http://dx.doi.org/10.1007/s11357- 014-9659-7
16. Bjedov I, Toivonen JM, Kerr F, Slack C, Jacobson J, Foley A, Partridge L. Mechanisms of life span extension by rapamycin in the fruit fly Drosophila melanogaster. Cell Metab 2010; 11:35-46; PMID:20074526; http://dx.doi.org/10.1016/j.cmet.2009.11.010
17. Selman C, Tullet JM, Wieser D, Irvine E, Lingard SJ, Choudhury AI, Claret M, Al-Qassab H, Carmignac D, Ramadani F, et al. Ribosomal protein S6 kinase 1 signaling regulates mammalian life span. Science 2009; 326:140-4; PMID:19797661; http://dx.doi.org/10.1126/science.1177221
18. Harrison DE, Strong R, Sharp ZD, Nelson JF, Astle CM, Flurkey K, Nadon NL, Wilkinson JE, Frenkel K, Carter CS, et al. Rapamycin fed late in life extends lifespan in genetically heterogeneous mice. Nature 2009; 460:392-5; PMID:19587680
19. Leontieva OV, Paszkiewicz GM, Blagosklonny MV. Weekly administration of rapamycin improves survival and biomarkers in obese male mice on high-fat diet. Aging Cell 2014; 13:616-22; PMID:24655348; http://dx.doi.org/10.1111/acel.12211
20. Muller FL, Lustgarten MS, Jang Y, Richardson A, Van Remmen H. Trends in oxidative aging theories. Free Radic Biol Med 2007; 43:477-503; PMID:17640558; http://dx.doi.org/10.1016/j.freeradbiomed.2007.03.034
21. Duttaroy A, Paul A, Kundu M, Belton A. A Sod2 null mutation confers severely reduced adult life span in Drosophila. Genetics 2003;165:2295-9; PMID:14704205
22. Curtis C, Landis GN, Folk D, Wehr NB, Hoe N, Waskar M, Abdueva D, Skvortsov D, Ford D, Luu A, et al. Transcriptional profiling of MnSOD-mediated lifespan extension in Drosophila reveals a species-general network of aging and metabolic genes. Genome Biol 2007; 8:R262; PMID:18067683; http://dx.doi.org/10.1186/gb-2007-8-12-r262
23. Stefanatos R, Sriram A, Kiviranta E, Mohan A, Ayala V, Jacobs HT, Pamplona R, Sanz A. dj-1beta regulates oxidative stress, insulin-like signaling and development in Drosophila melanogaster. Cell Cycle 2012; 11:3876-86; PMID:22983063; http://dx.doi.org/10.4161/cc.22073
24. Sanz A, Fernandez-Ayala DJ, Stefanatos RK, Jacobs HT. Mitochondrial ROS production correlates with, but does not directly regulate lifespan in Drosophila. Aging (Albany NY) 2010; 2:200-23; PMID:20453260
25. Owusu-Ansah E, Song W, Perrimon N. Muscle mitohormesis promotes longevity via systemic repression of insulin signaling. Cell 2013; 155:699-712; PMID:24243023; http://dx.doi.org/10.1016/j.cell.2013.09.021
26. Sestini EA, Carlson JC, Allsopp R. The effects ofambient temperature on life span, lipid peroxidation, superoxide dismutase, and phospholipase A2 activity in Drosophila melanogaster. Exp Gerontol 1991; 26:385-95; PMID:1936197; http://dx.doi.org/10.1016/0531-5565(91)90050-V
27. Miquel J, Lundgren PR, Bensch KG, Atlan H. Effects of temperature on the life span, vitality and fine structure of Drosophila melanogaster. Mech Ageing Dev 1976; 5:347-70; PMID:823384; http://dx.doi.org/10.1016/0047-6374(76)90034-8
28. Pearl R. The Rate of Living, Being an Account of Some Experimental Studies on the Biology of Life Duration. London: University of London Press, 1928.
29. Buffenstein R. The naked mole-rat: a new long-living model for human aging research. J Gerontol A Biol Sci Med Sci 2005; 60:1369-77; PMID:16339321; http://dx.doi.org/10.1093/gerona/60.11.1369
30. de Magalhaes JP, Costa J, Church GM. An analysis of the relationship between metabolism, developmental schedules, and longevity using phylogenetic independent contrasts. J Gerontol A Biol Sci Med Sci 2007; 62:149-60; PMID:17339640; http://dx.doi.org/10.1093/gerona/62.2.149
31. Brys K, Vanfleteren JR, Braeckman BP. Testing the rate-of-living/oxidative damage theory of aging in the nematode model Caenorhabditis elegans. Exp Gerontol 2007; 42:845-51; PMID:17379464; http://dx.doi.org/10.1016/j.exger.2007.02.004
32. Hulbert AJ, Clancy DJ, Mair W, Braeckman BP, Gems D, Partridge L. Metabolic rate is not reduced by dietary-restriction or by lowered insulin/IGF-1 signalling and is not correlated with individual lifespan in Drosophila melanogaster. Exp Gerontol 2004; 39:1137-43; PMID:15288688; http://dx.doi.org/10.1016/j.exger.2004.04.006
33. Speakman JR, Talbot DA, Selman C, Snart S, McLaren JS, Redman P, Krol E, Jackson DM, Johnson MS, Brand MD. Uncoupled and surviving: individual mice with high metabolism have greater mitochondrial uncoupling and live longer. Aging Cell 2004; 3:87-95; PMID:15153176; http://dx.doi.org/10.1111/j.1474-9728.2004.00097.x
34. Barja G. Mitochondrial oxygen consumption and reactive oxygen species production are independently modulated: implications for aging studies. Rejuvenation Res 2007; 10:215-24; PMID:17523876; http://dx.doi.org/10.1089/rej.2006.0516
35. Overgaard J, Sorensen JG, Petersen SO, Loeschcke V, Holmstrup M. Changes in membrane lipid composition following rapid cold hardening in Drosophila melanogaster. J Insect Physiol 2005; 51:1173-82; PMID:16112133; http://dx.doi.org/10.1016/j.jinsphys.2005.06.007
36. Pamplona R, Barja G, Portero-Otin M. Membrane fatty acid unsaturation, protection against oxidative stress, and maximum life span: a homeoviscous-longevity adaptation? Ann N Y Acad Sci 2002; 959:475-90; PMID:11976221; http://dx.doi.org/10.1111/j.1749-6632.2002.tb02118.x
37. Pamplona R, Barja G. An evolutionary comparative scan for longevity-related oxidative stress resistance mechanisms in homeotherms. Biogerontology 2011; 12:409-35; PMID:21755337; http://dx.doi.org/10.1007/s10522-011-9348-1
38. Wang PY, Neretti N, Whitaker R, Hosier S, Chang C, Lu D, Rogina B, Helfand SL. Long-lived Indy and calorie restriction interact to extend life span. Proc Natl Acad Sci U S A 2009; 106:9262-7; PMID:19470468; http://dx.doi.org/10.1073/pnas.0904115106
39. Harman D. Aging: a theory based on free radical and radiation chemistry. J Gerontol 1956; 11:298-300; PMID:13332224; http://dx.doi.org/10.1093/geronj/11.3.298
40. Vermeulen CJ, Bijlsma R. Changes in mortality patterns and temperature dependence of lifespan in Drosophila melanogaster caused by inbreeding. Heredity 2004; 92:275-81; PMID:14679396; http://dx.doi.org/ 10.1038/sj.hdy.6800412
41. Guderley H, St-Pierre J. Going with the flow or life in the fast lane: contrasting mitochondrial responses to thermal change. J Exp Biol 2002; 205:2237-49; PMID:12110658
42. Geer BW, Perille TJ. Effects of dietary sucrose and environmental temperature on fatty acid synthesis in Drosophila melanogaster. Insect Biochemistry 1977; 7:371-9; http://dx.doi.org/10.1016/0020-1790(77) 90040-3
43. Gomez A, Sanchez-Roman I, Gomez J, Cruces J, Mate I, Lopez-Torres M, Naudi A, Portero-Otin M, Pamplona R, De la Fuente M, et al. Lifelong treatment with atenolol decreases membrane fatty acid unsaturation and oxidative stress in heart and skeletal muscle mitochondria and improves immunity and behavior, 50. without changing mice longevity. Aging Cell 2014; 13:551-60; PMID:24612513; http://dx.doi.org/10.1111/acel.12205
44. Valencak TG, Ruf T. Feeding into old age: long-term effects of dietary fatty acid supplementation on tissue composition and life span in mice. J Comp Physiol B 2011; 181:289-98; PMID:20981551; http://dx.doi.51.org/10.1007/s00360-010-0520-8
45. Lopez-Dominguez JA, Ramsey JJ, Tran D, Imai DM, Koehne A, Laing ST, Griffey SM, Kim K, Taylor SL, Hagopian K, et al. The influence of dietary fat source on life Span in calorie restricted mice. J Gerontol A Biol Sci Med Sci 2014; http://dx.doi.org/10.1093/gerona/glu177
46. Sanz A, Caro P, Ayala V, Portero-Otin M, Pamplona R, Barja G. Methionine restriction decreases mitochon-drial oxygen radical generation and leak as well as oxidative damage to mitochondrial DNA and proteins. FASEB J 2006; 20:1064-73; PMID:16770005; http://dx.doi.org/10.1096/fj.05-5568com
47. Pamplona R, Portero-Otin M, Sanz A, Requena J, Barja G. Modification of the longevity-related degree of fatty acid unsaturation modulates oxidative damage to proteins and mitochondrial DNA in liver and brain. Exp Gerontol 2004; 39:725-33; PMID:15130667; http://dx.doi.org/10.1016/j.exger.2004.01.006
48. 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; PMID:17266679; http://dx.doi.org/10.1111/j.1474-9726.2006.00267.x
49. Bjedov I, Partridge L. A longer and healthier life with TOR down-regulation: genetics and drugs. Biochem Soc Trans 2011; 39:460-5; PMID:21428920; http://dx.doi.org/10.1042/BST0390460
50. Wu JJ, Liu J, Chen EB, Wang JJ, Cao L, Narayan N, Fergusson MM, Rovira II, Allen M, Springer DA, et al. Increased mammalian lifespan and a segmental and tissue-specific slowing of aging after genetic reduction of mTOR expression. Cell reports 2013; 4:913-20; PMID:23994476; http://dx.doi.org/10.1016/j.celrep.2013.07.030
51. Leontieva OV, Paszkiewicz GM, Blagosklonny MV. Mechanistic or mammalian target of rapamycin (mTOR) may determine robustness in young male mice at the cost of accelerated aging. Aging (Albany NY) 2012; 4:899-916; PMID:23443503
52. Yang W, Hekimi S. A mitochondrial superoxide signal triggers increased longevity in Caenorhabditis elegans. PLoS Biol 2010; 8:e1000556; PMID:21151885; http://dx.doi.org/10.1371/journal.pbio.1000556
53. Clancy DJ, Gems D, Harshman LG, Oldham S, Stocker H, Hafen E, Leevers SJ, Partridge L. Extension of life-span by loss of CHICO, a Drosophila insulin receptor substrate protein. Science 2001; 292:104-6; PMID:11292874; http://dx.doi.org/10.1126/science.1057991
54. Hashizume O, Shimizu A, Yokota M, Sugiyama A, Nakada K, Miyoshi H, Itami M, Ohira M, Nagase H, Takenaga K, et al. Specific mitochondrial DNA mutation in mice regulates diabetes and lymphoma development. Proc Natl Acad Sci USA 2012; 109:10528-33; PMID:22689997; http://dx.doi.org/10.1073/pnas.1202367109
55. Sanz A, Soikkeli M, Portero-Otin M, Wilson A, Kemppainen E, McIlroy G, Ellila S, Kemppainen KK, Tuomela T, Lakanmaa M, et al. Expression of the yeast NADH dehydrogenase Ndi1 in Drosophila confers increased lifespan independently of dietary restriction. Proc Natl Acad Sci USA 2010; 107:9105-10; PMID:20435911; http://dx.doi.org/10.1073/pnas.0911539107