Lithocholic acid extends longevity of chronologically aging yeast only if added at certain critical periods of their lifespan

Cell Cycle

Volumn 11, Issue 18, 2012, Pages 3443-3462

  Burstein, Michelle T ^a   Kyryakov, Pavlo ^a   Beach, Adam ^a   Richard, Vincent R ^a   Koupaki, Olivia ^a   Gomez Perez, Alejandra ^a   Leonov, Anna ^a   Levy, Sean ^a   Noohi, Forough ^a   Titorenko, Vladimir I ^a  

^a Civil and Environmental Engineering   (Canada)

Author keywords

Aging as a developmental program; Anti aging compounds; Caloric restriction; Cellular aging; Lithocholic bile acid; Longevity; Longevity control system; Longevity network; Longevity defining checkpoints; Yeast

Indexed keywords

HYDROGEN PEROXIDE; LITHOCHOLIC ACID; MITOCHONDRIAL DNA; PALMITOLEIC ACID;

AGING; APOPTOSIS; ARTICLE; CALORIC RESTRICTION; CELL ASSAY; CELL DEATH; CELL VIABILITY; CULTURE MEDIUM; DIET; FUNGUS CULTURE; FUNGUS GROWTH; GENETICS; LIFESPAN; LONGEVITY; MITOCHONDRION; NONHUMAN; SACCHAROMYCES CEREVISIAE; WILD TYPE;

EID: 84866773226     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.21754     Document Type: Article

References (85)

1. Greer EL, Brunet A. Signaling networks in aging. J Cell Sci 2008; 121:407-12; PMID:18256383; http://dx.doi.org/10.1242/jcs.021519
2. Fontana L, Partridge L, Longo VD. Extending healthy lifespan - from yeast to humans. Science 2010; 328:321-6; PMID:20395504; http://dx.doi.org/10.1126/ science.1172539
3. Kenyon CJ. The genetics of ageing. Nature 2010; 464:504-12; PMID:20336132; http://dx.doi.org/10.1038/nature08980
4. Longo VD, Shadel GS, Kaeberlein M, Kennedy B. Replicative and chronological aging in Saccharomyces cerevisiae. Cell Metab 2012; 16:18-31; PMID:22768836; http://dx.doi.org/10.1016/j.cmet.2012.06.002
5. Kowald A, Kirkwood TB. Towards a network theory of ageing: a model combining the free radical theory and the protein error theory. J Theor Biol 1994; 168:75-94; PMID:8022192; http://dx.doi.org/10.1006/jtbi.1994.1089
6. Kowald A, Kirkwood TB. A network theory of ageing: the interactions of defective mitochondria, aberrant proteins, free radicals and scavengers in the ageing process. Mutat Res 1996; 316:209-36; PMID:8649456; http://dx.doi.org/10. 1016/S0921-8734(96)90005-3
7. Kirkwood TB, Kowald A. Network theory of aging. Exp Gerontol 1997; 32:395-9; PMID:9315444; http://dx.doi.org/10.1016/S0531-5565(96)00171-4
8. Kirkwood TB, Boys RJ, Gillespie CS, Proctor CJ, Shanley DP, Wilkinson DJ. Towards an e-biology of ageing: integrating theory and data. Nat Rev Mol Cell Biol 2003; 4:243-9; PMID:12612643; http://dx.doi.org/10.1038/nrm1051
9. Murphy MP, Partridge L. Toward a control theory analysis of aging. Annu Rev Biochem 2008; 77:777-98; PMID:18318658; http://dx.doi.org/10.1146/annurev. biochem.77.070606.101605
10. Goldberg AA, Bourque SD, Kyryakov P, Gregg C, Boukh-Viner T, Beach A, et al. Effect of calorie restriction on the metabolic history of chronologically aging yeast. Exp Gerontol 2009; 44:555-71; PMID:19539741; http://dx.doi.org/10. 1016/j.exger.2009.06.001
11. Witten M. A return to time, cells, systems and aging: II. Relational and reliability theoretic approaches to the study of senescence in living systems. Mech Ageing Dev 1984; 27:323-40; PMID:6513610; http://dx.doi.org/10.1016/0047- 6374(84)90056-3
12. Kriete A, Sokhansanj BA, Coppock DL, West GB. Systems approaches to the networks of aging. Ageing Res Rev 2006; 5:434-48; PMID:16904954; http://dx.doi.org/10.1016/j.arr.2006.06.002
13. Budovsky A, Abramovich A, Cohen R, Chalifa-Caspi V, Fraifeld V. Longevity network: construction and implications. Mech Ageing Dev 2007; 128:117-24; PMID:17116322 http://dx.doi.org/10.1016/j.mad.2006.11.018
14. Curtis C, Landis GN, Folk D, Wehr NB, Hoe N, Waskar M, 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
15. Xue H, Xian B, Dong D, Xia K, Zhu S, Zhang Z, et al. A modular network model of aging. Mol Syst Biol 2007; 3:147; PMID:18059442; http://dx.doi.org/10. 1038/msb4100189
16. Managbanag JR, Witten TM, Bonchev D, Fox LA, Tsuchiya M, Kennedy BK, et al. Shortest-path network analysis is a useful approach toward identifying genetic determinants of longevity. PLoS ONE 2008; 3:e3802; PMID:19030232; http://dx.doi.org/10.1371/journal.pone.0003802
17. Barea F, Bonatto D. Aging defined by a chronologic-replicative protein network in Saccharomyces fcerevisiae: an interactome analysis. Mech Ageing Dev 2009; 130:444-60; PMID:19433103; http://dx.doi.org/10.1016/j.mad.2009.04.005
18. Lorenz DR, Cantor CR, Collins JJ. A network biology approach to aging in yeast. Proc Natl Acad Sci USA 2009; 106:1145-50; PMID:19164565; http://dx.doi.org/10.1073/pnas.0812551106
19. Simkó GI, Gyurkó D, Veres DV, Nánási T, Csermely P. Network strategies to understand the aging process and help age-related drug design. Genome Med 2009; 1:90; PMID:19804610; http://dx.doi.org/10.1186/gm90
20. Borklu Yucel E, Ulgen KO. A network-based approach on elucidating the multi-faceted nature of chronological aging in S. cerevisiae. PLoS ONE 2011; 6:e29284; PMID:22216232; http://dx.doi.org/10.1371/journal.pone.0029284
21. Dillin A, Hsu AL, Arantes-Oliveira N, Lehrer-Graiwer J, Hsin H, Fraser AG, et al. Rates of behavior and aging specified by mitochondrial function during development. Science 2002; 298:2398-401; PMID:12471266; http://dx.doi.org/10.1126/science.1077780
22. Rea SL, Ventura N, Johnson TE. Relationship between mitochondrial electron transport chain dysfunction, development, and life extension in Caenorhabditis elegans. PLoS Biol 2007; 5:e259; PMID:17914900; http://dx.doi.org/10.1371/journal.pbio.0050259
23. Butler JA, Ventura N, Johnson TE, Rea SL. Long-lived mitochondrial (Mit) mutants of Caenorhabditis elegans utilize a novel metabolism. FASEB J 2010; 24:4977-88; PMID:20732954; http://dx.doi.org/10.1096/fj.10-162941
24. Gallo M, Park D, Riddle DL. Increased longevity of some C. elegans mitochondrial mutants explained by activation of an alternative energy-producing pathway. Mech Ageing Dev 2011; 132:515-8; PMID:21884719; http://dx.doi.org/10. 1016/j.mad.2011.08.004
25. Durieux J, Wolff S, Dillin A. The cell-non-autonomous nature of electron transport chain-mediated longevity. Cell 2011; 144:79-91; PMID:21215371; http://dx.doi.org/10.1016/j.cell.2010.12.016
26. Dillin A, Crawford DK, Kenyon C. Timing requirements for insulin/IGF-1 signaling in C. elegans. Science 2002; 298:830-4; PMID:12399591; http://dx.doi.org/10.1126/science.1074240
27. Panowski SH, Dillin A. Signals of youth: endocrine regulation of aging in Caenorhabditis elegans. Trends Endocrinol Metab 2009; 20:259-64; PMID:19646896; http://dx.doi.org/10.1016/j.tem.2009.03.006
28. Panowski SH, Wolff S, Aguilaniu H, Durieux J, Dillin A. PHA-4/Foxa mediates diet-restrictioninduced longevity of C. elegans. Nature 2007; 447:550-5; PMID:17476212; http://dx.doi.org/10.1038/nature05837
29. Weindruch R, Walford RL. Dietary restriction in mice beginning at 1 year of age: effect on lifespan and spontaneous cancer incidence. Science 1982; 215:1415-8; PMID:7063854; http://dx.doi.org/10.1126/science.7063854
30. Yu BP, Masoro EJ, McMahan CA. Nutritional influences on aging of Fischer 344 rats: I. Physical, metabolic, and longevity characteristics. J Gerontol 1985; 40:657-70; PMID:4056321
31. Masoro EJ. Overview of caloric restriction and ageing. Mech Ageing Dev 2005; 126:913-22; PMID:15885745; http://dx.doi.org/10.1016/j.mad.2005.03.012
32. Harrison DE, Strong R, Sharp ZD, Nelson JF, Astle CM, Flurkey K, et al. Rapamycin fed late in life extends lifespan in genetically heterogeneous mice. Nature 2009; 460:392-5; PMID:19587680
33. Goldberg AA, Richard VR, Kyryakov P, Bourque SD, Beach A, Burstein MT, et al. Chemical genetic screen identifies lithocholic acid as an anti-aging compound that extends yeast chronological lifespan in a TOR-independent manner, by modulating housekeeping longevity assurance processes. Aging (Albany NY) 2010; 2:393-414; PMID:20622262
34. Kaeberlein M. Lessons on longevity from budding yeast. Nature 2010; 464:513-9; PMID:20336133; http://dx.doi.org/10.1038/nature08981
35. Blagosklonny MV, Hall MN. Growth and aging: a common molecular mechanism. Aging (Albany NY) 2009; 1:357-62; PMID:20157523
36. Anisimov VN, Zabezhinski MA, Popovich IG, Piskunova TS, Semenchenko AV, Tyndyk ML, et al. Rapamycin extends maximal lifespan in cancer-prone mice. Am J Pathol 2010; 176:2092-7; PMID:20363920; http://dx.doi.org/10.2353/ajpath.2010. 091050
37. Anisimov VN, Berstein LM, Popovich IG, Zabezhinski MA, Egormin PA, Piskunova TS, et al. If started early in life, metformin treatment increases lifespan and postpones tumors in female SHR mice. Aging (Albany NY) 2011; 3:148-57; PMID:21386129
38. Anisimov VN, Zabezhinski MA, Popovich IG, Piskunova TS, Semenchenko AV, Tyndyk ML, et al. Rapamycin increases lifespan and inhibits spontaneous tumorigenesis in inbred female mice. Cell Cycle 2011; 10:4230-6; PMID:22107964; http://dx.doi.org/10.4161/cc.10.24.18486
39. Miller RA, Harrison DE, Astle CM, Baur JA, Boyd AR, de Cabo R, et al. Rapamycin, but not resveratrol or simvastatin, extends lifespan of genetically heterogeneous mice. J Gerontol A Biol Sci Med Sci 2011; 66:191-201; PMID:20974732; http://dx.doi.org/10.1093/gerona/glq178
40. Guarente LP, Partridge L, Wallace DC, eds. Molecular Biology of Aging. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, 2008:610 pages.
41. Fannjiang Y, Cheng WC, Lee SJ, Qi B, Pevsner J, McCaffery JM, et al. Mitochondrial fission proteins regulate programmed cell death in yeast. Genes Dev 2004; 18:2785-97; PMID:15520274; http://dx.doi.org/10.1101/gad.1247904
42. Pozniakovsky AI, Knorre DA, Markova OV, Hyman AA, Skulachev VP, Severin FF. Role of mitochondria in the pheromone- and amiodarone-induced programmed death of yeast. J Cell Biol 2005; 168:257-69; PMID:15657396; http://dx.doi.org/10.1083/jcb.200408145
43. Pereira C, Silva RD, Saraiva L, Johansson B, Sousa MJ, Côrte-Real M. Mitochondria-dependent apoptosis in yeast. Biochim Biophys Acta 2008; 1783:1286-302; PMID:18406358.
44. Carmona-Gutierrez D, Eisenberg T, Büttner S, Meisinger C, Kroemer G, Madeo F. Apoptosis in yeast: triggers, pathways, subroutines. Cell Death Differ 2010; 17:763-73; PMID:20075938; http://dx.doi.org/10.1038/cdd.2009.219
45. Wissing S, Ludovico P, Herker E, Büttner S, Engelhardt SM, Decker T, et al. An AIF orthologue regulates apoptosis in yeast. J Cell Biol 2004; 166:969-74; PMID:15381687; http://dx.doi.org/10.1083/jcb.200404138
46. Büttner S, Eisenberg T, Carmona-Gutierrez D, Ruli D, Knauer H, Ruckenstuhl C, et al. Endonuclease G regulates budding yeast life and death. Mol Cell 2007; 25:233-46; PMID:17244531; http://dx.doi.org/10.1016/j.molcel.2006. 12.021
47. Ludovico P, Rodrigues F, Almeida A, Silva MT, Barrientos A, Côrte-Real M. Cytochrome c release and mitochondria involvement in programmed cell death induced by acetic acid in Saccharomyces cerevisiae. Mol Biol Cell 2002; 13:2598-606; PMID:12181332; http://dx.doi.org/10.1091/mbc.E01- 12-0161
48. Pereira C, Camougrand N, Manon S, Sousa MJ, Côrte-Real M. ADP/ATP carrier is required for mitochondrial outer membrane permeabilization and cytochrome c release in yeast apoptosis. Mol Microbiol 2007; 66:571-82; PMID:17822411; http://dx.doi.org/10.1111/j.1365-2958.2007.05926.x
49. Taylor RC, Cullen SP, Martin SJ. Apoptosis: controlled demolition at the cellular level. Nat Rev Mol Cell Biol 2008; 9:231-41; PMID:18073771; http://dx.doi.org/10.1038/nrm2312
50. Ludovico P, Rodrigues F, Almeida A, Silva MT, Barrientos A, Côrte-Real M. Cytochrome c release and mitochondria involvement in programmed cell death induced by acetic acid in Saccharomyces cerevisiae. Mol Biol Cell 2002; 13:2598-606; PMID:12181332; http://dx.doi.org/10.1091/mbc.E01- 12-0161
51. Silva RD, Sotoca R, Johansson B, Ludovico P, Sansonetty F, Silva MT, et al. Hyperosmotic stress induces metacaspase- and mitochondria-dependent apoptosis in Saccharomyces cerevisiae. Mol Microbiol 2005; 58:824-34; PMID:16238630; http://dx.doi.org/10.1111/j.1365-2958.2005.04868.x
52. Yang H, Ren Q, Zhang Z. Cleavage of Mcd1 by caspase-like protease Esp1 promotes apoptosis in budding yeast. Mol Biol Cell 2008; 19:2127-34. PMID:18321989; http://dx.doi.org/10.1091/mbc.E07-11-1113
53. Madeo F, Herker E, Maldener C, Wissing S, Lächelt S, Herlan M, et al. A caspase-related protease regulates apoptosis in yeast. Mol Cell 2002; 9:911-7; PMID:11983181; http://dx.doi.org/10.1016/S1097-2765(02)00501-4
54. Fabrizio P, Battistella L, Vardavas R, Gattazzo C, Liou LL, Diaspro A, et al. Superoxide is a mediator of an altruistic aging program in Saccharomyces cerevisiae. J Cell Biol 2004; 166:1055-67; PMID:15452146; http://dx.doi.org/10. 1083/jcb.200404002
55. Herker E, Jungwirth H, Lehmann KA, Maldener C, Fröhlich KU, Wissing S, et al. Chronological aging leads to apoptosis in yeast. J Cell Biol 2004; 164:501-7; PMID:14970189; http://dx.doi.org/10.1083/jcb.200310014
56. Mazzoni C, Herker E, Palermo V, Jungwirth H, Eisenberg T, Madeo F, et al. Yeast caspase 1 links messenger RNA stability to apoptosis in yeast. EMBO Rep 2005; 6:1076-81; PMID:16170310; http://dx.doi.org/10.1038/sj.embor.7400514
57. Allen C, Büttner S, Aragon AD, Thomas JA, Meirelles O, Jaetao JE, et al. Isolation of quiescent and non-quiescent cells from yeast stationary-phase cultures. J Cell Biol 2006; 174:89-100; PMID:16818721; http://dx.doi.org/10. 1083/jcb.200604072
58. Li W, Sun L, Liang Q, Wang J, Mo W, Zhou B. Yeast AMID homologue Ndi1p displays respiration-restricted apoptotic activity and is involved in chronological aging. Mol Biol Cell 2006; 17:1802-11; PMID:16436509; http://dx.doi.org/10.1091/mbc.E05-04-0333
59. Aragon AD, Rodriguez AL, Meirelles O, Roy S, Davidson GS, Tapia PH, et al. Characterization of differentiated quiescent and nonquiescent cells in yeast stationary-phase cultures. Mol Biol Cell 2008; 19:1271-8; PMID:18199684; http://dx.doi.org/10.1091/mbc.E07-07-0666
60. Fabrizio P, Longo VD. Chronological aging-induced apoptosis in yeast. Biochim Biophys Acta 2008; 1783:1280-5; PMID:18445486.
61. Laun P, Heeren G, Rinnerthaler M, Rid R, Kössler S, Koller L, et al. Senescence and apoptosis in yeast mother cell-specific aging and in higher cells: a short review. Biochim Biophys Acta 2008; 1783:1328-34; PMID:18342634.
62. Büttner S, Eisenberg T, Herker E, Carmona-Gutierrez D, Kroemer G, Madeo F. Why yeast cells can undergo apoptosis: death in times of peace, love, and war. J Cell Biol 2006; 175:521-5; PMID:17101700; http://dx.doi.org/10.1083/ jcb.200608098
63. Goldberg AA, Bourque SD, Kyryakov P, Boukh-Viner T, Gregg C, Beach A, et al. A novel function of lipid droplets in regulating longevity. Biochem Soc Trans 2009; 37:1050-5; PMID:19754450; http://dx.doi.org/10.1042/BST0371050
64. Beach A, Titorenko VI. In search of housekeeping pathways that regulate longevity. Cell Cycle 2011; 10:3042-4; PMID:21862878; http://dx.doi.org/10.4161/ cc.10.18.16947
65. Titorenko VI, Terlecky SR. Peroxisome metabolism and cellular aging. Traffic 2011; 12:252-9; PMID:21083858; http://dx.doi.org/10.1111/j.1600-0854. 2010.01144.x
66. Bitterman KJ, Medvedik O, Sinclair DA. Longevity regulation in Saccharomyces cerevisiae: linking metabolism, genome stability, and heterochromatin. Microbiol Mol Biol Rev 2003; 67:376-99; PMID:12966141; http://dx.doi.org/10.1128/MMBR.67.3.376-399.2003
67. Pang CY, Ma YS, Wei YU. MtDNA mutations, functional decline and turnover of mitochondria in aging. Front Biosci 2008; 13:3661-75; PMID:18508463; http://dx.doi.org/10.2741/2957
68. Sinclair DA, Oberdoerffer P. The ageing epigenome: damaged beyond repair? Ageing Res Rev 2009; 8:189-98; PMID:19439199; http://dx.doi.org/10.1016/j.arr. 2009.04.004
69. D'Autréaux B, Toledano MB. ROS as signalling molecules: mechanisms that generate specificity in ROS homeostasis. Nat Rev Mol Cell Biol 2007; 8:813-24; PMID:17848967; http://dx.doi.org/10.1038/nrm2256
70. Giorgio M, Trinei M, Migliaccio E, Pelicci PG. Hydrogen peroxide: a metabolic by-product or a common mediator of ageing signals? Nat Rev Mol Cell Biol 2007; 8:722-8; PMID:17700625; http://dx.doi.org/10.1038/nrm2240
71. Veal EA, Day AM, Morgan BA. Hydrogen peroxide sensing and signaling. Mol Cell 2007; 26:1-14; PMID:17434122; http://dx.doi.org/10.1016/j.molcel.2007.03. 016
72. Gems D, Partridge L. Stress-response hormesis and aging: "that which does not kill us makes us stronger. Cell Metab 2008; 7:200-3; PMID:18316025; http://dx.doi.org/10.1016/j.cmet.2008.01.001
73. Wei M, Fabrizio P, Hu J, Ge H, Cheng C, Li L, et al. Lifespan extension by calorie restriction depends on Rim15 and transcription factors downstream of Ras/PKA, Tor, and Sch9. PLoS Genet 2008; 4:e13; PMID:18225956; http://dx.doi.org/10.1371/journal.pgen.0040013
74. Bonawitz ND, Chatenay-Lapointe M, Pan Y, Shadel GS. Reduced TOR signaling extends chronological lifespan via increased respiration and upregulation of mitochondrial gene expression. Cell Metab 2007; 5:265-77; PMID:17403371; http://dx.doi.org/10.1016/j.cmet.2007.02.009
75. Pan Y, Shadel GS. Extension of chronological lifespan by reduced TOR signaling requires down-regulation of Sch9p and involves increased mitochondrial OXPHOS complex density. Aging (Albany NY) 2009; 1:131-45; PMID:20157595
76. Pan Y, Schroeder EA, Ocampo A, Barrientos A, Shadel GS. Regulation of yeast chronological lifespan by TORC1 via adaptive mitochondrial ROS signaling. Cell Metab 2011; 13:668-78; PMID:21641548; http://dx.doi.org/10.1016/j.cmet. 2011.03.018
77. Ocampo A, Liu J, Schroeder EA, Shadel GS, Barrientos A. Mitochondrial respiratory thresholds regulate yeast chronological lifespan and its extension by caloric restriction. Cell Metab 2012; 16:55-67; PMID:22768839; http://dx.doi.org/10.1016/j.cmet.2012.05.013
78. Kyryakov P, Beach A, Richard VR, Burstein MT, Leonov A, Levy S, et al. Caloric restriction extends yeast chronological lifespan by altering a pattern of age-related changes in trehalose concentration. Front Physiol 2012; 3:256; PMID:22783207; http://dx.doi.org/10.3389/fphys.2012.00256
79. Longo VD, Mitteldorf J, Skulachev VP. Programmed and altruistic ageing. Nat Rev Genet 2005; 6:866-72; PMID:16304601; http://dx.doi.org/10.1038/nrg1706
80. Skulachev VP, Longo VD. Aging as a mitochondria-mediated atavistic program: can aging be switched off? Ann N Y Acad Sci 2005; 1057:145-64; PMID:16399892; http://dx.doi.org/10.1196/annals.1356.009
81. Blagosklonny MV. Aging and immortality: quasiprogrammed senescence and its pharmacologic inhibition. Cell Cycle 2006; 5:2087-102; PMID:17012837; http://dx.doi.org/10.4161/cc.5.18.3288
82. Blagosklonny MV. Paradoxes of aging. Cell Cycle 2007; 6:2997-3003; PMID:18156807; http://dx.doi.org/10.4161/cc.6.24.5124
83. Blagosklonny MV. Program-like aging and mitochondria: instead of random damage by free radicals. J Cell Biochem 2007; 102:1389-99; PMID:17975792; http://dx.doi.org/10.1002/jcb.21602
84. Blagosklonny MV. TOR-driven aging: speeding car without brakes. Cell Cycle 2009; 8:4055-9; PMID:19923900; http://dx.doi.org/10.4161/cc.8.24.10310
85. Blagosklonny MV. Revisiting the antagonistic pleiotropy theory of aging: TOR-driven program and quasiprogram. Cell Cycle 2010; 9:3151-6; PMID:20724817; http://dx.doi.org/10.4161/cc.9.16.13120