Enhanced Longevity by Ibuprofen, Conserved in Multiple Species, Occurs in Yeast through Inhibition of Tryptophan Import

PLoS Genetics

Volumn 10, Issue 12, 2014, Pages

  He, Chong ^a   Tsuchiyama, Scott K ^a   Nguyen, Quynh T ^b   Plyusnina, Ekaterina N ^c,d   Terrill, Samuel R ^b   Sahibzada, Sarah ^b   Patel, Bhumil ^a   Faulkner, Alena R ^a   Shaposhnikov, Mikhail V ^c,d   Tian, Ruilin ^a   Tsuchiya, Mitsuhiro ^a   Kaeberlein, Matt ^e   Moskalev, Alexey A ^c,d,f   Kennedy, Brian K ^a   Polymenis, Michael ^b  

^a BUCK INSTITUTE FOR RESEARCH ON AGING   (United States)

^b TEXAS A AND M UNIVERSITY   (United States)

^c INSTITUTE OF BIOLOGY   (Russian Federation)

^d SYKTYVKAR STATE UNIVERSITY   (Russian Federation)

^e UNIVERSITY OF WASHINGTON   (United States)

^f MOSCOW INSTITUTE OF PHYSICS AND TECHNOLOGY   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

IBUPROFEN; PERMEASE; PROTEIN TAT2P; TRYPTOPHAN; UNCLASSIFIED DRUG; AMINO ACID TRANSPORTER; NONSTEROID ANTIINFLAMMATORY AGENT; SACCHAROMYCES CEREVISIAE PROTEIN; TAT2 PROTEIN, S CEREVISIAE;

AGING; AMINO ACID ANALYSIS; AMINO ACID TRANSPORT; ANIMAL EXPERIMENT; ARTICLE; CAENORHABDITIS ELEGANS; CELL CYCLE G1 PHASE; CELL CYCLE PROGRESSION; CELL SIZE; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; ENZYME ASSAY; IMMUNOBLOTTING; LONGEVITY; NONHUMAN; REAL TIME POLYMERASE CHAIN REACTION; SACCHAROMYCES CEREVISIAE; YEAST CELL; ANIMAL; DRUG EFFECTS; DRUG SCREENING; G1 PHASE CELL CYCLE CHECKPOINT; METABOLISM; PHYSIOLOGY; PROTEIN STABILITY; TRANSPORT AT THE CELLULAR LEVEL;

CAENORHABDITIS ELEGANS; DROSOPHILA MELANOGASTER; EUKARYOTA; SACCHAROMYCES CEREVISIAE;

AMINO ACID TRANSPORT SYSTEMS; ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; BIOLOGICAL TRANSPORT; CAENORHABDITIS ELEGANS; DROSOPHILA MELANOGASTER; DRUG EVALUATION, PRECLINICAL; G1 PHASE CELL CYCLE CHECKPOINTS; IBUPROFEN; LONGEVITY; PROTEIN STABILITY; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRYPTOPHAN;

EID: 84919608398     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004860     Document Type: Article

References (81)

1. Niccoli T, Partridge L, (2012) Ageing as a risk factor for disease. Curr Biol 22: R741–752.
2. Kennedy BK, Pennypacker JK, (2014) Drugs that modulate aging: the promising yet difficult path ahead. Transl Res 163: 456–465.
3. Lucanic M, Lithgow GJ, Alavez S, (2013) Pharmacological lifespan extension of invertebrates. Ageing Res Rev 12: 445–458.
4. McCormick MA, Kennedy BK, (2012) Genome-scale studies of aging: challenges and opportunities. Curr Genomics 13: 500–507.
5. Johnson SC, Rabinovitch PS, Kaeberlein M, (2013) mTOR is a key modulator of ageing and age-related disease. Nature 493: 338–345.
6. McCormick MA, Tsai SY, Kennedy BK, (2011) TOR and ageing: a complex pathway for a complex process. Philos Trans R Soc Lond B Biol Sci 366: 17–27.
7. Martin-Montalvo A, Mercken EM, Mitchell SJ, Palacios HH, Mote PL, et al. (2013) Metformin improves healthspan and lifespan in mice. Nat Commun 4: 2192.
8. Baur JA, Ungvari Z, Minor RK, Le Couteur DG, de Cabo R, (2012) Are sirtuins viable targets for improving healthspan and lifespan? Nat Rev Drug Discov 11: 443–461.
9. Hubbard BP, Sinclair DA, (2014) Small molecule SIRT1 activators for the treatment of aging and age-related diseases. Trends Pharmacol Sci 35: 146–154.
10. Lopez-Otin C, Blasco MA, Partridge L, Serrano M, Kroemer G, (2013) The hallmarks of aging. Cell 153: 1194–1217.
11. Wasko BM, Kaeberlein M, (2014) Yeast replicative aging: a paradigm for defining conserved longevity interventions. FEMS Yeast Research 14: 148–159.
12. Longo VD, Shadel GS, Kaeberlein M, Kennedy B, (2012) Replicative and Chronological Aging in Saccharomyces cerevisiae. Cell Metab 16: 18–31.
13. Steffen KK, Kennedy BK, Kaeberlein M (2009) Measuring Replicative Life Span in the Budding Yeast. J Vis Exp: e1209.
14. Steinkraus KA, Kaeberlein M, Kennedy BK, (2008) Replicative aging in yeast: the means to the end. Annu Rev Cell Dev Biol 24: 29–54.
15. Smith ED, Tsuchiya M, Fox LA, Dang N, Hu D, et al. (2008) Quantitative evidence for conserved longevity pathways between divergent eukaryotic species. Genome Res 18: 564–570.
16. Furey SA, Waksman JA, Dash BH, (1992) Nonprescription ibuprofen: side effect profile. Pharmacotherapy 12: 403–407.
17. Kellstein DE, Waksman JA, Furey SA, Binstok G, Cooper SA, (1999) The safety profile of nonprescription ibuprofen in multiple-dose use: a meta-analysis. J Clin Pharmacol 39: 520–532.
18. DeArmond B, Francisco CA, Lin JS, Huang FY, Halladay S, et al. (1995) Safety profile of over-the-counter naproxen sodium. Clin Ther 17: 587–601 discussion 586.
19. Rainsford KD, Roberts SC, Brown S, (1997) Ibuprofen and paracetamol: relative safety in non-prescription dosages. J Pharm Pharmacol 49: 345–376.
20. Rome LH, Lands WE, (1975) Structural requirements for time-dependent inhibition of prostaglandin biosynthesis by anti-inflammatory drugs. Proc Natl Acad Sci U S A 72: 4863–4865.
21. Vlad SC, Miller DR, Kowall NW, Felson DT, (2008) Protective effects of NSAIDs on the development of Alzheimer disease. Neurology 70: 1672–1677.
22. Gao X, Chen H, Schwarzschild MA, Ascherio A, (2011) Use of ibuprofen and risk of Parkinson disease. Neurology 76: 863–869.
23. McSharry C, (2011) Parkinson disease: Could over-the-counter treatment protect against Parkinson disease? Nat Rev Neurol 7: 244.
24. Cavalier-Smith T, (2010) Kingdoms Protozoa and Chromista and the eozoan root of the eukaryotic tree. Biol Lett 6: 342–345.
25. Simmons DL, Botting RM, Hla T, (2004) Cyclooxygenase isozymes: the biology of prostaglandin synthesis and inhibition. Pharmacol Rev 56: 387–437.
26. Morita M, Osoda K, Yamazaki M, Shirai F, Matsuoka N, et al. (2009) Effects of non-steroidal anti-inflammatory drugs on Abeta deposition in Abeta(1-42) transgenic C. elegans. Brain Res 1295: 186–191.
27. Tootle TL, Spradling AC, (2008) Drosophila Pxt: a cyclooxygenase-like facilitator of follicle maturation. Development 135: 839–847.
28. Varvas K, Kurg R, Hansen K, Jarving R, Jarving I, et al. (2009) Direct evidence of the cyclooxygenase pathway of prostaglandin synthesis in arthropods: genetic and biochemical characterization of two crustacean cyclooxygenases. Insect Biochem Mol Biol 39: 851–860.
29. Pages M, Rosello J, Casas J, Gelpi E, Gualde N, et al. (1986) Cyclooxygenase and lipoxygenase-like activity in Drosophila melanogaster. Prostaglandins 32: 729–740.
30. Tucker CL, Fields S, (2004) Quantitative genome-wide analysis of yeast deletion strain sensitivities to oxidative and chemical stress. Comp Funct Genomics 5: 216–224.
31. Schmidt A, Hall MN, Koller A, (1994) Two FK506 resistance-conferring genes in Saccharomyces cerevisiae, TAT1 and TAT2, encode amino acid permeases mediating tyrosine and tryptophan uptake. Mol Cell Biol 14: 6597–6606.
32. Ljungdahl PO, Daignan-Fornier B, (2012) Regulation of amino acid, nucleotide, and phosphate metabolism in Saccharomyces cerevisiae. Genetics 190: 885–929.
33. Regenberg B, During-Olsen L, Kielland-Brandt MC, Holmberg S, (1999) Substrate specificity and gene expression of the amino-acid permeases in Saccharomyces cerevisiae. Curr Genet 36: 317–328.
34. Heitman J, Koller A, Kunz J, Henriquez R, Schmidt A, et al. (1993) The immunosuppressant FK506 inhibits amino acid import in Saccharomyces cerevisiae. Mol Cell Biol 13: 5010–5019.
35. Loewith R, Hall MN, (2011) Target of rapamycin (TOR) in nutrient signaling and growth control. Genetics 189: 1177–1201.
36. Beck T, Schmidt A, Hall MN, (1999) Starvation induces vacuolar targeting and degradation of the tryptophan permease in yeast. J Cell Biol 146: 1227–1238.
37. Schmidt A, Beck T, Koller A, Kunz J, Hall MN, (1998) The TOR nutrient signalling pathway phosphorylates NPR1 and inhibits turnover of the tryptophan permease. EMBO J 17: 6924–6931.
38. Ghaemmaghami S, Huh WK, Bower K, Howson RW, Belle A, et al. (2003) Global analysis of protein expression in yeast. Nature 425: 737–741.
39. Belle A, Tanay A, Bitincka L, Shamir R, O'Shea EK, (2006) Quantification of protein half-lives in the budding yeast proteome. Proc Natl Acad Sci U S A 103: 13004–13009.
40. Mousley CJ, Yuan P, Gaur NA, Trettin KD, Nile AH, et al. (2012) A sterol-binding protein integrates endosomal lipid metabolism with TOR signaling and nitrogen sensing. Cell 148: 702–715.
41. Valenzuela L, Aranda C, Gonzalez A, (2001) TOR modulates GCN4-dependent expression of genes turned on by nitrogen limitation. J Bacteriol 183: 2331–2334.
42. Cherkasova VA, Hinnebusch AG, (2003) Translational control by TOR and TAP42 through dephosphorylation of eIF2alpha kinase GCN2. Genes Dev 17: 859–872.
43. Hinnebusch AG, (1985) A hierarchy of trans-acting factors modulates translation of an activator of amino acid biosynthetic genes in Saccharomyces cerevisiae. Mol Cell Biol 5: 2349–2360.
44. Crespo JL, Helliwell SB, Wiederkehr C, Demougin P, Fowler B, et al. (2004) NPR1 kinase and RSP5-BUL1/2 ubiquitin ligase control GLN3-dependent transcription in Saccharomyces cerevisiae. J Biol Chem 279: 37512–37517.
45. Tate JJ, Cooper TG, (2013) Five conditions commonly used to down-regulate tor complex 1 generate different physiological situations exhibiting distinct requirements and outcomes. J Biol Chem 288: 27243–27262.
46. Kaeberlein M, Powers RW, 3rdSteffen KK, Westman EA, Hu D, et al. (2005) Regulation of yeast replicative life span by TOR and Sch9 in response to nutrients. Science 310: 1193–1196.
47. Howell AS, Lew DJ, (2012) Morphogenesis and the cell cycle. Genetics 190: 51–77.
48. Hoose SA, Rawlings JA, Kelly MM, Leitch MC, Ababneh QO, et al. (2012) A systematic analysis of cell cycle regulators in yeast reveals that most factors act independently of cell size to control initiation of division. PLoS Genet 8: e1002590.
49. Truong SK, McCormick RF, Polymenis M, (2013) Genetic Determinants of Cell Size at Birth and Their Impact on Cell Cycle Progression in Saccharomyces cerevisiae. G3 (Bethesda) 3: 1525–1530.
50. Giaever G, Chu AM, Ni L, Connelly C, Riles L, et al. (2002) Functional profiling of the Saccharomyces cerevisiae genome. Nature 418: 387–391.
51. Jorgensen P, Nishikawa JL, Breitkreutz BJ, Tyers M, (2002) Systematic identification of pathways that couple cell growth and division in yeast. Science 297: 395–400.
52. Di Talia S, Skotheim JM, Bean JM, Siggia ED, Cross FR, (2007) The effects of molecular noise and size control on variability in the budding yeast cell cycle. Nature 448: 947–951.
53. Turner JJ, Ewald JC, Skotheim JM, (2012) Cell size control in yeast. Curr Biol 22: R350–359.
54. Strong R, Miller RA, Astle CM, Floyd RA, Flurkey K, et al. (2008) Nordihydroguaiaretic acid and aspirin increase lifespan of genetically heterogeneous male mice. Aging Cell 7: 641–650.
55. Ching TT, Chiang WC, Chen CS, Hsu AL, (2011) Celecoxib extends C. elegans lifespan via inhibition of insulin-like signaling but not cyclooxygenase-2 activity. Aging Cell 10: 506–519.
56. Janssen GM, Venema JF, (1985) Ibuprofen: plasma concentrations in man. J Int Med Res 13: 68–73.
57. Mehlisch DR, Sykes J (2013) Ibuprofen blood plasma levels and onset of analgesia. Int J Clin Pract Suppl: 3–8.
58. Braus GH, (1991) Aromatic amino acid biosynthesis in the yeast Saccharomyces cerevisiae: a model system for the regulation of a eukaryotic biosynthetic pathway. Microbiol Rev 55: 349–370.
59. De Marte ML, Enesco HE, (1986) Influence of low tryptophan diet on survival and organ growth in mice. Mech Ageing Dev 36: 161–171.
60. Oxenkrug GF, Navrotskaya V, Voroboyva L, Summergrad P, (2011) Extension of life span of Drosophila melanogaster by the inhibitors of tryptophan-kynurenine metabolism. Fly (Austin) 5: 307–309.
61. van der Goot AT, Nollen EA, (2013) Tryptophan metabolism: entering the field of aging and age-related pathologies. Trends Mol Med 19: 336–344.
62. Stone TW, Stoy N, Darlington LG, (2013) An expanding range of targets for kynurenine metabolites of tryptophan. Trends Pharmacol Sci 34: 136–143.
63. Braidy N, Guillemin GJ, Grant R, (2011) Effects of Kynurenine Pathway Inhibition on NAD Metabolism and Cell Viability in Human Primary Astrocytes and Neurons. Int J Tryptophan Res 4: 29–37.
64. Heitman J, Movva NR, Hall MN, (1991) Targets for cell cycle arrest by the immunosuppressant rapamycin in yeast. Science 253: 905–909.
65. Hartwell LH, Unger MW, (1977) Unequal division in Saccharomyces cerevisiae and its implications for the control of cell division. J Cell Biol 75: 422–435.
66. Johnston GC, Pringle JR, Hartwell LH, (1977) Coordination of growth with cell division in the yeast Saccharomyces cerevisiae. Exp Cell Res 105: 79–98.
67. Bilinski T, Zadrag-Tecza R, Bartosz G, (2012) Hypertrophy hypothesis as an alternative explanation of the phenomenon of replicative aging of yeast. FEMS Yeast Res 12: 97–101.
68. Zadrag R, Kwolek-Mirek M, Bartosz G, Bilinski T, (2006) Relationship between the replicative age and cell volume in Saccharomyces cerevisiae. Acta Biochimica Polonica 53: 747–751.
69. Yang J, Dungrawala H, Hua H, Manukyan A, Abraham L, et al. (2011) Cell size and growth rate are major determinants of replicative lifespan. Cell Cycle 10: 144–155.
70. Kaeberlein M, (2012) Hypertrophy and senescence factors in yeast aging. A reply to Bilinski et al. FEMS Yeast Res 12: 269–270.
71. Ganley AR, Breitenbach M, Kennedy BK, Kobayashi T, (2012) Yeast hypertrophy: cause or consequence of aging? Reply to Bilinski et al. FEMS Yeast Res 12: 267–268.
72. Delaney JR, Sutphin GL, Dulken B, Sim S, Kim JR, et al. (2011) Sir2 deletion prevents lifespan extension in 32 long-lived mutants. Aging Cell 10: 1089–1091.
73. Delaney JR, Murakami CJ, Olsen B, Kennedy BK, Kaeberlein M, (2011) Quantitative evidence for early life fitness defects from 32 longevity-associated alleles in yeast. Cell Cycle 10: 156–165.
74. Gems D, Partridge L, (2008) Stress-response hormesis and aging: "that which does not kill us makes us stronger". Cell Metab 7: 200–203.
75. Kaiser C, Michaelis S, Mitchell A, Cold Spring Harbor Laboratory. (1994) Methods in yeast genetics: a Cold Spring Harbor Laboratory course manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press. vii, 234 p. p.
76. Heinrikson RL, Meredith SC, (1984) Amino acid analysis by reverse-phase high-performance liquid chromatography: precolumn derivatization with phenylisothiocyanate. Anal Biochem 136: 65–74.
77. Kushnirov VV, (2000) Rapid and reliable protein extraction from yeast. Yeast 16: 857–860.
78. Sutphin GL, Kaeberlein M (2009) Measuring Caenorhabditis elegans Life Span on Solid Media. J Vis Exp: e1152.
79. Brejning J, Norgaard S, Scholer L, Morthorst TH, Jakobsen H, et al. (2014) Loss of NDG-4 extends lifespan and stress resistance in Caenorhabditis elegans. Aging Cell 13: 156–164.
80. Ashburner M (1989) Drosophila. A laboratory handbook.: Cold Spring Harbor, N.Y.: Cold Spring Harbor Laboratory, 1989. 1331 p.
81. Wang C, Li Q, Redden D, Weindruch R, Allison D, (2004) Statistical methods for testing effects on "maximum lifespan". Mech Ageing Dev 125: 629–632.