Lifespan Extension by Methionine Restriction Requires Autophagy-Dependent Vacuolar Acidification

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Health- or lifespan-prolonging regimes would be beneficial at both the individual and the social level. Nevertheless, up to date only very few experimental settings have been proven to promote longevity in mammals. Among them is the reduction of food intake (caloric restriction) or the pharmacological administration of caloric restriction mimetics like rapamycin. The latter one, however, is accompanied by not yet fully estimated and undesirable side effects. In contrast, the limitation of one specific amino acid, namely methionine, which has also been demonstrated to elongate the lifespan of mammals, has the advantage of being a well applicable regime. Therefore, understanding the underlying mechanism of the anti-aging effects of methionine restriction is of crucial importance. With the help of the model organism yeast, we show that limitation in methionine drastically enhances autophagy, a cellular process of self-digestion that is also switched on during caloric restriction. Moreover, we demonstrate that this occurs in causal conjunction with an efficient pH decrease in the organelle responsible for the digestive capacity of the cell (the vacuole). Finally, we prove that autophagy-dependent vacuolar acidification is necessary for methionine restriction-mediated lifespan extension.

Vyšlo v časopise: Lifespan Extension by Methionine Restriction Requires Autophagy-Dependent Vacuolar Acidification. PLoS Genet 10(5): e32767. doi:10.1371/journal.pgen.1004347
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004347

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Zdroje

1. OrentreichN, MatiasJR, DeFeliceA, ZimmermanJA (1993) Low methionine ingestion by rats extends life span. J Nutr 123: 269–274 Available: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=8429371.

2. Lopez-TorresM, BarjaG (2008) Lowered methionine ingestion as responsible for the decrease in rodent mitochondrial oxidative stress in protein and dietary restriction possible implications for humans. Biochim Biophys Acta 1780: 1337–1347 Available: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=18252204.

3. CaroP, GomezJ, SanchezI, NaudiA, AyalaV, et al. (2009) Forty percent methionine restriction decreases mitochondrial oxygen radical production and leak at complex I during forward electron flow and lowers oxidative damage to proteins and mitochondrial DNA in rat kidney and brain mitochondria. Rejuvenation Res 12: 421–434 Available: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=20041736.

4. GomezJ, CaroP, SanchezI, NaudiA, JoveM, et al. (2009) Effect of methionine dietary supplementation on mitochondrial oxygen radical generation and oxidative DNA damage in rat liver and heart. J Bioenerg Biomembr 41: 309–321 Available: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=19633937.

5. SanzA, CaroP, AyalaV, Portero-OtinM, PamplonaR, et al. (2006) Methionine restriction decreases mitochondrial oxygen radical generation and leak as well as oxidative damage to mitochondrial DNA and proteins. FASEB J 20: 1064–1073 Available: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=16770005.

6. AlversAL, FishwickLK, WoodMS, HuD, ChungHS, et al. (2009) Autophagy and amino acid homeostasis are required for chronological longevity in Saccharomyces cerevisiae. Aging Cell 8: 353–369 Available: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=19302372.

7. LevineB, KroemerG (2008) Autophagy in the pathogenesis of disease. Cell 132: 27–42 Available: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=18191218.

8. AlversAL, WoodMS, HuD, KaywellAC, DunnWA, et al. (2009) Autophagy is required for extension of yeast chronological life span by rapamycin. Autophagy 5: 847–849 Available: http://www.ncbi.nlm.nih.gov/pubmed/19458476. Accessed 19 December 2012.

9. EisenbergT, KnauerH, SchauerA, BüttnerS, RuckenstuhlC, et al. (2009) Induction of autophagy by spermidine promotes longevity. Nature cell biology 11: 1305–1314 Available: http://apps.webofknowledge.com/full_record.do?product = UA&search_mode = GeneralSearch&qid = 1&SID = N2ACH54LO89J@ODMOKC&page = 6&doc = 59. Accessed 5 November 2012.

10. MadeoF, TavernarakisN, KroemerG (2010) Can autophagy promote longevity? Nat Cell Biol 12: 842–846 Available: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=20811357.

11. MorselliE, MaiuriMC, MarkakiM, MegalouE, PasparakiA, et al. (2010) Caloric restriction and resveratrol promote longevity through the Sirtuin-1-dependent induction of autophagy. Cell Death Dis 1: e10 Available: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=21364612.

12. TavernarakisN, PasparakiA, TasdemirE, MaiuriMC, KroemerG (2008) The effects of p53 on whole organism longevity are mediated by autophagy. Autophagy 4: 870–873 Available: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=18728385.

13. TakeshigeK (1992) Autophagy in yeast demonstrated with proteinase-deficient mutants and conditions for its induction. The Journal of Cell Biology 119: 301–311 Available: http://jcb.rupress.org/content/119/2/301.abstract. Accessed 5 June 2013.

14. NakamuraN, MatsuuraA, WadaY, OhsumiY (1997) Acidification of Vacuoles Is Required for Autophagic Degradation in the Yeast, Saccharomyces cerevisiae. Journal of Biochemistry 121: 338–344 Available: http://jb.oxfordjournals.org/content/121/2/338.short. Accessed 5 June 2013.

15. HughesAL, GottschlingDE (2012) An early age increase in vacuolar pH limits mitochondrial function and lifespan in yeast. Nature 492: 261–265 Available: http://www.ncbi.nlm.nih.gov/pubmed/23172144. Accessed 5 June 2013.

16. LongoVD, GrallaEB, ValentineJS (1996) Superoxide dismutase activity is essential for stationary phase survival in Saccharomyces cerevisiae. Mitochondrial production of toxic oxygen species in vivo. The Journal of biological chemistry 271: 12275–12280 Available: http://www.ncbi.nlm.nih.gov/pubmed/8647826. Accessed 23 May 2013.

17. KlionskyDJ (2007) Autophagy: from phenomenology to molecular understanding in less than a decade. Nat Rev Mol Cell Biol 8: 931–937 Available: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=17712358.

18. OhsumiY (2001) Molecular dissection of autophagy: two ubiquitin-like systems. Nat Rev Mol Cell Biol 2: 211–216 Available: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=11265251.

19. ThummM (2002) Hitchhikers guide to the vacuole-mechanisms of cargo sequestration in the Cvt and autophagic pathways. Mol Cell 10: 1257–1258 Available: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=12503998.

20. ThomasD, Surdin-KerjanY (1997) Metabolism of sulfur amino acids in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 61: 503–532 Available: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=9409150.

21. BurtnerCR, MurakamiCJ, KennedyBK, KaeberleinM (2009) A molecular mechanism of chronological aging in yeast. Cell Cycle 8: 1256–1270 Available: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=19305133.

22. WuZ, LiuSQ, HuangD (2013) Dietary Restriction Depends on Nutrient Composition to Extend Chronological Lifespan in Budding Yeast Saccharomyces cerevisiae. PloS one 8: e64448 Available: http://dx.plos.org/10.1371/journal.pone.0064448. Accessed 25 May 2013.

23. RubinszteinDC, MarinoG, KroemerG (2011) Autophagy and aging. Cell 146: 682–695 Available: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=21884931.

24. PanY, SchroederEA, OcampoA, BarrientosA, ShadelGS (2011) Regulation of yeast chronological life span by TORC1 via adaptive mitochondrial ROS signaling. Cell Metab 13: 668–678 Available: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=21641548.

25. KanePM, YamashiroCT, WolczykDF, NeffN, GoeblM, et al. (1990) Protein splicing converts the yeast TFP1 gene product to the 69-kD subunit of the vacuolar H(+)-adenosine triphosphatase. Science (New York, NY) 250: 651–657 Available: http://www.ncbi.nlm.nih.gov/pubmed/2146742. Accessed 13 March 2014.

26. HirataR, OhsumkY, NakanoA, KawasakiH, SuzukiK, et al. (1990) Molecular structure of a gene, VMA1, encoding the catalytic subunit of H(+)-translocating adenosine triphosphatase from vacuolar membranes of Saccharomyces cerevisiae. The Journal of biological chemistry 265: 6726–6733 Available: http://www.ncbi.nlm.nih.gov/pubmed/2139027. Accessed 13 March 2014.

27. JacksonDD (1997) VMA12 Encodes a Yeast Endoplasmic Reticulum Protein Required for Vacuolar H+-ATPase Assembly. Journal of Biological Chemistry 272: 25928–25934 Available: http://www.jbc.org/content/272/41/25928.long. Accessed 29 August 2013.

28. KanePM (2007) The long physiological reach of the yeast vacuolar H+-ATPase. Journal of bioenergetics and biomembranes 39: 415–421 Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2901503&tool=pmcentrez&rendertype=abstract. Accessed 27 January 2014.

29. ArisJP, AlversAL, FerraiuoloRA, FishwickLK, HanvivatpongA, et al. (2013) Autophagy and leucine promote chronological longevity and respiration proficiency during calorie restriction in yeast. Experimental gerontology 48: 1107–19.

30. PettiAA, CrutchfieldCA, RabinowitzJD, BotsteinD (2011) Survival of starving yeast is correlated with oxidative stress response and nonrespiratory mitochondrial function. Proc Natl Acad Sci U S A 108: E1089–98.

31. SutterBM, WuX, LaxmanS, TuBP (2013) Methionine Inhibits Autophagy and Promotes Growth by Inducing the SAM-Responsive Methylation of PP2A. Cell 154: 403–415 Available: http://dx.doi.org/10.1016/j.cell.2013.06.041. Accessed 7 August 2013.

32. EisenbergT, SchroederS, AndryushkovaA, PendlT, KüttnerV, et al. (2014) Nucleocytosolic Depletion of the Energy Metabolite Acetyl-Coenzyme A Stimulates Autophagy and Prolongs Lifespan. Cell Metabolism 19: 431–444 Available: http://www.cell.com/cell-metabolism/fulltext/S1550-4131(14)00066-7. Accessed 6 March 2014.

33. LaxmanS, SutterBM, WuX, KumarS, GuoX, et al. (2013) Sulfur amino acids regulate translational capacity and metabolic homeostasis through modulation of tRNA thiolation. Cell 154: 416–429 Available: http://www.ncbi.nlm.nih.gov/pubmed/23870129. Accessed 29 January 2014.

34. StephanJ, FrankeJ, Ehrenhofer-MurrayAE (2013) Chemical genetic screen in fission yeast reveals roles for vacuolar acidification, mitochondrial fission, and cellular GMP levels in lifespan extension. Aging cell 12: 574–583 Available: http://www.ncbi.nlm.nih.gov/pubmed/23521895. Accessed 27 January 2014.

35. SuzukiSW, OnoderaJ, OhsumiY (2011) Starvation induced cell death in autophagy-defective yeast mutants is caused by mitochondria dysfunction. PLoS One 6: e17412 Available: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=21364763.

36. MatecicM, SmithDL, PanX, MaqaniN, BekiranovS, et al. (2010) A microarray-based genetic screen for yeast chronological aging factors. PLoS genetics 6: e1000921 Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2858703&tool=pmcentrez&rendertype=abstract. Accessed 26 January 2014.

37. PowersRW3rd, KaeberleinM, CaldwellSD, KennedyBK, FieldsS (2006) Extension of chronological life span in yeast by decreased TOR pathway signaling. Genes Dev 20: 174–184 Available: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=16418483.

38. GueldenerU, HeinischJ, KoehlerGJ, VossD, HegemannJH (2002) A second set of loxP marker cassettes for Cre-mediated multiple gene knockouts in budding yeast. Nucleic Acids Res 30: e23 Available: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=11884642.

39. GuldenerU, HeckS, FielderT, BeinhauerJ, HegemannJH (1996) A new efficient gene disruption cassette for repeated use in budding yeast. Nucleic Acids Res 24: 2519–2524 Available: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=8692690.

40. JankeC, MagieraMM, RathfelderN, TaxisC, ReberS, et al. (2004) A versatile toolbox for PCR-based tagging of yeast genes: new fluorescent proteins, more markers and promoter substitution cassettes. Yeast 21: 947–962 Available: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=15334558.

41. GietzRD, SchiestlRH, WillemsAR, WoodsRA (1995) Studies on the transformation of intact yeast cells by the LiAc/SS-DNA/PEG procedure. Yeast (Chichester, England) 11: 355–360 Available: http://www.ncbi.nlm.nih.gov/pubmed/7785336. Accessed 4 June 2013.

42. RuckenstuhlC, ButtnerS, Carmona-GutierrezD, EisenbergT, KroemerG, et al. (2009) The Warburg effect suppresses oxidative stress induced apoptosis in a yeast model for cancer. PLoS One 4: e4592 Available: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=19240798.

43. Büttner S, Carmona-Gutierrez D, Vitale I, Castedo M, Ruli D, et al.. (2007) Depletion of endonuclease G selectively kills polyploid cells. Cell cycle (Georgetown, Tex) 6: : 1072–1076. Available: http://www.ncbi.nlm.nih.gov/pubmed/17471024. Accessed 29 January 2014.

44. NodaT, KlionskyDJ (2008) The quantitative Pho8Delta60 assay of nonspecific autophagy. Methods in enzymology 451: 33–42 Available: http://www.ncbi.nlm.nih.gov/pubmed/19185711. Accessed 5 June 2013.

45. CampbellCL, ThorsnessPE (1998) Escape of mitochondrial DNA to the nucleus in yme1 yeast is mediated by vacuolar-dependent turnover of abnormal mitochondrial compartments. J Cell Sci 111 ((Pt 1) 2455–2464 Available: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=9683639.

46. MadeoF, HerkerE, MaldenerC, WissingS, LächeltS, et al. (2002) A caspase-related protease regulates apoptosis in yeast. Molecular cell 9: 911–917 Available: http://www.ncbi.nlm.nih.gov/pubmed/11983181. Accessed 13 November 2012.