Advertisement

Amino Acid Homeostasis and Chronological Longevity in Saccharomyces cerevisiae

  • John P. ArisEmail author
  • Laura K. Fishwick
  • Michelle L. Marraffini
  • Arnold Y. Seo
  • Christiaan Leeuwenburgh
  • William A. DunnJr.
Chapter
Part of the Subcellular Biochemistry book series (SCBI, volume 57)

Abstract

Understanding how non-dividing cells remain viable over long periods of time, which may be decades in humans, is of central importance in understanding mechanisms of aging and longevity. The long-term viability of non-dividing cells, known as chronological longevity, relies on cellular processes that degrade old components and replace them with new ones. Key among these processes is amino acid homeostasis. Amino acid homeostasis requires three principal functions: amino acid uptake, de novo synthesis, and recycling. Autophagy plays a key role in recycling amino acids and other metabolic building blocks, while at the same time removing damaged cellular components such as mitochondria and other organelles. Regulation of amino acid homeostasis and autophagy is accomplished by a complex web of pathways that interact because of the functional overlap at the level of recycling. It is becoming increasingly clear that amino acid homeostasis and autophagy play important roles in chronological longevity in yeast and higher organisms. Our goal in this chapter is to focus on mechanisms and pathways that link amino acid homeostasis, autophagy, and chronological longevity in yeast, and explore their relevance to aging and longevity in higher eukaryotes.

Keywords

Amino acid Homeostasis Chronological longevity Caloric restriction Autophagy 

Abbreviations

BCAA

branched side-chain amino acids

CLS

chronological life span

CR

calorie restriction

GAAC

general amino acid control

ISC

iron sulfur cluster

NCR

nitrogen catabolite repression

ROS

reactive oxygen species

TOR

target of rapamycin

Notes

Acknowledgements

We are grateful for the support that we have received from the NIH (AG023719 to JPA; AG17994 to CL; CA95552 to WAD), including the Claude D. Pepper Older Americans Independence Center (AG028740), and the University of Florida Institute on Aging. We acknowledge the Honors Program at the University of Florida, which has facilitated the participation of undergraduate students in our research efforts.

References

  1. Allen C, Buttner S, Aragon AD, Thomas JA, Meirelles O, Jaetao JE, Benn D, Ruby SW, Veenhuis M, Madeo F, Werner-Washburne M (2006) Isolation of quiescent and nonquiescent cells from yeast stationary-phase cultures. J Cell Biol 174:89–100PubMedGoogle Scholar
  2. Alvers AL, Fishwick LK, Wood MS, Hu D, Chung HS, Dunn WA, Jr, Aris JP (2009) Autophagy and amino acid homeostasis are required for chronological longevity in Saccharomyces cerevisiae. Aging Cell 8:353–369PubMedGoogle Scholar
  3. Amberg DC, Burke DJ, Strathern JN (2005) Methods in yeast genetics: a Cold Spring Harbor Laboratory course manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NYGoogle Scholar
  4. Andrews ZB (2010) Uncoupling protein-2 and the potential link between metabolism and longevity. Curr Aging Sci 3:102–112PubMedGoogle Scholar
  5. Aragon AD, Rodriguez AL, Meirelles O, Roy S, Davidson GS, Tapia PH, Allen C, Joe R, Benn D, Werner-Washburne M (2008) Characterization of differentiated quiescent and nonquiescent cells in yeast stationary-phase cultures. Mol Biol Cell 19:1271–1280PubMedGoogle Scholar
  6. Attardi G (2002) Role of mitochondrial DNA in human aging. Mitochondrion 2:27–37PubMedGoogle Scholar
  7. Ayala V, Naudi A, Sanz A, Caro P, Portero-Otin M, Barja G, Pamplona R (2007) Dietary protein restriction decreases oxidative protein damage, peroxidizability index, and mitochondrial complex I content in rat liver. J Gerontol A Biol Sci Med Sci 62:352–360PubMedGoogle Scholar
  8. Barros MH, Bandy B, Tahara EB, Kowaltowski AJ (2004) Higher respiratory activity decreases mitochondrial reactive oxygen release and increases life span in Saccharomyces cerevisiae. J Biol Chem 279:49883–49888PubMedGoogle Scholar
  9. Beckman KB, Ames BN (1998) The free radical theory of aging matures. Physiol Rev 78:547–581PubMedGoogle Scholar
  10. Bishop NA, Guarente L (2007) Genetic links between diet and lifespan: shared mechanisms from yeast to humans. Nat Rev Genet 8:835–844PubMedGoogle Scholar
  11. Boer VM, Amini S, Botstein D (2008) Influence of genotype and nutrition on survival and metabolism of starving yeast. Proc Natl Acad Sci USA 105:6930–6935PubMedGoogle Scholar
  12. Boer VM, Daran JM, Almering MJ, de Winde JH, Pronk JT (2005) Contribution of the Saccharomyces cerevisiae transcriptional regulator Leu3p to physiology and gene expression in nitrogen- and carbon-limited chemostat cultures. FEMS Yeast Res 5:885–897PubMedGoogle Scholar
  13. Bonawitz ND, Chatenay-Lapointe M, Pan Y, Shadel GS (2007) Reduced TOR signaling extends chronological life span via increased respiration and upregulation of mitochondrial gene expression. Cell Metab 5:265–277PubMedGoogle Scholar
  14. Bonawitz ND, Rodeheffer MS, Shadel GS (2006) Defective mitochondrial gene expression results in reactive oxygen species-mediated inhibition of respiration and reduction of yeast life span. Mol Cell Biol 26:4818–4829PubMedGoogle Scholar
  15. Borghouts C, Benguria A, Wawryn J, Jazwinski SM (2004) Rtg2 protein links metabolism and genome stability in yeast longevity. Genetics 166:765–777PubMedGoogle Scholar
  16. Brauer MJ, Huttenhower C, Airoldi EM, Rosenstein R, Matese JC, Gresham D, Boer VM, Troyanskaya OG, Botstein D (2008) Coordination of growth rate, cell cycle, stress response, and metabolic activity in yeast. Mol Biol Cell 19:352–367PubMedGoogle Scholar
  17. Brauer MJ, Saldanha AJ, Dolinski K, Botstein D (2005) Homeostatic adjustment and metabolic remodeling in glucose-limited yeast cultures. Mol Biol Cell 16:2503–2517PubMedGoogle Scholar
  18. Burtner CR, Murakami CJ, Kennedy BK, Kaeberlein M (2009) A molecular mechanism of chronological aging in yeast. Cell Cycle 8:1256–1270PubMedGoogle Scholar
  19. Buschlen S, Amillet JM, Guiard B, Fournier A, Marcireau C, Bolotin-Fukuhara M (2003) The S. cerevisiae HAP complex, a key regulator of mitochondrial function, coordinates nuclear and mitochondrial gene expression. Comp Funct Genomics 4:37–46PubMedGoogle Scholar
  20. Carlson M (1999) Glucose repression in yeast. Curr Opin Microbiol 2:202–207PubMedGoogle Scholar
  21. Chen Q, Ding Q, Keller JN (2005) The stationary phase model of aging in yeast for the study of oxidative stress and age-related neurodegeneration. Biogerontology 6:1–13PubMedGoogle Scholar
  22. Chen Q, Thorpe J, Ding Q, El-Amouri IS, Keller JN (2004) Proteasome synthesis and assembly are required for survival during stationary phase. Free Radic Biol Med 37:859–868PubMedGoogle Scholar
  23. Cheng C, Fabrizio P, Ge H, Wei M, Longo VD, Li LM (2007) Significant and systematic expression differentiation in long-lived yeast strains. PLoS One 2:e1095PubMedGoogle Scholar
  24. Cuervo AM (2008a) Autophagy and aging: keeping that old broom working. Trends Genet 24:604–612PubMedGoogle Scholar
  25. Cuervo AM (2008b) Calorie restriction and aging: the ultimate “cleansing diet”. J Gerontol A Biol Sci Med Sci 63:547–549PubMedGoogle Scholar
  26. Cuervo AM, Dice JF (2000) Age-related decline in chaperone-mediated autophagy. J Biol Chem 275:31505–31513PubMedGoogle Scholar
  27. Cyrne L, Martins L, Fernandes L, Marinho HS (2003) Regulation of antioxidant enzymes gene expression in the yeast Saccharomyces cerevisiae during stationary phase. Free Radic Biol Med 34:385–393PubMedGoogle Scholar
  28. Davidson GS, Joe RM, Roy S, Meirelles O, Allen CP, Wilson MR, Tapia PH, Manzanilla EE, Dodson AE, Chakraborty S, Carter M, Young S, Edwards B, Sklar L, Werner-Washburne M (2011) The proteomics of quiescent and nonquiescent cell differentiation in yeast stationary-phase cultures. Mol Biol Cell 22:988–998PubMedGoogle Scholar
  29. De Virgilio C, Loewith R (2006a) Cell growth control: little eukaryotes make big contributions. Oncogene 25:6392–6415PubMedGoogle Scholar
  30. De Virgilio C, Loewith R (2006b) The TOR signalling network from yeast to man. Int J Biochem Cell Biol 38:1476–1481PubMedGoogle Scholar
  31. Del Roso A, Vittorini S, Cavallini G, Donati A, Gori Z, Masini M, Pollera M, Bergamini E (2003) Ageing-related changes in the in vivo function of rat liver macroautophagy and proteolysis. Exp Gerontol 38:519–527PubMedGoogle Scholar
  32. Dietrich MO, Horvath TL (2010) The role of mitochondrial uncoupling proteins in lifespan. Pflugers Arch 459:269–275PubMedGoogle Scholar
  33. Dillon EL, Sheffield-Moore M, Paddon-Jones D, Gilkison C, Sanford AP, Casperson SL, Jiang J, Chinkes DL, Urban RJ (2009) Amino acid supplementation increases lean body mass, basal muscle protein synthesis, and insulin-like growth factor-I expression in older women. J Clin Endocrinol Metab 94:1630–1637PubMedGoogle Scholar
  34. Doudican NA, Song B, Shadel GS, Doetsch PW (2005) Oxidative DNA damage causes mitochondrial genomic instability in Saccharomyces cerevisiae. Mol Cell Biol 25:5196–5204PubMedGoogle Scholar
  35. Drummond MJ, Rasmussen BB (2008) Leucine-enriched nutrients and the regulation of mammalian target of rapamycin signalling and human skeletal muscle protein synthesis. Curr Opin Clin Nutr Metab Care 11:222–226PubMedGoogle Scholar
  36. Dumlao DS, Hertz N, Clarke S (2008) Secreted 3-isopropylmalate methyl ester signals invasive growth during amino acid starvation in Saccharomyces cerevisiae. Biochemistry 47:698–709PubMedGoogle Scholar
  37. Fabrizio P, Battistella L, Vardavas R, Gattazzo C, Liou LL, Diaspro A, Dossen JW, Gralla EB, Longo VD (2004) Superoxide is a mediator of an altruistic aging program in Saccharomyces cerevisiae. J Cell Biol 166:1055–1067PubMedGoogle Scholar
  38. Fabrizio P, Hoon S, Shamalnasab M, Galbani A, Wei M, Giaever G, Nislow C, Longo VD (2010) Genome-wide screen in Saccharomyces cerevisiae identifies vacuolar protein sorting, autophagy, biosynthetic, and tRNA methylation genes involved in life span regulation. PLoS Genet 6:e1001024PubMedGoogle Scholar
  39. Fabrizio P, Liou LL, Moy VN, Diaspro A, SelverstoneValentine J, Gralla EB, Longo VD (2003) SOD2 functions downstream of Sch9 to extend longevity in yeast. Genetics 163:35–46PubMedGoogle Scholar
  40. Fabrizio P, Longo VD (2003) The chronological life span of Saccharomyces cerevisiae. Aging Cell 2:73–81PubMedGoogle Scholar
  41. Fontana L, Partridge L, Longo VD (2010) Extending healthy life span – from yeast to humans. Science 328:321–326PubMedGoogle Scholar
  42. Garrido EO, Grant CM (2002) Role of thioredoxins in the response of Saccharomyces cerevisiae to oxidative stress induced by hydroperoxides. Mol Microbiol 43:993–1003PubMedGoogle Scholar
  43. Gimeno CJ, Ljungdahl PO, Styles CA, Fink GR (1992) Unipolar cell divisions in the yeast S. cerevisiae lead to filamentous growth: regulation by starvation and RAS. Cell 68:1077–1090PubMedGoogle Scholar
  44. Gomes P, Sampaio-Marques B, Ludovico P, Rodrigues F, Leao C (2007) Low auxotrophy-complementing amino acid concentrations reduce yeast chronological life span. Mech Ageing Dev 128:383–391PubMedGoogle Scholar
  45. Grandison RC, Piper MD, Partridge L (2009) Amino-acid imbalance explains extension of lifespan by dietary restriction in Drosophila. Nature 462:1061–1064PubMedGoogle Scholar
  46. Gray JV, Petsko GA, Johnston GC, Ringe D, Singer RA, Werner-Washburne M (2004) “Sleeping beauty”: quiescence in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 68:187–206PubMedGoogle Scholar
  47. Guarente L (2008) Mitochondria – a nexus for aging, calorie restriction, and sirtuins? Cell 132:171–176PubMedGoogle Scholar
  48. Hansen M, Taubert S, Crawford D, Libina N, Lee SJ, Kenyon C (2007) Lifespan extension by conditions that inhibit translation in Caenorhabditis elegans. Aging Cell 6:95–110PubMedGoogle Scholar
  49. Harbison CT, Gordon DB, Lee TI, Rinaldi NJ, Macisaac KD, Danford TW, Hannett NM, Tagne JB, Reynolds DB, Yoo J, Jennings EG, Zeitlinger J, Pokholok DK, Kellis M, Rolfe PA, Takusagawa KT, Lander ES, Gifford DK, Fraenkel E, Young RA (2004) Transcriptional regulatory code of a eukaryotic genome. Nature 431:99–104PubMedGoogle Scholar
  50. Harman D (1956) Aging: a theory based on free radical and radiation chemistry. J Gerontol 11:298–300PubMedGoogle Scholar
  51. Harman D (1972) The biologic clock: the mitochondria? J Am Geriatr Soc 20:145–147PubMedGoogle Scholar
  52. Harman D (2003) The free radical theory of aging. Antioxid Redox Signal 5:557–561PubMedGoogle Scholar
  53. Harris N, Bachler M, Costa V, Mollapour M, Moradas-Ferreira P, Piper PW (2005) Overexpressed Sod1p acts either to reduce or to increase the lifespans and stress resistance of yeast, depending on whether it is Cu(2+)-deficient or an active Cu,Zn-superoxide dismutase. Aging Cell 4:41–52PubMedGoogle Scholar
  54. Harris N, Costa V, MacLean M, Mollapour M, Moradas-Ferreira P, Piper PW (2003) Mnsod overexpression extends the yeast chronological (G0) life span but acts independently of Sir2p histone deacetylase to shorten the replicative life span of dividing cells. Free Radic Biol Med 34:1599–1606PubMedGoogle Scholar
  55. Hartwell LH (1974) Saccharomyces cerevisiae cell cycle. Bacteriol Rev 38:164–198PubMedGoogle Scholar
  56. Hazelwood LA, Daran JM, van Maris AJ, Pronk JT, Dickinson JR (2008) The Ehrlich pathway for fusel alcohol production: a century of research on Saccharomyces cerevisiae metabolism. Appl Environ Microbiol 74:2259–2266PubMedGoogle Scholar
  57. Henderson ST, Bonafe M, Johnson TE (2006) daf-16 protects the nematode Caenorhabditis elegans during food deprivation. J Gerontol A Biol Sci Med Sci 61:444–460PubMedGoogle Scholar
  58. Herker E, Jungwirth H, Lehmann KA, Maldener C, Frohlich KU, Wissing S, Buttner S, Fehr M, Sigrist S, Madeo F (2004) Chronological aging leads to apoptosis in yeast. J Cell Biol 164:501–507PubMedGoogle Scholar
  59. Herman PK (2002). Stationary phase in yeast. Curr Opin Microbiol 5:602–607PubMedGoogle Scholar
  60. Hinnebusch AG (2005) Translational regulation of GCN4 and the general amino acid control of yeast. Annu Rev Microbiol 59:407–450PubMedGoogle Scholar
  61. Hofman-Bang J (1999) Nitrogen catabolite repression in Saccharomyces cerevisiae. Mol Biotechnol 12:35–73PubMedGoogle Scholar
  62. Hu Y, Cooper TG, Kohlhaw GB (1995) The Saccharomyces cerevisiae Leu3 protein activates expression of GDH1, a key gene in nitrogen assimilation. Mol Cell Biol 15:52–57PubMedGoogle Scholar
  63. Hubbard VM, Valdor R, Macian F, Cuervo AM (2011) Selective autophagy in the maintenance of cellular homeostasis in aging organisms. Biogerontology. doi:10.1007/s10522-011-9331-xGoogle Scholar
  64. Jazwinski SM (2005) Rtg2 protein: at the nexus of yeast longevity and aging. FEMS Yeast Res 5:1253–1259PubMedGoogle Scholar
  65. Jones EW, Fink GR (1982) Regulation of amino acid and nucleotide biosynthesis in yeast. In: Strathern JN, Jones EW, Broach JR (eds) The molecular biology of the yeast saccharomyces metabolism and gene expression, pp 181–299. Cold Spring Harbor Laboratories, Cold Spring Harbor, NYGoogle Scholar
  66. Kaeberlein M (2010) Lessons on longevity from budding yeast. Nature 464:513–519PubMedGoogle Scholar
  67. Kanki T, Wang K, Cao Y, Baba M, Klionsky DJ (2009) Atg32 is a mitochondrial protein that confers selectivity during mitophagy. Dev Cell 17:98–109PubMedGoogle Scholar
  68. Kapahi P, Zid BM, Harper T, Koslover D, Sapin V, Benzer S (2004) Regulation of lifespan in Drosophila by modulation of genes in the TOR signaling pathway. Curr Biol 14:885–890PubMedGoogle Scholar
  69. Kenyon C (2005) The plasticity of aging: insights from long-lived mutants. Cell 120:449–460PubMedGoogle Scholar
  70. Klionsky DJ, Cuervo AM, Seglen PO (2007) Methods for monitoring autophagy from yeast to human. Autophagy 3:181–206PubMedGoogle Scholar
  71. Kohlhaw GB (2003) Leucine biosynthesis in fungi: entering metabolism through the back door. Microbiol Mol Biol Rev 67:1–15PubMedGoogle Scholar
  72. Kolkman A, Daran-Lapujade P, Fullaondo A, Olsthoorn MM, Pronk JT, Slijper M, Heck AJ (2006) Proteome analysis of yeast response to various nutrient limitations. Mol Syst Biol 2:2006 0026PubMedGoogle Scholar
  73. Kundu M, Thompson CB (2005) Macroautophagy versus mitochondrial autophagy: a question of fate? Cell Death Differ 12(Suppl 2):1484–1489PubMedGoogle Scholar
  74. Lapointe J, Hekimi S (2010) When a theory of aging ages badly. Cell Mol Life Sci 67:1–8PubMedGoogle Scholar
  75. Laun P, Heeren G, Rinnerthaler M, Rid R, Kossler S, Koller L, Breitenbach M (2008) Senescence and apoptosis in yeast mother cell-specific aging and in higher cells: a short review. Biochim Biophys Acta 1783:1328–1334PubMedGoogle Scholar
  76. Layman DK (2003) The role of leucine in weight loss diets and glucose homeostasis. J Nutr 133:261S–267SPubMedGoogle Scholar
  77. Lemasters JJ (2005) Selective mitochondrial autophagy, or mitophagy, as a targeted defense against oxidative stress, mitochondrial dysfunction, and aging. Rejuvenation Res 8:3–5PubMedGoogle Scholar
  78. Libert S, Zwiener J, Chu X, Vanvoorhies W, Roman G, Pletcher SD (2007) Regulation of Drosophila life span by olfaction and food-derived odors. Science 315:1133–1137PubMedGoogle Scholar
  79. Liu H, Styles CA, Fink GR (1996) Saccharomyces cerevisiae S288C has a mutation in FLO8, a gene required for filamentous growth. Genetics 144:967–978PubMedGoogle Scholar
  80. Liu Z, Butow RA (2006) Mitochondrial retrograde signaling. Annu Rev Genet 40:159–185PubMedGoogle Scholar
  81. Longo VD (2004) Ras: the other pro-aging pathway. Sci Aging Knowledge Environ 2004:pe36.Google Scholar
  82. Longo VD, Gralla EB, Valentine JS (1996) Superoxide dismutase activity is essential for stationary phase survival in Saccharomyces cerevisiae. Mitochondrial production of toxic oxygen species in vivo. J Biol Chem 271:12275–12280PubMedGoogle Scholar
  83. Longo VD, Liou LL, Valentine JS, Gralla EB (1999) Mitochondrial superoxide decreases yeast survival in stationary phase. Arch Biochem Biophys 365:131–142PubMedGoogle Scholar
  84. Longo VD, Mitteldorf J, Skulachev VP (2005) Opinion: programmed and altruistic ageing. Nat Rev Genet 6:866–872PubMedGoogle Scholar
  85. Madeo F, Tavernarakis N, Kroemer G (2010) Can autophagy promote longevity? Nat Cell Biol 12:842–846PubMedGoogle Scholar
  86. Mair W, Piper MD, Partridge L (2005) Calories do not explain extension of life span by dietary restriction in Drosophila. PLoS Biol 3:e223PubMedGoogle Scholar
  87. Mascarenhas C, Edwards-Ingram LC, Zeef L, Shenton D, Ashe MP, Grant CM (2008) Gcn4 is required for the response to peroxide stress in the yeast Saccharomyces cerevisiae. Mol Biol Cell 19:2995–3007PubMedGoogle Scholar
  88. Matecic M, Smith DL, Pan X, Maqani N, Bekiranov S, Boeke JD, Smith JS (2010) A microarray-based genetic screen for yeast chronological aging factors. PLoS Genet 6:e1000921PubMedGoogle Scholar
  89. McLarney MJ, Pellett PL, Young VR (1996) Pattern of amino acid requirements in humans: an interspecies comparison using published amino acid requirement recommendations. J Nutr 126:1871–1882PubMedGoogle Scholar
  90. Melendez A, Talloczy Z, Seaman M, Eskelinen EL, Hall DH, Levine B (2003) Autophagy genes are essential for dauer development and life-span extension in C. elegans. Science 301:1387–1391PubMedGoogle Scholar
  91. Merry BJ (2004) Oxidative stress and mitochondrial function with aging – the effects of calorie restriction. Aging Cell 3:7–12PubMedGoogle Scholar
  92. Miller RA, Buehner G, Chang Y, Harper JM, Sigler R, Smith-Wheelock M (2005) Methionine-deficient diet extends mouse lifespan, slows immune and lens aging, alters glucose, T4, IGF-I and insulin levels, and increases hepatocyte MIF levels and stress resistance. Aging Cell 4:119–125PubMedGoogle Scholar
  93. Millward DJ, Layman DK, Tome D, Schaafsma G (2008) Protein quality assessment: impact of expanding understanding of protein and amino acid needs for optimal health. Am J Clin Nutr 87:1576S–1581SPubMedGoogle Scholar
  94. Miquel J, Economos AC, Fleming J, Johnson JE Jr (1980) Mitochondrial role in cell aging. Exp Gerontol 15:575–591PubMedGoogle Scholar
  95. Mortimer RK, Johnson JR (1959) Life spans of individual yeast cells. Nature 183:1751–1752PubMedGoogle Scholar
  96. Müller I, Zimmermann M, Becker D, Flomer M (1980) Calendar life span versus budding life span of Saccharomyces cerevisiae. Mech Ageing Dev 12:47–52PubMedGoogle Scholar
  97. Murin R, Hamprecht B (2008) Metabolic and regulatory roles of leucine in neural cells. Neurochem Res 33:279–284PubMedGoogle Scholar
  98. Nair U, Klionsky DJ (2005) Molecular mechanisms and regulation of specific and nonspecific autophagy pathways in yeast. J Biol Chem 280:41785–41788PubMedGoogle Scholar
  99. Naudi A, Caro P, Jove M, Gomez J, Boada J, Ayala V, Portero-Otin M, Barja G, Pamplona R (2007) Methionine restriction decreases endogenous oxidative molecular damage and increases mitochondrial biogenesis and uncoupling protein 4 in rat brain. Rejuvenation Res 10:473–484PubMedGoogle Scholar
  100. Neiman AM (2005) Ascospore formation in the yeast Saccharomyces cerevisiae. Microbiol Mol Biol Rev 69:565–584PubMedGoogle Scholar
  101. Okamoto K, Kondo-Okamoto N, Ohsumi Y (2009) Mitochondria-anchored receptor Atg32 mediates degradation of mitochondria via selective autophagy. Dev Cell 17:87–97PubMedGoogle Scholar
  102. Oliveira GA, Tahara EB, GombertAK, BarrosMH, Kowaltowski AJ (2008) Increased aerobic metabolism is essential for the beneficial effects of caloric restriction on yeast life span. J Bioenerg Biomembr 40:381–388PubMedGoogle Scholar
  103. Onodera J, Ohsumi Y (2005) Autophagy is required for maintenance of amino acid levels and protein synthesis under nitrogen starvation. J Biol Chem 280:31582–31586PubMedGoogle Scholar
  104. Orentreich N, Matias JR, DeFelice A, Zimmerman JA (1993) Low methionine ingestion by rats extends life span. J Nutr 123:269–274PubMedGoogle Scholar
  105. Pan KZ, Palter JE, Rogers AN, Olsen A, Chen D, Lithgow GJ, Kapahi P (2007) Inhibition of mRNA translation extends lifespan in Caenorhabditis elegans. Aging Cell 6:111–119PubMedGoogle Scholar
  106. Parrella E, Longo VD (2010) Insulin/IGF-I and related signaling pathways regulate aging in nondividing cells: from yeast to the mammalian brain. Scient World J 10:161–177Google Scholar
  107. Pencharz PB, Ball RO (2003) Different approaches to define individual amino acid requirements. Annu Rev Nutr 23:101–116PubMedGoogle Scholar
  108. Piper MD, Bartke A (2008) Diet and aging. Cell Metab 8:99–104PubMedGoogle Scholar
  109. Piper MD, Mair W, Partridge L (2005) Counting the calories: the role of specific nutrients in extension of life span by food restriction. J Gerontol A Biol Sci Med Sci 60:549–555PubMedGoogle Scholar
  110. Piper PW (2006) Long-lived yeast as a model for ageing research. Yeast 23:215–226PubMedGoogle Scholar
  111. Piper PW, Harris NL, MacLean M (2006) Preadaptation to efficient respiratory maintenance is essential both for maximal longevity and the retention of replicative potential in chronologically ageing yeast. Mech Ageing Dev 127:733–740PubMedGoogle Scholar
  112. Powers RW, III, Kaeberlein M, Caldwell SD, Kennedy BK, Fields S (2006) Extension of chronological life span in yeast by decreased TOR pathway signaling. Genes Dev 20:174–184PubMedGoogle Scholar
  113. Ristow M, Zarse K (2010) How increased oxidative stress promotes longevity and metabolic health: the concept of mitochondrial hormesis (mitohormesis). Exp Gerontol 45:410–418PubMedGoogle Scholar
  114. Saldanha AJ, Brauer MJ, Botstein D (2004) Nutritional homeostasis in batch and steady-state culture of yeast. Mol Biol Cell 15:4089–4104PubMedGoogle Scholar
  115. Sherman F (2002) Getting started with yeast. Methods Enzymol 350:3–41PubMedGoogle Scholar
  116. Sinclair DA (2005) Toward a unified theory of caloric restriction and longevity regulation. Mech Ageing Dev 126:987–1002PubMedGoogle Scholar
  117. Smith ED, Kennedy BK, Kaeberlein M (2007) Genome-wide identification of conserved longevity genes in yeast and worms. Mech Ageing Dev 128:106–111PubMedGoogle Scholar
  118. Soeters PB, van de Poll MC, van Gemert WG, Dejong CH (2004) Amino acid adequacy in pathophysiological states. J Nutr 134:1575S–1582SPubMedGoogle Scholar
  119. Srinivasan V, Kriete A, Sacan A, Jazwinski SM (2010) Comparing the yeast retrograde response and NF-kappaB stress responses: implications for aging. Aging Cell 9:933–941PubMedGoogle Scholar
  120. Stanfel MN, Shamieh LS, Kaeberlein M, Kennedy BK (2009) The TOR pathway comes of age. Biochim Biophys Acta 1790:1067–1074PubMedGoogle Scholar
  121. Steffen KK, MacKay VL, Kerr EO, Tsuchiya M, Hu D, Fox LA, Dang N, Johnston ED, Oakes JA, Tchao BN, Pak DN, Fields S, Kennedy BK, Kaeberlein M (2008) Yeast life span extension by depletion of 60S ribosomal subunits is mediated by Gcn4. Cell 133:292–302PubMedGoogle Scholar
  122. Styles C (2002) How to set up a yeast laboratory. Methods Enzymol 350:42–71PubMedGoogle Scholar
  123. Tang L, Liu X, Clarke ND (2006) Inferring direct regulatory targets from expression and genome location analyses: a comparison of transcription factor deletion and overexpression. BMC Genomics 7:215PubMedGoogle Scholar
  124. Tate JJ, Georis I, Feller A, Dubois E, Cooper TG (2009) Rapamycin-induced Gln3 dephosphorylation is insufficient for nuclear localization: Sit4 and PP2A phosphatases are regulated and function differently. J Biol Chem 284:2522–2534PubMedGoogle Scholar
  125. Terman A, Gustafsson B, Brunk UT (2006) The lysosomal-mitochondrial axis theory of postmitotic aging and cell death. Chem-Biol Interact 163:29–37PubMedGoogle Scholar
  126. Thomson JM, Gaucher EA, Burgan MF, De Kee DW, Li T, Aris JP, Benner SA (2005) Resurrecting ancestral alcohol dehydrogenases from yeast. Nat Genet 37:630–635PubMedGoogle Scholar
  127. Vellai T, Takacs-Vellai K, Sass M, Klionsky DJ (2009) The regulation of aging: does autophagy underlie longevity? Trends Cell Biol 19:487–494PubMedGoogle Scholar
  128. Verstrepen KJ, Iserentant D, Malcorps P, Derdelinckx G, Van Dijck P, Winderickx J, Pretorius IS, Thevelein JM, Delvaux FR (2004) Glucose and sucrose: hazardous fast-food for industrial yeast? Trends Biotechnol 22:531–537PubMedGoogle Scholar
  129. Verstrepen KJ, Klis FM (2006) Flocculation, adhesion and biofilm formation in yeasts. Mol Microbiol 60:5–15PubMedGoogle Scholar
  130. Vijg J, Campisi J (2008) Puzzles, promises and a cure for ageing. Nature 454:1065–1071PubMedGoogle Scholar
  131. Wallace DC (2005) A mitochondrial paradigm of metabolic and degenerative diseases, aging, and cancer: a dawn for evolutionary medicine. Annu Rev Genet 39:359–407PubMedGoogle Scholar
  132. Wallace MA, Liou LL, Martins J, Clement MH, Bailey S, Longo VD, Valentine JS, Gralla EB (2004) Superoxide inhibits 4Fe-4S cluster enzymes involved in amino acid biosynthesis. Cross-compartment protection by CuZn-superoxide dismutase. J Biol Chem 279:32055–32062PubMedGoogle Scholar
  133. Ward WF (2002) Protein degradation in the aging organism. Prog Mol Subcell Biol 29:35–42PubMedGoogle Scholar
  134. Wohlgemuth SE, Seo AY, Marzetti E, Lees HA, Leeuwenburgh C (2010) Skeletal muscle autophagy and apoptosis during aging: effects of calorie restriction and life-long exercise. Exp Gerontol 45:138–148PubMedGoogle Scholar
  135. Yang Z, Klionsky DJ (2009) An overview of the molecular mechanism of autophagy. Curr Top Microbiol Immunol 335:1–32PubMedGoogle Scholar
  136. Yen WL, Klionsky DJ (2008) How to live long and prosper: autophagy, mitochondria, and aging. Physiology (Bethesda) 23:248–262Google Scholar
  137. Young VR, Borgonha S (2000) Nitrogen and amino acid requirements: the Massachusetts Institute of Technology amino acid requirement pattern. J Nutr 130:1841S–1849SPubMedGoogle Scholar
  138. Zaman S, Lippman SI, Zhao X, Broach JR (2008) How Saccharomyces responds to nutrients. Annu Rev Genet 42:27–81PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • John P. Aris
    • 1
    Email author
  • Laura K. Fishwick
    • 1
  • Michelle L. Marraffini
    • 1
  • Arnold Y. Seo
    • 1
  • Christiaan Leeuwenburgh
    • 2
  • William A. DunnJr.
    • 1
  1. 1.Department of Anatomy and Cell BiologyUniversity of FloridaGainesvilleUSA
  2. 2.Department of Aging and Geriatric ResearchUniversity of FloridaGainesvilleUSA

Personalised recommendations