Pyruvate imbalance mediates metabolic reprogramming and mimics lifespan extension by dietary restriction in Caenorhabditis elegans

Aging Cell

Volumn 10, Issue 1, 2011, Pages 39-54

  Mouchiroud, Laurent ^a   Molin, Laurent ^a   Kasturi, Prasad ^a,d   Triba, Mohamed N ^b,e   Dumas, Marc Emmanuel ^b   Wilson, Marieangela C ^c   Halestrap, Andrew P ^c   Roussel, Damien ^a   Masse, Ingrid ^a,e   Dallière, Nicolas ^a   Ségalat, Laurent ^a,e   Billaud, Marc ^a   Solari, Florence ^a  

^a UNIVERSITÉ DE LYON   (France)

^b CNRS FRE 3008   (France)

^c UNIVERSITY OF BRISTOL   (United Kingdom)

^d MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^e CENTRE DE GÉNÉTIQUE MOLÉCULAIRE ET CELLULAIRE   (France)

Author keywords

Caenorhabditis elegans; Dietary restriction; Hormesis; PTEN daf 18; Pyruvate

Indexed keywords

ADENYLATE KINASE; AMP ACTIVATED KINASE 2; DAF 18 PROTEIN; HEAT SHOCK TRANSCRIPTION FACTOR 1; MONOCARBOXYLATE TRANSPORTER; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PYRUVATE DEHYDROGENASE; PYRUVIC ACID; SIRTUIN 1; SLCF 1 PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FOXA; UNCLASSIFIED DRUG;

AGING; AMINO ACID SEQUENCE; ARTICLE; CAENORHABDITIS ELEGANS; DIET RESTRICTION; EPISTASIS; LIFESPAN; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RNA INTERFERENCE; WILD TYPE;

ANIMALIA; CAENORHABDITIS ELEGANS; MAMMALIA;

EID: 78651276219     PISSN: 14749718     EISSN: 14749726     Source Type: Journal    
DOI: 10.1111/j.1474-9726.2010.00640.x     Document Type: Article

References (49)

1. Apfeld J, O'Connor G, McDonagh T, DiStefano PS, Curtis R (2004) The AMP-activated protein kinase AAK-2 links energy levels and insulin-like signals to lifespan in C. elegans. Genes Dev. 18, 3004-3009.
2. Bishop NA, Guarente L (2007) Two neurons mediate diet-restriction-induced longevity in C. elegans. Nature 447, 545-549.
3. Blaise BJ, Giacomotto J, Elena B, Dumas ME, Toulhoat P, Segalat L, Emsley L (2007) Metabotyping of Caenorhabditis elegans reveals latent phenotypes. Proc. Natl. Acad. Sci. USA 104, 19808-19812.
4. Blaise BJ, Giacomotto J, Triba MN, Toulhoat P, Piotto M, Emsley L, Segalat L, Dumas ME, Elena B (2009) Metabolic profiling strategy of Caenorhabditis elegans by whole-organism nuclear magnetic resonance. J. Proteome. Res. 8, 2542-2550.
5. Bluher M, Kahn BB, Kahn CR (2003) Extended longevity in mice lacking the insulin receptor in adipose tissue. Science 299, 572-574.
6. Castelein N, Hoogewijs D, De Vreese A, Braeckman BP, Vanfleteren JR (2008) Dietary restriction by growth in axenic medium induces discrete changes in the transcriptional output of genes involved in energy metabolism in Caenorhabditis elegans. Biotechnol J. 3, 803-812.
7. Colman RJ, Anderson RM, Johnson SC, Kastman EK, Kosmatka KJ, Beasley TM, Allison DB, Cruzen C, Simmons HA, Kemnitz JW, Weindruch R (2009) Caloric restriction delays disease onset and mortality in rhesus monkeys. Science 325, 201-204.
8. Grandison RC, Piper MD, Partridge L (2009) Amino-acid imbalance explains extension of lifespan by dietary restriction in Drosophila. Nature 462, 1061-1064.
9. Greer EL, Brunet A (2009) Different dietary restriction regimens extend lifespan by both independent and overlapping genetic pathways in C. elegans. Aging Cell 8, 113-127.
10. Greer EL, Dowlatshahi D, Banko MR, Villen J, Hoang K, Blanchard D, Gygi SP, Brunet A (2007) An AMPK-FOXO pathway mediates longevity induced by a novel method of dietary restriction in C. elegans. Curr. Biol. 17, 1646-1656.
11. Halestrap AP, Meredith D (2004) The SLC16 gene family-from monocarboxylate transporters (MCTs) to aromatic amino acid transporters and beyond. Pflugers Arch. 447, 619-628.
12. Harding HP, Zhang Y, Zeng H, Novoa I, Lu PD, Calfon M, Sadri N, Yun C, Popko B, Paules R, Stojdl DF, Bell JC, Hettmann T, Leiden JM, Ron D (2003) An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol. Cell 11, 619-633.
13. Herndon LA, Schmeissner PJ, Dudaronek JM, Brown PA, Listner KM, Sakano Y, Paupard MC, Hall DH, Driscoll M (2002) Stochastic and genetic factors influence tissue-specific decline in ageing C. elegans. Nature 419, 808-814.
14. Holzenberger M, Dupont J, Ducos B, Leneuve P, Geloen A, Even PC, Cervera P, Le Bouc Y (2003) IGF-1 receptor regulates lifespan and resistance to oxidative stress in mice. Nature 421, 182-187.
15. Hsu AL, Murphy CT, Kenyon C (2003) Regulation of aging and age-related disease by DAF-16 and heat-shock factor. Science 300, 1142-1145.
16. Iwanaga T, Takebe K, Kato I, Karaki S, Kuwahara A (2006) Cellular expression of monocarboxylate transporters (MCT) in the digestive tract of the mouse, rat, and humans, with special reference to slc5a8. Biomed Res. 27, 243-254.
17. Kalaany NY, Sabatini DM (2009) Tumours with PI3K activation are resistant to dietary restriction. Nature 458, 725-731.
18. Kamath RS, Martinez-Campos M, Zipperlen P, Fraser AG, Ahringer J (2001) Effectiveness of specific RNA-mediated interference through ingested double-stranded RNA in Caenorhabditis elegans. J. Genome. Biol. 2: (1), research0002.1-research0002.10.
19. Kappeler L, De Magalhaes Filho CM, Dupont J, Leneuve P, Cervera P, Perin L, Loudes C, Blaise A, Klein R, Epelbaum J, Le Bouc Y, Holzenberger M (2008) Brain IGF-1 receptors control mammalian growth and lifespan through a neuroendocrine mechanism. PLoS Biol. 6, e254.
20. Kemp BJ, Church DL, Hatzold J, Conradt B, Lambie EJ (2009) Gem-1 encodes an SLC16 monocarboxylate transporter-related protein that functions in parallel to the gon-2 TRPM channel during gonad development in Caenorhabditis elegans. Genetics 181, 581-591.
21. Kenyon C, Chang J, Gensch E, Rudner A, Tabtiang R (1993) A C. elegans mutant that lives twice as long as wild type. Nature 366, 461-464.
22. Kimura K, Tanaka N, Nakamura N, Takano S, Ohkuma S (2007) Knockdown of mitochondrial heat shock protein 70 promotes progeria-like phenotypes in Caenorhabditis elegans. J. Biol. Chem. 282, 5910-5918.
23. Lakowski B, Hekimi S (1998) The genetics of caloric restriction in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 95, 13091-13096.
24. Lane MA, Ingram DK, Roth GS (1999) Calorie restriction in nonhuman primates: effects on diabetes and cardiovascular disease risk. Toxicol Sci. 52, 41-48.
25. Lee SS, Lee RY, Fraser AG, Kamath RS, Ahringer J, Ruvkun G (2003) A systematic RNAi screen identifies a critical role for mitochondria in C. elegans longevity. Nat. Genet. 33, 40-48.
26. Lee SJ, Murphy CT, Kenyon C (2009) Glucose shortens the life span of C. elegans by downregulating DAF-16/FOXO activity and aquaporin gene expression. Cell Metab. 10, 379-391.
27. Lin SJ, Kaeberlein M, Andalis AA, Sturtz LA, Defossez PA, Culotta VC, Fink GR, Guarente L (2002) Calorie restriction extends Saccharomyces cerevisiae lifespan by increasing respiration. Nature 418, 344-348.
28. Maeda H, Gleiser CA, Masoro EJ, Murata I, McMahan CA, Yu BP (1985) Nutritional influences on aging of Fischer 344 rats: II. Pathology. J. Gerontol. 40, 671-688.
29. Mair W, Panowski SH, Shaw RJ, Dillin A (2009) Optimizing dietary restriction for genetic epistasis analysis and gene discovery in C. elegans. PLoS ONE 4, e4535.
30. Masoro EJ (2005) Overview of caloric restriction and ageing. Mech. Ageing Dev. 126, 913-922.
31. Masse I, Molin L, Mouchiroud L, Vanhems P, Palladino F, Billaud M, Solari F (2008) A novel role for the SMG-1 kinase in lifespan and oxidative stress resistance in Caenorhabditis elegans. PLoS ONE 3, e3354.
32. Mattson MP, Wan R (2005) Beneficial effects of intermittent fasting and caloric restriction on the cardiovascular and cerebrovascular systems. J. Nutr. Biochem. 16, 129-137.
33. Ovens MJ, Davies AJ, Wilson MC, Murray CM, Halestrap AP (2010) AR-C155858 is a potent inhibitor of monocarboxylate transporters MCT1 and MCT2 that binds to an intracellular site involving transmembrane helices 7-10. Biochem. J. 425, 523-530.
34. Panowski SH, Wolff S, Aguilaniu H, Durieux J, Dillin A (2007) PHA-4/Foxa mediates diet-restriction-induced longevity of C. elegans. Nature 447, 550-555.
35. Partridge L, Gems D, Withers DJ (2005) Sex and death: what is the connection? Cell 120, 461-472.
36. Ralser M, Wamelink MM, Struys EA, Joppich C, Krobitsch S, Jakobs C, Lehrach H (2008) A catabolic block does not sufficiently explain how 2-deoxy-d-glucose inhibits cell growth. Proc. Natl. Acad. Sci. USA 105, 17807-17811.
37. Rea SL, Ventura N, Johnson TE (2007) Relationship between mitochondrial electron transport chain dysfunction, development, and life extension in Caenorhabditis elegans. PLoS Biol. 5, e259.
38. Schlotterer A, Kukudov G, Bozorgmehr F, Hutter H, Du X, Oikonomou D, Ibrahim Y, Pfisterer F, Rabbani N, Thornalley P, Sayed A, Fleming T, Humpert P, Schwenger V, Zeier M, Hamann A, Stern D, Brownlee M, Bierhaus A, Nawroth P, Morcos M (2009) C. elegans as model for the study of high glucose- mediated life span reduction. Diabetes 58, 2450-2456.
39. Schulz TJ, Zarse K, Voigt A, Urban N, Birringer M, Ristow M (2007) Glucose restriction extends Caenorhabditis elegans life span by inducing mitochondrial respiration and increasing oxidative stress. Cell Metab. 6, 280-293.
40. Selman C, Kerrison ND, Cooray A, Piper MD, Lingard SJ, Barton RH, Schuster EF, Blanc E, Gems D, Nicholson JK, Thornton JM, Partridge L, Withers DJ (2006) Coordinated multitissue transcriptional and plasma metabonomic profiles following acute caloric restriction in mice. Physiol. Genomics 27, 187-200.
41. Smith ED, Kaeberlein TL, Lydum BT, Sager J, Welton KL, Kennedy BK, Kaeberlein M (2008) Age- and calorie-independent life span extension from dietary restriction by bacterial deprivation in Caenorhabditis elegans. BMC Dev. Biol. 8, 49.
42. Steinkraus KA, Smith ED, Davis C, Carr D, Pendergrass WR, Sutphin GL, Kennedy BK, Kaeberlein M (2008) Dietary restriction suppresses proteotoxicity and enhances longevity by an hsf-1-dependent mechanism in Caenorhabditis elegans. Aging Cell 7, 394-404.
43. Tukiainen T, Tynkkynen T, Makinen VP, Jylanki P, Kangas A, Hokkanen J, Vehtari A, Grohn O, Hallikainen M, Soininen H, Kivipelto M, Groop PH, Kaski K, Laatikainen R, Soininen P, Pirttila T, Ala-Korpela M (2008) A multi-metabolite analysis of serum by 1H NMR spectroscopy: early systemic signs of Alzheimer's disease. Biochem. Biophys. Res. Commun. 375, 356-361.
44. Walford RL, Mock D, Verdery R, MacCallum T (2002) Calorie restriction in biosphere 2: alterations in physiologic, hematologic, hormonal, and biochemical parameters in humans restricted for a 2-year period. J. Gerontol. A Biol. Sci. Med. Sci. 57, B211-B224.
45. Wang Y, Tissenbaum HA (2006) Overlapping and distinct functions for a Caenorhabditis elegans SIR2 and DAF-16/FOXO. Mech. Ageing Dev. 127, 48-56.
46. Wang Z, Masternak MM, Al-Regaiey KA, Bartke A (2007) Adipocytokines and the regulation of lipid metabolism in growth hormone transgenic and calorie-restricted mice. Endocrinology 148, 2845-2853.
47. Wilson MC, Meredith D, Fox JE, Manoharan C, Davies AJ, Halestrap AP (2005) Basigin (CD147) is the target for organomercurial inhibition of monocarboxylate transporter isoforms 1 and 4: the ancillary protein for the insensitive MCT2 is EMBIGIN (gp70). J. Biol. Chem. 280, 27213-27221.
48. Winston WM, Sutherlin M, Wright AJ, Feinberg EH, Hunter CP (2007) Caenorhabditis elegans SID-2 is required for environmental RNA interference. Proc. Natl. Acad. Sci. USA 104, 10565-10570.
49. Wolkow CA, Munoz MJ, Riddle DL, Ruvkun G (2002) Insulin receptor substrate and p55 orthologous adaptor proteins function in the Caenorhabditis elegans daf-2/insulin-like signaling pathway. J. Biol. Chem. 277, 49591-49597.