The malate-aspartate NADH shuttle components are novel metabolic longevity regulators required for calorie restriction-mediated life span extension in yeast

Genes and Development

Volumn 22, Issue 7, 2008, Pages 931-944

  Easlon, Erin ^a   Tsang, Felicia ^a   Skinner, Craig ^a   Wang, Chen ^a   Lin, Su Ju ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Aging; Calorie restriction (CR); Metabolism; NADH shuttles; Respiration; Sir2

Indexed keywords

ASPARTATE AMINOTRANSFERASE; ASPARTIC ACID; GLYCEROL 3 PHOSPHATE DEHYDROGENASE; GLYCEROPHOSPHATE; MALATE DEHYDROGENASE; MALIC ACID; NICOTINAMIDE ADENINE DINUCLEOTIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; REGULATOR PROTEIN; SILENT INFORMATION REGULATOR PROTEIN 2;

AGING; ARTICLE; CALORIC RESTRICTION; CELL METABOLISM; FUNGAL METABOLISM; GENE MUTATION; LIFESPAN; METABOLIC DISORDER; MICROBIAL METABOLISM; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL RESPIRATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FAMILY; REGULATORY MECHANISM; YEAST;

ASPARTATE AMINOTRANSFERASES; ASPARTIC ACID; BIOLOGICAL TRANSPORT; BLOTTING, WESTERN; CELL NUCLEUS; CYTOPLASM; ELECTRON TRANSPORT; ENERGY METABOLISM; FUNGAL PROTEINS; GLYCEROLPHOSPHATE DEHYDROGENASE; MALATE DEHYDROGENASE; MALATES; MITOCHONDRIA; MUTATION; NAD; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; TIME FACTORS; YEASTS;

EID: 41649119244     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.1648308     Document Type: Article

References (79)

1. Aguilaniu, H., Gustafsson, L., Rigoulet, M., and Nystrom, T. 2003. Asymmetric inheritance of oxidatively damaged proteins during cytokinesis. Science 299: 1751-1753.
2. Albertyn, J., Hohmann, S., Thevelein, J.M., and Prior, B.A. 1994. GPD1, which encodes glycerol-3-phosphate dehydrogenase, is essential for growth under osmotic stress in Saccharomyces cerevisiae, and its expression is regulated by the high-osmolarity glycerol response pathway. Mol. Cell. Biol. 14: 4135-4144.
3. Anderson, R.M., Bitterman, K.J., Wood, J.G., Medvedik, O., and Sinclair, D.A. 2003. Nicotinamide and PNC1 govern lifespan extension by calorie restriction in Saccharomyces cerevisiae. Nature 423: 181-185.
4. Bakker, B.M., Bro, C., Kotter, P., Luttik, M.A., van Dijken, J.P., and Pronk, J.T. 2000. The mitochondrial alcohol dehydrogenase Adh3p is involved in a redox shuttle in Saccharomyces cerevisiae. J. Bacteriol. 182: 4730-4737.
5. Bakker, B.M., Overkamp, K.M., van Maris, A.J., Kotter, P., Luttik, M.A., van Dijken, J.P., and Pronk, J.T. 2001. Stoichiometry and compartmentation of NADH metabolism in Saccharomyces cerevisiae. FEMS Microbiol. Rev. 25: 15-37.
6. Bishop, N.A. and Guarente, L. 2007. Two neurons mediate diet-restriction-induced longevity in C. elegans. Nature 447: 545-549.
7. Bitterman, K.J., Anderson, R.M., Cohen, H.Y., Latorre-Esteves, M., and Sinclair, D.A. 2002. Inhibition of silencing and accelerated aging by nicotinamide, a putative negative regulator of yeast Sir2 and human SIRT1. J. Biol. Chem. 277: 45099-45107.
8. Brachmann, C.B., Davies, A., Cost, G.J., Caputo, E., Li, J., Hieter, P., and Boeke, J.D. 1998. Designer deletion strains derived from Saccharomyces cerevisiae S288C: A useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast 14: 115-132.
9. Bremer, J. and Davis, E.J. 1975. Studies on the active transfer of reducing equivalents into mitochondria via the malate-aspartate shuttle. Biochim. Biophys. Acta 376: 387-397.
10. Cavero, S., Vozza, A., del Arco, A., Palmieri, L., Villa, A., Blanco, E., Runswick, M.J., Walker, J.E., Cerdan, S., Palmieri, F., et al. 2003. Identification and metabolic role of the mitochondrial aspartate-glutamate transporter in Saccharomyces cerevisiae. Mol. Microbiol. 50: 1257-1269.
11. Chen, D., Steele, A.D., Lindquist, S., and Guarente, L. 2005. Increase in activity during calorie restriction requires Sirt1. Science 310: 1641.
12. Crespo, J.L., Powers, T., Fowler, B., and Hall, M.N. 2002. The TOR-controlled transcription activators GLN3, RTG1, and RTG3 are regulated in response to intracellular levels of glutamine. Proc. Natl. Acad. Sci. 99: 6784-6789.
13. Cronin, V.B., Maras, B., Barra, D., and Doonan, S. 1991. The amino acid sequence of the aspartate aminotransferase from baker's yeast (Saccharomyces cerevisiae). Biochem. J. 277: 335-340.
14. Cruz, F., Villalba, M., Garcia-Espinosa, M.A., Ballesteros, P., Bogonez, E., Satrustegui, J., and Cerdan, S. 2001. Intracellular compartmentation of pyruvate in primary cultures of cortical neurons as detected by (13)C NMR spectroscopy with multiple (13)C labels. J. Neurosci. Res. 66: 771-781.
15. Dilova, I., Easlon, E., and Lin, S.J. 2007. Calorie restriction and the nutrient sensing signaling pathways. Cell. Mol. Life Sci. 64: 752-767.
16. Easlon, E., Tsang, F., Dilova, I., Wang, C., Lu, S.P., Skinner, C., and Lin, S.J. 2007. The dihydrolipoamide acetyltransferase is a novel metabolic longevity factor and is required for calorie restriction-mediated life span extension. J. Biol. Chem. 282: 6161-6171.
17. +) in Saccharomyces cerevisiae, and its comparison with GPD1. Mol. Microbiol. 17: 95-107.
18. Erjavec, N. and Nystrom, T. 2007. Sir2p-dependent protein segregation gives rise to a superior reactive oxygen species management in the progeny of Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. 104: 10877-10881.
19. Erjavec, N., Larsson, L., Grantham, J., and Nystrom, T. 2007. Accelerated aging and failure to segregate damaged proteins in Sir2 mutants can be suppressed by overproducing the protein aggregation-remodeling factor Hsp104p. Genes & Dev. 21: 2410-2421.
20. Eto, K., Tsubamoto, Y., Terauchi, Y., Sugiyama, T., Kishimoto, T., Takahashi, N., Yamauchi, N., Kubota, N., Murayama, S., Aizawa, T., et al. 1999. Role of NADH shuttle system in glucose-induced activation of mitochondrial metabolism and insulin secretion. Science 283: 981-985.
21. Fabrizio, P. and Longo, V.D. 2003. The chronological life span of Saccharomyces cerevisiae. Aging Cell 2: 73-81.
22. Fabrizio, P., Pozza, F., Pletcher, S.D., Gendron, C.M., and Longo, V.D. 2001. Regulation of longevity and stress resistance by Sch9 in yeast. Science 292: 288-290.
23. Falcón, A.A. and Aris, J.P. 2003. Plasmid accumulation reduces life span in Saccharomyces cerevisiae. J. Biol. Chem. 278: 41607-41617.
24. Ferea, T.L., Botstein, D., Brown, P.O., and Rosenzweig, R.F. 1999. Systematic changes in gene expression patterns following adaptive evolution in yeast. Proc. Natl. Acad. Sci. 96: 9721-9726.
25. Forsburg, S.L. and Guarente, L. 1989. Identification and characterization of HAP4: A third component of the CCAAT-bound HAP2/HAP3 heteromer. Genes & Dev. 3: 1166-1178.
26. Gallo, C.M., Smith Jr., D.L., and Smith, J.S. 2004. Nicotinamide clearance by Pnc1 directly regulates Sir2-mediated silencing and longevity. Mol. Cell. Biol. 24: 1301-1312.
27. Grauslund, M. and Ronnow, B. 2000. Carbon source-dependent transcriptional regulation of the mitochondrial glycerol-3-phosphate dehydrogenase gene, GUT2, from Saccharomyces cerevisiae. Can. J. Microbiol. 46: 1096-1100.
28. Guarente, L. 2006. Sirtuins as potential targets for metabolic syndrome. Nature 444: 868-874.
29. Haigis, M.C., Mostoslavsky, R., Haigis, K.M., Fahie, K., Christodoulou, D.C., Murphy, A.J., Valenzuela, D.M., Yancopoulos, G.D., Karow, M., Blander, G., et al. 2006. SIRT4 inhibits glutamate dehydrogenase and opposes the effects of calorie restriction in pancreatic β cells. Cell 126: 941-954.
30. Imai, S., Armstrong, C.M., Kaeberlein, M., and Guarente, L. 2000. Transcriptional silencing and longevity protein Sir2 is an NAD-dependent histone deacetylase. Nature 403: 795-800.
31. Jazwinski, S.M. 2005. The retrograde response links metabolism with stress responses, chromatin-dependent gene activation, and genome stability in yeast aging. Gene 354: 22-27.
32. Jiang, J.C., Jaruga, E., Repnevskaya, M.V., and Jazwinski, S.M. 2000. An intervention resembling caloric restriction prolongs life span and retards aging in yeast. FASEB J. 14: 2135-2137.
33. Jiang, J.C., Wawryn, J., Shantha Kumara, H.M., and Jazwinski, S.M. 2002. Distinct roles of processes modulated by histone deacetylases Rpd3p, Hda1p, and Sir2p in life extension by caloric restriction in yeast. Exp. Gerontol. 37: 1023-1030.
34. Kaeberlein, M., McVey, M., and Guarente, L. 1999. The SIR2/3/4 complex and SIR2 alone promote longevity in Saccharomyces cerevisiae by two different mechanisms. Genes & Dev. 13: 2570-2580.
35. Kaeberlein, M., Andalis, A.A., Fink, G.R., and Guarente, L. 2002. High osmolarity extends life span in Saccharomyces cerevisiae by a mechanism related to calorie restriction. Mol. Cell. Biol. 22: 8056-8066.
36. Kaeberlein, M., Kirkland, K.T., Fields, S., and Kennedy, B.K. 2004. Sir2-independent life span extension by calorie restriction in yeast. PLoS Biol. 2: 1381-1387.
37. Kaeberlein, M., Hu, D., Kerr, E.O., Tsuchiya, M., Westman, E.A., Dang, N., Fields, S., and Kennedy, B.K. 2005a. Increased life span due to calorie restriction in respiratory-deficient yeast. PLoS Genet. 1: 614-621.
38. Kaeberlein, M., Powers III, R.W., Steffen, K.K., Westman, E.A., Hu, D., Dang, N., Kerr, E.O., Kirkland, K.T., Fields, S., and Kennedy, B.K. 2005b. Regulation of yeast replicative life span by TOR and Sch9 in response to nutrients. Science 310: 1193-1196.
39. Kresze, G.B. and Ronft, H. 1981. Pyruvate dehydrogenase complex from baker's yeast. 1. Purification and some kinetic and regulatory properties. Eur. J. Biochem. 119: 573-579.
40. Lamming, D.W., Latorre-Esteves, M., Medvedik, O., Wong, S.N., Tsang, F.A., Wang, C., Lin, S.J., and Sinclair, D.A. 2005. HST2 mediates SIR2-independent life-span extension by calorie restriction. Science 309: 1861-1864.
41. Landry, J., Sutton, A., Tafrov, S.T., Heller, R.C., Stebbins, J., Pillus, L., and Sternglanz, R. 2000. The silencing protein SIR2 and its homologs are NAD-dependent protein deacetylases. Proc. Natl. Acad. Sci. 97: 5807-5811.
42. Lawson, J.E., Niu, X.D., and Reed, L.J. 1991. Functional analysis of the domains of dihydrolipoamide acetyltransferase from Saccharomyces cerevisiae. Biochemistry (Mosc.) 30: 11249-11254.
43. Lin, S.J. and Guarente, L. 2003. Nicotinamide adenine dinucleotide, a metabolic regulator of transcription, longevity and disease. Curr. Opin. Cell Biol. 15: 241-246.
44. Lin, S.J., Defossez, P.A., and Guarente, L. 2000. Requirement of NAD and SIR2 for life-span extension by calorie restriction in Saccharomyces cerevisiae. Science 289: 2126-2128.
45. Lin, S.S., Manchester, J.K., and Gordon, J.I. 2001. Enhanced gluconeogenesis and increased energy storage as hallmarks of aging in Saccharomyces cerevisiae. J. Biol. Chem. 276: 36000-36007.
46. Lin, S.-J., Kaeberlein, M., Andalis, A.A., Sturtz, L.A., Defossez, P.-A., Culotta, V.C., Fink, G.R., and Guarente, L. 2002. Calorie restriction extends life span by shifting carbon toward respiration. Nature 418: 344-348.
47. Lin, S.J., Ford, E., Haigis, M., Liszt, G., and Guarente, L. 2004. Calorie restriction extends yeast life span by lowering the level of NADH. Genes & Dev. 18: 12-16.
48. Longtine, M.S., McKenzie III, A., Demarini, D.J., Shah, N.G., Wach, A., Brachat, A., Philippsen, P., and Pringle, J.R. 1998. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14: 953-961.
49. Martin, D.E., Soulard, A., and Hall, M.N. 2004. TOR regulates ribosomal protein gene expression via PKA and the Forkhead transcription factor FHL1. Cell 119: 969-979.
50. Meijer, A.J. and Van Dam, K. 1974. The metabolic significance of anion transport in mitochondria. Biochim. Biophys. Acta 346: 213-244.
51. Minard, K.I. and McAlister-Henn, L. 1991. Isolation, nucleotide sequence analysis, and disruption of the MDH2 gene from Saccharomyces cerevisiae: Evidence for three isozymes of yeast malate dehydrogenase. Mol. Cell. Biol. 11: 370-380.
52. Minard, K.I. and McAlister-Henn, L. 1992. Glucose-induced degradation of the MDH2 isozyme of malate dehydrogenase in yeast. J. Biol. Chem. 267: 17458-17464.
53. Morin, P.J., Subramanian, G.S., and Gilmore, T.D. 1992. AAT1, a gene encoding a mitochondrial aspartate aminotransferase in Saccharomyces cerevisiae. Biochim. Biophys. Acta 1171: 211-214.
54. Nisoli, E., Tonello, C., Cardile, A., Cozzi, V., Bracale, R., Tedesco, L., Falcone, S., Valerio, A., Cantoni, O., Clementi, E., et al. 2005. Calorie restriction promotes mitochondrial biogenesis by inducing the expression of eNOS. Science 310: 314-317.
55. Palaiologos, G., Hertz, L., and Schousboe, A. 1988. Evidence that aspartate aminotransferase activity and ketodicarboxylate carrier function are essential for biosynthesis of transmitter glutamate. J. Neurochem. 51: 317-320.
56. Palmieri, L., Palmieri, F., Runswick, M.J., and Walker, J.E. 1996. Identification by bacterial expression and functional reconstitution of the yeast genomic sequence encoding the mitochondrial dicarboxylate carrier protein. FEBS Lett. 399: 299-302.
57. Palmieri, L., Vozza, A., Agrimi, G., De Marco, V., Runswick, M.J., Palmieri, F., and Walker, J.E. 1999. Identification of the yeast mitochondrial transporter for oxaloacetate and sulfate. J. Biol. Chem. 274: 22184-22190.
58. Palmieri, L., Agrimi, G., Runswick, M.J., Fearnley, I.M., Palmieri, F., and Walker, J.E. 2001. Identification in Saccharomyces cerevisiae of two isoforms of a novel mitochondrial transporter for 2-oxoadipate and 2-oxoglutarate. J. Biol. Chem. 276: 1916-1922.
59. Panowski, S.H., Wolff, S., Aguilaniu, H., Durieux, J., and Dillin, A. 2007. PHA-4/Foxa mediates diet-restriction-induced longevity of C. elegans. Nature 447: 550-555.
60. Park, P.U., McVey, M., and Guarente, L. 2002. Separation of mother and daughter cells. Methods Enzymol. 351: 468-477.
61. Pronk, J.T., Yde Steensma, H., and Van Dijken, J.P. 1996. Pyruvate metabolism in Saccharomyces cerevisiae. Yeast 12: 1607-1633.
62. Rogina, B. and Helfand, S.L. 2004. Sir2 mediates longevity in the fly through a pathway related to calorie restriction. Proc. Natl. Acad. Sci. 101: 15998-16003.
63. Ronnow, B. and Kielland-Brandt, M.C. 1993. GUT2, a gene for mitochondrial glycerol 3-phosphate dehydrogenase of Saccharomyces cerevisiae. Yeast 9: 1121-1130.
64. Roth, G.S., Ingram, D.K., and Lane, M.A. 2001. Caloric restriction in primates and relevance to humans. Ann. N. Y. Acad. Sci. 928: 305-315.
65. Schneider, J.C. and Guarente, L. 1991. Regulation of the yeast CYT1 gene encoding cytochrome c1 by HAP1 and HAP2/3/4. Mol. Cell. Biol. 11: 4934-4942.
66. Sekito, T., Thornton, J., and Butow, R.A. 2000. Mitochondria-to-nuclear signaling is regulated by the subcellular localization of the transcription factors Rtg1p and Rtg3p. Mol. Biol. Cell 11: 2103-2115.
67. Shen, W., Wei, Y., Dauk, M., Tan, Y., Taylor, D.C., Selvaraj, G., and Zou, J. 2006. Involvement of a glycerol-3-phosphate dehydrogenase in modulating the NADH/NAD+ ratio provides evidence of a mitochondrial glycerol-3-phosphate shuttle in Arabidopsis. Plant Cell 18: 422-441.
68. Sherman, F., Fink, G.R., and Lawrence, C.W. 1978. Methods in yeast genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
69. Sinclair, D.A. and Guarente, L. 1997. Extrachromosomal rDNA circles - A cause of aging in yeast. Cell 91: 1033-1042.
70. +-dependent protein deacetylase activity in the Sir2 protein family. Proc. Natl. Acad. Sci. 97: 6658-6663.
71. Thielen, J. and Ciriacy, M. 1991. Biochemical basis of mitochondrial acetaldehyde dismutation in Saccharomyces cerevisiae. J. Bacteriol. 173: 7012-7017.
72. Thompson, L.M., Sutherland, P., Steffan, J.S., and McAlister-Henn, L. 1988. Gene sequence and primary structure of mitochondrial malate dehydrogenase from Saccharomyces cerevisiae. Biochemistry (Mosc.) 27: 8393-8400.
73. Tissenbaum, H.A. and Guarente, L. 2001. Increased dosage of a sir-2 gene extends lifespan in Caenorhabditis elegans. Nature 410: 227-230.
74. + transporter in Saccharomyces cerevisiae. J. Biol. Chem. 281: 1524-1531.
75. Wang, Y. and Tissenbaum, H.A. 2006. Overlapping and distinct functions for a Caenorhabditis elegans SIR2 and DAF-16/FOXO. Mech. Ageing Dev. 127: 48-56.
76. Wang, H.T., Rahaim, P., Robbins, P., and Yocum, R.R. 1994. Cloning, sequence, and disruption of the Saccharomyces diastaticus DAR1 gene encoding a glycerol-3-phosphate dehydrogenase. J. Bacteriol. 176: 7091-7095.
77. Weindruch, W. and Walford, R.L. 1998. The retardation of aging and diseases by dietary restriction. Charles C. Thomas, Springfield, IL.
78. Wood, J.G., Rogina, B., Lavu, S., Howitz, K., Helfand, S.L., Tatar, M., and Sinclair, D. 2004. Sirtuin activators mimic caloric restriction and delay ageing in metazoans. Nature 430: 686-689.
79. Young, E.T. and Pilgrim, D. 1985. Isolation and DNA sequence of ADH3, a nuclear gene encoding the mitochondrial isozyme of alcohol dehydrogenase in Saccharomyces cerevisiae. Mol. Cell. Biol. 5: 3024-3034.