Nicotinamide Riboside Promotes Sir2 Silencing and Extends Lifespan via Nrk and Urh1/Pnp1/Meu1 Pathways to NAD+

Cell

Volumn 129, Issue 3, 2007, Pages 473-484

  Belenky, Peter ^a   Racette, Frances G ^b   Bogan, Katrina L ^a   McClure, Julie M ^b   Smith, Jeffrey S ^b   Brenner, Charles ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NICOTINAMIDE ADENINE DINUCLEOTIDE; NICOTINAMIDE NUCLEOTIDE; NICOTINAMIDE RIBOSIDE; NICOTINAMIDE RIBOSIDE KINASE 1; NICOTINAMIDE RIBOSIDE KINASE 2; SILENT INFORMATION REGULATOR PROTEIN 2; UNCLASSIFIED DRUG;

AGING; AMINO ACID METABOLISM; ARTICLE; CALORIC RESTRICTION; CELL SURVIVAL; DNA RECOMBINATION; ENZYME SPECIFICITY; GENE FUNCTION; GENE LOCUS; GENE REPRESSION; GENE SILENCING; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN SYNTHESIS; YEAST CELL;

EUKARYOTA;

EID: 34247502715     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2007.03.024     Document Type: Article

References (66)

1. Aksoy S., Szumlanski C.L., and Weinshilboum R.M. Human liver nicotinamide N-methyltransferase. cDNA cloning, expression, and biochemical characterization. J. Biol. Chem. 269 (1994) 14835-14840
2. Anderson R.M., Bitterman K.J., Wood J.G., Medvedik O., Cohen H., Lin S.S., Manchester J.K., Gordon J.I., and Sinclair D.A. Manipulation of a nuclear NAD+ salvage pathway delays aging without altering steady-state NAD+ levels. J. Biol. Chem. 277 (2002) 18881-18890
3. Anderson R.M., Bitterman K.J., Wood J.G., Medvedik O., and Sinclair D.A. Nicotinamide and PNC1 govern lifespan extension by calorie restriction in Saccharomyces cerevisiae. Nature 423 (2003) 181-185
4. Anderson R.M., Latorre-Esteves M., Neves A.R., Lavu S., Medvedik O., Taylor C., Howitz K.T., Santos H., and Sinclair D.A. Yeast life-span extension by calorie restriction is independent of NAD fluctuation. Science 302 (2003) 2124-2126
5. Araki T., Sasaki Y., and Milbrandt J. Increased nuclear NAD biosynthesis and SIRT1 activation prevent axonal degeneration. Science 305 (2004) 1010-1013
6. Baur J.A., Pearson K.J., Price N.L., Jamieson H.A., Lerin C., Kalra A., Prabhu V.V., Allard J.S., Lopez-Lluch G., Lewis K., et al. Resveratrol improves health and survival of mice on a high-calorie diet. Nature 444 (2006) 337-342
7. Belenky P., Bogan K.L., and Brenner C. NAD(+) metabolism in health and disease. Trends Biochem. Sci. 32 (2007) 12-19
8. Benyo Z., Gille A., Kero J., Csiky M., Suchankova M.C., Nusing R.M., Moers A., Pfeffer K., and Offermanns S. GPR109A (PUMA-G/HM74A) mediates nicotinic acid-induced flushing. J. Clin. Invest. 115 (2005) 3634-3640
9. Bieganowski P., and Brenner C. Discoveries of nicotinamide riboside as a nutrient and conserved NRK genes establish a Preiss-Handler independent route to NAD+ in fungi and humans. Cell 117 (2004) 495-502
10. Bieganowski P., Pace H.C., and Brenner C. Eukaryotic NAD+ synthetase Qns1 contains an essential, obligate intramolecular thiol glutamine amidotransferase domain related to nitrilase. J. Biol. Chem. 278 (2003) 33049-33055
11. Bitterman K.J., Anderson R.M., Cohen H.Y., Latorre-Esteves M., and Sinclair D.A. Inhibition of silencing and accelerated aging by nicotinamide, a putative negative regulator of yeast Sir2 and human SIRT1. J. Biol. Chem. 277 (2002) 45099-45107
12. Borra M.T., Langer M.R., Slama J.T., and Denu J.M. Substrate specificity and kinetic mechanism of the Sir2 family of NAD+-dependent histone/protein deacetylases. Biochemistry 43 (2004) 9877-9887
13. Brachmann C.B., Davies A., Cost G.J., Caputo E., Li J., Hieter P., and Boeke J.D. 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 (1998) 115-132
14. Buck S.W., Sandmeier J.J., and Smith J.S. RNA polymerase I propagates unidirectional spreading of rDNA silent chromatin. Cell 111 (2002) 1003-1014
15. Burke D., Dawson D., and Stearns T. Methods in Yeast Genetics (2000), Cold Spring Harbor Press, Cold Spring Harbor, NY
16. Catz P., Shinn W., Kapetanovic I.M., Kim H., Kim M., Jacobson E.L., Jacobson M.K., and Green C.E. Simultaneous determination of myristyl nicotinate, nicotinic acid, and nicotinamide in rabbit plasma by liquid chromatography-tandem mass spectrometry using methyl ethyl ketone as a deproteinization solvent. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 829 (2005) 123-135
17. Degano M., Gopaul D.N., Scapin G., Schramm V.L., and Sacchettini J.C. Three-dimensional structure of the inosine-uridine nucleoside N-ribohydrolase from Crithidia fasciculata. Biochemistry 35 (1996) 5971-5981
18. Domergue R., Castano I., De Las Penas A., Zupancic M., Lockatell V., Hebel R.J., Johnson D., and Cormack B.P. Nicotinic acid limitation regulates silencing of Candida adhesins during UTI. Science 308 (2005) 866-870
19. Gallo C.M., Smith Jr. D.L., and Smith J.S. Nicotinamide clearance by Pnc1 directly regulates Sir2-mediated silencing and longevity. Mol. Cell. Biol. 24 (2004) 1301-1312
20. Ghislain M., Talla E., and Francois J.M. Identification and functional analysis of the Saccharomyces cerevisiae nicotinamidase gene, PNC1. Yeast 19 (2002) 215-224
21. Gottlieb S., and Esposito R.E. A new role for a yeast transcriptional silencer gene, SIR2, in regulation of recombination in ribosomal DNA. Cell 56 (1989) 771-776
22. Grossman L., and Kaplan N.O. Nicotinamide riboside phosphorylase from human erythrocytes. I. Phosphorolytic activity. J. Biol. Chem. 231 (1958) 717-726
23. Guarente L. Sir2 links chromatin silencing, metabolism, and aging. Genes Dev. 14 (2000) 1021-1026
24. Harden A., and Young W.J. The alcoholic fermentation of yeast-juice. Proc. R. Soc. Lond. B. Biol. Sci. 77 (1905) 405-420
25. Hsiao K., Chapman P., Nilsen S., Eckman C., Harigaya Y., Younkin S., Yang F., and Cole G. Correlative memory deficits, Abeta elevation, and amyloid plaques in transgenic mice. Science 274 (1996) 99-102
26. Imai S., Armstrong C.M., Kaeberlein M., and Guarente L. Transcriptional silencing and longevity protein Sir2 is an NAD-dependent histone deacetylase. Nature 403 (2000) 795-800
27. Imai T., and Anderson B.M. Nicotinamide riboside phosphorylase from beef liver: Purification and characterization. Arch. Biochem. Biophys. 254 (1987) 253-262
28. Kaeberlein M., Kirkland K.T., Fields S., and Kennedy B.K. Sir2-independent life span extension by calorie restriction in yeast. PLoS Biol. 2 (2004) E296
29. Kaeberlein M., McVey M., and Guarente L. The SIR2/3/4 complex and SIR2 alone promote longevity in Saccharomyces cerevisiae by two different mechanisms. Genes Dev. 13 (1999) 2570-2580
30. Kaneko S., Wang J., Kaneko M., Yiu G., Hurrell J.M., Chitnis T., Khoury S.J., and He Z. Protecting axonal degeneration by increasing nicotinamide adenine dinucleotide levels in experimental autoimmune encephalomyelitis models. J. Neurosci. 26 (2006) 9794-9804
31. Kennedy B.K., Austriaco Jr. N.R., and Guarente L. Daughter cells of Saccharomyces cerevisiae from old mothers display a reduced life span. J. Cell Biol. 127 (1994) 1985-1993
32. Krehl W.A., Trepley L.J., Sarma P.S., and Elvehjem C.A. Growth retarding effect of corn in niacin-low rations and its counteraction by tryptophan. Science 101 (1945) 489-490
33. Kurtz J.E., Exinger F., Erbs P., and Jund R. The URH1 uridine ribohydrolase of Saccharomyces cerevisiae. Curr. Genet. 41 (2002) 132-141
34. Lagauge M., Argmann C., Gerhart-Hines Z., Meziane H., Lerin C., Daussin F., Messadeq N., Milne J., Lambert P., Elliott P., et al. Resveratrol improves mitochondrial function and protects against metabolic disease by activating Sirt1 and PGC1-α. Cell 127 (2006) 1109-1122
35. Lecoq K., Belloc I., Desgranges C., Konrad M., and Daignan-Fornier B. YLR209c encodes Saccharomyces cerevisiae purine nucleoside phosphorylase. J. Bacteriol. 183 (2001) 4910-4913
36. Lewandowicz A., Tyler P.C., Evans G.B., Furneaux R.H., and Schramm V.L. Achieving the ultimate physiological goal in transition state analogue inhibitors for purine nucleoside phosphorylase. J. Biol. Chem. 278 (2003) 31465-31468
37. Lin S.J., Defossez P.A., and Guarente L. Requirement of NAD and SIR2 for life-span extension by calorie restriction in Saccharomyces cerevisiae. Science 289 (2000) 2126-2128
38. Lin S.J., Ford E., Haigis M., Liszt G., and Guarente L. Calorie restriction extends yeast life span by lowering the level of NADH. Genes Dev. 18 (2004) 12-16
39. Lin S.S., Manchester J.K., and Gordon J.I. Enhanced gluconeogenesis and increased energy storage as hallmarks of aging in Saccharomyces cerevisiae. J. Biol. Chem. 276 (2001) 36000-36007
40. Markert M.L. Purine nucleoside phosphorylase deficiency. Immunodefic. Rev. 3 (1991) 45-81
41. Mitterbauer R., Karl T., and Adam G. Saccharomyces cerevisiae URH1 (encoding uridine-cytidine N-ribohydrolase): Functional complementation by a nucleoside hydrolase from a protozoan parasite and by a mammalian uridine phosphorylase. Appl. Environ. Microbiol. 68 (2002) 1336-1343
42. Qin W., Yang T., Ho L., Zhao Z., Wang J., Chen L., Zhao W., Thiyagarajan M., MacGrogan D., Rodgers J.T., et al. Neuronal SIRT1 activation as a novel mechanism underlying the prevention of Alzheimer disease amyloid neuropathology by calorie restriction. J. Biol. Chem. 281 (2006) 21745-21754
43. Revollo J.R., Grimm A.A., and Imai S. The NAD biosynthesis pathway mediated by nicotinamide phosphoribosyltransferase regulates Sir2 activity in mammalian cells. J. Biol. Chem. 279 (2004) 50754-50763
44. Rodgers J.T., Lerin C., Haas W., Gygi S.P., Spiegelman B.M., and Puigserver P. Nutrient control of glucose homeostasis through a complex of PGC-1alpha and SIRT1. Nature 434 (2005) 113-118
45. Rogina B., and Helfand S.L. Sir2 mediates longevity in the fly through a pathway related to calorie restriction. Proc. Natl. Acad. Sci. USA 101 (2004) 15998-16003
46. Rongvaux A., Shea R.J., Mulks M.H., Gigot D., Urbain J., Leo O., and Andris F. Pre-B-cell colony-enhancing factor, whose expression is up-regulated in activated lymphocytes, is a nicotinamide phosphoribosyltransferase, a cytosolic enzyme involved in NAD biosynthesis. Eur. J. Immunol. 32 (2002) 3225-3234
47. Rowen J.W., and Kornberg A. The phosphorolysis of nicotinamide riboside. J. Biol. Chem. 193 (1951) 497-507
48. Sandmeier J.J., Celic I., Boeke J.D., and Smith J.S. Telomeric and rDNA silencing in Saccharomyces cerevisiae are dependent on a nuclear NAD(+) salvage pathway. Genetics 160 (2002) 877-889
49. Sasaki Y., Araki T., and Milbrandt J. Stimulation of nicotinamide adenine dinucleotide biosynthetic pathways delays axonal degeneration after axotomy. J. Neurosci. 26 (2006) 8484-8491
50. Sauve A.A., Wolberger C., Schramm V.L., and Boeke J.D. The biochemistry of Sirtuins. Annu. Rev. Biochem. 75 (2006) 435-465
51. Schramm V.L. Development of transition state analogues of purine nucleoside phosphorylase as anti-T-cell agents. Biochim. Biophys. Acta 1587 (2002) 107-117
52. Sherman F. Getting started with yeast. Methods Enzymol. 194 (1991) 3-21
53. Shi W., Schramm V.L., and Almo S.C. Nucleoside hydrolase from Leishmania major. Cloning, expression, catalytic properties, transition state inhibitors, and the 2.5-Å crystal structure. J. Biol. Chem. 274 (1999) 21114-21120
54. Sinclair D.A., and Guarente L. Extrachromosomal rDNA circles-a cause of aging in yeast. Cell 91 (1997) 1033-1042
55. Sinclair D.A., and Guarente L. Unlocking the secrets of longevity genes. Sci. Am. 294 (2006) 48-51 54-57
56. Smith J.S., and Boeke J.D. An unusual form of transcriptional silencing in yeast ribosomal DNA. Genes Dev. 11 (1997) 241-254
57. Smith J.S., Brachmann C.B., Celic I., Kenna M.A., Muhammad S., Starai V.J., Avalos J.L., Escalante-Semerena J.C., Grubmeyer C., Wolberger C., and Boeke J.D. A phylogenetically conserved NAD+-dependent protein deacetylase activity in the Sir2 protein family. Proc. Natl. Acad. Sci. USA 97 (2000) 6658-6663
58. Smith J.S., Caputo E., and Boeke J.D. A genetic screen for ribosomal DNA silencing defects identifies multiple DNA replication and chromatin-modulating factors. Mol. Cell. Biol. 19 (1999) 3184-3197
59. Subhi A.L., Diegelman P., Porter C.W., Tang B., Lu Z.J., Markham G.D., and Kruger W.D. Methylthioadenosine phosphorylase regulates ornithine decarboxylase by production of downstream metabolites. J. Biol. Chem. 278 (2003) 49868-49873
60. Tanner K.G., Landry J., Sternglanz R., and Denu J.M. Silent information regulator 2 family of NAD-dependent histone/protein deacetylases generates a unique product, 1-O-acetyl-ADP-ribose. Proc. Natl. Acad. Sci. USA 97 (2000) 14178-14182
61. Tanny J.C., and Moazed D. Coupling of histone deacetylation to NAD breakdown by the yeast silencing protein Sir2: Evidence for acetyl transfer from substrate to an NAD breakdown product. Proc. Natl. Acad. Sci. USA 98 (2001) 415-420
62. Tissenbaum H.A., and Guarente L. Increased dosage of a sir-2 gene extends lifespan in Caenorhabditis elegans. Nature 410 (2001) 227-230
63. Wang J., Zhai Q., Chen Y., Lin E., Gu W., McBurney M.W., and He Z. A local mechanism mediates NAD-dependent protection of axon degeneration. J. Cell Biol. 170 (2005) 349-355
64. Wickerham L.J. A critical evaluation of the nitrogen assimilation tests commonly used in the classification of yeasts. J Bacteriol. 52 (1946) 293-301
65. Wielgus-Kutrowska B., Kulikowska E., Wierzchowski J., Bzowska A., and Shugar D. Nicotinamide riboside, an unusual, non-typical, substrate of purified purine-nucleoside phosphorylases. Eur. J. Biochem. 243 (1997) 408-414
66. Winzeler E.A., Shoemaker D.D., Astromoff A., Liang H., Anderson K., Andre B., Bangham R., Benito R., Boeke J.D., Bussey H., et al. Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 285 (1999) 901-906