Mechanism of sirtuin nhibition by nicotinamide: Altering the NAD + cosubstrate specificity of a Sir2 enzyme

Molecular Cell

Volumn 17, Issue 6, 2005, Pages 855-868

  Avalos, José L ^a   Bever, Katherine M ^a   Wolberger, Cynthia ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NICOTINAMIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE; SIRTUIN; DRUG DERIVATIVE; HISTONE DEACETYLASE; NICOTINIC ACID; NICOTINIC ACID ADENINE DINUCLEOTIDE; SILENT INFORMATION REGULATOR PROTEIN; SIR2 PROTEIN, S CEREVISIAE; VASODILATOR AGENT;

APOPTOSIS; ARTICLE; CATALYSIS; CONTROLLED STUDY; DEACETYLATION; ENZYME ACTIVITY; GENE CONTROL; GENE SILENCING; GENETIC TRANSCRIPTION; MEMBRANE BINDING; NONHUMAN; PROTEIN STRUCTURE; ACETYLATION; AMINO ACID SEQUENCE; CHEMISTRY; ENZYME SPECIFICITY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; SEQUENCE HOMOLOGY;

ACETYLATION; AMINO ACID SEQUENCE; CATALYSIS; GENE EXPRESSION REGULATION, FUNGAL; HISTONE DEACETYLASES; MOLECULAR SEQUENCE DATA; NAD; NIACIN; NIACINAMIDE; SEQUENCE HOMOLOGY, AMINO ACID; SILENT INFORMATION REGULATOR PROTEINS, SACCHAROMYCES CEREVISIAE; SIRTUINS; SUBSTRATE SPECIFICITY; VASODILATOR AGENTS;

EID: 15244355745     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2005.02.022     Document Type: Article

References (53)

1. R.M. Anderson, K.J. Bitterman, J.G. Wood, O. Medvedik, H. Cohen, S.S. Lin, J.K. Manchester, J.I. Gordon, and D.A. Sinclair Manipulation of a nuclear NAD+ salvage pathway delays aging without altering steady-state NAD+ levels J. Biol. Chem. 277 2002 18881 18890
2. R.M. Anderson, K.J. Bitterman, J.G. Wood, O. Medvedik, and D.A. Sinclair Nicotinamide and PNC1 govern lifespan extension by calorie restriction in Saccharomyces cerevisiae Nature 423 2003 181 185
3. T. Araki, Y. Sasaki, and J. Milbrandt Increased nuclear NAD biosynthesis and SIRT1 activation prevent axonal degeneration Science 305 2004 1010 1013
4. J.L. Avalos, I. Celic, S. Muhammad, M.S. Cosgrove, J.D. Boeke, and C. Wolberger Structure of a Sir2 enzyme bound to an acetylated p53 peptide Mol. Cell 10 2002 523 535
5. J.L. Avalos, J.D. Boeke, and C. Wolberger Structural basis for the mechanism and regulation of Sir2 enzymes Mol. Cell 13 2004 639 648
6. C.E. Bell, T.O. Yeates, and D. Eisenberg Unusual conformation of nicotinamide adenine dinucleotide (NAD) bound to diphtheria toxin: a comparison with NAD bound to the oxidoreductase enzymes Protein Sci. 6 1997 2084 2096
7. C.B. Bennett, J.R. Snipe, J.W. Westmoreland, and M.A. Resnick SIR functions are required for the toleration of an unrepaired double-strand break in a dispensable yeast chromosome Mol. Cell. Biol. 21 2001 5359 5373
8. K.J. Bitterman, R.M. Anderson, H.Y. Cohen, M. Latorre-Esteves, and D.A. Sinclair 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
9. M.T. Borra, M.R. Langer, J.T. Slama, and J.M. Denu Substrate specificity and kinetic mechanism of the Sir2 family of NAD+-dependent histone/protein deacetylases Biochemistry 43 2004 9877 9887
10. C.B. Brachmann, J.M. Sherman, S.E. Devine, E.E. Cameron, L. Pillus, and J.D. Boeke The SIR2 gene family, conserved from bacteria to humans, functions in silencing, cell cycle progression, and chromosome stability Genes Dev. 9 1995 2888 2902
11. A. Brunet, L.B. Sweeney, J.F. Sturgill, K.F. Chua, P.L. Greer, Y. Lin, H. Tran, S.E. Ross, R. Mostoslavsky, and H.Y. Cohen Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase Science 303 2004 2011 2015
12. A.T. Brunger, P.D. Adams, G.M. Clore, W.L. DeLano, P. Gros, R.W. Grosse-Kunstleve, J.S. Jiang, J. Kuszewski, M. Nilges, and N.S. Pannu Crystallography & NMR system: a new software suite for macromolecular structure determination Acta Crystallogr. D Biol. Crystallogr. 54 1998 905 921
13. H.Y. Cohen, C. Miller, K.J. Bitterman, N.R. Wall, B. Hekking, B. Kessler, K.T. Howitz, M. Gorospe, R. de Cabo, and D.A. Sinclair Calorie restriction promotes mammalian cell survival by inducing the SIRT1 deacetylase Science 305 2004 390 392
14. J.M. Denu Linking chromatin function with metabolic networks: Sir2 family of NAD(+)-dependent deacetylases Trends Biochem. Sci. 28 2003 41 48
15. M.S. Finnin, J.R. Donigian, and N.P. Pavletich Structure of the histone deacetylase SIRT2 Nat. Struct. Biol. 8 2001 621 625
16. M. Fulco, R.L. Schiltz, S. Iezzi, M.T. King, P. Zhao, Y. Kashiwaya, E. Hoffman, R.L. Veech, and V. Sartorelli Sir2 regulates skeletal muscle differentiation as a potential sensor of the redox state Mol. Cell 12 2003 51 62
17. C.M. Gallo, D.L. Smith Jr., and J.S. Smith Nicotinamide clearance by Pnc1 directly regulates Sir2-mediated silencing and longevity Mol. Cell. Biol. 24 2004 1301 1312
18. S. Gottlieb, and R.E. Esposito A new role for a yeast transcriptional silencer gene, SIR2, in regulation of recombination in ribosomal DNA Cell 56 1989 771 776
19. S. Han, J.A. Craig, C.D. Putnam, N.B. Carozzi, and J.A. Tainer Evolution and mechanism from structures of an ADP-ribosylating toxin and NAD complex Nat. Struct. Biol. 6 1999 932 936
20. S. Imai, C.M. Armstrong, M. Kaeberlein, and L. Guarente Transcriptional silencing and longevity protein Sir2 is an NAD-dependent histone deacetylase Nature 403 2000 795 800
21. M.D. Jackson, M.T. Schmidt, N.J. Oppenheimer, and J.M. Denu Mechanism of nicotinamide inhibition and transglycosidation by Sir2 histone/protein deacetylases J. Biol. Chem. 278 2003 50985 50998
22. M. Kaeberlein, M. McVey, and L. Guarente The SIR2/3/4 complex and SIR2 alone promote longevity in Saccharomyces cerevisiae by two different mechanisms Genes Dev. 13 1999 2570 2580
23. J. Landry, A. Sutton, S.T. Tafrov, R.C. Heller, J. Stebbins, L. Pillus, and R. Sternglanz The silencing protein SIR2 and its homologs are NAD-dependent protein deacetylases Proc. Natl. Acad. Sci. USA 97 2000 5807 5811
24. S.J. Lin, P.A. Defossez, and L. Guarente Requirement of NAD and SIR2 for life-span extension by calorie restriction in Saccharomyces cerevisiae Science 289 2000 2126 2128
25. J. Luo, A.Y. Nikolaev, S. Imai, D. Chen, F. Su, A. Shiloh, L. Guarente, and W. Gu Negative control of p53 by Sir2alpha promotes cell survival under stress Cell 107 2001 137 148
26. M.A. McMurray, and D.E. Gottschling An age-induced switch to a hyper-recombinational state Science 301 2003 1908 1911
27. D.E. McRee XtalView/Xfit - A versatile program for manipulating atomic coordinates and electron density J. Struct. Biol. 125 1999 156 165
28. J. Min, J. Landry, R. Sternglanz, and R.M. Xu Crystal structure of a SIR2 homolog-NAD complex Cell 105 2001 269 279
29. M.C. Motta, N. Divecha, M. Lemieux, C. Kamel, D. Chen, W. Gu, Y. Bultsma, M. McBurney, and L. Guarente Mammalian SIRT1 represses forkhead transcription factors Cell 116 2004 551 563
30. B.J. North, B.L. Marshall, M.T. Borra, J.M. Denu, and E. Verdin The human Sir2 ortholog, SIRT2, is an NAD+-dependent tubulin deacetylase Mol. Cell 11 2003 437 444
31. R.A. Olsen, L. Liu, N. Ghaderi, A. Johns, M.E. Hatcher, and L.J. Mueller The amide rotational barriers in picolinamide and nicotinamide: NMR and ab initio studies J. Am. Chem. Soc. 125 2003 10125 10132
32. Z. Otwinowski, and W. Minor Processing of X-ray diffraction data collected in oscillation mode Methods Enzymol. 276 1997 307 326
33. F. Picard, M. Kurtev, N. Chung, A. Topark-Ngarm, T. Senawong, R. Machado De Oliveira, M. Leid, M.W. McBurney, and L. Guarente Sirt1 promotes fat mobilization in white adipocytes by repressing PPAR-gamma Nature 429 2004 771 776
34. J.J. Sandmeier, I. Celic, J.D. Boeke, and J.S. Smith Telomeric and rDNA silencing in Saccharomyces cerevisiae are dependent on a nuclear NAD(+) salvage pathway Genetics 160 2002 877 889
35. A.A. Sauve, and V.L. Schramm Sir2 regulation by nicotinamide results from switching between base exchange and deacetylation chemistry Biochemistry 42 2003 9249 9256
36. A.A. Sauve, and V.L. Schramm SIR2: the biochemical mechanism of NAD(+)-dependent protein deacetylation and ADP-ribosyl enzyme intermediates Curr. Med. Chem. 11 2004 807 826
37. A.A. Sauve, I. Celic, J. Avalos, H. Deng, J.D. Boeke, and V.L. Schramm Chemistry of gene silencing: the mechanism of NAD+-dependent deacetylation reactions Biochemistry 40 2001 15456 15463
38. A.A. Sauve, R.D. Moir, V.L. Schramm, and I.M. Willis Chemical activation of sir2-dependent silencing by relief of nicotinamide inhibition Mol. Cell 17 2005 595 601
39. M.T. Schmidt, B.C. Smith, M.D. Jackson, and J.M. Denu Coenzyme specificity of Sir2 protein deacetylases: implications for physiological regulation J. Biol. Chem. 279 2004 40122 40129
40. T. Senawong, V.J. Peterson, D. Avram, D.M. Shepherd, R.A. Frye, S. Minucci, and M. Leid Involvement of the histone deacetylase SIRT1 in chicken ovalbumin upstream promoter transcription factor (COUP-TF)-interacting protein 2-mediated transcriptional repression J. Biol. Chem. 278 2003 43041 43050
41. J.S. Smith, C.B. Brachmann, I. Celic, M.A. Kenna, S. Muhammad, V.J. Starai, J.L. Avalos, J.C. Escalante-Semerena, C. Grubmeyer, C. Wolberger, and J.D. Boeke A phylogenetically conserved NAD+-dependent protein deacetylase activity in the Sir2 protein family Proc. Natl. Acad. Sci. USA 97 2000 6658 6663
42. J.S. Smith, J. Avalos, I. Celic, S. Muhammad, C. Wolberger, and J.D. Boeke SIR2 family of NAD(+)-dependent protein deacetylases Methods Enzymol. 353 2002 282 300
43. V.J. Starai, I. Celic, R.N. Cole, J.D. Boeke, and J.C. Escalante-Semerena Sir2-dependent activation of acetyl-CoA synthetase by deacetylation of active lysine Science 298 2002 2390 2392
44. T. Takata, and F. Ishikawa Human Sir2-related protein SIRT1 associates with the bHLH repressors HES1 and HEY2 and is involved in HES1- and HEY2-mediated transcriptional repression Biochem. Biophys. Res. Commun. 301 2003 250 257
45. J.C. Tanny, D.S. Kirkpatrick, S.A. Gerber, S.P. Gygi, and D. Moazed Budding yeast silencing complexes and regulation of Sir2 activity by protein-protein interactions Mol. Cell. Biol. 24 2004 6931 6946
46. H.A. Tissenbaum, and L. Guarente Increased dosage of a sir-2 gene extends lifespan in Caenorhabditis elegans Nature 410 2001 227 230
47. A. Vagin, and A. Teplyakov MOLREP: an automated program for molecular replacement J. Appl. Crystallogr. 30 1997 1022 1025
48. A. Vaquero, M. Scher, D. Lee, H. Erdjument-Bromage, P. Tempst, and D. Reinberg Human SirT1 interacts with histone H1 and promotes formation of facultative heterochromatin Mol. Cell 16 2004 93 105
49. H. Vaziri, S.K. Dessain, E. Ng Eaton, S.I. Imai, R.A. Frye, T.K. Pandita, L. Guarente, and R.A. Weinberg hSIR2(SIRT1) functions as an NAD-dependent p53 deacetylase Cell 107 2001 149 159
50. J.G. Wood, B. Rogina, S. Lavu, K. Howitz, S.L. Helfand, M. Tatar, and D. Sinclair Sirtuin activators mimic caloric restriction and delay ageing in metazoans Nature 430 2004 686 689
51. F. Yeung, J.E. Hoberg, C.S. Ramsey, M.D. Keller, D.R. Jones, R.A. Frye, and M.W. Mayo Modulation of NF-kappaB-dependent transcription and cell survival by the SIRT1 deacetylase EMBO J. 23 2004 2369 2380
52. K. Zhao, X. Chai, and R. Marmorstein Structure of the yeast Hst2 protein deacetylase in ternary complex with 2′-O-acetyl ADP ribose and histone peptide Structure (Camb) 11 2003 1403 1411
53. K. Zhao, R. Harshaw, X. Chai, and R. Marmorstein Structural basis for nicotinamide cleavage and ADP-ribose transfer by NAD(+)-dependent Sir2 histone/protein deacetylases Proc. Natl. Acad. Sci. USA 101 2004 8563 8568