Resveratrol rescues SIRT1-dependent adult stem cell decline and alleviates progeroid features in laminopathy-based progeria

Cell Metabolism

Volumn 16, Issue 6, 2012, Pages 738-750

  Liu, Baohua ^a,b,c   Ghosh, Shrestha ^a   Yang, Xi ^a   Zheng, Huiling ^a,c,d   Liu, Xinguang ^c,d   Wang, Zimei ^a   Jin, Guoxiang ^a   Zheng, Bojian ^a   Kennedy, Brian K ^c,e   Suh, Yousin ^c,f   Kaeberlein, Matt ^c,g   Tryggvason, Karl ^h   Zhou, Zhongjun ^a,b  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

^b UNIVERSITY OF HONG KONG   (China)

^c GUANGDONG MEDICAL UNIVERSITY   (China)

^d Key Laboratory for Medical Molecular Diagnostics of Guangdong Province   (China)

^e BUCK INSTITUTE FOR RESEARCH ON AGING   (United States)

^f ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^g UNIVERSITY OF WASHINGTON   (United States)

^h KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

LAMIN A; PRELAMIN A; RESVERATROL; SIRTUIN 1; UNCLASSIFIED DRUG;

ADULT STEM CELL; ANIMAL EXPERIMENT; ARTICLE; BONE DENSITY; BONE STRUCTURE; CELL NUCLEUS MATRIX; CONTROLLED STUDY; DRUG PROTEIN BINDING; ENZYME ACTIVITY; HUMAN; HUMAN CELL; LAMINOPATHY; LIFESPAN; LONGEVITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROGERIA; PROTEIN PROTEIN INTERACTION; TRABECULAR BONE; WEIGHT REDUCTION;

ADULT STEM CELLS; ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; CELL LINE; ENZYME ACTIVATION; HEK293 CELLS; HUMANS; LAMIN TYPE A; LONGEVITY; MEMBRANE PROTEINS; METALLOENDOPEPTIDASES; MICE; MICE, KNOCKOUT; NUCLEAR MATRIX; NUCLEAR PROTEINS; PROGERIA; PROTEIN BINDING; PROTEIN PRECURSORS; RECOMBINANT PROTEINS; SIRTUIN 1; STILBENES;

MUS;

EID: 84870506099     PISSN: 15504131     EISSN: 19327420     Source Type: Journal    
DOI: 10.1016/j.cmet.2012.11.007     Document Type: Article

References (67)

1. R.R. Alcendor, S. Gao, P. Zhai, D. Zablocki, E. Holle, X. Yu, B. Tian, T. Wagner, S.F. Vatner, and J. Sadoshima Sirt1 regulates aging and resistance to oxidative stress in the heart Circ. Res. 100 2007 1512 1521
2. A.S. Banks, N. Kon, C. Knight, M. Matsumoto, R. Gutiérrez- Juárez, L. Rossetti, W. Gu, and D. Accili SirT1 gain of function increases energy efficiency and prevents diabetes in mice Cell Metab. 8 2008 333 341
3. J.A. Baur Biochemical effects of SIRT1 activators Biochim. Biophys. Acta 1804 2010 1626 1634
4. J.A. Baur, K.J. Pearson, N.L. Price, H.A. Jamieson, C. Lerin, A. Kalra, V.V. Prabhu, J.S. Allard, G. Lopez-Lluch, and K. Lewis Resveratrol improves health and survival of mice on a high-calorie diet Nature 444 2006 337 342
5. D. Beher, J. Wu, S. Cumine, K.W. Kim, S.C. Lu, L. Atangan, and M. Wang Resveratrol is not a direct activator of SIRT1 enzyme activity Chem. Biol. Drug Des. 74 2009 619 624
6. L. Bordone, D. Cohen, A. Robinson, M.C. Motta, E. van Veen, A. Czopik, A.D. Steele, H. Crowe, S. Marmor, and J. Luo SIRT1 transgenic mice show phenotypes resembling calorie restriction Aging Cell 6 2007 759 767
7. M.T. Borra, B.C. Smith, and J.M. Denu Mechanism of human SIRT1 activation by resveratrol J. Biol. Chem. 280 2005 17187 17195
8. 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
9. C. Burnett, S. Valentini, F. Cabreiro, M. Goss, M. Somogyvári, M.D. Piper, M. Hoddinott, G.L. Sutphin, V. Leko, and J.J. McElwee Absence of effects of Sir2 overexpression on lifespan in C. elegans and Drosophila Nature 477 2011 482 485
10. C.R. Burtner, and B.K. Kennedy Progeria syndromes and ageing: what is the connection? Nat. Rev. Mol. Cell Biol. 11 2010 567 578
11. C. Cantó, Z. Gerhart-Hines, J.N. Feige, M. Lagouge, L. Noriega, J.C. Milne, P.J. Elliott, P. Puigserver, and J. Auwerx AMPK regulates energy expenditure by modulating NAD+ metabolism and SIRT1 activity Nature 458 2009 1056 1060
12. K. Cao, C.D. Blair, D.A. Faddah, J.E. Kieckhaefer, M. Olive, M.R. Erdos, E.G. Nabel, and F.S. Collins Progerin and telomere dysfunction collaborate to trigger cellular senescence in normal human fibroblasts J. Clin. Invest. 121 2011 2833 2844
13. A. Chalkiadaki, and L. Guarente Sirtuins mediate mammalian metabolic responses to nutrient availability Nat. Rev. Endocrinol. 8 2012 287 296
14. D. Chen, A.D. Steele, S. Lindquist, and L. Guarente Increase in activity during calorie restriction requires Sirt1 Science 310 2005 1641
15. H.L. Cheng, R. Mostoslavsky, S. Saito, J.P. Manis, Y. Gu, P. Patel, R. Bronson, E. Appella, F.W. Alt, and K.F. Chua Developmental defects and p53 hyperacetylation in Sir2 homolog (SIRT1)-deficient mice Proc. Natl. Acad. Sci. USA 100 2003 10794 10799
16. H. Dai, L. Kustigian, D. Carney, A. Case, T. Considine, B.P. Hubbard, R.B. Perni, T.V. Riera, B. Szczepankiewicz, G.P. Vlasuk, and R.L. Stein SIRT1 activation by small molecules: kinetic and biophysical evidence for direct interaction of enzyme and activator J. Biol. Chem. 285 2010 32695 32703
17. M. Eriksson, W.T. Brown, L.B. Gordon, M.W. Glynn, J. Singer, L. Scott, M.R. Erdos, C.M. Robbins, T.Y. Moses, and P. Berglund Recurrent de novo point mutations in lamin A cause Hutchinson-Gilford progeria syndrome Nature 423 2003 293 298
18. J. Espada, I. Varela, I. Flores, A.P. Ugalde, J. Cadiñanos, A.M. Pendás, C.L. Stewart, K. Tryggvason, M.A. Blasco, J.M. Freije, and C. López-Otín Nuclear envelope defects cause stem cell dysfunction in premature-aging mice J. Cell Biol. 181 2008 27 35
19. L.G. Fong, D. Frost, M. Meta, X. Qiao, S.H. Yang, C. Coffinier, and S.G. Young A protein farnesyltransferase inhibitor ameliorates disease in a mouse model of progeria Science 311 2006 1621 1623
20. J.R. Gledhill, M.G. Montgomery, A.G. Leslie, and J.E. Walker Mechanism of inhibition of bovine F1-ATPase by resveratrol and related polyphenols Proc. Natl. Acad. Sci. USA 104 2007 13632 13637
21. A.A. Goodarzi, A.T. Noon, D. Deckbar, Y. Ziv, Y. Shiloh, M. Löbrich, and P.A. Jeggo ATM signaling facilitates repair of DNA double-strand breaks associated with heterochromatin Mol. Cell 31 2008 167 177
22. L.B. Gordon, M.E. Kleinman, D.T. Miller, D.S. Neuberg, A. Giobbie-Hurder, M. Gerhard-Herman, L.B. Smoot, C.M. Gordon, R. Cleveland, and B.D. Snyder Clinical trial of a farnesyltransferase inhibitor in children with Hutchinson-Gilford progeria syndrome Proc. Natl. Acad. Sci. USA 109 2012 16666 16671
23. W. Gu, and R.G. Roeder Activation of p53 sequence-specific DNA binding by acetylation of the p53 C-terminal domain Cell 90 1997 595 606
24. M.C. Haigis, and D.A. Sinclair Mammalian sirtuins: biological insights and disease relevance Annu. Rev. Pathol. 5 2010 253 295
25. M.K. Han, E.K. Song, Y. Guo, X. Ou, C. Mantel, and H.E. Broxmeyer SIRT1 regulates apoptosis and Nanog expression in mouse embryonic stem cells by controlling p53 subcellular localization Cell Stem Cell 2 2008 241 251
26. K.B. Harikumar, and B.B. Aggarwal Resveratrol: a multitargeted agent for age-associated chronic diseases Cell Cycle 7 2008 1020 1035
27. S.A. Hawley, F.A. Ross, C. Chevtzoff, K.A. Green, A. Evans, S. Fogarty, M.C. Towler, L.J. Brown, O.A. Ogunbayo, A.M. Evans, and D.G. Hardie Use of cells expressing gamma subunit variants to identify diverse mechanisms of AMPK activation Cell Metab. 11 2010 554 565
28. M.J. Hendzel, G.P. Delcuve, and J.R. Davie Histone deacetylase is a component of the internal nuclear matrix J. Biol. Chem. 266 1991 21936 21942
29. D. Herranz, M. Muñoz-Martin, M. Cañamero, F. Mulero, B. Martinez-Pastor, O. Fernandez-Capetillo, and M. Serrano Sirt1 improves healthy ageing and protects from metabolic syndrome-associated cancer Nat. Commun. 1 2010 3
30. R.H. Houtkooper, E. Pirinen, and J. Auwerx Sirtuins as regulators of metabolism and healthspan Nat. Rev. Mol. Cell Biol. 13 2012 225 238
31. K.T. Howitz, K.J. Bitterman, H.Y. Cohen, D.W. Lamming, S. Lavu, J.G. Wood, R.E. Zipkin, P. Chung, A. Kisielewski, and L.L. Zhang Small molecule activators of sirtuins extend Saccharomyces cerevisiae lifespan Nature 425 2003 191 196
32. M. Kaeberlein, T. McDonagh, B. Heltweg, J. Hixon, E.A. Westman, S.D. Caldwell, A. Napper, R. Curtis, P.S. DiStefano, and S. Fields Substrate-specific activation of sirtuins by resveratrol J. Biol. Chem. 280 2005 17038 17045
33. E.J. Kim, J.H. Kho, M.R. Kang, and S.J. Um Active regulator of SIRT1 cooperates with SIRT1 and facilitates suppression of p53 activity Mol. Cell 28 2007 277 290
34. J.E. Kim, J. Chen, and Z. Lou DBC1 is a negative regulator of SIRT1 Nature 451 2008 583 586
35. V. Krishnan, M.Z. Chow, Z. Wang, L. Zhang, B. Liu, X. Liu, and Z. Zhou Histone H4 lysine 16 hypoacetylation is associated with defective DNA repair and premature senescence in Zmpste24-deficient mice Proc. Natl. Acad. Sci. USA 108 2011 12325 12330
36. B.A. Kudlow, M.N. Stanfel, C.R. Burtner, E.D. Johnston, and B.K. Kennedy Suppression of proliferative defects associated with processing-defective lamin A mutants by hTERT or inactivation of p53 Mol. Biol. Cell 19 2008 5238 5248
37. S. Lavu, O. Boss, P.J. Elliott, and P.D. Lambert Sirtuins - novel therapeutic targets to treat age-associated diseases Nat. Rev. Drug Discov. 7 2008 841 853
38. F. Lin, and H.J. Worman Structural organization of the human gene encoding nuclear lamin A and nuclear lamin C J. Biol. Chem. 268 1993 16321 16326
39. B. Liu, and Z. Zhou Lamin A/C, laminopathies and premature ageing Histol. Histopathol. 23 2008 747 763
40. B. Liu, J. Wang, K.M. Chan, W.M. Tjia, W. Deng, X. Guan, J.D. Huang, K.M. Li, P.Y. Chau, and D.J. Chen Genomic instability in laminopathy-based premature aging Nat. Med. 11 2005 780 785
41. Y. Liu, Y. Wang, A.E. Rusinol, M.S. Sinensky, J. Liu, S.M. Shell, and Y. Zou Involvement of xeroderma pigmentosum group A (XPA) in progeria arising from defective maturation of prelamin A FASEB J. 22 2008 603 611
42. D.B. Lombard, S.D. Pletcher, C. Cantó, and J. Auwerx Ageing: longevity hits a roadblock Nature 477 2011 410 411
43. K. Manju, B. Muralikrishna, and V.K. Parnaik Expression of disease-causing lamin A mutants impairs the formation of DNA repair foci J. Cell Sci. 119 2006 2704 2714
44. C.R. Mantel, R.H. Wang, C. Deng, and H.E. Broxmeyer Sirt1, notch and stem cell "age asymmetry" Cell Cycle 7 2008 2821 2825
45. M.W. McBurney, X. Yang, K. Jardine, M. Hixon, K. Boekelheide, J.R. Webb, P.M. Lansdorp, and M. Lemieux The mammalian SIR2alpha protein has a role in embryogenesis and gametogenesis Mol. Cell. Biol. 23 2003 38 54
46. D. McClintock, D. Ratner, M. Lokuge, D.M. Owens, L.B. Gordon, F.S. Collins, and K. Djabali The mutant form of lamin A that causes Hutchinson-Gilford progeria is a biomarker of cellular aging in human skin PLoS ONE 2 2007 e1269
47. J. Méndez, and B. Stillman Chromatin association of human origin recognition complex, cdc6, and minichromosome maintenance proteins during the cell cycle: assembly of prereplication complexes in late mitosis Mol. Cell. Biol. 20 2000 8602 8612
48. J.C. Milne, P.D. Lambert, S. Schenk, D.P. Carney, J.J. Smith, D.J. Gagne, L. Jin, O. Boss, R.B. Perni, and C.B. Vu Small molecule activators of SIRT1 as therapeutics for the treatment of type 2 diabetes Nature 450 2007 712 716
49. X. Ou, H.D. Chae, R.H. Wang, W.C. Shelley, S. Cooper, T. Taylor, Y.J. Kim, C.X. Deng, M.C. Yoder, and H.E. Broxmeyer SIRT1 deficiency compromises mouse embryonic stem cell hematopoietic differentiation, and embryonic and adult hematopoiesis in the mouse Blood 117 2011 440 450
50. M. Pacholec, J.E. Bleasdale, B. Chrunyk, D. Cunningham, D. Flynn, R.S. Garofalo, D. Griffith, M. Griffor, P. Loulakis, and B. Pabst SRT1720, SRT2183, SRT1460, and resveratrol are not direct activators of SIRT1 J. Biol. Chem. 285 2010 8340 8351
51. S.J. Park, F. Ahmad, A. Philp, K. Baar, T. Williams, H. Luo, H. Ke, H. Rehmann, R. Taussig, and A.L. Brown Resveratrol ameliorates aging-related metabolic phenotypes by inhibiting cAMP phosphodiesterases Cell 148 2012 421 433
52. A.M. Pendás, Z. Zhou, J. Cadiñanos, J.M. Freije, J. Wang, K. Hultenby, A. Astudillo, A. Wernerson, F. Rodríguez, K. Tryggvason, and C. López-Otín Defective prelamin A processing and muscular and adipocyte alterations in Zmpste24 metalloproteinase-deficient mice Nat. Genet. 31 2002 94 99
53. P.T. Pfluger, D. Herranz, S. Velasco-Miguel, M. Serrano, and M.H. Tschöp Sirt1 protects against high-fat diet-induced metabolic damage Proc. Natl. Acad. Sci. USA 105 2008 9793 9798
54. N.L. Price, A.P. Gomes, A.J. Ling, F.V. Duarte, A. Martin-Montalvo, B.J. North, B. Agarwal, L. Ye, G. Ramadori, and J.S. Teodoro SIRT1 is required for AMPK activation and the beneficial effects of resveratrol on mitochondrial function Cell Metab. 15 2012 675 690
55. L.R. Saunders, A.D. Sharma, J. Tawney, M. Nakagawa, K. Okita, S. Yamanaka, H. Willenbring, and E. Verdin miRNAs regulate SIRT1 expression during mouse embryonic stem cell differentiation and in adult mouse tissues Aging (Albany NY) 2 2010 415 431
56. P. Scaffidi, and T. Misteli Reversal of the cellular phenotype in the premature aging disease Hutchinson-Gilford progeria syndrome Nat. Med. 11 2005 440 445
57. P. Scaffidi, and T. Misteli Lamin A-dependent nuclear defects in human aging Science 312 2006 1059 1063
58. P. Scaffidi, and T. Misteli Lamin A-dependent misregulation of adult stem cells associated with accelerated ageing Nat. Cell Biol. 10 2008 452 459
59. B.C. Smith, W.C. Hallows, and J.M. Denu Mechanisms and molecular probes of sirtuins Chem. Biol. 15 2008 1002 1013
60. K.M. Tsutsui, K. Sano, and K. Tsutsui Dynamic view of the nuclear matrix Acta Med. Okayama 59 2005 113 120
61. D.R. Valenzano, E. Terzibasi, T. Genade, A. Cattaneo, L. Domenici, and A. Cellerino Resveratrol prolongs lifespan and retards the onset of age-related markers in a short-lived vertebrate Curr. Biol. 16 2006 296 300
62. I. Varela, J. Cadiñanos, A.M. Pendás, A. Gutiérrez-Fernández, A.R. Folgueras, L.M. Sánchez, Z. Zhou, F.J. Rodríguez, C.L. Stewart, and J.A. Vega Accelerated ageing in mice deficient in Zmpste24 protease is linked to p53 signalling activation Nature 437 2005 564 568
63. J.M. Villalba, R. de Cabo, and F.J. Alcain A patent review of sirtuin activators: an update Expert Opin. Ther. Pat. 22 2012 355 367
64. M. Viswanathan, and L. Guarente Regulation of Caenorhabditis elegans lifespan by sir-2.1 transgenes Nature 477 2011 E1 E2
65. R.H. Wang, K. Sengupta, C. Li, H.S. Kim, L. Cao, C. Xiao, S. Kim, X. Xu, Y. Zheng, and B. Chilton Impaired DNA damage response, genome instability, and tumorigenesis in SIRT1 mutant mice Cancer Cell 14 2008 312 323
66. 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
67. W. Zhao, J.P. Kruse, Y. Tang, S.Y. Jung, J. Qin, and W. Gu Negative regulation of the deacetylase SIRT1 by DBC1 Nature 451 2008 587 590