Inhibition of SIRT1 reactivates silenced cancer genes without loss of promoter DNA hypermethylation

PLoS Genetics

Volumn 2, Issue 3, 2006, Pages 0344-0352

  Pruitt, Kevin ^a   Zinn, Rebekah L ^a,b   Ohm, Joyce E ^a   McGarvey, Kelly M ^a,b   Kang, Sung Hae L ^a   Watkins, D Neil ^a   Herman, James G ^a   Baylin, Stephen B ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

DNA; HISTONE DEACETYLASE 3; LYSINE; PROTEIN; SIRT1 PROTEIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; ANTINEOPLASTIC ANTIMETABOLITE; SIRT1 PROTEIN, HUMAN; SIRTUIN;

ACETYLATION; AGING; ARTICLE; BREAST CANCER; CANCER CELL; CANCER CELL CULTURE; CANCER GENETICS; CANCER INHIBITION; COLON CANCER; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; ENZYME INHIBITION; EPIGENETICS; GENE ACTIVATION; GENE EXPRESSION; GENE SILENCING; GENE TARGETING; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; PHENOTYPE; PROTEIN LOCALIZATION; TUMOR SUPPRESSOR GENE; BREAST TUMOR; CELL CULTURE; CELL STRAIN HCT116; COLON TUMOR; DRUG ANTAGONISM; DRUG EFFECT; FEMALE; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; METABOLISM; MOLECULAR GENETICS; PROMOTER REGION;

MAMMALIA;

ANTIMETABOLITES, ANTINEOPLASTIC; BREAST NEOPLASMS; COLONIC NEOPLASMS; CPG ISLANDS; DNA METHYLATION; EPIGENESIS, GENETIC; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE SILENCING; GENES, TUMOR SUPPRESSOR; HCT116 CELLS; HUMANS; MOLECULAR SEQUENCE DATA; PROMOTER REGIONS (GENETICS); SIRTUINS; TUMOR CELLS, CULTURED;

EID: 33645768490     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.0020040     Document Type: Article

References (56)

1. Herman JG, Baylin SB (2003) Gene silencing in cancer in association with promoter hypermethylation. N Engl J Med 349: 2042-2054.
2. Jones PA, Baylin SB (2002) The fundamental role of epigenetic events in cancer. Nat Rev Genet 3: 415-428.
3. Jones PA, Laird PW (1999) Cancer epigenetics comes of age. Nat Genet 21: 163-167.
4. Fahrner JA, Eguchi S, Herman JG, Baylin SB (2002) Dependence of histone modifications and gene expression on DNA hypermethylation in cancer. Cancer Res 62: 7213-7218.
5. Cameron EE, Bachman KE, Myohanen S, Herman JG, Baylin SB (1999) Synergy of demethylation and histone deacetylase inhibition in the reexpression of genes silenced in cancer. Nat Genet 21: 103-107.
6. Suzuki H, Gabrielson E, Chen W, Anbazhagan R, van Engeland M, et al. (2002) A genomic screen for genes upregulated by demethylation and histone deacetylase inhibition in human colorectal cancer. Nat Genet 31: 141-149.
7. Blander G, Guarente L (2004) The Sir2 family of protein deacetylases. Annu Rev Biochem 73: 417-435.
8. Picard F, Kurtev M, Chung N, Topark-Ngarm A, Senawong T, et al. (2004) Sirt1 promotes fat mobilization in white adipocytes by repressing PPAR-gamma. Nature 429: 771-776.
9. Senawong T, Peterson VJ, Leid M (2005) BCL11A-dependent recruitment of SIRT1 to a promoter template in mammalian cells results in histone deacetylation and transcriptional repression. Arch Biochem Biophys 434: 316-325.
10. Senawong T, Peterson VJ, Avram D, Shepherd DM, Frye RA, et al. (2003) 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: 43041-43050.
11. Vaquero A, Scher M, Lee D, Erdjument-Bromage H, Tempst P, et al. (2004) Human SirT1 interacts with histone H1 and promotes formation of facultative heterochromatin. Mol Cell 16: 93-105.
12. Bitterman KJ, Anderson RM, Cohen HY, Latorre-Esteves M, Sinclair DA (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.
13. Bedalov A, Gatbonton T, Irvine WP, Gottschling DE, Simon JA (2001) Identification of a small molecule inhibitor of Sir2p. Proc Natl Acad Sci U S A 98: 15113-15118.
14. Avalos JL, Bever KM, Wolberger C (2005) Mechanism of sirtuin inhibition by nicotinamide: Altering the NAD(+) cosubstrate specificity of a Sir2 enzyme. Mol Cell 17: 855-868.
15. Kelly WK, O'Connor OA, Krug LM, Chiao JH, Heaney M, et al. (2005) Phase I study of an oral histone deacetylase inhibitor, suberoylanilide hydroxamic acid, in patients with advanced cancer. J Clin Oncol 23: 3923-3931.
16. Drummond DC, Noble CO, Kirpotin DB, Guo Z, Scott GK, et al. (2005) Clinical development of histone deacetylase inhibitors as anticancer agents. Annu Rev Pharmacol Toxicol 45: 495-528.
17. Olaharski AJ, Rine J, Marshall BL, Babiarz J, Zhang L, et al. (2005) The favoring agent dihydrocoumarin reverses epigenetic silencing and inhibits sirtuin deacetylases. PLoS Genet 1: e77. DOI: 10.1371/journal.pgen.0010077
18. Guarente L (2000) Sir2 links chromatin silencing, metabolism, and aging. Genes Dev 14: 1021-1026.
19. Guarente L, Kenyon C (2000) Genetic pathways that regulate ageing in model organisms. Nature 408: 255-262.
20. Nemoto S, Fergusson MM, Finkel T (2004) Nutrient availability regulates SIRT1 through a forkhead-dependent pathway. Science 306: 2105-2108.
21. Vaziri H, Dessain SK, Ng Eaton E, Imai SI, Frye RA, et al. (2001) hSIR2(SIRT1) functions as an NAD-dependent p53 deacetylase. Cell 107: 149-159.
22. Luo J, Nikolaev AY, Imai S, Chen D, Su F, et al. (2001) Negative control of p53 by Sir2alpha promotes cell survival under stress. Cell 107: 137-148.
23. Langley E, Pearson M, Faretta M, Bauer UM, Frye RA, et al. (2002) Human SIR2 deacetylates p53 and antagonizes PML/p53-induced cellular senescence. EMBO J 21: 2383-2396.
24. Brunet A, Sweeney LB, Sturgill JF, Chua KF, Greer PL, et al. (2004) Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase. Science 303: 2011-2015.
25. Giannakou ME, Partridge L (2004) The interaction between FOXO and SIRT1: tipping the balance towards survival. Trends Cell Biol 14: 408-412.
26. Gottschling DE (2000) Gene silencing: Two faces of SIR2. Curr Biol 10: R708-R711.
27. Furuyama T, Banerjee R, Breen TR, Harte PJ (2004) SIR2 is required for polycomb silencing and is associated with an E(Z) histone methyltransferase complex. Curr Biol 14: 1812-1821.
28. Suzuki H, Watkins DN, Jair KW, Schuebel KE, Markowitz SD, et al. (2004) Epigenetic inactivation of SFRP genes allows constitutive WNT signaling in colorectal cancer. Nat Genet 36: 417-422.
29. Corn PG, Heath EI, Heitmiller R, Fogt F, Forastiere AA, ey al. (2001) Frequent hypermethylation of the 5′ CpG island of E-cadherin in esophageal adenocarcinoma. Clin Cancer Res 7: 2765-2769.
30. Strathdee G (2002) Epigenetic versus genetic alterations in the inactivation of E-cadherin. Semin Cancer Biol 12: 373-379.
31. Corn PG, Smith BD, Ruckdeschel ES, Douglas D, Baylin SB, et al. (2000) Ecadherin expression is silenced by 5′ CpG island methylation in acute leukemia. Clin Cancer Res 6: 4243-4248.
32. Herman JG, Umar A, Polyak K, Graff JR, Ahuja N, et al. (1998) Incidence and functional consequences of hMLH1 promoter hypermethylation in colorectal carcinoma. Proc Natl Acad Sci U S A 95: 6870-6875.
33. Kane MF, Loda M, Gaida GM, Lipman J, Mishra R, et al. (1997) Methylation of the hMLH1 promoter correlates with lack of expression of hMLH1 in sporadic colon tumors and mismatch repair-defective human tumor cell lines. Cancer Res 57: 808-811.
34. Akiyama Y, Watkins N, Suzuki H, Jair KW, van Engeland M, et al. (2003) GATA-4 and GATA-5 transcription factor genes and potential downstream antitumor target genes are epigenetically silenced in colorectal and gastric cancer. Mol Cell Biol 23: 8429-8439.
35. Graff JR, Gabrielson E, Fujii H, Baylin SB, Herman JG (2000) Methylation patterns of the E-cadherin 59 CpG island are unstable and reflect the dynamic, heterogeneous loss of E-cadherin expression during metastatic progression. J Biol Chem 275: 2727-2732.
36. Anderson RM, Bitterman KJ, Wood JG, Medvedik O, Sinclair DA (2003) Nicotinamide and PNC1 govern lifespan extension by calorie restriction in Saccharomyces cerevisiae. Nature 423: 181-185.
37. Posakony J, Hirao M, Stevens S, Simon JA, Bedalov A (2004) Inhibitors of Sir2: Evaluation of splitomicin analogues. J Med Chem 47: 2635-2644.
38. Herman JG, Graff JR, Myohanen S, Nelkin BD, Baylin SB (1996) Methylation-specific PCR: A novel PCR assay for methylation status of CpG islands. Proc Natl Acad Sci U S A 93: 9821-9826.
39. Imai S, Armstrong CM, Kaeberlein M, Guarente L (2000) Transcriptional silencing and longevity protein Sir2 is an NAD-dependent histone deacetylase. Nature 403: 795-800.
40. Suka N, Luo K, Grunstein M (2002) Sir2p and Sas2p opposingly regulate acetylation of yeast histone H4 lysine16 and spreading of heterochromatin. Nat Genet 32: 378-383.
41. Kimura A, Umehara T, Horikoshi M (2002) Chromosomal gradient of histone acetylation established by Sas2p and Sir2p functions as a shield against gene silencing. Nat Genet 32: 370-377.
42. Shankaranarayana GD, Motamedi MR, Moazed D, Grewal SI (2003) Sir2 regulates histone H3 lysine 9 methylation and heterochromatin assembly in fission yeast. Curr Biol 13: 1240-1246.
43. -/- colon carcinoma. Science 275: 1784-1787.
44. Morin PJ, Sparks AB, Korinek V, Barker N, Clevers H, et al. (1997) Activation of beta-catenin-Tcf signaling in colon cancer by mutations in beta-catenin or APC. Science 275: 1787-1790.
45. Tetsu O, McCormick F (1999) Beta-catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature 398: 422-426.
46. Pruitt K, Pestell RG, Der CJ (2000) Ras inactivation of the retinoblastoma pathway by distinct mechanisms in NIH 3T3 fibroblast and RIE-1 epithelial cells. J Biol Chem 275: 40916-40924.
47. Motta MC, Divecha N, Lemieux M, Kamel C, Chen D, et al. (2004) Mammalian SIRT1 represses forkhead transcription factors. Cell 116: 551-563.
48. Huguet EL, McMahon JA, McMahon AP, Bicknell R, Harris AL (1994) Differential expression of human Wnt genes 2, 3, 4, and 7B in human breast cell lines and normal and disease states of human breast tissue. Cancer Res 54: 2615-2621.
49. Yeung F, Hoberg JE, Ramsey CS, Keller MD, Jones DR, et al. (2004) Modulation of NF-kappaB-dependent transcription and cell survival by the SIRT1 deacetylase. EMBO J 23: 2369-2380.
50. Kuzmichev A, Margueron R, Vaquero A, Preissner TS, Scher M, et al. (2005) Composition and histone substrates of polycomb repressive group complexes change during cellular differentiation. Proc Natl Acad Sci U S A 102: 1859-1864.
51. Chen WY, Wang DH, Yen RC, Luo J, Gu W, et al. (2005) Tumor suppressor HIC1 directly regulates SIRT1 to modulate p53-dependent DNA-damage responses. Cell 123: 437-448.
52. Wood JG, Rogina B, Lavu S, Howitz K, Helfand SL, et al. (2004) Sirtuin activators mimic caloric restriction and delay ageing in metazoans. Nature 430: 686-689.
53. Ford J, Jiang M, Milner J (2005) Cancer-specific functions of SIRT1 enable human epithelial cancer cell growth and survival. Cancer Res 65: 10457-10463.
54. Toyota M, Issa JP (1999) CpG island methylator phenotypes in aging and cancer. Semin Cancer Biol 9: 349-357.
55. Fraga MF, Ballestar E, Villar-Garea A, Boix-Chornet M, Espada J, et al. (2005) Loss of acetylation at Lys16 and trimethylation at Lys20 of histone H4 is a common hallmark of human cancer. Nat Genet 37: 391-400.
56. Esteller M, Guo M, Moreno V, Peinado MA, Capella G, et al. (2002) Hypermethylation-associated inactivation of the cellular retinol-binding-protein 1 gene in human cancer. Cancer Res 62: 5902-5905.