Depletion of sirtuin 1 (SIRT1) leads to epigenetic modifications of telomerase (TERT) gene in hepatocellular carcinoma cells

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Zhang, Bin ^a   Chen, Juan ^b   Cheng, Alfred S L ^a   Ko, Ben C B ^c,d  

^a CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^b CHONGQING MEDICAL UNIVERSITY   (China)

^c The Hong Kong Polytechnic University Shenzhen Research Institute   (Hong Kong)

^d HONG KONG POLYTECHNIC UNIVERSITY   (Hong Kong)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE H3; MESSENGER RNA; SIRTUIN 1; TELOMERASE;

3' UNTRANSLATED REGION; ARTICLE; CANCER CELL CULTURE; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; ENZYME REGULATION; EPIGENETICS; GENE ACTIVATION; GENE EXPRESSION REGULATION; HISTONE ACETYLATION; HISTONE METHYLATION; HUMAN; HUMAN CELL; LIVER CELL CARCINOMA; MOLECULAR INTERACTION; PROMOTER REGION; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN PROCESSING; RNA STABILITY; TELOMERASE GENE; TRANSCRIPTION REGULATION;

CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE SILENCING; HISTONES; HUMANS; LIVER NEOPLASMS; RNA, SMALL INTERFERING; SIRTUIN 1; TELOMERASE;

EID: 84897058294     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0084931     Document Type: Article

References (37)

1. 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. doi:10.1038/35001622. (Pubitemid 30111843)
2. Haigis MC, Sinclair DA (2010) Mammalian sirtuins: biological insights and disease relevance. Annu Rev Pathol 5: 253-295. doi:10.1146/annurev.-pathol.4. 110807.092250.
3. Michan S, Sinclair D (2007) Sirtuins in mammals: insights into their biological function. Biochem J 404: 1-13. doi:10.1042/BJ20070140. (Pubitemid 46788079)
4. Palacios JA, Herranz D, De Bonis ML, Velasco S, Serrano M, et al. (2010) SIRT1 contributes to telomere maintenance and augments global homologous recombination. J Cell Biol 191: 1299-1313. doi:10.1083/jcb.201005160.
5. Ramy El R, Magroun N, Messadecq N, Gauthier LR, Boussin FD, et al. (2009) Functional interplay between Parp-1 and SirT1 in genome integrity and chromatin-based processes. Cell Mol Life Sci 66: 3219-3234. doi:10.1007/s00018- 009-0105-4.
6. Yuan J, Pu M, Zhang Z, Lou Z (2009) Histone H3-K56 acetylation is important for genomic stability in mammals. Cell cycle (Georgetown, Tex) 8: 1747-1753.
7. Haigis MC, Guarente LP (2006) Mammalian sirtuins-emerging roles in physiology, aging, and calorie restriction. Genes Dev 20: 2913-2921. doi:10.1101/gad.1467506. (Pubitemid 44771725)
8. Fang Y, Nicholl MB (2011) Sirtuin 1 in malignant transformation: Friend or foe? Cancer Lett 306: 10-14. doi:10.1016/j.canlet.2011.02.019.
9. Chen J, Zhang B, Wong N, Lo AWI, To K-F, et al. (2011) Sirtuin 1 is upregulated in a subset of hepatocellular carcinomas where it is essential for telomere maintenance and tumor cell growth. Cancer Res 71: 4138-4149. doi:10.1158/0008-5472.CAN-10-4274.
10. Chen H-C, Jeng Y-M, Yuan R-H, Hsu H-C, Chen Y-L (2012) SIRT1 promotes tumorigenesis and resistance to chemotherapy in hepatocellular carcinoma and its expression predicts poor prognosis. Ann Surg Oncol 19: 2011-2019. doi:10.1245/s10434-011-2159-4.
11. Choi HN, Bae JS, Jamiyandorj U, Noh SJ, Park HS, et al. (2011) Expression and role of SIRT1 in hepatocellular carcinoma. Oncol Rep 26: 503-510. doi:10.3892/or.2011.1301.
12. Huffman DM, Grizzle WE, Bamman MM, Kim J-S, Eltoum IA, et al. (2007) SIRT1 is significantly elevated in mouse and human prostate cancer. Cancer Res 67: 6612-6618. doi:10.1158/0008-5472.CAN-07-0085. (Pubitemid 47105506)
13. Byles V, Zhu L, Lovaas JD, Chmilewski LK, Wang J, et al. (2012) SIRT1 induces EMT by cooperating with EMT transcription factors and enhances prostate cancer cell migration and metastasis. Oncogene 31: 4619-4629. doi:10.1038/onc.2011.612.
14. Zinn RL, Pruitt K, Eguchi S, Baylin SB, Herman JG (2007) hTERT is expressed in cancer cell lines despite promoter DNA methylation by preservation of unmethylated DNA and active chromatin around the transcription start site. Cancer Res 67: 194-201. doi:10.1158/0008-5472.CAN-06-3396. (Pubitemid 46142775)
15. Kumaki Y, Oda M, Okano M (2008) QUMA: quantification tool for methylation analysis. Nucleic Acids Research 36: W170-W175. doi:10.1093/nar/gkn294.
16. Tong EHY, Guo J-J, Xu S-X, Mak K, Chung SK, et al. (2009) Inducible nucleosome depletion at OREBP-binding-sites by hypertonic stress. PLoS ONE 4: e8435. doi:10.1371/journal.pone.0008435.
17. Emerald BS, Chen Y, Zhu T, Zhu Z, Lee K-O, et al. (2007) AlphaCP1 mediates stabilization of hTERT mRNA by autocrine human growth hormone. J Biol Chem 282: 680-690. doi:10.1074/jbc.M600224200. (Pubitemid 47076669)
18. Moreira AL, Sampaio EP, Zmuidzinas A, Frindt P, Smith KA, et al. (1993) Thalidomide exerts its inhibitory action on tumor necrosis factor alpha by enhancing mRNA degradation. J Exp Med 177: 1675-1680. (Pubitemid 23146134)
19. Amat R, Planavila A, Chen SL, Iglesias R, Giralt M, et al. (2009) SIRT1 controls the transcription of the peroxisome proliferator-activated receptorgamma Co-activator-1alpha (PGC-1alpha) gene in skeletal muscle through the PGC-1alpha autoregulatory loop and interaction with MyoD. J Biol Chem 284: 21872-21880. doi:10.1074/jbc.M109.022749.
20. Li X, Zhang S, Blander G, Tse JG, Krieger M, et al. (2007) SIRT1 deacetylates and positively regulates the nuclear receptor LXR. Mol Cell 28: 91-106. doi:10.1016/j.molcel.2007.07.032. (Pubitemid 47531974)
21. Fulco M, Schiltz RL, Iezzi S, King MT, Zhao P, et al. (2003) Sir2 regulates skeletal muscle differentiation as a potential sensor of the redox state. Mol Cell 12: 51-62. (Pubitemid 36945036)
22. Renaud S, Loukinov D, Bosman FT, Lobanenkov V, Benhattar J (2005) CTCF binds the proximal exonic region of hTERT and inhibits its transcription. Nucleic Acids Research 33: 6850-6860. doi:10.1093/nar/gki989. (Pubitemid 41830489)
23. Horikawa I, Cable PL, Afshari C, Barrett JC (1999) Cloning and characterization of the promoter region of human telomerase reverse transcriptase gene. Cancer Res 59: 826-830. (Pubitemid 29086735)
24. Zhu Q, Liu C, Ge Z, Fang X, Zhang X, et al. (2008) Lysine-specific demethylase 1 (LSD1) Is required for the transcriptional repression of the telomerase reverse transcriptase (hTERT) gene. PLoS ONE 3: e1446. doi:10.1371/journal.-pone.0001446.
25. Portmann S, Fahrner R, Lechleiter A, Keogh A, Overney S, et al. (2013) Antitumor effect of SIRT1 inhibition in human HCC tumor models in vitro and in vivo. Mol Cancer Ther. doi:10.1158/1535-7163.MCT-12-0700.
26. de Lange T (2005) Shelterin: the protein complex that shapes and safeguards human telomeres. Genes Dev 19: 2100-2110. doi:10.1101/gad.1346005.
27. Osterhage JL, Friedman KL (2009) Chromosome end maintenance by telomerase. J Biol Chem 284: 16061-16065. doi:10.1074/jbc.R900011200.
28. Dvir-Ginzberg M, Gagarina V, Lee E-J, Hall DJ (2008) Regulation of cartilage-specific gene expression in human chondrocytes by SirT1 and nicotinamide phosphoribosyltransferase. J Biol Chem 283: 36300-36310. doi:10.1074/jbc.M803196200.
29. Pruitt K, Zinn RL, Ohm JE, Mcgarvey KM, Kang S-HL, et al. (2006) Inhibition of SIRT1 reactivates silenced cancer genes without loss of promoter DNA hypermethylation. PLoS Genet 2: e40. doi:10.1371/journal.pgen.0020040.
30. Zhang T, Kraus WL (2010) SIRT1-dependent regulation of chromatin and transcription: linking NAD(+) metabolism and signaling to the control of cellular functions. Biochim Biophys Acta 1804: 1666-1675. doi:10.1016/j.bbapap. 2009.10.022.
31. O'hagan HM, Mohammad HP, Baylin SB (2008) Double strand breaks can initiate gene silencing and SIRT1-dependent onset of DNA methylation in an exogenous promoter CpG island. PLoS Genet 4: e1000155. doi:10.1371/journal.pgen. 1000155.
32. O'hagan HM, Wang W, Sen S, Shields CD, Lee SS, et al. (2011) Oxidative Damage Targets Complexes Containing DNA Methyltransferases, SIRT1, and Polycomb Members to Promoter CpG Islands. Cancer Cell 20: 606-619. doi:10.1016/j.ccr. 2011.09.012.
33. 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. doi:10.1016/j.molcel.2004.08.031. (Pubitemid 39330155)
34. Vaquero A, Scher M, Erdjument-Bromage H, Tempst P, Serrano L, et al. (2007) SIRT1 regulates the histone methyl-transferase SUV39H1 during heterochromatin formation. Nature 450: 440-444. doi:10.1038/nature06268. (Pubitemid 350126745)
35. Lopatina NG, Poole JC, Saldanha SN, Hansen NJ, Key JS, et al. (2003) Control mechanisms in the regulation of telomerase reverse transcriptase expression in differentiating human teratocarcinoma cells. Biochem Biophys Res Commun 306: 650-659. (Pubitemid 37323812)
36. Renaud S, Loukinov D, Abdullaev Z, Guilleret I, Bosman FT, et al. (2007) Dual role of DNA methylation inside and outside of CTCF-binding regions in the transcriptional regulation of the telomerase hTERT gene. Nucleic Acids Research 35: 1245-1256. doi:10.1093/nar/gkl1125. (Pubitemid 46522976)
37. Kouzarides T (2007) Chromatin modifications and their function. Cell 128: 693-705. doi:10.1016/j.cell.2007.02.005.