Cancer-linked satellite 2 DNA hypomethylation does not regulate Sat2 non-coding RNA expression and is initiated by heat shock pathway activation

Epigenetics

Volumn 7, Issue 8, 2012, Pages 903-913

  Tilman, Gaëlle ^a   Arnoult, Nausica ^a   Lenglez, Sandrine ^a   Van Beneden, Amandine ^a   Loriot, Axelle ^a   De Smet, Charles ^a   Decottignies, Anabelle ^a  

^a DE DUVE INSTITUTE   (Belgium)

Author keywords

DNA hypomethylation; Heat shock response; Non coding RNA; Pericentromeric satellite DNA; Ras oncogene

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; DNA; RNA;

ARTICLE; CANCER CELL CULTURE; CARCINOGENESIS; CHROMOSOME REARRANGEMENT; CONTROLLED STUDY; DEMETHYLATION; DNA METHYLATION; FIBROBLAST; GENE; GENE EXPRESSION; GENE LOCUS; HEAT SHOCK; HUMAN; HUMAN CELL; HUMAN TISSUE; HYPERTHERMIA; IN VITRO STUDY; MELANOMA; NEOPLASM; NUCLEOTIDE SEQUENCE; ONCOGENE; PERICENTROMERIC SATELLITE 2 GENE; SAMPLE; TRANSCRIPTION REGULATION; UPREGULATION;

EID: 84864647917     PISSN: 15592294     EISSN: 15592308     Source Type: Journal    
DOI: 10.4161/epi.21107     Document Type: Article

References (48)

1. Ehrlich M. DNA hypomethylation in cancer cells. Epigenomics 2009; 1:239-259. PMID:20495664; http://dx.doi.org/10.2217/epi.09.33.
2. De Smet C, Loriot A. DNA hypomethylation in cancer: Epigenetic scars of a neoplastic journey. Epigenetics 2010; 5:206-213. PMID:20305381; http://dx.doi.org/10.4161/epi.5.3.11447.
3. Weisenberger DJ, Campan M, Long TI, Kim M, Woods C, Fiala E, et al. Analysis of repetitive element DNA methylation by MethyLight. Nucleic Acids Res 2005; 33:6823-6836. PMID:16326863; http://dx.doi.org/10.1093/nar/gki987.
4. Cadieux B, Ching TT, VandenBerg SR, Costello JF. Genome-wide hypomethylation in human glioblastomas associated with specific copy number alteration, methylenetetrahydrofolate reductase allele status and increased proliferation. Cancer Res 2006; 66:8469-8476; PMID:16951158; http://dx.doi.org/10.1158/0008-5472.CAN-06-1547.
5. Choi SH, Worswick S, Byun HM, Shear T, Soussa JC, Wolff EM, et al. Changes in DNA methylation of tandem DNA repeats are different from interspersed repeats in cancer. Int J Cancer 2009; 125:723-729. PMID:19437537; http://dx.doi.org/10.1002/ijc.24384.
6. Ehrlich M, Hopkins NE, Jiang G, Dome JS, Yu MC, Woods CB, et al. Satellite DNA hypomethylation in karyotyped Wilms tumors. Cancer Genet Cytogenet 2003; 141:97-105; PMID:12606126; http://dx.doi.org/10.1016/S0165-4608(02)00668-4.
7. Sawyer JR, Tian E, Thomas E, Koller M, Stangeby C, Sammartino G, et al. Evidence for a novel mechanism for gene amplification in multiple myeloma: 1q12 pericentromeric heterochromatin mediates breakage-fusion-bridge cycles of a 1q12 approximately 23 amplicon. Br J Haematol 2009; 147:484-494; PMID:19744130; http://dx.doi.org/10.1111/j.1365-2141.2009.07869.x.
8. Eymery A, Callanan M, Vourc'h C. The secret message of heterochromatin: new insights into the mechanisms and function of centromeric and pericentric repeat sequence transcription. Int J Dev Biol 2009; 53:259-268; PMID:19412885; http://dx.doi.org/10.1387/ijdb.082673ae.
9. Probst AV, Okamoto I, Casanova M, ElMarjou F, Le Baccon P, Almouzni G. A strand-specific burst in transcription of pericentric satellites is required for chromocenter formation and early mouse development. Dev Cell 2010; 19:625-638; PMID:20951352; http://dx.doi.org/10.1016/j.devcel.2010.09.002.
10. Jolly C, Metz A, Govin J, Vigneron M, Turner BM, Khochbin S, et al. Stress-induced transcription of satellite III repeats. J Cell Biol 2004; 164:25-33; PMID:14699086; http://dx.doi.org/10.1083/jcb.200306104.
11. Rizzi N, Denegri M, Chiodi I, Corioni M, Valgardsdottir R, Cobianchi F, et al. Transcriptional activation of a constitutive heterochromatic domain of the human genome in response to heat shock. Mol Biol Cell 2004; 15:543-551; PMID:14617804; http://dx.doi.org/10.1091/mbc.E03-07-0487.
12. Valgardsdottir R, Chiodi I, Giordano M, Rossi A, Bazzini S, Ghigna C, et al. Transcription of Satellite III non-coding RNAs is a general stress response in human cells. Nucleic Acids Res 2008; 36:423-434; PMID:18039709; http://dx.doi.org/10.1093/nar/gkm1056.
13. Eymery A, Souchier C, Vourc'h C, Jolly C. Heat shock factor 1 binds to and transcribes satellite II and III sequences at several pericentromeric regions in heat-shocked cells. Exp Cell Res 2010; 316:1845-855; PMID:20152833; http://dx.doi.org/10.1016/j.yexcr.2010.02.002.
14. Vourc'h C, Biamonti G. Transcription of satellite DNAs in mammals. Prog Mol Subcell Biol 2011; 51:95-118; PMID:21287135; http://dx.doi.org/10.1007/978-3-642-16502-3_5.
15. Ting DT, Lipson D, Paul S, Brannigan BW, Akhavanfard S, Coffman EJ, et al. Aberrant overexpression of satellite repeats in pancreatic and other epithelial cancers. Science 2011; 331:593-596; PMID:21233348; http://dx.doi.org/10.1126/science.1200801.
16. Eymery A, Horard B, ElAtifi-Borel M, Fourel G, Berger F, Vitte AL, et al. A transcriptomic analysis of human centromeric and pericentric sequences in normal and tumor cells. Nucleic Acids Res 2009; 37:6340-6354; PMID:19720732; http://dx.doi.org/10.1093/nar/gkp639.
17. Alexiadis V, Ballestas ME, Sanchez C, Winokur S, Vedanarayanan V, Warren M, et al. RNAPol-ChIP analysis of transcription from FSHD-linked tandem repeats and satellite DNA. Biochim Biophys Acta 2007; 1769:29-40; PMID:17239456.
18. de Koning AP, Gu W, Castoe TA, Batzer MA, Pollock DD. Repetitive elements may comprise over two-thirds of the human genome. PLoS Genet 2011; 7:1002384; PMID:22144907; http://dx.doi.org/10.1371/journal.pgen.1002384.
19. Lafferty-Whyte K, Cairney CJ, Will MB, Serakinci N, Daidone MG, Zaffaroni N, et al. A gene expression signature classifying telomerase and ALT immortalization reveals an hTERT regulatory network and suggests a mesenchymal stem cell origin for ALT. Oncogene 2009; 28:3765-3774; PMID:19684619; http://dx.doi.org/10.1038/onc.2009.238.
20. Hassan KM, Norwood T, Gimelli G, Gartler SM, Hansen RS. Satellite 2 methylation patterns in normal and ICF syndrome cells and association of hypomethylation with advanced replication. Hum Genet 2001; 109:452-462; PMID:11702227; http://dx.doi.org/10.1007/s004390100590.
21. Abravaya K, Phillips B, Morimoto RI. Heat shockinduced interactions of heat shock transcription factor and the human hsp70 promoter examined by in vivo footprinting. Mol Cell Biol 1991; 11:586-592; PMID:1986252.
22. Weber J, Salgaller M, Samid D, Johnson B, Herlyn M, Lassam N, et al. Expression of the MAGE-1 tumor antigen is upregulated by the demethylating agent 5-aza-2'-deoxycytidine. Cancer Res 1994; 54:1766-1771; PMID:7511051.
23. Nergadze SG, Farnung BO, Wischnewski H, Khoriauli L, Vitelli V, Chawla R, et al. CpG-island promoters drive transcription of human telomeres. RNA 2009; 15:2186-2194; PMID:19850908; http://dx.doi.org/10.1261/rna.1748309.
24. Zeng W, de Greef JC, Chen YY, Chien R, Kong X, Gregson HC, et al. Specific loss of histone H3 lysine 9 trimethylation and HP1γ/cohesin binding at D4Z4 repeats is associated with facioscapulohumeral dystrophy (FSHD). PLoS Genet 2009; 5:1000559; PMID:19593370; http://dx.doi.org/10.1371/journal.pgen.1000559.
25. Calderwood SK, Khaleque MA, Sawyer DB, Ciocca DR. Heat shock proteins in cancer: chaperones of tumorigenesis. Trends Biochem Sci 2006; 31:164-172; PMID:16483782; http://dx.doi.org/10.1016/j.tibs.2006.01.006.
26. Dai C, Whitesell L, Rogers AB, Lindquist S. Heat shock factor 1 is a powerful multifaceted modifier of carcinogenesis. Cell 2007; 130:1005-1018; PMID:17889646; http://dx.doi.org/10.1016/j.cell.2007.07.020.
27. Min JN, Huang L, Zimonjic DB, Moskophidis D, Mivechi NF. Selective suppression of lymphomas by functional loss of Hsf1 in a p53-deficient mouse model for spontaneous tumors. Oncogene 2007; 26:5086-5097; PMID:17310987; http://dx.doi.org/10.1038/sj.onc.1210317.
28. Meng L, Gabai VL, Sherman MY. Heat-shock transcription factor HSF1 has a critical role in human epidermal growth factor receptor-2-induced cellular transformation and tumorigenesis. Oncogene 2010; 29:5204-5213; PMID:20622894; http://dx.doi.org/10.1038/onc.2010.277.
29. Meng L, Hunt C, Yaglom JA, Gabai VL, Sherman MY. Heat shock protein Hsp72 plays an essential role in Her2-induced mammary tumorigenesis. Oncogene 2011; 30:2836-2845; PMID:21297664; http://dx.doi.org/10.1038/onc.2011.5.
30. De Smet C, De Backer O, Faraoni I, Lurquin C, Brasseur F, Boon T. The activation of human gene MAGE-1 in tumor cells is correlated with genomewide demethylation. Proc Natl Acad Sci USA 1996; 93:7149-7153; PMID:8692960; http://dx.doi.org/10.1073/pnas.93.14.7149.
31. Tilman G, Loriot A, Van Beneden A, Arnoult N, Londoño-Vallejo JA, De Smet C, et al. Subtelomeric DNA hypomethylation is not required for telomeric sister chromatid exchanges in ALT cells. Oncogene 2009; 28:1682-1693; PMID:19252523; http://dx.doi.org/10.1038/onc.2009.23.
32. Gabai VL, Yaglom JA, Waldman T, Sherman MY. Heat shock protein Hsp72 controls oncogene-induced senescence pathways in cancer cells. Mol Cell Biol 2009; 29:559-569; PMID:19001088; http://dx.doi.org/10.1128/MCB.01041-08.
33. Corey LL, Weirich CS, Benjamin IJ, Kingston RE. Localized recruitment of a chromatin-remodeling activity by an activator in vivo drives transcriptional elongation. Genes Dev 2003; 17:1392-1401; PMID:12782657; http://dx.doi.org/10.1101/gad.1071803.
34. Inouye S, Fujimoto M, Nakamura T, Takaki E, Hayashida N, Hai T, et al. Heat shock transcription factor 1 opens chromatin structure of interleukin-6 promoter to facilitate binding of an activator or a repressor. J Biol Chem 2007; 282:33210-33217; PMID:17766920; http://dx.doi.org/10.1074/jbc.M704471200.
35. Stanhill A, Levin V, Hendel A, Shachar I, Kazanov D, Arber N, et al. Ha-ras(val12) induces HSP70b transcription via the HSE/HSF1 system, but HSP70b expression is suppressed in Ha-ras(val12)-transformed cells. Oncogene 2006; 25:1485-1495; PMID:16278678; http://dx.doi.org/10.1038/sj.onc.1209193.
36. Macara IG, Lounsbury KM, Richards SA, McKiernan C, Bar-Sagi D. The Ras superfamily of GTPases. FASEB J 1996; 10:625-630; PMID:8621061.
37. Palii SS, Van Emburgh BO, Sankpal UT, Brown KD, Robertson KD. DNA methylation inhibitor 5-Aza-2'- deoxycytidine induces reversible genome-wide DNA damage that is distinctly influenced by DNA methyltransferases 1 and 3B. Mol Cell Biol 2008; 28:752-771; PMID:17991895; http://dx.doi.org/10.1128/MCB.01799-07.
38. Lindroth AM, Park YJ, McLean CM, Dokshin GA, Persson JM, Herman H, et al. Antagonism between DNA and H3K27 methylation at the imprinted Rasgrf1 locus. PLoS Genet 2008; 4:1000145; PMID:18670629; http://dx.doi.org/10.1371/journal.pgen.1000145.
39. Maison C, Bailly D, Roche D, Montes de Oca R, Probst AV, Vassias I, et al. SUMOylation promotes de novo targeting of HP1α to pericentric heterochromatin. Nat Genet 2011; 43:220-227; http://dx.doi.org/10.1038/ng.765.
40. Uemura M, Zheng Q, Koh CM, Nelson WG, Yegnasubramanian S, De Marzo AM. Overexpression of ribosomal RNA in prostate cancer is common but not linked to rDNA promoter hypomethylation. Oncogene 2012; 31:1254-1263; PMID:21822302; http://dx.doi.org/10.1038/onc.2011.319.
41. Hsieh CL. Dynamics of DNA methylation pattern. Curr Opin Genet Dev 2000; 10:224-228; PMID:10753782; http://dx.doi.org/10.1016/S0959-437X(00)00064-2.
42. Stadler MB, Murr R, Burger L, Ivanek R, Lienert F, Schöler A, et al. DNA-binding factors shape the mouse methylome at distal regulatory regions. Nature 2011; 480:490-495; PMID:22170606.
43. Yegnasubramanian S, Haffner MC, Zhang Y, Gurel B, Cornish TC, Wu Z, et al. DNA hypomethylation arises later in prostate cancer progression than CpG island hypermethylation and contributes to metastatic tumor heterogeneity. Cancer Res 2008; 68:8954-8967; PMID:18974140; http://dx.doi.org/10.1158/0008-5472.CAN-07-6088.
44. Mattiussi M, Tilman G, Lenglez S, Decottignies A. Human telomerase represses ROS-dependent cellular responses to Tumor Necrosis Factorα without affecting NFκB activation. Cell Signal 2012; 24:708-717; PMID:22108091; http://dx.doi.org/10.1016/j.cellsig.2011.11.004.
45. Bracken AP, Pasini D, Capra M, Prosperini E, Colli E, Helin K. EZH2 is downstream of the pRB-E2F pathway, essential for proliferation and amplified in cancer. EMBO J 2003; 22:5323-5335; PMID:14532106; http://dx.doi.org/10.1093/emboj/cdg542.
46. De Smet C, Loriot A, Boon T. Promoter-dependent mechanism leading to selective hypomethylation within the 5' region of gene MAGE-A1 in tumor cells. Mol Cell Biol 2004; 24:4781-4790; PMID:15143172; http://dx.doi.org/10.1128/MCB.24.11.4781-90.2004.
47. Loriot A, De Plaen E, Boon T, De Smet C. Transient downregulation of DNMT1 methyltransferase leads to activation and stable hypomethylation of MAGE-A1 in melanoma cells. J Biol Chem 2006; 281:10118-10126; PMID:16497664; http://dx.doi.org/10.1074/jbc.M510469200.
48. Ding XZ, Smallridge RC, Galloway RJ, Kiang JG. Rapid assay of HSF1 and HSF2 gene expression by RT-PCR. Mol Cell Biochem 1996; 158:189-192; PMID:8817481; http://dx.doi.org/10.1007/BF00225845.