Kinetics of DNA methylation inheritance by the Dnmt1-including complexes during the cell cycle
Tóm tắt
The clonal transmission of lineage-specific DNA methylation patterns in a mammalian genome during the cellular division is a crucial biological process controlled by the DNA methyltransferase Dnmt1, mainly. To investigate possible dynamic mechanisms of DNA methylation inheritance during the cell cycle, we used a Proximity Ligation In Situ Assay (P-LISA) to analyze the kinetic of formation and DNA recruitment of Dnmt1-including complexes. P-LISA, sequential chromatin immunoprecipitation and quantitative methylation specific PCR revealed that the Dnmt1/PCNA/UHRF1-including complexes are mainly formed and recruited on DNA during the S-phase of cell cycle, while the formation and the DNA recruitment of several Dnmt1/transcription factors-including complexes are not S-phase dependent but are G0/G1 and/or G2/M phases dependent. Our data confirm that DNA methylation inheritance occurs in S-phase, and demonstrate that DNA methylation inheritance can also occur in G0/G1 and G2/M phases of the cell cycle.
Tài liệu tham khảo
Gaudet F, Hodgson JG, Eden A, Jackson-Grusby L, Dausman J, Gray JW, Leonhardt H, Jaenisch R: Induction of tumors in mice by genomic hypomethylation. Science 2003, 300: 489–492. 10.1126/science.1083558
Li E, Bestor TH, Jaenisch R: Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell 1992, 69: 915–926. 10.1016/0092-8674(92)90611-F
Bird A: DNA methylation patterns and epigenetic memory. Genes Dev 2002, 16: 6–21. 10.1101/gad.947102
Hervouet E, Debien E, Cheray M, Hulin P, Loussouarn D, Martin SA, Vallette FM, Cartron PF: Disruption of Dnmt1/PCNA/UHRF1 interactions promotes tumorigenesis by inducing genome and gene-specific hypomethylations and chromosomal instability. PLoS One 2010, 5: e11333. 10.1371/journal.pone.0011333
Chen T, Hevi S, Gay F, Tsujimoto N, He T, Zhang B, Ueda Y, Li E: Complete inactivation of DNMT1 leads to mitotic catastrophe in human cancer cells. Nat Genet 2007, 39: 391–396. 10.1038/ng1982
Bostick M, Kim J, Estève P, Clark A, Pradhan S, Jacobsen S: UHRF1 plays a role in maintaining DNA methylation in mammalian cells. Science 2007, 27: 2187–2197.
Hervouet E, Lalier L, Debien E, Cheray M, Geairon A, Rogniaux H, FM V, Cartron PF: Tumor induction by disruption of the Dnmt1, PCNA and UHRF1 interactions. Nature Precedings 2008. [http://hdl.handle.net/10101/npre.2008.2509.1.]
Sharif J, Muto M, Takebayashi S, Suetake I, Iwamatsu A, Endo T, Shinga J, Mizutani-Koseki Y, Toyoda T, Okamura K, et al.: The SRA protein Np95 mediates epigenetic inheritance by recruiting Dnmt1 to methylated DNA. Nature 2007, 450: 908–912. 10.1038/nature06397
Bestor TH: The DNA methyltransferases of mammals. Hum Mol Genet 2000, 9: 2395–2402. 10.1093/hmg/9.16.2395
Jeong S, Liang G, Sharma S, Lin J, Choi S, Han H, Yoo C, Egger G, Yang A, Jones P: Selective anchoring of DNA methyltransferases 3A and 3B to nucleosomes containing methylated DNA. Mol Cell Biol 2009, 29: 5366–5376. 10.1128/MCB.00484-09
Hervouet E, Vallette FM, Cartron PF: Dnmt1/transcription factor interactions: an alternative mechanism of DNA methylation inheritance. Genes & Cancer 2010, 1: 434–443.
Jordan M, Toso R, Thrower D, Wilson L: Mechanism of mitotic block and inhibition of cell proliferation by taxol at low concentrations. Proc Natl Acad Sci USA 1993, 90: 9552–9556. 10.1073/pnas.90.20.9552
Pei H, Li C, Adereth Y, Hsu T, Watson D, Li R: Caspase-1 is a direct target gene of ETS1 and plays a role in ETS1-induced apoptosis. Cancer Res 2005, 65: 7205–7213. 10.1158/0008-5472.CAN-04-3566
Yoshida T, Maeda A, Tani N, Sakai T: Promoter structure and transcription initiation sites of the human death receptor 5/TRAIL-R2 gene. FEBS lett 2001, 507: 381–385. 10.1016/S0014-5793(01)02947-7
Chuang LS, Ian HI, Koh TW, Ng HH, Xu G, Li BF: Human DNA-(cytosine-5) methyltransferase-PCNA complex as a target for p21WAF1. Science 1997, 277: 1996–2000. 10.1126/science.277.5334.1996
Hermann A, Goyal R, Jeltsch A: The Dnmt1 DNA-(cytosine-C5)-methyltransferase methylates DNA processively with high preference for hemimethylated target sites. J Biol Chem 2004, 279: 48350–48359. 10.1074/jbc.M403427200
Easwaran H, Schermelleh L, Leonhardt H, Cardoso M: Replication-independent chromatin loading of Dnmt1 during G2 and M phases. EMBO Rep 2004, 5: 1181–1186. 10.1038/sj.embor.7400295
Spada F, Haemmer A, Kuch D, Rothbauer U, Schermelleh L, Kremmer E, Carell T, Längst G, Leonhardt H: DNMT1 but not its interaction with the replication machinery is required for maintenance of DNA methylation in human cells. J Cell Biol 2007, 176: 565–571. 10.1083/jcb.200610062
Schermelleh L, Haemmer A, Spada F, Rösing N, Meilinger D, Rothbauer U, Cardoso M, Leonhardt H: Dynamics of Dnmt1 interaction with the replication machinery and its role in postreplicative maintenance of DNA methylation. Nucleic Acids Res 2007, 35: 4301–4312. 10.1093/nar/gkm432
Métivier R, Gallais R, Tiffoche C, Le Péron C, Jurkowska R, Carmouche R, Ibberson D, Barath P, Demay F, Reid G, et al.: Cyclical DNA methylation of a transcriptionally active promoter. Nature 2008, 452: 45–50. 10.1038/nature06544
Singh A, Swarnalatha M, Kumar V: c-ETS1 facilitates G1/S-phase transition by up-regulating cyclin E and CDK2 genes and cooperates with hepatitis B virus × protein for their deregulation. J Biol Chem 2011, 286: 21961–21970. 10.1074/jbc.M111.238238
Tishler R, Calderwood S, Coleman C, Price B: Increases in sequence specific DNA binding by p53 following treatment with chemotherapeutic and DNA damaging agents. Cancer Res 1993, 53: 2212–2216.
Rizkallah R, Alexander K, Kassardjian A, Lüscher B, Hurt M: The transcription factor YY1 is a substrate for Polo-like kinase 1 at the G2/M transition of the cell cycle. PloS One 2011, 6: e15928. 10.1371/journal.pone.0015928
Hsieh S, Zhuang F, Wu Y, Chen J, Lee Y: Profiling the proteome dynamics during the cell cycle of human hepatoma cells. Proteomics 2008, 8: 2872–2884. 10.1002/pmic.200800196
Hervouet E, Vallette F, Cartron P: Impact of the DNA methyltransferases expression on the methylation status of apoptosis-associated genes in glioblastoma multiforme. Cell Death and Disease 2010., 1: doi:10.1038/cddis.2009.1037
Foltz G, Yoon J, Lee H, Ryken T, Sibenaller Z, Ehrich M, Hood L, Madan A: DNA methyltransferase-mediated transcriptional silencing in malignant glioma: a combined whole-genome microarray and promoter array analysis. Oncogene 2009, 28: 2667–2677. 10.1038/onc.2009.122
Datta J, Ghoshal K, Denny W, Gamage S, Brooke D, Phiasivongsa P, Redkar S, Jacob S: A new class of quinoline-based DNA hypomethylating agents reactivates tumor suppressor genes by blocking DNA methyltransferase 1 activity and inducing its degradation. Cancer Res 2009, 69: 4277–4285. 10.1158/0008-5472.CAN-08-3669
Winquist E, Knox J, Ayoub J, Wood L, Wainman N, Reid G, Pearce L, Shah A, Eisenhauer E: Phase II trial of DNA methyltransferase 1 inhibition with the antisense oligonucleotide MG98 in patients with metastatic renal carcinoma: a National Cancer Institute of Canada Clinical Trials Group investigational new drug study. Invest New Drugs 2006, 24: 159–167. 10.1007/s10637-006-5938-1
Söderberg O, Gullberg M, Jarvius M, Ridderstråle K, Leuchowius K, Jarvius J, Wester K, Hydbring P, Bahram F, Larsson L, Landegren U: Direct observation of individual endogenous protein complexes in situ by proximity ligation. Nat Methods 2006, 12.
Schaefer L, Schuster D, Schaffer J: Structured illumination microscopy: artefact analysis and reduction utilizing a parameter optimization approach. J Microsc 2004, 216: 165–174. 10.1111/j.0022-2720.2004.01411.x
Neil M, Juskaitis R, Wilson T: Method of obtaining optical sectioning by using structured light in a conventional microscope. Opt Lett 1997, 22: 1905–1907. 10.1364/OL.22.001905