DNA Topoisomerase 1α Promotes Transcriptional Silencing of Transposable Elements through DNA Methylation and Histone Lysine 9 Dimethylation in

English version České info

DNA topoisomerase is an enzyme that releases the torsional stress in DNA generated during DNA replication or transcription. Here, we uncovered an unexpected role of DNA topoisomerase 1α (TOP1α) in the maintenance of genome stability. Eukaryotic genomes are usually littered with transposable elements (TEs) and repeats, which pose threats to genome stability due to their tendency to move or recombine. Mechanisms are in place to silence these elements, such as RNA-directed DNA methylation (RdDM) and histone H3 lysine 9 dimethylation (H3K9me2) in plants. Two plant-specific RNA polymerases, Pol IV and Pol V, generate small and long noncoding RNAs, respectively, from TEs and repeats. These RNAs then recruit protein factors to deposit DNA methylation or H3K9me2 to silence the loci. In this study, we found that treatment of plants with camptothecin, a TOP1α inhibitor, or loss of function in TOP1α, led to the de-repression of RdDM target loci, which was accompanied by loss of H3K9me2 or DNA methylation. The role of TOP1α in RdDM could be attributed to its promotion of Pol V, but not Pol IV, transcription to generate long noncoding RNAs.

Vyšlo v časopise: DNA Topoisomerase 1α Promotes Transcriptional Silencing of Transposable Elements through DNA Methylation and Histone Lysine 9 Dimethylation in. PLoS Genet 10(7): e32767. doi:10.1371/journal.pgen.1004446
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004446

Souhrn

Zdroje

1. BirdA (2007) Perceptions of epigenetics. Nature 447: 396–398.

2. LawJA, JacobsenSE (2010) Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nature Rev Genet 11: 204–220.

3. HerrAJ, JensenMB, DalmayT, BaulcombeDC (2005) RNA polymerase IV directs silencing of endogenous DNA. Science 308: 118–120.

4. KannoT, HuettelB, MetteMF, AufsatzW, JaligotE, et al. (2005) Atypical RNA polymerase subunits required for RNA-directed DNA methylation. Nature Genetics 37: 761–765.

5. OnoderaY, HaagJR, ReamT, Costa NunesP, PontesO, et al. (2005) Plant nuclear RNA polymerase IV mediates siRNA and DNA methylation-dependent heterochromatin formation. Cell 120: 613–622.

6. PontierD, YahubyanG, VegaD, BulskiA, Saez-VasquezJ, et al. (2005) Reinforcement of silencing at transposons and highly repeated sequences requires the concerted action of two distinct RNA polymerases IV in Arabidopsis. Genes & Development 19: 2030–2040.

7. ZilbermanD, CaoX, JacobsenSE (2003) ARGONAUTE4 control of locus-specific siRNA accumulation and DNA and histone methylation. Science 299: 716–719.

8. WierzbickiAT, HaagJR, PikaardCS (2008) Noncoding transcription by RNA polymerase Pol IVb/Pol V mediates transcriptional silencing of overlapping and adjacent genes. Cell 135: 635–648.

9. WierzbickiAT, ReamTS, HaagJR, PikaardCS (2009) RNA polymerase V transcription guides ARGONAUTE4 to chromatin. Nature Genetics 41: 630–634.

10. ZemachA, KimMY, HsiehPH, Coleman-DerrD, Eshed-WilliamsL, et al. (2013) The Arabidopsis nucleosome remodeler DDM1 allows DNA methyltransferases to access H1-containing heterochromatin. Cell 153: 193–205.

11. EbbsML, BarteeL, BenderJ (2005) H3 lysine 9 methylation is maintained on a transcribed inverted repeat by combined action of SUVH6 and SUVH4 methyltransferases. Molecular and cellular biology 25: 10507–10515.

12. EbbsML, BenderJ (2006) Locus-specific control of DNA methylation by the Arabidopsis SUVH5 histone methyltransferase. The Plant cell 18: 1166–1176.

13. JacksonJP, LindrothAM, CaoX, JacobsenSE (2002) Control of CpNpG DNA methylation by the KRYPTONITE histone H3 methyltransferase. Nature 416: 556–560.

14. DuJ, ZhongX, BernatavichuteYV, StroudH, FengS, et al. (2012) Dual binding of chromomethylase domains to H3K9me2-containing nucleosomes directs DNA methylation in plants. Cell 151: 167–180.

15. EnkeRA, DongZ, BenderJ (2011) Small RNAs prevent transcription-coupled loss of histone H3 lysine 9 methylation in Arabidopsis thaliana. PLoS genetics 7: e1002350.

16. StroudH, DoT, DuJ, ZhongX, FengS, et al. (2014) Non-CG methylation patterns shape the epigenetic landscape in Arabidopsis. Nature structural & molecular biology 21: 64–72.

17. ChampouxJJ (2001) DNA topoisomerases: structure, function, and mechanism. Annual Review of Biochemistry 70: 369–413.

18. VosSM, TretterEM, SchmidtBH, BergerJM (2011) All tangled up: how cells direct, manage and exploit topoisomerase function. Nature Rev Mol Cell Biol 12: 827–841.

19. TakahashiT, MatsuharaS, AbeM, KomedaY (2002) Disruption of a DNA topoisomerase I gene affects morphogenesis in Arabidopsis. The Plant Cell 14: 2085–2093.

20. DinhTT, O'LearyM, WonSY, LiS, ArroyoL, et al. (2013) Generation of a luciferase-based reporter for CHH and CG DNA methylation in Arabidopsis thaliana. Silence 4: 1.

21. JaxelC, CapranicoG, KerriganD, KohnKW, PommierY (1991) Effect of local DNA sequence on topoisomerase I cleavage in the presence or absence of camptothecin. J Biol Chem 266: 20418–20423.

22. StakerBL, HjerrildK, FeeseMD, BehnkeCA, BurginABJr, et al. (2002) The mechanism of topoisomerase I poisoning by a camptothecin analog. PNAS 99: 15387–15392.

23. ManavellaPA, HagmannJ, OttF, LaubingerS, FranzM, et al. (2012) Fast-forward genetics identifies plant CPL phosphatases as regulators of miRNA processing factor HYL1. Cell 151: 859–870.

24. IrizarryRA, Ladd-AcostaC, CarvalhoB, WuH, BrandenburgSA, et al. (2008) Comprehensive high-throughput arrays for relative methylation (CHARM). Genome Res 18: 780–790.

25. LiQY, ZuYG, ShiRZ, YaoLP (2006) Review camptothecin: current perspectives. Current Medicinal Chemistry 13: 2021–2039.

26. GrafP, DolzblaszA, WurschumT, LenhardM, PfreundtU, et al. (2010) MGOUN1 encodes an Arabidopsis type IB DNA topoisomerase required in stem cell regulation and to maintain developmentally regulated gene silencing. The Plant cell 22: 716–728.

27. StroudH, GreenbergMV, FengS, BernatavichuteYV, JacobsenSE (2013) Comprehensive analysis of silencing mutants reveals complex regulation of the Arabidopsis methylome. Cell 152: 352–364.

28. BeckerC, HagmannJ, MullerJ, KoenigD, StegleO, et al. (2011) Spontaneous epigenetic variation in the Arabidopsis thaliana methylome. Nature 480: 245–249.

29. SchmitzRJ, SchultzMD, LewseyMG, O'MalleyRC, UrichMA, et al. (2011) Transgenerational epigenetic instability is a source of novel methylation variants. Science 334: 369–373.

30. WierzbickiAT, CocklinR, MayampurathA, ListerR, RowleyMJ, et al. (2012) Spatial and functional relationships among Pol V-associated loci, Pol IV-dependent siRNAs, and cytosine methylation in the Arabidopsis epigenome. Genes & development 26: 1825–1836.

31. BernatavichuteYV, ZhangX, CokusS, PellegriniM, JacobsenSE (2008) Genome-wide association of histone H3 lysine nine methylation with CHG DNA methylation in Arabidopsis thaliana. PloS One 3: e3156.

32. LippmanZ, GendrelAV, BlackM, VaughnMW, DedhiaN, et al. (2004) Role of transposable elements in heterochromatin and epigenetic control. Nature 430: 471–476.

33. TranRK, ZilbermanD, de BustosC, DittRF, HenikoffJG, et al. (2005) Chromatin and siRNA pathways cooperate to maintain DNA methylation of small transposable elements in Arabidopsis. Genome Biology 6: R90.

34. ZhengB, WangZ, LiS, YuB, LiuJY, et al. (2009) Intergenic transcription by RNA polymerase II coordinates Pol IV and Pol V in siRNA-directed transcriptional gene silencing in Arabidopsis. Genes & Development 23: 2850–2860.

35. LiCF, PontesO, El-ShamiM, HendersonIR, BernatavichuteYV, et al. (2006) An ARGONAUTE4-containing nuclear processing center colocalized with Cajal bodies in Arabidopsis thaliana. Cell 126: 93–106.

36. WonSY, LiS, ZhengB, ZhaoY, LiD, et al. (2012) Development of a luciferase-based reporter of transcriptional gene silencing that enables bidirectional mutant screening in Arabidopsis thaliana. Silence 3: 6.

37. LiuLF, WangJC (1987) Supercoiling of the DNA template during transcription. PNAS 84: 7024–7027.

38. Durand-DubiefM, PerssonJ, NormanU, HartsuikerE, EkwallK (2010) Topoisomerase I regulates open chromatin and controls gene expression in vivo. EMBO J 29: 2126–2134.

39. Durand-DubiefM, SvenssonJP, PerssonJ, EkwallK (2011) Topoisomerases, chromatin and transcription termination. Transcription 2: 66–70.

40. PikaardCS, HaagJR, PontesOM, BlevinsT, CocklinR (2013) A transcription fork model for Pol IV and Pol V-dependent RNA-directed DNA methylation. Cold Spring Harbor Symposia on Quantitative Biology 77: 205–212.

41. MaeshimaK, LaemmliUK (2003) A two-step scaffolding model for mitotic chromosome assembly. Developmental Cell 4: 467–480.

42. TadesseS, MascarenhasJ, KostersB, HasilikA, GraumannPL (2005) Genetic interaction of the SMC complex with topoisomerase IV in Bacillus subtilis. Microbiology 151: 3729–3737.

43. KannoT, BucherE, DaxingerL, HuettelB, BohmdorferG, et al. (2008) A structural-maintenance-of-chromosomes hinge domain-containing protein is required for RNA-directed DNA methylation. Nature Genetics 40: 670–675.

44. HuangHS, AllenJA, MabbAM, KingIF, MiriyalaJ, et al. (2012) Topoisomerase inhibitors unsilence the dormant allele of Ube3a in neurons. Nature 481: 185–189.

45. ChenPY, CokusSJ, PellegriniM (2010) BS Seeker: precise mapping for bisulfite sequencing. BMC Bioinformatics 11: 203.