AP endonucleases process 5-methylcytosine excision intermediates during active DNA demethylation in Arabidopsis

Lee, Ji-Yoon; Jang, Hosung; Shin, Hosub; Choi, Woo Lee; Mok, Young Geun; Huh, Jin Hoe

doi:10.1093/nar/gku834

Cited by 39 publications

(45 citation statements)

References 54 publications

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“…Repair of UV-B light-induced damage in repressor of silencing1 (ros1), mutated in a gene for a glycosylase that specifically removes methylated cytosines from DNA, is impaired only in the dark, as the negative effect is compensated in light-grown ros1 mutants by the up-regulation of photorepair-specific genes (Qüesta et al, 2013). Interestingly, the demethylation process results in DNA lesions, as it requires base excision repair to restore the DNA sequence (Lee et al, 2014). The decreased in DNA methylation1 (ddm1) mutant, without an SNF2 chromatin-remodeling factor that is crucial for establishing a correct methylation pattern, is generally affected in the repair of UV lightinduced damage (Qüesta et al, 2013).…”

Section: Chromatin Modifiers Connected With Ddrmentioning

confidence: 99%

DNA Damage Repair in the Context of Plant Chromatin

Donà

Scheid

2015

Plant Physiol.

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The integrity of DNA molecules is constantly challenged. All organisms have developed mechanisms to detect and repair multiple types of DNA lesions. The basic principles of DNA damage repair (DDR) in prokaryotes and unicellular and multicellular eukaryotes are similar, but the association of DNA with nucleosomes in eukaryotic chromatin requires mechanisms that allow access of repair enzymes to the lesions. This is achieved by chromatin-remodeling factors, and their necessity for efficient DDR has recently been demonstrated for several organisms and repair pathways. Plants share many features of chromatin organization and DNA repair with fungi and animals, but they differ in other, important details, which are both interesting and relevant for our understanding of genome stability and genetic diversity. In this Update, we compare the knowledge of the role of chromatin and chromatin-modifying factors during DDR in plants with equivalent systems in yeast and humans. We emphasize plant-specific elements and discuss possible implications.A DNA molecule in a eukaryotic chromosome has a diameter of 2 nm but a length in the range of centimeters. Being 10 7 times longer than it is wide would make it highly sensitive to breakage if it were not organized in compact and dynamic chromatin, with nucleosomes as basic units followed by multiple higher order levels of organization. Within this packaging, replication and transcription constitute an endogenous mechanical strain, while exposure of cells to physical or chemical hazard creates a wide range of DNA damage induced by external factors, including photoproducts, pyrimidine dimers, interstrand crosslinking, and single and double-strand breaks (DSBs). All organisms possess mechanisms that repair DNA molecules. DNA damage repair (DDR) systems for the various types of damage are overlapping as well as complementary, and their prevalence depends on the organism, the stage of the cell cycle, the site and the amount of damage, and the availability of intact templates. A coarse categorization distinguishes nucleotide excision repair, base excision repair, nonhomologous end joining (NHEJ), and homologous recombination (HR). Many schematic models for these DDR pathways describe the action and interaction of several repair components, but they are usually misleading in one aspect: DNA strands are illustrated as straight lines, neglecting the emerging role of chromatin for the location and the fate of DNA lesions. More realistically, we should envisage DNA lesions in the chromatin context like the leakage or burst of an in-ground pipe. Recognizing the defect, localizing it, excavating the broken parts, cleaning the ends, reconnecting them, and restoring the original state are mirrored in the subsequent steps of DDR: signaling, labeling, accessing, resecting, religating, and reassembling. Chromatin is expected to especially affect the access, resection, and restoration of the original arrangement, and several factors that can dissolve higher order structures, slide, evict, or exchange ...

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Section: Chromatin Modifiers Connected With Ddrmentioning

confidence: 99%

DNA Damage Repair in the Context of Plant Chromatin

Donà

Scheid

2015

Plant Physiol.

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“…In Arabidopsis, active DNA demethylation is initiated by the ROS1 family of bifunctional DNA glycosylases/lyases, which remove 5-methylcytosine and cleave the DNA backbone at the abasic site (Gong et al, 2002;Agius et al, 2006;Gehring et al, 2006;Morales-Ruiz et al, 2006;Penterman et al, 2007;Zhu, 2009). Then, either the DNA phosphatase ZDP or the AP endonuclease APE1L processes the 3 0 end of the abasic site to generate a hydroxyl group (Martinez-Macias et al, 2012;Lee et al, 2014;Li et al, 2015b). Immediately following that, a yet-to-be identified DNA polymerase and DNA ligase I act sequentially to promote the insertion of an unmethylated cytosine (Li et al, 2015c).…”

Section: Introductionmentioning

confidence: 99%

Retraction: ‘A pair of transposon‐derived proteins regulate active DNA demethylation in Arabidopsis’

Li¹,

Yuan²,

Wang³

et al. 2016

The EMBO Journal

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Fig 6D-E and Fig 7D, WT-LUC and idm1-14 were in an rdr6-11 background, while idap1-1 and idap2-1 were in wild type background. RDR6 has a demonstrated role in DNA methylation and transcriptional gene silencing, and the rdr6 mutation could therefore have a profound impact on gene silencing in these experiments. Thus, the observed reduced LUC luminescence in idap1-1 and idap2-1 mutants could have resulted from the combined effects of rdr6 and idap1 or idap2 mutations, which might change the main conclusion of this paper. Further experiments will be performed to confirm the phenotypes. All authors concur with this statement and wish to apologize for the inconvenience caused.'The EMBO Journal In Arabidopsis, IDM1 is a histone acetyltransferase that plays critical roles in preventing hypermethylation of DNA and transcriptional gene silencing, but the mechanism(s) by which IDM1 is targeted to specific genomic loci is still unclear. Here, we find two new components of the IDM1 complex, IDAP1 and IDAP2, which bear high similarities to the transposase and myb-like DNA-binding protein of PIF/Harbinger transposons, respectively. Dysfunction of IDAP1 or IDAP2 causes DNA hypermethylation and repression of reporter genes as well as endogenous genes. IDAP1 interacts with IDAP2, and they form a protein complex with IDM1. Furthermore, IDAP2 has DNA-binding activity, which facilitates the recruitment of IDM1 to its target loci. We propose that IDAP1 and IDAP2, co-opted from ancient PIF/ Harbinger-like transposon proteins, act together with IDM1 to regulate active DNA demethylation in higher plants.

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“…Another AP endonuclease, ARP, can also hydrolyze 3′-PUA, though not as efficiently as APE1L. 61 Processing of the 3′-phosphate that is generated by combined β- and δ-elimination is handled by a phosphatase known as zinc finger DNA 3′ phosphoesterase (ZDP), an enzyme that generates a 3′-OH terminus and is required for ROS1-initiated DNA demethylation. 62 …”

Section: Ber-mediated Dna Demethylation In Plantsmentioning

confidence: 99%

“…62,63 . Accordingly, recent studies indicate that the predominant product of DME-ROS1 enzymes is 3′-PUA generated by β-elimination, 61 which is then handled by APE1L and follow-on BER enzymes (Figure 6). …”

Section: Ber-mediated Dna Demethylation In Plantsmentioning

confidence: 99%

Role of Base Excision “Repair” Enzymes in Erasing Epigenetic Marks from DNA

Drohat

Coey

2016

Chem. Rev.

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Base excision repair (BER) is one of several DNA repair pathways found in all three domains of life. BER counters the mutagenic and cytotoxic effects of damage that occurs continuously to the nitrogenous bases in DNA, and its critical role in maintaining genomic integrity is well established. However, BER also performs essential functions in processes other than DNA repair, where it acts on naturally modified bases in DNA. A prominent example is the central role of BER in mediating active DNA demethylation, a multi-step process that erases the epigenetic mark, 5-methylcytosine (5mC), or derivatives thereof, converting them back to cytosine. Here, we review recent advances in the understanding of how BER mediates this critical component of epigenetic regulation, in plants and animals.

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AP endonucleases process 5-methylcytosine excision intermediates during active DNA demethylation in Arabidopsis

Cited by 39 publications

References 54 publications

DNA Damage Repair in the Context of Plant Chromatin

DNA Damage Repair in the Context of Plant Chromatin

Retraction: ‘A pair of transposon‐derived proteins regulate active DNA demethylation in Arabidopsis’

Role of Base Excision “Repair” Enzymes in Erasing Epigenetic Marks from DNA

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