Decrease in DNA methylation 1 interacts with chromomethylase and like heterochromatin protein 1 in
            Physcomitrella patens

ABSTRACT DNA methylation is involved in gene silencing and genomic stability in mammals, plants, and fungi. Genetics studies of Neurospora crassa have revealed that a DNA methyltransferase (DIM-2), a histone H3K9 methyltransferase (DIM-5), and heterochromatin protein 1 (HP1) are required for DNA methylation. We explored the interrelationships of these components of the methylation machinery. A yeast two-hybrid screen revealed that HP1 interacts with DIM-2. We confirmed the interaction in vivo and demonstrated that it involves a pair of PXVXL-related motifs in the N-terminal region of DIM-2 and the chromo shadow domain of HP1. Both regions are essential for proper DNA methylation. We also determined that DIM-2 and HP1 form a stable complex independently of the trimethylation of histone H3K9, although the association of DIM-2 with its substrate sequences depends on trimethyl-H3K9. The DIM-2/HP1 complex does not include DIM-5. We conclude that DNA methylation in Neurospora is largely or exclusively the result of a unidirectional pathway in which DIM-5 methylates histone H3K9 and then the DIM-2/HP1 complex recognizes the resulting trimethyl-H3K9 mark via the chromo domain of HP1.

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Sequence-unrelated long noncoding RNAs converged to modulate the activity of conserved epigenetic machineries across kingdoms

10.1101/2021.02.26.433017 ◽

2021 ◽

Author(s):

Camille Fonouni-Farde ◽

Aurélie Christ ◽

Thomas Blein ◽

Juan Sebastián Ramírez-Prado ◽

María Florencia Legascue ◽

...

Keyword(s):

Dna Methylation ◽

Transcriptional Activity ◽

Three Dimensional ◽

Noncoding Rnas ◽

Ring Finger ◽

Long Noncoding Rnas ◽

Heterochromatin Protein 1 ◽

Protein Variant ◽

Heterochromatin Protein ◽

Biosynthesis Gene

SUMMARYRNA-DNA hybrid (R-loop)-associated long noncoding RNAs (lncRNAs), including the Arabidopsis lncRNAAUXIN-REGULATED PROMOTER LOOP(APOLO), are emerging as important regulators of three-dimensional chromatin conformation and gene transcriptional activity. Here, we showed that in addition to the PRC1-component LIKE-HETEROCHROMATIN PROTEIN 1 (LHP1),APOLOinteracts with the methylcytosine-binding protein VARIANT IN METHYLATION 1 (VIM1), a conserved homolog of the mammalian DNA methylation regulator UBIQUITIN-LIKE CONTAINING PHD AND RING FINGER DOMAINS 1 (UHRF1). TheAPOLO-VIM1-LHP1 complex directly regulates the transcription of the auxin biosynthesis geneYUCCA2by dynamically determining DNA methylation and H3K27me3 deposition over its promoter during the plant thermomorphogenic response. Strikingly, we demonstrated that the lncRNAUHRF1 Protein Associated Transcript(UPAT), a direct interactor of UHRF1 in humans, can be recognized by VIM1 and LHP1 in plant cells, despite the lack of sequence homology betweenUPATandAPOLO. In addition, we showed that increased levels ofAPOLOorUPAThamper VIM1 and LHP1 binding toYUCCA2promoter. Collectively, our results uncover a new mechanism in which a plant lncRNA coordinates Polycomb action and DNA methylation, and reveal that evolutionary unrelated lncRNAs may exert similar functions across kingdoms.

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Heterochromatin protein 1 forms distinct complexes to direct histone deacetylation and DNA methylation

Nature Structural & Molecular Biology ◽

10.1038/nsmb.2274 ◽

2012 ◽

Vol 19 (5) ◽

pp. 471-477 ◽

Cited By ~ 39

Author(s):

Shinji Honda ◽

Zachary A Lewis ◽

Kenji Shimada ◽

Wolfgang Fischle ◽

Ragna Sack ◽

...

Keyword(s):

Dna Methylation ◽

Histone Deacetylation ◽

Heterochromatin Protein 1 ◽

Heterochromatin Protein

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Dual chromatin recognition by the histone deacetylase complex HCHC is required for proper DNA methylation in Neurospora crassa

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1614279113 ◽

2016 ◽

Vol 113 (41) ◽

pp. E6135-E6144 ◽

Cited By ~ 13

Author(s):

Shinji Honda ◽

Vincent T. Bicocca ◽

Jordan D. Gessaman ◽

Michael R. Rountree ◽

Ayumi Yokoyama ◽

...

Keyword(s):

Dna Methylation ◽

Neurospora Crassa ◽

Histone Deacetylase ◽

Histone Deacetylation ◽

H3k9 Methylation ◽

Heterochromatin Protein 1 ◽

Heterochromatin Protein ◽

Heterochromatin Formation ◽

H3k9 Trimethylation ◽

Shed Light

DNA methylation, heterochromatin protein 1 (HP1), histone H3 lysine 9 (H3K9) methylation, histone deacetylation, and highly repeated sequences are prototypical heterochromatic features, but their interrelationships are not fully understood. Prior work showed that H3K9 methylation directs DNA methylation and histone deacetylation via HP1 in Neurospora crassa and that the histone deacetylase complex HCHC is required for proper DNA methylation. The complex consists of the chromodomain proteins HP1 and chromodomain protein 2 (CDP-2), the histone deacetylase HDA-1, and the AT-hook motif protein CDP-2/HDA-1–associated protein (CHAP). We show that the complex is required for proper chromosome segregation, dissect its function, and characterize interactions among its components. Our analyses revealed the existence of an HP1-based DNA methylation pathway independent of its chromodomain. The pathway partially depends on CHAP but not on the CDP-2 chromodomain. CDP-2 serves as a bridge between the recognition of H3K9 trimethylation (H3K9me3) by HP1 and the histone deacetylase activity of HDA-1. CHAP is also critical for HDA-1 localization to heterochromatin. Specifically, the CHAP zinc finger interacts directly with the HDA-1 argonaute-binding protein 2 (Arb2) domain, and the CHAP AT-hook motifs recognize heterochromatic regions by binding to AT-rich DNA. Our data shed light on the interrelationships among the prototypical heterochromatic features and support a model in which dual recognition by the HP1 chromodomain and the CHAP AT-hooks are required for proper heterochromatin formation.

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Disruption of the Interaction between Transcriptional Intermediary Factor 1β and Heterochromatin Protein 1 Leads to a Switch from DNA Hyper- to Hypomethylation and H3K9 to H3K27 Trimethylation on the MEST Promoter Correlating with Gene Reactivation

Molecular Biology of the Cell ◽

10.1091/mbc.e08-05-0510 ◽

2009 ◽

Vol 20 (1) ◽

pp. 296-305 ◽

Cited By ~ 30

Author(s):

Raphaël Riclet ◽

Mariam Chendeb ◽

Jean-Luc Vonesch ◽

Dirk Koczan ◽

Hans-Juergen Thiesen ◽

...

Keyword(s):

Dna Methylation ◽

Transcriptional Repression ◽

Promoter Region ◽

Loss Of Function ◽

Dna Hypomethylation ◽

Dna Hypermethylation ◽

Heterochromatin Protein 1 ◽

Heterochromatin Protein ◽

H3k27 Trimethylation ◽

H3k9 Trimethylation

Here, we identified the imprinted mesoderm-specific transcript (MEST) gene as an endogenous TIF1β primary target gene and demonstrated that transcriptional intermediary factor (TIF) 1β, through its interaction with heterochromatin protein (HP) 1, is essential in establishing and maintaining a local heterochromatin-like structure on MEST promoter region characterized by H3K9 trimethylation and hypoacetylation, H4K20 trimethylation, DNA hypermethylation, and enrichment in HP1 that correlates with preferential association to foci of pericentromeric heterochromatin and transcriptional repression. On disruption of the interaction between TIF1β and HP1, TIF1β is released from the promoter region, and there is a switch from DNA hypermethylation and histone H3K9 trimethylation to DNA hypomethylation and histone H3K27 trimethylation correlating with rapid reactivation of MEST expression. Interestingly, we provide evidence that the imprinted MEST allele DNA methylation is insensitive to TIF1β loss of function, whereas the nonimprinted allele is regulated through a distinct TIF1β–DNA methylation mechanism.

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