Journal Article
. 2013 Sep; 502(7470):249-53.
doi: 10.1038/nature12488.

Uhrf1-dependent H3K23 ubiquitylation couples maintenance DNA methylation and replication

Atsuya Nishiyama 1 Luna Yamaguchi  Jafar Sharif  Yoshikazu Johmura  Takeshi Kawamura  Keiko Nakanishi  Shintaro Shimamura  Kyohei Arita  Tatsuhiko Kodama  Fuyuki Ishikawa  Haruhiko Koseki  Makoto Nakanishi  
  • PMID: 24013172
  •     35 References
  •     143 citations


Faithful propagation of DNA methylation patterns during DNA replication is critical for maintaining cellular phenotypes of individual differentiated cells. Although it is well established that Uhrf1 (ubiquitin-like with PHD and ring finger domains 1; also known as Np95 and ICBP90) specifically binds to hemi-methylated DNA through its SRA (SET and RING finger associated) domain and has an essential role in maintenance of DNA methylation by recruiting Dnmt1 to hemi-methylated DNA sites, the mechanism by which Uhrf1 coordinates the maintenance of DNA methylation and DNA replication is largely unknown. Here we show that Uhrf1-dependent histone H3 ubiquitylation has a prerequisite role in the maintenance DNA methylation. Using Xenopus egg extracts, we successfully reproduce maintenance DNA methylation in vitro. Dnmt1 depletion results in a marked accumulation of Uhrf1-dependent ubiquitylation of histone H3 at lysine 23. Dnmt1 preferentially associates with ubiquitylated H3 in vitro though a region previously identified as a replication foci targeting sequence. The RING finger mutant of Uhrf1 fails to recruit Dnmt1 to DNA replication sites and maintain DNA methylation in mammalian cultured cells. Our findings represent the first evidence, to our knowledge, of the mechanistic link between DNA methylation and DNA replication through histone H3 ubiquitylation.

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EMBO Rep, 2019 Aug 31; 20(10). PMID: 31468675    Free PMC article.
MiR-506 Targets UHRF1 to Inhibit Colorectal Cancer Proliferation and Invasion via the KISS1/PI3K/NF-κB Signaling Axis.
Yilin Lin, Zhihua Chen, +4 authors, Shaoqin Chen.
Front Cell Dev Biol, 2019 Dec 06; 7. PMID: 31803739    Free PMC article.
UHRF1-KAT7-mediated regulation of TUSC3 expression via histone methylation/acetylation is critical for the proliferation of colon cancer cells.
Kenzui Taniue, Tomoatsu Hayashi, +7 authors, Tetsu Akiyama.
Oncogene, 2019 Oct 05; 39(5). PMID: 31582837
Systematic analysis of the binding behaviour of UHRF1 towards different methyl- and carboxylcytosine modification patterns at CpG dyads.
Markus Schneider, Carina Trummer, +6 authors, Iris Antes.
PLoS One, 2020 Feb 23; 15(2). PMID: 32084194    Free PMC article.
Detecting and interpreting DNA methylation marks.
Ren Ren, John R Horton, +2 authors, Xiaodong Cheng.
Curr Opin Struct Biol, 2018 Jul 22; 53. PMID: 30031306    Free PMC article.
BAH domains and a histone-like motif in DNA methyltransferase 1 (DNMT1) regulate de novo and maintenance methylation in vivo.
Olya Yarychkivska, Zoha Shahabuddin, +2 authors, Timothy H Bestor.
J Biol Chem, 2018 Oct 21; 293(50). PMID: 30341171    Free PMC article.
Methylation of UHRF1 by SET7 is essential for DNA double-strand break repair.
Ja Young Hahm, Ji-Young Kim, +5 authors, Sang-Beom Seo.
Nucleic Acids Res, 2018 Oct 26; 47(1). PMID: 30357346    Free PMC article.
Epigenetic regulator UHRF1 inactivates REST and growth suppressor gene expression via DNA methylation to promote axon regeneration.
Young Mi Oh, Marcus Mahar, +3 authors, Valeria Cavalli.
Proc Natl Acad Sci U S A, 2018 Dec 12; 115(52). PMID: 30530687    Free PMC article.
Coordinated Dialogue between UHRF1 and DNMT1 to Ensure Faithful Inheritance of Methylated DNA Patterns.
Christian Bronner, Mahmoud Alhosin, Ali Hamiche, Marc Mousli.
Genes (Basel), 2019 Jan 24; 10(1). PMID: 30669400    Free PMC article.
DNA Methylation Reprogramming during Mammalian Development.
Yang Zeng, Taiping Chen.
Genes (Basel), 2019 Apr 03; 10(4). PMID: 30934924    Free PMC article.
Defining UHRF1 Domains that Support Maintenance of Human Colon Cancer DNA Methylation and Oncogenic Properties.
Xiangqian Kong, Jie Chen, +15 authors, Stephen B Baylin.
Cancer Cell, 2019 Apr 09; 35(4). PMID: 30956060    Free PMC article.
Stella protein facilitates DNA demethylation by disrupting the chromatin association of the RING finger-type E3 ubiquitin ligase UHRF1.
Wenlong Du, Qiang Dong, +6 authors, Yingfeng Li.
J Biol Chem, 2019 Apr 26; 294(22). PMID: 31018966    Free PMC article.
UHRF1 depletion and HDAC inhibition reactivate epigenetically silenced genes in colorectal cancer cells.
Takeshi Niinuma, Hiroshi Kitajima, +12 authors, Hiromu Suzuki.
Clin Epigenetics, 2019 May 09; 11(1). PMID: 31064417    Free PMC article.
SET8 prevents excessive DNA methylation by methylation-mediated degradation of UHRF1 and DNMT1.
Huifang Zhang, Qinqin Gao, +11 authors, Jiemin Wong.
Nucleic Acids Res, 2019 Aug 11; 47(17). PMID: 31400111    Free PMC article.
The Emerging Role of Ten-Eleven Translocation 1 in Epigenetic Responses to Environmental Exposures.
Tao Zhu, Anthony P Brown, Hong Ji.
Epigenet Insights, 2020 Mar 14; 13. PMID: 32166220    Free PMC article.
Two distinct modes of DNMT1 recruitment ensure stable maintenance DNA methylation.
Atsuya Nishiyama, Christopher B Mulholland, +16 authors, Makoto Nakanishi.
Nat Commun, 2020 Mar 08; 11(1). PMID: 32144273    Free PMC article.
Identification of berberine as a novel drug for the treatment of multiple myeloma via targeting UHRF1.
Chunming Gu, Zhao Yin, +6 authors, Jia Fei.
BMC Biol, 2020 Mar 28; 18(1). PMID: 32213189    Free PMC article.
Targeted DNA methylation of neurodegenerative disease genes via homology directed repair.
Christopher P Cali, Daniel S Park, Edward B Lee.
Nucleic Acids Res, 2019 Nov 05; 47(22). PMID: 31680172    Free PMC article.
Mammalian DNA methyltransferases: new discoveries and open questions.
Humaira Gowher, Albert Jeltsch.
Biochem Soc Trans, 2018 Aug 30; 46(5). PMID: 30154093    Free PMC article.
UHRF1: a jack of all trades, and a master epigenetic regulator during spermatogenesis.
Simon J Newkirk, Wenfeng An.
Biol Reprod, 2020 Feb 27; 102(6). PMID: 32101289    Free PMC article.
UHRF1 predicts poor prognosis by triggering cell cycle in lung adenocarcinoma.
Zhenbo Tu, Xinzhou Deng, +2 authors, Qiuping Zhang.
J Cell Mol Med, 2020 Jun 05; 24(14). PMID: 32495469    Free PMC article.
Developmental and hormonal regulation of ubiquitin-like with plant homeodomain and really interesting new gene finger domains 1 gene expression in ovarian granulosa and theca cells of cattle.
Maria Chiara Perego, Breanne C Morrell, +2 authors, Leon J Spicer.
J Anim Sci, 2020 Jul 03; 98(7). PMID: 32614952    Free PMC article.
Alternative splicing and allosteric regulation modulate the chromatin binding of UHRF1.
Maria Tauber, Sarah Kreuz, +13 authors, Wolfgang Fischle.
Nucleic Acids Res, 2020 Jul 02; 48(14). PMID: 32609811    Free PMC article.
Direct readout of heterochromatic H3K9me3 regulates DNMT1-mediated maintenance DNA methylation.
Wendan Ren, Huitao Fan, +22 authors, Jikui Song.
Proc Natl Acad Sci U S A, 2020 Jul 18; 117(31). PMID: 32675241    Free PMC article.
USP7 Is a Master Regulator of Genome Stability.
Gabrielle J Valles, Irina Bezsonova, Roger Woodgate, Nicholas W Ashton.
Front Cell Dev Biol, 2020 Aug 28; 8. PMID: 32850836    Free PMC article.
USP7 negatively controls global DNA methylation by attenuating ubiquitinated histone-dependent DNMT1 recruitment.
Jialun Li, Ruiping Wang, +17 authors, Jiemin Wong.
Cell Discov, 2020 Sep 05; 6. PMID: 32884836    Free PMC article.
Epigenetic mechanism and target therapy of UHRF1 protein complex in malignancies.
Busheng Xue, Jiansong Zhao, +3 authors, Yan Li.
Onco Targets Ther, 2019 Jan 23; 12. PMID: 30666134    Free PMC article.
A genetic link between epigenetic repressor AS1-AS2 and DNA replication factors in establishment of adaxial-abaxial leaf polarity of Arabidopsis.
Toan Quy Luong, Sumie Keta, +6 authors, Chiyoko Machida.
Plant Biotechnol (Tokyo), 2018 Jan 01; 35(1). PMID: 31275036    Free PMC article.
Molecular mechanisms of eukaryotic origin initiation, replication fork progression, and chromatin maintenance.
Zuanning Yuan, Huilin Li.
Biochem J, 2020 Sep 25; 477(18). PMID: 32970141    Free PMC article.
The histone and non-histone methyllysine reader activities of the UHRF1 tandem Tudor domain are dispensable for the propagation of aberrant DNA methylation patterning in cancer cells.
Robert M Vaughan, Ariana Kupai, +13 authors, Scott B Rothbart.
Epigenetics Chromatin, 2020 Oct 25; 13(1). PMID: 33097091    Free PMC article.
Roles of ASYMMETRIC LEAVES2 (AS2) and Nucleolar Proteins in the Adaxial-Abaxial Polarity Specification at the Perinucleolar Region in Arabidopsis.
Hidekazu Iwakawa, Hiro Takahashi, Yasunori Machida, Chiyoko Machida.
Int J Mol Sci, 2020 Oct 08; 21(19). PMID: 33022996    Free PMC article.
Investigating the Relationship Between Neuronal Cell Death and Early DNA Methylation After Ischemic Injury.
Mayumi Asada, Hideki Hayashi, +4 authors, Norio Takagi.
Front Neurosci, 2020 Nov 13; 14. PMID: 33177984    Free PMC article.
Pramel7 mediates ground-state pluripotency through proteasomal-epigenetic combined pathways.
Urs Graf, Elisa A Casanova, +16 authors, Paolo Cinelli.
Nat Cell Biol, 2017 Jun 13; 19(7). PMID: 28604677
The Growing Complexity of UHRF1-Mediated Maintenance DNA Methylation.
Si Xie, Chengmin Qian.
Genes (Basel), 2018 Dec 06; 9(12). PMID: 30513966    Free PMC article.
Structural Basis of DNMT1 and DNMT3A-Mediated DNA Methylation.
Wendan Ren, Linfeng Gao, Jikui Song.
Genes (Basel), 2018 Dec 14; 9(12). PMID: 30544982    Free PMC article.
A high-throughput screen of pharmacologically active compounds for inhibitors of UHRF1 reveals epigenetic activity of anthracycline derivative chemotherapeutic drugs.
Hugh Giovinazzo, David Walker, +8 authors, Srinivasan Yegnasubramanian.
Oncotarget, 2019 May 21; 10(32). PMID: 31105884    Free PMC article.
Maintenance DNA methylation is essential for regulatory T cell development and stability of suppressive function.
Kathryn A Helmin, Luisa Morales-Nebreda, +9 authors, Benjamin D Singer.
J Clin Invest, 2020 Sep 09; 130(12). PMID: 32897881    Free PMC article.
Recent evolution of a TET-controlled and DPPA3/STELLA-driven pathway of passive DNA demethylation in mammals.
Christopher B Mulholland, Atsuya Nishiyama, +21 authors, Heinrich Leonhardt.
Nat Commun, 2020 Nov 26; 11(1). PMID: 33235224    Free PMC article.
The ORC ubiquitin ligase OBI1 promotes DNA replication origin firing.
Philippe Coulombe, Joelle Nassar, +5 authors, Marcel Méchali.
Nat Commun, 2019 Jun 05; 10(1). PMID: 31160578    Free PMC article.
A role for LSH in facilitating DNA methylation by DNMT1 through enhancing UHRF1 chromatin association.
Mengmeng Han, Jialun Li, +9 authors, Jiemin Wong.
Nucleic Acids Res, 2020 Nov 11; 48(21). PMID: 33170271    Free PMC article.
In silico APC/C substrate discovery reveals cell cycle-dependent degradation of UHRF1 and other chromatin regulators.
Jennifer L Franks, Raquel C Martinez-Chacin, +15 authors, Michael J Emanuele.
PLoS Biol, 2020 Dec 12; 18(12). PMID: 33306668    Free PMC article.
Discovery of small molecules targeting the tandem tudor domain of the epigenetic factor UHRF1 using fragment-based ligand discovery.
Lyra Chang, James Campbell, +15 authors, Damian W Young.
Sci Rep, 2021 Jan 15; 11(1). PMID: 33441849    Free PMC article.
Kinetics and mechanisms of mitotic inheritance of DNA methylation and their roles in aging-associated methylome deterioration.
Xuan Ming, Zhuqiang Zhang, +7 authors, Bing Zhu.
Cell Res, 2020 Jun 26; 30(11). PMID: 32581343    Free PMC article.
F-box protein CFK1 interacts with and degrades de novo DNA methyltransferase in Arabidopsis.
Jiani Chen, Jie Liu, +8 authors, Xuehua Zhong.
New Phytol, 2020 Nov 21; 229(6). PMID: 33216996    Free PMC article.
Chromatin Regulation through Ubiquitin and Ubiquitin-like Histone Modifications.
Robert M Vaughan, Ariana Kupai, Scott B Rothbart.
Trends Biochem Sci, 2020 Dec 15; 46(4). PMID: 33308996    Free PMC article.
Staying true to yourself: mechanisms of DNA methylation maintenance in mammals.
Nataliya Petryk, Sebastian Bultmann, Till Bartke, Pierre-Antoine Defossez.
Nucleic Acids Res, 2020 Dec 11; 49(6). PMID: 33300031    Free PMC article.
DNMT1 reads heterochromatic H4K20me3 to reinforce LINE-1 DNA methylation.
Wendan Ren, Huitao Fan, +23 authors, Jikui Song.
Nat Commun, 2021 May 05; 12(1). PMID: 33941775    Free PMC article.
Moderate DNA hypomethylation suppresses intestinal tumorigenesis by promoting caspase-3 expression and apoptosis.
Xiaoya Duan, Yuanyong Huang, +7 authors, Jiemin Wong.
Oncogenesis, 2021 May 06; 10(5). PMID: 33947834    Free PMC article.
The interplay between DNA and histone methylation: molecular mechanisms and disease implications.
Yinglu Li, Xiao Chen, Chao Lu.
EMBO Rep, 2021 Apr 13; 22(5). PMID: 33844406    Free PMC article.
The language of chromatin modification in human cancers.
Shuai Zhao, C David Allis, Gang Greg Wang.
Nat Rev Cancer, 2021 May 19; 21(7). PMID: 34002060
HPF1-dependent PARP activation promotes LIG3-XRCC1-mediated backup pathway of Okazaki fragment ligation.
Soichiro Kumamoto, Atsuya Nishiyama, +4 authors, Makoto Nakanishi.
Nucleic Acids Res, 2021 Apr 20; 49(9). PMID: 33872376    Free PMC article.
Thymoquinone Is a Multitarget Single Epidrug That Inhibits the UHRF1 Protein Complex.
Omeima Abdullah, Ziad Omran, +3 authors, Mahmoud Alhosin.
Genes (Basel), 2021 May 01; 12(5). PMID: 33922029    Free PMC article.
lncRNA TRMP-S directs dual mechanisms to regulate p27-mediated cellular senescence.
Tian Shuai, Muhammad Riaz Khan, +4 authors, Fengmin Shao.
Mol Ther Nucleic Acids, 2021 Jun 08; 24. PMID: 34094715    Free PMC article.
Dnmt1 has de novo activity targeted to transposable elements.
Chuck Haggerty, Helene Kretzmer, +21 authors, Alexander Meissner.
Nat Struct Mol Biol, 2021 Jun 19; 28(7). PMID: 34140676    Free PMC article.
The multi-functionality of UHRF1: epigenome maintenance and preservation of genome integrity.
Monica Mancini, Elena Magnani, Filippo Macchi, Ian Marc Bonapace.
Nucleic Acids Res, 2021 May 04; 49(11). PMID: 33939809    Free PMC article.
Silencing UHRF1 Enhances Radiosensitivity of Esophageal Squamous Cell Carcinoma by Inhibiting the PI3K/Akt/mTOR Signaling Pathway.
Beina Hui, Shupei Pan, +6 authors, Xiaozhi Zhang.
Cancer Manag Res, 2021 Jul 01; 13. PMID: 34188537    Free PMC article.
The Molecular Basis of Depression: Implications of Sex-Related Differences in Epigenetic Regulation.
Ayako Kawatake-Kuno, Toshiya Murai, Shusaku Uchida.
Front Mol Neurosci, 2021 Jul 20; 14. PMID: 34276306    Free PMC article.
Nuclear Organization during Hepatogenesis in Zebrafish Requires Uhrf1.
Bhavani P Madakashira, Chi Zhang, +2 authors, Kirsten C Sadler.
Genes (Basel), 2021 Aug 07; 12(7). PMID: 34356097    Free PMC article.

;. PMID: 34426570
UHRF1 Suppresses HIV-1 Transcription and Promotes HIV-1 Latency by Competing with p-TEFb for Ubiquitination-Proteasomal Degradation of Tat.
Taizhen Liang, Qiao Zhang, +4 authors, Lin Li.
mBio, 2021 Sep 02; 12(4). PMID: 34465029    Free PMC article.
Insights into Conformational Dynamics and Allostery in DNMT1-H3Ub/USP7 Interactions.
Yu Zhu, Fei Ye, +3 authors, Guang Hu.
Molecules, 2021 Sep 11; 26(17). PMID: 34500587    Free PMC article.
Mutation-induced DNMT1 cleavage drives neurodegenerative disease.
Wencai Wang, Xingsen Zhao, +7 authors, Jiemin Wong.
Sci Adv, 2021 Sep 14; 7(36). PMID: 34516921    Free PMC article.
Interplay between chromatin marks in development and disease.
Sanne M Janssen, Matthew C Lorincz.
Nat Rev Genet, 2021 Oct 06; 23(3). PMID: 34608297
TIP60 governs the auto‑ubiquitination of UHRF1 through USP7 dissociation from the UHRF1/USP7 complex.
Tanveer Ahmad, Waseem Ashraf, +6 authors, Marc Mousli.
Int J Oncol, 2021 Sep 25; 59(5). PMID: 34558642    Free PMC article.
UHRF1 Could Be a Prognostic Biomarker and Correlated with Immune Cell Infiltration in Hepatocellular Carcinoma.
Danfeng Li, Binlie Chen, Yongming Zeng, Huaiming Wang.
Int J Gen Med, 2021 Oct 23; 14. PMID: 34675635    Free PMC article.
Misregulation of the expression and activity of DNA methyltransferases in cancer.
Isaiah K Mensah, Allison B Norvil, +4 authors, Humaira Gowher.
NAR Cancer, 2021 Dec 07; 3(4). PMID: 34870206    Free PMC article.
DNMT1 regulates the timing of DNA methylation by DNMT3 in an enzymatic activity-dependent manner in mouse embryonic stem cells.
Takamasa Ito, Musashi Kubiura-Ichimaru, +5 authors, Masako Tada.
PLoS One, 2022 Jan 06; 17(1). PMID: 34986190    Free PMC article.
HAUSP Is a Key Epigenetic Regulator of the Chromatin Effector Proteins.
Omeima Abdullah, Mahmoud Alhosin.
Genes (Basel), 2022 Jan 22; 13(1). PMID: 35052383    Free PMC article.
Gene repression through epigenetic modulation by PPARA enhances hepatocellular proliferation.
Daisuke Aibara, Shogo Takahashi, +5 authors, Frank J Gonzalez.
iScience, 2022 Apr 29; 25(5). PMID: 35479397    Free PMC article.
The disordered N-terminal domain of DNMT3A recognizes H2AK119ub and is required for postnatal development.
Tianpeng Gu, Dapeng Hao, +12 authors, Margaret A Goodell.
Nat Genet, 2022 May 10; 54(5). PMID: 35534561
Thioredoxin-Interacting Protein in Cancer and Diabetes.
Hiroshi Masutani.
Antioxid Redox Signal, 2021 Aug 14; 36(13-15). PMID: 34384271    Free PMC article.
The phosphorylation to acetylation/methylation cascade in transcriptional regulation: how kinases regulate transcriptional activities of DNA/histone-modifying enzymes.
Pin Zhao, Samiullah Malik.
Cell Biosci, 2022 Jun 07; 12(1). PMID: 35659740