Unoki M, Sasaki H. The UHRF protein family in epigenetics, development, and carcinogenesis. Proc Jpn Acad Ser B Phys Biol Sci. 2022;98(8):401–15.

Article  CAS  PubMed  PubMed Central  Google Scholar 

Mancini M, Magnani E, Macchi F, Bonapace IM. The multi-functionality of UHRF1: epigenome maintenance and preservation of genome integrity. Nucleic Acids Res. 2021;49(11):6053–68.

Article  CAS  PubMed  PubMed Central  Google Scholar 

Fujimori A, Matsuda Y, Takemoto Y, Hashimoto Y, Kubo E, Araki R, Fukumura R, Mita K, Tatsumi K, Muto M. Cloning and mapping of Np95 gene which encodes a novel nuclear protein associated with cell proliferation. Mamm Genome. 1998;9(12):1032–5.

Article  CAS  PubMed  Google Scholar 

Hopfner R, Mousli M, Jeltsch JM, Voulgaris A, Lutz Y, Marin C, Bellocq JP, Oudet P, Bronner C. ICBP90, a novel human CCAAT binding protein, involved in the regulation of topoisomerase IIalpha expression. Cancer Res. 2000;60(1):121–8.

CAS  PubMed  Google Scholar 

DaRosa PA, Harrison JS, Zelter A, Davis TN, Brzovic P, Kuhlman B, Klevit RE. A Bifunctional role for the UHRF1 UBL domain in the control of hemi-methylated DNA-dependent histone ubiquitylation. Mol Cell. 2018;72(4):753-765.e6.

Article  CAS  PubMed  PubMed Central  Google Scholar 

Cheng J, Yang Y, Fang J, Xiao J, Zhu T, Chen F, Wang P, Li Z, Yang H, Xu Y. Structural insight into coordinated recognition of trimethylated histone H3 lysine 9 (H3K9me3) by the plant homeodomain (PHD) and tandem tudor domain (TTD) of UHRF1 (ubiquitin-like, containing PHD and RING finger domains, 1) protein. J Biol Chem. 2013;288:1329–39.

Article  CAS  PubMed  Google Scholar 

Zhang J, Gao Q, Li P, Liu X, Jia Y, Wu W, Li J, Dong S, Koseki H, Wong J. S phase-dependent interaction with DNMT1 dictates the role of UHRF1 but not UHRF2 in DNA methylation maintenance. Cell Res. 2011;21:1723–39.

Article  CAS  PubMed  PubMed Central  Google Scholar 

Alhosin M, Omran Z, Zamzami MA, Al-Malki AL, Choudhry H, Mousli M, Bronner C. Signalling pathways in UHRF1-dependent regulation of tumor suppressor genes in cancer. J Exp Clin Cancer Res. 2016;35:174.

Article  PubMed  PubMed Central  Google Scholar 

Ishiyama S, Nishiyama A, Saeki Y, Moritsugu K, Morimoto D, Yamaguchi L, Arai N, Matsumura R, Kawakami T, Mishima Y, Hojo H, Shimamura S, Ishikawa F, Tajima S, Tanaka K, Ariyoshi M, Shirakawa M, Ikeguchi M, Kidera A, Suetake I, Arita K, Nakanishi M. Structure of the Dnmt1 reader module complexed with a unique two-mono-ubiquitin mark on histone H3 reveals the basis for DNA methylation maintenance. Mol Cell. 2017;68(2):350-360.e7.

Article  CAS  PubMed  Google Scholar 

Bostick M, Kim JK, Esteve PO, Clark A, Pradhan S, Jacobsen SE. UHRF1 plays a role in maintaining DNA methylation in mammalian cells. Science. 2007;317:1760–4.

Article  CAS  PubMed  Google Scholar 

Nishiyama A, Yamaguchi L, Sharif J, Johmura Y, Kawamura T, Nakanishi K, Shimamura S, Arita K, Kodama T, Ishikawa F, Koseki H, Nakanishi M. Uhrf1-dependent H3K23 ubiquitylation couples maintenance DNA methylation and replication. Nature. 2013;502(7470):249–53.

Article  CAS  PubMed  Google Scholar 

Miura M, Watanabe H, Sasaki T, Tatsumi K, Muto M. Dynamic changes in subnuclear NP95 location during the cell cycle and its spatial relationship with DNA replication foci. Exp Cell Res. 2001;263:202–8.

Article  CAS  PubMed  Google Scholar 

Mousli M, Hopfner R, Abbady AQ, Monté D, Jeanblanc M, Oudet P, Louis B, Bronner C. ICBP90 belongs to a new family of proteins with an expression that is deregulated in cancer cells. Br J Cancer. 2003;89(1):120–7.

Article  CAS  PubMed  PubMed Central  Google Scholar 

Bonapace IM, Latella L, Papait R, Nicassio F, Sacco A, Muto M, Crescenzi M, Di-Fiore PP. Np95 is regulated by E1A during mitotic reactivation of terminally differentiated cells and is essential for S phase entry. J Cell Biol. 2002;157:909–14.

Arima Y, Hirota T, Bronner C, Mousli M, Fujiwara T, Niwa S, Ishikawa H, Saya H. Down-regulation of nuclear protein ICBP90 by p53/p21Cip1/WAF1-dependent DNA-damage checkpoint signals contributes to cell cycle arrest at G1/S transition. Genes Cells. 2004;9(2):131–42.

Article  CAS  PubMed  Google Scholar 

Alhosin M, Sharif T, Mousli M, Etienne-Selloum N, Fuhrmann G, Schini-Kerth VB, Bronner C. Down-regulation of UHRF1, associated with re-expression of tumor suppressor genes, is a common feature of natural compounds exhibiting anti-cancer properties. J Exp Clin Cancer Res. 2011;30:41.

Article  CAS  PubMed  PubMed Central  Google Scholar 

Wang Y, Hu P, Wang F, Xi S, Wu S, Sun L, Du Y, Zheng J, Yang H, Tang M, Gao H, Luo H, Lv Y, Yan J, Ou X, Li Y. UHRF1 inhibition epigenetically reprograms cancer stem cells to suppress the tumorigenic phenotype of hepatocellular carcinoma. Cell Death Dis. 2023;14(6):381.

Article  CAS  PubMed  PubMed Central  Google Scholar 

Tu Z, Deng X, Hou S, Feng A, Zhang Q. UHRF1 predicts poor prognosis by triggering cell cycle in lung adenocarcinoma. J Cell Mol Med. 2020;24(14):8069–77.

Article  CAS  PubMed  PubMed Central  Google Scholar 

Ashraf W, Ahmad T, Almalki NAR, Krifa M, Zaayter L, Pizzi A, Muller CD, Hamiche A, Mély Y, Bronner C, Mousli M. Tannin extract from maritime pine bark exhibits anticancer properties by targeting the epigenetic UHRF1/DNMT1 tandem leading to the re-expression of TP73. Food Funct. 2022;13(1):316–26.

Article  CAS  PubMed  Google Scholar 

Unoki M, Nishidate T, Nakamura Y. ICBP90, an E2F–1 target, recruits HDAC1 and binds to methyl-CpG through its SRA domain. Oncogene. 2004;23:7601–10.

Article  CAS  PubMed  Google Scholar 

Park SA, Platt J, Lee JW, Lopez-Giraldez F, Herbst RS, Koo JS. E2F8 as a novel therapeutic target for lung cancer. J Natl Cancer Inst. 2015;107:151.

Article  Google Scholar 

Wu SM, Cheng WL, Liao CJ, Chi HC, Lin YH, Tseng YH, Tsai CY, Chen CY, Lin SL, Chen WJ, Yeh YH, Huang CY, Chen MH, et al. Negative modulation of the epigenetic regulator, UHRF1, by thyroid hormone receptors suppresses liver cancer cell growth. Int J Cancer. 2015;137:37–49.

Article  CAS  PubMed  Google Scholar 

Aebersold R, Agar JN, Amster IJ, Baker MS, Bertozzi CR, Boja ES, Costello CE, Cravatt BF, Fenselau C, Garcia BA, Ge Y, Gunawardena J, Hendrickson RC, Hergenrother PJ, Huber CG, Ivanov AR, Jensen ON, Jewett MC, Kelleher NL, Kiessling LL, Krogan NJ, Larsen MR, Loo JA, Ogorzalek Loo RR, Lundberg E, MacCoss MJ, Mallick P, Mootha VK, Mrksich M, Muir TW, Patrie SM, Pesavento JJ, Pitteri SJ, Rodriguez H, Saghatelian A, Sandoval W, Schlüter H, Sechi S, Slavoff SA, Smith LM, Snyder MP, Thomas PM, Uhlén M, Van Eyk JE, Vidal M, Walt DR, White FM, Williams ER, Wohlschlager T, Wysocki VH, Yates NA, Young NL, Zhang B. How many human proteoforms are there? Nat Chem Biol. 2018;14(3):206–14.

Article  CAS  PubMed  PubMed Central  Google Scholar 

Wei H, Mundade R, Lange KC, Lu T. Protein arginine methylation of non-histone proteins and its role in diseases. Cell Cycle. 2014;13:32–41.

Article  PubMed  Google Scholar 

Hamamoto R, Saloura V, Nakamura Y. Critical roles of non-histone protein lysine methylation in human tumorigenesis. Nat Rev Cancer. 2015;15:110–24.

Article  CAS  PubMed  Google Scholar 

Tien AL, Senbanerjee S, Kulkarni A, Mudbhary R, Goudreau B, Ganesan S, Sadler KC, Ukomadu C. UHRF1 depletion causes a G2/M arrest, activation of DNA damage response and apoptosis. Biochem J. 2011;435:175–85.

Article  CAS  PubMed  Google Scholar 

Liang CC, Zhan B, Yoshikawa Y, Haas W, Gygi SP, Cohn MA. UHRF1 is a sensor for DNA interstrand crosslinks and recruits FANCD2 to initiate the Fanconi anemia pathway. Cell Rep. 2015;10:1947–56.

Article  CAS  PubMed  PubMed Central  Google Scholar 

Ma H, Chen H, Guo X, Wang Z, Sowa ME, Zheng L, Hu S, Zeng P, Guo R, Diao J, Lan F, Harper JW, Shi YG, Xu Y, Shi Y. M phase phosphorylation of the epigenetic regulator UHRF1 regulates its physical association with the deubiquitylase USP7 and stability. Proc Natl Acad Sci USA. 2012;109(13):4828–33.

Article  CAS  PubMed  PubMed Central  Google Scholar 

Chen H, Ma H, Inuzuka H, Diao J, Lan F, Shi YG, Wei W, Shi Y. DNA damage regulates UHRF1 stability via the SCF(β-TrCP) E3 ligase. Mol Cell Biol. 2013;33(6):1139–48.

Article  CAS  PubMed  PubMed Central  Google Scholar 

Yang J, Liu K, Yang J, Jin B, Chen H, Zhan X, Li Z, Wang L, Shen X, Li M, Yu W, Mao Z. PIM1 induces cellular senescence through phosphorylation of UHRF1 at Ser311. Oncogene. 2017;36(34):4828–42.

Article  CAS  PubMed  Google Scholar 

Fu Y, Cao T, Zou X, Ye Y, Liu Y, Peng Y, Deng T, Yin L, Li X. AKT1 regulates UHRF1 protein stability and promotes the resistance to abiraterone in prostate cancer. Oncogenesis. 2023;12(1):1.

Article  PubMed  PubMed Central  Google Scholar 

Kori S, Jimenji T, Ekimoto T, Sato M, Kusano F, Oda T, Unoki M, Ikeguchi M, Arita K. Serine 298 Phosphorylation in Linker 2 of UHRF1 regulates ligand-binding property of its tandem tudor domain. J Mol Biol. 2020;432(14):4061–75.

Article  CAS  PubMed  Google Scholar 

Kori S, Ferry L, Matano S, Jimenji T, Kodera N, Tsusaka T, Matsumura R, Oda T, Sato M, Dohmae N, Ando T, Shinkai Y, Defossez PA, Arita K. Structure of the UHRF1 tandem tudor domain bound to a methylated non-histone Protein, LIG1, reveals rules for binding and regulation. Structure. 2019;27(3):485-496.e7.