The Epigenetics Orchestra of Notch Signaling: A Symphony for Cancer Therapy

References

• Sato C , ZhaoG , IlaganMX. An overview of Notch signaling in adult tissue renewal and maintenance. Curr. Alzheimer Res.9(2), 227–240 (2012).
   PubMed Web of Science ®Google Scholar
• Andersen P , UosakiH , ShenjeLT , KwonC. Non-canonical Notch signaling: emerging role and mechanism. Trends Cell Biol.22(5), 257–265 (2012).
   PubMed Web of Science ®Google Scholar
• Turkoz M , TownsendRR , KopanR. The Notch intracellular domain has an RBPj-independent role during mouse hair follicular development. J. Invest. Dermatol.136(6), 1106–1115 (2016).
   PubMed Web of Science ®Google Scholar
• Aster JC , PearWS , BlacklowSC. The varied roles of Notch in cancer. Annu. Rev. Pathol.12, 245–275 (2017).
   PubMed Web of Science ®Google Scholar
• Hibdon ES , RazumilavaN , KeeleyTMet al. Notch and mTOR signaling pathways promote human gastric cancer cell proliferation. Neoplasia21(7), 702–712 (2019).
   PubMed Web of Science ®Google Scholar
• Ghoshal P , NgangaAJ , Moran-GiuatiJet al. Loss of the SMRT/NCoR2 corepressor correlates with JAG2 overexpression in multiple myeloma. Cancer Res.69(10), 4380–4387 (2009).
   PubMed Web of Science ®Google Scholar
• Jin L , VuT , YuanG , DattaPK. STRAP promotes stemness of human colorectal cancer via epigenetic regulation of the NOTCH pathway. Cancer Res.77(20), 5464–5478 (2017).
   PubMed Web of Science ®Google Scholar
• Zhang TH , LiangLZ , LiuXLet al. Long non-coding RNA MALAT1 interacts with miR-124 and modulates tongue cancer growth by targeting JAG1. Oncol. Rep.37(4), 2087–2094 (2017).
   PubMed Web of Science ®Google Scholar
• Wang L , LongH , ZhengQ , BoX , XiaoX , LiB. Circular RNA circRHOT1 promotes hepatocellular carcinoma progression by initiation of NR2F6 expression. Mol. Cancer18(1), 119 (2019).
   PubMed Web of Science ®Google Scholar
• Kuwabara S , YamakiM , YuH , ItohM. Notch signaling regulates the expression of glycolysis-related genes in a context-dependent manner during embryonic development. Biochem. Biophys. Res. Commun.503(2), 803–808 (2018).
   PubMed Web of Science ®Google Scholar
• Weidenbusch M , RodlerS , SongSet al. Gene expression profiling of the Notch–AhR–IL22 axis at homeostasis and in response to tissue injury. Biosci. Rep.37(6), 1–14 (2017).
   Google Scholar
• Magee CN , MurakamiN , BorgesTJet al. Notch-1 inhibition promotes immune regulation in transplantation via regulatory T cell-dependent mechanisms. Circulation140(10), 846–863 (2019).
   PubMed Web of Science ®Google Scholar
• Ibrahim SA , GadallaR , El-GhonaimyEAet al. Syndecan-1 is a novel molecular marker for triple negative inflammatory breast cancer and modulates the cancer stem cell phenotype via the IL-6/STAT3, Notch and EGFR signaling pathways. Mol. Cancer16(1), 57 (2017).
   PubMed Web of Science ®Google Scholar
• Brahmi M , BallyO , EberstL , CassierP. Therapeutic targeting of Notch signaling in cancer. Bull. Cancer104(10), 883–891 (2017).
   PubMed Web of Science ®Google Scholar
• Kushwah R , GuezguezB , LeeJB , HopkinsCI , BhatiaM. Pleiotropic roles of Notch signaling in normal, malignant, and developmental hematopoiesis in the human. EMBO Rep.15(11), 1128–1138 (2014).
   PubMed Web of Science ®Google Scholar
• Yan B , LiuL , ZhaoYet al. Xiaotan Sanjie decoction attenuates tumor angiogenesis by manipulating Notch-1-regulated proliferation of gastric cancer stem-like cells. World J. Gastroenterol.20(36), 13105–13118 (2014).
   PubMed Web of Science ®Google Scholar
• Huang Z , LinS , LongCet al. Notch signaling pathway mediates doxorubicin-driven apoptosis in cancers. Cancer Manag. Res.10, 1439–1448 (2018).
   PubMed Web of Science ®Google Scholar
• Bigas A , EspinosaL. Notch signaling in cell–cell communication pathways. Curr. Stem Cell Rep.2(4), 349–355 (2016).
   Google Scholar
• Li Z , FischerM , SatkunarajahM , ZhouD , WithersSG , RiniJM. Structural basis of Notch O-glucosylation and O-xylosylation by mammalian protein-O-glucosyltransferase 1 (POGLUT1). Nat. Commun.8(1), 185 (2017).
   PubMedGoogle Scholar
• D’souza B , Meloty-KapellaL , WeinmasterG. Canonical and non-canonical Notch ligands. In: Current Topics in Developmental Biology.Elsevier, 73–129 (2010).
   Google Scholar
• Arnett KL , SeegarTC , BlacklowSC. Structural biology of Notch signaling. In: Targeting Notch in Cancer.Springer, 1–33 (2018).
   Google Scholar
• Bray SJ . Notch signalling in context. Nat. Rev. Mol. Cell Biol.17(11), 722–735 (2016).
   PubMed Web of Science ®Google Scholar
• Lovendahl KN , BlacklowSC , GordonWR. The molecular mechanism of Notch activation. In: Molecular Mechanisms of Notch Signaling.Springer, 47–58 (2018).
   Google Scholar
• Seegar TCM , KillingsworthLB , SahaNet al. Structural basis for regulated proteolysis by the alpha-secretase ADAM10. Cell171(7), 1638–1648e7 (2017).
   PubMed Web of Science ®Google Scholar
• Sosa Iglesias V , TheysJ , GrootAJet al. Synergistic effects of NOTCH/gamma-secretase inhibition and standard of care treatment modalities in non-small cell lung cancer cells. Front. Oncol.8(460), 460 (2018).
   PubMedGoogle Scholar
• Jang J , ByunSH , HanDet al. Notch intracellular domain deficiency in nuclear localization activity retains the ability to enhance neural stem cell character and block neurogenesis in mammalian brain development. Stem Cells Dev.23(23), 2841–2850 (2014).
   PubMed Web of Science ®Google Scholar
• Andersen P , UosakiH , ShenjeLT , KwonC. Non-canonical Notch signaling: emerging role and mechanism. Trends Cell Biol.22(5), 257–265 (2012).
   PubMed Web of Science ®Google Scholar
• Krishna BM , JanaS , SinghalJet al. Notch signaling in breast cancer: from pathway analysis to therapy. Cancer Lett.461, 123–131 (2019).
   PubMed Web of Science ®Google Scholar
• Huang Q , LiJ , ZhengJ , WeiA. The carcinogenic role of the Notch signaling pathway in the development of hepatocellular carcinoma. J. Cancer10(6), 1570–1579 (2019).
   PubMed Web of Science ®Google Scholar
• Lim JS , IbasetaA , FischerMMet al. Intratumoural heterogeneity generated by Notch signalling promotes small-cell lung cancer. Nature545(7654), 360–364 (2017).
   PubMed Web of Science ®Google Scholar
• Hu YY , ZhengMH , ZhangR , LiangYM , HanH. Notch signaling pathway and cancer metastasis. Adv. Exp. Med. Biol.727, 186–198 (2012).
   PubMed Web of Science ®Google Scholar
• Landor SK , LendahlU. The interplay between the cellular hypoxic response and Notch signaling. Exp. Cell Res.356(2), 146–151 (2017).
   PubMed Web of Science ®Google Scholar
• Ayaz F , OsborneBA. Non-canonical notch signaling in cancer and immunity. Front. Oncol.4, 345 (2014).
   PubMedGoogle Scholar
• Osipo C , GoldeTE , OsborneBA , MieleLA. Off the beaten pathway: the complex cross talk between Notch and NF-κB. Lab. Invest.88(1), 11 (2008).
   PubMed Web of Science ®Google Scholar
• Perumalsamy LR , NagalaM , BanerjeeP , SarinA. A hierarchical cascade activated by non-canonical Notch signaling and the mTOR–Rictor complex regulates neglect-induced death in mammalian cells. Cell Death Differ.16(6), 879–889 (2009).
   PubMed Web of Science ®Google Scholar
• Ang HL , TergaonkarV. Notch and NFκB signaling pathways: do they collaborate in normal vertebrate brain development and function?BioEssays29(10), 1039–1047 (2007).
   PubMed Web of Science ®Google Scholar
• Traustadottir GA , JensenCH , ThomassenMet al. Evidence of non-canonical NOTCH signaling: delta-like 1 homolog (DLK1) directly interacts with the NOTCH1 receptor in mammals. Cell. Signal.28(4), 246–254 (2016).
   PubMed Web of Science ®Google Scholar
• Wang MM . Notch signaling and Notch signaling modifiers. Int. J. Biochem. Cell Biol.43(11), 1550–1562 (2011).
   PubMed Web of Science ®Google Scholar
• Du J , WangX , ZhangX , ZhangX , JiangH. DNER modulates the length, polarity and synaptogenesis of spiral ganglion neurons via the Notch signaling pathway. Mol. Med. Rep.17(2), 2357–2365 (2018).
   PubMed Web of Science ®Google Scholar
• Ballester-Lopez C , ConlonTM , ErtuzZet al. The Notch ligand DNER regulates macrophage IFNγ release in chronic obstructive pulmonary disease. EBioMedicine43, 562–575 (2019).
   PubMed Web of Science ®Google Scholar
• Pan W , SongXY , HuQB , ZhangM , XuXH. TSP2 acts as a suppresser of cell invasion, migration and angiogenesis in medulloblastoma by inhibiting the Notch signaling pathway. Brain Res.1718, 223–230 (2019).
   PubMed Web of Science ®Google Scholar
• Rauen T , RaffetsederU , FryeBCet al. YB-1 acts as a ligand for Notch-3 receptors and modulates receptor activation. J. Biol. Chem.284(39), 26928–26940 (2009).
   PubMed Web of Science ®Google Scholar
• Tang H , XiaoWR , LiaoYYet al. EGFL7 silencing inactivates the Notch signaling pathway; enhancing cell apoptosis and suppressing cell proliferation in human cutaneous melanoma. Neoplasma66(2), 187–196 (2019).
   PubMed Web of Science ®Google Scholar
• Gupta R , HongD , IborraF , SarnoS , EnverT. NOV (CCN3) functions as a regulator of human hematopoietic stem or progenitor cells. Science316(5824), 590–593 (2007).
   PubMed Web of Science ®Google Scholar
• Vatanmakanian M , TavallaieM , GhadamiS. Imatinib independent aberrant methylation of NOV/CCN3 in chronic myelogenous leukemia patients: a mechanism upstream of BCR-ABL1 function?Cell Commun. Signal.17(1), 38 (2019).
   PubMedGoogle Scholar
• Meng H , ZhangX , HankensonKD , WangMM. Thrombospondin 2 potentiates notch3/jagged1 signaling. J. Biol. Chem.284(12), 7866–7874 (2009).
   PubMed Web of Science ®Google Scholar
• Shi J , LiP , ZouL , ChenP , ZhangLP. Extracellular Y-box binding protein-1 promotes proliferation and metastasis of HepG2 cells through Notch3 receptor. Zhonghua Gan Zang Bing Za Zhi24(3), 202–206 (2016).
   PubMedGoogle Scholar
• Lindquist JA , MertensPR. Cold shock proteins: from cellular mechanisms to pathophysiology and disease. Cell Commun. Signal.16(1), 63 (2018).
   PubMedGoogle Scholar
• Ke B , FanC , TuW , FangX. The role of Y-box binding protein 1 in kidney injury: friend or foe?Cell. Physiol. Biochem.46(1), 314–321 (2018).
   PubMedGoogle Scholar
• Hong G , KuekV , ShiJet al. EGFL7: master regulator of cancer pathogenesis, angiogenesis and an emerging mediator of bone homeostasis. J. Cell. Physiol.233(11), 8526–8537 (2018).
   PubMed Web of Science ®Google Scholar
• Palmer WH , DengWM. Ligand-independent mechanisms of Notch activity. Trends Cell Biol.25(11), 697–707 (2015).
   PubMed Web of Science ®Google Scholar
• Sakamoto K , YamaguchiS , AndoRet al. The nephroblastoma overexpressed gene (NOV/ccn3) protein associates with Notch1 extracellular domain and inhibits myoblast differentiation via Notch signaling pathway. J. Biol. Chem.277(33), 29399–29405 (2002).
   PubMed Web of Science ®Google Scholar
• Thibout H , MartinerieC , CreminonCet al. Characterization of human NOV in biological fluids: an enzyme immunoassay for the quantification of human NOV in sera from patients with diseases of the adrenal gland and of the nervous system. J. Clin. Endocrinol. Metab.88(1), 327–336 (2003).
   PubMed Web of Science ®Google Scholar
• Miyamoto A , LauR , HeinPW , ShipleyJM , WeinmasterG. Microfibrillar proteins MAGP-1 and MAGP-2 induce Notch1 extracellular domain dissociation and receptor activation. J. Biol. Chem.281(15), 10089–10097 (2006).
   PubMed Web of Science ®Google Scholar
• Aithal MG , RajeswariN. Role of Notch signalling pathway in cancer and its association with DNA methylation. J. Genet.92(3), 667–675 (2013).
   PubMed Web of Science ®Google Scholar
• Wang J , SullengerBA , RichJN. Notch signaling in cancer stem cells. ( 0065–2598 [Print]).
   Google Scholar
• Capaccione KM , PineSR. The Notch signaling pathway as a mediator of tumor survival. ( 1460–2180 [Electronic]).
   Google Scholar
• Xiao W , GaoZ , DuanY , YuanW , KeY. Notch signaling plays a crucial role in cancer stem-like cells maintaining stemness and mediating chemotaxis in renal cell carcinoma. J. Exp. Clin. Cancer Res.36(1), 41 (2017).
   PubMedGoogle Scholar
• Natsuizaka M , WhelanKA , KagawaSet al. Interplay between Notch1 and Notch3 promotes EMT and tumor initiation in squamous cell carcinoma. Nat. Commun.8(1), 1758 (2017).
   PubMedGoogle Scholar
• De Francesco EM , MaggioliniM , MustiAM. Crosstalk between Notch, HIF-1α and GPER in breast cancer EMT. Int. J. Mol. Sci.19(7), 2011 (2018).
   PubMed Web of Science ®Google Scholar
• Pandya Thakkar N , PereiraBMV , KatakiaYTet al. Elevated H3K4me3 through MLL2-WDR82 upon hyperglycemia causes jagged ligand dependent notch activation to interplay with differentiation state of endothelial cells. Font. Cell Dev. Biol.10, 839109 (2022).
   PubMed Web of Science ®Google Scholar
• Gottlieb TM , LealJF , SegerR , TayaY , OrenM. Cross-talk between Akt, p53 and Mdm2: possible implications for the regulation of apoptosis. ( 0950–9232 [Print]).
   Google Scholar
• Dotto GP . Crosstalk of Notch with p53 and p63 in cancer growth control. Nat. Rev. Cancer9(8), 587–595 (2009).
   PubMed Web of Science ®Google Scholar
• Radtke F , RajK. The role of Notch in tumorigenesis: oncogene or tumour suppressor?Nat. Rev. Cancer3(10), 756–767 (2003).
   PubMed Web of Science ®Google Scholar
• South AP , ChoRJ , AsterJC. The double-edged sword of Notch signaling in cancer. Semin. Cell Dev. Biol.23(4), 458–464 (2012).
   PubMed Web of Science ®Google Scholar
• Roy G , YangT , LiuS , LuoY-L , LiuY , ZhongQ. Epigenetic regulation of MAP3K8 in EBV-associated gastric carcinoma. Int. J. Mol. Sci.24(3), 1964 (2023).
   PubMed Web of Science ®Google Scholar
• Ellisen LW , BirdJ , WestDCet al. TAN-1, the human homolog of the Drosophila notch gene, is broken by chromosomal translocations in T lymphoblastic neoplasms. ( 0092–8674 [Print]).
   Google Scholar
• Reynolds TC , SmithSD , SklarJ. Analysis of DNA surrounding the breakpoints of chromosomal translocations involving the beta T cell receptor gene in human lymphoblastic neoplasms. ( 0092–8674 [Print]).
   Google Scholar
• Girard L , HannaZ , BeaulieuNet al. Frequent provirus insertional mutagenesis of Notch1 in thymomas of MMTVD/myc transgenic mice suggests a collaboration of c-myc and Notch1 for oncogenesis. Genes Dev.10(15), 1930–1944 (1996).
   PubMed Web of Science ®Google Scholar
• Tohda S . NOTCH signaling roles in acute myeloid leukemia cell growth and interaction with other stemness-related signals. Anticancer Res.34(11), 6259–6264 (2014).
   PubMed Web of Science ®Google Scholar
• Gallahan D , KozakC , CallahanR. A new common integration region (int-3) for mouse mammary tumor virus on mouse chromosome 17. J. Virol.61(1), 218–220 (1987).
   PubMed Web of Science ®Google Scholar
• Reedijk M , OdorcicS , ChangLet al. High-level coexpression of JAG1 and NOTCH1 is observed in human breast cancer and is associated with poor overall survival. Cancer Res.65(18), 8530 (2005).
   PubMed Web of Science ®Google Scholar
• Zagouras P , StifaniS , BlaumuellerCM , CarcangiuML , Artavanis-TsakonasS. Alterations in Notch signaling in neoplastic lesions of the human cervix. Proc. Natl Acad. Sci. USA92(14), 6414–6418 (1995).
   PubMed Web of Science ®Google Scholar
• Zhang Y , LiB , JiZZ , ZhengPS. Notch1 regulates the growth of human colon cancers. Cancer116(22), 5207–5218 (2010).
   PubMed Web of Science ®Google Scholar
• Westhoff B , ColalucaIN , D’ArioGet al. Alterations of the Notch pathway in lung cancer. Proc. Natl Acad. Sci. USA106(52), 22293–22298 (2009).
   PubMed Web of Science ®Google Scholar
• Klinakis A , LobryC , Abdel-WahabOet al. A novel tumour-suppressor function for the Notch pathway in myeloid leukaemia. Nature473(7346), 230–233 (2011).
   PubMed Web of Science ®Google Scholar
• Lowell S , WattFM. Delta regulates keratinocyte spreading and motility independently of differentiation. Mech. Dev.107(1–2), 133–140 (2001).
   PubMed Web of Science ®Google Scholar
• Rampias T , VgenopoulouP , AvgerisMet al. A new tumor suppressor role for the Notch pathway in bladder cancer. Nat. Med.20(10), 1199–1205 (2014).
   PubMed Web of Science ®Google Scholar
• Zhu B , SunL , LuoWet al. Activated Notch signaling augments cell growth in hepatocellular carcinoma via up-regulating the nuclear receptor NR4A2. Oncotarget8(14), 23289–23302 (2017).
   PubMedGoogle Scholar
• Thélu J , RossioP , FavierB. Notch signalling is linked to epidermal cell differentiation level in basal cell carcinoma, psoriasis and wound healing. BMC Dermatol.2, 7–7 (2002).
   PubMedGoogle Scholar
• Lo Muzio L , PannoneG , StaibanoSet al. WNT-1 expression in basal cell carcinoma of head and neck. An immunohistochemical and confocal study with regard to the intracellular distribution of beta-catenin. Anticancer Res.22(2A), 565–576 (2002).
   PubMed Web of Science ®Google Scholar
• Sriuranpong V , BorgesMW , RaviRKet al. Notch signaling induces cell cycle arrest in small cell lung cancer cells. Cancer Res.61(7), 3200–3205 (2001).
   PubMed Web of Science ®Google Scholar
• Zhang Y , LiD , FengFet al. Progressive and prognosis value of Notch receptors and ligands in hepatocellular carcinoma: a systematic review and meta-analysis. Sci. Rep.7(1), 14809 (2017).
   PubMedGoogle Scholar
• Wang M , XueL , CaoQ , LinYet al. Expression of Notch1, Jagged1 and beta-catenin and their clinicopathological significance in hepatocellular carcinoma. ( 0028–2685 [Print]).
   Google Scholar
• Sun L , LiuM , SunGCet al. Notch signaling activation in cervical cancer cells induces cell growth arrest with the involvement of the nuclear receptor NR4A2. J. Cancer7(11), 1388–1395 (2016).
   PubMed Web of Science ®Google Scholar
• Yoshikawa A , GotandaY , SuzukiYet al. Age- and gender-specific distributions of hepatitis B virus (HBV) genotypes in Japanese HBV-positive blood donors. Transfusion49(7), 1314–1320 (2009).
   PubMed Web of Science ®Google Scholar
• Wang L , QinH , ChenB , XinX , LiJ , HanH. Overexpressed active Notch1 induces cell growth arrest of HeLa cervical carcinoma cells. Int. J. Gynecol. Cancer17(6), 1283–1292 (2007).
   PubMed Web of Science ®Google Scholar
• Suman S , DasTP , AnkemMK , DamodaranC. Targeting Notch signaling in colorectal cancer. Curr. Colorectal Cancer Rep.10(4), 411–416 (2014).
   PubMedGoogle Scholar
• Galluzzo P , BocchettaM. Notch signaling in lung cancer. Expert Rev. Anticancer Ther.11(4), 533–540 (2011).
   PubMed Web of Science ®Google Scholar
• Motooka Y , FujinoK , SatoY , KudohS , SuzukiM , ItoT. Pathobiology of Notch2 in lung cancer. Pathology49(5), 486–493 (2017).
   PubMed Web of Science ®Google Scholar
• Di Ianni M , BaldoniS , RosatiEet al. A new genetic lesion in B-CLL: a NOTCH1 PEST domain mutation. ( 1365–2141 [Electronic]).
   Google Scholar
• Puente XS , PinyolM , QuesadaVet al. Whole-genome sequencing identifies recurrent mutations in chronic lymphocytic leukaemia. Nature475(7354), 101–105 (2011).
   PubMed Web of Science ®Google Scholar
• Agrawal N , FrederickMJ , PickeringCRet al. Exome sequencing of head and neck squamous cell carcinoma reveals inactivating mutations in NOTCH1. Science333(6046), 1154–1157 (2011).
   PubMed Web of Science ®Google Scholar
• Pickering CR , ZhouJH , LeeJJet al. Mutational landscape of aggressive cutaneous squamous cell carcinoma. Clin. Cancer Res.20(24), 6582–6592 (2014).
   PubMed Web of Science ®Google Scholar
• Song Y , LiL , OuYet al. Identification of genomic alterations in oesophageal squamous cell cancer. Nature509(7498), 91–95 (2014).
   PubMed Web of Science ®Google Scholar
• George J , LimJS , JangSJet al. Comprehensive genomic profiles of small cell lung cancer. Nature524(7563), 47–53 (2015).
   PubMed Web of Science ®Google Scholar
• Rekhtman N , PietanzaMC , HellmannMDet al. Next-generation sequencing of pulmonary large cell neuroendocrine carcinoma reveals small cell carcinoma-like and non-small cell carcinoma-like subsets. Clin. Cancer Res.22(14), 3618–3629 (2016).
   PubMed Web of Science ®Google Scholar
• Cancer Genome Atlas Research Network , BratDJ , VerhaakRGet al.Comprehensive, integrative genomic analysis of diffuse lower-grade gliomas. N. Engl. J. Med.372(26), 2481–2498 (2015).
   PubMed Web of Science ®Google Scholar
• Biswas S , RaoCM. Epigenetics in cancer: fundamentals and beyond. Pharmacol. Ther.173, 118–134 (2017).
   PubMed Web of Science ®Google Scholar
• Kagohara LT , Stein-O’BrienGL , KelleyDet al. Epigenetic regulation of gene expression in cancer: techniques, resources and analysis. Brief Funct. Genomics17(1), 49–63 (2017).
   Web of Science ®Google Scholar
• Bernstein BE , MeissnerA , LanderES. The mammalian epigenome. Cell128(4), 669–681 (2007).
   PubMed Web of Science ®Google Scholar
• Du Q , LuuPL , StirzakerC , ClarkSJ. Methyl-CpG-binding domain proteins: readers of the epigenome. Epigenomics7(6), 1051–1073 (2015).
   PubMed Web of Science ®Google Scholar
• Chen QW , ZhuXY , LiYY , MengZQ. Epigenetic regulation and cancer (review). Oncol. Rep.31(2), 523–532 (2014).
   PubMed Web of Science ®Google Scholar
• Arrowsmith CH , BountraC , FishPV , LeeK , SchapiraM. Epigenetic protein families: a new frontier for drug discovery. Nat. Rev. Drug Discov.11(5), 384–400 (2012).
   PubMed Web of Science ®Google Scholar
• Falkenberg KJ , JohnstoneRW. Histone deacetylases and their inhibitors in cancer, neurological diseases and immune disorders. Nat. Rev. Drug Discov.13(9), 673 (2014).
   PubMed Web of Science ®Google Scholar
• Pande V . Understanding the complexity of epigenetic target space: miniperspective. J. Med. Chem.59(4), 1299–1307 (2016).
   PubMed Web of Science ®Google Scholar
• Brownell JE , AllisCD. Special HATs for special occasions: linking histone acetylation to chromatin assembly and gene activation. Curr. Opin. Genet. Dev.6(2), 176–184 (1996).
   PubMed Web of Science ®Google Scholar
• Ruiz-Carrillo A , WanghLJ , AllfreyVG. Processing of newly synthesized histone molecules. Science190(4210), 117–128 (1975).
   PubMed Web of Science ®Google Scholar
• Baxter E , WindlochK , GannonF , LeeJS. Epigenetic regulation in cancer progression. Cell Biosci.4(1), 45 (2014).
   PubMedGoogle Scholar
• Huang Y , GreeneE , StewartTMet al. Inhibition of lysine-specific demethylase 1 by polyamine analogues results in reexpression of aberrantly silenced genes. Proc. Natl Acad. Sci. USA104(19), 8023–8028 (2007).
   PubMed Web of Science ®Google Scholar
• Shi Y , LanF , MatsonCet al. Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell119(7), 941–953 (2004).
   PubMed Web of Science ®Google Scholar
• Banerjee T , ChakravartiD. A peek into the complex realm of histone phosphorylation. Mol. Cell. Biol.05631–05611 (2011).
   Web of Science ®Google Scholar
• Kschonsak M , HaeringCH. Shaping mitotic chromosomes: from classical concepts to molecular mechanisms. BioEssays37(7), 755–766 (2015).
   PubMed Web of Science ®Google Scholar
• Nowak SJ , CorcesVG. Phosphorylation of histone H3: a balancing act between chromosome condensation and transcriptional activation. Trends Genet.20(4), 214–220 (2004).
   PubMed Web of Science ®Google Scholar
• Rossetto D , AvvakumovN , CoteJ. Histone phosphorylation: a chromatin modification involved in diverse nuclear events. Epigenetics7(10), 1098–1108 (2012).
   PubMed Web of Science ®Google Scholar
• Aihara H , NakagawaT , YasuiKet al. Nucleosomal histone kinase-1 phosphorylates H2A Thr 119 during mitosis in the early Drosophila embryo. Genes Dev.18(8), 877–888 (2004).
   PubMed Web of Science ®Google Scholar
• Lowndes NF , TohGW. DNA repair: the importance of phosphorylating histone H2AX. Curr. Biol.15(3), R99–R102 (2005).
   PubMed Web of Science ®Google Scholar
• Pinto DMS , FlausA. Structure and function of histone H2AX. In: Genome Stability and Human Diseases.Springer, 55–78 (2010).
   Google Scholar
• Cole AJ , Clifton-BlighR , MarshDJ. Histone H2B monoubiquitination: roles to play in human malignancy. Endocr. Relat. Cancer22(1), T19–T33 (2015).
   PubMed Web of Science ®Google Scholar
• Wang Z , LiY , KongD , AhmadA , BanerjeeS , SarkarFH. Cross-talk between miRNA and Notch signaling pathways in tumor development and progression. Cancer Lett.292(2), 141–148 (2010).
   PubMed Web of Science ®Google Scholar
• Geisler S , CollerJ. RNA in unexpected places: long non-coding RNA functions in diverse cellular contexts. Nat. Rev. Mol. Cell Biol.14(11), 699–712 (2013).
   PubMed Web of Science ®Google Scholar
• Reicher A , FoßeltederJ , KwongLN , PichlerM. Crosstalk between the Notch signaling pathway and long non-coding RNAs. Cancer Lett.420, 91–96 (2018).
   PubMed Web of Science ®Google Scholar
• Wang KC , ChangHY. Molecular mechanisms of long noncoding RNAs. Mol. Cell43(6), 904–914 (2011).
   PubMed Web of Science ®Google Scholar
• Pan Y , MaoY , JinR , JiangL. Crosstalk between the Notch signaling pathway and non-coding RNAs in gastrointestinal cancers. Oncol. Lett.15(1), 31–40 (2018).
   PubMed Web of Science ®Google Scholar
• Piazzi G , BazzoliF , RicciardielloL. Epigenetic silencing of Notch signaling in gastrointestinal cancers. Cell Cycle11(23), 4323–4327 (2012).
   PubMed Web of Science ®Google Scholar
• Piazzi G , FiniL , SelgradMet al. Epigenetic regulation of delta-like1 controls Notch1 activation in gastric cancer. Oncotarget2(12), 1291–1301 (2011).
   PubMedGoogle Scholar
• Gaykalova DA , ZizkovaV , GuoTet al. Integrative computational analysis of transcriptional and epigenetic alterations implicates DTX1 as a putative tumor suppressor gene in HNSCC. Oncotarget8(9), 15349 (2017).
   PubMedGoogle Scholar
• Hernandez-Vargas H , LambertM-P , LeCalvez-Kelm Fet al. Hepatocellular carcinoma displays distinct DNA methylation signatures with potential as clinical predictors. PLOS ONE5(3), e9749 (2010).
   PubMed Web of Science ®Google Scholar
• Zhu Y , YeM , XuHet al. Methylation status of CpG sites in the NOTCH4 promoter region regulates NOTCH4 expression in patients with tetralogy of Fallot. Mol. Med. Rep.22(5), 4412–4422 (2020).
   PubMed Web of Science ®Google Scholar
• Bhagat TD , ZouY , HuangSet al. Notch pathway is activated via genetic and epigenetic alterations and is a therapeutic target in clear cell renal cancer. J. Biol. Chem.M116, 745208 (2016).
   Google Scholar
• Kuang SQ , FangZ , Zweidler-MckayPAet al. Epigenetic inactivation of Notch–Hes pathway in human B-cell acute lymphoblastic leukemia. PLOS ONE8(4), e61807 (2013).
   PubMed Web of Science ®Google Scholar
• Scourzic L , CouronneL , PedersenMTet al. DNMT3A(R882H) mutant and Tet2 inactivation cooperate in the deregulation of DNA methylation control to induce lymphoid malignancies in mice. Leukemia30(6), 1388–1398 (2016).
   PubMed Web of Science ®Google Scholar
• Arzate-Mejia RG , Valle-GarciaD , Recillas-TargaF. Signaling epigenetics: novel insights on cell signaling and epigenetic regulation. IUBMB Life63(10), 881–895 (2011).
   PubMed Web of Science ®Google Scholar
• Cierpicki T , RisnerLE , GrembeckaJet al. Structure of the MLL CXXC domain-DNA complex and its functional role in MLL-AF9 leukemia. Nat. Struct. Mol. Biol.17(1), 62–68 (2010).
   PubMed Web of Science ®Google Scholar
• Huang YC , LinSJ , ShihHYet al. Epigenetic regulation of NOTCH1 and NOTCH3 by KMT2A inhibits glioma proliferation. Oncotarget8(38), 63110–63120 (2017).
   PubMedGoogle Scholar
• Rauen T , GrammatikosAP , HedrichCMet al. cAMP-responsive element modulator alpha (CREMalpha) contributes to decreased Notch-1 expression in T cells from patients with active systemic lupus erythematosus (SLE). J. Biol. Chem.287(51), 42525–42532 (2012).
   PubMed Web of Science ®Google Scholar
• Xia Y , CaoX , XueXet al. Development of hair cells in inner ear is associated with expression and promoter methylation of Notch-1 in postnatal mice. Int. J. Clin. Exp. Med.8(9), 15542 (2015).
   PubMed Web of Science ®Google Scholar
• Moshkin YM , KanTW , GoodfellowHet al. Histone chaperones ASF1 and NAP1 differentially modulate removal of active histone marks by LID-RPD3 complexes during NOTCH silencing. Mol. Cell35(6), 782–793 (2009).
   PubMed Web of Science ®Google Scholar
• Sawarkar R , ParoR. Interpretation of developmental signaling at chromatin: the polycomb perspective. Dev. Cell19(5), 651–661 (2010).
   PubMed Web of Science ®Google Scholar
• De Koning L , CorpetA , HaberJE , AlmouzniG. Histone chaperones: an escort network regulating histone traffic. Nat. Struct. Mol. Biol.14(11), 997–1007 (2007).
   PubMed Web of Science ®Google Scholar
• Eitoku M , SatoL , SendaT , HorikoshiM. Histone chaperones: 30 years from isolation to elucidation of the mechanisms of nucleosome assembly and disassembly. Cell. Mol. Life Sci.65(3), 414–444 (2008).
   PubMed Web of Science ®Google Scholar
• Pile LA , SchlagEM , WassarmanDA. The SIN3/RPD3 deacetylase complex is essential for G2 phase cell cycle progression and regulation of SMRTER corepressor levels. Mol. Cell. Biol.22(14), 4965–4976 (2002).
   PubMed Web of Science ®Google Scholar
• Vaquero A , SternglanzR , ReinbergD. NAD+-dependent deacetylation of H4 lysine 16 by class III HDACs. Oncogene26(37), 5505–5520 (2007).
   PubMed Web of Science ®Google Scholar
• Majidinia M , DarbandSG , KavianiM , NabaviSM , Jahanban-EsfahlanR , YousefiB. Cross-regulation between Notch signaling pathway and miRNA machinery in cancer. DNA Repair66–67, 30–41 (2018).
   PubMed Web of Science ®Google Scholar
• Kefas B , ComeauL , FloydDHet al. The neuronal microRNA miR-326 acts in a feedback loop with notch and has therapeutic potential against brain tumors. J. Neurosci.29(48), 15161–15168 (2009).
   PubMed Web of Science ®Google Scholar
• Xing CG , ZhuBS , FanXQet al. Effects of LY294002 on the invasiveness of human gastric cancer in vivo in nude mice. World J. Gastroenterol.15(40), 5044–5052 (2009).
   PubMed Web of Science ®Google Scholar
• Song G , ZhangY , WangL. MicroRNA-206 targets notch3, activates apoptosis, and inhibits tumor cell migration and focus formation. J. Biol. Chem.284(46), 31921–31927 (2009).
   PubMed Web of Science ®Google Scholar
• Cai H , YaoJ , AnYet al. lncRNA HOTAIR acts as competing endogenous RNA to control the expression of Notch3 via sponging miR-613 in pancreatic cancer. Oncotarget8(20), 32905 (2017).
   PubMedGoogle Scholar
• Raveh E , MatoukIJ , GilonM , HochbergA. The H19 long non-coding RNA in cancer initiation, progression and metastasis – a proposed unifying theory. Mol. Cancer14(1), 184 (2015).
   PubMedGoogle Scholar
• Zhang K , HanX , ZhangZet al. The liver-enriched lnc-LFAR1 promotes liver fibrosis by activating TGFβ and Notch pathways. Nat. Commun.8(1), 144 (2017).
   PubMedGoogle Scholar
• Kong D , WangY. Retracted: knockdown of lncRNA HULC inhibits proliferation, migration, invasion, and promotes apoptosis by sponging miR-122 in osteosarcoma. J. Cell. Biochem.119(1), 1050–1061 (2018).
   PubMed Web of Science ®Google Scholar
• Lee M , KimHJ , KimSWet al. The long non-coding RNA HOTAIR increases tumour growth and invasion in cervical cancer by targeting the Notch pathway. Oncotarget7(28), 44558–44571 (2016).
   PubMedGoogle Scholar
• Rani N , NowakowskiTJ , ZhouHet al. A primate lncRNA mediates notch signaling during neuronal development by sequestering miRNA. Neuron90(6), 1174–1188 (2016).
   PubMed Web of Science ®Google Scholar
• Ohtsuka M , LingH , IvanCet al. H19 noncoding RNA, an independent prognostic factor, regulates essential Rb-E2F and CDK8-beta-catenin signaling in colorectal cancer. EBioMedicine13, 113–124 (2016).
   PubMed Web of Science ®Google Scholar
• Durinck K , WallaertA , VanDe Walle Iet al. The Notch driven long non-coding RNA repertoire in T-cell acute lymphoblastic leukemia. Haematologica99(12), 1808–1816 (2014).
   PubMed Web of Science ®Google Scholar
• Katsushima K , NatsumeA , OhkaFet al. Targeting the Notch-regulated non-coding RNA TUG1 for glioma treatment. Nat. Commun.7, 13616 (2016).
   PubMed Web of Science ®Google Scholar
• Ounzain S , MichelettiR , ArnanCet al. CARMEN, a human super enhancer-associated long noncoding RNA controlling cardiac specification, differentiation and homeostasis. J. Mol. Cell. Cardiol.89(Pt A), 98–112 (2015).
   PubMedGoogle Scholar
• Ebbesen KK , KjemsJ , HansenTB. Circular RNAs: identification, biogenesis and function. Biochim. Biophys. Acta1859(1), 163–168 (2016).
   PubMed Web of Science ®Google Scholar
• Ntziachristos P , LimJS , SageJ , AifantisI. From fly wings to targeted cancer therapies: a centennial for notch signaling. Cancer Cell25(3), 318–334 (2014).
   PubMed Web of Science ®Google Scholar
• Olsauskas-Kuprys R , ZlobinA , OsipoC. Gamma secretase inhibitors of Notch signaling. Onco Targets Ther.6, 943–955 (2013).
   PubMed Web of Science ®Google Scholar
• Clarke EE , ChurcherI , EllisSet al. Intra- or intercomplex binding to the gamma-secretase enzyme. A model to differentiate inhibitor classes. J. Biol. Chem.281(42), 31279–31289 (2006).
   PubMed Web of Science ®Google Scholar
• Kummar S , O’SullivanCoyne G , DoKTet al. Clinical activity of the gamma-secretase inhibitor PF-03084014 in adults with desmoid tumors (aggressive fibromatosis). J. Clin. Oncol.35(14), 1561–1569 (2017).
   PubMed Web of Science ®Google Scholar
• Wei P , WallsM , QiuMet al. Evaluation of selective γ-secretase inhibitor PF-03084014 for its antitumor efficacy and gastrointestinal safety to guide optimal clinical trial design. Mol. Cancer Ther.9(6), 1618–1628 (2010).
   PubMed Web of Science ®Google Scholar
• Takebe N , NguyenD , YangSX. Targeting notch signaling pathway in cancer: clinical development advances and challenges. Pharmacol. Ther.141(2), 140–149 (2014).
   PubMed Web of Science ®Google Scholar
• Huynh C , PolisenoL , SeguraMFet al. The novel gamma secretase inhibitor RO4929097 reduces the tumor initiating potential of melanoma. PLOS ONE6(9), e25264 (2011).
   PubMed Web of Science ®Google Scholar
• Zhang C , QinS , XieHet al. RO4929097, a selective γ-secretase inhibitor, inhibits subretinal fibrosis via suppressing Notch and ERK1/2 signaling in laser-induced mouse model. Invest. Ophthalmol. Vis. Sci.63(10), 14 (2022).
   Web of Science ®Google Scholar
• Ryeom SW . The cautionary tale of side effects of chronic Notch1 inhibition. J. Clin. Invest.121(2), 508–509 (2011).
   PubMed Web of Science ®Google Scholar
• Wu Y , Cain-HomC , ChoyLet al. Therapeutic antibody targeting of individual Notch receptors. Nature464(7291), 1052–1057 (2010).
   PubMed Web of Science ®Google Scholar
• Zheng X , PangB , GuGet al. Melatonin inhibits glioblastoma stem-like cells through suppression of EZH2-NOTCH1 signaling axis. Int. J. Biol. Sci.13(2), 245–253 (2017).
   PubMed Web of Science ®Google Scholar
• Palermo R , ChecquoloS , GiovencoAet al. Acetylation controls Notch3 stability and function in T-cell leukemia. Oncogene31(33), 3807–3817 (2012).
   PubMed Web of Science ®Google Scholar
• Mohammed TA , HolenKD , Jaskula-SztulRet al. A pilot phase II study of valproic acid for treatment of low-grade neuroendocrine carcinoma. Oncologist16(6), 835–843 (2011).
   PubMed Web of Science ®Google Scholar
• Stockhausen MT , SjolundJ , ManetopoulosC , AxelsonH. Effects of the histone deacetylase inhibitor valproic acid on Notch signalling in human neuroblastoma cells. Br. J. Cancer92(4), 751–759 (2005).
   PubMed Web of Science ®Google Scholar
• A Sun L , HeQ , TsaiCet al. HDAC inhibitors suppressed small cell lung cancer cell growth and enhanced the suppressive effects of receptor-targeting cytotoxins via upregulating somatostatin receptor II. Am. J. Transl. Res.10(2), 545–553 (2018).
   PubMed Web of Science ®Google Scholar
• Tsai C , LeslieJS , Franko-TobinLGet al. Valproic acid suppresses cervical cancer tumor progression possibly via activating Notch1 signaling and enhances receptor-targeted cancer chemotherapeutic via activating somatostatin receptor type II. Arch. Gynecol. Obstet.288(2), 393–400 (2013).
   PubMed Web of Science ®Google Scholar
• Franko-Tobin LG , MackeyLV , HuangWet al. Notch1-mediated tumor suppression in cervical cancer with the involvement of SST signaling and its application in enhanced SSTR-targeted therapeutics. Oncologist17(2), 220–232 (2012).
   PubMed Web of Science ®Google Scholar
• Sen P , GhoshSS. γ-Secretase inhibitor potentiates the activity of suberoylanilide hydroxamic acid by inhibiting its ability to induce epithelial to mesenchymal transition and stemness via Notch pathway activation in triple-negative breast cancer cells. ACS Pharmacol. Transl. Sci.6(10), 1396–1415 (2023).
   PubMedGoogle Scholar
• Butler LM , AgusDB , ScherHIet al. Suberoylanilide hydroxamic acid, an inhibitor of histone deacetylase, suppresses the growth of prostate cancer cells in vitro and in vivo. Cancer Res.60(18), 5165–5170 (2000).
   PubMed Web of Science ®Google Scholar
• Vigushin DM , AliS , PacePEet al. Trichostatin A is a histone deacetylase inhibitor with potent antitumor activity against breast cancer in vivo. Clin. Cancer Res.7(4), 971–976 (2001).
   PubMed Web of Science ®Google Scholar
• Hu W , LuC , DongHHet al. Biological roles of the Delta family Notch ligand Dll4 in tumor and endothelial cells in ovarian cancer. Cancer Res.71(18), 6030–6039 (2011).
   PubMed Web of Science ®Google Scholar
• Liu Q , ZhengJM , ChenJKet al. Histone deacetylase 5 promotes the proliferation of glioma cells by upregulation of Notch 1. Mol. Med. Rep.10(4), 2045–2050 (2014).
   PubMed Web of Science ®Google Scholar
• Pandya K , MeekeK , ClementzAGet al. Targeting both Notch and ErbB-2 signalling pathways is required for prevention of ErbB-2-positive breast tumour recurrence. Br. J. Cancer105(6), 796–806 (2011).
   PubMed Web of Science ®Google Scholar
• Farnie G , WillanPM , ClarkeRB , BundredNJ. Combined inhibition of ErbB1/2 and Notch receptors effectively targets breast ductal carcinoma in situ (DCIS) stem/progenitor cell activity regardless of ErbB2 status. PLOS ONE8(2), e56840 (2013).
   PubMed Web of Science ®Google Scholar
• Ma Y , RenY , HanEQet al. Inhibition of the Wnt–beta-catenin and Notch signaling pathways sensitizes osteosarcoma cells to chemotherapy. Biochem. Biophys. Res. Commun.431(2), 274–279 (2013).
   PubMed Web of Science ®Google Scholar
• Jin R , NakadaM , TengLet al. Combination therapy using Notch and Akt inhibitors is effective for suppressing invasion but not proliferation in glioma cells. Neurosci. Lett.534, 316–321 (2013).
   PubMed Web of Science ®Google Scholar
• Shepherd C , BanerjeeL , CheungCWet al. PI3K/mTOR inhibition upregulates NOTCH-MYC signalling leading to an impaired cytotoxic response. Leukemia27(3), 650–660 (2013).
   PubMed Web of Science ®Google Scholar
• Yao J , QianC , ShuT , ZhangX , ZhaoZ , LiangY. Combination treatment of PD98059 and DAPT in gastric cancer through induction of apoptosis and downregulation of WNT/beta-catenin. Cancer Biol. Ther.14(9), 833–839 (2013).
   PubMed Web of Science ®Google Scholar
• Doody RS , RamanR , FarlowMet al. A phase 3 trial of semagacestat for treatment of Alzheimer’s disease. N. Engl. J. Med.369(4), 341–350 (2013).
   PubMed Web of Science ®Google Scholar
• Siemers ER , QuinnJF , KayeJet al. Effects of a gamma-secretase inhibitor in a randomized study of patients with Alzheimer disease. Neurology66(4), 602–604 (2006).
   PubMed Web of Science ®Google Scholar
• Fleisher AS , RamanR , SiemersERet al. Phase 2 safety trial targeting amyloid beta production with a gamma-secretase inhibitor in Alzheimer disease. Arch. Neurol.65(8), 1031–1038 (2008).
   PubMedGoogle Scholar
• Mandasari M , SawangarunW , KatsubeK , KayamoriK , YamaguchiA , SakamotoK. A facile one-step strategy for the generation of conditional knockout mice to explore the role of Notch1 in oroesophageal tumorigenesis. Biochem. Biophys. Res. Commun.469(3), 761–767 (2016).
   PubMed Web of Science ®Google Scholar
• Han N , HuG , ShiLet al. Notch1 ablation radiosensitizes glioblastoma cells. Oncotarget8(50), 88059–88068 (2017).
   PubMedGoogle Scholar
• Huo L , WeiW , WuSet al. Effect of dihydroarteminin combined with siRNA targeting Notch1 on Notch1/c-Myc signaling in T-cell lymphoma cells. Exp. Ther. Med.15(3), 3059–3065 (2018).
   PubMed Web of Science ®Google Scholar
• Yamaguchi N , OyamaT , ItoEet al. NOTCH3 signaling pathway plays crucial roles in the proliferation of ErbB2-negative human breast cancer cells. Cancer Res.68(6), 1881–1888 (2008).
   PubMed Web of Science ®Google Scholar
• Lewis NA , KleinRH , KellyC , YeeJ , KnoepflerPS. Histone H3.3 K27M chromatin functions implicate a network of neurodevelopmental factors including ASCL1 and NEUROD1 in DIPG. Epigenetics Chromatin15(1), 18 (2022).
   PubMed Web of Science ®Google Scholar