456
Views
1
CrossRef citations to date
0
Altmetric
Review

CRISPR-Mediated Modification of DNA Methylation Pattern in the New Era of cancer therapy

ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon & ORCID Icon
Pages 1845-1859 | Received 18 Mar 2020, Accepted 11 Sep 2020, Published online: 13 Nov 2020

References

  • Abdollahpour-Alitappeh M , HashemiKarouei SM , LotfiniaM , AmanzadehA , Habibi-AnbouhiM. A developed antibody-drug conjugate rituximab-vcMMAE shows a potent cytotoxic activity against CD20-positive cell line. Artif. Cells. Nanomed. Biotechnol.46(Suppl. 2), 1–8 (2018).
  • Azad M , KavianiS , NoruziniaMet al. Gene expression status and methylation pattern in promoter of P15INK4b and P16INK4a in cord blood CD34+ stem cells. IJBC16(7), 822 (2013).
  • Vogelstein B , PapadopoulosN , VelculescuVE , ZhouS , DiazLA , KinzlerKW. Cancer genome landscapes. Science339(6127), 1546–1558 (2013).
  • Jones PA , IssaJ , BaylinS. Targeting the cancer epigenome for therapy. Nat. Rev. Genet.17(10), 630–641 (2016).
  • Zhang Z-M , LuR , WangPet al. Structural basis for DNMT3A-mediated de novo DNA methylation. Nature554(7692), 387–391 (2018).
  • Ho L , JothiR , RonanJ , CuiK , ZhaoK , CrabtreeG. An embryonic stem cell chromatin remodeling complex, esBAF, is an essential component of the core pluripotency transcriptional network. Proc. Natl. Acad. Sci. U. S. A.106(13), 5187–5191 (2009).
  • Zeng W , BallARJr , YokomoriK. HP1: Heterochromatin binding proteins working the genome. Epigenetics5(4), 287–292 (2010).
  • Wakefield R , SmithB , NanXet al. The solution structure of the domain from MeCP2 that binds to methylated DNA. J. Mol. Biol.291(5), 1055–1065 (1999).
  • Chetverina D , FujiokaM , ErokhinM , GeorgievP , JaynesJB , SchedlP. Boundaries of loop domains (insulators): determinants of chromosome form and function in multicellular eukaryotes. Bioessays39(3), 1600233 (2017).
  • Hanssen LL , KassoufMT , OudelaarAMet al. Tissue-specific CTCF-cohesin-mediated chromatin architecture delimits enhancer interactions and function in vivo. Nat. Cell Biol.19(8), 952–961 (2017).
  • Viré E , BrennerC , DeplusRet al. The Polycomb group protein EZH2 directly controls DNA methylation. Nature439(7078), 871–874 (2006).
  • Ito S , LiS , DaiQet al. Tet Proteins Can Convert 5Methylcytosine to 5-Formylcytosine and 5-Carboxylcytosine. Science333(6047), 1300–1303 (2011).
  • Gagné ML , BoulayK , TopisirovicI , HuotMÉ , MalletteFA. Oncogenic activities of IDH1/2 mutations: from epigenetics to cellular signaling. Trends Cell. Biol.27(10), 738–752 (2017).
  • Zhou X , ZhuangZ , WangWet al. OGG1 is essential in oxidative stress induced DNA demethylation. Cell. Signal28(9), 1163–1171 (2016).
  • He Y , LiB , LiZet al. TetMediated formation of 5carboxylcytosine and its excision by TDG in mammalian DNA. Science333(6047), 1303–1307 (2011).
  • Conticello SG , ThomasCJ , Petersen-MahrtSK , NeubergerMS. Evolution of the AID/APOBEC family of polynucleotide (deoxy)cytidine deaminases. Mol. Biol. Evol.22(2), 367–377 (2005).
  • Ghorban K , ShanakiM , MobarraNet al. Apolipoproteins A1, B, and other prognostic biochemical cardiovascular risk factors in patients with beta-thalassemia major. Hematology21(2), 113–120 (2016).
  • Shi Y , WhetstineJ. Dynamic regulation of histone lysine methylation by demethylases. Mol. Cell.1–14 (2007).
  • Ciccone D . KDM1B is a histone H3K4 demethylase required to establish maternal genomic imprints. Nature461(7262), 415–418 (2009).
  • Wissmann M . Cooperative demethylation by JMJD2C and LSD1 promotes androgen receptordependent gene expression. Nat. Cell Biol.9(3), 347–353 (2007).
  • Sun XJ , ManN , TanY , NimerSD , WangL. The role of histone acetyltransferases in normal and malignant hematopoiesis. Front. Oncol.5, 108 (2015).
  • Sanchez R , ZhouM. The role of human bromodomains in chromatin biology and gene transcription. Curr. Opin. Drug Discov Devel.12(5), 659–665 (2009).
  • Seto E , YoshidaM. Erasers of histone acetylation: the histone deacetylase enzymes. Cold Spring Harb. Perspect. Biol.6(4), a018713 (2014).
  • Marot D , OpolonP , Brailly-TabardSet al. The tumor suppressor activity induced by adenovirus-mediated BRCA1 overexpression is not restricted to breast cancers. Gene. Ther.13(3), 235–244 (2006).
  • Esteller M . Epigenetics in Biology and Medicine. CRC pressFL, USA (2008).
  • Hoseini M , SahmaniM , ForoughiF , KhazaeiMonfared Y , AzadM. Evaluating the role of PTEN promoter methylation in patients predisposed to hypercoagulable states via methylation specific PCR. Rep. Biochem. Mol. Biol.7(2), 223–229 (2019).
  • Esteller M . Cancer epigenomics: DNA methylomes and histone-modification maps. Nature8(4), 286–298 (2007).
  • Hanada M , DeliaD , AielloA , StadtmauerE , ReedJC. bcl-2 Gene hypomethylation and high-level expression in B-cell chronic lymphocytic leukemia. Blood82(6), 1820–1828 (1993).
  • Nishigaki M , AoyagiK , DanjohIet al. Discovery of aberrant expression of R-RAS by cancer-linked DNA hypomethylation in gastric cancer using microarrays. Cancer Res.65(6), 2115–2124 (2005).
  • Hou HA , KuoYY , LiuCYet al. DNMT3A mutations in acute myeloid leukemia: stability during disease evolution and clinical implications. Blood119(2), 559–568 (2012).
  • Yamashita Y , YuanJ , SuetakeIet al. Array-based genomic resequencing of human leukemia. Oncogene29(25), 3723–3731 (2010).
  • Steensma DP , BejarR , JaiswalSet al. Clonal hematopoiesis of indeterminate potential and its distinction from myelodysplastic syndromes. Blood126(1), 9–16 (2015).
  • Rahmani T , AzadM , ChahardouliB , NasiriH , VatanmakanianM , KavianiS. Patterns of DNMT1 promoter methylation in patients with acute lymphoblastic leukemia. Int. J. Hematol. Oncol. Stem Cell. Res.11(3), 172–177 (2017).
  • Marcais A , WaastL , BruneauJet al. Adult T cell leukemia aggressivenness correlates with loss of both 5-hydroxymethylcytosine and TET2 expression. Oncotarget8(32), 52256–52268 (2017).
  • Bodor C , GrossmannV , PopovNet al. EZH2 mutations are frequent and represent an early event in follicular lymphoma. blood122(18), 3165–3168 (2013).
  • Dang L , JinS , SuS. IDH mutations in glioma and acute myeloid leukemia. Trends Mol. Med.16(9), 387–397 (2010).
  • Ghiam A , CairnsR , ThomsJet al. IDH mutation status in prostate cancer. Oncogene31(33), 3826 (2011).
  • Kipp B , VossJ , KerrSet al. Isocitrate dehydrogenase 1 and 2 mutations in cholangiocarcinoma. Hum. Pathol.43(10), 1552–1558 (2012).
  • Ropero S , EstellerM. The role of histone deacetylases (HDACs) in human cancer. Mol. Oncol.1(1), 19–25 (2007).
  • Jiang Y , Ortega-MolinaA , GengHet al. CREBBP inactivation promotes the development of HDAC3-dependent lymphomas. Cancer Disc.7(1), 38–53 (2016).
  • Shain A , PollackJ. The spectrum of SWI/SNF mutations, ubiquitous in human cancers. PLoS One.8(1), e55119 (2013).
  • Kadoch C , HargreavesD , HodgesCet al. Proteomic and bioinformatic analysis of mammalian SWI/SNF complexes identifies extensive roles in human malignancy. Nat. Genet.45, 592–601 (2013).
  • Rebhandl S , HuemerM , GreilR , GeisbergerR. AID/APOBEC deaminases and cancer. Oncoscience2(4), 320–333 (2015).
  • Sahmani M , VatanmakanianM , GoudarziM , MobarraN , AzadM. Microchips and their significance in isolation of circulating tumor cells and monitoring of cancers. Asian. Pac. J. Cancer Prev.17(3), 879–894 (2016).
  • Yaghoubi S , KarimiMH , LotfiniaMet al. Potential drugs used in the antibody-drug conjugate (ADC) architecture for cancer therapy. J. Cell. Physiol.235(1), 31–64 (2020).
  • Yaghoubi S , NajminejadH , DabaghianMet al. How hypoxia regulate exosomes in ischemic diseases and cancer microenvironment? IUBMB Life 72(7), 1286–1305 (2020).
  • Xiong X , ChenM , LimWA , ZhaoD , QiLS. CRISPR/Cas9 for human genome engineering and disease research. Annu. Rev. Genomics Hum. Genet.17, 131–154 (2016).
  • Fu Y , SanderJD , ReyonD , CascioVM , JoungJK. Improving CRISPR-Cas nuclease specificity using truncated guide RNAs. Nat. Biotechnol.32(3), 279–284 (2014).
  • Barrangou R , FremauxC , DeveauHet al. CRISPR provides acquired resistance against viruses in prokaryotes. Science315(5819), 1709–1712 (2007).
  • Komor AC , BadranAH , LiuDR. CRISPR-based technologies for the manipulation of eukaryotic genomes. Cell168(1–2), 20–36 (2017).
  • Gasiunas G , BarrangouR , HorvathP , SiksnysV. Cas9-crRNA ribonucleoprotein complex mediates specific DNA cleavage for adaptive immunity in bacteria. Proc. Natl Acad. Sci.109(39), 2579–2586 (2012).
  • Bibikova M , CarrollD , SegalDJet al. Stimulation of homologous recombination through targeted cleavage by chimeric nucleases. Mol. Cell. Biol.21(1), 289–297 (2001).
  • Cong L , RanFA , CoxDet al. Multiplex genome engineering using CRISPR/Cas systems. Science339(6121), 819–823 (2013).
  • Makarova KS , HaftDH , BarrangouRet al. Evolution and classification of the CRISPR-Cas systems. Nat. Rev. Microbiol.9(6), 467–477 (2011).
  • Konermann S , BrighamMD , TrevinoAEet al. Genome-scale transcriptional activation by an engineered CRISPR-Cas9 complex. Nature517(7536), 583–588 (2015).
  • Kampmann M . CRISPRi and CRISPRa screens in mammalian cells for precision biology and medicine. ACS Chem. Biol.13(2), 406–416 (2017).
  • He ZY , ZhangYG , YangYHet al. In vivo ovarian cancer gene therapy using CRISPR-Cas9. Hum. Gene Ther.29(2), 223–233 (2018).
  • Xiaoshu X , LeiSQ. A CRISPR-dCas9 toolbox for genetic engineering and synthetic biology. J. Mol. Biol.431(1), 34–47 (2019).
  • Mcdonald JI , CelikH , RoisLEet al. Reprogrammable CRISPR/Cas9-based system for inducing site specific DNA methylation. Biology5(6), 866–874 (2016).
  • Vojta A , DobrinicP , TadicVet al. Repurposing the CRISPR-Cas9 system for targeted DNA methylation. Nucleic Acids Res.44(12), 5615–5628 (2016).
  • Stepper P , KungulovskiG , JurkowskaRZet al. Efficient targeted DNA methylation with chimeric dCas9-Dnmt3a-Dnmt3L methyltransferase. Nucleic Acids Res.45(4), 1703–1713 (2017).
  • Amabile A , MigliaraA , CapassoPet al. Inheritable silencing of endogenous genes by hit-and-run targeted epigenetic editing. Cell167(1), 219–232 (2016).
  • Liua Y , MaaS , ChangaJet al. Programmable targeted epigenetic editing using CRISPR system in Bombyx mori. Insect Biochem. Mol. Biol.110, 105–111 (2019).
  • Choudhury SR , CuiY , LubeckaK , StefanskaB , IrudayarajJ. CRISPR-dCas9 mediated TET1 targeting for selective DNA demethylation at BRCA1 promoter. Oncotarget7(29), 46545–46556 (2016).
  • Xu X , TaoY , GaoXet al. CRISPR-based approach for targeted DNA demethylation. Cell Discov.2, 16009 (2016).
  • Braun S , KirklandJ , ChoryE , HusmannD , CalarcoJ , CrabtreeG. Rapid and reversible epigenome editing by endogenous chromatin regulators. Nat. Commun.8(1), 1–8 (2017).
  • Morita S , NoguchiH , HoriiTet al. Targeted DNA demethylation in vivo using dCas9-peptide repeat and scFv-TET1 catalytic domain fusions. Nat. Biotechnol.34(10), 1060–1065 (2016).
  • Gregory DJ , ZhangY , KobzikL , FedulovAV. Specific transcriptional enhancement of inducible nitric oxide synthase by targeted promoter demethylation. Epigenetics8(11), 1205–1212 (2013).
  • Hilton IB , D’ippolitoAM , VockleyCMet al. Epigenome editing by a CRISPR-Cas9-based acetyltransferase activates genes from promoters and enhancers. Nat. Biotechnol.33(5), 510–517 (2015).
  • Kwon DY , ZhaoY-T , LamonicaJM , ZhouZ. Locus-specific histone deacetylation using a synthetic CRISPR-Cas9-based HDAC. Nature8(1), 1–8 (2017).
  • O’geen H , BatesSL , CarterSSet al. Ezh2-dCas9 and KRAB-dCas9 enable engineering of epigenetic memory in a context-dependent manner. Epigenetics Chromatin12(1), 26 (2019).
  • Yeo N , ChavezA , Lance-ByrneAet al. An enhanced CRISPR repressor for targeted mammalian gene regulation. Nat. Methods15(8), 611–616 (2018).
  • Kearns NA , PhamH , TabaketalB. Functional annotation of native enhancers with a Cas9–histone demethylase fusion. Nat. Methods12(5), 401–403 (2015).
  • Parrilla-Doblas JT , ArizaRR , Roldán-ArjonaT. Targeted DNA demethylation in human cells by fusion of a plant 5-methylcytosine DNA glycosylase to a sequence-specific DNA binding domain. Epigenetics12(4), 296–303 (2017).
  • Blanas A , CornelissenLaM , KotsiasMet al. Transcriptional activation of fucosyltransferase (FUT) genes using the CRISPR-dCas9-VPR technology reveals potent N-glycome alterations in colorectal cancer cells. Glycobiology29(2), 137–150 (2019).
  • Tanenbaum ME , GilbertLA , QiLS , WeissmanJS , RDV. A protein-tagging system for signal amplification in gene expression and fluorescence imaging. Cell159(3), 635–646 (2014).
  • Huang YH , SuJ , LeiYet al. DNA epigenome editing using CRISPR-Cas SunTag-directed DNMT3A. Genome Biol.18(1), 176 (2017).
  • Lei Y , ZhangX , SuJet al. Targeted DNA methylation in vivo using an engineered dCas9-MQ1 fusion protein. Nat. Commun.8(1), 1–10 (2017).
  • Xiong T , MeisterGE , WorkmanREet al. Targeted DNA methylation in human cells using engineered dCas9-methyltransferases. Sci. Rep.7(1), 1–14 (2017).
  • Lu A , WangJ , SunWet al. Reprogrammable CRISPR/dCas9-based recruitmentof DNMT1for site-specificDNA demethylation and gene regulation. Cell Discov.5(1), 1–4 (2019).
  • Morgan SL , MarianoNCA , BermudezBet al. Manipulation of nuclear architecture through CRISPR-mediated chromosomal looping. Nat. Commun.8(1), 1–9 (2017).
  • Wang H , XuX , NguyenCM , KipnissNH , RussaML , QiLS. CRISPR-mediated programmable 3D genome positioning and nuclear organization. Cell175, 1405–1417 (2018).
  • Qi LS , LarsonMH , GilbertLAet al. Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression. Cell152(5), 1173–1183 (2013).
  • Gilbert LA , LarsonMH , MorsutLet al. CRISPR-mediated modular RNA-guided regulation of transcription in eukaryotes. Cell154(2), 442–451 (2013).
  • Chavez A , ScheimanJ , VoraSet al. Highly efficient Cas9-mediated transcriptional programming. Nat. Methods12(4), 326–328 (2015).
  • Konermann S , AlE. Genome-scale transcriptional activation by an engineered CRISPR-Cas9 complex. Nature517(7536), 583–588 (2015).
  • Xu X , QiLS. A CRISPR–dCas Toolbox for genetic engineering and synthetic biology. J. Mol. Biol.431(1), 34–47 (2018).
  • Kunii A , HaraY , TakenagaMet al. Three-component repurposed technology for enhanced expression: highly accumulable transcriptional activators via branched tag arrays. CRISPR J.1(5), 337–347 (2018).
  • Chen T , GaoD , ZhangRet al. Chemically controlled epigenome editing through an inducible dCas9 system. J. Am. Chem. Soc.139(33), 11337–11340 (2017).
  • Nihongaki Y , YamamotoS , KawanoF , SuzukiH , SatoM. CRISPR-Cas9-based photoactivatable transcription system. Chem. Biol.22(2), 169–174 (2015).
  • Nguyen DP , MiyaokaY , GilbertLAet al. Ligand-binding domains of nuclear receptors facilitate tight control of split CRISPR activity. Nat. Commun.7(1), 1–10 (2016).
  • Schwarz KA , DaringerNM , DolbergTB , LeonardJN. Rewiring human cellular input–output using modular extracellular sensors. Nat. Chem. Biol.13(2), 202–209 (2017).
  • Guo Y , XuQ , CanzioDet al. CRISPR inversion of CTCF Sites alters genome topology and enhancer/promoter function. Cell162(4), 900–910 (2015).
  • Okada M , KanamoriM , SomeyaK , NakatsukasaH , YoshimuraA. Stabilization of Foxp3 expression by CRISPR-dCas9-based epigenome editing in mouse primary T cells. Epigenetics Chromatin10(1), 24 (2017).
  • Moses C , NugentF , WaryahCB , Garcia-BlojB , HarveyAR , BlancafortP. Activating PTEN tumor suppressor expression with the CRISPR/dCas9 system. Mol. Ther. Nucleic Acids.14, 287–300 (2019).
  • Wu J , HeK , ZhangYet al. Inactivation of SMARCA2 by promoter hypermethylation drives lung cancer development. Gene687, 193–199 (2019).
  • Dehghanifard A , KavianiS , AbrounSet al. Various signaling pathways in multiple myeloma cells and effects of treatment on these pathways. Clin. Lymphoma. Myeloma. Leuk.18(5), 311–320 (2018).
  • Kim V , MearsBM , PowellBH , WitwerKW. Mutant Cas9-transcriptional activator activates HIV-1 in U1 cells in the presence and absence of LTR-specific guide RNAs. Matters (Zur) doi:10.19185/matters.201611000027 (2017).
  • Roy B , ZhaoJ , YangCet al. CRISPR/cascade9-mediated genome editing challenges and opportunities. Front. Genet.9, 240 (2018).
  • Lee CM , CradickTJ , FineEJ , BaoG. Nuclease target site selection for maximizing on-target activity and minimizing off-target effects in genome editing. Mol. Ther.24(3), 475–487 (2016).
  • Zischewski J , FischerR , BortesiL. Detectionofon-target and off target mutations generated by CRISPR/Cas9 and other sequence-specific nucleases. Biotechnol. Adv.35(1), 95–104 (2017).
  • Gupta RM , MusunuruK. Expanding the genetic editing tool kit: ZFNs, TALENs, and CRISPR-Cas9. J. Clin. Invest.124(10), 4154–4161 (2014).
  • Ran FA , HsuPD , LinCYet al. Double nicking by RNA guided CRISPR cas9 for enhanced genome editing specificity. Cell154(6), 1380–1389 (2013).
  • Kleinstiver BP , PattanayakV , PrewMSet al. High-fidelity CRISPR-Cas9 nucleases with no detectable genome-wide off-target effects. Nature529(7587), 490–495 (2016).
  • Tsai SQ , WyvekensN , KhayterCet al. Dimeric CRISPR RNA-guided FokI nucleases for highly specific genome editing. Nat. Biotechnol.32(6), 569–576 (2014).
  • Zetsche B , GootenbergJS , AbudayyehOOet al. Cpf1 is a single RNA-guided endonuclease of a class 2 CRISPR-Cas system. Cell163(3), 759–771 (2015).
  • Shen CC , HsuMN , ChangCWet al. Synthetic switch to minimize CRISPR off-target effects by self-restricting Cas9 transcription and translation. Nucleic Acids Res.47(3), e13 (2018).
  • Maruyama T , DouganSK , TruttmannMC , BilateAM , IngramJR , PloeghHL. Increasing the efficiency of precise genome editing with CRISPR-Cas9 by inhibition of nonhomologous end joining. Nat. Biotechnol.33(5), 538–542 (2015).
  • Cox DBT , GootenbergJS , AbudayyehOOet al. RNA editing with CRISPR-Cas13. Science358(6366), 1019–1027 (2017).
  • Liu C , ZhangL , LiuH , ChengK. Delivery strategies of the CRISPR-Cas9 gene editing system for therapeutic applications. J. Control.Release266, 17–26 (2017).
  • Ran FA , CongL , YanWXet al. In vivo genome editing using Staphylococcus aureus Cas9. Nature520(7546), 186–191 (2015).
  • Xue W , ChenS , YinHet al. CRISPR-mediated direct mutation of cancer genes in the mouse liver. Nature514(7522), 380–384 (2014).
  • Kotterman MA , SchafferDV. Engineering adeno-associated viruses for clinical gene therapy. Nat. Rev. Genet.15(7), 445–451 (2014).
  • Yin H , SongCQ , DorkinJRet al. Therapeutic genome editing by combined viral and non-viral delivery of CRISPR system components in vivo. Nat. Biotechnol.34(3), 328–333 (2016).
  • Lombardo A , GenoveseP , BeausejourCMet al. Gene editing in human stem cells using zinc finger nucleases and integrase-defective lentiviral vector delivery. Nat. Biotechnol.25(11), 1298–1306 (2007).
  • Maali A , AtashiA , GhaffariS , KouchakiR , AbdolmalekiF , AzadM. A review on leukemia and iPSC Technology: application in novel treatment and future. Curr. Stem Cell Res. Ther.13(8), 665–675 (2018).
  • Swiech L , HeidenreichM , BanerjeeAet al. In vivo interrogation of gene function in the mammalian brain using CRISPR Cas9. Nat. Biotechnol.33(1), 102–106 (2015).

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.