AccScience Publishing / ITPS / Online First / DOI: 10.36922/itps.3654
Submit to ITPS
Cite this article
218
Download
1419
Views
Journal Browser
Volume | Year
Issue
Search
Forthcoming Issue
Current Issue
View All
News and Announcements
View All
REVIEW

Enhancers and super-enhancers as master regulators in cancer

Pouya Sarvari1†* ,  Pourya Sarvari1† ,  Ivonne Ramirez-Diaz2 ,  Karla Rubio2
Show Less
1 Iran’s National Elite Foundation, Tehran, Iran
2 International Laboratory EPIGEN-CONCYTEP-BUAP; Puebla, Mexico
INNOSC Theranostics and Pharmacological Sciences 2024, 7(3), 3654 https://doi.org/10.36922/itps.3654
Submitted: 13 May 2024 | Accepted: 12 July 2024 | Published: 24 July 2024
© 2024 by the Author(s). This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution 4.0 International License ( https://creativecommons.org/licenses/by/4.0/ )
Download PDF
Cite
XML
Abstract

Gene expression regulation is one of the most fundamental cellular processes, enabling the activation of a gene to produce either the translatable protein-coding transcript (mRNA) or a functional non-coding RNA with gene regulatory functions, ultimately determining cell identity and function. Although gene expression regulation can occur at transcriptional, translational, and post-translational levels, transcription initiation is the first and the most important step in gene expression, facilitating the transfer of biological information from DNA to protein. Enhancers and super-enhancers are among the master regulators of tissue- and cell-specific transcription regulation involved in cell differentiation and tumor formation. Despite four decades passing since the first discovery of enhancers in eukaryotes and extensive efforts undertaken to identify enhancers on a genomic scale during the last decade, the discovery of enhancers still faces certain limitations and needs further investigation. The perturbation of enhancer function due to genetic or epigenetic changes is closely linked to a range of human disorders, including the development and progression of cancers. Thus, the detection of early cancer-related enhancer activity and the subsequent normalization of expression abnormalities using enhancer-targeting CRISPR epigenetic editing, as well as enhancer-targeting pharmaceuticals, are regarded as groundbreaking therapeutic tactics in preclinical stages.

Keywords
CRISPR
Epigenetic editing
Enhancer-promoter loop
Enhancer-targeting drugs
Non-coding transcript
Super-enhancers
Transcription
Funding
None.
Conflict of interest
The authors declare that they have no competing interests.
References
  1. Maston GA, Evans SK, Green MR. Transcriptional regulatory elements in the human genome. Annu Rev Genomics Hum Genet. 2006;7(1):29-59. doi: 10.1146/annurev.genom.7.080505.115623

 

  1. Kvon EZ, Waymack R, Gad M, Wunderlich Z. Enhancer redundancy in development and disease. Nat Rev Genet. 2021;22(5):324-336. doi: 10.1038/s41576-020-00311-x

 

  1. Vieira KF, Levings PP, Hill MA, et al. Recruitment of transcription complexes to the beta-globin gene locus in vivo and in vitro. J Biol Chem. 2004;279(48):50350-50357. doi: 10.1074/jbc.M408883200

 

  1. Rodriguez-Jato S, Nicholls RD, Driscoll DJ, Yang TP. Characterization of cis-and trans-acting elements in the imprinted human SNURF-SNRPN locus. Nucleic Acids Res. 2005;33(15):4740-4753. doi: 10.1093/nar/gki786

 

  1. Panigrahi A, O’Malley BW. Mechanisms of enhancer action: The known and the unknown. Genome Biol. 2021;22(1):108. doi: 10.1186/s13059-021-02322-1

 

  1. Tang F, Yang Z, Tan Y, Li Y. Super-enhancer function and its application in cancer targeted therapy. NPJ Precis Oncol. 2020;4(1):2. doi: 10.1038/s41698-020-0108-z

 

  1. Pott S, Lieb JD. What are super-enhancers? Nat Genet. 2015;47(1):8-12. doi: 10.1038/ng.3167

 

  1. Huang J, Li K, Cai W, et al. Dissecting super-enhancer hierarchy based on chromatin interactions. Nat Commun. 2018;9(1):943. doi: 10.1038/s41467-018-03279-9

 

  1. Beacon TH, Delcuve GP, López C, et al. The dynamic broad epigenetic (H3K4me3, H3K27ac) domain as a mark of essential genes. Clin Epigenetics. 2021;13:1-17. doi: 10.1186/s13148-021-01126-1

 

  1. Creyghton MP, Cheng AW, Welstead GG, et al. Histone H3K27ac separates active from poised enhancers and predicts developmental state. Proc Natl Acad Sci U S A. 2010;107(50):21931-21936. doi: 10.1073/pnas.1016071107

 

  1. Zentner GE, Tesar PJ, Scacheri PC. Epigenetic signatures distinguish multiple classes of enhancers with distinct cellular functions. Genome Res. 2011;21(8):1273-1283. doi: 10.1101/gr.122382.111

 

  1. Raisner R, Kharbanda S, Jin L, et al. Enhancer activity requires CBP/P300 bromodomain-dependent histone H3K27 acetylation. Cell Rep. 2018;24(7):1722-1729. doi: 10.1016/j.celrep.2018.07.041

 

  1. Durbin AD, Wang T, Wimalasena VK, et al. EP300 selectively controls the enhancer landscape of MYCN-amplified neuroblastoma. Cancer Discov. 2022;12(3):730-751. doi: 10.1158/2159-8290.CD-21-0385

 

  1. Rubio K, Singh I, Dobersch S, et al. Inactivation of nuclear histone deacetylases by EP300 disrupts the MiCEE complex in idiopathic pulmonary fibrosis. Nat Commun. 2019;10(1):2229. doi: 10.1038/s41467-019-10066-7

 

  1. Hah N, Benner C, Chong LW, Yu RT, Downes M, Evans RM. Inflammation-sensitive super enhancers form domains of coordinately regulated enhancer RNAs. Proc Natl Acad Sci U S A. 2015;112(3):E297-E302. doi: 10.1073/pnas.1424028112

 

  1. Kim TK, Hemberg M, Gray JM, et al. Widespread transcription at neuronal activity-regulated enhancers. Nature. 2010;465(7295):182-187. doi: 10.1038/nature09033

 

  1. De Santa F, Barozzi I, Mietton F, et al. A large fraction of extragenic RNA pol II transcription sites overlap enhancers. PLoS Biol. 2010;8(5):e1000384. doi: 10.1371/journal.pbio.1000384

 

  1. Djebali S, Davis CA, Merkel A, et al. Landscape of transcription in human cells. Nature. 2012; 489(7414):101-108. doi: 10.1038/nature11233

 

  1. Hasty P, Montagna C. Chromosomal rearrangements in cancer: Detection and potential causal mechanisms. Mol Cell Oncol. 2014;1(1):e29904. doi: 10.4161/mco.29904

 

  1. Harewood L, Fraser PJ. The impact of chromosomal rearrangements on regulation of gene expression. Hum Mol Genet. 2014;23(R1):R76-R82. doi: 10.1093/hmg/ddu278

 

  1. Alonso S, Dow LE. Engineering chromosome rearrangements in cancer. Dis Model Mech. 2021;14(9):dmm049078. doi: 10.1242/dmm.049078

 

  1. Willis NA, Rass E, Scully RJ. Deciphering the code of the cancer genome: Mechanisms of chromosome rearrangement. Trends Cancer. 2015;1(4):217-230. doi: 10.1016/j.trecan.2015.10.007

 

  1. Ryan RJ, Drier Y, Whitton H, et al. Detection of enhancer-associated rearrangements reveals mechanisms of oncogene dysregulation in B-cell lymphoma. Cancer Discov. 2015;5(10):1058-1071. doi: 10.1158/2159-8290.CD-15-0370

 

  1. Gröschel S, Sanders MA, Hoogenboezem R, et al. A single oncogenic enhancer rearrangement causes concomitant EVI1 and GATA2 deregulation in leukemia. Cell. 2014; 157(2):369-381. doi: 10.1016/j.cell.2014.02.019

 

  1. Kandaswamy R, Sava GP, Speedy HE, et al. Genetic predisposition to chronic lymphocytic leukemia is mediated by a BMF super-enhancer polymorphism. Cell Rep. 2016;16(8):2061-2067. doi: 10.1016/j.celrep.2016.07.053

 

  1. Bonev B, Cavalli G. Organization and function of the 3D genome. Nat Rev Genet. 2016;17(11):661-678. doi: 10.1038/nrg.2016.112

 

  1. Dixon JR, Selvaraj S, Yue F, et al. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature. 2012;485(7398):376-380. doi: 10.1038/nature11082

 

  1. Giorgio E, Robyr D, Spielmann M, et al. A large genomic deletion leads to enhancer adoption by the lamin B1 gene: A second path to autosomal dominant adult-onset demyelinating leukodystrophy (ADLD). Hum Mol Genet. 2015;24(11):3143-3154. doi: 10.1093/hmg/ddv065

 

  1. Lupiáñez DG, Kraft K, Heinrich V, et al. Disruptions of topological chromatin domains cause pathogenic rewiring of gene-enhancer interactions. Cell. 2015;161(5):1012-1025. doi: 10.1016/j.cell.2015.04.004

 

  1. Lupiáñez DG, Spielmann M, Mundlos S. Breaking TADs: How alterations of chromatin domains result in disease. Trends Genet. 2016;32(4):225-237. doi: 10.1016/j.tig.2016.01.003

 

  1. Akdemir KC, Le VT, Chandran S, et al. Disruption of chromatin folding domains by somatic genomic rearrangements in human cancer. Nat Genet. 2020;52(3):294-305. doi: 10.1038/s41588-019-0564-y

 

  1. Flavahan WA, Drier Y, Liau BB, et al. Insulator dysfunction and oncogene activation in IDH mutant gliomas. Nature. 2016;529(7584):110-114. doi: 10.1038/nature16490

 

  1. Ji X, Dadon DB, Powell BE, et al. 3D chromosome regulatory landscape of human pluripotent cells. Cell Stem Cell. 2016;18(2):262-275. doi: 10.1016/j.stem.2015.11.007

 

  1. Whyte WA, Orlando DA, Hnisz D, et al. Master transcription factors and mediator establish super-enhancers at key cell identity genes. Cell. 2013;153(2):307-319. doi: 10.1016/j.cell.2013.03.035

 

  1. Koutsi MA, Pouliou M, Champezou L, et al. Typical enhancers, super-enhancers, and cancers. Cancers (Basel). 2022;14(18):4375. doi: 10.3390/cancers14184375

 

  1. Yoshino S, Suzuki HI. The molecular understanding of super-enhancer dysregulation in cancer. Nagoya J Med Sci. 2022;84(2):216. doi: 10.18999/nagjms.84.2.216

 

  1. See YX, Chen K, Fullwood MJ. MYC overexpression leads to increased chromatin interactions at super-enhancers and MYC binding sites. Genome Res. 2022;32(4):629-642. doi: 10.1101/gr.276313.121

 

  1. Di Palma J. ERC cholecystography. J Clin Gastroenterol. 1988;10(1):117-118.

 

  1. Jia Y, Zhou J, Tan TK, et al. Super enhancer-mediated upregulation of HJURP promotes growth and survival of t (4; 14)-positive multiple myeloma. Cancer Res. 2022;82(3):406-418. doi: 10.1158/0008-5472.CAN-21-0921

 

  1. Kelly MR, Wisniewska K, Regner MJ, et al. A multi-omic dissection of super-enhancer driven oncogenic gene expression programs in ovarian cancer. Nat Commun. 2022; 13(1):4247. doi: 10.1038/s41467-022-31919-8

 

  1. Neumayr C, Haberle V, Serebreni L, et al. Differential cofactor dependencies define distinct types of human enhancers. Nature. 2022;606(7913):406-413. doi: 10.1038/s41586-022-04779-x

 

  1. Zhang J, Yue W, Zhou Y, Liao M, Chen X, Hua J. Super enhancers-functional cores under the 3D genome. Cell Prolif. 2021;54(2):e12970. doi: 10.1111/cpr.12970

 

  1. Benecke AG, Eilebrecht SJ. RNA-mediated regulation of HMGA1 function. Biomolecules. 2015;5(2):943-957. doi: 10.3390/biom5020943

 

  1. Yang Z, Yik JH, Chen R, et al. Recruitment of P-TEFb for stimulation of transcriptional elongation by the bromodomain protein Brd4. Mol Cell. 2005;19(4):535-545. doi: 10.1016/j.molcel.2005.06.029

 

  1. Dong J, Li J, Li Y, Ma Z, Yu Y, Wang CY. Transcriptional super-enhancers control cancer stemness and metastasis genes in squamous cell carcinoma. Nat Commun. 2021;12(1):3974. doi: 10.1038/s41467-021-24137-1

 

  1. Hnisz D, Shrinivas K, Young RA, Chakraborty AK, Sharp PA. A phase separation model for transcriptional control. Nat Commun. 2021;12(1):3974.

 

  1. Hnisz D, Abraham BJ, Lee TI, et al. Super-enhancers in the control of cell identity and disease. Cell. 2013;155(4):934-947. doi: 10.1016/j.cell.2013.09.053

 

  1. Holehouse AS, Pappu RV. Functional implications of intracellular phase transitions. Biochemistry. 2018; 57(17):2415-2423. doi: 10.1021/acs.biochem.7b01136

 

  1. Grosveld F, Van Staalduinen J, Stadhouders R. Transcriptional regulation by (super) enhancers: From discovery to mechanisms. Annu Rev Genomics Hum Genet. 2021;22(1):127-146. doi: 10.1146/annurev-genom-122220-093818

 

  1. Ryu K, Park G, Cho WK. Emerging insights into transcriptional condensates. Exp Mol Med. 2024;56:820-826. doi: 10.1038/s12276-024-01228-9

 

  1. Sabari BR, Dall’Agnese A, Boija A, et al. Coactivator condensation at super-enhancers links phase separation and gene control. Science. 2018;361(6400):eaar3958. doi: 10.1126/science.aar3958

 

  1. Cerne F. Hospitals not immune to high cost of stress. Hospitals. 1988;62(19):69-70.

 

  1. Bakshi S, McKee C, Walker K, Brown C, Chaudhry GR. Toxicity of JQ1 in neuronal derivatives of human umbilical cord mesenchymal stem cells. Oncotarget. 2018;9(73):33853-33864. doi: 10.18632%2Foncotarget.26127

 

  1. Mohammed Ismail W, Mazzone A, Ghiraldini FG, et al. MacroH2A histone variants modulate enhancer activity to repress oncogenic programs and cellular reprogramming. Commun Biol. 2023;6(1):215. doi: 10.1038/s42003-023-04571-1

 

  1. Fang MY, Markmiller S, Vu AQ, et al. Small-molecule modulation of TDP-43 recruitment to stress granules prevents persistent TDP-43 accumulation in ALS/FTD. Neuron. 2019;103(5):802-819.e11. doi: 10.1016/j.neuron.2019.05.048

 

  1. Napoli S, Munz N, Guidetti F, Bertoni FJ. Enhancer RNAs (eRNAs) in cancer: The jacks of all trades. Cancers. 2022;14(8):1978. doi: 10.3390/cancers14081978

 

  1. Olmedo-Suárez MÁ, Ramírez-Díaz I, Pérez-González A, et al. Epigenetic regulation in exposome-induced tumorigenesis: Emerging roles of ncRNAs. Biomolecules. 2022;12(4):513. doi: 10.3390/biom12040513

 

  1. Pérez-González A, Ramírez-Díaz I, Guzmán-Linares J, Sarvari P, Sarvari P, Rubio KJ. ncRNAs orchestrate chemosensitivity induction by neddylation blockades. Cancers (Basel). 2024;16(4):825. doi: 10.3390/cancers16040825

 

  1. Niderla-Bielińska J, Jankowska-Steifer E, Włodarski PJ. Non-coding RNAs and human diseases: Current status and future perspectives. Int J Mol Sci. 2023;24(14):11679. doi: 10.3390/ijms241411679

 

  1. Chen B, Dragomir MP, Yang C, et al. Targeting non-coding RNAs to overcome cancer therapy resistance. Signal Transduct Target Ther. 2022;7(1):121. doi: 10.1038/s41392-022-00975-3

 

  1. Andersson R, Gebhard C, Miguel-Escalada I, et al. An atlas of active enhancers across human cell types and tissues. Nature. 2014;507(7493):455-461. doi: 10.1038/nature12787

 

  1. Arner E, Daub CO, Vitting-Seerup K, et al. Transcribed enhancers lead waves of coordinated transcription in transitioning mammalian cells. Science. 2015; 347(6225):1010-1014. doi: 10.1126/science.1259418

 

  1. Pefanis E, Wang J, Rothschild G, et al. RNA exosome-regulated long non-coding RNA transcription controls super-enhancer activity. Cell. 2015;161(4):774-789. doi: 10.1016/j.cell.2015.04.034

 

  1. Schaukowitch K, Joo JY, Liu X, Watts JK, Martinez C, Kim TK. Enhancer RNA facilitates NELF release from immediate early genes. Mol Cell. 2014;56(1):29-42. doi: 10.1016/j.molcel.2014.08.023

 

  1. Onoguchi M, Hirabayashi Y, Koseki H, Gotoh Y. A noncoding RNA regulates the neurogenin1 gene locus during mouse neocortical development. Proc Natl Acad Sci U S A. 2012;109(42):16939-16944. doi: 10.1073/pnas.1202956109

 

  1. Lam MT, Li W, Rosenfeld MG, Glass CK. Enhancer RNAs and regulated transcriptional programs. Trends Biochem Sci. 2014;39(4):170-182. doi: 10.1016/j.tibs.2014.02.007

 

  1. Melo CA, Drost J, Wijchers PJ, et al. eRNAs are required for p53-dependent enhancer activity and gene transcription. Mol cell. 2013;49(3):524-535. doi: 10.1016/j.molcel.2012.11.021

 

  1. Mousavi K, Zare H, Dell’Orso S, et al. eRNAs promote transcription by establishing chromatin accessibility at defined genomic loci. Mol cell. 2013;51(5):606-617. doi: 10.1016/j.molcel.2013.07.022

 

  1. Lam MT, Cho H, Lesch HP, et al. Rev-Erbs repress macrophage gene expression by inhibiting enhancer-directed transcription. Nature. 2013;498(7455):511-515. doi: 10.1038/nature12209

 

  1. Chen H, Liang H. A high-resolution map of human enhancer RNA loci characterizes super-enhancer activities in cancer. Cancer Cell. 2020;38(5):701-715. doi: 10.1016/j.ccell.2020.08.020

 

  1. Zhu Y, Sun L, Chen Z, Whitaker JW, Wang T, Wang W. Predicting enhancer transcription and activity from chromatin modifications. Nucleic Acids Res. 2013; 41(22):10032-10043.

 

  1. Mikhaylichenko O, Bondarenko V, Harnett D, et al. The degree of enhancer or promoter activity is reflected by the levels and directionality of eRNA transcription. Genes Dev. 2018;32(1):42-57. doi: 10.1101/gad.308619.117

 

  1. Melgar MF, Collins FS, Sethupathy P. Discovery of active enhancers through bidirectional expression of short transcripts. Genome Biol. 2011;12:R113. doi: 10.1186/gb-2011-12-11-r113

 

  1. Kleftogiannis D, Kalnis P, Bajic VB. Progress and challenges in bioinformatics approaches for enhancer identification. Brief Bioinform. 2016;17(6):967-979. doi: 10.1093/bib/bbv101

 

  1. Wang D, Garcia-Bassets I, Benner C, et al. Reprogramming transcription by distinct classes of enhancers functionally defined by eRNA. Nature. 2011;474(7351):390-394. doi: 10.1038/nature10006

 

  1. Li W, Notani D, Ma Q, et al. Functional roles of enhancer RNAs for oestrogen-dependent transcriptional activation. Nature. 2013;498(7455):516-520. doi: 10.1038/nature12210

 

  1. Lee JH, Xiong F, Li W. Enhancer RNAs in cancer: Regulation, mechanisms and therapeutic potential. RNA Biol. 2020;17(11):1550-1559. doi: 10.1080/15476286.2020.1712895

 

  1. McCleland ML, Mesh K, Lorenzana E, et al. CCAT1 is an enhancer-templated RNA that predicts BET sensitivity in colorectal cancer. J Clin Invest. 2016;126(2):639-652. doi: 10.1172/JCI83265

 

  1. Xiang JF, Yin QF, Chen T, et al. Human colorectal cancer-specific CCAT1-L lncRNA regulates long-range chromatin interactions at the MYC locus. Cell Res. 2014;24(5):513-531. doi: 10.1038/cr.2014.35

 

  1. Zhang Z, Lee JH, Ruan H, et al. Transcriptional landscape and clinical utility of enhancer RNAs for eRNA-targeted therapy in cancer. Nat Commun. 2019;10(1):4562. doi: 10.1038/s41467-019-12543-5

 

  1. Jiao W, Chen Y, Song H, et al. HPSE enhancer RNA promotes cancer progression through driving chromatin looping and regulating hnRNPU/p300/EGR1/HPSE axis. Oncogene. 2018;37(20):2728-2745. doi: 10.1038/s41388-018-0128-0

 

  1. Qin N, Ma Z, Wang C, et al. Comprehensive characterization of functional eRNAs in lung adenocarcinoma reveals novel regulators and a prognosis-related molecular subtype. Theranostics. 2020;10(24):11264. doi: 10.7150%2Fthno.47039

 

  1. Colebatch AJ, Dobrovic A, Cooper WA. TERT gene: Its function and dysregulation in cancer. J Clin Pathol. 2019;72(4):281-284. doi: 10.1136/jclinpath-2018-205653

 

  1. McKay JD, Hung RJ, Gaborieau V, et al. Lung cancer susceptibility locus at 5p15.33. Nat Genet. 2008; 40(12):1404-1406. doi: 10.1038/ng.254

 

  1. Broderick P, Wang Y, Vijayakrishnan J, et al. Deciphering the impact of common genetic variation on lung cancer risk: A genome-wide association study. Cancer Res. 2009;69(16):6633-6641. doi: 10.1158/0008-5472.CAN-09-0680

 

  1. Jiang Y, Jiang YY, Xie JJ, et al. Co-activation of super-enhancer-driven CCAT1 by TP63 and SOX2 promotes squamous cancer progression. Nat Commun. 2018;9(1):3619. doi: 10.1038/s41467-018-06081-9

 

  1. Benoist C, Chambon P. In vivo sequence requirements of the SV40 early promoter region. Nature. 1981;290(5804):304-310. doi: 10.1038/290304a0

 

  1. Barral A, Déjardin J. The chromatin signatures of enhancers and their dynamic regulation. Nucleus. 2023;14(1):2160551. doi: 10.1080/19491034.2022.2160551

 

  1. Heintzman ND, Hon GC, Hawkins RD, et al. Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature. 2009;459(7243):108-112. doi: 10.1038/nature07829

 

  1. Ernst J, Kheradpour P, Mikkelsen TS, et al. Mapping and analysis of chromatin state dynamics in nine human cell types. Nature. 2011;473(7345):43-49. doi: 10.1038/nature09906

 

  1. Nguyen TC, Cao X, Yu P, et al. Mapping RNA-RNA interactome and RNA structure in vivo by MARIO. Nat Commun. 2016;7(1):12023. doi: 10.1038/ncomms12023

 

  1. Hafner M, Landthaler M, Burger L, et al. Transcriptome-wide identification of RNA-binding protein and microRNA target sites by PAR-CLIP. Cell. 2010;141(1):129-141. doi: 10.1016/j.cell.2010.03.009

 

  1. Chi SW, Zang JB, Mele A, Darnell RB. Argonaute HITS-CLIP decodes microRNA-mRNA interaction maps. Nature. 2009;460(7254):479-486. doi: 10.1038/nature08170

 

  1. Wu W, Yan Z, Nguyen TC, Bouman Chen Z, Chien S, Zhong S. Mapping RNA-chromatin interactions by sequencing with iMARGI. Nat Protoc. 2019;14(11):3243-3272. doi: 10.1038/s41596-019-0229-4

 

  1. Wen X, Luo Z, Zhao W, et al. Single-cell multiplex chromatin and RNA interactions in ageing human brain. Nature. 2024;628(8008):648-656. doi: 10.1038/s41586-024-07239-w

 

  1. Zhou B, Li X, Luo D, Lim DH, Zhou Y, Fu XD. GRID-seq for comprehensive analysis of global RNA-chromatin interactions. Nat Protoc. 2019;14(7):2036-2068. doi: 10.1038/s41596-019-0172-4

 

  1. Nagari A, Murakami S, Malladi VS, Kraus WL. Computational approaches for mining GRO-Seq data to identify and characterize active enhancers. Methods Mol Biol. 2017;1468:121-138. doi: 10.1007/978-1-4939-4035-6_10

 

  1. Hah N, Murakami S, Nagari A, Danko CG, Kraus WL. Enhancer transcripts mark active estrogen receptor binding sites. Genome Res. 2013;23(8):1210-1223. doi: 10.1101/gr.152306.112

 

  1. Jia Q, Chen S, Tan Y, Li Y, Tang F. Oncogenic super-enhancer formation in tumorigenesis and its molecular mechanisms. Exp Mol Med. 2020;52(5):713-723. doi: 10.1038/s12276-020-0428-7

 

  1. Kravchuk EV, Ashniev GA, Gladkova MG, et al. Experimental validation and prediction of super-enhancers: Advances and challenges. Cells. 2023;12(8):1191. doi: 10.3390/cells12081191

 

  1. Huang J, Liu X, Li D, et al. Dynamic control of enhancer repertoires drives lineage and stage-specific transcription during hematopoiesis. Dev Cell. 2016;36(1):9-23. doi: 10.1016/j.devcel.2015.12.014

 

  1. Hay D, Hughes JR, Babbs C, et al. Genetic dissection of the α-globin super-enhancer in vivo. Nat Genet. 2016;48(8):895-903. doi: 10.1038/ng.3605

 

  1. Honnell V, Norrie JL, Patel AG, et al. Identification of a modular super-enhancer in murine retinal development. Nat Commun. 2022;13(1):253. doi: 10.1038/s41467-021-27924-y

 

  1. Claringbould A, Zaugg JB. Enhancers in disease: Molecular basis and emerging treatment strategies. Trends Mol Med. 2021;27(11):1060-1073. doi: 10.1016/j.molmed.2021.07.012

 

  1. Chen YL, Li XL, Li G, et al. BRD4 inhibitor GNE987 exerts anti-cancer effects by targeting super-enhancers in neuroblastoma. Cell Biosci. 2022;12(1):33. doi: 10.1186/s13578-022-00769-8

 

  1. Housden BE, Muhar M, Gemberling M, et al. Loss-of-function genetic tools for animal models: Cross-species and cross-platform differences. Nat Rev Genet. 2017;18(1):24-40. doi: 10.1038/nrg.2016.118

 

  1. Sztal TE, Stainier DY. Transcriptional adaptation: A mechanism underlying genetic robustness. Development. 2020;147(15):dev186452. doi: 10.1242/dev.186452

 

  1. Sarvari P, Rasouli SJ, Allanki S, et al. The E3 ubiquitin-protein ligase Rbx1 regulates cardiac wall morphogenesis in zebrafish. Dev Biol. 2021;480:1-12. doi: 10.1016/j.ydbio.2021.07.019

 

  1. Frangoul H, Altshuler D, Cappellini MD, et al. CRISPR-Cas9 gene editing for sickle cell disease and β-thalassemia. N Engl J Med. 2021;384(3):252-260. doi: 10.1056/NEJMoa2031054

 

  1. Sarvari P, Sarvari P, Ramírez-Díaz I, Mahjoubi F, Rubio K. Advances of epigenetic biomarkers and epigenome editing for early diagnosis in breast cancer. Int J Mol Sci. 2022;23(17):9521. doi: 10.3390/ijms23179521

 

  1. Sarvari P, Sarvari P. Mitochondria: The master regulator of aging. INNOSC Theranostics Pharmacol Sci. 2024;7(2):1726. doi: 10.36922/itps.1726

 

  1. Che W, Ye S, Cai A, Cui X, Sun Y. CRISPR-Cas13a targeting the enhancer RNA-SMAD7e inhibits bladder cancer development both in vitro and in vivo. Front Mol Biosci. 2020;7:607740. doi: 10.3389/fmolb.2020.607740

 

  1. Mill CP, Fiskus W, DiNardo CD, et al. RUNX1-targeted therapy for AML expressing somatic or germline mutation in RUNX1. Blood. 2019;134(1):59-73. doi: 10.1182/blood.2018893982

 

  1. Vincent CA, Nissen I, Dakhel S, Hörnblad A, Remeseiro S. Epigenomic perturbation of novel EGFR enhancers reduces the proliferative and invasive capacity of glioblastoma and increases sensitivity to temozolomide. BMC Cancer. 2023;23(1):945. doi: 10.1186/s12885-023-11418-9

 

  1. Sarvari P, Sarvari P. Advances in nanoparticle-based drug delivery in cancer treatment. Glob Transl Med. 2023;2:0394. doi: 10.36922/gtm.0394

 

  1. Huang CS, You X, Dai C, et al. Targeting super‐enhancers via nanoparticle‐facilitated BRD4 and CDK7 inhibitors synergistically suppresses pancreatic ductal adenocarcinoma. Adv Sci (Weinh). 2020;7(7):1902926. doi: 10.1002/advs.201902926
Share
Back to top
INNOSC Theranostics and Pharmacological Sciences, Electronic ISSN: 2705-0823 Print ISSN: 2705-0734, Published by AccScience Publishing
We use cookies on our website to ensure you get the best experience.
Read more about our cookies here
Accept