Multi‐omics analysis reveals the functional transcription and potential translation of enhancers
Open accessAbstract
Enhancer can transcribe RNAs, however, most of them were neglected in traditional RNA‐seq analysis workflow. Here, we developed a Pipeline for Enhancer Transcription (PET, http://fun-science.club/PET) for quantifying enhancer RNAs (eRNAs) from RNA‐seq. By applying this pipeline on lung cancer samples and cell lines, we showed that the transcribed enhancers are enriched with histone marks and transcription factor motifs (JUNB, Hand1‐Tcf3 and GATA4). By training a machine learning model, we demonstrate that enhancers can predict prognosis better than their nearby genes. Integrating the Hi‐C, ChIP‐seq and RNA‐seq data, we observe that transcribed enhancers associate with cancer hallmarks or oncogenes, among which LcsMYC‐1 (Lung cancer‐specific MYC eRNA‐1) potentially supports MYC expression. Surprisingly, a significant proportion of transcribed enhancers contain small protein‐coding open reading frames (sORFs) and can be translated into microproteins. Our study provides a computational method for eRNA quantification and deepens our understandings of the DNA, RNA and protein nature of enhancers.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Total RNA-seq can detect more eRNAs than polyA RNA-seq because not all eRNAs are polyadenylated.
“Given that not all eRNAs are polyadenylated, total RNA-seq, compared to polyA RNA-seq, can detect more eRNAs (78, 79).”
From Comprehensive characterization of the transcriptional landscape in Alzheimer’s disease (AD) brains (2025) · cites this paper as [79]
In the comparison of sequencing methods (Figure 1 discussion; page not provided), total RNA-seq detected slightly more eRNAs than polyA RNA-seq in K562 cells (3,809 versus 3,613). The paper does not establish that incomplete polyadenylation caused this difference; it concludes that there was no large difference in eRNA quantification between the methods. (LLM, conf=0.88)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
Love, M. I., Huber, W., & Anders, S. (2014) · Genome Biology · doi:10.1186/s13059-014-0550-8 · Cited by 95,106 · see citing works
Fast gapped-read alignment with Bowtie 2
Langmead, B., & Salzberg, S. L. (2012) · Nature Methods · doi:10.1038/nmeth.1923 · Cited by 56,400 · see citing works
STAR: ultrafast universal RNA-seq aligner
Dobin, A., Davis, C. A., Schlesinger, F., Drenkow, J., Zaleski, C., Jha, S., Batut, P., Chaisson, M., & Gingeras, T. R. (2013) · Bioinformatics · doi:10.1093/bioinformatics/bts635 · Cited by 51,709 · see citing works
featureCounts: an efficient general purpose program for assigning sequence reads to genomic features
Liao, Y., Smyth, G. K., & Shi, W. (2014) · Bioinformatics · doi:10.1093/bioinformatics/btt656 · Cited by 27,219 · see citing works
Landscape of transcription in human cells
Djebali, S., Davis, C. A., Merkel, A., Dobin, A., Lassmann, T., Mortazavi, A., Tanzer, A., Lagarde, J., Lin, W., Schlesinger, F., et al. (2012) · Nature · doi:10.1038/nature11233 · Cited by 5,187 · see citing works
ChIPseeker: an R/Bioconductor package for ChIP peak annotation, comparison and visualization
Yu, G., Wang, L.-G., & He, Q. (2015) · Bioinformatics · doi:10.1093/bioinformatics/btv145 · Cited by 4,399 · see citing works
Histone H3K27ac separates active from poised enhancers and predicts developmental state
Creyghton, M. P., Cheng, A. W., Welstead, G. G., Kooistra, T., Carey, B. W., Steine, E. J., Hanna, J., Lodato, M. A., Frampton, G. M., Sharp, P. A., et al. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1016071107 · Cited by 4,302 · see citing works
Master Transcription Factors and Mediator Establish Super-Enhancers at Key Cell Identity Genes
Whyte, W. A., Orlando, D. A., Hnisz, D., Abraham, B. J., Lin, C. Y., Kagey, M. H., Rahl, P. B., Lee, T. I., & Young, R. A. (2013) · Cell · doi:10.1016/j.cell.2013.03.035 · Cited by 4,143 · see citing works
Super-enhancers in the control of cell identity and disease
Hnisz, D., Abraham, B. J., Lee, T. I., Lau, A., Saint-André, V., Sigova, A. A., Hoke, H. A., & Young, R. A. (2013) · Cell · doi:10.1016/j.cell.2013.09.053 · Cited by 3,662 · see citing works
Lung cancer: current therapies and new targeted treatments
Hirsch, F. R., Scagliotti, G. V., Mulshine, J. L., Kwon, R., Curran, W. J., Wu, Y.-L. L. C., & Paz-Ares, L. G. (2016) · The Lancet · doi:10.1016/s0140-6736(16)30958-8 · Cited by 3,278 · see citing works
Self-citationWidespread transcription at neuronal activity-regulated enhancers
Kim, T.-K., Hemberg, M., Gray, J. M., Costa, A. M., Bear, D. M., Wu, J., Harmin, D. A., Laptewicz, M., Barbara-Haley, K., Kuersten, S., et al. (2010) · Nature · doi:10.1038/nature09033 · Cited by 2,450 · see citing works
Shigematsu, H., Lin, L., Takahashi, T., Nomura, M., Suzuki, M., Wistuba, I. I., Fong, K. M., Lee, H., Toyooka, S., Shimizu, N., et al. (2005) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/dji055 · Cited by 2,377 · see citing works
A User's Guide to the Encyclopedia of DNA Elements (ENCODE)
The ENCODE Project Consortium (2011) · PLoS Biology · doi:10.1371/journal.pbio.1001046 · Cited by 1,495 · see citing works
Modification of Enhancer Chromatin: What, How, and Why?
Calo, E., & Wysocka, J. (2013) · Molecular Cell · doi:10.1016/j.molcel.2013.01.038 · Cited by 1,457 · see citing works
Big data and machine learning algorithms for health-care delivery
Ngiam, K. Y., & Khor, I. W. (2019) · The Lancet Oncology · doi:10.1016/s1470-2045(19)30149-4 · Cited by 1,424 · see citing works
Long-range enhancer–promoter contacts in gene expression control
Schoenfelder, S., & Fraser, P. (2019) · Nature Reviews Genetics · doi:10.1038/s41576-019-0128-0 · Cited by 1,102 · see citing works
Javierre, B. M., Burren, O. S., Wilder, S. P., Kreuzhuber, R., Hill, S. M., Sewitz, S., Cairns, J., Wingett, S. W., Várnai, C., Thiecke, M. J., et al. (2016) · Cell · doi:10.1016/j.cell.2016.09.037 · Cited by 1,046 · see citing works
Oser, M. G., Niederst, M. J., Sequist, L. V. D., & Engelman, J. A. (2015) · The Lancet Oncology · doi:10.1016/s1470-2045(14)71180-5 · Cited by 939 · see citing works
MYC Activation Is a Hallmark of Cancer Initiation and MaintenancePreprint
Gabay, M., Li, Y., & Felsher, D. W. (2014) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a014241 · Cited by 808 · see citing works
Xiang, J., Yin, Q.-F., Chen, T., Zhang, Y., Zhang, X.-O., Wu, Z., Zhang, S., Wang, H., Ge, J., Lu, X., et al. (2014) · Cell Research · doi:10.1038/cr.2014.35 · Cited by 729 · see citing works
Core, L. J., Martins, A. L., Danko, C. G., Waters, C. T., Siepel, A., & Lis, J. T. (2014) · Nature Genetics · doi:10.1038/ng.3142 · Cited by 693 · see citing works
Peptidomic discovery of short open reading frame–encoded peptides in human cells
Slavoff, S. A., Mitchell, A. J., Schwaid, A. G., Cabili, M. N., Ma, J., Levin, J. Z., Karger, A., Budnik, B., Rinn, J. L., & Saghatelian, A. (2012) · Nature Chemical Biology · doi:10.1038/nchembio.1120 · Cited by 678 · see citing works
Gainor, J. F., Varghese, A. M., Ou, S. I., Kabraji, S. K., Awad, M. M., Katayama, R., Pawlak, A. C., Mino-Kenudson, M. A., Yeap, B. Y., Riely, G. J., et al. (2013) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-13-0318 · Cited by 609 · see citing works
A pan-cancer proteomic perspective on The Cancer Genome Atlas
Akbani, R., Ng, P. K. S., Werner, H. M. J., Shahmoradgoli, M., Zhang, F., Ju, Z., Liu, W., Yang, J.-Y., Yoshihara, K., Li, J., et al. (2014) · Nature Communications · doi:10.1038/ncomms4887 · Cited by 600 · see citing works
Wang, Y., Song, F., Zhang, B., Zhang, L., Xu, J., Kuang, D., Li, D., Choudhary, M. N. K., Li, Y., Hu, M., et al. (2018) · Genome biology · doi:10.1186/s13059-018-1519-9 · Cited by 552 · see citing works
Enhancer RNAs and regulated transcriptional programs
Lam, M. T. Y., Li, W., Rosenfeld, M. G., & Glass, C. K. (2014) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2014.02.007 · Cited by 502 · see citing works
Enhancer transcripts mark active estrogen receptor binding sitesPreprint
Hah, N., Murakami, S., Nagari, A., Danko, C. G., & Kraus, W. L. (2013) · Genome Research · doi:10.1101/gr.152306.112 · Cited by 475 · see citing works
Enhancer RNA Facilitates NELF Release from Immediate Early Genes
Schaukowitch, K., Joo, J., Liu, X., Watts, J. K., Martinez, C., & Kim, T.-K. (2014) · Molecular Cell · doi:10.1016/j.molcel.2014.08.023 · Cited by 445 · see citing works
Machine learning for real-time prediction of complications in critical care: a retrospective study
Meyer, A., Zverinski, D., Pfahringer, B., Kempfert, J., Kuehne, T., Sündermann, S. H., Stamm, C., Hofmann, T., Falk, V., & Eickhoff, C. (2018) · The Lancet Respiratory Medicine · doi:10.1016/s2213-2600(18)30300-x · Cited by 350 · see citing works
A Myc enhancer cluster regulates normal and leukaemic haematopoietic stem cell hierarchies
Bahr, C., von Paleske, L., Uslu, V. V., Remeseiro, S., Takayama, N., Ng, S. W., Murison, A., Langenfeld, K., Petretich, M., Scognamiglio, R., et al. (2018) · Nature · doi:10.1038/nature25193 · Cited by 328 · see citing works
FANTOM5 CAGE profiles of human and mouse samples
Noguchi, S., Arakawa, T., Fukuda, S., Furuno, M., Hasegawa, A., Hori, F., Ishikawa-Kato, S., Kaida, K., Kaiho, A., Kanamori-Katayama, M., et al. (2017) · Scientific Data · doi:10.1038/sdata.2017.112 · Cited by 310 · see citing works
A Pan-Cancer Analysis of Enhancer Expression in Nearly 9000 Patient Samples
Chen, H., Li, C., Peng, X., Zhou, Z., Weinstein, J. N., Johnson, R., Demchok, J. A., Felau, I., Kasapi, M., Ferguson, M. L., et al. (2018) · Cell · doi:10.1016/j.cell.2018.03.027 · Cited by 298 · see citing works
Self-citationMakarewich, C. A., & Olson, E. N. (2017) · Trends in Cell Biology · doi:10.1016/j.tcb.2017.04.006 · Cited by 280 · see citing works
The microprotein Minion controls cell fusion and muscle formation
Zhang, Q., Vashisht, A. A., O'Rourke, J. R., Corbel, S. Y., Moran, R., Romero, A., Miraglia, L. J., Zhang, J., Durrant, E. S., Schmedt, C., et al. (2017) · Nature Communications · doi:10.1038/ncomms15664 · Cited by 268 · see citing works
Transcriptional landscape and clinical utility of enhancer RNAs for eRNA-targeted therapy in cancer
Zhang, Z., Lee, J., Ruan, H., Ye, Y., Krakowiak, J., Hu, Q., Xiang, Y., Gong, J., Zhou, B., Wang, L., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-12543-5 · Cited by 263 · see citing works
Ren, G., Jin, W., Cui, K., Rodrigez, J., Hu, G., Zhang, Z., Larson, D. R., & Zhao, K. (2017) · Molecular Cell · doi:10.1016/j.molcel.2017.08.026 · Cited by 255 · see citing works
Accurate annotation of human protein-coding small open reading frames
Martinez, T. F., Chu, Q., Donaldson, C. J., Tan, D., Shokhirev, M. N., & Saghatelian, A. (2019) · Nature Chemical Biology · doi:10.1038/s41589-019-0425-0 · Cited by 232 · see citing works
CCAT1 is an enhancer-templated RNA that predicts BET sensitivity in colorectal cancer
McCleland, M. L., Mesh, K., Lorenzana, E. G., Chopra, V. S., Segal, E., Watanabe, C. K., Haley, B., Mayba, O., Yaylaoglu, M., Gnad, F., et al. (2016) · Journal of Clinical Investigation · doi:10.1172/jci83265 · Cited by 220 · see citing works
An update on sORFs.org: a repository of small ORFs identified by ribosome profiling
Olexiouk, V., Criekinge, W. V., & Menschaert, G. (2017) · Nucleic Acids Research · doi:10.1093/nar/gkx1130 · Cited by 194 · see citing works
Diller, G., Kempny, A., Babu‐Narayan, S. V., Henrichs, M., Brida, M., Uebing, A. S., Lammers, A. E., Baumgartner, H., Li, W., Wort, S. J., et al. (2018) · European Heart Journal · doi:10.1093/eurheartj/ehy915 · Cited by 191 · see citing works
A Muscle-Specific Enhancer RNA Mediates Cohesin Recruitment and Regulates Transcription In trans
Tsai, P.-F., Dell’Orso, S., Rodriguez, J., Vivanco, K. O., Ko, K.-D., Jiang, K., Juan, A. H., Sarshad, A. A., Vian, L., Tran, M. D., et al. (2018) · Molecular Cell · doi:10.1016/j.molcel.2018.06.008 · Cited by 178 · see citing works
Polycarpou‐Schwarz, M., Groß, M., Mestdagh, P., Schott, J., Grund, S. E., Hildenbrand, C., Rom, J., Aulmann, S., Sinn, H., Vandesompele, J., et al. (2018) · Oncogene · doi:10.1038/s41388-018-0281-5 · Cited by 175 · see citing works
LIF promotes tumorigenesis and metastasis of breast cancer through the AKT-mTOR pathway
Li, X., Yang, Q., Yu, H., Wu, L., Zhao, Y., Zhang, C., Yue, X., Liu, Z., Wu, H., Haffty, B. G., et al. (2014) · Oncotarget · doi:10.18632/oncotarget.1772 · Cited by 154 · see citing works
Aberrant Super‐Enhancer Landscape in Human Hepatocellular Carcinoma
Tsang, F. H., Law, C., Tang, T. C. C., Cheng, C. L., Chin, D. W., Tam, V., Wei, L., Wong, C. C., Ng, I. O., & Wong, C. (2019) · Hepatology · doi:10.1002/hep.30544 · Cited by 153 · see citing works
JunB promotes Th17 cell identity and restrains alternative CD4+ T-cell programs during inflammation
Carr, T. M., Wheaton, J. D., Houtz, G. M., & Ciofani, M. (2017) · Nature Communications · doi:10.1038/s41467-017-00380-3 · Cited by 141 · see citing works
The MYC Enhancer-ome: Long-Range Transcriptional Regulation of MYC in Cancer
Lancho, O., & Herranz, D. (2018) · Trends in cancer · doi:10.1016/j.trecan.2018.10.003 · Cited by 137 · see citing works
Ansari, R. E., Craze, M. L., Miligy, I. M., Diez, M., Nolan, C. C., Ellis, I. O., Rakha, E. A., & Green, A. R. (2018) · Breast Cancer Research · doi:10.1186/s13058-018-0946-6 · Cited by 136 · see citing works
A global transcriptional network connecting noncoding mutations to changes in tumor gene expression
Zhang, W., Bojorquez-Gomez, A., Velez, D. O., Xu, G., Sanchez, K. S., Shen, J. P., Chen, K., Licon, K., Melton, C. A., Olson, K. M., et al. (2018) · Nature Genetics · doi:10.1038/s41588-018-0091-2 · Cited by 122 · see citing works
Comprehensive, integrated, and phased whole-genome analysis of the primary ENCODE cell line K562Preprint
Zhou, B., Ho, S. S., Greer, S., Zhu, X., Bell, J., Arthur, J. G., Spies, N., Zhang, X., Byeon, S., Pattni, R., et al. (2019) · Genome Research · doi:10.1101/gr.234948.118 · Cited by 120 · see citing works
Enhancer RNA profiling predicts transcription factor activityPreprint
Azofeifa, J. G., Allen, M. A., Hendrix, J., Read, T., Rubin, J. D., & Dowell, R. D. (2018) · Genome Research · doi:10.1101/gr.225755.117 · Cited by 118 · see citing works
Update of the FANTOM web resource: high resolution transcriptome of diverse cell types in mammals
Lizio, M., Harshbarger, J., Abugessaisa, I., Noguchi, S., Kondo, A., Severin, J., Mungall, C., Arenillas, D. J., Mathelier, A., Medvedeva, Y. A., et al. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw995 · Cited by 115 · see citing works
Jiao, W., Chen, Y., Song, H., Li, D., Mei, H., Yang, F., Fang, E., Wang, X., Huang, K., Zheng, L., et al. (2018) · Oncogene · doi:10.1038/s41388-018-0128-0 · Cited by 115 · see citing works
LINC00116 codes for a mitochondrial peptide linking respiration and lipid metabolism
Chugunova, A. A., Loseva, E., Mazin, P., Mitina, A., Navalayeu, T., Bilan, D. S., Vishnyakova, P., Marey, M. V., Golovina, A. Y., Serebryakova, M. V., et al. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1809105116 · Cited by 115 · see citing works
Condensin I and II Complexes License Full Estrogen Receptor α-Dependent Enhancer Activation
Li, W., Hu, Y., Oh, S., Ma, Q., Merkurjev, D., Song, X., Zhou, X., Liu, Z., Tanasă, B., He, X., et al. (2015) · Molecular Cell · doi:10.1016/j.molcel.2015.06.002 · Cited by 112 · see citing works
Emerging Targeted Therapies for the Treatment of Non-small Cell Lung Cancer
Halliday, P. R., Blakely, C. M., & Bivona, T. G. (2019) · Current Oncology Reports · doi:10.1007/s11912-019-0770-x · Cited by 108 · see citing works
Tan, S. H., Leong, W. Z., Ngoc, P. C. T., Tan, T. K., Bertulfo, F. C., Lim, M. C., An, Ö., Li, Z., Yeoh, A. E. J., Fullwood, M. J., et al. (2019) · Blood · doi:10.1182/blood.2018874503 · Cited by 73 · see citing works
The Role of De Novo Noncoding Regulatory Mutations in Neurodevelopmental Disorders
Turner, T. N., & Eichler, E. E. (2018) · Trends in Neurosciences · doi:10.1016/j.tins.2018.11.002 · Cited by 69 · see citing works
Lung cancer deficient in the tumor suppressor GATA4 is sensitive to TGFBR1 inhibition
Gao, L., Hu, Y., Tian, Y., Fan, Z., Wang, K., Li, H., Zhou, Q., Zeng, G., Hu, X., Yu, L., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-09295-7 · Cited by 67 · see citing works
Intracellular sodium sensing: SIK1 network, hormone action and high blood pressure
Jaitovich, A., & Bertorello, A. M. (2010) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2010.03.009 · Cited by 61 · see citing works
Enhancer-Derived RNA: A Primer
Liu, F. (2017) · Genomics Proteomics & Bioinformatics · doi:10.1016/j.gpb.2016.12.006 · Cited by 60 · see citing works
Ben‐Ali, M., Yang, J., Chan, K. W., Ben‐Mustapha, I., Mekki, N., Benabdessalem, C., Mellouli, F., Béjaoui, M., Yang, W., Aissaouï, L., et al. (2017) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2017.04.037 · Cited by 55 · see citing works
ID1 Promotes Breast Cancer Metastasis by S100A9 Regulation
Gumireddy, K., Li, A., Kossenkov, A. V., Cai, K. Q., Liu, Q., Yan, J., Xu, H., Showe, L. C., Zhang, L., & Huang, Q. (2014) · Molecular Cancer Research · doi:10.1158/1541-7786.mcr-14-0049 · Cited by 50 · see citing works
Tawara, K., Bolin, C. M., Koncinsky, J., Kadaba, S., Covert, H. J., Sutherland, C., Bond, L., Kronz, J. D., Garbow, J. R., & Jorcyk, C. L. (2018) · Breast Cancer Research · doi:10.1186/s13058-018-0971-5 · Cited by 49 · see citing works
Enhancer RNAs: a missing regulatory layer in gene transcription
Mao, R., Wu, Y., Ming, Y., Xu, Y., Wang, S., Chen, X., Wang, X., & Fan, Y. (2018) · Science China Life Sciences · doi:10.1007/s11427-017-9370-9 · Cited by 42 · see citing works
Self-citationMirtschink, P., Bischof, C., Pham, M. D., Sharma, R., Khadayate, S. P., Rossi, G., Fankhauser, N., Traub, S., Sossalla, S. T., Hagag, E., et al. (2019) · Circulation · doi:10.1161/circulationaha.118.036769 · Cited by 34 · see citing works
Lung Cancer: A Brief Review of Epidemiology and Screening
Gouvinhas, C., de Mello, R. A., Oliveira, D. S., Castro‐Lopes, J. M., Castelo‐Branco, P., dos Santos, R. S., Hespanhol, V. P., & Pozza, D. H. (2018) · Future Oncology · doi:10.2217/fon-2017-0486 · Cited by 33 · see citing works
MYC-Induced Epigenetic Activation of GATA4 in Lung Adenocarcinoma
Castro, I. C., Breiling, A., Luetkenhaus, K., Ceteci, F., Hausmann, S., Kreß, S., Lyko, F., Rudel, T., & Rapp, U. R. (2012) · Molecular Cancer Research · doi:10.1158/1541-7786.mcr-12-0414-t · Cited by 20 · see citing works
Prabhash, K. (2019) · South Asian Journal of Cancer · doi:10.4103/sajc.sajc_227_18 · Cited by 13 · see citing works
Long noncoding RNA TMEM75 promotes colorectal cancer progression by activation of SIM2
Jin, X., Liu, G., Zhang, X., & Du, N. (2018) · Gene · doi:10.1016/j.gene.2018.06.096 · Cited by 13 · see citing works
Camp, N. J., Farnham, J. M., Allen‐Brady, K., & Cannon‐Albright, L. (2007) · The Prostate · doi:10.1002/pros.20631 · Cited by 11 · see citing works
Flagged first, then by citations
3 of the 73 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Spatiotemporal Immune Landscape of Colorectal Cancer Liver Metastasis at Single-Cell Level
Wu, Y., Yang, S., Ma, J., Chen, Z., Song, G., Rao, D., Cheng, Y., Huang, S., Liu, Y., Jiang, S., et al. (2021) · Cancer Discovery · doi:10.1158/2159-8290.cd-21-0316 · Cited by 1,199 · see citing works
Self-citationNeutrophil profiling illuminates anti-tumor antigen-presenting potency
Wu, Y. C., Ma, J., Yang, X., Fang, N., Zhang, T., Ji, S., Rao, D., Feng, H., Gao, K., Gu, X., et al. (2024) · Cell · doi:10.1016/j.cell.2024.02.005 · Cited by 441 · see citing works
Self-citationMulti-omics integration analysis: Tools and applications in environmental toxicology
Shi, C., Cheng, L., Yu, Y., Chen, S., Dai, Y., Yang, J., Zhang, H., Chen, J., & Geng, N. (2024) · Environmental Pollution · doi:10.1016/j.envpol.2024.124675 · Cited by 82 · see citing works
The current status and future of PD-L1 in liver cancer
Hao, L.-Y., Li, S.-H., Deng, J.-L., Li, N., Yu, F., Jiang, Z., Zhang, J., Shi, X., & Hu, X.-Y. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1323581 · Cited by 59 · see citing works
Non-coding RNAs and glioma: Focus on cancer stem cells
Rajabi, A., Kayedi, M., Rahimi, S., Dashti, F., Mirazimi, S. M. A., Homayoonfal, M., Mahdian, S. M. A., Hamblin, M. R., Tamtaji, O. R., Afrasiabi, A., et al. (2022) · Molecular Therapy — Oncolytics · doi:10.1016/j.omto.2022.09.005 · Cited by 22 · see citing works
Deng, X., Yu, Y. V., & Jin, Y. N. (2024) · Cell Death Discovery · doi:10.1038/s41420-024-02185-y · Cited by 22 · see citing works
Experimental Validation and Prediction of Super-Enhancers: Advances and Challenges
Kravchuk, E. V., Ashniev, G. A., Gladkova, M. G., Орлов, А. В., Vasileva, A. V., Boldyreva, A., Burenin, A. G., Skirda, A. M., Nikitin, P. I., & Orlova, N. N. (2023) · Cells · doi:10.3390/cells12081191 · Cited by 19 · see citing works
Bu, X., Liu, S., Wen, D., Kan, A., Xu, Y., Lin, X., & Shi, M. (2022) · Molecular Therapy — Oncolytics · doi:10.1016/j.omto.2022.07.001 · Cited by 10 · see citing works
Huang, P., Zhang, B., Zhao, J., & Li, M. D. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.827657 · Cited by 10 · see citing works
Comprehensive characterization of the transcriptional landscape in Alzheimer’s disease (AD) brains
Chen, C., Zhang, Z., Liu, Y., Hong, W., Karahan, H., Wang, J., Li, W., Diao, L., Yu, M., Saykin, A. J., et al. (2025) · Science Advances · doi:10.1126/sciadv.adn1927 · Cited by 6 · see citing works
“Given that not all eRNAs are polyadenylated, total RNA-seq, compared to polyA RNA-seq, can detect more eRNAs ( 78 , 79 ).”
Bu, X., Liu, S., Zhang, Z.-Q., Wu, J., Pan, S., & Hu, Y. (2023) · Clinical & Translational Oncology · doi:10.1007/s12094-023-03319-x · Cited by 4 · see citing works
Yang, B. Y., Zheng, Q., Li, G., Liao, B., Lin, Z., & He, H. (2025) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2025.1657720 · Cited by 3 · see citing works
Shen, Y., Wu, Y. C., & Gu, L. (2020) · Annals of Translational Medicine · doi:10.21037/atm-20-3650 · Cited by 3 · see citing works
Self-citationZhang, R., Chen, Z., Li, T., Feng, D., Liu, X., Wang, X., Han, H., Lei, Y., Li, X., Li, B., et al. (2025) · Briefings in Functional Genomics · doi:10.1093/bfgp/elaf007 · Cited by 2 · see citing works
Multi-Omics Data Analysis for Cancer Research: Colorectal Cancer, Liver Cancer and Lung Cancer
Zhang, H., Gong, X., & Tang, M. (2023) · Translational bioinformatics · doi:10.1007/978-981-19-8210-1_5 · Cited by 2 · see citing works
Bu, X., Wen, D., Zhou, T., Xiao, L., Zhang, Z.-Q., Zhao, X., & Hu, Y. (2025) · Discover Oncology · doi:10.1007/s12672-025-02879-4
Enhancer RNAs contribute to genome reprogramming driven by a GATA3 noncoding variant in leukaemia
Barbosa, T. C., Poubel, C. P., Maciel, A. L. T., Blunck, C. B., Santos, R., Boroni, M., Mansur, M. B., & Emerenciano, M. (2025) · Scientific Reports · doi:10.1038/s41598-025-10262-0
Deciphering the eRNA landscape and revealing target aberrant pathways in prostate cancer
Yu, C., Wen, Y. H., Li, Y., Song, B., Hu, Y., Meng, Z., Yan, Z., Du, W., & Rong, H. (2026) · BMC Cancer · doi:10.1186/s12885-026-15675-2
- Authors
- Wu, Y., Yang, Y., Gu, H., Tao, B., Zhang, E., Wei, J., Wang, Z., Liu, A., Sun, R., Chen, M., Fan, Y., & Mao, R.
- Affiliations
- Nantong University (CN)
- First Affiliated Hospital of Zhengzhou University (CN)
- Department of Respiratory Medicine Nantong Sixth People's Hospital Nantong Jiangsu China
- Corresponding author
- Fan, Yihui
- Mao, Renfang
- ORCID
- Venue
- International Journal of Cancer
- Publisher
- Wiley
- Published
- 2020-07
- Volume
- 147
- Issue
- 8
- Pages
- 2210-2224
- ISSN
- 0020-7136 (ISSN-L)
- 1097-0215
- OpenAlex
- W3037502154
- Cited by
- 18
- References
- 73
- Citations by year
- 2026: 1 · 2025: 5 · 2024: 3 · 2023: 4 · 2022: 3 · 2021: 1 · 2020: 1
- FWCI
- 0.73
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- International Journal of Cancer (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Natural Science Foundation of China (30801350, 81600386, 81641164, 31770935)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer-related molecular mechanisms research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
- Keywords
- enhancer RNA, enhancer transcription, lung cancer, histone modifications, transcription factor binding motifs, prognostic factors, c-Myc, small open reading frames, microproteins, cancer hallmarks, multi-omics integration
- MeSH terms
- A549 Cells, Enhancer Elements, Genetic, HeLa Cells, Humans, RNA, Transcription Factors, Transcription, Genetic, Protein Biosynthesis, Genes, myc, Open Reading Frames, K562 Cells, Cell Line, Tumor, Hep G2 Cells, MCF-7 Cells
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review