{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,14]],"date-time":"2026-03-14T06:42:18Z","timestamp":1773470538216,"version":"3.50.1"},"reference-count":25,"publisher":"Oxford University Press (OUP)","issue":"21","license":[{"start":{"date-parts":[[2019,3,27]],"date-time":"2019-03-27T00:00:00Z","timestamp":1553644800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/journals\/pages\/open_access\/funder_policies\/chorus\/standard_publication_model"}],"funder":[{"name":"The Natural Science Foundation of Ningbo","award":["2017A610154"],"award-info":[{"award-number":["2017A610154"]}]},{"name":"The Scientific Innovation Team Project of Ningbo","award":["2016C51001"],"award-info":[{"award-number":["2016C51001"]}]},{"name":"The Student Research and Innovation Program of Ningbo University","award":["2018SRIP1904"],"award-info":[{"award-number":["2018SRIP1904"]}]},{"DOI":"10.13039\/501100020738","name":"K.C. Wong Magna Fund in Ningbo University","doi-asserted-by":"crossref","id":[{"id":"10.13039\/501100020738","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2019,11,1]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:sec>\n                  <jats:title>Motivation<\/jats:title>\n                  <jats:p>Genome-scale CRISPR\/Cas9 system has been a democratized gene editing technique and widely used to investigate gene functions in some biological processes and diseases especially cancers. Aiming to characterize gene aberrations and assess their effects on cancer, we designed a pipeline to identify the essential genes for pan-cancer.<\/jats:p>\n               <\/jats:sec>\n               <jats:sec>\n                  <jats:title>Methods<\/jats:title>\n                  <jats:p>CRISPR screening data were used to identify the essential genes that were collected from published data and integrated by Robust Rank Aggregation algorithm. Then, hypergeometrics test and random walks with restart (RWR) were used to predict additional essential genes on broader scale. Finally, the expression status and potential roles of these genes were explored based on TCGA portal and regulatory network analysis.<\/jats:p>\n               <\/jats:sec>\n               <jats:sec>\n                  <jats:title>Results<\/jats:title>\n                  <jats:p>We collected 926 samples from 10 CRISPR-based screening studies involving 33 different types of cancer to identify cancer-essential genes, which consists of 799 protein-coding genes (PCGs) and 97 long non-coding RNAs (lncRNAs). Then, we constructed a \u2018bi-colored\u2019 network with both PCGs and lncRNAs and applied it to predict additional essential genes including 495 PCGs and 280 lncRNAs on a broader scale using hypergeometrics test and RWR. After obtaining all essential genes, we further investigated their potential roles in cancer and found that essential genes have higher and more stable expression levels, and are associated with multiple cancer-associated biological processes and survival time. The regulatory network analysis detected two intriguing modules of essential genes participating in the regulation of cell cycle and ribosome biogenesis in cancer.<\/jats:p>\n               <\/jats:sec>\n               <jats:sec>\n                  <jats:title>Availability and implementation<\/jats:title>\n                  <jats:p>\u2003<\/jats:p>\n               <\/jats:sec>\n               <jats:sec>\n                  <jats:title>Supplementary information<\/jats:title>\n                  <jats:p>Supplementary data are available at Bioinformatics online.<\/jats:p>\n               <\/jats:sec>","DOI":"10.1093\/bioinformatics\/btz230","type":"journal-article","created":{"date-parts":[[2019,3,26]],"date-time":"2019-03-26T15:13:43Z","timestamp":1553613223000},"page":"4344-4349","source":"Crossref","is-referenced-by-count":8,"title":["Genome-wide identification of the essential protein-coding genes and long non-coding RNAs for human pan-cancer"],"prefix":"10.1093","volume":"35","author":[{"given":"Yuwei","family":"Zhang","sequence":"first","affiliation":[{"name":"Department of Preventative Medicine, Zhejiang Provincial Key Laboratory of Pathological and Physiological Technology, Medicine School of Ningbo University , Ningbo, Zhejiang, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yang","family":"Tao","sequence":"additional","affiliation":[{"name":"Department of Preventative Medicine, Zhejiang Provincial Key Laboratory of Pathological and Physiological Technology, Medicine School of Ningbo University , Ningbo, Zhejiang, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Huihui","family":"Ji","sequence":"additional","affiliation":[{"name":"Zhejiang Provincial Key Laboratory of Pathophysiology, School of Medicine, Ningbo University , Zhejiang, Ningbo, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Wei","family":"Li","sequence":"additional","affiliation":[{"name":"Center for Genetic Medicine Research, Children\u2019s National Medical Center, Department of Genomics and Precision Medicine, George Washington University , Washington, DC, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Xingli","family":"Guo","sequence":"additional","affiliation":[{"name":"School of Computer Science and Technology, Xidian University, Xi\u2019an, Shaanxi Province 710071, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Derry Minyao","family":"Ng","sequence":"additional","affiliation":[{"name":"Department of Preventative Medicine, Zhejiang Provincial Key Laboratory of Pathological and Physiological Technology, Medicine School of Ningbo University , Ningbo, Zhejiang, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Maria","family":"Haleem","sequence":"additional","affiliation":[{"name":"Department of Preventative Medicine, Zhejiang Provincial Key Laboratory of Pathological and Physiological Technology, Medicine School of Ningbo University , Ningbo, Zhejiang, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yang","family":"Xi","sequence":"additional","affiliation":[{"name":"Zhejiang Provincial Key Laboratory of Pathophysiology, School of Medicine, Ningbo University , Zhejiang, Ningbo, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Changzheng","family":"Dong","sequence":"additional","affiliation":[{"name":"Department of Preventative Medicine, Zhejiang Provincial Key Laboratory of Pathological and Physiological Technology, Medicine School of Ningbo University , Ningbo, Zhejiang, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jinshun","family":"Zhao","sequence":"additional","affiliation":[{"name":"Department of Preventative Medicine, Zhejiang Provincial Key Laboratory of Pathological and Physiological Technology, Medicine School of Ningbo University , Ningbo, Zhejiang, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Lina","family":"Zhang","sequence":"additional","affiliation":[{"name":"Department of Preventative Medicine, Zhejiang Provincial Key Laboratory of Pathological and Physiological Technology, Medicine School of Ningbo University , Ningbo, Zhejiang, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Xiaohong","family":"Zhang","sequence":"additional","affiliation":[{"name":"Department of Preventative Medicine, Zhejiang Provincial Key Laboratory of Pathological and Physiological Technology, Medicine School of Ningbo University , Ningbo, Zhejiang, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yangyang","family":"Xie","sequence":"additional","affiliation":[{"name":"Anorectal Surgery, Ningbo Second Hospital , Ningbo, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Xiaoyu","family":"Dai","sequence":"additional","affiliation":[{"name":"Anorectal Surgery, Ningbo Second Hospital , Ningbo, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Qi","family":"Liao","sequence":"additional","affiliation":[{"name":"Department of Preventative Medicine, Zhejiang Provincial Key Laboratory of Pathological and Physiological Technology, Medicine School of Ningbo University , Ningbo, Zhejiang, China"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"286","published-online":{"date-parts":[[2019,3,27]]},"reference":[{"key":"2023062712524302600_btz230-B1","doi-asserted-by":"crossref","first-page":"D844","DOI":"10.1093\/nar\/gku770","article-title":"The Candidate Cancer Gene Database: a database of cancer driver genes from forward genetic screens in mice","volume":"43","author":"Abbott","year":"2015","journal-title":"Nucleic Acids Res"},{"key":"2023062712524302600_btz230-B2","doi-asserted-by":"crossref","first-page":"2.","DOI":"10.1186\/1471-2105-4-2","article-title":"An automated method for finding molecular complexes in large protein interaction networks","volume":"4","author":"Bader","year":"2003","journal-title":"BMC Bioinformatics"},{"key":"2023062712524302600_btz230-B3","doi-asserted-by":"crossref","first-page":"465","DOI":"10.1007\/s13402-018-0395-3","article-title":"Interplay between NRF1, E2F4 and MYC transcription factors regulating common target genes contributes to cancer development and progression","volume":"41","author":"Bhawe","year":"2018","journal-title":"Cell. Oncol"},{"key":"2023062712524302600_btz230-B4","doi-asserted-by":"crossref","first-page":"22","DOI":"10.1016\/j.gde.2017.10.003","article-title":"Ribosome biogenesis and cancer: basic and translational challenges","volume":"48","author":"Bustelo","year":"2017","journal-title":"Curr. Opin. Genet. Dev"},{"key":"2023062712524302600_btz230-B5","doi-asserted-by":"crossref","first-page":"10","DOI":"10.1038\/s41417-017-0006-x","article-title":"LncRNA-SNHG16 predicts poor prognosis and promotes tumor proliferation through epigenetically silencing p21 in bladder cancer","volume":"25","author":"Cao","year":"2017","journal-title":"Cancer Gene Ther"},{"key":"2023062712524302600_btz230-B6","doi-asserted-by":"crossref","first-page":"1310.","DOI":"10.3390\/ijms19051310","article-title":"Noncoding RNA: RNA regulatory networks in cancer","volume":"19","author":"Chan","year":"2018","journal-title":"Int. J. Mol. Sci"},{"key":"2023062712524302600_btz230-B7","doi-asserted-by":"crossref","first-page":"819","DOI":"10.1126\/science.1231143","article-title":"Multiplex genome engineering using CRISPR\/Cas systems","volume":"339","author":"Cong","year":"2013","journal-title":"Science"},{"key":"2023062712524302600_btz230-B8","doi-asserted-by":"crossref","first-page":"190","DOI":"10.1016\/j.acthis.2017.01.009","article-title":"Ribosome biogenesis and cancer","volume":"119","author":"Derenzini","year":"2017","journal-title":"Acta Histochem"},{"key":"2023062712524302600_btz230-B9","first-page":"e12.","article-title":"Challenges of CRISPR\/Cas9 applications for long non-coding RNA genes","volume":"45","author":"Goyal","year":"2017","journal-title":"Nucleic Acids Res"},{"key":"2023062712524302600_btz230-B10","doi-asserted-by":"crossref","first-page":"733.","DOI":"10.15252\/msb.20145216","article-title":"Measuring error rates in genomic perturbation screens: gold standards for human functional genomics","volume":"10","author":"Hart","year":"2014","journal-title":"Mol. Syst. Biol"},{"key":"2023062712524302600_btz230-B11","doi-asserted-by":"crossref","first-page":"1515","DOI":"10.1016\/j.cell.2015.11.015","article-title":"High-resolution CRISPR screens reveal fitness genes and genotype-specific cancer liabilities","volume":"163","author":"Hart","year":"2015","journal-title":"Cell"},{"key":"2023062712524302600_btz230-B12","doi-asserted-by":"crossref","first-page":"2719","DOI":"10.1534\/g3.117.041277","article-title":"Evaluation and design of genome-wide CRISPR\/SpCas9 knockout screens","volume":"7","author":"Hart","year":"2017","journal-title":"G3"},{"key":"2023062712524302600_btz230-B13","doi-asserted-by":"crossref","first-page":"573","DOI":"10.1093\/bioinformatics\/btr709","article-title":"Robust rank aggregation for gene list integration and meta-analysis","volume":"28","author":"Kolde","year":"2012","journal-title":"Bioinformatics"},{"key":"2023062712524302600_btz230-B14","doi-asserted-by":"crossref","first-page":"554.","DOI":"10.1186\/s13059-014-0554-4","article-title":"MAGeCK enables robust identification of essential genes from genome-scale CRISPR\/Cas9 knockout screens","volume":"15","author":"Li","year":"2014","journal-title":"Genome Biol"},{"key":"2023062712524302600_btz230-B15","article-title":"Long noncoding RNA PVT1 as a novel predictor of metastasis, clinicopathological characteristics and prognosis in human cancers: a meta-analysis","author":"Liu","year":"2018","journal-title":"Pathol. Oncol. Res"},{"key":"2023062712524302600_btz230-B16","doi-asserted-by":"crossref","first-page":"eaah7111","DOI":"10.1126\/science.aah7111","article-title":"CRISPRi-based genome-scale identification of functional long noncoding RNA loci in human cells","volume":"355","author":"Liu","year":"2017","journal-title":"Science"},{"key":"2023062712524302600_btz230-B17","doi-asserted-by":"crossref","first-page":"172","DOI":"10.1158\/2159-8290.CD-11-0224","article-title":"Essential gene profiles in breast, pancreatic, and ovarian cancer cells","volume":"2","author":"Marcotte","year":"2012","journal-title":"Cancer Discov"},{"key":"2023062712524302600_btz230-B18","doi-asserted-by":"crossref","first-page":"648","DOI":"10.1093\/nar\/gkq758","article-title":"The NIP7 protein is required for accurate pre-rRNA processing in human cells","volume":"39","author":"Morello","year":"2011","journal-title":"Nucleic Acids Res"},{"key":"2023062712524302600_btz230-B19","doi-asserted-by":"crossref","first-page":"D980","DOI":"10.1093\/nar\/gkv1094","article-title":"Lnc2Cancer: a manually curated database of experimentally supported lncRNAs associated with various human cancers","volume":"44","author":"Ning","year":"2016","journal-title":"Nucleic Acids Res"},{"key":"2023062712524302600_btz230-B20","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1038\/nrc.2017.104","article-title":"Ribosome biogenesis in cancer: new players and therapeutic avenues","volume":"18","author":"Pelletier","year":"2017","journal-title":"Nat. Rev. Cancer"},{"key":"2023062712524302600_btz230-B21","doi-asserted-by":"crossref","first-page":"D362","DOI":"10.1093\/nar\/gkw937","article-title":"The STRING database in 2017: quality-controlled protein\u2013protein association networks, made broadly accessible","volume":"45","author":"Szklarczyk","year":"2017","journal-title":"Nucleic Acids Res"},{"key":"2023062712524302600_btz230-B22","first-page":"4796","article-title":"The ribosome biogenesis factor yUtp23\/hUTP23 coordinates key interactions in the yeast and human pre-40S particle and hUTP23 contains an essential PIN domain","volume":"45","author":"Wells","year":"2017","journal-title":"Nucleic Acids Res"},{"key":"2023062712524302600_btz230-B23","doi-asserted-by":"crossref","first-page":"2786.","DOI":"10.12659\/MSM.907389","article-title":"Expression of the long intergenic non-protein coding RNA 665 (LINC00665) gene and the cell cycle in hepatocellular carcinoma using The Cancer Genome Atlas, the Gene Expression Omnibus, and Quantitative Real-Time Polymerase Chain Reaction","volume":"24","author":"Wen","year":"2018","journal-title":"Med. Sci. Monit"},{"key":"2023062712524302600_btz230-B24","doi-asserted-by":"crossref","first-page":"23757","DOI":"10.18632\/oncotarget.8121","article-title":"Upregulation of E2F8 promotes cell proliferation and tumorigenicity in breast cancer by modulating G1\/S phase transition","volume":"7","author":"Ye","year":"2016","journal-title":"Oncotarget"},{"key":"2023062712524302600_btz230-B25","doi-asserted-by":"crossref","first-page":"1279","DOI":"10.1038\/nbt.3715","article-title":"Genome-scale deletion screening of human long non-coding RNAs using a paired-guide RNA CRISPR-Cas9 library","volume":"34","author":"Zhu","year":"2016","journal-title":"Nat. Biotechnol"}],"container-title":["Bioinformatics"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/academic.oup.com\/bioinformatics\/advance-article-pdf\/doi\/10.1093\/bioinformatics\/btz230\/28492229\/btz230.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/bioinformatics\/article-pdf\/35\/21\/4344\/50721923\/bioinformatics_35_21_4344.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/bioinformatics\/article-pdf\/35\/21\/4344\/50721923\/bioinformatics_35_21_4344.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,6,27]],"date-time":"2023-06-27T12:53:22Z","timestamp":1687870402000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/bioinformatics\/article\/35\/21\/4344\/5421514"}},"subtitle":[],"editor":[{"given":"Russell","family":"Schwartz","sequence":"additional","affiliation":[],"role":[{"role":"editor","vocabulary":"crossref"}]}],"short-title":[],"issued":{"date-parts":[[2019,3,27]]},"references-count":25,"journal-issue":{"issue":"21","published-print":{"date-parts":[[2019,11,1]]}},"URL":"https:\/\/doi.org\/10.1093\/bioinformatics\/btz230","relation":{},"ISSN":["1367-4803","1367-4811"],"issn-type":[{"value":"1367-4803","type":"print"},{"value":"1367-4811","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2019,11,1]]},"published":{"date-parts":[[2019,3,27]]}}}