Biochemical and molecular study of long non-coding RNAs (HOTTIP, ZEB-AS1 and MEG-3) in hepatocellular carcinoma

Hepatocellular carcinoma (HCC) is a main cause of cancer death worldwide. The high mortality of HCC patients is linked to delayed diagnosis. Long non-coding RNAs (lncRNAs) have been demonstrated as significant controllers of various human cancers. This study aimed to clarify the potential diagnostic...

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Published inMeta Gene Vol. 26; p. 100808
Main Authors Soliman, Shimaa E., ElTorgoman, Abdel Monem A., Assar, Mohamed F.A., El Abd, Naglaa S., Gohar, Suzy F., Girgis, Raouth E.
Format Journal Article
LanguageEnglish
Published Elsevier B.V 01.12.2020
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Abstract Hepatocellular carcinoma (HCC) is a main cause of cancer death worldwide. The high mortality of HCC patients is linked to delayed diagnosis. Long non-coding RNAs (lncRNAs) have been demonstrated as significant controllers of various human cancers. This study aimed to clarify the potential diagnostic and prognostic value of lncRNAs (HOTTIP, ZEB-AS1 and MEG3) in HCC. This study included 150 subjects (50 HCC patients, 50 cirrhotic patients and 50 healthy subjects). lncRNA gene expression was estimated by real-time PCR. HOTTIP and ZEB-AS1 levels were higher in HCC patients than in cirrhotic patients and healthy individuals (P < 0.001). The level of MEG-3 was significantly lower in the HCC group than in the cirrhotic and control groups (P < 0.001). In HCC patients, higher HOTTIP and ZEB-AS1 were linked with nodal and distant metastases, and lower MEG-3 was correlated with larger tumour size; additionally, higher HOTTIP and lower MEG-3 were associated with lower overall survival. ROC curve analysis revealed cut-off values >10.35 > 15 and < 2.3 for HOTTIP, ZEB-AS1 and MEG-3, respectively. HOTTIP, ZEB-AS1 and MEG-3 could be considered diagnostic biomarkers for HCC, and HOTTIP and MEG-3 may represent prognostic biomarkers for HCC.
AbstractList Hepatocellular carcinoma (HCC) is a main cause of cancer death worldwide. The high mortality of HCC patients is linked to delayed diagnosis. Long non-coding RNAs (lncRNAs) have been demonstrated as significant controllers of various human cancers. This study aimed to clarify the potential diagnostic and prognostic value of lncRNAs (HOTTIP, ZEB-AS1 and MEG3) in HCC. This study included 150 subjects (50 HCC patients, 50 cirrhotic patients and 50 healthy subjects). lncRNA gene expression was estimated by real-time PCR. HOTTIP and ZEB-AS1 levels were higher in HCC patients than in cirrhotic patients and healthy individuals (P < 0.001). The level of MEG-3 was significantly lower in the HCC group than in the cirrhotic and control groups (P < 0.001). In HCC patients, higher HOTTIP and ZEB-AS1 were linked with nodal and distant metastases, and lower MEG-3 was correlated with larger tumour size; additionally, higher HOTTIP and lower MEG-3 were associated with lower overall survival. ROC curve analysis revealed cut-off values >10.35 > 15 and < 2.3 for HOTTIP, ZEB-AS1 and MEG-3, respectively. HOTTIP, ZEB-AS1 and MEG-3 could be considered diagnostic biomarkers for HCC, and HOTTIP and MEG-3 may represent prognostic biomarkers for HCC.
ArticleNumber 100808
Author El Abd, Naglaa S.
ElTorgoman, Abdel Monem A.
Soliman, Shimaa E.
Assar, Mohamed F.A.
Gohar, Suzy F.
Girgis, Raouth E.
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Cites_doi 10.1517/14728222.2014.941285
10.1074/jbc.M702029200
10.1158/0008-5472.CAN-09-3885
10.1002/hep.26740
10.1038/onc.2011.193
10.3748/wjg.v23.i32.5860
10.1016/S0140-6736(11)61347-0
10.1111/liv.12746
10.1053/j.gastro.2006.08.026
10.1016/S1590-8658(10)60507-5
10.3322/caac.20085
10.1186/s12967-016-1085-4
10.1038/jid.2011.142
10.23736/S0026-4806.16.04668-1
10.1016/j.cellsig.2014.01.008
10.1002/mc.22270
10.3390/ijms21082883
10.4161/rna.20481
10.18632/oncotarget.12981
10.1038/modpathol.2008.82
10.1038/nature08975
10.1038/nature09819
10.1210/en.2009-0657
10.1002/ijc.30211
10.3816/CLM.2008.n.021
10.1097/MCG.0b013e3182872f29
10.1371/journal.pgen.1005726
10.1053/j.gastro.2007.04.061
10.1371/journal.pgen.1003569
10.1158/0008-5472.CAN-07-2559
10.1038/nrc1934
10.1146/annurev-genom-090711-163752
10.1159/000438577
10.1038/onc.2015.223
10.1016/j.cell.2013.08.028
10.3892/ijo.2017.4164
10.1016/j.bbrc.2014.08.001
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Keywords Real-time PCR
Hepatocellular carcinoma
lncRNAs (HOTTIP, ZEB-AS1, MEG3)
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References Li, Xie, Shen, Cheng, Shi, Wu, Deng, Chen, Shen, Peng, Li, Zhan, Zhu (bb0080) 2016; 35
Panzitt, Tschernatsch, Guelly, Moustafa, Stradner, Strohmaier, Buck (bb0115) 2007; 132
Ge, Yan, Jin, Yang, Yu, Zhou, Han, Yuan, Yang (bb0035) 2015; 11
Kim, Park, Lee (bb0070) 2020; 21
Farazi, DePinho (bb0025) 2006; 6
Hu, Li, Ding, Pu, Liu, Xiong (bb0065) 2017; 108
Zhang, Rice, Wang, Chen, Zhong, Nakayama, Zhou, Klibanski (bb0185) 2010(b); 151
Orom, Shiekhattar (bb0110) 2013; 154
Benetatos, Dasoula, Hatzimichael, Georgiou, Syrrou, Bourantas (bb0005) 2008; 8
Wels, Joshi, Koefinger, Bergler, Schaider (bb0160) 2011; 131
Gutschner, Diederichs (bb0050) 2012; 9
Taby, Issa (bb0140) 2010; 60
Hangauer, Vaughn, McManus (bb0060) 2013; 9
Li, Guan, Liu, Gan (bb0075) 2019; 17
Zhao, Greene, Gray, Lawless (bb0195) 2014; 18
Mittal, El-Serag (bb0095) 2013; 47
Zhang, Huang, Cai1, Yu, Chen, Pan, He, Lv, Feng, Chen (bb0190) 2017; 51
Han (bb0055) 2012; 13
Graham, Zhau, Odero-Marah, Osunkoya, Kimbro, Tighiouart (bb0040) 2008; 68
Nordenstedt, White, El-Serag (bb0105) 2010; 42
Zhou, Zhong, Wang, Zhang, Batista, Gejman (bb0200) 2007; 282
El-Serag, Rudolph (bb0020) 2007; 132
Liu, Lin (bb0085) 2016; 8
Xiong, Han, Wu, Zhao, Han, Wang, Ping, Zheng, Feng, Qin, He (bb0165) 2018; 10
Zhang, Matsuura, Kleiner, Zamboni, Alter, Farci (bb0175) 2016; 14
Gupta, Shah, Wang, Kim, Horlings, Wong, Tsai (bb0045) 2010; 464
Zhang, Gejman, Mahta, Zhong, Rice, Zhou (bb0180) 2010(a); 70
Chen, He, Wang, Liu, Huang (bb0015) 2017; 8
Zhan, Huang, Meng, Song, Wu, Miu, Zhan, Li (bb0170) 2014; 26
Forner, Llovet, Bruix (bb0030) 2012; 379
Singh, Spoelstra, Jean, Howe, Torkko, Clark, Darling, Shroyer, Horwitz, Broaddus, Richer (bb0130) 2008; 21
Niu, Niu, Wang (bb0100) 2017; 23
Wang, Yang, Liu, Sanyal, Corces-Zimmerman, Chen, Lajoie, Protacio, Flynn, Gupta, Wysocka, Lei, Dekker, Helms, Chang (bb0155) 2011; 472
Luo, Wang, Wu, Tao, Xiao, Wang, Min, Zeng, Jiang (bb0090) 2015; 37
Braconi, Kogure, Valeri1, Huang, Nuovo, S Costinean, Negrini, Miotto, Croce, Pate (bb0010) 2011; 30
Petrick, Braunlin, Laversanne, Valery, Bray, McGlynn (bb0120) 2016; 139
Toiyama, Okugawa, Goel (bb0145) 2014; 455
Quagliata, Matter, Piscuoglio, Arabi, Ruiz, Procino, Kovac, Moretti, Makowska, Boldanova (bb0125) 2014; 59
Zhuo, Tang, Lin, Jiang, Zhang, Ji, Wang, Sun (bb0205) 2016; 55
Tsang, Au, Wei, Fan, Lee, Wong, Ng, Wong (bb0150) 2015; 35
Liu (10.1016/j.mgene.2020.100808_bb0085) 2016; 8
Benetatos (10.1016/j.mgene.2020.100808_bb0005) 2008; 8
Hangauer (10.1016/j.mgene.2020.100808_bb0060) 2013; 9
Zhang (10.1016/j.mgene.2020.100808_bb0180) 2010; 70
Wels (10.1016/j.mgene.2020.100808_bb0160) 2011; 131
Wang (10.1016/j.mgene.2020.100808_bb0155) 2011; 472
Farazi (10.1016/j.mgene.2020.100808_bb0025) 2006; 6
Hu (10.1016/j.mgene.2020.100808_bb0065) 2017; 108
Toiyama (10.1016/j.mgene.2020.100808_bb0145) 2014; 455
Braconi (10.1016/j.mgene.2020.100808_bb0010) 2011; 30
Gutschner (10.1016/j.mgene.2020.100808_bb0050) 2012; 9
Tsang (10.1016/j.mgene.2020.100808_bb0150) 2015; 35
Luo (10.1016/j.mgene.2020.100808_bb0090) 2015; 37
Singh (10.1016/j.mgene.2020.100808_bb0130) 2008; 21
Zhang (10.1016/j.mgene.2020.100808_bb0190) 2017; 51
Quagliata (10.1016/j.mgene.2020.100808_bb0125) 2014; 59
Zhang (10.1016/j.mgene.2020.100808_bb0175) 2016; 14
Mittal (10.1016/j.mgene.2020.100808_bb0095) 2013; 47
Li (10.1016/j.mgene.2020.100808_bb0080) 2016; 35
Gupta (10.1016/j.mgene.2020.100808_bb0045) 2010; 464
Kim (10.1016/j.mgene.2020.100808_bb0070) 2020; 21
Xiong (10.1016/j.mgene.2020.100808_bb0165) 2018; 10
Chen (10.1016/j.mgene.2020.100808_bb0015) 2017; 8
Zhao (10.1016/j.mgene.2020.100808_bb0195) 2014; 18
Zhou (10.1016/j.mgene.2020.100808_bb0200) 2007; 282
El-Serag (10.1016/j.mgene.2020.100808_bb0020) 2007; 132
Orom (10.1016/j.mgene.2020.100808_bb0110) 2013; 154
Taby (10.1016/j.mgene.2020.100808_bb0140) 2010; 60
Panzitt (10.1016/j.mgene.2020.100808_bb0115) 2007; 132
Ge (10.1016/j.mgene.2020.100808_bb0035) 2015; 11
Han (10.1016/j.mgene.2020.100808_bb0055) 2012; 13
Forner (10.1016/j.mgene.2020.100808_bb0030) 2012; 379
Zhang (10.1016/j.mgene.2020.100808_bb0185) 2010; 151
Li (10.1016/j.mgene.2020.100808_bb0075) 2019; 17
Petrick (10.1016/j.mgene.2020.100808_bb0120) 2016; 139
Nordenstedt (10.1016/j.mgene.2020.100808_bb0105) 2010; 42
Zhan (10.1016/j.mgene.2020.100808_bb0170) 2014; 26
Zhuo (10.1016/j.mgene.2020.100808_bb0205) 2016; 55
Graham (10.1016/j.mgene.2020.100808_bb0040) 2008; 68
Niu (10.1016/j.mgene.2020.100808_bb0100) 2017; 23
References_xml – volume: 282
  start-page: 24731
  year: 2007
  end-page: 24742
  ident: bb0200
  article-title: Activation of p53 by MEG3 non-coding RNA
  publication-title: J. Biol. Chem.
  contributor:
    fullname: Gejman
– volume: 8
  start-page: 14126
  year: 2017
  end-page: 14132
  ident: bb0015
  article-title: Long noncoding RNA HOTTIP as a novel predictor of lymph node metastasis and survival in human cancer: a systematic review and meta-analysis
  publication-title: Oncotarget
  contributor:
    fullname: Huang
– volume: 11
  year: 2015
  ident: bb0035
  article-title: MiRNA-192 [corrected] and miRNA-204 directly suppress lncRNA HOTTIP and interrupt GLS1-mediated Glutaminolysis in hepatocellular carcinoma
  publication-title: PLoS Genet.
  contributor:
    fullname: Yang
– volume: 8
  start-page: 171
  year: 2008
  end-page: 175
  ident: bb0005
  article-title: Promoter hypermethylation of the MEG3 (DLK1/MEG3) imprinted gene in multiple myeloma
  publication-title: Clin. Lymphoma Myeloma
  contributor:
    fullname: Bourantas
– volume: 9
  year: 2013
  ident: bb0060
  article-title: Pervasive transcription of the human genome produces thousands of previously unidentified long intergenic noncoding RNAs
  publication-title: PLoS Genet.
  contributor:
    fullname: McManus
– volume: 472
  start-page: 120
  year: 2011
  end-page: 124
  ident: bb0155
  article-title: A long noncoding RNA maintains active chromatin to coordinate homeotic gene expression
  publication-title: Nature.
  contributor:
    fullname: Chang
– volume: 379
  start-page: 1245
  year: 2012
  end-page: 1255
  ident: bb0030
  article-title: Hepatocellular carcinoma
  publication-title: Lancet.
  contributor:
    fullname: Bruix
– volume: 10
  start-page: 605
  year: 2018
  end-page: 617
  ident: bb0165
  article-title: Interplay between long noncoding RNA ZEB1-AS1and miR-101/ZEB1 axis regulates proliferation and migration of colorectal cancer cells
  publication-title: Am. J. Transl. Res.
  contributor:
    fullname: He
– volume: 37
  start-page: 2209
  year: 2015
  end-page: 2220
  ident: bb0090
  article-title: Long non-coding RNA MEG3 inhibits cell proliferation and induces apoptosis in prostate cancer
  publication-title: Cell. Physiol. Biochem.
  contributor:
    fullname: Jiang
– volume: 70
  start-page: 2350
  year: 2010(a)
  end-page: 2358
  ident: bb0180
  article-title: Maternally expressed gene 3, an imprinted noncoding RNA gene, is associated with meningioma pathogenesis and progression
  publication-title: Cancer Res.
  contributor:
    fullname: Zhou
– volume: 154
  start-page: 1190
  year: 2013
  end-page: 1193
  ident: bb0110
  article-title: Long noncoding RNAs usher in a new era in the biology of enhancers
  publication-title: Cell
  contributor:
    fullname: Shiekhattar
– volume: 9
  start-page: 703
  year: 2012
  end-page: 719
  ident: bb0050
  article-title: The hallmarks of cancer: a long non-coding RNA point of view
  publication-title: RNA Biol.
  contributor:
    fullname: Diederichs
– volume: 21
  start-page: 2883
  year: 2020
  ident: bb0070
  article-title: LncRNAs act as a link between chronic liver disease and hepatocellular carcinoma
  publication-title: Int. J. Mol. Sci.
  contributor:
    fullname: Lee
– volume: 23
  start-page: 5860
  year: 2017
  end-page: 5874
  ident: bb0100
  article-title: Long non-coding RNAs in hepatocellular carcinoma: potential roles and clinical implications
  publication-title: World J. Gastroenterol.
  contributor:
    fullname: Wang
– volume: 132
  start-page: 330
  year: 2007
  end-page: 342
  ident: bb0115
  article-title: Characterization of HULC, a novel gene with striking up-regulation in hepatocellular carcinoma, as noncoding RNA
  publication-title: Gastroenterology
  contributor:
    fullname: Buck
– volume: 131
  start-page: 1877
  year: 2011
  end-page: 1885
  ident: bb0160
  article-title: Transcriptional activation of ZEB1 by Slug leads to cooperative regulation of the epithelialmesenchymal transition-like phenotype in melanoma
  publication-title: J. Invest. Dermatol.
  contributor:
    fullname: Schaider
– volume: 47
  start-page: S2
  year: 2013
  end-page: S6
  ident: bb0095
  article-title: Epidemiology of hepatocellular carcinoma: consider the population
  publication-title: J. Clin. Gastroenterol.
  contributor:
    fullname: El-Serag
– volume: 60
  start-page: 376
  year: 2010
  end-page: 392
  ident: bb0140
  article-title: Cancer epigenetics
  publication-title: CA Cancer J. Clin.
  contributor:
    fullname: Issa
– volume: 26
  start-page: 1075
  year: 2014
  end-page: 1081
  ident: bb0170
  article-title: Promising roles of mammalian E2Fs in hepatocellular carcinoma
  publication-title: Cell. Signal.
  contributor:
    fullname: Li
– volume: 8
  start-page: 4095
  year: 2016
  end-page: 4105
  ident: bb0085
  article-title: Long noncoding RNA ZEB1 AS1 acts as an oncogene in osteosarcoma by epigenetically activating ZEB1
  publication-title: Am. J. Transl. Res.
  contributor:
    fullname: Lin
– volume: 59
  start-page: 911
  year: 2014
  end-page: 923
  ident: bb0125
  article-title: Long noncoding RNA HOTTIP/HOXA13 expression is associated with disease progression and predicts outcome in hepatocellular carcinoma patients
  publication-title: Hepatology.
  contributor:
    fullname: Boldanova
– volume: 464
  start-page: 1071
  year: 2010
  end-page: 1076
  ident: bb0045
  article-title: Long non-coding RNA HOTAIR reprograms chromatin state to promote cancer metastasis
  publication-title: Nature.
  contributor:
    fullname: Tsai
– volume: 455
  start-page: 43
  year: 2014
  end-page: 57
  ident: bb0145
  article-title: DNA methylation and microRNA biomarkers for noninvasive detection of gastric and colorectal cancer
  publication-title: Biochem. Biophys. Res. Commun.
  contributor:
    fullname: Goel
– volume: 108
  start-page: 95
  year: 2017
  end-page: 97
  ident: bb0065
  article-title: Long noncoding RNA HOTTIP, a novel potential prognostic marker in cancers
  publication-title: Minerva Med.
  contributor:
    fullname: Xiong
– volume: 21
  start-page: 912
  year: 2008
  end-page: 923
  ident: bb0130
  article-title: ZEB1 expression in type I vs type II endometrial cancers: a marker of aggressive disease
  publication-title: Mod. Pathol.
  contributor:
    fullname: Richer
– volume: 35
  start-page: 1575
  year: 2016
  end-page: 1584
  ident: bb0080
  article-title: Up-regulation of long noncoding RNA ZEB1-AS1 promotes tumor metastasis and predicts poor prognosis in hepatocellular carcinoma
  publication-title: Oncogene.
  contributor:
    fullname: Zhu
– volume: 35
  start-page: 1597
  year: 2015
  end-page: 1606
  ident: bb0150
  article-title: Long non-coding RNA HOTTIP is frequently upregulated in hepatocellular carcinoma and is targeted by tumour suppressive miR-125b
  publication-title: Liver Int.
  contributor:
    fullname: Wong
– volume: 30
  start-page: 4750
  year: 2011
  end-page: 4756
  ident: bb0010
  article-title: microRNA-29 can regulate expression of the long non-coding RNA gene MEG3 in hepatocellular cancer
  publication-title: Oncogene.
  contributor:
    fullname: Pate
– volume: 132
  start-page: 2557
  year: 2007
  end-page: 2576
  ident: bb0020
  article-title: Hepatocellular carcinoma: epidemiology and molecular carcinogenesis
  publication-title: Gastroenterology.
  contributor:
    fullname: Rudolph
– volume: 151
  start-page: 939
  year: 2010(b)
  end-page: 947
  ident: bb0185
  article-title: Maternally expressed gene 3 (MEG3)noncoding ribonucleic acid: isoform structure, expression, and functions
  publication-title: Endocrinology.
  contributor:
    fullname: Klibanski
– volume: 6
  start-page: 674
  year: 2006
  end-page: 687
  ident: bb0025
  article-title: Hepatocellular carcinoma pathogenesis: from genes to environment
  publication-title: Nat. Rev. Cancer
  contributor:
    fullname: DePinho
– volume: 17
  start-page: 3539
  year: 2019
  end-page: 3547
  ident: bb0075
  article-title: LncRNA ZEB1-AS1 reduces liver cancer cell proliferation by targeting miR-365a-3p
  publication-title: Exp. Ther. Med.
  contributor:
    fullname: Gan
– volume: 139
  start-page: 1534
  year: 2016
  end-page: 1545
  ident: bb0120
  article-title: International trends in liver cancer incidence, overall and by histologic subtype, 1978–2007
  publication-title: Int. J. Cancer
  contributor:
    fullname: McGlynn
– volume: 51
  start-page: 1705
  year: 2017
  end-page: 1721
  ident: bb0190
  article-title: Long non-coding RNA HOTTIP promotes hepatocellular carcinoma tumorigenesis and development: a comprehensive investigation based on bioinformatics, qRT-PCR and meta-analysis of 393 cases
  publication-title: Int. J. Oncol.
  contributor:
    fullname: Chen
– volume: 68
  start-page: 2479
  year: 2008
  end-page: 2488
  ident: bb0040
  article-title: Insulin-like growth factor-I-dependent up-regulation of ZEB1 drives epithelial-to-mesenchymal transition in human prostate cancer cells
  publication-title: Cancer Res.
  contributor:
    fullname: Tighiouart
– volume: 42
  start-page: S206
  year: 2010
  end-page: S214
  ident: bb0105
  article-title: The changing pattern of epidemiology in hepatocellular carcinoma
  publication-title: Dig. Liver Dis.
  contributor:
    fullname: El-Serag
– volume: 14
  start-page: 328
  year: 2016
  ident: bb0175
  article-title: Analysis of long noncoding RNA expression in hepatocellular carcinoma of different viral etiology
  publication-title: J. Transl. Med.
  contributor:
    fullname: Farci
– volume: 55
  start-page: 209
  year: 2016
  end-page: 219
  ident: bb0205
  article-title: The aberrant expression of MEG3 regulated by UHRF1 predicts the prognosis of hepatocellular carcinoma
  publication-title: Mol. Carcinog.
  contributor:
    fullname: Sun
– volume: 13
  start-page: 171
  year: 2012
  end-page: 205
  ident: bb0055
  article-title: Functional genomic studies: insights into the pathogenesis of liver cancer
  publication-title: Annu. Rev. Genomics Hum. Genet.
  contributor:
    fullname: Han
– volume: 18
  start-page: 1207
  year: 2014
  end-page: 1218
  ident: bb0195
  article-title: Long noncoding RNAs in liver cancer: what we know in 2014
  publication-title: Expert Opin. Ther. Targets
  contributor:
    fullname: Lawless
– volume: 18
  start-page: 1207
  year: 2014
  ident: 10.1016/j.mgene.2020.100808_bb0195
  article-title: Long noncoding RNAs in liver cancer: what we know in 2014
  publication-title: Expert Opin. Ther. Targets
  doi: 10.1517/14728222.2014.941285
  contributor:
    fullname: Zhao
– volume: 17
  start-page: 3539
  year: 2019
  ident: 10.1016/j.mgene.2020.100808_bb0075
  article-title: LncRNA ZEB1-AS1 reduces liver cancer cell proliferation by targeting miR-365a-3p
  publication-title: Exp. Ther. Med.
  contributor:
    fullname: Li
– volume: 282
  start-page: 24731
  year: 2007
  ident: 10.1016/j.mgene.2020.100808_bb0200
  article-title: Activation of p53 by MEG3 non-coding RNA
  publication-title: J. Biol. Chem.
  doi: 10.1074/jbc.M702029200
  contributor:
    fullname: Zhou
– volume: 70
  start-page: 2350
  year: 2010
  ident: 10.1016/j.mgene.2020.100808_bb0180
  article-title: Maternally expressed gene 3, an imprinted noncoding RNA gene, is associated with meningioma pathogenesis and progression
  publication-title: Cancer Res.
  doi: 10.1158/0008-5472.CAN-09-3885
  contributor:
    fullname: Zhang
– volume: 59
  start-page: 911
  year: 2014
  ident: 10.1016/j.mgene.2020.100808_bb0125
  article-title: Long noncoding RNA HOTTIP/HOXA13 expression is associated with disease progression and predicts outcome in hepatocellular carcinoma patients
  publication-title: Hepatology.
  doi: 10.1002/hep.26740
  contributor:
    fullname: Quagliata
– volume: 30
  start-page: 4750
  year: 2011
  ident: 10.1016/j.mgene.2020.100808_bb0010
  article-title: microRNA-29 can regulate expression of the long non-coding RNA gene MEG3 in hepatocellular cancer
  publication-title: Oncogene.
  doi: 10.1038/onc.2011.193
  contributor:
    fullname: Braconi
– volume: 23
  start-page: 5860
  year: 2017
  ident: 10.1016/j.mgene.2020.100808_bb0100
  article-title: Long non-coding RNAs in hepatocellular carcinoma: potential roles and clinical implications
  publication-title: World J. Gastroenterol.
  doi: 10.3748/wjg.v23.i32.5860
  contributor:
    fullname: Niu
– volume: 379
  start-page: 1245
  year: 2012
  ident: 10.1016/j.mgene.2020.100808_bb0030
  article-title: Hepatocellular carcinoma
  publication-title: Lancet.
  doi: 10.1016/S0140-6736(11)61347-0
  contributor:
    fullname: Forner
– volume: 10
  start-page: 605
  year: 2018
  ident: 10.1016/j.mgene.2020.100808_bb0165
  article-title: Interplay between long noncoding RNA ZEB1-AS1and miR-101/ZEB1 axis regulates proliferation and migration of colorectal cancer cells
  publication-title: Am. J. Transl. Res.
  contributor:
    fullname: Xiong
– volume: 35
  start-page: 1597
  year: 2015
  ident: 10.1016/j.mgene.2020.100808_bb0150
  article-title: Long non-coding RNA HOTTIP is frequently upregulated in hepatocellular carcinoma and is targeted by tumour suppressive miR-125b
  publication-title: Liver Int.
  doi: 10.1111/liv.12746
  contributor:
    fullname: Tsang
– volume: 132
  start-page: 330
  year: 2007
  ident: 10.1016/j.mgene.2020.100808_bb0115
  article-title: Characterization of HULC, a novel gene with striking up-regulation in hepatocellular carcinoma, as noncoding RNA
  publication-title: Gastroenterology
  doi: 10.1053/j.gastro.2006.08.026
  contributor:
    fullname: Panzitt
– volume: 42
  start-page: S206
  issue: Suppl. 3
  year: 2010
  ident: 10.1016/j.mgene.2020.100808_bb0105
  article-title: The changing pattern of epidemiology in hepatocellular carcinoma
  publication-title: Dig. Liver Dis.
  doi: 10.1016/S1590-8658(10)60507-5
  contributor:
    fullname: Nordenstedt
– volume: 60
  start-page: 376
  year: 2010
  ident: 10.1016/j.mgene.2020.100808_bb0140
  article-title: Cancer epigenetics
  publication-title: CA Cancer J. Clin.
  doi: 10.3322/caac.20085
  contributor:
    fullname: Taby
– volume: 14
  start-page: 328
  year: 2016
  ident: 10.1016/j.mgene.2020.100808_bb0175
  article-title: Analysis of long noncoding RNA expression in hepatocellular carcinoma of different viral etiology
  publication-title: J. Transl. Med.
  doi: 10.1186/s12967-016-1085-4
  contributor:
    fullname: Zhang
– volume: 131
  start-page: 1877
  year: 2011
  ident: 10.1016/j.mgene.2020.100808_bb0160
  article-title: Transcriptional activation of ZEB1 by Slug leads to cooperative regulation of the epithelialmesenchymal transition-like phenotype in melanoma
  publication-title: J. Invest. Dermatol.
  doi: 10.1038/jid.2011.142
  contributor:
    fullname: Wels
– volume: 108
  start-page: 95
  year: 2017
  ident: 10.1016/j.mgene.2020.100808_bb0065
  article-title: Long noncoding RNA HOTTIP, a novel potential prognostic marker in cancers
  publication-title: Minerva Med.
  doi: 10.23736/S0026-4806.16.04668-1
  contributor:
    fullname: Hu
– volume: 26
  start-page: 1075
  year: 2014
  ident: 10.1016/j.mgene.2020.100808_bb0170
  article-title: Promising roles of mammalian E2Fs in hepatocellular carcinoma
  publication-title: Cell. Signal.
  doi: 10.1016/j.cellsig.2014.01.008
  contributor:
    fullname: Zhan
– volume: 55
  start-page: 209
  year: 2016
  ident: 10.1016/j.mgene.2020.100808_bb0205
  article-title: The aberrant expression of MEG3 regulated by UHRF1 predicts the prognosis of hepatocellular carcinoma
  publication-title: Mol. Carcinog.
  doi: 10.1002/mc.22270
  contributor:
    fullname: Zhuo
– volume: 21
  start-page: 2883
  issue: 8
  year: 2020
  ident: 10.1016/j.mgene.2020.100808_bb0070
  article-title: LncRNAs act as a link between chronic liver disease and hepatocellular carcinoma
  publication-title: Int. J. Mol. Sci.
  doi: 10.3390/ijms21082883
  contributor:
    fullname: Kim
– volume: 9
  start-page: 703
  year: 2012
  ident: 10.1016/j.mgene.2020.100808_bb0050
  article-title: The hallmarks of cancer: a long non-coding RNA point of view
  publication-title: RNA Biol.
  doi: 10.4161/rna.20481
  contributor:
    fullname: Gutschner
– volume: 8
  start-page: 14126
  year: 2017
  ident: 10.1016/j.mgene.2020.100808_bb0015
  article-title: Long noncoding RNA HOTTIP as a novel predictor of lymph node metastasis and survival in human cancer: a systematic review and meta-analysis
  publication-title: Oncotarget
  doi: 10.18632/oncotarget.12981
  contributor:
    fullname: Chen
– volume: 21
  start-page: 912
  year: 2008
  ident: 10.1016/j.mgene.2020.100808_bb0130
  article-title: ZEB1 expression in type I vs type II endometrial cancers: a marker of aggressive disease
  publication-title: Mod. Pathol.
  doi: 10.1038/modpathol.2008.82
  contributor:
    fullname: Singh
– volume: 464
  start-page: 1071
  year: 2010
  ident: 10.1016/j.mgene.2020.100808_bb0045
  article-title: Long non-coding RNA HOTAIR reprograms chromatin state to promote cancer metastasis
  publication-title: Nature.
  doi: 10.1038/nature08975
  contributor:
    fullname: Gupta
– volume: 472
  start-page: 120
  issue: 7341
  year: 2011
  ident: 10.1016/j.mgene.2020.100808_bb0155
  article-title: A long noncoding RNA maintains active chromatin to coordinate homeotic gene expression
  publication-title: Nature.
  doi: 10.1038/nature09819
  contributor:
    fullname: Wang
– volume: 151
  start-page: 939
  year: 2010
  ident: 10.1016/j.mgene.2020.100808_bb0185
  article-title: Maternally expressed gene 3 (MEG3)noncoding ribonucleic acid: isoform structure, expression, and functions
  publication-title: Endocrinology.
  doi: 10.1210/en.2009-0657
  contributor:
    fullname: Zhang
– volume: 139
  start-page: 1534
  year: 2016
  ident: 10.1016/j.mgene.2020.100808_bb0120
  article-title: International trends in liver cancer incidence, overall and by histologic subtype, 1978–2007
  publication-title: Int. J. Cancer
  doi: 10.1002/ijc.30211
  contributor:
    fullname: Petrick
– volume: 8
  start-page: 171
  year: 2008
  ident: 10.1016/j.mgene.2020.100808_bb0005
  article-title: Promoter hypermethylation of the MEG3 (DLK1/MEG3) imprinted gene in multiple myeloma
  publication-title: Clin. Lymphoma Myeloma
  doi: 10.3816/CLM.2008.n.021
  contributor:
    fullname: Benetatos
– volume: 47
  start-page: S2
  issue: Suppl
  year: 2013
  ident: 10.1016/j.mgene.2020.100808_bb0095
  article-title: Epidemiology of hepatocellular carcinoma: consider the population
  publication-title: J. Clin. Gastroenterol.
  doi: 10.1097/MCG.0b013e3182872f29
  contributor:
    fullname: Mittal
– volume: 11
  year: 2015
  ident: 10.1016/j.mgene.2020.100808_bb0035
  article-title: MiRNA-192 [corrected] and miRNA-204 directly suppress lncRNA HOTTIP and interrupt GLS1-mediated Glutaminolysis in hepatocellular carcinoma
  publication-title: PLoS Genet.
  doi: 10.1371/journal.pgen.1005726
  contributor:
    fullname: Ge
– volume: 132
  start-page: 2557
  year: 2007
  ident: 10.1016/j.mgene.2020.100808_bb0020
  article-title: Hepatocellular carcinoma: epidemiology and molecular carcinogenesis
  publication-title: Gastroenterology.
  doi: 10.1053/j.gastro.2007.04.061
  contributor:
    fullname: El-Serag
– volume: 9
  year: 2013
  ident: 10.1016/j.mgene.2020.100808_bb0060
  article-title: Pervasive transcription of the human genome produces thousands of previously unidentified long intergenic noncoding RNAs
  publication-title: PLoS Genet.
  doi: 10.1371/journal.pgen.1003569
  contributor:
    fullname: Hangauer
– volume: 68
  start-page: 2479
  year: 2008
  ident: 10.1016/j.mgene.2020.100808_bb0040
  article-title: Insulin-like growth factor-I-dependent up-regulation of ZEB1 drives epithelial-to-mesenchymal transition in human prostate cancer cells
  publication-title: Cancer Res.
  doi: 10.1158/0008-5472.CAN-07-2559
  contributor:
    fullname: Graham
– volume: 6
  start-page: 674
  year: 2006
  ident: 10.1016/j.mgene.2020.100808_bb0025
  article-title: Hepatocellular carcinoma pathogenesis: from genes to environment
  publication-title: Nat. Rev. Cancer
  doi: 10.1038/nrc1934
  contributor:
    fullname: Farazi
– volume: 13
  start-page: 171
  year: 2012
  ident: 10.1016/j.mgene.2020.100808_bb0055
  article-title: Functional genomic studies: insights into the pathogenesis of liver cancer
  publication-title: Annu. Rev. Genomics Hum. Genet.
  doi: 10.1146/annurev-genom-090711-163752
  contributor:
    fullname: Han
– volume: 37
  start-page: 2209
  year: 2015
  ident: 10.1016/j.mgene.2020.100808_bb0090
  article-title: Long non-coding RNA MEG3 inhibits cell proliferation and induces apoptosis in prostate cancer
  publication-title: Cell. Physiol. Biochem.
  doi: 10.1159/000438577
  contributor:
    fullname: Luo
– volume: 35
  start-page: 1575
  year: 2016
  ident: 10.1016/j.mgene.2020.100808_bb0080
  article-title: Up-regulation of long noncoding RNA ZEB1-AS1 promotes tumor metastasis and predicts poor prognosis in hepatocellular carcinoma
  publication-title: Oncogene.
  doi: 10.1038/onc.2015.223
  contributor:
    fullname: Li
– volume: 154
  start-page: 1190
  year: 2013
  ident: 10.1016/j.mgene.2020.100808_bb0110
  article-title: Long noncoding RNAs usher in a new era in the biology of enhancers
  publication-title: Cell
  doi: 10.1016/j.cell.2013.08.028
  contributor:
    fullname: Orom
– volume: 51
  start-page: 1705
  year: 2017
  ident: 10.1016/j.mgene.2020.100808_bb0190
  article-title: Long non-coding RNA HOTTIP promotes hepatocellular carcinoma tumorigenesis and development: a comprehensive investigation based on bioinformatics, qRT-PCR and meta-analysis of 393 cases
  publication-title: Int. J. Oncol.
  doi: 10.3892/ijo.2017.4164
  contributor:
    fullname: Zhang
– volume: 8
  start-page: 4095
  year: 2016
  ident: 10.1016/j.mgene.2020.100808_bb0085
  article-title: Long noncoding RNA ZEB1 AS1 acts as an oncogene in osteosarcoma by epigenetically activating ZEB1
  publication-title: Am. J. Transl. Res.
  contributor:
    fullname: Liu
– volume: 455
  start-page: 43
  year: 2014
  ident: 10.1016/j.mgene.2020.100808_bb0145
  article-title: DNA methylation and microRNA biomarkers for noninvasive detection of gastric and colorectal cancer
  publication-title: Biochem. Biophys. Res. Commun.
  doi: 10.1016/j.bbrc.2014.08.001
  contributor:
    fullname: Toiyama
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Snippet Hepatocellular carcinoma (HCC) is a main cause of cancer death worldwide. The high mortality of HCC patients is linked to delayed diagnosis. Long non-coding...
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elsevier
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Publisher
StartPage 100808
SubjectTerms Hepatocellular carcinoma
lncRNAs (HOTTIP, ZEB-AS1, MEG3)
Real-time PCR
Title Biochemical and molecular study of long non-coding RNAs (HOTTIP, ZEB-AS1 and MEG-3) in hepatocellular carcinoma
URI https://dx.doi.org/10.1016/j.mgene.2020.100808
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