Downregulation of LINC00886 facilitates epithelial-mesenchymal transition through SIRT7/ELF3/miR-144 pathway in esophageal squamous cell carcinoma.


Journal

Clinical & experimental metastasis
ISSN: 1573-7276
Titre abrégé: Clin Exp Metastasis
Pays: Netherlands
ID NLM: 8409970

Informations de publication

Date de publication:
08 2022
Historique:
received: 12 01 2022
accepted: 28 04 2022
pubmed: 27 5 2022
medline: 3 8 2022
entrez: 26 5 2022
Statut: ppublish

Résumé

LINC00886 has been reported to be down-regulated in laryngeal squamous cell carcinoma, and aberrant DNA methylation status of it has been screened in several tumor types. However, the roles of LINC00886 in esophageal squamous cell carcinoma (ESCC) remained unclarified. The present study was to investigate the expression level, epigenetic inactivation mechanisms, and functions of LINC00886 in ESCC tumorigenesis. Frequent down-regulation of LINC00886 was verified in esophageal cancer cells and ESCC tissues. There are CpG islands spanning the promoter and exon 1 regions of LINC00886 gene, and DNA hypermethylation of proximal promoter led to transcriptional inhibition of LINC00886, moreover, histone modification also played certain roles in LINC00886 transcription. LINC00886 functioned as a tumor suppressor by inhibiting proliferation, migration, and invasion of esophageal cancer cells. LINC00886 was down-regulated following TGF-β1 treatment in esophageal cancer cells and participated in epithelial-mesenchymal transition (EMT) process by regulating EMT-related genes, especially ZEB1 and ZEB2. ELF3 was proved to be one of the downstream target genes of LINC00886. LINC00886 may interact with and recruit SIRT7 to decrease acetylation level of H3K18 on the promoter region of ELF3 to inhibit its expression. Furthermore, ELF3 may promote EMT process via promoting ZEB1 and ZEB2 expression through binding to the promoter region of miR-144 to suppress miR-144-3p transcriptional activity in ESCC. These data suggest that LINC00886 may act as a tumor suppressor gene in ESCC and its down-regulation through epigenetic mechanisms promotes EMT process via SIRT7/ELF3/miR-144 pathway in ESCC. Thus, LINC00886 may be a potential therapeutic target for ESCC treatment.

Identifiants

pubmed: 35616822
doi: 10.1007/s10585-022-10171-w
pii: 10.1007/s10585-022-10171-w
doi:

Substances chimiques

DNA-Binding Proteins 0
ELF3 protein, human 0
MIRN144 microRNA, human 0
MicroRNAs 0
Proto-Oncogene Proteins c-ets 0
RNA, Long Noncoding 0
SIRT7 protein, human 0
Transcription Factors 0
Sirtuins EC 3.5.1.-

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

661-677

Informations de copyright

© 2022. The Author(s), under exclusive licence to Springer Nature B.V.

Références

Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A (2018) Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 68:394–424
doi: 10.3322/caac.21492
Lagergren J, Smyth E, Cunningham D, Lagergren P (2017) Oesophageal cancer. Lancet 390:2383–2396
doi: 10.1016/S0140-6736(17)31462-9
Abnet CC, Arnold M, Wei WQ (2018) Epidemiology of esophageal squamous cell carcinoma. Gastroenterology 154:360–373
doi: 10.1053/j.gastro.2017.08.023
Zhang R, Jia M, Li P, Han J, Huang K, Li Q, Qiao Y, Xu T, Ruan P, Hu Q, Fan G, Song Q, Fu Z (2019) Radiotherapy improves the survival of patients with metastatic esophageal squamous cell carcinoma: a propensity score matched analysis of surveillance, epidemiology, and end results database. Dis Esophagus 32(1):doy704
doi: 10.1093/dote/doy074
Slack FJ, Chinnaiyan AM (2019) The role of non-coding RNAs in oncology. Cell 179:1033–1055
doi: 10.1016/j.cell.2019.10.017
Bach DH, Lee SK (2018) Long noncoding RNAs in cancer cells. Cancer Lett 419:152–166
doi: 10.1016/j.canlet.2018.01.053
Chen L, Dzakah EE, Shan G (2018) Targetable long non-coding RNAs in cancer treatments. Cancer Lett 418:119–124
doi: 10.1016/j.canlet.2018.01.042
Anastasiadou E, Jacob LS, Slack FJ (2018) Non-coding RNA networks in cancer. Nat Rev Cancer 18(1):5–18
doi: 10.1038/nrc.2017.99
Amin V, Harris RA, Onuchic V, Jackson AR, Charnecki T, Paithankar S, Lakshmi Subramanian S, Riehle K, Coarfa C, Milosavljevic A (2015) Epigenomic footprints across 111 reference epigenomes reveal tissue-specific epigenetic regulation of lincRNAs. Nat Commun 6:6370
doi: 10.1038/ncomms7370
Wang Z, Yang B, Zhang M, Guo W, Wu Z, Wang Y, Jia L, Li S, Cancer Genome Atlas Research Network, Xie W, Yang D (2018) LncRNA epigenetic landscape analysis identifies EPIC1 as an oncogenic lncRNA that interacts with MYC and promotes cell-cycle progression in cancer. Cancer Cell 33:706–720
doi: 10.1016/j.ccell.2018.03.006
Lan L, Cao H, Chi W, Meng W, Zhao L, Cui W, Wang B (2020) Aberrant DNA hypermethylation-silenced LINC00886 gene accelerates malignant progression of laryngeal carcinoma. Pathol Res Pract 216:152877
doi: 10.1016/j.prp.2020.152877
Cameron EE, Bachman KE, Myöhänen S, Herman JG, Baylin SB (1999) Synergy of demethylation and histone deacetylase inhibition in the re-expression of genes silenced in cancer. Nat Genet 21:103–107
doi: 10.1038/5047
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402–408
doi: 10.1006/meth.2001.1262
Yu L, Liu C, Vandeusen J, Becknell B, Dai Z, Wu YZ, Raval A, Liu TH, Ding W, Mao C, Liu S, Smith LT, Lee S, Rassenti L, Marcucci G, Byrd J, Caligiuri MA, Plass C (2005) Global assessment of promoter methylation in a mouse model of cancer identifies ID4 as a putative tumor-suppressor gene in human leukemia. Nat Genet 37:265–274
doi: 10.1038/ng1521
Carafa V, Rotili D, Forgione M, Cuomo F, Serretiello E, Hailu GS, Jarho E, Lahtela-Kakkonen M, Mai A, Altucci L (2016) Sirtuin functions and modulation: from chemistry to the clinic. Clin Epigenet 8:61
doi: 10.1186/s13148-016-0224-3
Phatak P, Noe M, Asrani K, Chesnick IE, Greenwald BD, Donahue JM (2021) MicroRNA-141-3p regulates cellular proliferation, migration, and invasion in esophageal cancer by targeting tuberous sclerosis complex 1. Mol Carcinog 60:125–137
doi: 10.1002/mc.23274
Ishibashi O, Akagi I, Ogawa Y, Inui T (2018) MiR-141-3p is upregulated in esophageal squamous cell carcinoma and targets pleckstrin homology domain leucine-rich repeat protein phosphatase-2, a negative regulator of the PI3K/AKT pathway. Biochem Biophys Res Commun 501:507–513
doi: 10.1016/j.bbrc.2018.05.025
Gao Z, Liu R, Liao J, Yang M, Pan E, Yin L, Pu Y (2016) Possible tumor suppressive role of the miR-144/451 cluster in esophageal carcinoma as determined by principal component regression analysis. Mol Med Rep 14:3805–3813
doi: 10.3892/mmr.2016.5691
Wang P, Yang Z, Ye T, Shao F, Li J, Sun N, He J (2020) lncTUG1/miR-144-3p affect the radiosensitivity of esophageal squamous cell carcinoma by competitively regulating c-MET. J Exp Clin Cancer Res 39:7
doi: 10.1186/s13046-019-1519-y
Cedar H, Bergman Y (2009) Linking DNA methylation and histone modification: patterns and paradigms. Nat Rev Genet 10:295–304
doi: 10.1038/nrg2540
Ma X, Yu L, Wang P, Yang X (2017) Discovering DNA methylation patterns for long non-coding RNAs associated with cancer subtypes. Comput Biol Chem 69:164–170
doi: 10.1016/j.compbiolchem.2017.03.014
Hashimoto H, Vertino PM, Cheng X (2010) Molecular coupling of DNA methylation and histone methylation. Epigenomics 2:657–669
doi: 10.2217/epi.10.44
Dong Z, Zhang A, Liu S, Lu F, Guo Y, Zhang G, Xu F, Shi Y, Shen S, Liang J, Guo W (2017) Aberrant methylation-mediated silencing of lncRNA MEG3 functions as a ceRNA in esophageal cancer. Mol Cancer Res 15:800–810
doi: 10.1158/1541-7786.MCR-16-0385
Guo W, Liu S, Dong Z, Guo Y, Ding C, Shen S, Liang J, Shan B (2018) Aberrant methylation-mediated silencing of lncRNA CTC-276P9.1 is associated with malignant progression of esophageal squamous cell carcinoma. Clin Exp Metastasis 35:53–68
doi: 10.1007/s10585-018-9881-2
Dong Z, Liang X, Wu X, Kang X, Guo Y, Shen S, Liang J, Guo W (2019) Promoter hypermethylation-mediated downregulation of tumor suppressor gene SEMA3B and lncRNA SEMA3B-AS1 correlates with progression and prognosis of esophageal squamous cell carcinoma. Clin Exp Metastasis 36:225–241
doi: 10.1007/s10585-019-09964-3
Dong Z, Li S, Wu X, Niu Y, Liang X, Yang L, Guo Y, Shen S, Liang J, Guo W (2019) Aberrant hypermethylation-mediated downregulation of antisense lncRNA ZNF667-AS1 and its sense gene ZNF667 correlate with progression and prognosis of esophageal squamous cell carcinoma. Cell Death Dis 10:930
doi: 10.1038/s41419-019-2171-3
Matějka VM, Fínek J, Králíčková M (2017) Epithelial-mesenchymal transition in tumor tissue and its role for matastatic spread of cancer. Klin Onkol 30:20–27
doi: 10.14735/amko201720
Feng Y, Gao L, Cui G, Cao Y (2020) LncRNA NEAT1 facilitates pancreatic cancer growth and metastasis through stabilizing ELF3 mRNA. Am J Cancer Res 10(1):237–248
pubmed: 32064164 pmcid: 7017733
Zheng L, Xu M, Xu J, Wu K, Fang Q, Liang Y, Zhou S, Cen D, Ji L, Han W, Cai X (2018) ELF3 promotes epithelial-mesenchymal transition by protecting ZEB1 from miR-141-3p-mediated silencing in hepatocellular carcinoma. Cell Death Dis 9(3):387
doi: 10.1038/s41419-018-0399-y
Yeung TL, Leung CS, Wong KK, Gutierrez-Hartmann A, Kwong J, Gershenson DM, Mok SC (2017) ELF3 is a negative regulator of epithelial-mesenchymal transition in ovarian cancer cells. Oncotarget 8:16951–16963
doi: 10.18632/oncotarget.15208
Li T, Tang C, Huang Z, Yang L, Dai H, Tang B, Xiao B, Li J, Lei X (2021) miR-144-3p inhibited the growth, metastasis and epithelial-mesenchymal transition of colorectal adenocarcinoma by targeting ZEB1/2. Aging (Albany NY) 13:17349–17369
doi: 10.18632/aging.203225

Auteurs

Zhiming Dong (Z)

Laboratory of Pathology, Hebei Cancer Institute, The Fourth Hospital of Hebei Medical University, Jiankang Road 12, Shijiazhuang, 050011, Hebei, China.

Liu Yang (L)

Laboratory of Pathology, Hebei Cancer Institute, The Fourth Hospital of Hebei Medical University, Jiankang Road 12, Shijiazhuang, 050011, Hebei, China.

Juntao Lu (J)

Laboratory of Pathology, Hebei Cancer Institute, The Fourth Hospital of Hebei Medical University, Jiankang Road 12, Shijiazhuang, 050011, Hebei, China.

Yanli Guo (Y)

Laboratory of Pathology, Hebei Cancer Institute, The Fourth Hospital of Hebei Medical University, Jiankang Road 12, Shijiazhuang, 050011, Hebei, China.

Supeng Shen (S)

Laboratory of Pathology, Hebei Cancer Institute, The Fourth Hospital of Hebei Medical University, Jiankang Road 12, Shijiazhuang, 050011, Hebei, China.

Jia Liang (J)

Laboratory of Pathology, Hebei Cancer Institute, The Fourth Hospital of Hebei Medical University, Jiankang Road 12, Shijiazhuang, 050011, Hebei, China.

Wei Guo (W)

Laboratory of Pathology, Hebei Cancer Institute, The Fourth Hospital of Hebei Medical University, Jiankang Road 12, Shijiazhuang, 050011, Hebei, China. guowei7303@163.com.

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