Skip to main content
Erschienen in: Tumor Biology 8/2014

01.08.2014 | Research Article

Long noncoding RNA SPRY4-IT1 is upregulated in esophageal squamous cell carcinoma and associated with poor prognosis

Erschienen in: Tumor Biology | Ausgabe 8/2014

Einloggen, um Zugang zu erhalten

Abstract

LncRNA SPRY4-IT1 has been shown to promote the progression of melanoma. However, the role of lncRNA SPRY4-IT1 in human esophageal squamous cell carcinoma (ESCC) remains unclear. The purpose of this study is to investigate the clinical significance and biological functions of SPRY4-IT1 in ESCC. The expression levels of lncRNA SPRY4-IT in 92 ESCC patients and 8 ESCC cell lines were evaluated by quantitative reverse transcriptase polymerase chain reaction (qRT-PCR). The prognostic significance was evaluated using Kaplan–Meier and Cox regression analyses. Small interfering RNA (siRNA) was used to suppress SPRY4-IT1 expression in ESCC cell lines. Both in vitro and in vivo assays were performed to further explore its role in tumor progression. SPRY4-IT1 levels were significantly higher in ESCC tissues and cells than in corresponding adjacent noncancerous tissues and nontumorigenic esophageal epithelial cells, and the ESCC patients with higher SPRY4-IT1 expression had an advanced clinical stage and poorer prognosis than those with lower SPRY4-IT1 expression. The multivariate analysis revealed that SPRY4-IT1 expression level is an independent prognostic factor in ESCC patients. In vitro assays demonstrated that knockdown of SPRY4-IT1 reduced cell proliferation, invasiveness, and migration. In vivo assays demonstrated that knockdown of SPRY4-IT1 decreases cell growth. SPRY4-IT1 is a novel molecule involved in ESCC progression, which may provide a potential prognostic biomarker and a potential target for therapeutic intervention.
Literatur
1.
Zurück zum Zitat Kamangar F, Doers GM, Anderson WF. Patterns of cancer incidence, mortality, and prevalence across five continents: defining priorities to reduce cancer disparities in different geographic regions of the world. J Clin Oncol. 2006;24:2137–50.PubMedCrossRef Kamangar F, Doers GM, Anderson WF. Patterns of cancer incidence, mortality, and prevalence across five continents: defining priorities to reduce cancer disparities in different geographic regions of the world. J Clin Oncol. 2006;24:2137–50.PubMedCrossRef
2.
Zurück zum Zitat Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. Cancer J Clin. 2011;61:69–90.CrossRef Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. Cancer J Clin. 2011;61:69–90.CrossRef
3.
Zurück zum Zitat Matsushima K, Isomoto H, Kohno S, Nakao K. MicroRNAs and esophageal squamous cell carcinoma. Digestion. 2010;82:138–44.PubMedCrossRef Matsushima K, Isomoto H, Kohno S, Nakao K. MicroRNAs and esophageal squamous cell carcinoma. Digestion. 2010;82:138–44.PubMedCrossRef
4.
Zurück zum Zitat Prensner JR, Chinnaiyan AM. The emergence of lncRNAs in cancer biology. Cancer Discuter. 2011;1:391–407.CrossRef Prensner JR, Chinnaiyan AM. The emergence of lncRNAs in cancer biology. Cancer Discuter. 2011;1:391–407.CrossRef
5.
Zurück zum Zitat Tang F, Zhang R, He Y, Zou M, Guo L, Xi T. MicroRNA-125b induces metastasis by targeting STARD13 in MCF-7 and MDA-MB-231 breast cancer cells. PLoS One. 2012;7:e35435.PubMedCentralPubMedCrossRef Tang F, Zhang R, He Y, Zou M, Guo L, Xi T. MicroRNA-125b induces metastasis by targeting STARD13 in MCF-7 and MDA-MB-231 breast cancer cells. PLoS One. 2012;7:e35435.PubMedCentralPubMedCrossRef
6.
Zurück zum Zitat Jang J, Jeon HS, Sun Z, Aubry MC, Tang H, Park CH, et al. Increased miR-708 expression in NSCLC and its association with poor survival in lung adenocarcinoma in non smokers. Clin Cancer Res. 2012;18:3658–67.PubMedCentralPubMedCrossRef Jang J, Jeon HS, Sun Z, Aubry MC, Tang H, Park CH, et al. Increased miR-708 expression in NSCLC and its association with poor survival in lung adenocarcinoma in non smokers. Clin Cancer Res. 2012;18:3658–67.PubMedCentralPubMedCrossRef
7.
Zurück zum Zitat Xu K, Liang X, Shen K, Cui D, Zheng Y, Xu J, et al. MiR-297 modulates multidrug resistance in human colorectal carcinoma by down-regulating MRP-2. Biochem J. 2012;446:291–300.PubMedCrossRef Xu K, Liang X, Shen K, Cui D, Zheng Y, Xu J, et al. MiR-297 modulates multidrug resistance in human colorectal carcinoma by down-regulating MRP-2. Biochem J. 2012;446:291–300.PubMedCrossRef
8.
Zurück zum Zitat Buurman R, Gürlevik E, Schäffer V, Eilers M, Sandbothe M, Kreipe H, et al. Histone deacetylases activate hepatocyte growth factor signaling by repressing microRNA-449 in hepatocellular carcinoma cells. Gastroenterology. 2012;143:811–20.PubMedCrossRef Buurman R, Gürlevik E, Schäffer V, Eilers M, Sandbothe M, Kreipe H, et al. Histone deacetylases activate hepatocyte growth factor signaling by repressing microRNA-449 in hepatocellular carcinoma cells. Gastroenterology. 2012;143:811–20.PubMedCrossRef
9.
Zurück zum Zitat Zhao X, Dou W, He L, Liang S, Tie J, Liu C, et al. MicroRNA-7 functions as an anti-metastatic microRNA in gastric cancer by targeting insulin-like growth factor-1 receptor. Oncogene. 2012;32:1363–72.PubMedCrossRef Zhao X, Dou W, He L, Liang S, Tie J, Liu C, et al. MicroRNA-7 functions as an anti-metastatic microRNA in gastric cancer by targeting insulin-like growth factor-1 receptor. Oncogene. 2012;32:1363–72.PubMedCrossRef
10.
Zurück zum Zitat Li SQ, Wang HM, Cao XF. Potential clinical insights into microRNAs and their target genes in esophageal carcinoma. Biomarkers. 2011;16:629–36.PubMedCrossRef Li SQ, Wang HM, Cao XF. Potential clinical insights into microRNAs and their target genes in esophageal carcinoma. Biomarkers. 2011;16:629–36.PubMedCrossRef
13.
Zurück zum Zitat Guttman M, Rinn JL. Modular regulatory principles of large non-coding RNAs. Nature. 2012;482:339–46.PubMedCrossRef Guttman M, Rinn JL. Modular regulatory principles of large non-coding RNAs. Nature. 2012;482:339–46.PubMedCrossRef
14.
Zurück zum Zitat Flockhart RJ, Webster DE, Qu K, Mascarenhas N, Kovalski J, Kretz M, et al. BRAFV600E remodels the melanocyte transcriptome and induces BANCR to regulate melanoma cell migration. Genome Res. 2012;22:1006–14.PubMedCentralPubMedCrossRef Flockhart RJ, Webster DE, Qu K, Mascarenhas N, Kovalski J, Kretz M, et al. BRAFV600E remodels the melanocyte transcriptome and induces BANCR to regulate melanoma cell migration. Genome Res. 2012;22:1006–14.PubMedCentralPubMedCrossRef
15.
Zurück zum Zitat Silva JM, Boczek NJ, Berres MW, Ma X, Smith DI. LSINCT5 is over expressed in breast and ovarian cancer and affects cellular proliferation. RNA Biol. 2011;8:496–505.PubMedCrossRef Silva JM, Boczek NJ, Berres MW, Ma X, Smith DI. LSINCT5 is over expressed in breast and ovarian cancer and affects cellular proliferation. RNA Biol. 2011;8:496–505.PubMedCrossRef
16.
Zurück zum Zitat Wang J, Liu X, Wu H, Ni P, Gu Z, Qiao Y, et al. CREB up-regulates long non-coding RNA, HULC expression through interaction with microRNA-372 in liver cancer. Nucleic Acid Res. 2010;38:5366–83.PubMedCentralPubMedCrossRef Wang J, Liu X, Wu H, Ni P, Gu Z, Qiao Y, et al. CREB up-regulates long non-coding RNA, HULC expression through interaction with microRNA-372 in liver cancer. Nucleic Acid Res. 2010;38:5366–83.PubMedCentralPubMedCrossRef
17.
Zurück zum Zitat Chen FJ, Sun M, Li SQ, Wu QQ, Ji L, Liu ZL, et al. Upregulation of the long non-coding RNA HOTAIR promotes esophageal squamous cell carcinoma metastasis and poor prognosis. Mol Carcin. 2012;52:908–15.CrossRef Chen FJ, Sun M, Li SQ, Wu QQ, Ji L, Liu ZL, et al. Upregulation of the long non-coding RNA HOTAIR promotes esophageal squamous cell carcinoma metastasis and poor prognosis. Mol Carcin. 2012;52:908–15.CrossRef
18.
Zurück zum Zitat Lv XB, Lian GY, Wang HR, Song E, Yao H, Wang MH. Long noncoding RNA HOTAIR is a prognostic marker for esophageal squamous cell carcinoma progression and survival. PLoS One. 2013;8:e63516.PubMedCentralPubMedCrossRef Lv XB, Lian GY, Wang HR, Song E, Yao H, Wang MH. Long noncoding RNA HOTAIR is a prognostic marker for esophageal squamous cell carcinoma progression and survival. PLoS One. 2013;8:e63516.PubMedCentralPubMedCrossRef
19.
Zurück zum Zitat Khaitan D, Dinger ME, Mazar J, Crawford J, Smith MA, Mattick JS, et al. The melanoma-upregulated long noncoding RNA SPRY4-IT1 modulates apoptosis and invasion. Cancer Resh. 2011;71:3852–62.CrossRef Khaitan D, Dinger ME, Mazar J, Crawford J, Smith MA, Mattick JS, et al. The melanoma-upregulated long noncoding RNA SPRY4-IT1 modulates apoptosis and invasion. Cancer Resh. 2011;71:3852–62.CrossRef
20.
Zurück zum Zitat Shimada Y, Imamura M, Wagata T, Yamaguchi N, Tobe T. Characterization of 21 newly established esophageal cancer cell lines. Cancer. 1992;69:277–84.PubMedCrossRef Shimada Y, Imamura M, Wagata T, Yamaguchi N, Tobe T. Characterization of 21 newly established esophageal cancer cell lines. Cancer. 1992;69:277–84.PubMedCrossRef
21.
Zurück zum Zitat Kanda Y, Nishiyama Y, Shimada Y, Imamura M, Nomura H, Hiai H, et al. Analysis of gene amplification and over expression in human esophageal carcinoma cell lines. Int J Cancer. 1994;58:291–7.PubMedCrossRef Kanda Y, Nishiyama Y, Shimada Y, Imamura M, Nomura H, Hiai H, et al. Analysis of gene amplification and over expression in human esophageal carcinoma cell lines. Int J Cancer. 1994;58:291–7.PubMedCrossRef
22.
Zurück zum Zitat Kim K, Jutooru I, Chadalapaka G, Johnson G, Frank J, Burghardt R, et al. HOTAIR is a negative prognostic factor and exhibits pro-oncogenic activity in pancreatic cancer. Oncogene. 2013;32:1616–25.PubMedCentralPubMedCrossRef Kim K, Jutooru I, Chadalapaka G, Johnson G, Frank J, Burghardt R, et al. HOTAIR is a negative prognostic factor and exhibits pro-oncogenic activity in pancreatic cancer. Oncogene. 2013;32:1616–25.PubMedCentralPubMedCrossRef
23.
Zurück zum Zitat Mercer TR, Dinger ME, Mattick JS. Long non-coding RNAs: insights into functions. Nat Rev Genet. 2009;10:155–9.PubMedCrossRef Mercer TR, Dinger ME, Mattick JS. Long non-coding RNAs: insights into functions. Nat Rev Genet. 2009;10:155–9.PubMedCrossRef
24.
Zurück zum Zitat Ponjavic J, Ponting C, Lunter G. Functionality or transcriptional noise? Evidence for selection of long non coding RNAs. Genome Res. 2007;17:556–65.PubMedCentralPubMedCrossRef Ponjavic J, Ponting C, Lunter G. Functionality or transcriptional noise? Evidence for selection of long non coding RNAs. Genome Res. 2007;17:556–65.PubMedCentralPubMedCrossRef
25.
Zurück zum Zitat Struhl K. Transcriptional noise and the fidelity of initiation by RNA polymerase II. Nat Struct Mol Biol. 2007;14:103–5.PubMedCrossRef Struhl K. Transcriptional noise and the fidelity of initiation by RNA polymerase II. Nat Struct Mol Biol. 2007;14:103–5.PubMedCrossRef
26.
Zurück zum Zitat Spizzo R, Almeida MI, Colombatti A, Calin GA. Long non-coding RNAs and cancer: a new frontier of translational research. Oncogene. 2012;31:4577–87.PubMedCentralPubMedCrossRef Spizzo R, Almeida MI, Colombatti A, Calin GA. Long non-coding RNAs and cancer: a new frontier of translational research. Oncogene. 2012;31:4577–87.PubMedCentralPubMedCrossRef
27.
Zurück zum Zitat Moran VA, Perera RJ, Khalil AM. Emerging functional and mechanistic paradigms of mammalian long non-coding RNAs. Nucleic Acids Res. 2012;40:6391–400.PubMedCentralPubMedCrossRef Moran VA, Perera RJ, Khalil AM. Emerging functional and mechanistic paradigms of mammalian long non-coding RNAs. Nucleic Acids Res. 2012;40:6391–400.PubMedCentralPubMedCrossRef
Metadaten
Titel
Long noncoding RNA SPRY4-IT1 is upregulated in esophageal squamous cell carcinoma and associated with poor prognosis
Publikationsdatum
01.08.2014
Erschienen in
Tumor Biology / Ausgabe 8/2014
Print ISSN: 1010-4283
Elektronische ISSN: 1423-0380
DOI
https://doi.org/10.1007/s13277-014-2013-y

Weitere Artikel der Ausgabe 8/2014

Tumor Biology 8/2014 Zur Ausgabe

Update Onkologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.