Differential expression profiles of microRNAs as potential biomarkers for the early diagnosis of esophageal squamous cell carcinoma

Yang,Miao; Liu,Ran; Sheng,Jingyi; Liao,Juan; Wang,Yi; Pan,Enchun; Guo,Wei; Pu,Yuepu; Yin,Lihong

doi:10.3892/or.2012.2105

Differential expression profiles of microRNAs as potential biomarkers for the early diagnosis of esophageal squamous cell carcinoma

Authors:
- Miao Yang
- Ran Liu
- Jingyi Sheng
- Juan Liao
- Yi Wang
- Enchun Pan
- Wei Guo
- Yuepu Pu
- Lihong Yin
View Affiliations

Affiliations: Key Laboratory of Environmental Medicine Engineering, Ministry of Education, School of Public Health, Southeast University, Nanjing, Jiangsu 210009, P.R. China, Huaian Center for Disease Control and Prevention, Huaian, Jiangsu 223001, P.R. China, The First People's Hospital of Huaian, Huaian, Jiangsu 223000, P.R. China
Published online on: October 23, 2012 https://doi.org/10.3892/or.2012.2105
Pages: 169-176

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

Esophageal squamous cell carcinoma (ESCC) is one of the most lethal malignancies worldwide. To reduce the high morbidity and mortality of the disease, sensitive and specific biomarkers for early detection are urgently needed. Tumor-specific microRNAs (miRNAs) seem to be potential biomarkers for the early diagnosis and treatment of cancer. In this study, differentially expressed miRNAs in tumor tissues and adjacent non-tumor tissues were detected by miRNA microarrays. Stem-loop real-time reverse transcription PCR was conducted to verify the candidate miRNAs discovered by microarray analysis. The data showed that hsa-miR-338-3p, hsa-miR‑218 and hsa-miR-139-5p were downregulated in tumor tissues compared with adjacent non-tumor tissues, while hsa-miR‑183, hsa-miR-574-5p, hsa-miR-21* and hsa-miR‑601 were upregulated in tumor tissues. Multiple regression analysis revealed the aberrant expression of hsa-miR-338-3p, hsa‑miR-139-5p, hsa-miR‑574-5p and hsa-miR-601 increased the risk of esophageal cancer. Furthermore, we found hsa-miR-21* was significantly increased in heavy drinking patients. Therefore, there is a set of differentially expressed miRNAs in esophageal cancer which may be associated with the incidence and development of ESCC. Differential expression profiles of miRNAs in ESCC may be promising biomarkers for the early screening of high-risk populations and early detection.

View Figures

View References

1	Jinyi Z, Quanyong X, Ran T, Jie Y, Ping L and Ming W: Analysis on surveillance of cause death in Jiangsu province during 2007. Jiangsu J Prev Med 2008. 19:74–75. 2008.
2	Rice TW, Rusch VW, Apperson-Hansen C, et al: Worldwide esophageal cancer collaboration. Dis Esophagus. 22:1–8. 2009. View Article : Google Scholar
3	Calin GA and Croce CM: MicroRNA signatures in human cancers. Nat Rev Cancer. 6:857–866. 2006. View Article : Google Scholar : PubMed/NCBI
4	Ambros V: The functions of animal microRNAs. Nature. 431:350–355. 2004. View Article : Google Scholar : PubMed/NCBI
5	Lu J, Getz G, Miska EA, et al: MicroRNA expression profiles classify human cancers. Nature. 435:834–838. 2005. View Article : Google Scholar : PubMed/NCBI
6	Manikandan J, Aarthi JJ, Kumar SD and Pushparaj PN: Oncomirs: the potential role of non-coding microRNAs in understanding cancer. Bioinformation. 2:330–334. 2008. View Article : Google Scholar : PubMed/NCBI
7	Schetter AJ, Heegaard NHH and Harris CC: Inflammation and cancer: interweaving microRNA, free radical, cytokine and p53 pathways. Carcinogenesis. 31:37–49. 2010. View Article : Google Scholar : PubMed/NCBI
8	Kwak PB, Iwasaki S and Tomari Y: The microRNA pathway and cancer. Cancer Sci. 101:2309–2315. 2010. View Article : Google Scholar : PubMed/NCBI
9	Ahmed FE: Role of miRNA in carcinogenesis and biomarker selection: a methodological view. Expert Rev Mol Diagn. 7:569–603. 2007. View Article : Google Scholar : PubMed/NCBI
10	Kan T and Meltzer SJ: MicroRNAs in Barrett’s esophagus and esophageal adenocarcinoma. Curr Opin Pharmacol. 9:727–732. 2009.
11	Yang HS, Gu J, Wang KK, et al: MicroRNA expression signatures in Barrett’s esophagus and esophageal adenocarcinoma. Clin Cancer Res. 15:5744–5752. 2009.
12	Livak KJ and Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(-Delta Delta C) method. Methods. 25:402–408. 2001. View Article : Google Scholar : PubMed/NCBI
13	Esquela-Kerscher A and Slack FJ: Oncomirs - microRNAs with a role in cancer. Nat Rev Cancer. 6:259–269. 2006. View Article : Google Scholar
14	Chen X, Hu ZB, Wang WJ, et al: Identification of ten serum microRNAs from a genome-wide serum microRNA expression profile as novel noninvasive biomarkers for nonsmall cell lung cancer diagnosis. Int J Cancer. 130:1620–1628. 2012. View Article : Google Scholar : PubMed/NCBI
15	Hu YX, Correa AM, Hoque A, et al: Prognostic significance of differentially expressed miRNAs in esophageal cancer. Int J Cancer. 128:132–143. 2011. View Article : Google Scholar : PubMed/NCBI
16	Wiggins JF, Ruffino L, Kelnar K, et al: Development of a lung cancer therapeutic based on the tumor suppressor microRNA-34. Cancer Res. 70:5923–5930. 2010. View Article : Google Scholar : PubMed/NCBI
17	Guo Y, Chen Z, Zhang L, et al: Distinctive microRNA profiles relating to patient survival in esophageal squamous cell carcinoma. Cancer Res. 68:26–33. 2008. View Article : Google Scholar : PubMed/NCBI
18	Ogawa R, Ishiguro H, Kuwabara Y, et al: Expression profiling of micro-RNAs in human esophageal squamous cell carcinoma using RT-PCR. Med Mol Morphol. 42:102–109. 2009. View Article : Google Scholar : PubMed/NCBI
19	Feber A, Xi L, Luketich JD, et al: MicroRNA expression profiles of esophageal cancer. J Thorac Cardiovasc Surg. 135:255–260. 2008. View Article : Google Scholar
20	Guo J, Miao Y, Xiao B, et al: Differential expression of microRNA species in human gastric cancer versus non-tumorous tissues. J Gastroenterol Hepatol. 24:652–657. 2009. View Article : Google Scholar : PubMed/NCBI
21	Fridman E, Dotan Z, Barshack I, et al: Accurate molecular classification of renal tumors using microRNA expression. J Mol Diagn. 12:687–696. 2010. View Article : Google Scholar : PubMed/NCBI
22	Hiroki E, Akahira J, Suzuki F, et al: Changes in microRNA expression levels correlate with clinicopathological features and prognoses in endometrial serous adenocarcinomas. Cancer Sci. 101:241–249. 2010. View Article : Google Scholar : PubMed/NCBI
23	Yoshino H, Chiyomaru T, Enokida H, et al: The tumour-suppressive function of miR-1 and miR-133a targeting TAGLN2 in bladder cancer. Br J Cancer. 104:808–818. 2011. View Article : Google Scholar : PubMed/NCBI
24	Miles GD, Seiler M, Rodriguez L, Rajagopal G and Bhanot G: Identifying microRNA/mRNA dysregulations in ovarian cancer. BMC Res Notes. 5:1642012. View Article : Google Scholar : PubMed/NCBI
25	Au SL, Wong CC, Lee JM, et al: Enhancer of zeste homolog 2 epigenetically silences multiple tumor suppressor microRNAs to promote liver cancer metastasis. Hepatology. 56:622–631. 2012. View Article : Google Scholar : PubMed/NCBI
26	Yu JJ, Wang Y, Dong RF, Huang XY, Ding SN and Qiu HF: Circulating microRNA-218 was reduced in cervical cancer and correlated with tumor invasion. J Cancer Res Clin Oncol. 138:671–674. 2012. View Article : Google Scholar : PubMed/NCBI
27	Tatarano S, Chiyomaru T, Kawakami K, et al: miR-218 on the genomic loss region of chromosome 4p15.31 functions as a tumor suppressor in bladder cancer. Int J Oncol. 39:13–21. 2011.PubMed/NCBI
28	Gao CP, Zhang ZY, Liu WZ, Xiao SD, Gu WQ and Lu H: Reduced microRNA-218 expression is associated with high nuclear factor kappa B activation in gastric cancer. Cancer. 116:41–49. 2010.PubMed/NCBI
29	Huang XH, Chen JS, Wang Q, et al: miR-338-3p suppresses invasion of liver cancer cell by targeting smoothened. J Pathol. 225:463–472. 2011. View Article : Google Scholar : PubMed/NCBI
30	Yu J, Li A, Hong SM, Hruban RH and Goggins M: MicroRNA alterations of pancreatic intraepithelial neoplasias. Clin Cancer Res. 18:981–992. 2012. View Article : Google Scholar : PubMed/NCBI
31	Foss KM, Sima C, Ugolini D, Neri M, Allen KE and Weiss GJ: miR-1254 and miR-574-5p: serum-based microRNA biomarkers for early-stage non-small cell lung cancer. J Thorac Oncol. 6:482–488. 2011. View Article : Google Scholar : PubMed/NCBI
32	Yao Y, Suo AL, Li ZF, et al: MicroRNA profiling of human gastric cancer. Mol Med Rep. 2:963–970. 2009.PubMed/NCBI
33	Ohdaira H, Nakagawa H and Yoshida K: Profiling of molecular pathways regulated by microRNA 601. Comput Biol Chem. 33:429–433. 2009. View Article : Google Scholar : PubMed/NCBI
34	Lowery AJ, Miller N, Dwyer RM and Kerin MJ: Dysregulated miR-183 inhibits migration in breast cancer cells. BMC Cancer. 10:5022010. View Article : Google Scholar : PubMed/NCBI
35	Schaefer A, Jung M, Mollenkopf HJ, et al: Diagnostic and prognostic implications of microRNA profiling in prostate carcinoma. Int J Cancer. 126:1166–1176. 2010.PubMed/NCBI
36	Li J, Fu H, Xu C, et al: miR-183 inhibits TGF-beta1-induced apoptosis by downregulation of PDCD4 expression in human hepatocellular carcinoma cells. BMC Cancer. 10:3542010. View Article : Google Scholar : PubMed/NCBI
37	Bandres E, Cubedo E, Agirre X, et al: Identification by real-time PCR of 13 mature microRNAs differentially expressed in colorectal cancer and non-tumoral tissues. Mol Cancer. 5:292006. View Article : Google Scholar : PubMed/NCBI
38	Sarver AL, Li LH and Subramanian S: MicroRNA miR-183 functions as an oncogene by targeting the transcription factor EGR1 and promoting tumor cell migration. Cancer Res. 70:9570–9580. 2010. View Article : Google Scholar : PubMed/NCBI
39	Li GR, Luna C, Qiu JM, Epstein DL and Gonzalez P: Targeting of integrin beta1 and kinesin 2alpha by microRNA 183. J Biol Chem. 285:5461–5471. 2010. View Article : Google Scholar : PubMed/NCBI
40	Kanasaki K, Kanda Y, Palmsten K, et al: Integrin beta1-mediated matrix assembly and signaling are critical for the normal development and function of the kidney glomerulus. Dev Biol. 313:584–593. 2008. View Article : Google Scholar : PubMed/NCBI
41	Wederell ED and de Iongh RU: Extracellular matrix and integrin signaling in lens development and cataract. Semin Cell Dev Biol. 17:759–776. 2006. View Article : Google Scholar : PubMed/NCBI
42	O’Donnell KA, Wentzel EA, Zeller KI, Dang CV and Mendell JT: c-Myc-regulated microRNAs modulate E2F1 expression. Nature. 435:839–843. 2005.PubMed/NCBI
43	Iorio MV, Ferracin M, Liu CG, et al: MicroRNA gene expression deregulation in human breast cancer. Cancer Res. 65:7065–7070. 2005. View Article : Google Scholar : PubMed/NCBI
44	Yanaihara N, Caplen N, Bowman E, et al: Unique microRNA molecular profiles in lung cancer diagnosis and prognosis. Cancer Cell. 9:189–198. 2006. View Article : Google Scholar : PubMed/NCBI
45	Greither T, Grochola LF, Udelnow A, Lautenschlager C, Wurl P and Taubert H: Elevated expression of microRNAs 155, 203, 210 and 222 in pancreatic tumors is associated with poorer survival. Int J Cancer. 126:73–80. 2010. View Article : Google Scholar : PubMed/NCBI
46	Jiang SA, Zhang HW, Lu MH, et al: MicroRNA-155 functions as an OncomiR in breast cancer by targeting the suppressor of cytokine signaling 1 gene. Cancer Res. 70:3119–3127. 2010. View Article : Google Scholar : PubMed/NCBI
47	Wang G, Chan ES, Kwan BC, et al: Expression of microRNAs in the urine of patients with bladder cancer. Clin Genitourin Cancer. 10:106–113. 2012. View Article : Google Scholar : PubMed/NCBI
48	Chiang YP, Song YX, Wang ZN, et al: microRNA-192,-194 and-215 are frequently downregulated in colorectal cancer. Exp Ther Med. 3:560–566. 2012.PubMed/NCBI
49	Rossing M, Borup R, Henao R, et al: Down-regulation of microRNAs controlling tumourigenic factors in follicular thyroid carcinoma. J Mol Endocrinol. 48:11–23. 2012. View Article : Google Scholar : PubMed/NCBI
50	Wang LL, Zhang ZF, Li Q, et al: Ethanol exposure induces differential microRNA and target gene expression and teratogenic effects which can be suppressed by folic acid supplementation. Hum Reprod. 24:562–579. 2009. View Article : Google Scholar : PubMed/NCBI
51	Soares AR, Pereira PM, Ferreira V, et al: Ethanol exposure induces upregulation of specific microRNAs in zebrafish embryos. Toxicol Sci. 127:18–28. 2012. View Article : Google Scholar : PubMed/NCBI
52	Miranda RC, Pietrzykowski AZ, Tang Y, et al: MicroRNAs: master regulators of ethanol abuse and toxicity? Alcohol Clin Exp Res. 34:575–587. 2010. View Article : Google Scholar : PubMed/NCBI