Esophageal cancer is a common cause of cancer-related deaths worldwide. Squamous cell carcinoma (SCC) is the major histological type of esophageal cancer in developing countries including China, and the prognosis is very poor. Many microRNAs are involved in several important biological and pathologic processes, and promote tumorigenesis. To better understand the prognostic and therapeutic roles of microRNAs in ESCC, we reviewed the diagnosis and prognosis associated oncogenic microRNAs (e.g. miR-21 and miR-17-92 cluster) and tumor suppressor microRNAs (e.g. miR-375, miR-133a and miR-133b), and diagnosis and prognosis associated oncogenic target genes(e.g. PDCD4 and CCND1) and tumor suppressor target genes (e.g. EZH2 and PDK1). We also summarized the prognostic microRNA and target gene pairs(e.g. miR-296 and CCND1, miR214 and EZH2). Taken together, our review highlights the opportunities and challenges for microRNAs in the molecular diagnosis and target therapy of ESCC.
PingZ., MinD., WanqingC. and NiL., Cancer trends in China, Japanese Journal of Clinical Oncology40(5) (2010), 281-285.
2.
JemalA., SiegelR., WardE., HaoY., XuJ. and ThunM.J., Cancer statistics, CA Cancer J Clin59 (2009), 225-249.
3.
MacfarlaneL.A. and MurphyP.R., MicroRNA: Biogenesis, function and role in cancer, Current Genomics11(25) (2010), 537-561.
4.
BartelD.P., MicroRNAs: Genomics, biogenesis, mechanism, and function, Cell116 (2004), 281-297.
5.
CalinG.A. and CroceC.M., MicroRNA signatures in human cancers, Nature Reviews Cancer6 (2006), 857-866.
6.
YongG., ZhaoliC., LiangZ., FangZ., SushengS., XiaoliF., BaozhongL., XinM., XiM. and MingyongL., Distinctive microRNA profiles relating to patient survival in esophageal squamous cell carcinoma, Cancer Research68 (2008), 26-33.
7.
ChenZ., LiuX., HuZ., WangY., LiuM., LiuX., LiH., JiR., GuoQ. and ZhouY., Identification and characterization of tumor suppressor and oncogenic miRNAs in gastric cancer, Oncology Letters10 (2015).
8.
LiuF., ZhengS., LiuT., LiuQ., LiangM., LiX., SheyhidinI., LuX. and LiuW., MicroRNA-21 promotes the proliferation and inhibits apoptosis in Eca109 via activating ERK1/2/MAPK pathway, Mol Cell Biochem381 (2013), 115-125.
9.
AllgayerH., MicroRNA-21 (miR-21) post-transcriptionally downregulates tumor suppressor PDCD4 and stimulates invasion, intravasation and metastasis in colorectal cancer, Oncogene27 (2008), 2128-2136.
10.
HezovaR., KovarikovaA., SrovnalJ., ZemanovaM., HarustiakT., EhrmannJ., HajduchM., SvobodaM., SachlovaM. and SlabyO., Diagnostic and prognostic potential of miR-21, miR-29c, miR-148 and miR-203 in adenocarcinoma and squamous cell carcinoma of esophagus, Diagn Pathol10 (2015), 42.
11.
AkagiI., MiyashitaM., IshibashiO., MishimaT., KikuchiK., MakinoH., NomuraT., HagiwaraN., UchidaE. and TakizawaT., Relationship between altered expression levels of MIR21, MIR143, MIR145, and MIR205 and clinicopathologic features of esophageal squamous cell carcinoma, Dis Esophagus24 (2011), 523-530.
12.
LiP., MaoW.M., ZhengZ.G., DongZ.M. and LingZ.Q., Down-regulation of PTEN expression modulated by dysregulated miR-21 contributes to the progression of esophageal cancer, Dig Dis Sci58 (2013), 3483-3493.
13.
WangN., ZhangC.Q., HeJ.H., DuanX.F., WangY.Y., JiX., ZangW.Q., LiM., MaY.Y., WangT. and ZhaoG.Q., MiR-21 down-regulation suppresses cell growth, invasion and induces cell apoptosis by targeting FASL, TIMP3, and RECK genes in esophageal carcinoma, Dig Dis Sci58 (2013), 1863-1870.
14.
WuC., LiM., HuC. and DuanH., Clinical significance of serum miR-223, miR-25 and miR-375 in patients with esophageal squamous cell carcinoma, Mol Biol Rep41 (2014), 1257-1266.
15.
WuC., WangC., GuanX., LiuY., LiD., ZhouX., ZhangY., ChenX., WangJ., ZenK., ZhangC.Y. and ZhangC., Diagnostic and prognostic implications of a serum miRNA panel in oesophageal squamous cell carcinoma, PLoS One9 (2014), e92292.
16.
LiQ., ZouC., ZouC., HanZ., XiaoH., WeiH., WangW., ZhangL., ZhangX. and TangQ., MicroRNA-25 functions as a potential tumor suppressor in colon cancer by targeting Smad7, Cancer Letters335 (2013), 168-174.
17.
ZhangH., ZuoZ., LuX., WangL., WangH. and ZhuZ., MiR-25 regulates apoptosis by targeting bim in human ovarian cancer, Oncology Reports27 (2012), 594-598.
18.
XuX., ChenZ., ZhaoX., WangJ., DingD., WangZ., TanF., TanX., ZhouF., SunJ., SunN., GaoY., ShaoK., LiN., QiuB. and HeJ., MicroRNA-25 promotes cell migration and invasion in esophageal squamous cell carcinoma, Biochem Biophys Res Commun421 (2012), 640-645.
19.
OsadaH. and TakahashiT., let-7 and miR-17-92: Small-sized major players in lung cancer development, Cancer Science102 (2011), 9– 17.
LiuM., WangZ., YangS., ZhangW., HeS., HuC., ZhuH., QuanL., BaiJ. and XuN., TNF-alpha is a novel target of miR-19a, Int J Oncol38 (2011), 1013-1022.
22.
XuX.L., JiangY.H., FengJ.G., SuD., ChenP.C. and MaoW.M., MicroRNA-17, microRNA-18a, and microRNA-19a are prognostic indicators in esophageal squamous cell carcinoma, Ann Thorac Surg97 (2014), 1037-1045.
23.
ChenZ.L., ZhaoX.H., WangJ.W., LiB.Z., WangZ., SunJ., TanF.W., DingD.P., XuX.H., ZhouF., TanX.G., HangJ., ShiS.S., FengX.L. and HeJ., microRNA-92a promotes lymph node metastasis of human esophageal squamous cell carcinoma via E-cadherin, J Biol Chem286 (2011), 10725-10734.
24.
KutanziK.R., YurchenkoO.V., BelandF.A., CheckhunV.F. and PogribnyI.P., MicroRNA-mediated drug resistance in breast cancer, Clinical Epigenetics2 (2011), 171-185.
25.
IsozakiY., HoshinoI., NohataN., KinoshitaT., AkutsuY., HanariN., MoriM., YoneyamaY., AkanumaN., TakeshitaN., MaruyamaT., SekiN., NishinoN., YoshidaM. and MatsubaraH., Identification of novel molecular targets regulated by tumor suppressive miR-375 induced by histone acetylation in esophageal squamous cell carcinoma, Int J Oncol41 (2012), 985-994.
26.
Kar LokK., KwongD.L.W., Tim Hon-ManC., Simon Ying-KitL., LeileiC., YanL., Yan-RuQ. and Xin-YuanG., MicroRNA-375 inhibits tumour growth and metastasis in oesophageal squamous cell carcinoma through repressing insulin-like growth factor 1 receptor, Gut61 (2012), 33-42.
27.
NijiroN., ToyoyukiH., HidekiE. and NaohikoS., microRNA-1/133a and microRNA-206/133b clusters: dysregulation and functional roles in human cancers, Oncotarget3 (2012), 9-21.
28.
ChenG., PengJ., ZhuW., TaoG., SongY., ZhouX. and WangW., Combined downregulation of microRNA-133a and microRNA-133b predicts chemosensitivity of patients with esophageal squamous cell carcinoma undergoing paclitaxel-based chemotherapy, Med Oncol31 (2014), 263.
29.
AkanumaN., HoshinoI., AkutsuY., MurakamiK., IsozakiY., MaruyamaT., YusupG., QinW., ToyozumiT., TakahashiM., SuitoH., HuX., SekinoN. and MatsubaraH., MicroRNA-133a regulates the mRNAs of two invadopodia-related proteins, FSCN1 and MMP14, in esophageal cancer, Br J Cancer110 (2014), 189-198.
30.
SuzukiS., YokoboriT., TanakaN., SakaiM., SanoA., InoseT., SohdaM., NakajimaM., MiyazakiT., KatoH. and KuwanoH., CD47 expression regulated by the miR-133a tumor suppressor is a novel prognostic marker in esophageal squamous cell carcinoma, Oncol Rep28 (2012), 465-472.
31.
XingX. and LiZ., Expression of miR-143 and miR-145 and their functional study in gastric carcinoma, Zhonghua Wei Chang Wai Ke Za Zhi = Chinese Journal of Gastrointestinal Surgery18 (2015).
32.
ZhuH., DoughertyU., RobinsonV., MustafiR., PekowJ., KupferS., LiY.C., HartJ., GossK. and FicheraA., EGFR signals downregulate tumor suppressors miR-143 and miR-145 in Western diet-promoted murine colon cancer: Role of G1 regulators, Molecular Cancer Research9 (2011), 960-975.
33.
LiuR., LiaoJ., YangM., ShengJ., YangH., WangY. et al., The cluster of miR-143 and miR-145 affects the risk for esophageal squamous cell carcinoma through co-regulating fascin homolog 1, Plos One7 (2012), e33987-e33987.
34.
FassanM., CagolM., PennelliG., RizzettoC., GiacomelliL., BattagliaG., ZaninottoG., AnconaE., RuolA. and RuggeM., Programmed cell death 4 protein in esophageal cancer, Oncol Rep24 (2010), 135-139.
35.
LiY., GuoH., DongD., WuH. and LiE., Expression and prognostic relevance of cyclophilin A and matrix metalloproteinase 9 in esophageal squamous cell carcinoma, Diagn Pathol8 (2013), 207.
36.
WangM.T., ChenG., AnS.J., ChenZ.H., HuangZ.M., XiaoP., BenX.S., XieZ., ChenS.L., LuoD.L., TangJ.M., LinJ.Y., ZhangX.C. and WuY.L., Prognostic significance of cyclinD1 amplification and the co-alteration of cyclinD1/pRb/ppRb in patients with esophageal squamous cell carcinoma, Dis Esophagus25 (2012), 664-670.
37.
LiY., YuH., LuoR.Z., ZhangY., ZhangM.F., WangX. and JiaW.H., Elevated expression of Rad51 is correlated with decreased survival in resectable esophageal squamous cell carcinoma, J Surg Oncol104 (2011), 617-222.
38.
HaS.Y. and KimS.H., Co-expression of Bmi1 and EZH2 as an independent poor prognostic factor in esophageal squamous cell carcinoma, Pathol Res Pract208 (2012), 462-469.
39.
YangZ., WuZ., LiuT., HanL., WangC., YangB. and ZhengF., Upregulation of PDK1 associates with poor prognosis in esophageal squamous cell carcinoma with facilitating tumorigenicity in vitro, Med Oncol31 (2014), 337.
40.
CaoH.H., ZhangS.Y., ShenJ.H., WuZ.Y., WuJ.Y., WangS.H., LiE.M. and XuL.Y., A three-protein signature and clinical outcome in esophageal squamous cell carcinoma, Oncotarget6 (2015), 5435-5448.
41.
HongL., HanY., ZhangH., LiM., GongT., SunL., WuK., ZhaoQ. and FanD., The prognostic and chemotherapeutic value of miR-296 in esophageal squamous cell carcinoma, Ann Surg251 (2010), 1056-1063.
42.
HuangS.D., YangY., ZhuangC.W., LiB.L., GongD.J., WangS.G., ZengZ.Y. and ChengH.Z., MicroRNA-98 and microRNA-214 post-transcriptionally regulate enhancer of zeste homolog 2 and inhibit migration and invasion in human esophageal squamous cell carcinoma, Molecular Cancer11 (2012), 756-756.
43.
ChenY., WangX., LiF., ZhangL., MaL. and LiuY., Relationship between expression of P27, Fragile Histidine Triad (FHT), phosphatase and tensin homolog deleted on chromosome ten (PTEN), P73, and prognosis in esophageal squamous cell carcinoma, Ann Diagn Pathol19 (2015), 33-36.
44.
HarazonoY., MuramatsuT., EndoH., UzawaN., KawanoT., HaradaK., InazawaJ. and KozakiK., MiR-655 Is an EMT-Suppressive microrna targeting ZEB1 and TGFBR2, Plos One8 (2013), e62757-e62757.
45.
HirashimaK., BabaY., WatanabeM., KarashimaR.I., SatoN., YuI., HiyoshiY., NagaiY., HayashiN. and IyamaK.I., Phosphorylated mTOR expression is associated with poor prognosis for patients with esophageal squamous cell carcinoma, Annals of Surgical Oncology17(8) (2010), 2486-2493.
46.
KuoY.Z., TaiY.H., LoH.I., ChenY.L., ChengH.C., FangW.Y., LinS.H., YangC.L., TsaiS.T. and WuL.W., MiR-99a exerts anti-metastasis through inhibiting myotubularin-related protein 3 expression in oral cancer, Oral Dis20 (2014), e65-e75.
47.
SunN., ChangL., ChangT., LiX. et al., MicroRNA-195-Cdc42 axis acts as a prognostic factor of esophageal squamous cell carcinoma, International Journal of Clinical and Experimental Pathology7 (2014).
48.
ZhouY. and HongL., Prediction value of miR-483 and miR-214 in prognosis and multidrug resistance of esophageal squamous cell carcinoma, Genet Test Mol Biomarkers17 (2013), 470-474.
49.
ShenW.W., ZhiZ., ZhuW.X. and FuG.H., MiR-142-3p functions as a tumor suppressor by targeting CD133, ABCG2, and Lgr5 in colon cancer cells, Journal of Molecular Medicine91 (2013), 989-1000.
50.
IliopoulosD., JaegerS.A., HirschH.A., BulykM.L. and StruhlK., STAT3 activation of miR-21 and miR-181b-1, via PTEN and CYLD, are part of the epigenetic switch linking inflammation to cancer, Molecular Cell39 (2010), 493-506.
51.
TanakaK., MiyataH., YamasakiM., SugimuraK., TakahashiT., KurokawaY., NakajimaK., TakiguchiS., MoriM. and DokiY., Circulating miR-200c levels significantly predict response to chemotherapy and prognosis of patients undergoing neoadjuvant chemotherapy for esophageal cancer, Ann Surg Oncol20(3) (2013), S607-S615.
52.
ChenM.L., LiuS.L. and WangX.K., MiR-200c inhibits invasion and migration in human colon cancer cells SW480/620 by targeting ZEB1, Clinical and Experimental Metastasis29 (2012), 457-469.
53.
HumphreysK.J., MckinnonR.A. and MichaelM.Z., MiR-18a inhibits CDC42 and plays a tumour suppressor role in colorectal cancer cells, Plos One9 (2014), e112288-e112288.
54.
MurataT., TakayamaK., KatayamaS., UranoT., Horie-InoueK., IkedaK., TakahashiS., KawazuC., HasegawaA. and OuchiY., MiR-148a is an androgen-responsive microRNA that promotes LNCaP prostate cell growth by repressing its target CAND1 expression, Prostate Cancer and Prostatic Diseases13 (2010), 356-361.
55.
XuM., JinH., XuC.X., SunB., SongZ.G., BiW.Z. and WangY., MiR-382 inhibits osteosarcoma metastasis and relapse by targeting Y box-binding protein 1, Molecular Therapy the Journal of the American Society of Gene Therapy23 (2014).
56.
ZhangM., ZhouS., ZhangL., ZhangJ., CaiH., ZhuJ., HuangC. and WangJ., MiR-518b is down-regulated, and involved in cell proliferation and invasion by targeting Rap1b in esophageal squamous cell carcinoma, FEBS Letters586 (2012), 3508-3521.
57.
SiegelR., DeSantisC., VirgoK., SteinK., MariottoA., SmithT., CooperD., GanslerT., LerroC., FedewaS., LinC., LeachC., CannadyR.S., ChoH., ScoppaS., HacheyM., KirchR., JemalA. and WardE., Cancer treatment and survivorship statistics, 2012, CA Cancer J Clin62 (2012), 220-241.
58.
ZhaoY., SchetterA.J., YangG.B., NguyenG., MatheE.A., LiP., CaiH., YuL., LiuF. and HangD., MicroRNA and inflammatory gene expression as prognostic marker for overall survival in esophageal squamous cell carcinoma, International Journal of Cancer132 (2013), 2901-2909.
59.
YokoboriT., SuzukiS., TanakaN., InoseT., SohdaM., SanoA., SakaiM., NakajimaM., MiyazakiT. and KatoH., MiR-150 is associated with poor prognosis in esophageal squamous cell carcinoma via targeting the EMT inducer ZEB1, Cancer Science104 (2013), 48-54.
60.
SunJ., ChenZ., TanX., ZhouF., TanF., GaoY., SunN., XuX., ShaoK. and HeJ., MicroRNA-99a/100 promotes apoptosis by targeting mTOR in human esophageal squamous cell carcinoma, Medical Oncology30 (2013), 758-758.
61.
JiangchaoL., XiaodongL., YanL., HongY., LijingW., YanruQ., HaiboL., LiF. and Xin-YuanG., Cell-Specific Detection of miR-375 Downregulation for predicting the prognosis of esophageal squamous cell carcinoma by miRNA in situ hybridization, Plos One8 (2013), e53582-e53582.
62.
LiuR., YangM., MengY., LiaoJ., ShengJ., PuY., YinL. and KimS.J., Tumor-suppressive function of miR-139-5p in esophageal squamous cell carcinoma, Plos One8 (2013), e77068-e77068.
63.
ZhangM., YangQ., ZhangL., ZhouS., YeW., YaoQ., LiZ., HuangC., WenQ. and WangJ., MiR-302b is a potential molecular marker of esophageal squamous cell carcinoma and functions as a tumor suppressor by targeting ErbB4, Journal of Experimental and Clinical Cancer Research Cr33 (2014), 1-10.
64.
WangX.C., ZhangZ.B., WangY.Y., WuH.Y., LiD.G., MengA.M. and FanF.Y., Increased miRNA-22 expression sensitizes esophageal squamous cell carcinoma to irradiation, Journal of Radiation Research54 (2012), 401-408.
65.
SongY., LiJ., ZhuY., DaiY., ZengT., LiuL., LiJ., WangH., QinY. and ZengM., MicroRNA-9 promotes tumor metastasis via repressing E-cadherin in esophageal squamous cell carcinoma, Oncotarget5 (2014), 11669.
66.
ZhangH.F., ZhangK., LiaoL.D., LiL.Y., DuZ.P., WuB.L., WuJ.Y., XuX.E., ZengF.M., ChenB., CaoH.H., ZhuM.X., DaiL.H., LongL., WuZ.Y., LaiR., XuL.Y. and LiE.M., MiR-200b suppresses invasiveness and modulates the cytoskeletal and adhesive machinery in esophageal squamous cell carcinoma cells via targeting Kindlin-2, Carcinogenesis35 (2014), 292-301.
67.
ZhangB.J., GongH.Y., FangZ., LiuD.J. and LiuH.X., Up-regulation of miR-335 predicts a favorable prognosis in esophageal squamous cell carcinoma, Int J Clin Exp Pathol7 (2014).
68.
LiuK., LiL., RusidanmuA., WangY. and LvX., Down-regulation of mir-1294 is related to dismal prognosis of patients with esophageal squamous cell carcinoma through elevating C-MYC expression, Cellular Physiology and Biochemistry36 (2015), 100-110.
69.
QiB., LuJ.G., YaoW.J., ChangT.M., QinX.G., JiY.H., WangT.Y., LiuS.G., LiH.C. and LiuY.Z., Downregulation of microRNA-382 is associated with poor outcome of esophageal squamous cell carcinoma, World Journal of Gastroenterology: WJG21 (2015), 6884.
MoriY., IshiguroH., KuwabaraY., KimuraM., MitsuiA., OgawaR., KatadaT., HarataK., TanakaT. and ShiozakiM., MicroRNA-21 induces cell proliferation and invasion in esophageal squamous cell carcinoma, Molecular Medicine Reports2 (2009), 235-239.
72.
LiuR., GuJ., JiangP., ZhengY., LiuX., JiangX., HuangE., XiongS., XuF. and LiuG., DNMT1-MicroRNA126 epigenetic circuit contributes to esophageal squamous cell carcinoma growth via ADAM9-EGFR-AKT signaling, Clinical Cancer Research21 (2015), 854-863.
73.
LiH., ZhengD., ZhangB., LiuL., OuJ., ChenW., XiongS., GuY. and YangJ., Mir-208 promotes cell proliferation by repressing SOX6 expression in human esophageal squamous cell carcinoma, J Transl Med12 (2014), 196.
74.
FassanM., CagolM., PennelliG., RizzettoC., GiacomelliL., BattagliaG., ZaninottoG., AnconaE., RuolA. and RuggeM., Programmed cell death 4 protein in esophageal cancer, Oncology Reports24 (2010), 135-139.
75.
YangX., WangQ., DaiW., ZhangJ. and ChenX., Overexpression of zinc finger E-box binding homeobox factor 1 promotes tumor invasiveness and confers unfavorable prognosis in esophageal squamous cell carcinoma, Tumor Biology35 (2014), 11977-11984.
76.
ImsumranA., AdachiY., YamamotoH., LiR., WangY., MinY., PiaoW., NoshoK., ArimuraY. and ShinomuraY., Insulin-like growth factor-I receptor as a marker for prognosis and a therapeutic target in human esophageal squamous cell carcinoma, Carcinogenesis28 (2007), 947-956.
77.
LiY., GuoH., DongD., WuH. and LiE., Expression and prognostic relevance of cyclophilin A and matrix metalloproteinase 9 in esophageal squamous cell carcinoma, Diagnostic Pathology8 (2013).
78.
XuS., JojiK., HiroharuY., DaisukeS. and HirokazuN., Nuclear translocation of HER-4/c-erbB-4 is significantly correlated with prognosis of esophageal squamous cell carcinoma, Journal of Surgical Oncology97 (2008), 44-50.
