microRNAs in esophageal cancer (Review)

He,Bin; Yin,Bangliang; Wang,Baoxiang; Xia,Zhenkun; Chen,Chen; Tang,Jingqun

doi:10.3892/mmr.2012.975

microRNAs in esophageal cancer (Review)

Authors:
- Bin He
- Bangliang Yin
- Baoxiang Wang
- Zhenkun Xia
- Chen Chen
- Jingqun Tang
View Affiliations

Affiliations: Department of Cardiothoracic Surgery, the Second Xiangya Hospital of Central South University, Changsha, Hunan 410011, P.R. China
Published online on: June 29, 2012 https://doi.org/10.3892/mmr.2012.975
Pages: 459-465

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 cancer (EC) is one of the most common malignant tumors worldwide. EC is usually diagnosed at a locally advanced stage or at a stage with involvement of lymph nodes. Despite aggressive treatment, the overall five-year survival rate remains poor. microRNAs (miRNAs) are small, non-coding endogenous RNAs that negatively regulate gene expression at the post-transcriptional and/or translational level. Accumulating evidence suggests that the deregulation of miRNAs not only results in cancer progression, but also directly promotes tumor initiation. Previous studies found that miRNAs are frequently deregulated in EC, indicating that miRNAs are important in tumorigenesis. In this review, we summarize therecently recognized miRNA expression and its impact on the biology of EC and the potential applications for EC.

View Figures

View References

1	Parkin DM, Bray F, Ferlay J and Pisani P: Global cancer statistics, 2002. CA Cancer J Clin. 55:74–108. 2005.
2	Enzinger PC and Mayer RJ: Esophageal cancer. N Engl J Med. 349:2241–2252. 2003.
3	Mishima T, Akagi I, Miyashita M, Ishibashi O, Mizuguchi Y, Tajiri T, et al: Study of microRNA expression profiles of esophageal cancer. J Nippon Med Sch. 76:432009.
4	Lakshmipathy U and Hart RP: Concise review: microRNA expression in multi-potent mesenchymal stromal cells. Stem Cells. 26:356–363. 2008.
5	Calin GA, Sevignani C, Dumitru CD, Hyslop T, Noch E, Yendamuri S, et al: Human microRNA genes are frequently located at fragile sites and genomic regions involved in cancers. Proc Natl Acad Sci USA. 101:2999–3004. 2004.
6	Tsai WC, Hsu PW, Lai TC, et al: MicroRNA-122, a tumor suppressor microRNA that regulates intrahepatic metastasis of hepatocellular carcinoma. Hepatology. 49:1571–1582. 2009.
7	Ferdin J, Kunej T and Calin GA: Non-coding RNAs: identification of cancer-associated microRNAs by gene profiling. Technol Cancer Res Treat. 9:123–138. 2010.
8	Paranjape T, Slack FJ and Weidhaas JB: MicroRNAs: tools for cancer diagnostics. Gut. 58:1546–1554. 2009.
9	Lee Y, Kim M, Han J, Yeom KH, Lee S, Baek SH and Kim VN: MicroRNA genes are transcribed by RNA polymerase II. EMBO J. 23:40512–4060. 2004.
10	Cho WC: MicroRNAs in cancer - from research to therapy. Biochim Biophys Acta. 1805:209–217. 2010.
11	Cai X, Hagedorn CH and Cullen BR: Human microRNAs are processed from capped, polyadenylated transcripts that can also function as mRNAs. RNA. 10:19572–1966. 2004.
12	Lee Y, Ahn C, Han J, Choi H, Kim J, Yim J, Lee J, Provost P, et al: The nuclear RNase III Drosha initiates microRNA processing. Nature. 425:415–419. 2003.
13	Bohnsaek MT, CzaPlinski K and Gorlieh D: Exportin5 is a RanGTP-dependent dsRNA-binding protein that mediates nuclear export of pre-miRNAs. RNA. 10:185–191. 2004.
14	Denli AM, Tops BB, Plasterk RH, Ketting RF and Hannon GJ: Processing of primary microRNAs by the Microprocessor complex. Nature. 432:231–235. 2004.
15	Gregory RI and Shiekhattar R: MicroRNA biogenesis and cancer. Cancer Res. 65:3509–3512. 2005.
16	Joshua-Tor L: The Argonautes. Cold Spring Harb Symp Quant Biol. 71:67–72. 2006.
17	Esquela-Kerscher A and Slack FJ: Oncomirs - microRNAs with a role in cancer. Nat Rev Cancer. 6:259–269. 2006.
18	Lee RC, Feinbaum RL and Ambros V: The C. elegans heterochronic gene encodes small RNAs with antisense complementarity to lin-14. Cell. 75:843–854. 1993.
19	Wang B, Doench JG and Novina CD: Analysis of microRNA effector functions in vitro. Methods. 43:91–104. 2007.
20	Calin GA, Dumitru CD, Shimizu M, Bichi R, Zupo S, Noch E, Aldler H, et al: Frequent deletions and down-regulation of micro-RNA genes miR15 and miR16 at 13q14 in chronic lymphocytic leukemia. Proc Natl Acad Sci USA. 99:15524–15529. 2002.
21	Cimmino A, Calin GA, Fabbri M, Iorio MV, Ferracin M, Shimizu M, et al: miR-15 and miR-16 induce apoptosis by targeting BCL2. Proc Natl Acad Sci USA. 102:13944–13949. 2005.
22	Takamizawa J, Konishi H, Yanagisawa K, Tomida S, Osada H, et al: Reduced expression of the let-7 microRNAs in human lung cancers in association with shortened postoperative survival. Cancer Res. 64:3753–3756. 2004.
23	Johnson SM, Lin SY and Slack FJ: The time of appearance of the C. elegans let-7 microRNA is transcriptionally controlled utilizing a temporal regulatory element in its promoter. Dev Biol. 259:364–379. 2003.
24	Mott JL, Kobayashi S, Bronk SF and Gores GJ: miR-29 regulates Mcl-1 protein expression and apoptosis. Oncogene. 26:6133–6140. 2007.
25	Gramantieri L, Ferracin M, Fornari F, Veronese A, Sabbioni S, Liu CG, et al: Cyclin G1 is a target of miR-122a, a microRNA frequently down-regulated in human hepatocellular carcinoma. Cancer Res. 67:6092–6099. 2007.
26	Raver-Shapira N, Marciano E, Meiri E, Spector Y, Rosenfeld N, et al: Transcriptional activation of miR-34a contributes to p53-mediated apoptosis. Mol Cell. 26:731–743. 2007.
27	Raver-Shapira N and Oren M: Tiny actors, great roles: microRNAs in p53's service. Cell Cycle. 6:2656–2661. 2007.
28	Wu H, Zhu S and Mo YY: Suppression of cell growth and invasion by miR-205 in breast cancer. Cell Res. 19:439–448. 2009.
29	Nelson KM and Weiss GJ: MicroRNAs and cancer: past, present, and potential future. Mol Cancer Ther. 7:3655–3660. 2008.
30	Lee YS and Dutta A: MicroRNAs in cancer. Annu Rev Pathol. 4:199–227. 2009.
31	Latronico MV, Catalucci D and Condorelli G: MicroRNA and cardiac pathologies. Physiol Genomics. 34:239–242. 2008.
32	He L, Thomson JM, Hemann MT, Hernando-Monge E, Mu D, Goodson S, et al: A miRNA polycistron as a potential human oncogene. Nature. 435:828–833. 2005.
33	O'Donnell KA, Wentzel EA, Zeller KI, Dang CV and Mendell JT: c-Myc-regulated microRNAs modulate E2F1 expression. Nature. 435:839–843. 2005.
34	Mu P, Han YC, Betel D, Yao E, Squatrito M, Ogrodowski P, et al: Genetic dissection of the miR-17-92 cluster of microRNAs in Myc-induced B-cell lymphomas. Genes Dev. 23:2806–2811. 2009.
35	Zhu S, Si ML, Wu H and Mo YY: MicroRNA-21 targets the tumor suppressor gene tropomyosin 1 (TPM1). J Biol Chem. 282:14328–14336. 2007.
36	Ma L, Teruya-Feldstein J and Weinberg RA: Tumour invasion and metastasis initiated by microRNA-10b in breast cancer. Nature. 449:682–688. 2007.
37	Feber A, Xi L, Luketich JD, Pennathur A, Landreneau RJ, Wu M, et al: MicroRNA expression profiles of esophageal cancer. J Thorac Cardiovasc Surg. 135:255–260. 2008.
38	Guo Y, Chen Z, Zhang L, Shi S, Feng X, et al: Distinctive microRNA profiles relating to patient survival in esophageal squamous cell carcinoma. Cancer Res. 68:26–33. 2008.
39	Mathé EA, Nguyen GH, Bowman ED, Zhao Y, Budhu A, Schetter AJ, Braun R, Reimers M, Kumamoto K, Hughes D, et al: MicroRNA expression in squamous cell carcinoma and adenocarcinoma of the esophagus: associations with survival. Clin Cancer Res. 15:6192–6200. 2009.
40	Kan T and Meltzer SJ: MicroRNAs in Barrett's esophagus and esophageal adenocarcinoma. Curr Opin Pharmacol. 9:727–732. 2009.
41	Maru DM, Singh RR, Hannah C, Albarracin CT, Li YX, Abraham R, Romans AM, Yao H, Luthra MG, Anandasabapathy S, et al: MicroRNA-196a is a potential marker of progression during Barrett's metaplasia-dysplasia-invasive adenocarcinoma sequence in esophagus. Am J Pathol. 174:1940–1948. 2009.
42	Ogawa R, Ishiguro H, Kuwabara Y, Kimura M, Mitsui A, Katada T, Harata K, Tanaka T and Fujii Y: Expression profiling of micro-RNAs in human esophageal squamous cell carcinoma using RT-PCR. Med Mol Morphol. 42:102–109. 2009.
43	Zhang T, Zhao D, Wang Q, Yu X, Cui Y, Guo L and Lu SH: MicroRNA-1322 regulates ECRG2 allele specifically and acts as a potential biomarker in patients with esophageal squamous cell carcinoma. Mol Carcinog. Feb 7–2012.(Epub ahead of print).
44	Lin RJ, Xiao DW, Liao LD, Chen T, Xie ZF, Huang WZ, Wang WS, Jiang TF, Wu BL, Li EM and Xu LY: MiR-142-3p as a potential prognostic biomarker for esophageal squamous cell carcinoma. J Surg Oncol. 105:175–182. 2012.
45	Leidner RS, Ravi L, Leahy P, Chen Y, Bednarchik B, Streppel M, Canto M, Wang SJ, Maitra A, Willis J, et al: The microRNAs, MiR-31 and MiR-375, as candidate markers in Barrett's esophageal carcinogenesis. Genes Chromosomes Cancer. 51:473–479. 2012.
46	Hu Y, Correa AM, Hoque A, Guan B, Ye F, Huang J, Swisher SG, Wu TT, Ajani JA and Xu XC: Prognostic significance of differentially expressed miRNAs in esophageal cancer. Int J Cancer. 128:132–143. 2011.
47	Komatsu S, Ichikawa D, Takeshita H, Tsujiura M, Morimura R, Nagata H, Kosuga T, Iitaka D, Konishi H, Shiozaki A, et al: Circulating microRNAs in plasma of patients with oesophageal squamous cell carcinoma. Br J Cancer. 28;105:104–111. 2011.
48	Zhang C, Wang C, Chen X, Yang C, Li K, Wang J, Dai J, Hu Z, Zhou X, Chen L, et al: Expression profile of microRNAs in serum: a fingerprint for esophageal squamous cell carcinoma. Clin Chem. 56:1871–1879. 2010.
49	Zhang T, Wang Q, Zhao D, Cui Y, Cao B, Guo L and Lu SH: The oncogenetic role of microRNA-31 as a potential biomarker in oesophageal squamous cell carcinoma. Clin Sci (Lond). 121:437–447. 2011.
50	Kano M, Seki N, Kikkawa N, Fujimura L, Hoshino I, Akutsu Y, Chiyomaru T, Enokida H, Nakagawa M and Matsubara H: miR-145, miR-133a and miR-133b: Tumor-suppressive miRNAs target FSCN1 in esophageal squamous cell carcinoma. Int J Cancer. 127:2804–2814. 2010.
51	Wu BL, Xu LY, Du ZP, Liao LD, Zhang HF, Huang Q, Fang GQ and Li EM: MiRNA profile in esophageal squamous cell carcinoma: downregulation of miR-143 and miR-145. World J Gastroenterol. 17:79–88. 2011.
52	Matsushima K, Isomoto H, Kohno S and Nakao K: MicroRNAs and esophageal squamous cell carcinoma. Digestion. 82:138–144. 2010.
53	Tian Y, Luo A, Cai Y, Su Q, Ding F, Chen H and Liu Z: MicroRNA-10b promotes migration and invasion through KLF4 in human esophageal cancer cell lines. J Biol Chem. 285:7986–7994. 2010.
54	Chen ZL, Zhao XH, Wang JW, Li BZ, Wang Z, Sun J, Tan FW, Ding DP, Xu XH, Zhou F, et al: microRNA-92a promotes lymph node metastasis of human esophageal squamous cell carcinoma via E-cadherin. J Biol Chem. 286:10725–10734. 2011.
55	Li S, Li Z, Guo F, Qin X, Liu B, Lei Z, Song Z, Sun L, Zhang HT, You J and Zhou Q: miR-223 regulates migration and invasion by targeting Artemin in human esophageal carcinoma. J Biomed Sci. 18:242011.
56	Hummel R, Hussey DJ, Michael MZ, Haier J, Bruewer M, Senninger N and Watson DI: miRNAs and their association with locoregional staging and survival following surgery for esophageal carcinoma. Ann Surg Oncol. 18:253–260. 2011.
57	Mori Y, Ishiguro H, Kuwabara Y, Kimura M, Mitsui A, Ogawa R, Katada T, Harata K, Tanaka T, Shiozaki M and Fujii Y: MicroRNA-21 induces cell proliferation and invasion in esophageal squamous cell carcinoma. Mol Med Rep. 2:235–239. 2009.
58	Hiyoshi Y, Kamohara H, Karashima R, Sato N, Imamura Y, Nagai Y, Yoshida N, Toyama E, Hayashi N, Watanabe M and Baba H: MicroRNA-21 regulates the proliferation and invasion in esophageal squamous cell carcinoma. Clin Cancer Res. 15:1915–1922. 2009.
59	Ma WJ, Lv GD, Tuersun A, Liu Q, Liu H, Zheng ST, Huang CG, Feng JG, Wang X, Lin RY, Sheyhidin I and Lu XM: Role of microRNA-21 and effect on PTEN in Kazakh's esophageal squamous cell carcinoma. Mol Biol Rep. 38:3253–3260. 2011.
60	Feber A, Xi L, Pennathur A, Gooding WE, Bandla S, Wu M, Luketich JD, Godfrey TE and Litle VR: MicroRNA prognostic signature for nodal metastases and survival in esophageal adenocarcinoma. Ann Thorac Surg. 91:1523–1530. 2011.
61	Ohashi S, Natsuizaka M, Naganuma S, Kagawa S, Kimura S, Itoh H, Kalman RA, Nakagawa M, Darling DS, Basu D, et al: NOTCH3-mediated squamous cell differentiation program limits expansion of EMT-competent cells that express the ZEB transcription factors. Cancer Res. 71:6836–6847. 2011.
62	Matsushima K, Isomoto H, Yamaguchi N, Inoue N, Machida H, Nakayama T, Hayashi T, Kunizaki M, Hidaka S, Nagayasu T, et al: MiRNA-205 modulates cellular invasion and migration via regulating zinc finger E-box binding homeobox 2 expression in esophageal squamous cell carcinoma cells. J Transl Med. 9:302011.
63	Kong KL, Kwong DL, Chan TH, Law SY, Chen L, Li Y, Qin YR and Guan XY: MicroRNA-375 inhibits tumour growth and metastasis in oesophageal squamous cell carcinoma through repressing insulin-like growth factor 1 receptor. Gut. 61:33–42. 2012.
64	Kurashige J, Watanabe M, Iwatsuki M, Kinoshita K, Saito S, Hiyoshi Y, Kamohara H, Baba Y, Mimori K and Baba H: Overexpression of microRNA-223 regulates the ubiquitin ligase FBXW7 in oesophageal squamous cell carcinoma. Br J Cancer. 106:182–188. 2012.
65	Ding DP, Chen ZL, Zhao XH, Wang JW, Sun J, Wang Z, Tan FW and Tan XG: miR-29c induces cell cycle arrest in esophageal squamous cell carcinoma by modulating cyclin E expression. Carcinogenesis. 32:1025–1032. 2011.
66	Kan T, Sato F, Ito T, Matsumura N, David S, Cheng Y, Agarwal R, Paun BC, Jin Z, Olaru AV, et al: The miR-106b-25 polycistron, activated by genomic amplification, functions as an oncogene by suppressing p21 and Bim. Gastroenterology. 136:1689–1700. 2009.
67	He L, He X, Lim LP, de Stanchina E, et al: A microRNA component of the p53 tumour suppressor network. Nature. 447:1130–1134. 2007.
68	Wijnhoven BP, Hussey DJ, Watson DI, Tsykin A, Smith CM, et al: microRNA profiling of Barrett's oesophagus and oesophageal adenocarcinoma. Br J Surg. 97:853–861. 2010.
69	Lee KH, Goan YG, Hsiao M, Lee CH, et al: MicroRNA-373 (miR-373) post-transcriptionally regulates large tumor suppressor, homolog2 (LATS2) and stimulates proliferation in human esophageal cancer. Exp Cell Res. 315:2529–2538. 2009.
70	Luthra R, Singh RR, Luthra MG, Li YX, Hannah C, Romans AM, Barkoh BA, Chen SS, Ensor J, Maru DM, et al: MicroRNA-196a targets annexin A1: a microRNA-mediated mechanism of annexin A1 downregulation in cancers. Oncogene. 27:6667–6678. 2008.
71	Yuan Y, Zeng ZY, Liu XH, Gong DJ, Tao J, Cheng HZ and Huang SD: MicroRNA-203 inhibits cell proliferation by repressing ΔNp63 expression in human esophageal squamous cell carcinoma. BMC Cancer. 11:572011.
72	Liu M, Wang Z, Yang S, Zhang W, He S, Hu C, Zhu H, Quan L, Bai J and Xu N: TNF-α is a novel target of miR-19a. Int J Oncol. 38:1013–1022. 2011.
73	Tsuchiya S, Fujiwara T, Sato F, Shimada Y, Tanaka E, Sakai Y, Shimizu K and Tsujimoto G: MicroRNA-210 regulates cancer cell proliferation through targeting fibroblast growth factor receptor-like 1 (FGFRL1). J Biol Chem. 286:420–428. 2011.
74	Ryan BM, Robles AI and Harris CC: Genetic variation in microRNA networks: the implications for cancer research. Nat Rev Cancer. 10:389–402. 2010.
75	Wang K, Guo H, Hu H, Xiong G, Guan X, Li J, Xu X, Yang K and Bai Y: A functional variation in pre-microRNA-196a is associated with susceptibility of esophageal squamous cell carcinoma risk in Chinese Han. Biomarkers. 15:614–618. 2010.
76	Ye Y, Wang KK, Gu J, Yang H, et al: Genetic variations in microRNA-related genes are novel susceptibility loci for esophageal cancer risk. Cancer Prev Res (Phila). 1:460–469. 2008.
77	Guo H, Wang K, Xiong G, Hu H, Wang D, Xu X, Guan X, Yang K and Bai Y: A functional variant in microRNA-146a is associated with risk of esophageal squamous cell carcinoma in Chinese Han. Fam Cancer. 9:599–603. 2010.
78	Wu Y, Xiao Y, Ding X, Zhuo Y, Ren P, Zhou C and Zhou J: A miR-200b/200c/429-binding site polymorphism in the 3′ untranslated region of the AP-2α gene is associated with cisplatin resistance. PLoS One. 6:e290432011.
79	Kim VN: MicroRNA biogenesis: coordinated cropping and dicing. Nat Rev Mol Cell Biol. 6:376–385. 2005.
80	Saito Y, Liang G, Egger G, Friedman JM, Chuang JC, Coetzee GA and Jones PA: Specific activation of microRNA-127 with downregulation of the proto-oncogene BCL6 by chromatin-modifying drugs in human cancer cells. Cancer Cell. 9:435–443. 2006.
81	Esteller M: Epigenetics in cancer. N Engl J Med. 358:1148–1159. 2008.
82	Li X, Lin R and Li J: Epigenetic silencing of microRNA-375 regulates PDK1 expression in esophageal cancer. Dig Dis Sci. 56:2849–2856. 2011.
83	Chen X, Hu H, Guan X, Xiong G, Wang Y, Wang K, Li J, Xu X and Yang K: CpG island methylation status of miRNAs in esophageal squamous cell carcinoma. Int J Cancer. 130:1607–1613. 2012.
84	Hummel R, Wang T, Watson DI, Michael MZ, Van der Hoek M, Haier J and Hussey DJ: Chemotherapy-induced modification of microRNA expression in esophageal cancer. Oncol Rep. 26:1011–1017. 2011.
85	Imanaka Y, Tsuchiya S, Sato F, Shimada Y, Shimizu K and Tsujimoto G: MicroRNA-141 confers resistance to cisplatin-induced apoptosis by targeting YAP1 in human esophageal squamous cell carcinoma. J Hum Genet. 56:270–276. 2011.
86	Zhang H, Li M, Han Y, Hong L, Gong T, Sun L and Zheng X: Down-regulation of miR-27a might reverse multidrug resistance of esophageal squamous cell carcinoma. Dig Dis Sci. 55:2545–2551. 2010.
87	Hong L, Han Y, Zhang H, Li M, Gong T, Sun L, Wu K, Zhao Q and Fan D: The prognostic and chemotherapeutic value of miR-296 in esophageal squamous cell carcinoma. Ann Surg. 51:1056–1063. 2010.
88	Hamano R, Miyata H, Yamasaki M, Kurokawa Y, Hara J, Moon JH, Nakajima K, Takiguchi S, Fujiwara Y, Mori M and Doki Y: Overexpression of miR-200c induces chemoresistance in esophageal cancers mediated through activation of the Akt signaling pathway. Clin Cancer Res. 17:3029–3038. 2011.
89	Hummel R, Watson DI, Smith C, Kist J, Michael MZ, Haier J and Hussey DJ: Mir-148a improves response to chemotherapy in sensitive and resistant oesophageal adenocarcinoma and squamous cell carcinoma cells. J Gastrointest Surg. 15:429–438. 2011.
90	Zheng ZF, Su HF, Zou Y, Peng Z and Wu SX: Expression profiles of microRNAs in radioresistant esophageal cell line. Zhonghua Yi Xue Za Zhi. 91:639–642. 2011.(In Chinese).