MiR-139-5p inhibits migration and invasion of colorectal cancer by downregulating AMFR and NOTCH1

doi:10.1007/s13238-014-0093-5

Protein & Cell

2014, Vol. 5

Issue (11): 851-861 https://doi.org/10.1007/s13238-014-0093-5

本期目录

MiR-139-5p inhibits migration and invasion of colorectal cancer by downregulating AMFR and NOTCH1

Mingxu Song¹,Yuan Yin¹,Jiwei Zhang¹,Binbin Zhang¹,Zehua Bian¹,Chao Quan¹,Leyuan Zhou³,Yaling Hu¹,Qifeng Wang⁴,Shujuan Ni⁴,Bojian Fei²,Weili Wang²,Xiang Du⁴,Dong Hua¹,Zhaohui Huang^1,^*(

)

1. Wuxi Oncology Institute, the Affiliated Hospital of Jiangnan University, Wuxi 214062, China
2. Department of Surgical Oncology, the Affiliated Hospital of Jiangnan University, Wuxi 214062, China
3. Department of Radiation Oncology, the Affiliated Hospital of Jiangnan University, Wuxi 214062, China
4. Department of Pathology, Fudan University Shanghai Cancer Center, Shanghai 200032, China

全文: PDF(1727 KB)

Abstract：

MicroRNAs (miRNAs) that exert function by posttranscriptional suppression have recently brought insight in our understanding of the role of non-protein-coding RNAs in carcinogenesis and metastasis. In this study, we described the function and molecular mechanism of miR-139-5p in colorectal cancer (CRC) and its potential clinical application in CRC. We found that miR-139-5p was significantly downregulated in 73.8% CRC samples compared with adjacent noncancerous tissues (NCTs), and decreased miR-139-5p was associated with poor prognosis. Functional analyses demonstrated that ectopic expression of miR-139-5p suppressed CRC cell migration and invasion in vitro and metastasis in vivo. Mechanistic investigations revealed that miR-139-5p suppress CRC cell invasion and metastasis by targeting AMFR and NOTCH1. Knockdown of the two genes phenocopied the inhibitory effect of miR-139-5p on CRC metastasis. Furthermore, the protein levels of the two genes were upregulated in CRC samples compared with NCTs, and inversely correlated with the miR-139-5p expression. Increased NOTCH1 protein expression was correlated with poor prognosis of CRC patients. Together, our data indicate that miR-139-5p is a potential tumor suppressor and prognostic factor for CRC, and targeting miR-139-5p may repress the metastasis of CRC and improve survival.

Key words： miR-139-5p AMFR NOTCH1 colorectal cancer metastasis prognosis

收稿日期: 2014-06-14 出版日期: 2014-11-20

Corresponding Author(s): Zhaohui Huang

引用本文:

. [J]. Protein & Cell, 2014, 5(11): 851-861.
Mingxu Song,Yuan Yin,Jiwei Zhang,Binbin Zhang,Zehua Bian,Chao Quan,Leyuan Zhou,Yaling Hu,Qifeng Wang,Shujuan Ni,Bojian Fei,Weili Wang,Xiang Du,Dong Hua,Zhaohui Huang. MiR-139-5p inhibits migration and invasion of colorectal cancer by downregulating AMFR and NOTCH1. Protein Cell, 2014, 5(11): 851-861.

链接本文:

https://academic.hep.com.cn/pac/CN/10.1007/s13238-014-0093-5
https://academic.hep.com.cn/pac/CN/Y2014/V5/I11/851

1	Asangani IA, Rasheed SA, Nikolova DA, Leupold JH, Colburn NH, Post S, Allgayer H (2008) MicroRNA-21 (miR-21) post-transcriptionally downregulates tumor suppressor Pdcd4 and stimulates invasion, intravasation and metastasis in colorectal cancer. Oncogene 27: 2128-2136 https://doi.org/10.1038/sj.onc.1210856
2	Bao W, Fu HJ, Xie QS, Wang L, Zhang R, Guo ZY, Zhao J, Meng YL, Ren XL, Wang T (2011) HER2 interacts with CD44 to upregulate CXCR4 via epigenetic silencing of microRNA-139 in gastric cancer cells. Gastroenterology141(2076-2087): e2076
3	Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell116: 281-297 https://doi.org/10.1016/S0092-8674(04)00045-5
4	Bouyssou JM, Manier S, Huynh D, Issa S, Roccaro AM, Ghobrial IM (2014) Regulation of microRNAs in cancer metastasis. Biochim Biophys Acta1845(2): 255-265
5	Bu P, Chen KY, Chen JH, Wang L, Walters J, Shin YJ, Goerger JP, Sun J, Witherspoon M, Rakhilin N (2013) A microRNA miR-34a-regulated bimodal switch targets Notch in colon cancer stem cells. Cell Stem Cell 12: 602-615 https://doi.org/10.1016/j.stem.2013.03.002
6	Chen X, Guo X, Zhang H, Xiang Y, Chen J, Yin Y, Cai X, Wang K, Wang G, Ba Y (2009) Role of miR-143 targeting KRAS in colorectal tumorigenesis. Oncogene28: 1385-1392 https://doi.org/10.1038/onc.2008.474
7	Chiu CG, St-Pierre P, Nabi IR, Wiseman SM (2008) Autocrine motility factor receptor: a clinical review. Expert Rev Anticancer Ther8: 207-217 https://doi.org/10.1586/14737140.8.2.207
8	Chu D, Li Y, Wang W, Zhao Q, Li J, Lu Y, Li M, Dong G, Zhang H, Xie H (2010) High level of Notch1 protein is associated with poor overall survival in colorectal cancer. Ann Surg Oncol17: 1337-1342 https://doi.org/10.1245/s10434-009-0893-7
9	Esquela-Kerscher A, Slack FJ (2006) Oncomirs—microRNAs with a role in cancer. Nat Rev Cancer6: 259-269 https://doi.org/10.1038/nrc1840
10	Fang S, Ferrone M, Yang C, Jensen JP, Tiwari S, Weissman AM (2001) The tumor autocrine motility factor receptor, gp78, is a ubiquitin protein ligase implicated in degradation from the endoplasmic reticulum. Proc Natl Acad Sci USA98: 14422-14427 https://doi.org/10.1073/pnas.251401598
11	Gu W, Li X, Wang J (2013) miR-139 regulates the proliferation and invasion of hepatocellular carcinoma through the WNT/TCF-4 pathway. Oncol Rep31(1): 397-404
12	Guo J, Miao Y, Xiao B, Huan R, Jiang Z, Meng D, Wang Y (2009) Differential expression of microRNA species in human gastric cancer versus non-tumorous tissues. J Gastroenterol Hepatol24: 652-657 https://doi.org/10.1111/j.1440-1746.2008.05666.x
13	Guo H, Hu X, Ge S, Qian G, Zhang J (2012) Regulation of RAP1B by miR-139 suppresses human colorectal carcinoma cell proliferation. Int J Biochem Cell Biol44: 1465-1472 https://doi.org/10.1016/j.biocel.2012.05.015
14	Hellstrom M, Phng LK, Hofmann JJ, Wallgard E, Coultas L, Lindblom P, Alva J, Nilsson AK, Karlsson L, Gaiano N (2007) Dll4 signalling through Notch1 regulates formation of tip cells during angiogenesis. Nature445: 776-780 https://doi.org/10.1038/nature05571
15	Hristova NR, Tagscherer KE, Fassl A, Kopitz J, Roth W (2013) Notch1-dependent regulation of p27 determines cell fate in colorectal cancer. Int J Oncol43: 1967-1975
16	Hu YY, Zheng MH, Zhang R, Liang YM, Han H (2012) Notch signaling pathway and cancer metastasis. Adv Exp Med Biol727: 186-198 https://doi.org/10.1007/978-1-4614-0899-4_14
17	Huang Z, Huang S, Wang Q, Liang L, Ni S, Wang L, Sheng W, He X, Du X (2011) MicroRNA-95 promotes cell proliferation and targets sorting Nexin 1 in human colorectal carcinoma. Cancer Res71: 2582-2589 https://doi.org/10.1158/0008-5472.CAN-10-3032
18	Hurst DR, Edmonds MD, Welch DR (2009) Metastamir: the field of metastasis-regulatory microRNA is spreading. Cancer Res69: 7495-7498 https://doi.org/10.1158/0008-5472.CAN-09-2111
19	Hwang WL, Jiang JK, Yang SH, Huang TS, Lan HY, Teng HW, Yang CY, Tsai YP, Lin CH, Wang HW (2014) MicroRNA-146a directs the symmetric division of Snail-dominant colorectal cancer stem cells. Nat Cell Biol16: 268-280 https://doi.org/10.1038/ncb2910
20	Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D (2011) Global cancer statistics. CA Cancer J Clin61: 69-90 https://doi.org/10.3322/caac.20107
21	Jiang WG, Raz A, Douglas-Jones A, Mansel RE (2006) Expression of autocrine motility factor (AMF) and its receptor, AMFR, in human breast cancer. J Histochem Cytochem54: 231-241 https://doi.org/10.1369/jhc.5A6785.2005
22	Kanbe K, Chigira M, Watanabe H (1994) Effects of protein kinase inhibitors on the cell motility stimulated by autocrine motility factor. Biochim Biophys Acta1222: 395-399 https://doi.org/10.1016/0167-4889(94)90046-9
23	Kawanishi K, Doki Y, Shiozaki H, Yano M, Inoue M, Fukuchi N, Utsunomiya T, Watanabe H, Monden M (2000) Correlation between loss of E-cadherin expression and overexpression of autocrine motility factor receptor in association with progression of human gastric cancers. Am J Clin Pathol113: 266-274 https://doi.org/10.1309/JH4Q-25Q5-0TRV-W99U
24	Kho DH, Nangia-Makker P, Balan V, Hogan V, Tait L, Wang Y, Raz A (2013) Autocrine motility factor promotes HER2 cleavage and signaling in breast cancer cells. Cancer Res73: 1411-1419 https://doi.org/10.1158/0008-5472.CAN-12-2149
25	Krishnan K, Steptoe AL, Martin HC, Pattabiraman DR, Nones K, Waddell N, Mariasegaram M, Simpson PT, Lakhani SR, Vlassov A (2013) miR-139-5p is a regulator of metastatic pathways in breast cancer. RNA19: 1767-1780 https://doi.org/10.1261/rna.042143.113
26	Li Y, VandenBoom TG2nd, Kong D, Wang Z, Ali S, Philip PA, Sarkar FH (2009) Up-regulation of miR-200 and let-7 by natural agents leads to the reversal of epithelial-to-mesenchymal transition in gemcitabine-resistant pancreatic cancer cells. Cancer Res 69: 6704-6712 https://doi.org/10.1158/0008-5472.CAN-09-1298
27	Li RY, Chen LC, Zhang HY, Du WZ, Feng Y, Wang HB, Wen JQ, Liu X, Li XF, Sun Y (2013) MiR-139 inhibits Mcl-1 expression and potentiates TMZ-induced apoptosis in glioma. CNS Neurosci Ther19: 477-483 https://doi.org/10.1111/cns.12089
28	Liu R, Yang M, Meng Y, Liao J, Sheng J, Pu Y, Yin L, Kim SJ (2013) Tumor-suppressive function of miR-139-5p in esophageal squamous cell carcinoma. PLoS One8: e77068 https://doi.org/10.1371/journal.pone.0077068
29	Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C (T)) Method. Methods25: 402-408 https://doi.org/10.1006/meth.2001.1262
30	Manikandan J, Aarthi JJ, Kumar SD, Pushparaj PN (2008) Oncomirs: the potential role of non-coding microRNAs in understanding cancer. Bioinformation2: 330-334 https://doi.org/10.6026/97320630002330
31	Miele L, Golde T, Osborne B (2006) Notch signaling in cancer. Curr Mol Med6: 905-918 https://doi.org/10.2174/156652406779010830
32	Mo YY, Tang H, Miele L (2013) Notch-associated microRNAs in cancer. Curr Drug Targets14: 1157-1166 https://doi.org/10.2174/13894501113149990188
33	Nakamori S, Watanabe H, Kameyama M, Imaoka S, Furukawa H, Ishikawa O, Sasaki Y, Kabuto T, Raz A (1994) Expression of autocrine motility factor receptor in colorectal cancer as a predictor for disease recurrence. Cancer74: 1855-1862 https://doi.org/10.1002/1097-0142(19941001)74:7<1855::AID-CNCR2820740705>3.0.CO;2-1
34	Nicoloso MS, Spizzo R, Shimizu M, Rossi S, Calin GA (2009) MicroRNAs-the micro steering wheel of tumour metastases. Nat Rev Cancer9: 293-302 https://doi.org/10.1038/nrc2619
35	Reedijk M, Odorcic S, Zhang H, Chetty R, Tennert C, Dickson BC, Lockwood G, Gallinger S, Egan SE (2008) Activation of Notch signaling in human colon adenocarcinoma. Int J Oncol33: 1223-1229
36	Shen K, Liang Q, Xu K, Cui D, Jiang L, Yin P, Lu Y, Li Q, Liu J (2012) MiR-139 inhibits invasion and metastasis of colorectal cancer by targeting the type I insulin-like growth factor receptor. Biochem Pharmacol84: 320-330 https://doi.org/10.1016/j.bcp.2012.04.017
37	Skrtic A, Korac P, Kristo DR, Ajdukovic Stojisavljevic R, Ivankovic D, Dominis M (2010) Immunohistochemical analysis of NOTCH1 and JAGGED1 expression in multiple myeloma and monoclonal gammopathy of undetermined significance. Hum Pathol41: 1702-1710 https://doi.org/10.1016/j.humpath.2010.05.002
38	Sureban SM, May R, Mondalek FG, Qu D, Ponnurangam S, Pantazis P, Anant S, Ramanujam RP, Houchen CW (2011) Nanoparticle-based delivery of siDCAMKL-1 increases microRNA-144 and inhibits colorectal cancer tumor growth via a Notch-1 dependent mechanism. J Nanobiotechnol9: 40 https://doi.org/10.1186/1477-3155-9-40
39	Taniguchi K, Yonemura Y, Nojima N, Hirono Y, Fushida S, Fujimura T, Miwa K, Endo Y, Yamamoto H, Watanabe H (1998) The relation between the growth patterns of gastric carcinoma and the expression of hepatocyte growth factor receptor (c-met), autocrine motility factor receptor, and urokinase-type plasminogen activator receptor. Cancer82: 2112-2122 https://doi.org/10.1002/(SICI)1097-0142(19980601)82:11<2112::AID-CNCR5>3.0.CO;2-X
40	Tsai YC, Mendoza A, Mariano JM, Zhou M, Kostova Z, Chen B, Veenstra T, Hewitt SM, Helman LJ, Khanna C (2007) The ubiquitin ligase gp78 promotes sarcoma metastasis by targeting KAI1 for degradation. Nat Med13: 1504-1509 https://doi.org/10.1038/nm1686
41	Wang L, Hou G, Xue L, Li J, Wei P, Xu P (2010) Autocrine motility factor receptor signaling pathway promotes cell invasion via activation of ROCK-2 in esophageal squamous cell cancer cells. Cancer Invest28: 993-1003 https://doi.org/10.3109/07357907.2010.483503
42	Wang Q, Huang Z, Guo W, Ni S, Xiao X, Wang L, Huang D, Tan C, Xu Q, Zha R (2014) MicroRNA-202-3p Inhibits Cell Proliferation by Targeting ADP-Ribosylation Factor-like 5A in Human Colorectal Carcinoma. Clin Cancer Res20: 1146-1157 https://doi.org/10.1158/1078-0432.CCR-13-1023
43	Wong CC, Wong CM, Tung EK, Au SL, Lee JM, Poon RT, Man K, Ng IO (2011) The microRNA miR-139 suppresses metastasis and progression of hepatocellular carcinoma by down-regulating Rhokinase 2. Gastroenterology140: 322-331 https://doi.org/10.1053/j.gastro.2010.10.006
44	Yanagawa T, Funasaka T, Tsutsumi S, Watanabe H, Raz A (2004) Novel roles of the autocrine motility factor/phosphoglucose isomerase in tumor malignancy. Endocr Relat Cancer11: 749-759 https://doi.org/10.1677/erc.1.00811
45	Zhang L, Dong Y, Zhu N, Tsoi H, Zhao Z, Wu CW, Wang K, Zheng S, Ng SS, Chan FK (2014) microRNA-139-5p exerts tumor suppressor function by targeting NOTCH1 in colorectal cancer. Mol Cancer13: 124 https://doi.org/10.1186/1476-4598-13-124

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