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Published in: Cancer Cell International 1/2018

Open Access 01-12-2018 | Primary Research

Long non-coding RNA MIAT promotes growth and metastasis of colorectal cancer cells through regulation of miR-132/Derlin-1 pathway

Authors: Zhaoxia Liu, Hai Wang, Hongwei Cai, Ye Hong, Yan Li, Dongming Su, Zhining Fan

Published in: Cancer Cell International | Issue 1/2018

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Abstract

Objective

Recently, long non-coding RNA (lncRNA) MIAT has been demonstrated as an oncogenic gene in several types of cancer. However, the role and mechanism of MIAT in colorectal cancer (CRC) have not been investigated.

Methods

Real-time PCR was used to measure MIAT expression in CRC tissues and cells. Small interfering RNA specific for MIAT (si-MIAT) was used to down-regulate MIAT expression in CRC cells. The interaction of MIAT and miR-132 was measured by RNA pull-down assay. The effect of si-MIAT on CRC cells apoptosis and metastasis were measured by flow cytometry assay, invasion and migration assay, respectively.

Results

In present study, we found that MIAT was highly expressed in CRC tissues and cells. MIAT knockdown inhibited proliferation, migration and invasion and enhanced apoptosis of CRC cells. Further, we demonstrated that MIAT acted as a competing endogenous RNA for miR-132, antagonized its functions, and resulted in the de-repression of its target gene Derlin-1, which acted as an oncogene in promoting growth and metastasis of CRC cells. In LOVO and SW480 cells with si-MIAT, miR-132 inhibitor resulted in an increase of cell proliferation, migration and invasion and a decrease of cell apoptosis, which was partially abolished by transfection of Derlin-1 shRNA.

Conclusions

Our data indicated that highly expressed MIAT was an oncogenic lncRNA that promoted the growth and metastasis of CRC through miR-132/Derlin-1 axis.
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Literature
1.
go back to reference Tenesa A, Dunlop MG. New insights into the aetiology of colorectal cancer from genome-wide association studies. Nat Rev Genet. 2009;10(6):353–8.CrossRefPubMed Tenesa A, Dunlop MG. New insights into the aetiology of colorectal cancer from genome-wide association studies. Nat Rev Genet. 2009;10(6):353–8.CrossRefPubMed
2.
go back to reference Zhang P, Ji DB, Han HB, Shi YF, Du CZ, Gu J. Downregulation of miR-193a-5p correlates with lymph node metastasis and poor prognosis in colorectal cancer. World J Gastroenterol. 2014;20(34):12241–8.CrossRefPubMedPubMedCentral Zhang P, Ji DB, Han HB, Shi YF, Du CZ, Gu J. Downregulation of miR-193a-5p correlates with lymph node metastasis and poor prognosis in colorectal cancer. World J Gastroenterol. 2014;20(34):12241–8.CrossRefPubMedPubMedCentral
3.
go back to reference Kita Y, Yonemori K, Osako Y, Baba K, Mori S, Maemura K, Natsugoe S. Noncoding RNA and colorectal cancer: its epigenetic role. J Hum Genet. 2017;62(1):41–7.CrossRefPubMed Kita Y, Yonemori K, Osako Y, Baba K, Mori S, Maemura K, Natsugoe S. Noncoding RNA and colorectal cancer: its epigenetic role. J Hum Genet. 2017;62(1):41–7.CrossRefPubMed
4.
go back to reference Rokavec M, Horst D, Hermeking H. Cellular model of colon cancer progression reveals signatures of mRNAs, miRNA, lncRNAs, and epigenetic modifications associated with metastasis. Cancer Res. 2017;77(8):1854–67.CrossRefPubMed Rokavec M, Horst D, Hermeking H. Cellular model of colon cancer progression reveals signatures of mRNAs, miRNA, lncRNAs, and epigenetic modifications associated with metastasis. Cancer Res. 2017;77(8):1854–67.CrossRefPubMed
5.
go back to reference Qin J, Ke J, Xu J, Wang F, Zhou Y, Jiang Y, Wang Z. Downregulation of microRNA-132 by DNA hypermethylation is associated with cell invasion incolorectal cancer. Onco Targets Ther. 2015;8:3639–48.PubMedPubMedCentral Qin J, Ke J, Xu J, Wang F, Zhou Y, Jiang Y, Wang Z. Downregulation of microRNA-132 by DNA hypermethylation is associated with cell invasion incolorectal cancer. Onco Targets Ther. 2015;8:3639–48.PubMedPubMedCentral
6.
go back to reference Mokutani Y, Uemura M, Munakata K, Okuzaki D, Haraguchi N, Takahashi H, Nishimura J, Hata T, Murata K, Takemasa I, Mizushima T, Doki Y, Mori M, Yamamoto H. Down-regulation of microRNA-132 is associated with poor prognosis of colorectal cancer. Ann Surg Oncol. 2016;23(Suppl 5):599–608.CrossRefPubMedPubMedCentral Mokutani Y, Uemura M, Munakata K, Okuzaki D, Haraguchi N, Takahashi H, Nishimura J, Hata T, Murata K, Takemasa I, Mizushima T, Doki Y, Mori M, Yamamoto H. Down-regulation of microRNA-132 is associated with poor prognosis of colorectal cancer. Ann Surg Oncol. 2016;23(Suppl 5):599–608.CrossRefPubMedPubMedCentral
7.
go back to reference Zheng YB, Luo HP, Shi Q, Hao ZN, Ding Y, Wang QS, Li SB, Xiao GC, Tong SL. miR-132 inhibits colorectal cancer invasion and metastasis via directly targeting ZEB2. World J Gastroenterol. 2014;20(21):6515–22.CrossRefPubMedPubMedCentral Zheng YB, Luo HP, Shi Q, Hao ZN, Ding Y, Wang QS, Li SB, Xiao GC, Tong SL. miR-132 inhibits colorectal cancer invasion and metastasis via directly targeting ZEB2. World J Gastroenterol. 2014;20(21):6515–22.CrossRefPubMedPubMedCentral
8.
9.
go back to reference Liao J, He Q, Li M, Chen Y, Liu Y, Wang J. LncRNA MIAT: myocardial infarction associated and more. Gene. 2016;578(2):158–61.CrossRefPubMed Liao J, He Q, Li M, Chen Y, Liu Y, Wang J. LncRNA MIAT: myocardial infarction associated and more. Gene. 2016;578(2):158–61.CrossRefPubMed
10.
go back to reference Li DS, Ainiwaer JL, Sheyhiding I, Zhang Z, Zhang LW. Identification of key long non-coding RNAs as competing endogenous RNAs for miRNA-mRNA in lung adenocarcinoma. Eur Rev Med Pharmacol Sci. 2016;20(11):2285–95.PubMed Li DS, Ainiwaer JL, Sheyhiding I, Zhang Z, Zhang LW. Identification of key long non-coding RNAs as competing endogenous RNAs for miRNA-mRNA in lung adenocarcinoma. Eur Rev Med Pharmacol Sci. 2016;20(11):2285–95.PubMed
11.
go back to reference Thomson DW, Dinger ME. Endogenous microRNA sponges: evidence and controversy. Nat Rev Genet. 2016;17(5):272–83.CrossRefPubMed Thomson DW, Dinger ME. Endogenous microRNA sponges: evidence and controversy. Nat Rev Genet. 2016;17(5):272–83.CrossRefPubMed
12.
go back to reference Tan X, He X, Jiang Z, Wang X, Ma L, Liu L, Wang X, Fan Z, Su D. Derlin-1 is overexpressed in human colon cancer and promotes cancer cell proliferation. Mol Cell Biochem. 2015;408(1–2):205–13.CrossRefPubMed Tan X, He X, Jiang Z, Wang X, Ma L, Liu L, Wang X, Fan Z, Su D. Derlin-1 is overexpressed in human colon cancer and promotes cancer cell proliferation. Mol Cell Biochem. 2015;408(1–2):205–13.CrossRefPubMed
13.
go back to reference Malek E, Jagannathan S, Driscoll JJ. Correlation of long non-coding RNA expression with metastasis, drug resistance and clinical outcome in cancer. Oncotarget. 2014;5(18):8027–38.CrossRefPubMedPubMedCentral Malek E, Jagannathan S, Driscoll JJ. Correlation of long non-coding RNA expression with metastasis, drug resistance and clinical outcome in cancer. Oncotarget. 2014;5(18):8027–38.CrossRefPubMedPubMedCentral
15.
go back to reference Crea F, Venalainen E, Ci X, Cheng H, Pikor L, Parolia A, Xue H, Nur Saidy NR, Lin D, Lam W, Collins C, Wang Y. The role of epigenetics and long noncoding RNA MIAT in neuroendocrine prostate cancer. Epigenomics. 2016;8(5):721–31.CrossRefPubMed Crea F, Venalainen E, Ci X, Cheng H, Pikor L, Parolia A, Xue H, Nur Saidy NR, Lin D, Lam W, Collins C, Wang Y. The role of epigenetics and long noncoding RNA MIAT in neuroendocrine prostate cancer. Epigenomics. 2016;8(5):721–31.CrossRefPubMed
16.
go back to reference Sattari A, Siddiqui H, Moshiri F, Ngankeu A, Nakamura T, Kipps TJ, Croce CM. Upregulation of long noncoding RNA MIAT in aggressive form of chronic lymphocytic leukemias. Oncotarget. 2016;7(34):54174–82.CrossRefPubMedPubMedCentral Sattari A, Siddiqui H, Moshiri F, Ngankeu A, Nakamura T, Kipps TJ, Croce CM. Upregulation of long noncoding RNA MIAT in aggressive form of chronic lymphocytic leukemias. Oncotarget. 2016;7(34):54174–82.CrossRefPubMedPubMedCentral
17.
go back to reference Jia L, Xing J, Ding Y, Shen Y, Shi X, Ren W, Wan M, Guo J, Zheng S, Liu Y, Liang X, Su D. Hyperuricemia causes pancreatic β-cell death and dysfunction through NF-κB signaling pathway. PLoS ONE. 2013;8(10):e78284.CrossRefPubMedPubMedCentral Jia L, Xing J, Ding Y, Shen Y, Shi X, Ren W, Wan M, Guo J, Zheng S, Liu Y, Liang X, Su D. Hyperuricemia causes pancreatic β-cell death and dysfunction through NF-κB signaling pathway. PLoS ONE. 2013;8(10):e78284.CrossRefPubMedPubMedCentral
18.
go back to reference Ding Y, Xu Y, Shuai X, Shi X, Chen X, Huang W, Liu Y, Liang X, Zhang Z, Su D. Reg3α overexpression protects pancreatic beta-cells from cytokine-induced damage and improves islet transplant outcome. Mol Med. 2014;20(1):548–58. Ding Y, Xu Y, Shuai X, Shi X, Chen X, Huang W, Liu Y, Liang X, Zhang Z, Su D. Reg3α overexpression protects pancreatic beta-cells from cytokine-induced damage and improves islet transplant outcome. Mol Med. 2014;20(1):548–58.
19.
go back to reference Xu YM, Wang HJ, Chen F, Guo WH, Wang YY, Li HY, Tang JH, Ding Y, Shen YC, Li M, Xuan WY, Liu LH, Wang J, Wang XR, Gao ZJ, Liang XB, Su DM. HRD1 suppresses the growth and metastasis of breast cancer cells by promoting IGF-1R degradation. Oncotarget. 2015;6(40):42854–67.CrossRefPubMedPubMedCentral Xu YM, Wang HJ, Chen F, Guo WH, Wang YY, Li HY, Tang JH, Ding Y, Shen YC, Li M, Xuan WY, Liu LH, Wang J, Wang XR, Gao ZJ, Liang XB, Su DM. HRD1 suppresses the growth and metastasis of breast cancer cells by promoting IGF-1R degradation. Oncotarget. 2015;6(40):42854–67.CrossRefPubMedPubMedCentral
Metadata
Title
Long non-coding RNA MIAT promotes growth and metastasis of colorectal cancer cells through regulation of miR-132/Derlin-1 pathway
Authors
Zhaoxia Liu
Hai Wang
Hongwei Cai
Ye Hong
Yan Li
Dongming Su
Zhining Fan
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Cancer Cell International / Issue 1/2018
Electronic ISSN: 1475-2867
DOI
https://doi.org/10.1186/s12935-017-0477-8

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