Onco-miR-24 regulates cell growth and apoptosis by targeting BCL2L11 in gastric cancer
Received date: 30 Sep 2015
Accepted date: 19 Nov 2015
Published date: 13 Mar 2016
Copyright
Gastric cancer is one of the most common malignancies worldwide; however, the molecular mechanism in tumorigenesis still needs exploration. BCL2L11 belongs to the BCL-2 family, and acts as a central regulator of the intrinsic apoptotic cascade and mediates cell apoptosis.Although miRNAs have been reported to be involved in each stage of cancer development, the role of miR-24 in GC has not been reported yet. In the present study, miR-24 was found to be up-regulated while the expression of BCL2L11 was inhibited in tumor tissues of GC. Studies from both in vitro and in vivo shown that miR-24 regulates BCL2L11 expression by directly binding with 3′UTR of mRNA, thus promoting cell growth, migration while inhibiting cell apoptosis. Therefore, miR-24 is a novel onco-miRNA that can be potential drug targets for future clinical use.
Key words: gastric cancer; BCL2L11; miR-24; tumorigenesis; cell apoptosis; proliferation; migration
Haiyang Zhang , Jingjing Duan , Yanjun Qu , Ting Deng , Rui Liu , Le Zhang , Ming Bai , Jialu Li , Tao Ning , Shaohua Ge , Xia Wang , Zhenzhen Wang , Qian Fan , Hongli Li , Guoguang Ying , Dingzhi Huang , Yi Ba . Onco-miR-24 regulates cell growth and apoptosis by targeting BCL2L11 in gastric cancer[J]. Protein & Cell, 2016 , 7(2) : 141 -151 . DOI: 10.1007/s13238-015-0234-5
1 |
Ambros V (2004) The functions of animal microRNAs. Nature 431:350–355
|
2 |
Amit D, Tamir S, Birman T, Gofrit ON, Hochberg A (2011) Development of targeted therapy for bladder cancer mediated by a double promoter plasmid expressing diphtheria toxin under the control of IGF2-P3 and IGF2-P4 regulatory sequences. Int J Clin Exp Med 4:91–102
|
3 |
Andrews WJ, Brown ED, Dellett M, Hogg RE, Simpson DA (2015) Rapid quantification of microRNAs in plasma using a fast real-time PCR system. Biotechniques 58:244–252
|
4 |
Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281–297
|
5 |
Chen C, Ridzon DA, Broomer AJ, Zhou Z, Lee DH, Nguyen JT, Barbisin M, Xu NL, Mahuvakar VR, Andersen MR et al (2005) Real-time quantification of microRNAs by stem-loop RT-PCR. Nucleic Acids Res 33:e179
|
6 |
Concannon CG, Tuffy LP, Weisova P, Bonner HP, Davila D, Bonner C, Devocelle MC, Strasser A, Ward MW, Prehn JH (2010) AMP kinase-mediated activation of the BH3-only protein Bim couples energy depletion to stress-induced apoptosis. JCell Biol 189:83–94
|
7 |
Dai Y, Grant S (2015) BCL2L11/Bim as a dual-agent regulating autophagy and apoptosis in drug resistance. Autophagy 11:416–418
|
8 |
Frank DO, Dengjel J, Wilfling F, Kozjak-Pavlovic V, Hacker G, Weber A (2015) The pro-apoptotic BH3-only protein Bim interacts with components of the translocase of the outer mitochondrial membrane (TOM). PLoS One 10:e0123341
|
9 |
Fujita T(2009) Gastric cancer. Lancet, 374:1593–1594; author reply 1594–1595
|
10 |
Ge Y, Zhao K, Qi Y, Min X, Shi Z, Qi X, Shan Y, Cui L, Zhou M, Wang Y et al (2013) Serum microRNA expression profile as a biomarker for the diagnosis of pertussis. Mol Biol Rep 40:1325–1332
|
11 |
Hagenbuchner J, Kuznetsov A, Hermann M, Hausott B, Obexer P, Ausserlechner MJ (2012) FOXO3-induced reactive oxygen species are regulated by BCL2L11 (Bim) and SESN3. J Cell Sci 125:1191–1203
|
12 |
Hartgrink HH, Jansen EP, van Grieken NC, van deVelde CJ (2009) Gastric cancer. Lancet 374:477–490
|
13 |
Hohenberger P, Gretschel S(2003) Gastric cancer. Lancet 362:305–315
|
14 |
Huang C, Li J, Hong K, Xia Z, Xu Y, Cheng X (2015) BH3-only protein Bim is upregulated and mediates the apoptosis of cardiomyocytes under glucose and oxygen-deprivation conditions. Cell Biol Int 39:318–325
|
15 |
Kilbride SM, Farrelly AM, Bonner C, Ward MW, Nyhan KC, Concannon CG, Wollheim CB, Byrne MM, Prehn JH (2010) AMP-activated protein kinase mediates apoptosis in response to bioenergetic stress through activation of the pro-apoptotic Bcl-2 homology domain-3-only protein BMF. J Biol Chem 285:36199–36206
|
16 |
Li J, Zhang Y, Liu Y, Dai X, Li W, Cai X, Yin Y, Wang Q, Xue Y, Wang C et al (2013) Microvesicle-mediated transfer of microRNA-150 from monocytes to endothelial cells promotes angiogenesis. J Biol Chem 288:23586–23596
|
17 |
Li Y, Peng T, Li L, Wang X, Duan R, Gao H, Guan W, Lu J, Teng J, Jia Y (2014) MicroRNA-9 regulates neural apoptosis in methylmalonic acidemia via targeting BCL2L11. Int J Dev Neurosci 36:19–24
|
18 |
Li J, Zhang Y, Li D, Liu Y, Chu D, Jiang X, Hou D, Zen K, Zhang CY (2015) Small non-coding RNAs transfer through mammalian placenta and directly regulate fetal gene expression. Protein Cell 6:391–396
|
19 |
Lim LP, Lau NC, Garrett-Engele P, Grimson A, Schelter JM, Castle J, Bartel DP, Linsley PS, Johnson JM (2005) Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 433:769–773
|
20 |
Lin SC, Liu CJ, Lin JA, Chiang WF, Hung PS, Chang KW (2010) miR-24 up-regulation in oral carcinoma: positive association from clinical and in vitro analysis. Oral Oncol 46:204–208
|
21 |
Lin XJ, Chong Y, Guo ZW, Xie C, Yang XJ, Zhang Q, Li SP, Xiong Y, Yuan Y, Min J et al (2015)A serum microRNA classifier for early detection of hepatocellular carcinoma: a multicentre, retrospective, longitudinal biomarker identification study with a nested case-control study. Lancet Oncol 16:804–815
|
22 |
Liu R, Zhang C, Hu Z, Li G, Wang C, Yang C, Huang D, Chen X, Zhang H, Zhuang R et al (2011) A five-microRNA signature identified from genome-wide serum microRNA expression profiling serves as a fingerprint for gastric cancer diagnosis. Eur J Cancer 47:784–791
|
23 |
Liu R, Chen X, Du Y, Yao W, Shen L, Wang C, Hu Z, Zhuang R, Ning G, Zhang C et al(2012)Serum microRNA expressionprofile asa biomarker in the diagnosis and prognosis of pancreatic cancer. Clin Chem 58:610–618
|
24 |
Liu YC, Zhao LM, Li DM, Yin Y, Zhang CY, Li J, Zhang YJ (2013) Microvesicle-delivery miR-150 promotes tumorigenesis by up-regulating VEGF, and the neutralization of miR-150 attenuate tumor development. Protein Cell 4:932–941
|
25 |
Luo S, Rubinsztein DC (2013) BCL2L11/BIM: a novel molecular link between autophagy and apoptosis. Autophagy 9:104–105
|
26 |
Luo Y, Wang C, Chen X, Zhong T, Cai X, Chen S, Shi Y, Hu J, Guan X, Xia Z et al (2013) Increased serum and urinary microRNAs in childrenwithidiopathicnephroticsyndrome. Clin Chem59:658–666
|
27 |
Mansha M, Hussain A, Kofler A, Grubbauer C, Goetsch K, Ploner C, Kofler R (2013) “Bam,” a novel glucocorticoid-induced BH3-only transcript from the BCL2L11/Bim locus, does not appear to be translated. LeukLymphoma 54:353–358
|
28 |
Manyam BV, Mallick IH, Abdel-Wahab MM, Reddy CA, Remzi FH, Kalady MF, Lavery I, Koyfman SA (2015) The impact of preoperative radiation therapy on locoregional recurrence in patients with stage IV rectal cancer treated with definitive surgical resection and contemporary chemotherapy. J Gastrointest Surg 19:1676–1683
|
29 |
McBride SM, Raut CP, Lapidus M, Devlin PM, Marcus KJ, Bertagnolli M, George S, Baldini EH (2013) Locoregional recurrence after preoperative radiation therapy for retroperitoneal sarcoma: adverse impact of multifocaldisease and potential implications of dose escalation. Ann Surg Oncol 20:2140–2147
|
30 |
Naito Y,Oue N, Pham TT,Yamamoto M, Fujihara M, Ishida T, Mukai S, Sentani K, Sakamoto N, Hida E et al (2015) Characteristic miR-24 expression in gastric cancers among atomic bomb survivors. Pathobiology 82:68–75
|
31 |
Organista-Nava J, Gomez-Gomez Y, Illades-Aguiar B, Del Carmen Alarcon-Romero L, Saavedra-Herrera MV, Rivera-Ramirez AB, Garzon-Barrientos VH, Leyva-Vazquez MA (2015) High miR-24 expression is associated with risk of relapse and poor survival in acute leukemia. Oncol Rep 33:1639–1649
|
32 |
Qin W, Shi Y, Zhao B, Yao C, Jin L, Ma J, Jin Y (2010) miR-24 regulates apoptosis by targeting the open reading frame (ORF) region ofFAF1 in cancer cells. PLoS One 5:e9429
|
33 |
Tchernitsa O, Kasajima A, Schafer R, Kuban RJ, Ungethum U, Gyorffy B, Neumann U, Simon E, Weichert W, Ebert MP et al (2010) Systematic evaluation of the miRNA-ome and its downstream effects on mRNA expression identifies gastric cancer progression. J Pathol 222:310–319
|
34 |
Tsukamoto Y, Nakada C, Noguchi T, Tanigawa M, Nguyen LT, Uchida T, Hijiya N, Matsuura K, Fujioka T, Seto M et al (2010) MicroRNA-375 is downregulated in gastric carcinomas and regulates cell survival by targeting PDK1 and 14-3-3zeta. Cancer Res 70:2339–2349
|
35 |
Volinia S, Calin GA, Liu CG, Ambs S, Cimmino A, Petrocca F, Visone R, Iorio M, Roldo C, Ferracin M et al (2006) A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci USA 103:2257–2261
|
36 |
Wang C, Hu J, Lu M, Gu H, Zhou X, Chen X, Zen K, Zhang CY, Zhang T, Ge J et al (2015) A panel of five serum miRNAs as a potential diagnostic tool for early-stage renal cell carcinoma. Sci Rep 5:7610
|
37 |
Xiong HQ, Gunderson LL,Yao J, Ajani JA(2003) Chemoradiationfor resectable gastric cancer. Lancet Oncol 4:498–505
|
38 |
Yin Y,Cai X, Chen X, Liang HW, Zhang YJ, Li J, Wang ZY, Chen XL, Zhang W, Yokoyama S et al (2014) Tumor-secreted miR-214 induces regulatoryTcells:a major link between immune evasion and tumor growth. Cell Resh 24:1164–1180
|
39 |
Zhang Y, Liu D, Chen X, Li J, Li L, Bian Z, Sun F, Lu J, Yin Y, Cai X et al (2010) Secreted monocytic miR-150 enhances targeted endothelial cell migration. Mol Cell 39:133–144
|
40 |
Zhang YQ, Li LM,Yu JX, Zhu DH, Zhang YJ, Li XH, Gu HW, Zhang CY, Zen K(2014) Microvesicle-mediated delivery of transforming growth factor beta1siRNA for the suppressionof tumor growthin mice. Biomaterials 35:4390–4400
|
41 |
Zhang H,Yang H, Zhang C, Jing Y, Wang C, Liu C, Zhang R, Wang J, Zhang J, Zen K et al (2015) Investigation of microRNA expressionin human serum during the aging process. JGerontol A Biol Sci Med Sci 70:102–109
|
42 |
Zhao G, Liu L, Zhao T, Jin S, Jiang S, Cao S, Han J, Xin Y, Dong Q, Liu X et al (2015) Upregulation of miR-24 promotes cell proliferation by targeting NAIF1 in non-small cell lung cancer. Tumour Biol 36:3693–3701
|
43 |
Zhu D, Pan C, Li L, Bian Z, Lv Z, Shi L, Zhang J, Li D, Gu H, Zhang CY et al (2013) MicroRNA-17/20a/106a modulate macrophage inflammatory responses through targeting signal-regulatory protein alpha. J Allergy Clin Immunol 132(426–436):e428
|
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