MicroRNA-100 promotes the autophagy of hepatocellular carcinoma cells by inhibiting the expression of mTOR and IGF-1R

Oncotarget

Volumn 5, Issue 15, 2014, Pages 6218-6228

  Ge, Yi Yuan ^a   Shi, Qing ^a   Zheng, Zhi Yuan ^a   Gong, Jiao ^a   Zeng, Chunxian ^a   Yang, Jine ^a   Zhuang, Shi Mei ^a  

^a SUN YAT SEN UNIVERSITY   (China)

Author keywords

Autophagy; Hepatocellular carcinoma; IGF 1R; MiR 100; mTOR

Indexed keywords

BECLIN 1; CHLOROQUINE; MAMMALIAN TARGET OF RAPAMYCIN; MICRORNA 100; PROTEIN P62; SOMATOMEDIN C RECEPTOR; MICRORNA; MIRN100 MICRORNA, HUMAN; MTOR PROTEIN, HUMAN; TARGET OF RAPAMYCIN KINASE;

3' UNTRANSLATED REGION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTOPHAGY; CANCER CELL LINE; CARCINOMA CELL; DOWN REGULATION; GENETIC TRANSFECTION; HEK293 CELL LINE; HEPG2 CELL LINE; HUMAN; HUMAN CELL; IN VIVO STUDY; LIVER CELL CARCINOMA; MALE; MITOCHONDRIAL MEMBRANE POTENTIAL; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; NUDE MOUSE; PROTEIN EXPRESSION; RNA BINDING; TRANSMISSION ELECTRON MICROSCOPY; TUMOR XENOGRAFT; UPREGULATION; WESTERN BLOTTING; ANIMAL; ANTAGONISTS AND INHIBITORS; BAGG ALBINO MOUSE; BIOSYNTHESIS; GENETICS; LIVER TUMOR; METABOLISM; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE; XENOGRAFT;

ANIMALS; APOPTOSIS; AUTOPHAGY; CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; HEK293 CELLS; HEP G2 CELLS; HETEROGRAFTS; HUMANS; LIVER NEOPLASMS; MALE; MICE; MICE, INBRED BALB C; MICE, NUDE; MICRORNAS; RECEPTOR, IGF TYPE 1; TOR SERINE-THREONINE KINASES; TRANSFECTION;

EID: 84906267952     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.2189     Document Type: Article

References (40)

1. Rubinsztein DC, Codogno P and Levine B. Autophagy modulation as a potential therapeutic target for diverse diseases. Nat Rev Drug Discov. 2013; 11(9):709-730.
2. Yang Z and Klionsky DJ. Eaten alive: a history of macroautophagy. Nat Cell Biol. 2010; 12(9):814-822.
3. Rautou PE, Mansouri A, Lebrec D, Durand F, Valla D and Moreau R. Autophagy in liver diseases. J Hepatol. 2010; 53(6):1123-1134.
4. Ding ZB, Shi YH, Zhou J, Qiu SJ, Xu Y, Dai Z, Shi GM, Wang XY, Ke AW, Wu B and Fan J. Association of autophagy defect with a malignant phenotype and poor prognosis of hepatocellular carcinoma. Cancer Res. 2008; 68(22):9167-9175.
5. Inui M, Martello G and Piccolo S. MicroRNA control of signal transduction. Nat Rev Mol Cell Biol. 2010; 11(4):252-263.
6. Zhai H, Fesler A and Ju J. MicroRNA: a third dimension in autophagy. Cell Cycle. 2013; 12(2):246-250.
7. Zhu H, Wu H, Liu X, Li B, Chen Y, Ren X, Liu CG and Yang JM. Regulation of autophagy by a beclin 1-targeted microRNA, miR-30a, in cancer cells. Autophagy. 2009; 5(6):816-823.
8. Frankel LB, Wen J, Lees M, Hoyer-Hansen M, Farkas T, Krogh A, Jaattela M and Lund AH. microRNA-101 is a potent inhibitor of autophagy. The EMBO Journal. 2011; 30(22):4628-4641.
9. Zhai H, Song B, Xu X, Zhu W and Ju J. Inhibition of autophagy and tumor growth in colon cancer by miR-502. Oncogene. 2013; 32(12):1570-1579.
10. Li X, Zhang Y, Zhang H, Liu X, Gong T, Li M, Sun L, Ji G, Shi Y, Han Z, Han S, Nie Y, Chen X, Zhao Q, Ding J, Wu K, et al. miRNA-223 promotes gastric cancer invasion and metastasis by targeting tumor suppressor EPB41L3. Mol Cancer Res. 2011; 9(7):824-833.
11. Zhang H, Luo XQ, Zhang P, Huang LB, Zheng YS, Wu J, Zhou H, Qu LH, Xu L and Chen YQ. MicroRNA patterns associated with clinical prognostic parameters and CNS relapse prediction in pediatric acute leukemia. PloS one. 2009; 4(11):e7826.
12. Su H, Yang JR, Xu T, Huang J, Xu L, Yuan Y and Zhuang SM. MicroRNA-101, down-regulated in hepatocellular carcinoma, promotes apoptosis and suppresses tumorigenicity. Cancer Res. 2009; 69(3):1135-1142.
13. Petrelli A, Perra A, Schernhuber K, Cargnelutti M, Salvi A, Migliore C, Ghiso E, Benetti A, Barlati S, Ledda-Columbano GM, Portolani N, De Petro G, Columbano A and Giordano S. Sequential analysis of multistage hepatocarcinogenesis reveals that miR-100 and PLK1 dysregulation is an early event maintained along tumor progression. Oncogene. 2012; 31(42):4517-4526.
14. Gebeshuber CA and Martinez J. miR-100 suppresses IGF2 and inhibits breast tumorigenesis by interfering with proliferation and survival signaling. Oncogene. 2013; 32(27):3306-3310.
15. Xu C, Zeng Q, Xu W, Jiao L, Chen Y, Zhang Z, Wu C, Jin T, Pan A, Wei R, Yang B and Sun Y. miRNA-100 inhibits human bladder urothelial carcinogenesis by directly targeting mTOR. Mol Cancer Ther. 2013; 12(2):207-219.
16. Liu J, Lu KH, Liu ZL, Sun M, De W and Wang ZX. MicroRNA-100 is a potential molecular marker of nonsmall cell lung cancer and functions as a tumor suppressor by targeting polo-like kinase 1. BMC Cancer. 2012; 12:519.
17. Li XJ, Luo XQ, Han BW, Duan FT, Wei PP and Chen YQ. MicroRNA-100/99a, deregulated in acute lymphoblastic leukaemia, suppress proliferation and promote apoptosis by regulating the FKBP51 and IGF1R/mTOR signalling pathways. Br J Cancer. 2013; 109(8):2189-2198.
18. Zheng YS, Zhang H, Zhang XJ, Feng DD, Luo XQ, Zeng CW, Lin KY, Zhou H, Qu LH, Zhang P and Chen YQ. MiR-100 regulates cell differentiation and survival by targeting RBSP3, a phosphatase-like tumor suppressor in acute myeloid leukemia. Oncogene. 2012; 31(1):80-92.
19. Mizushima N, Yoshimori T and Levine B. Methods in mammalian autophagy research. Cell. 2010; 140(3):313-326.
20. Scarlatti F, Maffei R, Beau I, Codogno P and Ghidoni R. Role of non-canonical Beclin 1-independent autophagy in cell death induced by resveratrol in human breast cancer cells. Cell Death Differ. 2008; 15(8):1318-1329.
21. Ravikumar B, Sarkar S, Davies JE, Futter M, Garcia-Arencibia M, Green-Thompson ZW, Jimenez-Sanchez M, Korolchuk VI, Lichtenberg M, Luo S, Massey DC, Menzies FM, Moreau K, Narayanan U, Renna M, Siddiqi FH, et al. Regulation of mammalian autophagy in physiology and pathophysiology. Physiol Rev. 2010; 90(4):1383-1435.
22. Doghman M, El Wakil A, Cardinaud B, Thomas E, Wang J, Zhao W, Peralta-Del Valle MH, Figueiredo BC, Zambetti GP and Lalli E. Regulation of insulin-like growth factormammalian target of rapamycin signaling by microRNA in childhood adrenocortical tumors. Cancer Res. 2010; 70(11):4666-4675.
23. Neufeld TP. TOR-dependent control of autophagy: biting the hand that feeds. Curr Opin Cell Biol. 2010; 22(2):157-168.
24. Aita VM, Liang XH, Murty VV, Pincus DL, Yu W, Cayanis E, Kalachikov S, Gilliam TC and Levine B. Cloning and genomic organization of beclin 1, a candidate tumor suppressor gene on chromosome 17q21. Genomics. 1999; 59(1):59-65.
25. Kang MR, Kim MS, Oh JE, Kim YR, Song SY, Kim SS, Ahn CH, Yoo NJ and Lee SH. Frameshift mutations of autophagy-related genes ATG2B, ATG5, ATG9B and ATG12 in gastric and colorectal cancers with microsatellite instability. J Pathol. 2009; 217(5):702-706.
26. Kim MS, Jeong EG, Ahn CH, Kim SS, Lee SH and Yoo NJ. Frameshift mutation of UVRAG, an autophagy-related gene, in gastric carcinomas with microsatellite instability. Hum Pathol. 2008; 39(7):1059-1063.
27. Fujii S, Mitsunaga S, Yamazaki M, Hasebe T, Ishii G, Kojima M, Kinoshita T, Ueno T, Esumi H and Ochiai A. Autophagy is activated in pancreatic cancer cells and correlates with poor patient outcome. Cancer Sci. 2008; 99(9):1813-1819.
28. Chang CP, Yang MC, Liu HS, Lin YS and Lei HY. Concanavalin A induces autophagy in hepatoma cells and has a therapeutic effect in a murine in situ hepatoma model. Hepatology. 2007; 45(2):286-296.
29. Gao M, Yeh PY, Lu YS, Hsu CH, Chen KF, Lee WC, Feng WC, Chen CS, Kuo ML and Cheng AL. OSU-03012, a novel celecoxib derivative, induces reactive oxygen speciesrelated autophagy in hepatocellular carcinoma. Cancer Res. 2008; 68(22):9348-9357.
30. Song J, Qu Z, Guo X, Zhao Q, Zhao X, Gao L, Sun K, Shen F, Wu M and Wei L. Hypoxia-induced autophagy contributes to the chemoresistance of hepatocellular carcinoma cells. Autophagy. 2009; 5(8):1131-1144.
31. Francipane MG and Lagasse E. mTOR pathway in colorectal cancer: an update. Oncotarget. 2014; 5(1):49-66.
32. Llovet JM and Bruix J. Molecular targeted therapies in hepatocellular carcinoma. Hepatology. 2008; 48(4):1312-1327.
33. Ulanet DB, Ludwig DL, Kahn CR and Hanahan D. Insulin receptor functionally enhances multistage tumor progression and conveys intrinsic resistance to IGF-1R targeted therapy. Proc Natl Acad Sci U S A. 2010; 107(24):10791-10798.
34. Iglesias-Bartolome R and Gutkind SJ. Exploiting the mTOR paradox for disease prevention. Oncotarget. 2012; 3(10):1061-1063.
35. Tovar V, Alsinet C, Villanueva A, Hoshida Y, Chiang DY, Sole M, Thung S, Moyano S, Toffanin S, Minguez B, Cabellos L, Peix J, Schwartz M, Mazzaferro V, Bruix J and Llovet JM. IGF activation in a molecular subclass of hepatocellular carcinoma and pre-clinical efficacy of IGF-1R blockage. J Hepatol. 2010; 52(4):550-559.
36. Pirrotta MT, Bernardeschi P and Fiorentini G. Targetedtherapy in advanced renal cell carcinoma. Curr Med Chem. 2011; 18(11):1651-1657.
37. Treiber G. mTOR inhibitors for hepatocellular cancer: a forward-moving target. Expert Rev Anticancer Ther. 2009; 9(2):247-261.
38. O'Reilly KE, Rojo F, She QB, Solit D, Mills GB, Smith D, Lane H, Hofmann F, Hicklin DJ, Ludwig DL, Baselga J and Rosen N. mTOR inhibition induces upstream receptor tyrosine kinase signaling and activates Akt. Cancer Res. 2006; 66(3):1500-1508.
39. Quek R, Wang Q, Morgan JA, Shapiro GI, Butrynski JE, Ramaiya N, Huftalen T, Jederlinic N, Manola J, Wagner AJ, Demetri GD and George S. Combination mTOR and IGF-1R inhibition: phase I trial of everolimus and figitumumab in patients with advanced sarcomas and other solid tumors. Clin Cancer Res. 2011; 17(4):871-879.
40. Xiong Y, Fang JH, Yun JP, Yang J, Zhang Y, Jia WH and Zhuang SM. Effects of microRNA-29 on apoptosis, tumorigenicity, and prognosis of hepatocellular carcinoma. Hepatology. 2009; 51(3):836-845.