miR-192, a prognostic indicator, targets the SLC39A6/SNAIL pathway to reduce tumor metastasis in human hepatocellular carcinoma

Oncotarget

Volumn 7, Issue 3, 2016, Pages 2672-2683

  Lian, Junwei ^a   Jing, Ying ^a   Dong, Qiongzhu ^b,c   Huan, Lin ^a   Chen, Di ^a   Bao, Chunyang ^d   Wang, Qifeng ^d   Zhao, Fangyu ^a   Li, Jinjun ^a   Yao, Ming ^a   Qin, Lunxiu ^b,c   Liang, Linhui ^b,d   He, Xianghuo ^a,b,d  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b FUDAN UNIVERSITY   (China)

^c FUDAN UNIVERSITY   (China)

^d FUDAN UNIVERSITY SHANGHAI CANCER CENTER   (China)

Author keywords

Hepatocellular carcinoma; Metastasis; MiR 192; Prognosis; SLC39A6

Indexed keywords

MICRORNA 192; SOLUTE CARRIER FAMILY 39 MEMBER 6 PROTEIN; TRANSCRIPTION FACTOR SNAIL; TUMOR PROTEIN; UNCLASSIFIED DRUG; UVOMORULIN; CATION TRANSPORT PROTEIN; MESSENGER RNA; MICRORNA; MIRN192 MICRORNA, HUMAN; SLC39A6 PROTEIN, HUMAN; SNAI1 PROTEIN, HUMAN; TUMOR MARKER;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER PROGNOSIS; CELL INVASION; CELL MIGRATION; CONTROLLED STUDY; DOWN REGULATION; FEMALE; GAIN OF FUNCTION MUTATION; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; HCC LM3 CELL LINE; HEPATOCELLULAR CARCINOMA CELL LINE; HUMAN; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; LIVER CELL CARCINOMA; LOSS OF FUNCTION MUTATION; MALE; METASTASIS; MHCC 97H CELL LINE; MHCC 97L CELL LINE; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PROTEIN EXPRESSION; TUMOR INVASION; ANIMAL; APOPTOSIS; BAGG ALBINO MOUSE; CANCER GRADING; CANCER STAGING; CARCINOMA, HEPATOCELLULAR; CELL PROLIFERATION; DRUG SCREENING; ENZYME IMMUNOASSAY; FOLLOW UP; GENETICS; LIVER NEOPLASMS; METABOLISM; MIDDLE AGED; NUDE MOUSE; PATHOLOGY; PROGNOSIS; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SECONDARY; SURVIVAL RATE; TUMOR CELL CULTURE; WESTERN BLOTTING;

ANIMALS; APOPTOSIS; BIOMARKERS, TUMOR; BLOTTING, WESTERN; CARCINOMA, HEPATOCELLULAR; CATION TRANSPORT PROTEINS; CELL PROLIFERATION; FEMALE; FOLLOW-UP STUDIES; HUMANS; IMMUNOENZYME TECHNIQUES; LIVER NEOPLASMS; MALE; MICE; MICE, INBRED BALB C; MICE, NUDE; MICRORNAS; MIDDLE AGED; NEOPLASM GRADING; NEOPLASM INVASIVENESS; NEOPLASM PROTEINS; NEOPLASM STAGING; PROGNOSIS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SNAIL FAMILY TRANSCRIPTION FACTORS; SURVIVAL RATE; TUMOR CELLS, CULTURED; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84962259452     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.6603     Document Type: Article

References (38)

1. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin. 2011; 61:69-90.
2. Forner A, Llovet JM, Bruix J. Hepatocellular carcinoma. Lancet. 2012; 379:1245-1255.
3. Hao K, Luk JM, Lee NP, Mao M, Zhang C, Ferguson MD, Lamb J, Dai H, Ng IO, Sham PC, Poon RT. Predicting prognosis in hepatocellular carcinoma after curative surgery with common clinicopathologic parameters. BMC Cancer. 2009; 9:389.
4. Mehlen P, Puisieux A. Metastasis: a question of life or death. Nat Rev Cancer. 2006; 6:449-458.
5. Nguyen DX, Massague J. Genetic determinants of cancer metastasis. Nat Rev Genet. 2007; 8:341-352.
6. Monteiro J, Fodde R. Cancer stemness and metastasis: therapeutic consequences and perspectives. Eur J Cancer. 2010; 46:1198-1203.
7. Fidler IJ. The pathogenesis of cancer metastasis: the 'seed and soil' hypothesis revisited. Nat Rev Cancer. 2003; 3:453-458.
8. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell. 2004; 116:281-297.
9. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell. 2009; 136:215-233.
10. Lewis BP, Burge CB, Bartel DP. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell. 2005; 120:15-20.
11. Garzon R, Calin GA, Croce CM. MicroRNAs in Cancer. Annu Rev Med. 2009; 60:167-179.
12. Calin GA, Ferracin M, Cimmino A, Di Leva G, Shimizu M, Wojcik SE, Iorio MV, Visone R, Sever NI, Fabbri M, Iuliano R, Palumbo T, Pichiorri F, et al. A MicroRNA signature associated with prognosis and progression in chronic lymphocytic leukemia. N Engl J Med. 2005; 353:1793-1801.
13. Calin GA, Liu CG, Sevignani C, Ferracin M, Felli N, Dumitru CD, Shimizu M, Cimmino A, Zupo S, Dono M, Dell'Aquila ML, Alder H, Rassenti L, et al. MicroRNA profiling reveals distinct signatures in B cell chronic lymphocytic leukemias. Proc Natl Acad Sci U S A. 2004; 101:11755-11760.
14. Calin GA, Croce CM. MicroRNA signatures in human cancers. Nat Rev Cancer. 2006; 6:857-866.
15. Li Y, Tian B, Yang J, Zhao L, Wu X, Ye SL, Liu YK, Tang ZY. Stepwise metastatic human hepatocellular carcinoma cell model system with multiple metastatic potentials established through consecutive in vivo selection and studies on metastatic characteristics. J Cancer Res Clin Oncol. 2004; 130:460-468.
16. Tang ZY, Ye SL, Liu YK, Qin LX, Sun HC, Ye QH, Wang L, Zhou J, Qiu SJ, Li Y, Ji XN, Liu H, Xia JL, et al. A decade's studies on metastasis of hepatocellular carcinoma. J Cancer Res Clin Oncol. 2004; 130:187-196.
17. Sussman D, Smith LM, Anderson ME, Duniho S, Hunter JH, Kostner H, Miyamoto JB, Nesterova A, Westendorf L, Van Epps HA, Whiting N, Benjamin DR. SGN-LIV1A: a novel antibody-drug conjugate targeting LIV-1 for the treatment of metastatic breast cancer. Mol Cancer Ther. 2014; 13:2991-3000.
18. Shen R, Xie F, Shen H, liu Q, Zheng T, Kou X, Wang D, Yang J. Negative correlation of LIV-1 and E-cadherin expression in hepatocellular carcinoma cells. PLoS One. 2013; 8:e56542.
19. Taylor KM, Hiscox S, Nicholson RI. Zinc transporter LIV-1: a link between cellular development and cancer progression. Trends Endocrinol Metab. 2004; 15:461-463.
20. Unno J, Satoh K, Hirota M, Kanno A, Hamada S, Ito H, Masamune A, Tsukamoto N, Motoi F, Egawa S, Unno M, Horii A, Shimosegawa T. LIV-1 enhances the aggressive phenotype through the induction of epithelial to mesenchymal transition in human pancreatic carcinoma cells. Int J Oncol. 2009; 35:813-821.
21. Hogstrand C, Kille P, Ackland ML, Hiscox S, Taylor KM. A mechanism for epithelial-mesenchymal transition and anoikis resistance in breast cancer triggered by zinc channel ZIP6 and STAT3 (signal transducer and activator of transcription 3). Biochem J. 2013; 455:229-237.
22. Lue HW, Yang X, Wang R, Qian W, Xu RZ, Lyles R, Osunkoya AO, Zhou BP, Vessella RL, Zayzafoon M, Liu ZR, Zhau HE, Chung LW. LIV-1 promotes prostate cancer epithelial-to-mesenchymal transition and metastasis through HB-EGF shedding and EGFR-mediated ERK signaling. PLoS One. 2011; 6:e27720.
23. Jia D, Jing Y, Zhang Z, Liu L, Ding J, Zhao F, Ge C, Wang Q, Chen T, Yao M, Li J, Gu J, He X. Amplification of MPZL1/PZR promotes tumor cell migration through Src-mediated phosphorylation of cortactin in hepatocellular carcinoma. Cell research. 2014; 24:204-217.
24. Feng J, Wang J, Chen M, Chen G, Wu Z, Ying L, Zhuo Q, Zhang J, Wang W. miR-200a suppresses cell growth and migration by targeting MACC1 and predicts prognosis in hepatocellular carcinoma. Oncol Rep. 2015; 33:713-720.
25. Pichler M, Ress AL, Winter E, Stiegelbauer V, Karbiener M, Schwarzenbacher D, Scheideler M, Ivan C, Jahn SW, Kiesslich T, Gerger A, Bauernhofer T, Calin GA, et al. MiR-200a regulates epithelial to mesenchymal transition-related gene expression and determines prognosis in colorectal cancer patients. Br J Cancer. 2014; 110:1614-1621.
26. Lu Y, Lu J, Li X, Zhu H, Fan X, Zhu S, Wang Y, Guo Q, Wang L, Huang Y, Zhu M, Wang Z. MiR-200a inhibits epithelial-mesenchymal transition of pancreatic cancer stem cell. BMC Cancer. 2014; 14:85.
27. Taylor KM, Morgan HE, Smart K, Zahari NM, Pumford S, Ellis IO, Robertson JF, Nicholson RI. The emerging role of the LIV-1 subfamily of zinc transporters in breast cancer. Mol Med. 2007; 13:396-406.
28. Shen R, Xie F, Shen H, Liu Q, Zheng T, Kou X, Wang D, Yang J. Negative correlation of LIV-1 and E-cadherin expression in hepatocellular carcinoma cells. PLOS One. 2013; 8:e56542.
29. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011; 144:646-674.
30. Li Y, Tang Y, Ye L, Liu B, Liu K, Chen J, Xue Q. Establishment of a hepatocellular carcinoma cell line with unique metastatic characteristics through in vivo selection and screening for metastasis-related genes through cDNA microarray. J Cancer Res Clin Oncol. 2003; 129:43-51.
31. Wei J, Zhang Y, Luo Y, Wang Z, Bi S, Song D, Dai Y, Wang T, Qiu L, Wen L, Yuan L, Yang JY. Aldose reductase regulates miR-200a-3p/141-3p to coordinate Keap1-Nrf2, Tgfbeta1/2, and Zeb1/2 signaling in renal mesangial cells and the renal cortex of diabetic mice. Free radical biology & medicine. 2014; 67:91-102.
32. Geng L, Chaudhuri A, Talmon G, Wisecarver JL, Are C, Brattain M, Wang J. MicroRNA-192 suppresses liver metastasis of colon cancer. Oncogene. 2014; 33:5332-5340.
33. Khella HW, Bakhet M, Allo G, Jewett MA, Girgis AH, Latif A, Girgis H, Von Both I, Bjarnason GA, Yousef GM. miR-192, miR-194 and miR-215: a convergent microRNA network suppressing tumor progression in renal cell carcinoma. Carcinogenesis. 2013; 34:2231-2239.
34. Feng S, Cong S, Zhang X, Bao X, Wang W, Li H, Wang Z, Wang G, Xu J, Du B, Qu D, Xiong W, Yin M, et al. MicroRNA-192 targeting retinoblastoma 1 inhibits cell proliferation and induces cell apoptosis in lung cancer cells. Nucleic acids research. 2011; 39:6669-6678.
35. Chen Q, Ge X, Zhang Y, Xia H, Yuan D, Tang Q, Chen L, Pang X, Leng W, Bi F. Plasma miR-122 and miR-192 as potential novel biomarkers for the early detection of distant metastasis of gastric cancer. Oncol Rep. 2014; 31:1863-1870.
36. Grattan BJ, Freake HC. Zinc and cancer: implications for LIV-1 in breast cancer. Nutrients. 2012; 4:648-675.
37. Wang Y, Shi J, Chai K, Ying X, Zhou BP. The Role of Snail in EMT and Tumorigenesis. Current cancer drug targets. 2013; 13:963-972.
38. Cano A, Perez-Moreno MA, Rodrigo I, Locascio A, Blanco MJ, del Barrio MG, Portillo F, Nieto MA. The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nat Cell Biol. 2000; 2:76-83.