MicroRNA-93 activates c-Met/PI3K/Akt pathway activity in hepatocellular carcinoma by directly inhibiting PTEN and CDKN1A

Oncotarget

Volumn 6, Issue 5, 2015, Pages 3211-3224

  Ohta, Katsuya ^a   Hoshino, Hiromitsu ^a   Wang, Jinhua ^a   Ono, Shigeshi ^a   Iida, Yuuki ^a   Hata, Keisuke ^a   Huang, Sharon K ^a   Colquhoun, Steven ^b   Hoon, Dave S B ^a  

^a SAINT JOHN'S HEALTH CENTER   (United States)

^b CEDARS SINAI MEDICAL CENTER   (United States)

Author keywords

Drug sensitivity; Hepatocellular carcinoma; miR 93; Sorafenib and tivantinib

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 1A; MICRORNA; MICRORNA 93; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; SCATTER FACTOR; SCATTER FACTOR RECEPTOR; SORAFENIB; TIVANTINIB; UNCLASSIFIED DRUG; 2 PYRROLIDONE DERIVATIVE; 3' UNTRANSLATED REGION; CARBANILAMIDE DERIVATIVE; CDKN1A PROTEIN, HUMAN; MIRN93 MICRORNA, HUMAN; NICOTINAMIDE; PROTEIN KINASE B; PROTEIN KINASE INHIBITOR; PTEN PROTEIN, HUMAN; QUINOLINE DERIVATIVE;

3' UNTRANSLATED REGION; ADULT; ARTICLE; CANCER PROGNOSIS; CARCINOGENESIS; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN CELL; IN VITRO STUDY; LIVER CELL CARCINOMA; MALE; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; TUMOR SUPPRESSOR GENE; AGED; ANALOGS AND DERIVATIVES; ANTAGONISTS AND INHIBITORS; APOPTOSIS; BINDING SITE; CELL MOTION; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENE SILENCING; GENETIC TRANSFECTION; GENETICS; HEP-G2 CELL LINE; LIVER TUMOR; METABOLISM; MIDDLE AGED; PATHOLOGY; PROGNOSIS; TIME FACTOR; UPREGULATION; VERY ELDERLY;

3' UNTRANSLATED REGIONS; ADULT; AGED; AGED, 80 AND OVER; APOPTOSIS; BINDING SITES; CARCINOMA, HEPATOCELLULAR; CELL MOVEMENT; CELL PROLIFERATION; CYCLIN-DEPENDENT KINASE INHIBITOR P21; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE KNOCKDOWN TECHNIQUES; HEP G2 CELLS; HUMANS; LIVER NEOPLASMS; MALE; MICRORNAS; MIDDLE AGED; NIACINAMIDE; PHENYLUREA COMPOUNDS; PHOSPHATIDYLINOSITOL 3-KINASE; PROGNOSIS; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-AKT; PROTO-ONCOGENE PROTEINS C-MET; PTEN PHOSPHOHYDROLASE; PYRROLIDINONES; QUINOLINES; TIME FACTORS; TRANSFECTION; UP-REGULATION;

EID: 84923274132     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.3085     Document Type: Article

References (38)

1. Llovet JM, Ricci S, Mazzaferro V, Hilgard P, Gane E, Blanc J-F, de Oliveira AC, Santoro A, Raoul J-L and Forner A. Sorafenib in advanced hepatocellular carcinoma. New England Journal of Medicine. 2008; 359(4):378-390.
2. Cheng A-L, Kang Y-K, Chen Z, Tsao C-J, Qin S, Kim JS, Luo R, Feng J, Ye S and Yang T-S. Efficacy and safety of sorafenib in patients in the Asia-Pacific region with advanced hepatocellular carcinoma: a phase III randomised, double-blind, placebo-controlled trial. The lancet oncology. 2009; 10(1):25-34.
3. National Comprehensive Cancer Network. NCCN Guidelines Version 2.2014 Hepatobiliary Cancers. www. nccn.org.
4. Santoro A, Rimassa L, Borbath I, Daniele B, Salvagni S, Van Laethem JL, Van Vlierberghe H, Trojan J, Kolligs FT and Weiss A. Tivantinib for second-line treatment of advanced hepatocellular carcinoma: a randomised, placebocontrolled phase 2 study. The lancet oncology. 2012.
5. Aravalli RN, Steer CJ and Cressman EN. Molecular mechanisms of hepatocellular carcinoma. Hepatology. 2008; 48(6):2047-2063.
6. Arzumanyan A, Reis HM and Feitelson MA. Pathogenic mechanisms in HBV-and HCV-associated hepatocellular carcinoma. Nature Reviews Cancer. 2013; 13(2):123-135.
7. Li J, Yen C, Liaw D, Podsypanina K, Bose S, Wang SI, Puc J, Miliaresis C, Rodgers L and McCombie R. PTEN, a putative protein tyrosine phosphatase gene mutated in human brain, breast, and prostate cancer. science. 1997; 275(5308):1943-1947.
8. Laurent-Puig P, Cayre A, Manceau G, Buc E, Bachet J-B, Lecomte T, Rougier P, Lievre A, Landi B and Boige V. Analysis of PTEN, BRAF, and EGFR status in determining benefit from cetuximab therapy in wild-type KRAS metastatic colon cancer. Journal of Clinical Oncology. 2009; 27(35):5924-5930.
9. Bleau A-M, Hambardzumyan D, Ozawa T, Fomchenko EI, Huse JT, Brennan CW and Holland EC. PTEN/PI3K/ Akt pathway regulates the side population phenotype and ABCG2 activity in glioma tumor stem-like cells. Cell stem cell. 2009; 4(3):226-235.
10. Vivanco I and Sawyers CL. The phosphatidylinositol 3-kinase-AKT pathway in human cancer. Nature Reviews Cancer. 2002; 2(7):489-501.
11. Sun H, Lesche R, Li D-M, Liliental J, Zhang H, Gao J, Gavrilova N, Mueller B, Liu X and Wu H. PTEN modulates cell cycle progression and cell survival by regulating phosphatidylinositol 3, 4, 5,-trisphosphate and Akt/protein kinase B signaling pathway. Proceedings of the National Academy of Sciences. 1999; 96(11):6199-6204.
12. Engelman JA, Luo J and Cantley LC. The evolution of phosphatidylinositol 3-kinases as regulators of growth and metabolism. Nature Reviews Genetics. 2006; 7(8):606-619.
13. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell. 2004; 116(2):281-297.
14. Calin GA and Croce CM. MicroRNA-cancer connection: the beginning of a new tale. Cancer research. 2006; 66(15):7390-7394.
15. Karreth FA, Tay Y, Perna D, Ala U, Tan SM, Rust AG, DeNicola G, Webster KA, Weiss D and Perez-Mancera PA. In vivo identification of tumor-suppressive PTEN ceRNAs in an oncogenic BRAF-induced mouse model of melanoma. Cell. 2011; 147(2):382-395.
16. Croce CM and Calin GA. miRNAs, cancer, and stem cell division. Cell. 2005; 122(1):6-7.
17. Nicoloso MS, Spizzo R, Shimizu M, Rossi S and Calin GA. MicroRNAs-the micro steering wheel of tumour metastases. Nature Reviews Cancer. 2009; 9(4):293-302.
18. Spizzo R, Nicoloso MS, Croce CM and Calin GA. SnapShot: microRNAs in cancer. Cell. 2009; 137(3):586-586. e581.
19. Hand NJ, Master ZR, Eauclaire SF, Weinblatt DE, Matthews RP and Friedman JR. The microRNA-30 family is required for vertebrate hepatobiliary development. Gastroenterology. 2009; 136(3):1081-1090.
20. Girard M, Jacquemin E, Munnich A, Lyonnet S and Henrion-Caude A. miR-122, a paradigm for the role of microRNAs in the liver. Journal of hepatology. 2008; 48(4):648-656.
21. Gailhouste L, Gomez-Santos L, Hagiwara K, Hatada I, Kitagawa N, Kawaharada K, Thirion M, Kosaka N, Takahashi Ru and Shibata T. miR-148a plays a pivotal role in the liver by promoting the hepatospecific phenotype and suppressing the invasiveness of transformed cells. Hepatology. 2013; 58(3):1153-1165.
22. Meng F, Henson R, Lang M, Wehbe H, Maheshwari S, Mendell JT, Jiang J, Schmittgen TD and Patel T. Involvement of human micro-RNA in growth and response to chemotherapy in human cholangiocarcinoma cell lines. Gastroenterology. 2006; 130(7):2113-2129.
23. Giordano S and Columbano A. MicroRNAs: New tools for diagnosis, prognosis, and therapy in hepatocellular carcinoma. Hepatology. 2013; 57(2):840-847.
24. Sato Y, Nakata K, Kato Y, Shima M, Ishii N, Koji T, Taketa K, Endo Y and Nagataki S. Early recognition of hepatocellular carcinoma based on altered profiles of alpha-fetoprotein. New England Journal of Medicine. 1993; 328(25):1802-1806.
25. Gherardi E, Birchmeier W, Birchmeier C and Woude GV. Targeting MET in cancer: rationale and progress. Nature Reviews Cancer. 2012; 12(2):89-103.
26. Singh S, Singh PP, Roberts LR and Sanchez W. Chemopreventive strategies in hepatocellular carcinoma. Nature Reviews Gastroenterology & Hepatology. 2014; 11(1):45-54.
27. Fu X, Tian J, Zhang L, Chen Y and Hao Q. Involvement of microRNA-93, a new regulator of PTEN/Akt signaling pathway, in regulation of chemotherapeutic drug cisplatin chemosensitivity in ovarian cancer cells. FEBS letters. 2012; 586(9):1279-1286.
28. Llovet JM, Decaens T, Raoul J-L, Boucher E, Kudo M, Chang C, Kang Y-K, Assenat E, Lim H-Y and Boige V. Brivanib in patients with advanced hepatocellular carcinoma who were intolerant to sorafenib or for whom sorafenib failed: Results from the randomized phase III BRISK-PS study. Journal of Clinical Oncology. 2013; 31(28):3509-3516.
29. Villanueva A, Newell P, Chiang DY, Friedman SL and Llovet JM. (2007). Genomics and signaling pathways in hepatocellular carcinoma. Seminars in liver disease: Copyright© 2007 by Thieme Medical Publishers, Inc., 333 Seventh Avenue, New York, NY 10001, USA.), pp. 055- 076.
30. Zhang L, He T, Cui H, Wang Y, Huang C and Hang F. Effects of AFP Gene Silencing on Apoptosis and Proliferation of a Hepatocellular Carcinoma Cell Line. Discovery medicine. 2012; 14(75):115-124.
31. Tangkijvanich P, Anukulkarnkusol N, Suwangool P, Lertmaharit S, Hanvivatvong O, Kullavanijaya P and Poovorawan Y. Clinical characteristics and prognosis of hepatocellular carcinoma: analysis based on serum alphafetoprotein levels. Journal of clinical gastroenterology. 2000; 31(4):302-308.
32. Isom HC and Georgoff I. Quantitative assay for albuminproducing liver cells after simian virus 40 transformation of rat hepatocytes maintained in chemically defined medium. Proceedings of the National Academy of Sciences. 1984; 81(20):6378-6382.
33. Trinklein ND, Aldred SJF, Saldanha AJ and Myers RM. Identification and functional analysis of human transcriptional promoters. Genome research. 2003; 13(2):308-312.
34. Koyanagi K, O'Day SJ, Gonzalez R, Lewis K, Robinson WA, Amatruda TT, Kuo C, Wang H-J, Milford R and Morton DL. Microphthalmia transcription factor as a molecular marker for circulating tumor cell detection in blood of melanoma patients. Clinical Cancer Research. 2006; 12(4):1137-1143.
35. Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL, Vandesompele J and Wittwer CT. The MIQE guidelines: minimum information for publication of quantitative realtime PCR experiments. Clin Chem. 2009; 55(4):611-622.
36. Nguyen T, Kuo C, Nicholl MB, Sim MS, Turner RR, Morton DL and Hoon DS. Downregulation of microRNA- 29c is associated with hypermethylation of tumor-related genes and disease outcome in cutaneous melanoma. Epigenetics. 2011; 6(3):388-394.
37. Narita N, Tanemura A, Murali R, Scolyer RA, Huang S, Arigami T, Yanagita S, Chong KK, Thompson JF, Morton DL and Hoon DS. Functional RET G691S polymorphism in cutaneous malignant melanoma. Oncogene. 2009; 28(34):3058-3068.
38. McShane LM, Altman DG, Sauerbrei W, Taube SE, Gion M and Clark GM. REporting recommendations for tumour MARKer prognostic studies (REMARK). Eur J Cancer. 2005; 41(12):1690-1696.