MiR-199a-3p regulates mTOR and c-Met to influence the doxorubicin sensitivity of human hepatocarcinoma cells

Cancer Research

Volumn 70, Issue 12, 2010, Pages 5184-5193

  Fornari, Francesca ^a   Milazzo, Maddalena ^a   Chieco, Pasquale ^a   Negrini, Massimo ^c   Calin, George Adrian ^d   Grazi, Gian Luca ^b   Pollutri, Daniela ^a   Croce, Carlo Maria ^e   Bolondi, Luigi ^a   Gramantieri, Laura ^a,f  

^a UNIVERSITY OF BOLOGNA   (Italy)

^b UNIVERSITY OF BOLOGNA   (Italy)

^c UNIVERSITY OF FERRARA   (Italy)

^d UNIVERSITY OF TEXAS   (United States)

^e OHIO STATE UNIVERSITY   (United States)

^f CRBA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

DOXORUBICIN; MAMMALIAN TARGET OF RAPAMYCIN; MICRORNA; MICRORNA 199A 3P; RAPAMYCIN; SCATTER FACTOR RECEPTOR; UNCLASSIFIED DRUG;

ADULT; AGED; APOPTOSIS; ARTICLE; CANCER INVASION; CARCINOMA CELL; CELL CYCLE G1 PHASE; CELL HYPOXIA; CELL INVASION; CONTROLLED STUDY; DRUG SENSITIVITY; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; LIVER CELL CARCINOMA; MALE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECURRENT CANCER; REGULATORY MECHANISM;

AGED; AGED, 80 AND OVER; ANTIBIOTICS, ANTINEOPLASTIC; APOPTOSIS; BLOTTING, WESTERN; CARCINOMA, HEPATOCELLULAR; CELL ADHESION; CELL CYCLE; CELL MOVEMENT; CELL PROLIFERATION; DOXORUBICIN; DRUG RESISTANCE, NEOPLASM; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LIVER CIRRHOSIS; LIVER NEOPLASMS; LUCIFERASES; MALE; MICRORNAS; MIDDLE AGED; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS C-MET; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER;

EID: 77953773201     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-10-0145     Document Type: Article

References (40)

1. Laurent-Puig P, Legoix P, Bluteau O, et al. Genetic alterations associated with hepatocellular carcinomas define distinct pathways of hepatocarcinogenesis. Gastroenterology 2001;120:1763-73.
2. Chiang DY, Villanueva A, Hoshida Y, et al. Focal gains of VEGFA and molecular classification of hepatocellular carcinoma. Cancer Res 2008;68:6779-88.
3. Llovet JM, Ricci S, Mazzaferro V, et al. Sorafenib in advanced hepatocellular carcinoma. N Engl J Med 2008;359:378-90.
4. Ajani J, Allgood V. Molecular mechanisms in cancer: What should clinicians know? Semin Oncol 2005;32:2-4.
5. Ebos JM, Lee CR, Cruz-Munoz W, Bjarnason GA, Christensen JG, Kerbel RS. Accelerated metastasis after short-term treatment with a potent inhibitor of tumor angiogenesis. Cancer Cell 2009;15:232-9.
6. Iorio MV, Croce CM. MicroRNAs in cancer: small molecules with a huge impact. J Clin Oncol 2009;27:5848-56.
7. Jiang J, Gusev Y, Aderca I, et al. Association of MicroRNA expression in hepatocellular carcinomas with hepatitis infection, cirrhosis, and patient survival. Clin Cancer Res 2008;14:419-27.
8. Budhu A, Jia HL, Forgues M, et al. Identification of metastasis-related microRNAs in hepatocellular carcinoma. Hepatology 2008;47: 897-907. (Pubitemid 351449681)
9. Gramantieri L, Fornari F, Callegari E, et al. MicroRNA involvement in hepatocellular carcinoma. J Cell Mol Med 2008;12:2189-204.
10. Ladeiro Y, Couchy G, Balabaud C, et al. MicroRNA profiling in hepatocellular tumors is associated with clinical features and oncogene/ tumor suppressor gene mutations. Hepatology 2008;47:1955-63.
11. Gramantieri L, Ferracin M, Fornari F, et al. Cyclin G1 is a target of miR-122a, a microRNA frequently down-regulated in human hepatocellular carcinoma. Cancer Res 2007;67:6092-9.
12. Ichimi T, Enokida H, Okuno Y, et al. Identification of novel microRNA targets based on microRNA signatures in bladder cancer. Int J Cancer 2009;125:345-52.
13. Iorio MV, Visone R, Di Leva G, et al. MicroRNA signatures in human ovarian cancer. Cancer Res 2007;67:8699-707.
14. Landgraf P, Rusu M, Sheridan R, et al. A mammalian microRNA expression atlas based on small RNA library sequencing. Cell 2007;129:1401-14.
15. Dolganiuc A, Petrasek J, Kodys K, et al. MicroRNA expression profile in Lieber-DeCarli diet-induced alcoholic and methionine choline deficient diet-induced nonalcoholic steatohepatitis models in mice. Alcohol Clin Exp Res 2009;33:1704-10.
16. Kim S, Lee UJ, Kim MN, et al. MicroRNA miR-199a* regulates the MET proto-oncogene and the downstream extracellular signal-regulated kinase 2 (ERK2). J Biol Chem 2008;283:18158-66.
17. Lin EA, Kong L, Bai XH, Luan Y, Liu CJ. MiR-199a, a bone morphogenic protein 2-responsive MicroRNA, regulates chondrogenesis via direct targeting to Smad1. J Biol Chem 2009;284:11326-35.
18. Oskowitz AZ, Lu J, Penfornis P, et al. Human multipotent stromal cells from bone marrow and microRNA: regulation of differentiation and leukemia inhibitory factor expression. Proc Natl Acad Sci U S A 2008;105:18372-7.
19. Migliore C, Petrelli A, Ghiso E, et al. MicroRNAs impair MET-mediated invasive growth. Cancer Res 2008;68:10128-36.
20. Villanueva A, Chiang DY, Newell P, et al. Pivotal role ofmTORsignaling in hepatocellular carcinoma. Gastroenterology 2008;135:1972-83.
21. Zhou L, Huang Y, Li J, Wang Z. The mTOR pathway is associated with the poor prognosis of human hepatocellular carcinoma. Med Oncol 2010;27:255-61.
22. Edmondson HA, Steiner PE. Primary carcinoma of the liver: a study of 100 cases among 48,900 necropsies. Cancer 1954;7:462-503.
23. Fornari F, Gramantieri L, Ferracin M, et al. MiR-221 controls CDKN1C/p57 and CDKN1B/p27 expression in human hepatocellular carcinoma. Oncogene 2008;27:5651-61.
24. Huynh H, Chow KH, Soo KC, et al. RAD001 (everolimus) inhibits tumour growth in xenograft models of human hepatocellular carcinoma. J Cell Mol Med 2009;13:1371-80.
25. Piguet AC, Semela D, Keogh A, et al. Inhibition of mTOR in combination with doxorubicin in an experimental model of hepatocellular carcinoma. J Hepatol 2008;49:78-87.
26. Buitrago-Molina LE, Pothiraju D, Lamle J, et al. Rapamycin delays tumor development in murine livers by inhibiting proliferation of hepatocytes with DNA damage. Hepatology 2009;50:500-9.
27. Land SC, Tee AR. Hypoxia-inducible factor 1α is regulated by the mammalian target of rapamycin (mTOR) via an mTOR signaling motif. J Biol Chem 2007;282:20534-43.
28. Rane S, He M, Sayed D, et al. Downregulation of miR-199a derepresses hypoxia-inducible factor-1α and Sirtuin 1 and recapitulates hypoxia preconditioning in cardiac myocytes. Circ Res 2009;104: 879-86.
29. Imamura H, Matsuyama Y, Tanaka E, et al. Risk factors contributing to early and late phase intrahepatic recurrence of hepatocellular carcinoma after hepatectomy. J Hepatol 2003;38:200-7.
30. Vignot S, Faivre S, Aguirre D, Raymond E. MTOR-targeted therapy of cancer with rapamycin derivatives. Ann Oncol 2005;16:525-37.
31. Meric-Bernstam F, Gonzalez-Angulo AM. Targeting the mTOR signaling network for cancer therapy. J Clin Oncol 2009;27:2278-87.
32. Salvi A, Arici B, Portolani N, Giulini SM, De Petro G, Barlati S. In vitro c-met inhibition by antisense RNA and plasmid-based RNAi downmodulates migration and invasion of hepatocellular carcinoma cells. Int J Oncol 2007;31:451-60.
33. Salvi A, Sabelli C, Moncini S, et al. MicroRNA-23b mediates urokinase and c-met downmodulation and a decreased migration of human hepatocellular carcinoma cells. FEBS J 2009;276: 2966-82.
34. Li N, Fu H, Tie Y, et al. miR-34a inhibits migration and invasion by down-regulation of c-Met expression in human hepatocellular carcinoma cells. Cancer Lett 2009;275:44-53.
35. Lin PY, Fosmire SP, Park SH, et al. Attenuation of PTEN increases p21 stability and cytosolic localization in kidney cancer cells: a potential mechanism of apoptosis resistance. Mol Cancer 2007;6:16-30.
36. Beuvink I, Boulay A, Fumagalli S, et al. The mTOR inhibitor RAD001 sensitizes tumor cells to DNA-damaged induced apoptosis through inhibition of p21 translation. Cell 2005;120:747-59.
37. Yang H, Magilnick N, Noureddin M, Mato JM, Lu SC. Effect of hepatocyte growth factor on methionine adenosyltransferase genes and growth is cell density-dependent in HepG2 cells. J Cell Physiol 2007; 210:766-73.
38. Tam KH, Yang ZF, Lau CK, Lam CT, Pang RW, Poon RT. Inhibition of mTOR enhances chemosensitivity in hepatocellular carcinoma. Cancer Lett 2009;273:201-9.
39. Comoglio PM, Trusolino L. Invasive growth: from development to metastasis. J Clin Invest 2002;109:857-62.
40. Tong AW, Nemunaitis J. Modulation of miRNA activity in human cancer: a new paradigm for cancer gene therapy? Cancer Gene Ther 2008;15:341-55.