Targeting c-Met in Cancer by MicroRNAs: Potential Therapeutic Applications in Hepatocellular Carcinoma

Drug Development Research

Volumn 76, Issue 7, 2015, Pages 357-367

  Karagonlar, Zeynep F ^a,b   Korhan, Peyda ^a,c   Atabey, Neşe ^a  

^a DOKUZ EYLUL UNIVERSITY   (Turkey)

^b IZMIR UNIVERSITY OF ECONOMICS   (Turkey)

^c IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

c Met; hepatocellular carcinoma; hepatocyte growth factor; miRNA; targeted therapy

Indexed keywords

MICRORNA; MICRORNA 122; MICRORNA 148A; MICRORNA 181A 5P; MICRORNA 199A 3P; MICRORNA 26A; MICRORNA 34; MICRORNA 93; SCATTER FACTOR; SCATTER FACTOR RECEPTOR; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ANGIOGENESIS; ANTIANGIOGENIC ACTIVITY; APOPTOSIS; AUTOPHOSPHORYLATION; BINDING AFFINITY; CANCER INHIBITION; CELL CYCLE ARREST; CELL INVASION; CELL MIGRATION; CELL MOTILITY; CELL PROLIFERATION; DIMERIZATION; DRUG MECHANISM; HUMAN; LIVER CARCINOGENESIS; LIVER CELL CARCINOMA; MOLECULAR DOCKING; NONHUMAN; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; REVIEW; SENESCENCE; SIGNAL TRANSDUCTION; ANTAGONISTS AND INHIBITORS; CARCINOMA, HEPATOCELLULAR; DRUG EFFECTS; DRUG RESISTANCE; GENETICS; LIVER NEOPLASMS; METABOLISM; MOLECULARLY TARGETED THERAPY; PROCEDURES;

CARCINOMA, HEPATOCELLULAR; DRUG RESISTANCE, NEOPLASM; HUMANS; LIVER NEOPLASMS; MICRORNAS; MOLECULAR TARGETED THERAPY; PROTO-ONCOGENE PROTEINS C-MET;

EID: 84945456707     PISSN: 02724391     EISSN: 10982299     Source Type: Journal    
DOI: 10.1002/ddr.21274     Document Type: Review

References (104)

1. Acunzo M, Visone R, Romano G, Veronese A, Lovat F, Palmieri D, Bottoni A, Garofalo M, Gasparini P, Condorelli G, et al., 2012. miR-130a targets MET and induces TRAIL-sensitivity in NSCLC by downregulating miR-221 and 222. Oncogene 31: 634-642.
2. Agostini M, Knight RA., 2014. miR-34: from bench to bedside. Oncotarget 5: 872-881.
3. Bandiera S, Pfeffer S, Baumert TF, Zeisel MB., 2015. miR-122-a key factor and therapeutic target in liver disease. J Hepatol 62: 448-457.
4. Bartel DP., 2009. MicroRNAs: target recognition and regulatory functions. Cell 136: 215-233.
5. Bottaro DP, Rubin JS, Faletto DL, Chan AM, Kmiecik TE, Vande Woude GF, Aaronson SA., 1991. Identification of the hepatocyte growth factor receptor as the c-met proto-oncogene product. Science 251: 802-804.
6. Bozkaya G, Korhan P, Cokakli M, Erdal E, Sagol O, Karademir S, Korch C, Atabey N., 2012. Cooperative interaction of MUC1 with the HGF/c-Met pathway during hepatocarcinogenesis. Mol Cancer 11: 64.
7. Bumcrot D, Manoharan M, Koteliansky V, Sah DW., 2006. RNAi therapeutics: a potential new class of pharmaceutical drugs. Nat Chem Biol 2: 711-719.
8. Buurman R, Gurlevik E, Schaffer V, Eilers M, Sandbothe M, Kreipe H, Wilkens L, Schlegelberger B, Kuhnel F, Skawran B., 2012. Histone deacetylases activate hepatocyte growth factor signaling by repressing microRNA-449 in hepatocellular carcinoma cells. Gastroenterology 143: 811-820.e1-15.
9. Calin GA, Sevignani C, Dumitru CD, Hyslop T, Noch E, Yendamuri S, Shimizu M, Rattan S, Bullrich F, Negrini M, et al., 2004. Human microRNA genes are frequently located at fragile sites and genomic regions involved in cancers. Proc Natl Acad Sci USA 101: 2999-3004.
10. Canadas I, Taus A, Gonzalez I, Villanueva X, Gimeno J, Pijuan L, Domine M, Sanchez-Font A, Vollmer I, Menendez S, et al., 2014. High circulating hepatocyte growth factor levels associate with epithelial to mesenchymal transition and poor outcome in small cell lung cancer patients. Oncotarget 5: 5246-5256.
11. Cecchi F, Wright C, Bottaro D., 2010. Experimental Cancer Therapeutics Targeting the Hepatocyte Growth Factor/Met Signaling Pathway. Center for Cancer Research, National Cancer Institute, Bethesda, MD. https://ccrod.cancer.gov/confluence/display/CCRHGF/Home. (Accessed June 15, 2015.)
12. Chai ZT, Kong J, Zhu XD, Zhang YY, Lu L, Zhou JM, Wang LR, Zhang KZ, Zhang QB, Ao JY, et al., 2013. MicroRNA-26a inhibits angiogenesis by down-regulating VEGFA through the PIK3C2alpha/Akt/HIF-1alpha pathway in hepatocellular carcinoma. PLoS One 8: e77957.
13. Chen Y, Gao D-Y, Huang L., 2015. In vivo delivery of miRNAs for cancer therapy: challenges and strategies. Adv Drug Deliv Rev 81: 128-141.
14. Cheng CY, Hwang CI, Corney DC, Flesken-Nikitin A, Jiang L, Oner GM, Munroe RJ, Schimenti JC, Hermeking H, Nikitin AY., 2014. miR-34 cooperates with p53 in suppression of prostate cancer by joint regulation of stem cell compartment. Cell Rep 6: 1000-1007.
15. Coulouarn C, Factor VM, Andersen JB, Durkin ME, Thorgeirsson SS., 2009. Loss of miR-122 expression in liver cancer correlates with suppression of the hepatic phenotype and gain of metastatic properties. Oncogene 28: 3526-3536.
16. Croce CM., 2009. Causes and consequences of microRNA dysregulation in cancer. Nat Rev Genet 10: 704-714.
17. Daige CL, Wiggins JF, Priddy L, Nelligan-Davis T, Zhao J, Brown D., 2014. Systemic delivery of a miR34a mimic as a potential therapeutic for liver cancer. Mol Cancer Ther 13: 2352-2360.
18. Dang Y, Luo D, Rong M, Chen G., 2013. Underexpression of miR-34a in hepatocellular carcinoma and its contribution towards enhancement of proliferating inhibitory effects of agents targeting c-MET. PLoS One 8: e61054.
19. Duan Z, Choy E, Harmon D, Liu X, Susa M, Mankin H, Hornicek F., 2011. MicroRNA-199a-3p is downregulated in human osteosarcoma and regulates cell proliferation and migration. Mol Cancer Ther 10: 1337-1345.
20. Eder JP, Vande Woude GF, Boerner SA, LoRusso PM., 2009. Novel therapeutic inhibitors of the c-Met signaling pathway in cancer. Clin Cancer Res 15: 2207-2214.
21. Esau CC., 2008. Inhibition of microRNA with antisense oligonucleotides. Methods 44: 55-60.
22. Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, Parkin DM, Forman D, Bray F., 2015. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer 136: E359-E386.
23. Ferracin M, Lupini L, Salamon I, Saccenti E, Zanzi MV, Rocchi A, Da Ros L, Zagatti B, Musa G, Bassi C, et al., 2015. Absolute quantification of cell-free microRNAs in cancer patients. Oncotarget 6: 14545-14555.
24. Fornari F, Gramantieri L, Giovannini C, Veronese A, Ferracin M, Sabbioni S, Calin GA, Grazi GL, Croce CM, Tavolari S, et al., 2009. MiR-122/cyclin G1 interaction modulates p53 activity and affects doxorubicin sensitivity of human hepatocarcinoma cells. Cancer Res 69: 5761-5777.
25. Fornari F, Milazzo M, Chieco P, Negrini M, Calin GA, Grazi GL, Pollutri D, Croce CM, Bolondi L, Gramantieri L., 2010. MiR-199a-3p regulates mTOR and c-Met to influence the doxorubicin sensitivity of human hepatocarcinoma cells. Cancer Res 70: 5184-5193.
26. Friedman RC, Farh KK, Burge CB, Bartel DP., 2009. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 19: 92-105.
27. Fu P, Du F, Yao M, Lv K, Liu Y., 2014. MicroRNA-185 inhibits proliferation by targeting c-Met in human breast cancer cells. Exp Ther Med 8: 1879-1883.
28. Furlan A, Kherrouche Z, Montagne R, Copin MC, Tulasne D., 2014. Thirty years of research on met receptor to move a biomarker from bench to bedside. Cancer Res 74: 6737-6744.
29. Gailhouste L, Gomez-Santos L, Hagiwara K, Hatada I, Kitagawa N, Kawaharada K, Thirion M, Kosaka N, Takahashi RU, Shibata T, et al., 2013. miR-148a plays a pivotal role in the liver by promoting the hepatospecific phenotype and suppressing the invasiveness of transformed cells. Hepatology 58: 1153-1165.
30. Gao Y, Zeng F, Wu JY, Li HY, Fan JJ, Mai L, Zhang J, Ma DM, Li Y, Song FZ., 2015. MiR-335 inhibits migration of breast cancer cells through targeting oncoprotein c-Met. Tumour Biol 36: 2875-2883.
31. Garber K., 2014. MET inhibitors start on road to recovery. Nat Rev Drug Discov 13: 563-565.
32. Garzon R, Marcucci G, Croce CM., 2010. Targeting microRNAs in cancer: rationale, strategies and challenges. Nat Rev Drug Discov 9: 775-789.
33. Giordano S, Columbano A., 2013. MicroRNAs: new tools for diagnosis, prognosis, and therapy in hepatocellular carcinoma? Hepatology 57: 840-847.
34. Han C, Zhou Y, An Q, Li F, Li D, Zhang X, Yu Z, Zheng L, Duan Z, Kan Q., 2015. MicroRNA-1 (miR-1) inhibits gastric cancer cell proliferation and migration by targeting MET. Tumour Biol 1-9.
35. He AR, Goldenberg AS., 2013. Treating hepatocellular carcinoma progression following first-line sorafenib: therapeutic options and clinical observations. Therap Adv Gastroenterol 6: 447-458.
36. Henry JC, Park JK, Jiang J, Kim JH, Nagorney DM, Roberts LR, Banerjee S, Schmittgen TD., 2010. miR-199a-3p targets CD44 and reduces proliferation of CD44 positive hepatocellular carcinoma cell lines. Biochem Biophys Res Commun 403: 120-125.
37. Hermeking H., 2010. The miR-34 family in cancer and apoptosis. Cell Death Differ 17: 193-199.
38. Hosoda H, Izumi H, Tukada Y, Takagiwa J, Chiaki T, Yano M, Arai H., 2012. Plasma hepatocyte growth factor elevation may be associated with early metastatic disease in primary lung cancer patients. Ann Thorac Cardiovasc Surg 18: 1-7.
39. Hou J, Lin L, Zhou W, Wang Z, Ding G, Dong Q, Qin L, Wu X, Zheng Y, Yang Y, et al., 2011. Identification of miRNomes in human liver and hepatocellular carcinoma reveals miR-199a/b-3p as therapeutic target for hepatocellular carcinoma. Cancer Cell 19: 232-243.
40. Hu G, Chen D, Li X, Yang K, Wang H, Wu W., 2010. miR-133b regulates the MET proto-oncogene and inhibits the growth of colorectal cancer cells in vitro and in vivo. Cancer Biol Ther 10: 190-197.
41. Huang J, Dong B, Zhang J, Kong W, Chen Y, Xue W, Liu D, Huang Y., 2014. miR-199a-3p inhibits hepatocyte growth factor/c-Met signaling in renal cancer carcinoma. Tumour Biol 35: 5833-5843.
42. Jin L, Fuchs A, Schnitt SJ, Yao Y, Joseph A, Lamszus K, Park M, Goldberg ID, Rosen EM., 1997. Expression of scatter factor and c-met receptor in benign and malignant breast tissue. Cancer 79: 749-760.
43. Jopling CL., 2008. Regulation of hepatitis C virus by microRNA-122. Biochem Soc Trans 36 (Pt 6): 1220-1223.
44. Kaposi-Novak P, Lee JS, Gomez-Quiroz L, Coulouarn C, Factor VM, Thorgeirsson SS., 2006. Met-regulated expression signature defines a subset of human hepatocellular carcinomas with poor prognosis and aggressive phenotype. J Clin Invest 116: 1582-1595.
45. Kasahara K, Arao T, Sakai K, Matsumoto K, Sakai A, Kimura H, Sone T, Horiike A, Nishio M, Ohira T, et al., 2010. Impact of serum hepatocyte growth factor on treatment response to epidermal growth factor receptor tyrosine kinase inhibitors in patients with non-small cell lung adenocarcinoma. Clin Cancer Res 16: 4616-4624.
46. Kentsis A, Reed C, Rice KL, Sanda T, Rodig SJ, Tholouli E, Christie A, Valk PJ, Delwel R, Ngo V, et al., 2012. Autocrine activation of the MET receptor tyrosine kinase in acute myeloid leukemia. Nat Med 18: 1118-1122.
47. Kinose Y, Sawada K, Nakamura K, Sawada I, Toda A, Nakatsuka E, Hashimoto K, Mabuchi S, Takahashi K, Kurachi H, et al., 2015. The hypoxia-related microRNA miR-199a-3p displays tumor suppressor functions in ovarian carcinoma. Oncotarget 6: 11342-11356.
48. Korhan P, Erdal E, Atabey N., 2014a. MiR-181a-5p is downregulated in hepatocellular carcinoma and suppresses motility, invasion and branching-morphogenesis by directly targeting c-Met. Biochem Biophys Res Commun 450: 1304-1312.
49. Korhan P, Erdal E, Kandemis E, Cokakli M, Nart D, Yilmaz F, Can A, Atabey N., 2014b. Reciprocal activating crosstalk between c-Met and caveolin 1 promotes invasive phenotype in hepatocellular carcinoma. PLoS One 9: e105278.
50. Kota J, Chivukula RR, O'Donnell KA, Wentzel EA, Montgomery CL, Hwang HW, Chang TC, Vivekanandan P, Torbenson M, Clark KR, et al., 2009. Therapeutic microRNA delivery suppresses tumorigenesis in a murine liver cancer model. Cell 137: 1005-1017.
51. Ladeiro Y, Couchy G, Balabaud C, Bioulac-Sage P, Pelletier L, Rebouissou S, Zucman-Rossi J., 2008. MicroRNA profiling in hepatocellular tumors is associated with clinical features and oncogene/tumor suppressor gene mutations. Hepatology 47: 1955-1963.
52. Lanford RE, Hildebrandt-Eriksen ES, Petri A, Persson R, Lindow M, Munk ME, Kauppinen S, Orum H., 2010. Therapeutic silencing of microRNA-122 in primates with chronic hepatitis C virus infection. Science 327: 198-201.
53. Levitzki A, Klein S., 2010. Signal transduction therapy of cancer. Mol Aspects Med 31: 287-329.
54. Li Z, Rana TM., 2014. Therapeutic targeting of microRNAs: current status and future challenges. Nat Rev Drug Discov 13: 622-638.
55. Liu G, Wong-Staal F, Li QX., 2007. Development of new RNAi therapeutics. Histol Histopathol 22: 211-217.
56. Lu J, Getz G, Miska EA, Alvarez-Saavedra E, Lamb J, Peck D, Sweet-Cordero A, Ebert BL, Mak RH, Ferrando AA, et al., 2005. MicroRNA expression profiles classify human cancers. Nature 435: 834-8.
57. Luo W, Huang B, Li Z, Li H, Sun L, Zhang Q, Qiu X, Wang E., 2013. MicroRNA-449a is downregulated in non-small cell lung cancer and inhibits migration and invasion by targeting c-Met. PLoS One 8: e64759.
58. Lv M, Zhang X, Li M, Chen Q, Ye M, Liang W, Ding L, Cai H, Fu D, Lv Z., 2013. miR-26a and its target CKS2 modulate cell growth and tumorigenesis of papillary thyroid carcinoma. PLoS One 8: e67591.
59. Ma Y, Qin H, Cui Y., 2013. MiR-34a targets GAS1 to promote cell proliferation and inhibit apoptosis in papillary thyroid carcinoma via PI3K/Akt/Bad pathway. Biochem Biophys Res Commun 441: 958-963.
60. Malvezzi M, Bertuccio P, Levi F, La Vecchia C, Negri E., 2014. European cancer mortality predictions for the year 2014. Ann Oncol 25: 1650-1656.
61. Maroun CR, Rowlands T., 2014. The Met receptor tyrosine kinase: a key player in oncogenesis and drug resistance. Pharmacol Ther 142: 316-338.
62. Matsumoto K, Nakamura T., 2006. Hepatocyte growth factor and the Met system as a mediator of tumor-stromal interactions. Int J Cancer 119: 477-483.
63. Maulik G, Shrikhande A, Kijima T, Ma PC, Morrison PT, Salgia R., 2002. Role of the hepatocyte growth factor receptor, c-Met, in oncogenesis and potential for therapeutic inhibition. Cytokine Growth Factor Rev 13: 41-59.
64. Merchant M, Ma X, Maun HR, Zheng Z, Peng J, Romero M, Huang A, Yang NY, Nishimura M, Greve J, et al., 2013. Monovalent antibody design and mechanism of action of onartuzumab, a MET antagonist with anti-tumor activity as a therapeutic agent. Proc Natl Acad Sci USA 110: E2987-E2996.
65. Minna E, Romeo P, De Cecco L, Dugo M, Cassinelli G, Pilotti S, Degl'Innocenti D, Lanzi C, Casalini P, Pierotti MA, et al., 2014. miR-199a-3p displays tumor suppressor functions in papillary thyroid carcinoma. Oncotarget 5: 2513-2528.
66. Murakami Y, Yasuda T, Saigo K, Urashima T, Toyoda H, Okanoue T, Shimotohno K., 2006. Comprehensive analysis of microRNA expression patterns in hepatocellular carcinoma and non-tumorous tissues. Oncogene 25: 2537-2545.
67. Nakamura T, Sakai K, Nakamura T, Matsumoto K., 2011. Hepatocyte growth factor twenty years on: much more than a growth factor. J Gastroenterol Hepatol 26 (Suppl 1): 188-202.
68. Nassirpour R, Mehta PP, Yin MJ., 2013. miR-122 regulates tumorigenesis in hepatocellular carcinoma by targeting AKT3. PLoS One 8: e79655.
69. Niu G, Li B, Sun J, Sun L., 2015. miR-454 is down-regulated in osteosarcomas and suppresses cell proliferation and invasion by directly targeting c-Met. Cell Prolif 48: 348-355.
70. Ohta K, Hoshino H, Wang J, Ono S, Iida Y, Hata K, Huang SK, Colquhoun S, Hoon DS., 2015. MicroRNA-93 activates c-Met/PI3K/Akt pathway activity in hepatocellular carcinoma by directly inhibiting PTEN and CDKN1A. Oncotarget 6: 3211-3224.
71. Peng Y, Guo JJ, Liu YM, Wu XL., 2014. MicroRNA-34A inhibits the growth, invasion and metastasis of gastric cancer by targeting PDGFR and MET expression. Biosci Rep 34 (3): e00112.
72. Peters S, Adjei AA., 2012. MET: a promising anticancer therapeutic target. Nat Rev Clin Oncol 9: 314-326.
73. Rahib L, Smith BD, Aizenberg R, Rosenzweig AB, Fleshman JM, Matrisian LM., 2014. Projecting cancer incidence and deaths to 2030: the unexpected burden of thyroid, liver, and pancreas cancers in the United States. Cancer Res 74: 2913-2921.
74. Reid JF, Sokolova V, Zoni E, Lampis A, Pizzamiglio S, Bertan C, Zanutto S, Perrone F, Camerini T, Gallino G, et al., 2012. miRNA profiling in colorectal cancer highlights miR-1 involvement in MET-dependent proliferation. Mol Cancer Res 10: 504-515.
75. Rimassa L, Porta C, Borbath I, Daniele B, Finn RS, Raoul J-L, Schwartz LH, He AR, Trojan J, Peck-Radosavljevic M, et al., 2014. Tivantinib in MET-high hepatocellular carcinoma patients and the ongoing Phase III clinical trial. Hepat Oncol 1: 181-188.
76. Roberts AP, Lewis AP, Jopling CL., 2011. miR-122 activates hepatitis C virus translation by a specialized mechanism requiring particular RNA components. Nucleic Acids Res 39: 7716-7729.
77. Rokavec M, Li H, Jiang L, Hermeking H., 2014. The p53/miR-34 axis in development and disease. J Mol Cell Biol 6: 214-230.
78. Sakai K, Aoki S, Matsumoto K., 2015. Hepatocyte growth factor and Met in drug discovery. J Biochem 157: 271-284.
79. Scudellari M., 2014. Drug development: try and try again. Nature 516: S4-S6.
80. Siegel R, Ma J, Zou Z, Jemal A., 2014. Cancer statistics, 2014. CA Cancer J Clin 64: 9-29.
81. Siemens H, Neumann J, Jackstadt R, Mansmann U, Horst D, Kirchner T, Hermeking H., 2013. Detection of miR-34a promoter methylation in combination with elevated expression of c-Met and beta-catenin predicts distant metastasis of colon cancer. Clin Cancer Res 19: 710-720.
82. Sun L, Bian G, Meng Z, Dang G, Shi D, Mi S., 2015. MiR-144 Inhibits Uveal melanoma cell proliferation and invasion by regulating c-Met expression. PLoS One 10: e0124428.
83. Tamura K, Fukuoka M., 2003. Molecular target-based cancer therapy: tyrosine kinase inhibitors. Int J Clin Oncol 8: 207-211.
84. Tan S, Li R, Ding K, Lobie PE, Zhu T., 2011. miR-198 inhibits migration and invasion of hepatocellular carcinoma cells by targeting the HGF/c-MET pathway. FEBS Lett 585: 2229-2234.
85. Trusolino L, Bertotti A, Comoglio PM., 2010. MET signalling: principles and functions in development, organ regeneration and cancer. Nat Rev Mol Cell Biol 11: 834-848.
86. Tsai WC, Hsu PW, Lai TC, Chau GY, Lin CW, Chen CM, Lin CD, Liao YL, Wang JL, Chau YP, et al., 2009. MicroRNA-122, a tumor suppressor microRNA that regulates intrahepatic metastasis of hepatocellular carcinoma. Hepatology 49: 1571-1582.
87. Ujiie H, Tomida M, Akiyama H, Nakajima Y, Okada D, Yoshino N, Takiguchi Y, Tanzawa H., 2012. Serum hepatocyte growth factor and interleukin-6 are effective prognostic markers for non-small cell lung cancer. Anticancer Res 32: 3251-3258.
88. Utsugi T., 2013. New challenges and inspired answers for anticancer drug discovery and development. Jpn J Clin Oncol 43: 945-953.
89. Varnholt H, Drebber U, Schulze F, Wedemeyer I, Schirmacher P, Dienes HP, Odenthal M., 2008. MicroRNA gene expression profile of hepatitis C virus-associated hepatocellular carcinoma. Hepatology 47: 1223-1232.
90. Villanueva A, Hernandez-Gea V, Llovet JM., 2013. Medical therapies for hepatocellular carcinoma: a critical view of the evidence. Nat Rev Gastroenterol Hepatol 10: 34-42.
91. 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.
92. Wen Z, Zhao S, Liu S, Liu Y, Li X, Li S., 2015. MicroRNA-148a inhibits migration and invasion of ovarian cancer cells via targeting sphingosine-1-phosphate receptor 1. Mol Med Rep 12: 3775-3780.
93. Wilson TR, Fridlyand J, Yan Y, Penuel E, Burton L, Chan E, Peng J, Lin E, Wang Y, Sosman J, et al., 2012. Widespread potential for growth-factor-driven resistance to anticancer kinase inhibitors. Nature 487: 505-509.
94. Wu ZS, Wu Q, Wang CQ, Wang XN, Huang J, Zhao JJ, Mao SS, Zhang GH, Xu XC, Zhang N., 2011. miR-340 inhibition of breast cancer cell migration and invasion through targeting of oncoprotein c-Met. Cancer 117: 2842-2852.
95. Xiang Q, Chen W, Ren M, Wang J, Zhang H, Deng DY, Zhang L, Shang C, Chen Y., 2014. Cabozantinib suppresses tumor growth and metastasis in hepatocellular carcinoma by a dual blockade of VEGFR2 and MET. Clin Cancer Res 20: 2959-2070.
96. Xu X, Ho W, Zhang X, Bertrand N, Farokhzad O., 2015 Cancer nanomedicine: from targeted delivery to combination therapy. Trends Mol Med 21: 223-232.
97. Yang X, Zhang XF, Lu X, Jia HL, Liang L, Dong QZ, Ye QH, Qin LX., 2014. MicroRNA-26a suppresses angiogenesis in human hepatocellular carcinoma by targeting hepatocyte growth factor-cMet pathway. Hepatology 59: 1874-1885.
98. Yang YM, Lee CG, Koo JH, Kim TH, Lee JM, An J, Kim KM, Kim SG., 2015. Galpha12 overexpressed in hepatocellular carcinoma reduces microRNA-122 expression via HNF4alpha inactivation, which causes c-Met induction. Oncotarget 6: 19056-19069.
99. You H, Ding W, Dang H, Jiang Y, Rountree CB., 2011. c-Met represents a potential therapeutic target for personalized treatment in hepatocellular carcinoma. Hepatology 54: 879-889.
100. Zeng C, Wang R, Li D, Lin XJ, Wei QK, Yuan Y, Wang Q, Chen W, Zhuang SM., 2010. A novel GSK-3 beta-C/EBP alpha-miR-122-insulin-like growth factor 1 receptor regulatory circuitry in human hepatocellular carcinoma. Hepatology 52: 1702-1712.
101. Zhan Q, Fang Y, Deng X, Chen H, Jin J, Lu X, Peng C, Li H, Shen B., 2015. The interplay between miR-148a and DNMT1 might be exploited for pancreatic cancer therapy. Cancer Invest, 33: 267-275.
102. Zhang JP, Zeng C, Xu L, Gong J, Fang JH, Zhuang SM., 2014. MicroRNA-148a suppresses the epithelial-mesenchymal transition and metastasis of hepatoma cells by targeting Met/Snail signaling. Oncogene 33: 4069-4076.
103. Zhao H, Li M, Li L, Yang X, Lan G, Zhang Y., 2013. MiR-133b is down-regulated in human osteosarcoma and inhibits osteosarcoma cells proliferation, migration and invasion, and promotes apoptosis. PLoS One 8: e83571.
104. Zhou JY, Chen X, Zhao J, Bao Z, Chen X, Zhang P, Liu ZF, Zhou JY., 2014. MicroRNA-34a overcomes HGF-mediated gefitinib resistance in EGFR mutant lung cancer cells partly by targeting MET. Cancer Lett 351: 265-271.