Elevated hepatocyte growth factor expression as an autocrine c-Met activation mechanism in acquired resistance to sorafenib in hepatocellular carcinoma cells

Cancer Science

Volumn 107, Issue 4, 2016, Pages 407-416

  Firtina Karagonlar, Zeynep ^a,b   Koc, Dogukan ^b   Iscan, Evin ^b   Erdal, Esra ^b   Atabey, Neşe ^b  

^a IZMIR UNIVERSITY OF ECONOMICS   (Turkey)

^b DOKUZ EYLUL UNIVERSITY   (Turkey)

Author keywords

C Met; Hepatocarcinogenesis; Hepatocyte growth factor; Liver cancer; Sorafenib

Indexed keywords

CYTOKERATIN 19; GELATINASE B; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; N (3 CHLOROPHENYL) 3 [3,5 DIMETHYL 4 (4 METHYL 1 PIPERAZINYLCARBONYL) 1H PYRROL 2 YLMETHYLENE] 2,3 DIHYDRO N METHYL 2 OXO 1H INDOLE 5 SULFONAMIDE; NEUTRALIZING ANTIBODY; PROTEIN KINASE B; SCATTER FACTOR; SCATTER FACTOR RECEPTOR; SORAFENIB; UVOMORULIN; ((3Z)-N-(3-CHLOROPHENYL)-3-((3,5-DIMETHYL-4-((4-METHYLPIPERAZIN-1-YL)CARBONYL)-1H-PYRROL-2-YL)METHYLENE)-N-METHYL-2-OXO-2,3-DIHYDRO-1H-INDOLE-5-SULFONAMIDE); CARBANILAMIDE DERIVATIVE; INDOLE DERIVATIVE; NICOTINAMIDE; PIPERAZINE DERIVATIVE; SULFONAMIDE;

APOPTOSIS; ARTICLE; AUTOCRINE EFFECT; CANCER RESISTANCE; CELL INVASION; CELL MIGRATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DRUG EXPOSURE; DRUG MECHANISM; DRUG POTENTIATION; ENZYME PHOSPHORYLATION; GENE ACTIVATION; GENE EXPRESSION; HEPATOCELLULAR CARCINOMA CELL LINE; HUMAN; HUMAN CELL; LIVER CELL CARCINOMA; PRIORITY JOURNAL; UPREGULATION; WESTERN BLOTTING; ANALOGS AND DERIVATIVES; BIOSYNTHESIS; CARCINOMA, HEPATOCELLULAR; CELL PROLIFERATION; DRUG EFFECTS; DRUG RESISTANCE; GENE EXPRESSION REGULATION; GENETICS; LIVER NEOPLASMS; PATHOLOGY; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ANTIBODIES, NEUTRALIZING; APOPTOSIS; AUTOCRINE COMMUNICATION; CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; CELL PROLIFERATION; DRUG RESISTANCE, NEOPLASM; GENE EXPRESSION REGULATION, NEOPLASTIC; HEPATOCYTE GROWTH FACTOR; HUMANS; INDOLES; LIVER NEOPLASMS; NIACINAMIDE; PHENYLUREA COMPOUNDS; PIPERAZINES; PROTO-ONCOGENE PROTEINS C-MET; SIGNAL TRANSDUCTION; SULFONAMIDES;

EID: 84963646095     PISSN: 13479032     EISSN: 13497006     Source Type: Journal    
DOI: 10.1111/cas.12891     Document Type: Article

References (57)

1. Forner A, Llovet JM, Bruix J. Hepatocellular carcinoma. Lancet 2012; 379: 1245-55.
2. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin 2011; 61: 69-90.
3. Villanueva A, Hernandez-Gea V, Llovet JM. Medical therapies for hepatocellular carcinoma: a critical view of the evidence. Nat Rev Gastroenterol Hepatol 2013; 10: 34-42.
4. Thomas MB. Systemic therapy for hepatocellular carcinoma. Cancer J 2008; 14: 123-7.
5. Llovet JM, Ricci S, Mazzaferro V et al. Sorafenib in advanced hepatocellular carcinoma. N Engl J Med 2008; 359: 378-90.
6. Mendez-Sanchez N, Vasquez-Fernandez F, Zamora-Valdes D, Uribe M. Sorafenib, a systemic therapy for hepatocellular carcinoma. Ann Hepatol 2008; 7: 46-51.
7. Gauthier A, Ho M. Role of sorafenib in the treatment of advanced hepatocellular carcinoma: an update. Hepatol Res 2013; 43: 147-54.
8. Villanueva A, Llovet JM. Second-line therapies in hepatocellular carcinoma: emergence of resistance to sorafenib. Clin Cancer Res 2012; 18: 1824-6.
9. Zhai B, Sun XY. Mechanisms of resistance to sorafenib and the corresponding strategies in hepatocellular carcinoma. World J Hepatol 2013; 5: 345-52.
10. Sun H, Zhu MS, Wu WR, Shi XD, Xu LB. Role of anti-angiogenesis therapy in the management of hepatocellular carcinoma: the jury is still out. World J Hepatol 2014; 6: 830-5.
11. Chen KF, Chen HL, Tai WT et al. Activation of phosphatidylinositol 3-kinase/Akt signaling pathway mediates acquired resistance to sorafenib in hepatocellular carcinoma cells. J Pharmacol Exp Ther 2011; 337: 155-61.
12. Tai WT, Cheng AL, Shiau CW et al. Dovitinib induces apoptosis and overcomes sorafenib resistance in hepatocellular carcinoma through SHP-1-mediated inhibition of STAT3. Mol Cancer Ther 2012; 11: 452-63.
13. Su JC, Tseng PH, Wu SH et al. SC-2001 overcomes STAT3-mediated sorafenib resistance through RFX-1/SHP-1 activation in hepatocellular carcinoma. Neoplasia 2014; 16: 595-605.
14. He AR, Goldenberg AS. Treating hepatocellular carcinoma progression following first-line sorafenib: therapeutic options and clinical observations. Therap Adv Gastroenterol 2013; 6: 447-58.
15. Bottaro DP, Rubin JS, Faletto DL et al. Identification of the hepatocyte growth factor receptor as the c-met proto-oncogene product. Science 1991; 251: 802-4.
16. Cecchi F, Rabe DC, Bottaro DP. Targeting the HGF/Met signalling pathway in cancer. Eur J Cancer 2010; 46: 1260-70.
17. Naldini L, Weidner KM, Vigna E et al. Scatter factor and hepatocyte growth factor are indistinguishable ligands for the MET receptor. EMBO J 1991; 10: 2867-78.
18. Huh CG, Factor VM, Sanchez A, Uchida K, Conner EA, Thorgeirsson SS. Hepatocyte growth factor/c-met signaling pathway is required for efficient liver regeneration and repair. Proc Natl Acad Sci 2004; 101: 4477-82.
19. Borowiak M, Garratt AN, Wustefeld T, Strehle M, Trautwein C, Birchmeier C. Met provides essential signals for liver regeneration. Proc Natl Acad Sci 2004; 101: 10608-13.
20. Trusolino L, Bertotti A, Comoglio PM. MET signalling: principles and functions in development, organ regeneration and cancer. Nat Rev Mol Cell Biol 2010; 11: 834-48.
21. Birchmeier C, Birchmeier W, Gherardi E, Vande Woude GF. Met, metastasis, motility and more. Nat Rev Mol Cell Biol 2003; 4: 915-25.
22. Organ SL, Tsao MS. An overview of the c-MET signaling pathway. Ther Adv Med Oncol 2011; 3: S7-19.
23. Christensen JG, Burrows J, Salgia R. c-Met as a target for human cancer and characterization of inhibitors for therapeutic intervention. Cancer Lett 2005; 225: 1-26.
24. Maroun CR, Rowlands T. The Met receptor tyrosine kinase: a key player in oncogenesis and drug resistance. Pharmacol Ther 2014; 142: 316-38.
25. Noguchi O, Enomoto N, Ikeda T, Kobayashi F, Marumo F, Sato C. Gene expressions of c-met and hepatocyte growth factor in chronic liver disease and hepatocellular carcinoma. J Hepatol 1996; 24: 286-92.
26. Kondo S, Ojima H, Tsuda H et al. Clinical impact of c-Met expression and its gene amplification in hepatocellular carcinoma. Int J Clin Oncol 2013; 18: 207-13.
27. Kaposi-Novak P, Lee JS, Gomez-Quiroz L, Coulouarn C, Factor VM, Thorgeirsson SS. Met-regulated expression signature defines a subset of human hepatocellular carcinomas with poor prognosis and aggressive phenotype. J Clin Invest 2006; 116: 1582-95.
28. Marx-Stoelting P, Borowiak M, Knorpp T, Birchmeier C, Buchmann A, Schwarz M. Hepatocarcinogenesis in mice with a conditional knockout of the hepatocyte growth factor receptor c-Met. Int J Cancer 2009; 124: 1767-72.
29. Chow AK, Ng L, Lam CS et al. The enhanced metastatic potential of hepatocellular carcinoma (HCC) cells with sorafenib resistance. PLoS ONE 2013; 8: e78675.
30. Chen W, Wu J, Shi H et al. Hepatic stellate cell coculture enables sorafenib resistance in Huh7 cells through HGF/c-Met/Akt and Jak2/Stat3 pathways. Biomed Res Int 2014; 2014: 764981.
31. Canadas I, Rojo F, Taus A et al. Targeting epithelial-to-mesenchymal transition with Met inhibitors reverts chemoresistance in small cell lung cancer. Clin Cancer Res 2014; 20: 938-50.
32. Liska D, Chen CT, Bachleitner-Hofmann T, Christensen JG, Weiser MR. HGF rescues colorectal cancer cells from EGFR inhibition via MET activation. Clin Cancer Res 2011; 17: 472-82.
33. Turke AB, Zejnullahu K, Wu YL et al. Preexistence and clonal selection of MET amplification in EGFR mutant NSCLC. Cancer Cell 2010; 17: 77-88.
34. Cokakli M, Erdal E, Nart D et al. Differential expression of Caveolin-1 in hepatocellular carcinoma: correlation with differentiation state, motility and invasion. BMC Cancer 2009; 9: 65.
35. Korhan P, Erdal E, Kandemis E et al. Reciprocal activating crosstalk between c-Met and caveolin 1 promotes invasive phenotype in hepatocellular carcinoma. PLoS ONE 2014; 9: e105278.
36. Yuzugullu H, Benhaj K, Ozturk N et al. Canonical Wnt signaling is antagonized by noncanonical Wnt5a in hepatocellular carcinoma cells. Mol Cancer 2009; 8: 90.
37. Bozkaya G, Korhan P, Cokakli M et al. Cooperative interaction of MUC1 with the HGF/c-Met pathway during hepatocarcinogenesis. Mol Cancer 2012; 11: 64.
38. Singh A, Settleman J. EMT, cancer stem cells and drug resistance: an emerging axis of evil in the war on cancer. Oncogene 2010; 29: 4741-51.
39. Zhai B, Hu F, Jiang X et al. Inhibition of Akt reverses the acquired resistance to sorafenib by switching protective autophagy to autophagic cell death in hepatocellular carcinoma. Mol Cancer Ther 2014; 13: 1589-98.
40. Gedaly R, Galuppo R, Musgrave Y et al. PKI-587 and sorafenib alone and in combination on inhibition of liver cancer stem cell proliferation. J Surg Res 2013; 185: 225-30.
41. van Malenstein H, Dekervel J, Verslype C et al. Long-term exposure to sorafenib of liver cancer cells induces resistance with epithelial-to-mesenchymal transition, increased invasion and risk of rebound growth. Cancer Lett 2013; 329: 74-83.
42. Ozen E, Gozukizil A, Erdal E, Uren A, Bottaro DP, Atabey N. Heparin inhibits Hepatocyte Growth Factor induced motility and invasion of hepatocellular carcinoma cells through early growth response protein 1. PLoS ONE 2012; 7: e42717.
43. Bean J, Brennan C, Shih JY et al. MET amplification occurs with or without T790M mutations in EGFR mutant lung tumors with acquired resistance to gefitinib or erlotinib. Proc Natl Acad Sci 2007; 104: 20932-7.
44. Engelman JA, Zejnullahu K, Mitsudomi T et al. MET amplification leads to gefitinib resistance in lung cancer by activating ERBB3 signaling. Science 2007; 316: 1039-43.
45. Yano S, Wang W, Li Q et al. Hepatocyte growth factor induces gefitinib resistance of lung adenocarcinoma with epidermal growth factor receptor-activating mutations. Cancer Res 2008; 68: 9479-87.
46. Yano S, Yamada T, Takeuchi S et al. Hepatocyte growth factor expression in EGFR mutant lung cancer with intrinsic and acquired resistance to tyrosine kinase inhibitors in a Japanese cohort. J Thorac Oncol 2011; 6: 2011-7.
47. Shattuck DL, Miller JK, Carraway KL 3rd, Sweeney C. Met receptor contributes to trastuzumab resistance of Her2-overexpressing breast cancer cells. Cancer Res 2008; 68: 1471-7.
48. Minuti G, Cappuzzo F, Duchnowska R et al. Increased MET and HGF gene copy numbers are associated with trastuzumab failure in HER2-positive metastatic breast cancer. Br J Cancer 2012; 107: 793-9.
49. 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.
50. Paez-Ribes M, Allen E, Hudock J et al. Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis. Cancer Cell 2009; 15: 220-31.
51. Straussman R, Morikawa T, Shee K et al. Tumour micro-environment elicits innate resistance to RAF inhibitors through HGF secretion. Nature 2012; 487: 500-4.
52. Wilson TR, Fridlyand J, Yan Y et al. Widespread potential for growth-factor-driven resistance to anticancer kinase inhibitors. Nature 2012; 487: 505-9.
53. Xiang Q, Chen W, Ren M et al. Cabozantinib suppresses tumor growth and metastasis in hepatocellular carcinoma by a dual blockade of VEGFR2 and MET. Clin Cancer Res 2014; 20: 2959-70.
54. Jiang X, Feng K, Zhang Y et al. Sorafenib and DE605, a novel c-Met inhibitor, synergistically suppress hepatocellular carcinoma. Oncotarget 2015; 6: 12340-56.
55. Kentsis A, Reed C, Rice KL et al. Autocrine activation of the MET receptor tyrosine kinase in acute myeloid leukemia. Nat Med 2012; 18: 1118-22.
56. Xie Q, Bradley R, Kang L et al. Hepatocyte growth factor (HGF) autocrine activation predicts sensitivity to MET inhibition in glioblastoma. Proc Natl Acad Sci 2012; 109: 570-5.
57. Pennacchietti S, Cazzanti M, Bertotti A et al. Microenvironment-derived HGF overcomes genetically determined sensitivity to anti-MET drugs. Cancer Res 2014; 74: 6598-609.