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PMID: 28862760 Published · ppublish English Journal Article Review

Recent developments of c-Met as a therapeutic target in hepatocellular carcinoma.

Hepatology (Baltimore, Md.) ·Vol. 67 ·No. 3 ·2018-00-00 ·Pages 1132-1149

Bouattour M, Raymond E, Qin S, Cheng AL, Stammberger U, Locatelli G, Faivre S

Abstract

Aberrant c-Met activity has been implicated in the development of hepatocellular carcinoma (HCC), suggesting that c-Met inhibition may have therapeutic potential. However, clinical trials of nonselective kinase inhibitors with c-Met activity (tivantinib, cabozantinib, foretinib, and golvatinib) in patients with HCC have failed so far to demonstrate significant efficacy. This lack of observed efficacy is likely due to several factors, including trial design, lack of patient selection according to tumor c-Met status, and the prevalent off-target activity of these agents, which may indicate that c-Met inhibition is incomplete. In contrast, selective c-Met inhibitors (tepotinib, capmatinib) can be dosed at a level predicted to achieve complete inhibition of tumor c-Met activity. Moreover, results from early trials can be used to optimize the design of clinical trials of these agents. Preliminary results suggest that selective c-Met inhibitors have antitumor activity in HCC, with acceptable safety and tolerability in patients with Child-Pugh A liver function. Ongoing trials have been designed to assess the efficacy and safety of selective c-Met inhibition compared with standard therapy in patients with HCC that were selected based on tumor c-Met status. Thus, c-Met inhibition continues to be an active area of research in HCC, with well-designed trials in progress to investigate the benefit of selective c-Met inhibitors. (Hepatology 2018;67:1132-1149).

MeSH Terms
Antineoplastic Agents/adverse effects,therapeutic use Carcinoma, Hepatocellular/drug therapy Humans Liver/metabolism,pathology Liver Neoplasms/drug therapy Molecular Targeted Therapy/adverse effects,methods Protein Kinase Inhibitors/adverse effects,therapeutic use Proto-Oncogene Proteins c-met/antagonists & inhibitors Signal Transduction/drug effects
Chemicals
Antineoplastic Agents Protein Kinase Inhibitors Proto-Oncogene Proteins c-met
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Bouattour Mohamed ORCID
Digestive Oncology Department, Beaujon University Hospital, Clichy, France.
Raymond Eric
Oncology Unit, Groupe Hospitalier Paris Saint Joseph, Paris, France.
Qin Shukui
Medical Oncology Department, Nanjing Bayi Hospital, Nanjing, China.
Cheng Ann-Lii
National Taiwan University Hospital, Taipei, Taiwan, ROC.
Stammberger Uz
Merck KGaA, Darmstadt, Germany.
Locatelli Giuseppe
Merck KGaA, Darmstadt, Germany.
Faivre Sandrine
Medical Oncology Department, Beaujon University Hospital, Clichy, France.
References (76)
76 references, click to expand
  1. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012.
    Int J Cancer. 2015 Mar 1;136(5):E359-86 PMID: 25220842
  2. Expression of hepatocyte growth factor (HGF) and HGF receptor (c-met) proteins in liver diseases: an immunohistochemical study.
    Liver. 1999 Apr;19(2):151-9 PMID: 10220746
  3. c-Met as a Target for Personalized Therapy.
    Transl Oncogenomics. 2015 Nov 23;7(Suppl 1):13-31 PMID: 26628860
  4. c-Met represents a potential therapeutic target for personalized treatment in hepatocellular carcinoma.
    Hepatology. 2011 Sep 2;54(3):879-89 PMID: 21618573
  5. Development of molecularly targeted therapies in hepatocellular carcinoma: where do we go now?
    Clin Cancer Res. 2010 Jan 15;16(2):390-7 PMID: 20068087
  6. Targeting the HGF/c-MET pathway in hepatocellular carcinoma.
    Clin Cancer Res. 2013 May 1;19(9):2310-8 PMID: 23388504
  7. Volitinib, a potent and highly selective c-Met inhibitor, effectively blocks c-Met signaling and growth in c-MET amplified gastric cancer patient-derived tumor xenograft models.
    Mol Oncol. 2015 Jan;9(1):323-33 PMID: 25248999
  8. Population pharmacokinetic analysis from phase I and phase II studies of the humanized monovalent antibody, onartuzumab (MetMAb), in patients with advanced solid tumors.
    J Clin Pharmacol. 2013 Nov;53(11):1103-11 PMID: 23922054
  9. [Effects of c-met-siRNA on the growth and invasion of hepatocellular carcinoma MHCC97-H cells].
    Zhonghua Gan Zang Bing Za Zhi. 2006 Jul;14(7):499-504 PMID: 16867270
  10. A novel kinase inhibitor, INCB28060, blocks c-MET-dependent signaling, neoplastic activities, and cross-talk with EGFR and HER-3.
    Clin Cancer Res. 2011 Nov 15;17 (22):7127-38 PMID: 21918175
  11. Tivantinib for second-line treatment of advanced hepatocellular carcinoma: a randomised, placebo-controlled phase 2 study.
    Lancet Oncol. 2013 Jan;14(1):55-63 PMID: 23182627
  12. Trends in the development of MET inhibitors for hepatocellular carcinoma.
    Future Oncol. 2016 May;12 (10 ):1275-86 PMID: 26984595
  13. Angiogenesis and the tumor microenvironment: vascular endothelial growth factor and beyond.
    Semin Oncol. 2014 Apr;41(2):235-51 PMID: 24787295
  14. Cabozantinib (XL184), a novel MET and VEGFR2 inhibitor, simultaneously suppresses metastasis, angiogenesis, and tumor growth.
    Mol Cancer Ther. 2011 Dec;10(12):2298-308 PMID: 21926191
  15. Cross-talk between RON receptor tyrosine kinase and other transmembrane receptors.
    Histol Histopathol. 2001 Apr;16(2):623-31 PMID: 11332718
  16. The c-Met Inhibitor MSC2156119J Effectively Inhibits Tumor Growth in Liver Cancer Models.
    Cancers (Basel). 2014 Aug 19;6(3):1736-52 PMID: 25256830
  17. Molecular changes in hepatic metabolism and transport in cirrhosis and their functional importance.
    World J Gastroenterol. 2016 Jan 7;22(1):72-88 PMID: 26755861
  18. Somatic mutations in the kinase domain of the Met/hepatocyte growth factor receptor gene in childhood hepatocellular carcinomas.
    Cancer Res. 1999 Jan 15;59(2):307-10 PMID: 9927037
  19. How do mechanisms of hepatocarcinogenesis (HBV, HCV, and NASH) affect our understanding and approach to HCC?
    Am Soc Clin Oncol Educ Book. 2013;:null PMID: 23714479
  20. Stem cell and hepatocyte proliferation in hepatitis C cirrhosis and hepatocellular carcinoma: transplant implications.
    Ann Hepatol. 2013 Jan-2014 Feb;13(1):45-53 PMID: 24378265
  21. Phase 1 trial of tivantinib in combination with sorafenib in adult patients with advanced solid tumors.
    Invest New Drugs. 2015 Feb;33(1):159-68 PMID: 25294187
  22. Novel therapeutic inhibitors of the c-Met signaling pathway in cancer.
    Clin Cancer Res. 2009 Apr 1;15(7):2207-14 PMID: 19318488
  23. Foretinib (GSK1363089), a multi-kinase inhibitor of MET and VEGFRs, inhibits growth of gastric cancer cell lines by blocking inter-receptor tyrosine kinase networks.
    Invest New Drugs. 2012 Aug;30(4):1352-60 PMID: 21655918
  24. Molecular Targeted Therapy for Hepatocellular Carcinoma: Present Status and Future Directions.
    Biol Pharm Bull. 2015;38(7):986-91 PMID: 26133708
  25. ARQ 197, a novel and selective inhibitor of the human c-Met receptor tyrosine kinase with antitumor activity.
    Mol Cancer Ther. 2010 Jun;9(6):1544-53 PMID: 20484018
  26. Knockdown of c-Met by adenovirus-delivered small interfering RNA inhibits hepatocellular carcinoma growth in vitro and in vivo.
    Mol Cancer Ther. 2005 Oct;4(10):1577-84 PMID: 16227408
  27. Hypoxia promotes invasive growth by transcriptional activation of the met protooncogene.
    Cancer Cell. 2003 Apr;3(4):347-61 PMID: 12726861
  28. Targeting MET in cancer: rationale and progress.
    Nat Rev Cancer. 2012 Jan 24;12(2):89-103 PMID: 22270953
  29. Cabozantinib suppresses tumor growth and metastasis in hepatocellular carcinoma by a dual blockade of VEGFR2 and MET.
    Clin Cancer Res. 2014 Jun 1;20(11):2959-70 PMID: 24700742
  30. Sorafenib in advanced hepatocellular carcinoma.
    N Engl J Med. 2008 Jul 24;359(4):378-90 PMID: 18650514
  31. MET inhibitors for treatment of advanced hepatocellular carcinoma: A review.
    World J Gastroenterol. 2015 May 14;21(18):5445-53 PMID: 25987766
  32. Phase I study of tivantinib in Japanese patients with advanced hepatocellular carcinoma: Distinctive pharmacokinetic profiles from other solid tumors.
    Cancer Sci. 2015 May;106(5):611-7 PMID: 25711511
  33. Advances in the study of molecularly targeted agents to treat hepatocellular carcinoma.
    Drug Discov Ther. 2014 Aug;8(4):154-64 PMID: 25262594
  34. Hepatocyte growth factor: A regulator of inflammation and autoimmunity.
    Autoimmun Rev. 2015 Apr;14(4):293-303 PMID: 25476732
  35. Integrative biomarker analyses indicate etiological variations in hepatocellular carcinoma.
    J Hepatol. 2016 Aug;65(2):296-304 PMID: 27130844
  36. Met provides essential signals for liver regeneration.
    Proc Natl Acad Sci U S A. 2004 Jul 20;101(29):10608-13 PMID: 15249655
  37. Hallmarks of cancer: the next generation.
    Cell. 2011 Mar 4;144(5):646-74 PMID: 21376230
  38. Sorafenib: complexities of Raf-dependent and Raf-independent signaling are now unveiled.
    Med Mol Morphol. 2011 Dec;44(4):183-9 PMID: 22179180
  39. A Phase I/II Multicenter Study of Single-Agent Foretinib as First-Line Therapy in Patients with Advanced Hepatocellular Carcinoma.
    Clin Cancer Res. 2017 May 15;23 (10 ):2405-2413 PMID: 27821605
  40. Activation of MET via diverse exon 14 splicing alterations occurs in multiple tumor types and confers clinical sensitivity to MET inhibitors.
    Cancer Discov. 2015 Aug;5(8):850-9 PMID: 25971938
  41. Actionable gene expression-based patient stratification for molecular targeted therapy in hepatocellular carcinoma.
    PLoS One. 2013 Jun 13;8(6):e64260 PMID: 23785399
  42. Seminars in clinical pharmacology: an introduction to MET inhibitors for the medical oncologist.
    Ann Oncol. 2013 Jan;24(1):14-20 PMID: 23110808
  43. Hepatocyte growth factor twenty years on: Much more than a growth factor.
    J Gastroenterol Hepatol. 2011 Jan;26 Suppl 1:188-202 PMID: 21199531
  44. Tivantinib (ARQ 197) exhibits antitumor activity by directly interacting with tubulin and overcomes ABC transporter-mediated drug resistance.
    Mol Cancer Ther. 2014 Dec;13(12):2978-90 PMID: 25313010
  45. Potential molecular, cellular and microenvironmental mechanism of sorafenib resistance in hepatocellular carcinoma.
    Cancer Lett. 2015 Oct 10;367(1):1-11 PMID: 26170167
  46. Met activation and receptor dimerization in cancer: a role for the Sema domain.
    Cell Cycle. 2005 May;4(5):683-5 PMID: 15846105
  47. Sunitinib in hepatocellular carcinoma: redefining appropriate dosing, schedule, and activity end points.
    J Clin Oncol. 2009 Dec 10;27(35):e248-50; author reply e251-2 PMID: 19901099
  48. Immune Checkpoint Inhibition in Hepatocellular Carcinoma: Basics and Ongoing Clinical Trials.
    Oncology. 2017;92 Suppl 1:50-62 PMID: 28147363
  49. Foretinib demonstrates anti-tumor activity and improves overall survival in preclinical models of hepatocellular carcinoma.
    Angiogenesis. 2012 Mar;15(1):59-70 PMID: 22187171
  50. Relationship between the proliferative capability of hepatocytes and the intrahepatic expression of hepatocyte growth factor and c-Met in the course of cirrhosis development in rats.
    Int J Mol Med. 2006 May;17(5):857-64 PMID: 16596271
  51. A survey of c-MET expression and amplification in 287 patients with hepatocellular carcinoma.
    Anticancer Res. 2013 Nov;33(11):5179-86 PMID: 24222167
  52. GSK3 alpha and beta are new functionally relevant targets of tivantinib in lung cancer cells.
    ACS Chem Biol. 2014 Feb 21;9(2):353-8 PMID: 24215125
  53. Met as a therapeutic target in HCC: facts and hopes.
    J Hepatol. 2014 Feb;60(2):442-52 PMID: 24045150
  54. Invasive growth: a MET-driven genetic programme for cancer and stem cells.
    Nat Rev Cancer. 2006 Aug;6(8):637-45 PMID: 16862193
  55. Preclinical Evaluation of AMG 337, a Highly Selective Small Molecule MET Inhibitor, in Hepatocellular Carcinoma.
    Mol Cancer Ther. 2016 Jun;15(6):1227-37 PMID: 27196749
  56. Integrative transcriptome analysis reveals common molecular subclasses of human hepatocellular carcinoma.
    Cancer Res. 2009 Sep 15;69(18):7385-92 PMID: 19723656
  57. A Phase-1b study of tivantinib (ARQ 197) in adult patients with hepatocellular carcinoma and cirrhosis.
    Br J Cancer. 2013 Jan 15;108(1):21-4 PMID: 23287988
  58. MET signalling: principles and functions in development, organ regeneration and cancer.
    Nat Rev Mol Cell Biol. 2010 Dec;11(12):834-48 PMID: 21102609
  59. HIF-1, O(2), and the 3 PHDs: how animal cells signal hypoxia to the nucleus.
    Cell. 2001 Oct 5;107(1):1-3 PMID: 11595178
  60. LY2875358, a neutralizing and internalizing anti-MET bivalent antibody, inhibits HGF-dependent and HGF-independent MET activation and tumor growth.
    Clin Cancer Res. 2014 Dec 1;20(23):6059-70 PMID: 25231402
  61. E7050: a dual c-Met and VEGFR-2 tyrosine kinase inhibitor promotes tumor regression and prolongs survival in mouse xenograft models.
    Cancer Sci. 2010 Jan;101(1):210-5 PMID: 19832844
  62. Survival rate in patients with hepatocellular carcinoma: a retrospective analysis of 389 patients.
    Br J Cancer. 2005 May 23;92(10):1862-8 PMID: 15870713
  63. Negative Trials for Foreseeable Safety Reasons in Advanced Hepatocellular Carcinoma: How Long Are We Going to Take Lightly Pharmacokinetics of Tyrosine Kinase Inhibitors?
    J Clin Oncol. 2015 Aug 1;33(22):2484-5 PMID: 26033820
  64. EMD 1214063 and EMD 1204831 constitute a new class of potent and highly selective c-Met inhibitors.
    Clin Cancer Res. 2013 Jun 1;19(11):2941-51 PMID: 23553846
  65. Association between serum hepatocyte growth factor and survival in untreated hepatocellular carcinoma.
    J Gastroenterol. 2004 Dec;39(12):1182-8 PMID: 15622483
  66. Synergistic effects of foretinib with HER-targeted agents in MET and HER1- or HER2-coactivated tumor cells.
    Mol Cancer Ther. 2011 Mar;10(3):518-30 PMID: 21252284
  67. Regorafenib for patients with hepatocellular carcinoma who progressed on sorafenib treatment (RESORCE): a randomised, double-blind, placebo-controlled, phase 3 trial.
    Lancet. 2017 Jan 7;389(10064):56-66 PMID: 27932229
  68. Hepatocellular carcinoma: epidemiology and molecular carcinogenesis.
    Gastroenterology. 2007 Jun;132(7):2557-76 PMID: 17570226
  69. Ligand-independent activation of MET through IGF-1/IGF-1R signaling.
    Int J Cancer. 2013 Oct 1;133(7):1536-46 PMID: 23526299
  70. Comprehensive multiplatform biomarker analysis of 350 hepatocellular carcinomas identifies potential novel therapeutic options.
    J Surg Oncol. 2016 Jan;113(1):55-61 PMID: 26661118
  71. Phase 1 dose-escalation trial evaluating the combination of the selective MET (mesenchymal-epithelial transition factor) inhibitor tivantinib (ARQ 197) plus erlotinib.
    Cancer. 2012 Dec 1;118(23):5903-11 PMID: 22605616
  72. Pathophysiology of Liver Fibrosis.
    Dig Dis. 2015;33(4):492-7 PMID: 26159264
  73. Hepatocellular Carcinoma: Risk Factors, Diagnosis and Treatment.
    Open Access Maced J Med Sci. 2015 Dec 15;3(4):732-6 PMID: 27275318
  74. Targeting the HGF/Met signaling pathway in cancer therapy.
    Expert Opin Ther Targets. 2012 Jun;16(6):553-72 PMID: 22530990
  75. Gene expressions of c-met and hepatocyte growth factor in chronic liver disease and hepatocellular carcinoma.
    J Hepatol. 1996 Mar;24(3):286-92 PMID: 8778194
  76. Loss of c-Met accelerates development of liver fibrosis in response to CCl(4) exposure through deregulation of multiple molecular pathways.
    Biochim Biophys Acta. 2012 Jun;1822(6):942-51 PMID: 22386877
Article Info
Journal
Hepatology (Baltimore, Md.)
Abbr.
Hepatology
ISSN
1527-3350
Published
2018-00-00
Epub
2018-00-01
Pages
1132-1149
Language
English
Region
United States
NLM ID
8302946
PMCID
PMC5873445
Subset
IM
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