Dysregulation of the Met pathway in non-small cell lung cancer: Implications for drug targeting and resistance

Translational Lung Cancer Research

Volumn 4, Issue 3, 2015, Pages 242-252

  Sacco, Joseph J ^a   Clague, Michael J ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

Epidermal growth factor receptor (EGFR); Hepatocyte growth factor (HGF); Lung cancer; Met; Non small cell lung cancer (NSCLC)

Indexed keywords

CBL PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR 3; MONOCLONAL ANTIBODY; SCATTER FACTOR RECEPTOR;

DRUG TARGETING; EXON; GENE AMPLIFICATION; GENE MUTATION; HUMAN; NON SMALL CELL LUNG CANCER; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; PROTEIN STRUCTURE; PROTEIN TARGETING; REVIEW; SIGNAL TRANSDUCTION;

EID: 84960078071     PISSN: 22186751     EISSN: 22264477     Source Type: Journal    
DOI: 10.3978/j.issn.2218-6751.2015.03.05     Document Type: Review

References (90)

1. Black A, Morris D. Personalized medicine in metastatic non-small-cell lung cancer: promising targets and current clinical trials. Curr Oncol 2012;19:S73-85
2. Bos M, Gardizi M, Schildhaus HU, et al. Activated RET and ROS: two new driver mutations in lung adenocarcinoma. Transl Lung Cancer Res 2013;2:112-21
3. Shaw AT, Ou SH, Bang YJ, et al. Crizotinib in ROS1- rearranged non-small-cell lung cancer. N Engl J Med 2014;371:1963-71
4. Cooper CS, Park M, Blair DG, et al. Molecular cloning of a new transforming gene from a chemically transformed human cell line. Nature 1984;311:29-33
5. Birchmeier C, Birchmeier W, Gherardi E, et al. Met, metastasis, motility and more. Nat Rev Mol Cell Biol 2003;4:915-25
6. Schmidt L, Duh FM, Chen F, et al. Germline and somatic mutations in the tyrosine kinase domain of the MET proto-oncogene in papillary renal carcinomas. Nat Genet 1997;16:68-73
7. Olivero M, Rizzo M, Madeddu R, et al. Overexpression and activation of hepatocyte growth factor/scatter factor in human non-small-cell lung carcinomas. Br J Cancer 1996;74:1862-8
8. Ma PC, Jagadeeswaran R, Jagadeesh S, et al. Functional expression and mutations of c-Met and its therapeutic inhibition with SU11274 and small interfering RNA in non-small cell lung cancer. Cancer Res 2005;65:1479-88
9. Ma PC, Tretiakova MS, MacKinnon AC, et al. Expression and mutational analysis of MET in human solid cancers. Genes Chromosomes Cancer 2008;47:1025-37
10. Ichimura E, Maeshima A, Nakajima T, et al. Expression of c-met/HGF receptor in human non-small cell lung carcinomas in vitro and in vivo and its prognostic significance. Jpn J Cancer Res 1996;87:1063-9
11. Nakamura Y, Niki T, Goto A, et al. c-Met activation in lung adenocarcinoma tissues: an immunohistochemical analysis. Cancer Sci 2007;98:1006-13
12. Tsuta K, Kozu Y, Mimae T, et al. c-MET/phospho-MET protein expression and MET gene copy number in nonsmall cell lung carcinomas. J Thorac Oncol 2012;7:331-9
13. Cancer Genome Atlas Research Network. Comprehensive molecular profiling of lung adenocarcinoma. Nature 2014;511:543-50
14. 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 U S A 2007;104:20932-7
15. Go H, Jeon YK, Park HJ, et al. High MET gene copy number leads to shorter survival in patients with non-small cell lung cancer. J Thorac Oncol 2010;5:305-13
16. Onozato R, Kosaka T, Kuwano H, et al. Activation of MET by gene amplification or by splice mutations deleting the juxtamembrane domain in primary resected lung cancers. J Thorac Oncol 2009;4:5-11
17. Seo JS, Ju YS, Lee WC, et al. The transcriptional landscape and mutational profile of lung adenocarcinoma. Genome Res 2012;22:2109-19
18. 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
19. Cui JJ. Targeting receptor tyrosine kinase MET in cancer: small molecule inhibitors and clinical progress. J Med Chem 2014;57:4427-53
20. Gherardi E, Birchmeier W, Birchmeier C, et al. Targeting MET in cancer: rationale and progress. Nat Rev Cancer 2012;12:89-103
21. McDermott U, Sharma SV, Dowell L, et al. Identification of genotype-correlated sensitivity to selective kinase inhibitors by using high-throughput tumor cell line profiling. Proc Natl Acad Sci U S A 2007;104:19936-41
22. Spigel DR, Edelman MJ, O'Byrne K, et al. Onartuzumab plus erlotinib versus erlotinib in previously treated stage IIIb or IV NSCLC: Results from the pivotal phase III randomized, multicenter, placebo-controlled METLung (OAM4971g) global trial. J Clin Oncol 2014;abstr 8000
23. Azuma K, Yoshioka H, Yamamoto N, et al. Tivantinib plus erlotinib versus placebo plus erlotinib in Asian patients with previously treated nonsquamous NSCLC with wildtype EGFR: First report of a phase III ATTENTION trial. J Clin Oncol 2014;abstr 8044
24. ESMO News. Available online: http://www.esmo.org/ Conferences/Past-Conferences/European-Cancer- Congress-2013/News/A-Phase-III-Study-of-Tivantinib- Plus-Erlotinib-Did-Not-Meet-a-Primary-Endpointin- Patients-with-Locally-advanced-or-Metastatic-Nonsquamous- NSCLC, accessed on Jan 22, 2015
25. Camidge DR, Ou SI, Shapiro G, et al. Efficacy and safety of crizotinib in patients with advanced c-MET-amplified non-small cell lung cancer (NSCLC). J Clin Oncol 2014;abstr 8001
26. Koeppen H, Rost S, Yauch RL. Developing biomarkers to predict benefit from HGF/MET pathway inhibitors. J Pathol 2014;232:210-8
27. Naldini L, Tamagnone L, Vigna E, et al. Extracellular proteolytic cleavage by urokinase is required for activation of hepatocyte growth factor/scatter factor. EMBO J 1992;11:4825-33
28. Lokker NA, Mark MR, Luis EA, et al. Structure-function analysis of hepatocyte growth factor: identification of variants that lack mitogenic activity yet retain high affinity receptor binding. EMBO J 1992;11:2503-10
29. Niemann HH. Structural insights into Met receptor activation. Eur J Cell Biol 2011;90:972-81
30. Weidner KM, Di Cesare S, Sachs M, et al. Interaction between Gab1 and the c-Met receptor tyrosine kinase is responsible for epithelial morphogenesis. Nature 1996;384:173-6
31. Schaeper U, Gehring NH, Fuchs KP, et al. Coupling of Gab1 to c-Met, Grb2, and Shp2 mediates biological responses. J Cell Biol 2000;149:1419-32
32. Rodrigues GA, Falasca M, Zhang Z, et al. A novel positive feedback loop mediated by the docking protein Gab1 and phosphatidylinositol 3-kinase in epidermal growth factor receptor signaling. Mol Cell Biol 2000;20:1448-59
33. Gual P, Giordano S, Williams TA, et al. Sustained recruitment of phospholipase C-gamma to Gab1 is required for HGF-induced branching tubulogenesis. Oncogene 2000;19:1509-18
34. Maroun CR, Naujokas MA, Holgado-Madruga M, et al. The tyrosine phosphatase SHP-2 is required for sustained activation of extracellular signal-regulated kinase and epithelial morphogenesis downstream from the met receptor tyrosine kinase. Mol Cell Biol 2000;20:8513-25
35. Rosário M, Birchmeier W. How to make tubes: signaling by the Met receptor tyrosine kinase. Trends Cell Biol 2003;13:328-35
36. Kermorgant S, Parker PJ. Receptor trafficking controls weak signal delivery: a strategy used by c-Met for STAT3 nuclear accumulation. J Cell Biol 2008;182:855-63
37. Lee YY, Kim HP, Kang MJ, et al. Phosphoproteomic analysis identifies activated MET-axis PI3K/AKT and MAPK/ERK in lapatinib-resistant cancer cell line. Exp Mol Med 2013;45:e64
38. Clague MJ. Met receptor: a moving target. Sci Signal 2011;4:pe40
39. Hammond DE, Urbé S, Vande Woude GF, et al. Downregulation of MET, the receptor for hepatocyte growth factor. Oncogene 2001;20:2761-70
40. Hammond DE, Carter S, McCullough J, et al. Endosomal dynamics of Met determine signaling output. Mol Biol Cell 2003;14:1346-54
41. Abella JV, Peschard P, Naujokas MA, et al. Met/ Hepatocyte growth factor receptor ubiquitination suppresses transformation and is required for Hrs phosphorylation. Mol Cell Biol 2005;25:9632-45
42. Peschard P, Fournier TM, Lamorte L, et al. Mutation of the c-Cbl TKB domain binding site on the Met receptor tyrosine kinase converts it into a transforming protein. Mol Cell 2001;8:995-1004
43. Barrow R, Joffre C, Ménard L, et al. Measuring the role for Met endosomal signaling in tumorigenesis. Methods Enzymol 2014;535:121-40
44. Kong-Beltran M, Seshagiri S, Zha J, et al. Somatic mutations lead to an oncogenic deletion of met in lung cancer. Cancer Res 2006;66:283-9
45. Cancer Genome Atlas Research Network. Comprehensive genomic characterization of squamous cell lung cancers. Nature 2012;489:519-25
46. Gao J, Aksoy BA, Dogrusoz U, et al. Integrative analysis of complex cancer genomics and clinical profiles using the cBioPortal. Sci Signal 2013;6:pl1
47. 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
48. Kubo T, Yamamoto H, Lockwood WW, et al. MET gene amplification or EGFR mutation activate MET in lung cancers untreated with EGFR tyrosine kinase inhibitors. Int J Cancer 2009;124:1778-84
49. Tanizaki J, Okamoto I, Sakai K, et al. Differential roles of trans-phosphorylated EGFR, HER2, HER3, and RET as heterodimerisation partners of MET in lung cancer with MET amplification. Br J Cancer 2011;105:807-13
50. Tanizaki J, Okamoto I, Okamoto K, et al. MET tyrosine kinase inhibitor crizotinib (PF-02341066) shows differential antitumor effects in non-small cell lung cancer according to MET alterations. J Thorac Oncol 2011;6:1624-31
51. Joffre C, Barrow R, Ménard L, et al. A direct role for Met endocytosis in tumorigenesis. Nat Cell Biol 2011;13:827-37
52. Tengs T, Lee JC, Paez JG, et al. A transforming MET mutation discovered in non-small cell lung cancer using microarray-based resequencing. Cancer Lett 2006;239:227-33
53. Krishnaswamy S, Kanteti R, Duke-Cohan JS, et al. Ethnic differences and functional analysis of MET mutations in lung cancer. Clin Cancer Res 2009;15:5714-23
54. Tyner JW, Fletcher LB, Wang EQ, et al. MET receptor sequence variants R970C and T992I lack transforming capacity. Cancer Res 2010;70:6233-7
55. Acunzo M, Romano G, Palmieri D, et al. Cross-talk between MET and EGFR in non-small cell lung cancer involves miR-27a and Sprouty2. Proc Natl Acad Sci U S A 2013;110:8573-8
56. Heegaard NH, Schetter AJ, Welsh JA, et al. Circulating micro-RNA expression profiles in early stage nonsmall cell lung cancer. Int J Cancer 2012;130:1378-86
57. Luo W, Huang B, Li Z, et al. MicroRNA-449a is downregulated in non-small cell lung cancer and inhibits migration and invasion by targeting c-Met. PLoS One 2013;8:e64759
58. Lee JM, Yoo JK, Yoo H, et al. The novel miR-7515 decreases the proliferation and migration of human lung cancer cells by targeting c-Met. Mol Cancer Res 2013;11:43-53
59. Jiang C, Chen H, Shao L, et al. MicroRNA-1 functions as a potential tumor suppressor in osteosarcoma by targeting Med1 and Med31. Oncol Rep 2014;32:1249-56
60. Huang J, Dong B, Zhang J, et al. miR-199a-3p inhibits hepatocyte growth factor/c-Met signaling in renal cancer carcinoma. Tumour Biol 2014;35:5833-43
61. Takeyama H, Yamamoto H, Yamashita S, et al. Decreased miR-340 expression in bone marrow is associated with liver metastasis of colorectal cancer. Mol Cancer Ther 2014;13:976-85
62. Menges CW, Kadariya Y, Altomare D, et al. Tumor suppressor alterations cooperate to drive aggressive mesotheliomas with enriched cancer stem cells via a p53- miR-34a-c-Met axis. Cancer Res 2014;74:1261-71
63. Yang X, Zhang XF, Lu X, et al. MicroRNA-26a suppresses angiogenesis in human hepatocellular carcinoma by targeting hepatocyte growth factor-cMet pathway. Hepatology 2014;59:1874-85
64. Hagman Z, Haflidadottir BS, Ansari M, et al. The tumour suppressor miR-34c targets MET in prostate cancer cells. Br J Cancer 2013;109:1271-8
65. Xu X, Chen H, Lin Y, et al. MicroRNA-409-3p inhibits migration and invasion of bladder cancer cells via targeting c-Met. Mol Cells 2013;36:62-8
66. Hu Z, Lin Y, Chen H, et al. MicroRNA-101 suppresses motility of bladder cancer cells by targeting c-Met. Biochem Biophys Res Commun 2013;435:82-7
67. Wang LG, Ni Y, Su BH, et al. MicroRNA-34b functions as a tumor suppressor and acts as a nodal point in the feedback loop with Met. Int J Oncol 2013;42:957-62
68. Luo C, Tetteh PW, Merz PR, et al. miR-137 inhibits the invasion of melanoma cells through downregulation of multiple oncogenic target genes. J Invest Dermatol 2013;133:768-75
69. Chen L, Zhang J, Feng Y, et al. MiR-410 regulates MET to influence the proliferation and invasion of glioma. Int J Biochem Cell Biol 2012;44:1711-7
70. Buurman R, Gürlevik E, Schäffer V, et al. Histone deacetylases activate hepatocyte growth factor signaling by repressing microRNA-449 in hepatocellular carcinoma cells. Gastroenterology 2012;143:811-20
71. Yan K, Gao J, Yang T, et al. MicroRNA-34a inhibits the proliferation and metastasis of osteosarcoma cells both in vitro and in vivo. PLoS One 2012;7:e33778
72. Dong F, Lou D. MicroRNA-34b/c suppresses uveal melanoma cell proliferation and migration through multiple targets. Mol Vis 2012;18:537-46
73. Reid JF, Sokolova V, Zoni E, et al. miRNA profiling in colorectal cancer highlights miR-1 involvement in METdependent proliferation. Mol Cancer Res 2012;10:504-15
74. Tsuruta T, Kozaki K, Uesugi A, et al. miR-152 is a tumor suppressor microRNA that is silenced by DNA hypermethylation in endometrial cancer. Cancer Res 2011;71:6450-62
75. Bouchie A. First microRNA mimic enters clinic. Nat Biotechnol 2013;31:577
76. Avan A, Quint K, Nicolini F, et al. Enhancement of the antiproliferative activity of gemcitabine by modulation of c-Met pathway in pancreatic cancer. Curr Pharm Des 2013;19:940-50
77. 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
78. Patnaik A, Weiss GJ, Papadopoulos KP, et al. Phase I ficlatuzumab monotherapy or with erlotinib for refractory advanced solid tumours and multiple myeloma. Br J Cancer 2014;111:272-80
79. Wu Y, Yang JC, Kim D, et al. Safety and efficacy of INC280 in combination with gefitinib (gef) in patients with EGFRmutated (mut), MET-positive NSCLC: A single-arm phase lb/ll study. J Clin Oncol 2014; abstr 8017
80. Mok TSK, Park K, Geater SL, et al. A randomized phase (PH) 2 study with exploratory biomarker analysis of ficlatuzumab (F) a humanized hepatocyte growth factor (HGF) inhibitory mAb in combination with gefitinib (G) versus G in Asian patients (pts) with lung adenocarcinoma (LA). ESMO 2012;Abstract 2342
81. Basilico C, Hultberg A, Blanchetot C, et al. Four individually druggable MET hotspots mediate HGFdriven tumor progression. J Clin Invest 2014;124:3172-86
82. Lee JM, Kim B, Lee SB, et al. Cbl-independent degradation of Met: ways to avoid agonism of bivalent Met-targeting antibody. Oncogene 2014;33:34-43
83. Spigel DR, Ervin TJ, Ramlau RA, et al. Randomized phase II trial of Onartuzumab in combination with erlotinib in patients with advanced non-small-cell lung cancer. J Clin Oncol 2013;31:4105-14
84. Chen X, Ding G, Gao Q, et al. A human anti-c-Met Fab fragment conjugated with doxorubicin as targeted chemotherapy for hepatocellular carcinoma. PLoS One 2013;8:e63093
85. Verma S, Miles D, Gianni L, et al. Trastuzumab emtansine for HER2-positive advanced breast cancer. N Engl J Med 2012;367:1783-91
86. Ou SH, Kwak EL, Siwak-Tapp C, et al. Activity of crizotinib (PF02341066), a dual mesenchymal-epithelial transition (MET) and anaplastic lymphoma kinase (ALK) inhibitor, in a non-small cell lung cancer patient with de novo MET amplification. J Thorac Oncol 2011;6:942-6
87. Garber K. MET inhibitors start on road to recovery. Nat Rev Drug Discov 2014;13:563-5
88. Lutterbach B, Zeng Q, Davis LJ, et al. Lung cancer cell lines harboring MET gene amplification are dependent on Met for growth and survival. Cancer Res 2007;67:2081-8
89. Matsubara D, Ishikawa S, Oguni S, et al. Molecular predictors of sensitivity to the MET inhibitor PHA665752 in lung carcinoma cells. J Thorac Oncol 2010;5:1317-24
90. Kim ES, Herbst RS, Wistuba II, et al. The BATTLE trial: personalizing therapy for lung cancer. Cancer Discov 2011;1:44-53.