Microenvironment-derived HGF overcomes genetically determined sensitivity to anti-MET drugs

Cancer Research

Volumn 74, Issue 22, 2014, Pages 6598-6609

  Pennacchietti, Selma ^a,b,c   Cazzanti, Manuela ^a,b   Bertotti, Andrea ^a,b   Rideout, William M ^d   Han, May ^d   Gyuris, Jeno ^d   Perera, Timothy ^e   Comoglio, Paolo M ^a,b   Trusolino, Livio ^a,b   Michieli, Paolo ^a,b  

^a UNIVERSITY OF TURIN   (Italy)

^b CANDIOLO CANCER INSTITUTE   (Italy)

^c UNIVERSITY OF TURIN   (Italy)

^d AVEO ONCOLOGY   (United States)

^e JANSSEN RESEARCH AND DEVELOPMENT   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

5 (2,6 DICHLOROBENZYLSULFONYL) 3 [3,5 DIMETHYL 4 [2 (1 PYRROLIDINYLMETHYL) 1 PYRROLIDINYLCARBONYL] 1H PYRROL 2 YLMETHYLENE] 1,3 DIHYDRO 2H INDOL 2 ONE; CRIZOTINIB; FICLATUZUMAB; JNJ 38877605; MONOCLONAL ANTIBODY; PEGYLATED DN30 F(AB) FRAGMENT; PROTEIN TYROSINE KINASE INHIBITOR; SCATTER FACTOR; SCATTER FACTOR RECEPTOR; UNCLASSIFIED DRUG; EPIDERMAL GROWTH FACTOR RECEPTOR 3; PHOSPHATIDYLINOSITOL 3 KINASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; C MET GENE; CANCER CELL CULTURE; CANCER INHIBITION; CANCER RESISTANCE; CANCER SURVIVAL; CELL VIABILITY; COLORECTAL CARCINOMA; CONTROLLED STUDY; DRUG DOSE COMPARISON; DRUG POTENCY; DRUG POTENTIATION; DRUG SENSITIVITY; DRUG TARGETING; HUMAN; HUMAN CELL; IC50; IN VIVO STUDY; INTRACELLULAR SIGNALING; KNOCKOUT MOUSE; LUNG CARCINOMA; NONHUMAN; PHARMACOGENETICS; STOMACH CARCINOMA; TREATMENT OUTCOME; TUMOR MICROENVIRONMENT; ANIMAL; ANTAGONISTS AND INHIBITORS; MOUSE; PHYSIOLOGY; SCID MOUSE; SIGNAL TRANSDUCTION;

ANIMALS; ANTIBODIES, MONOCLONAL; HEPATOCYTE GROWTH FACTOR; MICE; MICE, SCID; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-MET; RECEPTOR, ERBB-3; SIGNAL TRANSDUCTION; TUMOR MICROENVIRONMENT;

EID: 84918502616     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-14-0761     Document Type: Article

References (45)

1. Comoglio PM, Giordano S, Trusolino L. Drug development of MET inhibitors: targeting oncogene addiction and expedience. Nat Rev Drug Discov 2008;7:504-16.
2. Christensen JG, Schreck R, Burrows J, Kuruganti P, Chan E, Le P, et al. A selective small molecule inhibitor of c-MET kinase inhibits c-METdependent phenotypes in vitro and exhibits cytoreductive antitumor activity in vivo. Cancer Res 2003;63:7345-55.
3. Smolen GA, Sordella R, Muir B, Mohapatra G, Barmettler A, Archibald H, et al. Amplification of MET may identify a subset of cancers with extreme sensitivity to the selective tyrosine kinase inhibitor PHA-665752. Proc Natl Acad Sci US A 2006;103:2316-21.
4. McDermott U, Sharma SV, Dowell L, Greninger P, Montagut C, Lamb J, et al. Identification of genotype-correlated sensitivity to selective kinase inhibitors by using high-throughput tumor cell line profiling. Proc Natl Acad Sci US A 2007;104:19936-41.
5. Lutterbach B, Zeng Q, Davis LJ, Hatch H, Hang G, Kohl NE, et al. Lung cancer cell lines harboring MET gene amplification are dependent on MET for growth and survival. Cancer Res 2007;67:2081-8.
6. Pacchiana G, Chiriaco C, Stella MC, Petronzelli F, De Santis R, Galluzzo M, et al. Monovalency unleashes the full therapeutic potential of the DN-30 anti-MET antibody. J Biol Chem 2010;285:36149-57.
7. Basilico C, Pennacchietti S, Vigna E, Chiriaco C, Arena S, Bardelli A, et al. Tivantinib (ARQ197) displays cytotoxic activity that is independent of its ability to bind MET. Clin Cancer Res 2013;19:2381-92.
8. Katayama R, Aoyama A, Yamori T, Qi J, Oh-hara T, Song Y, et al. Cytotoxic activity of tivantinib (ARQ 197) is not due solely to c-MET inhibition. Cancer Res 2013;73:3087-96.
9. De Bacco F, Luraghi P, Medico E, Reato G, Girolami F, Perera T, et al. Induction of MET by ionizing radiation and its role in radioresistance and invasive growth of cancer. J Natl Cancer Inst 2011;103:645-61.
10. Cui JJ, Tran-Dubé M, Shen H, Nambu M, Kung PP, Pairish M, et al. Structure based drug design of crizotinib (PF-02341066), a potent and selective dual inhibitor of mesenchymal-epithelial transition factor (c-MET) kinase and anaplastic lymphoma kinase (ALK). J Med Chem 2011;54:6342-63.
11. Ou SH, Kwak EL, Siwak-Tapp C, Dy J, Bergethon K, Clark JW, 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.
12. Lennerz JK, Kwak EL, Ackerman A, Michael M, Fox SB, Bergethon K, et al. MET amplification identifies a small and aggressive subgroup of esophagogastric adenocarcinoma with evidence of responsiveness to crizotinib. J Clin Oncol 2011;29:4803-10.
13. Engelman JA, Zejnullahu K, Mitsudomi T, Song Y, Hyland C, Park JO, et al. MET amplification leads to gefitinib resistance in lung cancer by activating HER3 signaling. Science 2007;316:1039-43.
14. Bean J, Brennan C, Shih JY, Riely G, Viale A, Wang L, 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 US A 2007;104:20932-7.
15. Suda K, Murakami I, Katayama T, Tomizawa K, Osada H, Sekido Y, et al. Reciprocal and complementary role of MET amplification and EGFR T790M mutation in acquired resistance to kinase inhibitors in lung cancer. Clin Cancer Res 2010;16:5489-98.
16. Engelman JA, Jänne PA, Mermel C, Pearlberg J, Mukohara T, Fleet C, et al. ErbB-3 mediates phosphoinositide 3-kinase activity in gefitinibsensitive non-small cell lung cancer cell lines. Proc Natl Acad Sci US A 2005;102:3788-93.
17. Yano S, Wang W, Li Q, Matsumoto K, Sakurama H, Nakamura T, et al. Hepatocyte growth factor induces gefitinib resistance of lung adenocarcinoma with epidermal growth factor receptor-activating mutations. Cancer Res 2008;68:9479-87.
18. Yamada T, Matsumoto K, Wang W, Li Q, Nishioka Y, Sekido Y, et al. Hepatocyte growth factor reduces susceptibility to an irreversible epidermal growth factor receptor inhibitor in EGFR-T790M mutant lung cancer. Clin Cancer Res 2010;16:174-83.
19. Turke AB, Zejnullahu K, Wu YL, Song Y, Dias-Santagata D, Lifshits E, et al. Preexistence and clonal selection of MET amplification in EGFR mutant NSCLC. Cancer Cell 2010;17:77-88.
20. Yano S, Yamada T, Takeuchi S, Tachibana K, Minami Y, Yatabe Y, 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.
21. Han JY, Kim JY, Lee SH, Yoo NJ, Choi BG. Association between plasma hepatocyte growth factor and gefitinib resistance in patients with advanced non-small cell lung cancer. Lung Cancer 2011;74:293-9.
22. Straussman R, Morikawa T, Shee K, Barzily-Rokni M, Qian ZR, Du J, et al. Tumour micro-environment elicits innate resistance to RAF inhibitors through HGF secretion. Nature 2012;487:500-4.
23. Wilson TR, Fridlyand J, Yan Y, Penuel E, Burton L, Chan E, et al. Widespread potential for growth-factor-driven resistance to anticancer kinase inhibitors. Nature 2012;487:505-9.
24. Bertotti A, Burbridge MF, Gastaldi S, Galimi F, Torti D, Medico E, et al. Only a subset of MET-activated pathways are required to sustain oncogene addiction. Sci Signal 2009;2: ra80.
25. D'Arcangelo M, Cappuzzo F. Focus on the potential role of ficlatuzumab in the treatment of non-small cell lung cancer. Biologics 2013;7:61-8.
26. Giordano S, Ponzetto C, Di Renzo MF, Cooper CS, Comoglio PM. Tyrosine kinase receptor indistinguishable from the c-MET protein. Nature 1989;339:155-6.
27. Amendola M, Venneri MA, Biffi A, Vigna E, Naldini L. Coordinate dualgene transgenesis by lentiviral vectors carrying synthetic bidirectional promoters. Nat Biotechnol 2005;23:108-16.
28. Longati P, Bardelli A, Ponzetto C, Naldini L, Comoglio PM. Tyrosines 1234-1235 are critical for activation of the tyrosine kinase encoded by the MET proto-oncogene (HGF receptor). Oncogene 1994;9:49-57.
29. Ruco LP, Ranalli T, Marzullo A, Bianco P, Prat M, Comoglio PM, et al. Expression of Met protein in thyroid tumours. J Pathol 1996;180:266-70.
30. Bardelli A, Corso S, Bertotti A, Hobor S, Valtorta E, Siravegna G, et al. Amplification of the MET receptor drives resistance to anti-EGFR therapies in colorectal cancer. Cancer Discov 2013;3:658-73.
31. Birchmeier C, Birchmeier W, Gherardi E, Vande Woude GF. Met, metastasis, motility and more. Nat Rev Mol Cell Biol 2003;4:915-25.
32. Tamagnone L, Comoglio PM. Control of invasive growth by hepatocyte growth factor (HGF) and related scatter factors. Cytokine Growth Factor Rev 1997;8:129-42.
33. Rong S, Oskarsson M, Faletto D, Tsarfaty I, Resau JH, Nakamura T, et al. Tumorigenesis induced by coexpression of human hepatocyte growth factor and the human met protooncogene leads to high levels of expression of the ligand and receptor. Cell Growth Differ 1993;4:563-9.
34. Zhang YW, Su Y, Lanning N, Gustafson M, Shinomiya N, Zhao P, et al. Enhanced growth of human met-expressing xenografts in a new strain of immunocompromised mice transgenic for human hepatocyte growth factor/scatter factor. Oncogene 2005;24:101-6.
35. Bertotti A, Migliardi G, Galimi F, Sassi F, Torti D, Isella C, et al. A molecularly annotated platform of patient-derived xenografts ("xenopatients") identifies HER2 as an effective therapeutic target in cetuximab-resistant colorectal cancer. Cancer Discov 2011;1:508-23.
36. Lee JM, Kim B, Lee SB, Jeong Y, Oh YM, Song YJ, et al. Cblindependent degradation of MET: ways to avoid agonism of bivalent MET-targeting antibody. Oncogene 2014;33:34-43.
37. Greenall SA, Gherardi E, Liu Z, Donoghue JF, Vitali AA, Li Q, et al. Nonagonistic bivalent antibodies that promote c-MET degradation and inhibit tumor growth and others specific for tumor related c-MET. PLoS One 2012;7:e34658.
38. Michalopoulos GK, De Frances MC. Liver regeneration. Science 1997;276:60-6.
39. Bhowmick NA, Neilson EG, Moses HL. Stromal fibroblasts in cancer initiation and progression. Nature 2004;432:332-7.
40. Nakamura T, Sakai K, Nakamura T, Matsumoto K. Hepatocyte growth factor twenty years on: much more than a growth factor. J Gastroenterol Hepatol 2011;26 Suppl 1:188-202.
41. 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.
42. Owen KA, Qiu D, Alves J, Schumacher AM, Kilpatrick LM, Li J, et al. Pericellular activation of hepatocyte growth factor by the transmembrane serine proteases matriptase and hepsin, but not by the membrane-associated protease uPA. Biochem J 2010;426:219-28.
43. Gordon MS, Sweeney CS, Mendelson DS, Eckhardt SG, Anderson A, Beaupre DM, et al. Safety, pharmacokinetics, and pharmacodynamics of AMG 102, a fully human hepatocyte growth factor-neutralizing monoclonal antibody, in a first-in-human study of patients with advanced solid tumors. Clin Cancer Res 2010;16:699-710.
44. Kim KJ, Wang L, Su YC, Gillespie GY, Salhotra A, Lal B, et al. Systemic anti-hepatocyte growth factor monoclonal antibody therapy induces the regression of intracranial glioma xenografts. Clin Cancer Res 2006;12:1292-8.
45. De Palma M, Hanahan D. The biology of personalized cancer medicine: facing individual complexities underlying hallmark capabilities. Mol Oncol 2012;6:111-27.