Pharmacological inhibition of KIT activates MET signaling in gastrointestinal stromal tumors

Cancer Research

Volumn 75, Issue 10, 2015, Pages 2061-2070

  Cohen, Noah A ^a   Zeng, Shan ^a   Seifert, Adrian M ^a   Kim, Teresa S ^a   Sorenson, Eric C ^a   Greer, Jonathan B ^a   Beckman, Michael J ^a   Santamaria Barria, Juan A ^a   Crawley, Megan H ^a   Green, Benjamin L ^a   Rossi, Ferdinand ^a   Besmer, Peter ^a   Antonescu, Cristina R ^a   DeMatteo, Ronald P ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CABOZANTINIB; CRIZOTINIB; IMATINIB; SCATTER FACTOR RECEPTOR; ANILIDE; ANTINEOPLASTIC AGENT; BENZAMIDE DERIVATIVE; INDOLE DERIVATIVE; MET PROTEIN, HUMAN; PIPERAZINE DERIVATIVE; PYRIDINE DERIVATIVE; PYRIMIDINE DERIVATIVE; PYRROLE DERIVATIVE; STEM CELL FACTOR RECEPTOR; SUNITINIB;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CELL CULTURE; CANCER CELL LINE; CELL POPULATION; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOTOXICITY; DRUG MECHANISM; DRUG POTENTIATION; DRUG SENSITIVITY; DRUG TARGETING; GASTROINTESTINAL STROMAL TUMOR; HUMAN; HUMAN CELL; HUMAN TISSUE; HYPOXEMIA; IN VITRO STUDY; IN VIVO STUDY; KIT GENE; MET GENE; MOUSE; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; RNA INTERFERENCE; TUMOR XENOGRAFT; UPREGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; DRUG EFFECTS; DRUG SCREENING; GASTROINTESTINAL NEOPLASMS; GASTROINTESTINAL STROMAL TUMORS; GENETICS; IC50; METABOLISM; NONOBESE DIABETIC MOUSE; PATHOLOGY; SCID MOUSE; SIGNAL TRANSDUCTION; TUMOR CELL LINE; TUMOR VOLUME;

ANILIDES; ANIMALS; ANTINEOPLASTIC AGENTS; BENZAMIDES; CELL LINE, TUMOR; GASTROINTESTINAL NEOPLASMS; GASTROINTESTINAL STROMAL TUMORS; HUMANS; IMATINIB MESYLATE; INDOLES; INHIBITORY CONCENTRATION 50; MICE, INBRED C57BL; MICE, INBRED NOD; MICE, SCID; PIPERAZINES; PROTO-ONCOGENE PROTEINS C-KIT; PROTO-ONCOGENE PROTEINS C-MET; PYRIDINES; PYRIMIDINES; PYRROLES; SIGNAL TRANSDUCTION; TUMOR BURDEN; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84942857701     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-14-2564     Document Type: Article

References (42)

1. Ducimetiere F, Lurkin A, Ranchere-Vince D, Decouvelaere AV, Peoc'h M, Istier L, et al. Incidence of sarcoma histotypes and molecular subtypes in a prospective epidemiological study with central pathology review and molecular testing. PLoS ONE 2011;6:e20294.
2. Joensuu H, DeMatteo RP. The management of gastrointestinal stromal tumors: a model for targeted and multidisciplinary therapy of malignancy. Annu Rev Med 2012;63:247-58.
3. Hirota S, Isozaki K, Moriyama Y, Hashimoto K, Nishida T, Ishiguro S, et al. Gain-of-function mutations of c-kit in human gastrointestinal stromal tumors. Science 1998;279:577-80.
4. Heinrich MC, Corless CL, Duensing A, McGreevey L, Chen CJ, Joseph N, et al. PDGFRA activating mutations in gastrointestinal stromal tumors. Science 2003;299:708-10.
5. Miettinen M, Wang ZF, Sarlomo-Rikala M, Osuch C, Rutkowski P, Lasota J. Succinate dehydrogenase-deficient GISTs: a clinicopathologic, immunohistochemical, and molecular genetic study of 66 gastric GISTs with predilection to young age. Am J Surg Pathol 2011;35: 1712-21.
6. DeMatteo RP, Lewis JJ, Leung D, Mudan SS, Woodruff JM, Brennan MF. Two hundred gastrointestinal stromal tumors: recurrence patterns and prognostic factors for survival. Ann Surg 2000;231:51-8.
7. Dematteo RP, Heinrich MC, El-Rifai WM, Demetri G. Clinical management of gastrointestinal stromal tumors: before and after STI-571. Hum Pathol 2002;33:466-77.
8. Demetri GD, von Mehren M, Blanke CD, Van den Abbeele AD, Eisenberg B, Roberts PJ, et al. Efficacy and safety of imatinib mesylate in advanced gastrointestinal stromal tumors. N Engl J Med 2002;347: 472-80.
9. Verweij J, Casali PG, Zalcberg J, LeCesne A, Reichardt P, Blay JY, et al. Progression-free survival in gastrointestinal stromal tumours with highdose imatinib: randomised trial. Lancet 2004;364:1127-34.
10. Blanke CD, Demetri GD, von Mehren M, Heinrich MC, Eisenberg B, Fletcher JA, et al. Long-term results from a randomized phase II trial of standard-versus higher-dose imatinib mesylate for patients with unresectable or metastatic gastrointestinal stromal tumors expressing KIT. J Clin Oncol 2008;26:620-5.
11. Antonescu CR, Besmer P, Guo T, Arkun K, Hom G, Koryotowski B, et al. Acquired resistance to imatinib in gastrointestinal stromal tumor occurs through secondary gene mutation. Clin Cancer Res 2005;11: 4182-90.
12. Debiec-Rychter M, Cools J, Dumez H, Sciot R, Stul M, Mentens N, et al. Mechanisms of resistance to imatinib mesylate in gastrointestinal stromal tumors and activity of the PKC412 inhibitor against imatinib-resistant mutants. Gastroenterology 2005;128:270-9.
13. Takahashi T, Serada S, Ako M, Fujimoto M, Miyazaki Y, Nakatsuka R, et al. New findings of kinase switching in gastrointestinal stromal tumor under imatinib using phosphoproteomic analysis. Int J Cancer 2013; 133:2737-43.
14. Mahadevan D, Cooke L, Riley C, Swart R, Simons B, Della Croce K, et al. A novel tyrosine kinase switch is a mechanism of imatinib resistance in gastrointestinal stromal tumors. Oncogene 2007;26:3909-19.
15. Demetri GD, van Oosterom AT, Garrett CR, Blackstein ME, Shah MH, Verweij J, et al. Efficacy and safety of sunitinib in patients with advanced gastrointestinal stromal tumour after failure of imatinib: a randomised controlled trial. Lancet 2006;368:1329-38.
16. Demetri GD, Reichardt P, Kang YK, Blay JY, Rutkowski P, Gelderblom H, et al. Efficacy and safety of regorafenib for advanced gastrointestinal stromal tumours after failure of imatinib and sunitinib (GRID): an international, multicentre, randomised, placebo-controlled, phase 3 trial. Lancet 2013;381:295-302.
17. Gherardi E, Birchmeier W, Birchmeier C, Vande Woude G. Targeting MET in cancer: rationale and progress. Nat Rev Cancer 2012;12:89-103.
18. 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.
19. 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 ERBB3 signaling. Science 2007;316:1039-43.
20. Shattuck DL, Miller JK, Carraway KL III, Sweeney C. Met receptor contributes to trastuzumab resistance of Her2-over expressing breast cancer cells. Cancer Res 2008;68:1471-7.
21. 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.
22. Pennacchietti S, Michieli P, Galluzzo M, Mazzone M, Giordano S, Comoglio PM. Hypoxia promotes invasive growth by transcriptional activation of the met protooncogene. Cancer Cell 2003;3:347-61.
23. Zou HY, Li Q, Lee JH, Arango ME, McDonnell SR, Yamazaki S, et al. An orally available small-molecule inhibitor of c-Met, PF-2341066, exhibits cytoreductive antitumor efficacy through antiproliferative and antiangiogenic mechanisms. Cancer Res 2007;67:4408-17.
24. Yakes FM, Chen J, Tan J, Yamaguchi K, Shi Y, Yu P, et al. Cabozantinib (XL184), a novel MET and VEGFR2 inhibitor, simultaneously suppresses metastasis, angiogenesis, and tumor growth. Mol Cancer Ther 2011;10: 2298-308.
25. Sommer G, Agosti V, Ehlers I, Rossi F, Corbacioglu S, Farkas J, et al. Gastrointestinal stromal tumors in a mouse model by targeted mutation of the Kit receptor tyrosine kinase. Proc Natl Acad Sci U S A 2003;100: 6706-11.
26. Tuveson DA, Willis NA, Jacks T, Griffin JD, Singer S, Fletcher CD, et al. STI571 inactivation of the gastrointestinal stromal tumor c-KIT oncoprotein: biological and clinical implications. Oncogene 2001;20:5054-8.
27. Taguchi T, Sonobe H, Toyonaga S, Yamasaki I, Shuin T, Takano A, et al. Conventional and molecular cytogenetic characterization of anew human cell line, GIST-T1, established from gastrointestinal stromal tumor. Lab Invest 2002;82:663-5.
28. Kim TS, Cavnar MJ, Cohen NA, Sorenson EC, Greer JB, Seifert AM, et al. Increased KIT Inhibition Enhances Therapeutic Efficacy in Gastrointestinal Stromal Tumor. Clin Cancer Res 2014;20:2350-62.
29. Zeng S, Feirt N, Goldstein M, Guarrera J, Ippagunta N, Ekong U, et al. Blockade of receptor for advanced glycation end product (RAGE) attenuates ischemia and reperfusion injury to the liver in mice. Hepatology 2004;39:422-32.
30. Ma PC, Tretiakova MS, MacKinnon AC, Ramnath N, Johnson C, Dietrich S, et al. Expression and mutational analysis of MET in human solid cancers. Genes Chromosomes Cancer 2008;47:1025-37.
31. Weidner KM, Di Cesare S, Sachs M, Brinkmann V, Behrens J, Birchmeier W. Interaction between Gab1 and the c-Met receptor tyrosine kinase is responsible for epithelial morphogenesis. Nature 1996;384:173-6.
32. Birchmeier C, Birchmeier W, Gherardi E, Vande Woude GF. Met, metastasis, motility and more. Nat Rev Mol Cell Biol 2003;4:915-25.
33. Arteel GE, Thurman RG, Yates JM, Raleigh JA. Evidence that hypoxia markers detect oxygen gradients in liver: pimonidazole and retrograde perfusion of rat liver. Br J Cancer 1995;72:889-95.
34. Rothschild SI, Gautschi O. Crizotinib in the treatment of non-small-cell lung cancer. Clin Lung Cancer 2013;14:473-80.
35. Elisei R, Schlumberger MJ, Muller SP, Schoffski P, Brose MS, Shah MH, et al. Cabozantinib in progressive medullary thyroid cancer. J Clin Oncol 2013;31:3639-46.
36. Johannessen CM, Boehm JS, Kim SY, Thomas SR, Wardwell L, Johnson LA, et al. COT drives resistancetoRAF inhibition through MAP kinase pathway reactivation. Nature 2010;468:968-72.
37. Chong CR, Janne PA. The quest to overcome resistance to EGFR-targeted therapies in cancer. Nat Med 2013;19:1389-400.
38. Xu Z, Huo XY, Tang CN, Ye H, Lou F, Chen SY, et al. Frequent mutations in MLH1, MET, KIT, PDGFRA, and PIK3CA genes in human gastrointestinal stromal tumors. J Clin Oncol 2013;31:(suppl;abstr 10544).
39. Heinrich MC, Griffith DJ, Druker BJ, Wait CL, Ott KA, Zigler AJ. Inhibition of c-kit receptor tyrosine kinase activity by STI 571, a selective tyrosine kinase inhibitor. Blood 2000;96:925-32.
40. Botchkareva NV, Khlgatian M, Longley BJ, Botchkarev VA, Gilchrest BA. SCF/c-kit signaling is required for cyclic regenerati9on of the hair pigmentation unit. Faseb J 2001;15:645-58.
41. Imamura M, Yamamoto H, Nakamura N, Oda Y, Yao T, Kakeji Y, et al. Prognostic significance of angiogenesis in gastrointestinal stromal tumor. Mod Pathol 2007;20:529-37.
42. Miettinen M, Lasota J. Gastrointestinal stromal tumors: pathology and prognosis at different sites. Semin Diagn Pathol 2006;23:70-83.