Novel MET/TIE2/VEGFR2 inhibitor altiratinib inhibits tumor growth and invasiveness in bevacizumab-resistant glioblastoma mouse models

Neuro-Oncology

Volumn 18, Issue 9, 2016, Pages 1230-1241

  Piao, Yuji ^a   Park, Soon Young ^a   Henry, Verlene ^a   Smith, Bryan D ^b   Tiao, Ningyi ^a   Flynn, Daniel L ^a,b   De Groot, John F ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b Deciphera Pharmaceuticals LLC   (United States)

Author keywords

altiratinib; bevacizumab; glioma; MET; TIE2 expressing monocytes

Indexed keywords

ALTIRATINIB; BEVACIZUMAB; SCATTER FACTOR RECEPTOR; ANGIOPOIETIN RECEPTOR; ANTINEOPLASTIC AGENT; KDR PROTEIN, HUMAN; MET PROTEIN, HUMAN; PROTEIN KINASE INHIBITOR; VASCULOTROPIN RECEPTOR 2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; CANCER INHIBITION; CANCER STEM CELL; CANCER SURVIVAL; CAPILLARY DENSITY; CELL INFILTRATION; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG EFFECT; FEMALE; GLIOBLASTOMA; HUMAN; HUMAN CELL; MONOCYTE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REVIEW; TUMOR INVASION; TUMOR VOLUME; ANIMAL; ANTAGONISTS AND INHIBITORS; APOPTOSIS; BRAIN NEOPLASMS; CELL PROLIFERATION; DRUG EFFECTS; DRUG RESISTANCE; DRUG SCREENING; METABOLISM; NEOVASCULARIZATION, PATHOLOGIC; NUDE MOUSE; PATHOLOGY; TUMOR CELL CULTURE;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; BEVACIZUMAB; BRAIN NEOPLASMS; CELL PROLIFERATION; DRUG RESISTANCE, NEOPLASM; FEMALE; GLIOBLASTOMA; HUMANS; MICE; MICE, NUDE; NEOPLASM INVASIVENESS; NEOVASCULARIZATION, PATHOLOGIC; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-MET; RECEPTOR, TIE-2; TUMOR CELLS, CULTURED; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84985949313     PISSN: 15228517     EISSN: 15235866     Source Type: Journal    
DOI: 10.1093/neuonc/now030     Document Type: Review

References (44)

1. Reardon DA, Wen PY. Glioma in 2014: unravelling tumour heterogeneity-implications for therapy. Nat Rev Clin Oncol. 2015; 12(2):69-70.
2. Khasraw M, Ameratunga M, Grommes C. Bevacizumab for the treatment of high-grade glioma: an update after phase III trials. Expert Opin Biol Ther. 2014;14(5):729-740.
3. Norden AD, Young GS, Setayesh K, et al. Bevacizumab for recurrent malignant gliomas: efficacy, toxicity, and patterns of recurrence. Neurology. 2008;70(10):779-787.
4. 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(4): 347-361.
5. di Tomaso E, Snuderl M, Kamoun WS, et al. Glioblastoma recurrence after cediranib therapy in patients: lack of rebound revascularization as mode of escape. Cancer Res. 2011;71(1): 19-28.
6. 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(3):220-231.
7. Piao Y, Liang J, Holmes L, Henry V, Sulman E, de Groot JF. Acquired resistance to anti-VEGF therapy in glioblastoma is associated with a mesenchymal transition. Clin Cancer Res. 2013;19(16):4392-4403.
8. Lu KV, Chang JP, Parachoniak CA, et al. VEGF inhibits tumor cell invasion and mesenchymal transition through a MET/VEGFR2 complex. Cancer Cell. 2012;22(1):21-35.
9. Edakuni G, Sasatomi E, Satoh T, Tokunaga O, Miyazaki K. Expression of the hepatocyte growth factor/c-Met pathway is increased at the cancer front in breast carcinoma. Pathol Int. 2001;51(3): 172-178.
10. Galimi F, Torti D, Sassi F, et al. Genetic and expression analysis of MET, MACC1, and HGF in metastatic colorectal cancer: response to met inhibition in patient xenografts and pathologic correlations. Clin Cancer Res. 2011;17(10):3146-3156.
11. 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(1):68-73.
12. 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(4):1479-1488.
13. Koochekpour S, Jeffers M, Rulong S, et al. Met and hepatocyte growth factor/scatter factor expression in human gliomas. Cancer Res. 1997;57(23):5391-5398.
14. Bhowmick NA, Neilson EG, Moses HL. Stromal fibroblasts in cancer initiation and progression. Nature. 2004;432(7015):332-337.
15. Chi AS, Batchelor TT, Dias-Santagata D, et al. Prospective, high-throughput molecular profiling of human gliomas. J Neurooncol. 2012;110(1):89-98.
16. Cancer Genome Atlas Research N. Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature. 2008;455(7216):1061-1068.
17. Pierscianek D, Kim YH, Motomura K, et al. MET gain in diffuse astrocytomas is associated with poorer outcome. Brain Pathol. 2013;23(1):13-18.
18. Kong DS, Song SY, Kim DH, et al. Prognostic significance of c-Met expression in glioblastomas. Cancer. 2009;115(1):140-148.
19. Boccaccio C, Comoglio PM. Invasive growth: a MET-driven genetic programme for cancer and stem cells. Nat Rev Cancer. 2006;6(8): 637-645.
20. McCubrey JA, Steelman LS, Chappell WH, et al. Roles of the Raf/ MEK/ERK pathway in cell growth, malignant transformation and drug resistance. Biochim Biophys Acta. 2007;1773(8):1263-1284.
21. Bowers DC, Fan S,Walter KA, et al. Scatter factor/hepatocyte growth factor protects against cytotoxic death in human glioblastoma via phosphatidylinositol 3-kinase-and AKT-dependent pathways. Cancer Res. 2000;60(15):4277-4283.
22. Joo KM, Jin J, Kim E, et al. MET signaling regulates glioblastoma stem cells. Cancer Res. 2012;72(15):3828-3838.
23. Olmez OF, Cubukcu E, Evrensel T, et al. The immunohistochemical expression of c-Met is an independent predictor of survival in patients with glioblastoma multiforme. Clin Transl Oncol. 2014; 16(2):173-177.
24. Lathia JD, Li M, Sinyuk M, et al. High-throughput flow cytometry screening reveals a role for junctional adhesion molecule a as a cancer stem cell maintenance factor. Cell Rep. 2014;6(1): 117-129.
25. Verhaak RG, Hoadley KA, Purdom E, et al. Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell. 2010;17(1):98-110.
26. Phillips HS, Kharbanda S, Chen R, et al. Molecular subclasses of high-grade glioma predict prognosis, delineate a pattern of disease progression, and resemble stages in neurogenesis. Cancer Cell. 2006;9(3):157-173.
27. De Bacco F, Casanova E, Medico E, et al. The MET oncogene is a functional marker of a glioblastoma stem cell subtype. Cancer Res. 2012;72(17):4537-4550.
28. Lal B, Xia S, Abounader R, Laterra J. Targeting the c-Met pathway potentiates glioblastoma responses to gamma-radiation. Clin Cancer Res. 2005;11(12):4479-4486.
29. De Palma M, Venneri MA, Galli R, et al. Tie2 identifies a hematopoietic lineage of proangiogenic monocytes required for tumor vessel formation and a mesenchymal population of pericyte progenitors. Cancer Cell. 2005;8(3):211-226.
30. Gabrusiewicz K, Liu D, Cortes-Santiago N, et al. Anti-vascular endothelial growth factor therapy-induced glioma invasion is associated with accumulation of Tie2-expressing monocytes. Oncotarget. 2014;5(8):2208-2220.
31. Piao Y, Liang J, Holmes L, et al. Glioblastoma resistance to anti-VEGF therapy is associated with myeloid cell infiltration, stem cell accumulation, and a mesenchymal phenotype. Neuro Oncol. 2012;14(11):1379-1392.
32. Kim H, Verhaak RG. Transcriptional mimicry by tumor-associated stroma. Nat Genet. 2015;47(4):307-309.
33. Smith BD, Kaufman MD, Leary CB, et al. Altiratinib inhibits tumor growth, invasion, angiogenesis, and microenvironment-mediated drug resistance via balanced inhibition of MET, TIE2, and VEGFR2. Mol Cancer Ther. 2015;14(9):2013-2034.
34. He H, Nilsson CL, Emmett MR, et al. Glycomic and transcriptomic response of GSC11 glioblastoma stem cells to STAT3 phosphorylation inhibition and serum-induced differentiation. J Proteome Res. 2010;9(5):2098-2108.
35. Euhus DM, Hudd C, LaRegina MC, Johnson FE. Tumormeasurement in the nude mouse. J Surg Oncol. 1986;31(4):229-234.
36. Christensen JG, Schreck R, Burrows J, et al. A selective small molecule inhibitor of c-Met kinase inhibits c-Met-dependent phenotypes in vitro and exhibits cytoreductive antitumor activity in vivo. Cancer Res. 2003;63(21):7345-7355.
37. Smolen GA, Sordella R, Muir B, 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 USA. 2006;103(7):2316-2321.
38. 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 USA. 2012;109(2):570-575.
39. Zhang Y, Farenholtz KE, Yang Y, et al. Hepatocyte growth factor sensitizes brain tumors to c-MET kinase inhibition. Clin Cancer Res. 2013;19(6):1433-1444.
40. Hashizume H, Falcon BL, Kuroda T, et al. Complementary actions of inhibitors of angiopoietin-2 and VEGF on tumor angiogenesis and growth. Cancer Res. 2010;70(6):2213-2223.
41. Rigamonti N, Kadioglu E, Keklikoglou I, Wyser Rmili C, Leow CC, De Palma M. Role of angiopoietin-2 in adaptive tumor resistance to VEGF signaling blockade. Cell Rep. 2014;8(3):696-706.
42. Xin X, Yang S, Ingle G, et al. Hepatocyte growth factor enhances vascular endothelial growth factor-induced angiogenesis in vitro and in vivo. Am J Pathol. 2001;158(3):1111-1120.
43. Sennino B, Ishiguro-Oonuma T, Wei Y, et al. Suppression of tumor invasion and metastasis by concurrent inhibition of c-Met and VEGF signaling in pancreatic neuroendocrine tumors. Cancer Discov. 2012;2(3):270-287.
44. Venneri MA, De Palma M, Ponzoni M, et al. Identification of proangiogenic TIE2-expressing monocytes (TEMs) in human peripheral blood and cancer. Blood. 2007;109(12):5276-5285.