Altiratinib inhibits tumor growth, invasion, angiogenesis, and microenvironment-mediated drug resistance via balanced inhibition of MET, TIE2, and VEGFR2

Molecular Cancer Therapeutics

Volumn 14, Issue 9, 2015, Pages 2023-2034

  Smith, Bryan D ^a   Kaufman, Michael D ^a   Leary, Cynthia B ^a   Turner, Benjamin A ^a   Wise, Scott C ^a   Ahn, Yu Mi ^a   Booth, R John ^a   Caldwell, Timothy M ^a   Ensinger, Carol L ^a   Hood, Molly M ^a   Lu, Wei Ping ^a   Patt, Tristan W ^a   Patt, William C ^a   Rutkoski, Thomas J ^a   Samarakoon, Thiwanka ^a   Telikepalli, Hanumaiah ^a   Vogeti, Lakshminarayana ^a   Vogeti, Subha ^a   Yates, Karen M ^a   Chun, Lawrence ^b   Stewart, Lance J ^b   Clare, Michael ^a   Flynn, Daniel L ^a,c   more..

^a Deciphera Pharmaceuticals   (United States)

^b Emerald BioSystems   (United States)

^c Deciphera Pharmaceuticals LLC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALTIRATINIB; ANGIOPOIETIN RECEPTOR; BEVACIZUMAB; CABOZANTINIB; GOLVATINIB; PACLITAXEL; SCATTER FACTOR RECEPTOR; TIVANTINIB; VASCULOTROPIN RECEPTOR 2; AMINOPYRIDINE DERIVATIVE; ANILIDE; ANTINEOPLASTIC AGENT; B RAF KINASE; DCC-2701; PROTEIN KINASE INHIBITOR; RECOMBINANT PROTEIN; SCATTER FACTOR;

A549 CELL LINE; ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD BRAIN BARRIER; BRAIN CANCER; BRAIN METASTASIS; BRAIN TISSUE; BREAST TUMOR; CANCER INHIBITION; CANCER RESISTANCE; CONTROLLED STUDY; DRUG DESIGN; DRUG DISTRIBUTION; DRUG EFFICACY; DRUG MECHANISM; FEMALE; GLIOMA; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LUNG METASTASIS; MELANOMA CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; TUMOR GROWTH; TUMOR INVASION; TUMOR MICROENVIRONMENT; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL MOTION; CELL PROLIFERATION; CHEMICAL STRUCTURE; CHEMISTRY; COMBINATION DRUG THERAPY; CONFORMATION; DISEASE MODEL; DRUG EFFECTS; DRUG RESISTANCE; DRUG SCREENING; EXPERIMENTAL MELANOMA; GENETICS; IC50; METABOLISM; MONOCYTE; NEOVASCULARIZATION (PATHOLOGY); STROMA CELL; TUMOR CELL LINE;

AMINOPYRIDINES; ANILIDES; ANIMALS; ANTINEOPLASTIC AGENTS; BEVACIZUMAB; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; DRUG DESIGN; DRUG RESISTANCE, NEOPLASM; DRUG THERAPY, COMBINATION; FEMALE; HEPATOCYTE GROWTH FACTOR; HUMANS; INHIBITORY CONCENTRATION 50; MELANOMA, EXPERIMENTAL; MICE; MODELS, MOLECULAR; MOLECULAR CONFORMATION; MONOCYTES; NEOVASCULARIZATION, PATHOLOGIC; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS B-RAF; PROTO-ONCOGENE PROTEINS C-MET; RECEPTOR, TIE-2; RECOMBINANT PROTEINS; STROMAL CELLS; TUMOR MICROENVIRONMENT; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84942085999     PISSN: 15357163     EISSN: 15388514     Source Type: Journal    
DOI: 10.1158/1535-7163.MCT-14-1105     Document Type: Article

References (50)

1. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011;144:646.
2. Blumenschein GR Jr, Mills GB, Gonzalez-Angulo AM. Targeting the hepatocyte growth factor-cMET axis in cancer therapy. J Clin Oncol 2012;30:3287-96.
3. Mazzone M, Basilico C, Cavassa S, Pennacchietti S, Risio M, Naldini L, et al. An uncleavable form of pro-scatter factor suppresses tumor growth and dissemination in mice. J Clin Invest 2004;114:1418-32.
4. Rong S, Segal S, Anver M, Resau JH, Vande Woude GF. Invasiveness and metastasis of NIH 3T3 cells induced by Met-hepatocyte growth factor/scatter factor autocrine stimulation. Proc Natl Acad Sci U S A 1994;91:4731-5.
5. Bottaro DP, Rubin JS, Faletto DL, Chan AM, Kmiecik TE, Vande Woude GF, et al. Identification of the hepatocyte growth factor receptor as the c-met proto-oncogene product. Science 1991;251:802-4.
6. Tuck AB, Park M, Sterns EE, Boag A, Elliott BE. Coexpression of hepatocyte growth factor and receptor (Met) in human breast carcinoma. Am J Pathol 1996;148:225-32.
7. Koochekpour S, Jeffers M, Rulong S, Taylor G, Klineberg E, Hudson EA, et al. Met and hepatocyte growth factor/scatter factor expression in human gliomas. Cancer Res 1997;57:5391-8.
8. Mitra AK, Sawada K, Tiwari P, Mui K, Gwin K, Lengyel E. Ligand independent activation of c-Met by fibronectin and a5b1-integrin regulates ovarian cancer invasion and metastasis. Oncogene 2011;30:1566-76.
9. Conrotto P, Valdembri D, Corso S, Serini G, Tamagnone L, Comoglio PM, et al. Sema4D induces angiogenesis through Met recruitment by Plexin B1. Blood 2005;105:4321-9.
10. Troiani T, Martinelli E, Napolitano S, Vitagliano D, Pia Ciuffreda L, Costantino S, et al. Increased TGF-a as a mechanism of acquired resistance to the anti-EGFR inhibitor cetuximab through EGFR -MET interaction and activation of MET signaling in colon cancer cells. Clin Cancer Res 2013;19:6751-65.
11. Danilkovitch-Miagkova A, Zbar B. Dysregulation of Met receptor tyrosine kinase activity in invasive tumors. J Clin Invest 2002;109:863-7.
12. Beroukhim R, Getz G, Nghiemphu L, Barretina J, Hsueh T, Linhart D, et al. Assessing the significance of chromosomal aberrations in cancer: methodology and application to glioma. Proc Natl Acad Sci U S A 2007;104:20007-12.
13. Tong CY, Hui AB, Yin XL, Pang JC, Zhu XL, Poon WS, et al. Detection of oncogene amplifications in medulloblastomas by comparative genomic hybridization and array-based comparative genomic hybridization. J Neurosurg 2004;100:187-93.
14. Cappuzzo F, Ciuleanu T, Stelmakh L, Cicenas S, Szczesna A, Juhasz E, et al. SATURN: a double-blind, randomized, phase III study of maintenance erlotinib versus placebo following nonprogression with first-line platinum-based chemotherapy in patients with advanced NSCLC. J Clin Oncol 2009;27:No 15S.
15. Houldsworth J, Cordon-Cardo C, Ladanyi M, Kelsen DP, Chaganti RS. Gene amplification in gastric and esophageal adenocarcinomas. Cancer Res 1990;50:6417-22.
16. Umeki K, Shiota G, Kawasaki H. Clinical significance of c-met oncogene alterations in human colorectal cancer. Oncology 1999;56:314-21.
17. Schmidt L, Duh F-M, Chen F, Kishida T, Glenn G, Choyke P, 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.
18. Lee JH, Han SU, Cho H, Jennings B, Gerrard B, Dean M, et al. A novel germline juxtamembrane Met mutation in human gastric cancer. Oncogene 2000;19:4947-53.
19. Jagadeeswaran R, Ma PC, Seiwert TY, Jagadeeswaran S, Zumba O, Nallasura V, et al. Functional analysis of c-Met/hepatocyte growth factor pathway in malignant pleural mesothelioma. Cancer Res 2006;66:352-61.
20. Puri N, Ahmed S, Janamanci V, Tretiakova M, Zumba O, Krausz T, et al. C-Met is a potentially new therapeutic target for treatment of human melanoma. Clin Cancer Res 2007;13:2246-53.
21. Di Renzo MF, Olivero M, Maretone T, Maffe A, Maggiora P, Stefani AD, et al. Somatic mutations of the MET oncogene are selected during metastatic spread of human HNSC carcinomas. Oncogene 2000;19:1547-55.
22. Straussman R, Morikawa T, Shee K, Barzily-Rokni M, Qian ZR, Du J, Davis A, 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. Lu KV, Chang JP, Parachoniak CA, Pandika MM, Aghi MK, Meyronet D, et al. VEGF inhibits tumor cell invasion and mesenchymal transition through a MET/VEGFR2 complex. Cancer Cell 2012;22:21-35.
25. Jahangiri A, De Lay M, Miller LM, Carbonell WS, Hu YL, Lu K, et al. Gene expression profile identifies tyrosine kinase c-Met as a targetable mediator of antiangiogenic therapy resistance. Clin Cancer Res 2013;19:1773-83.
26. 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;19:4392-403.
27. Wang W, Li Q, Yamada T, Matsumoto K, Matsumoto I, Oda M, et al. Crosstalk to stromal fibroblasts induces resistance of lung cancer to epidermal growth factor receptor tyrosine kinase inhibitors. Clin Cancer Res 2009;15:6630-8.
28. 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;12:2011-7.
29. Kitajima Y, Ide T, Ohtsuka T, Miyazaki K. Induction of hepatocyte growth factor activator gene expression under hypoxia activates the hepatocyte growth factor/c-Met system via hypoxia inducible factor-1 in pancreatic cancer. Cancer Sci 2008;99:1341-7.
30. Xin X, Yang S, Ingle G, Zlot C, Rangell L, Kowalski J, et al. Hepatocyte growth factor enhances vascular endothelial growth factor-induced angiogenesis in vitro and in vivo. Am J Pathol 2001;158:1111-20.
31. Van Belle E, Witzenbichler B, Chen D, Silver M, Chang L, Schwall R, et al. Potentiated angiogenic effect of scatter factor/hepatocyte growth factor via induction of vascular endothelial growth factor. Circulation 1998;97:381-90.
32. Sennino B, Ishiguro-Oonuma T, Wei Y, Naylor RM, Williamson CW, Bhagwandin V, 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:OF1-OF18.
33. Sennino B, Ishiguro-Oonuma T, Schriver BJ, Christensen JG, McDonald DM. Inhibition of c-Met reduces lymphatic metastasis in RIP-Tag2 transgenic mice. Cancer Res 2013;73:3692-703.
34. Mazzieri R, Pucci F, Moi D, Zonari E, Ranghetti A, Berti A, et al. Targeting the ANG2/TIE2 axis inhibits tumor growth and metastasis by impairing angiogenesis and disabling rebounds of proangiogenic myeloid cells. Cancer Cell 2011;19:512-26.
35. Schulz P, Fischer C, Detjen KM, Rieke S, Hilfenhaus G, von Marschall Z, et al. Angiopoietin-2 drives lymphatic metastasis of pancreatic cancer. FASEB J 2011;25:3325-35.
36. 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;8:1-11.
37. Brunckhorst MK, Wang H, Lu R, Yu Q. Angiopoietin-4 promotes glioblastoma progression by enhancing tumor cell viability and angiogenesis. Cancer Res 2010;70:7283-93.
38. Hata K, Udagawa J, Fujiwaki R, Nakayama K, Otani H, Miyazaki K. Expression of angiopoietin-1, angiopoietin-2, and Tie2 genes in normal ovary with corpus luteum and in ovarian cancer. Oncology 2002;62:340-8.
39. Hashizume H, Falcón BL, Kuroda T, Baluk P, Coxon A, Yu D, et al. Complementary actions of inhibitors of angiopoietin-2 and VEGF on tumor angiogenesis and growth. Cancer Res 2010;70:2213-23.
40. Gabrusiewicz K, Liu D, Cortes-Santiago N, Hossain MB, Conrad CA, Aldape KD, et al. Anti-vascular endothelial growth factor therapy-induced glioma invasion is associated with accumulation of Tie2-expressing monocytes. Oncotarget 2014;5:2208-20.
41. Schindler T, Bornmann W, Pellicena P, Miller WT, Clarkson B, Kuriyan J. Structural mechanism for STI-571 inhibition of Abelson tyrosine kinase. Science 2000;289:1938-42.
42. Morrison JF, Walsh C. The behavior and significance of slow-binding enzyme inhibitors, Adv. Enzymol 1988;61:201-301.
43. Chan WW, Wise SC, Kaufman MD, Ahn YM, Ensinger CL, Haack T, et al. Conformational control inhibition of the BCR-ABL1 tyrosine kinase, including the gatekeeper T315I mutant, by the switch-control inhibitor DCC-2036. Cancer Cell 2011;19:556-68.
44. Xie Q, Bradley R, Kang L, Koeman J, Ascierto ML, Worschech A, et al. Hepatocyte growth factor (HGF) autocrine activation predicts sensitivity to MET inhibition in glioblastoma. Proc Natl Acad Sci U S A 2012;109:570-5.
45. Ding S, Merkulova-Rainon T, Han ZC, Tobelem G. HGF receptor upregulation contributes to the angiogenic phenotype of human endothelial cells and promotes angiogenesis in vitro. Blood 2003;101:4816-22.
46. Peinado H, Alečković M, Lavotshkin S, Matei I, Costa-Silva B, Moreno-Bueno G, et al. Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. Nat Med 2012;18:883-91.
47. Guy CT, Cardiff RD, Muller WJ. Induction of mammary tumors by expression of polyomavirus middle T oncogene: a transgenic mouse model for metastatic disease. Mol Cell Biol 1992;12:954-61.
48. Huang H, Lai JY, Do J, Liu D, Li L, Del Rosario J, etal. Specifically targeting angiopoietin-2 inhibits angiogenesis, Tie2-expressing monocyte infiltration, and tumor growth. Clin Cancer Res 2011;17:1001-11.
49. Liu D, Zhang Y, Dang C, Ma Q, Lee W, Chen W. siRNA directed against TrkA sensitizes human pancreatic cancer cells to apoptosis induced by gemcitabine through an inactivation of PI3K/Akt-dependent pathway. Oncol Rep 2007;18:673-7.
50. Stransky N, Cerami E, Schalm S, Kim JL, Lengauer C. The landscape of kinase fusions in cancer. Nat Commun 2014;5:4846.