Vandetanib is effective in EGFR-mutant lung cancer cells with PTEN deficiency

Experimental Cell Research

Volumn 319, Issue 4, 2013, Pages 417-423

  Takeda, Hiromasa ^a   Takigawa, Nagio ^b   Ohashi, Kadoaki ^a   Minami, Daisuke ^a   Kataoka, Itaru ^a   Ichihara, Eiki ^a   Ochi, Nobuaki ^a   Tanimoto, Mitsune ^a   Kiura, Katsuyuki ^c  

^a OKAYAMA UNIVERSITY   (Japan)

^b KAWASAKI MEDICAL SCHOOL   (Japan)

^c OKAYAMA UNIVERSITY HOSPITAL   (Japan)

Author keywords

EGFR; Gefitinib; Lung cancer; PTEN; Vandetanib; VEGFR

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; GEFITINIB; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN KINASE B; SHORT HAIRPIN RNA; VANDETANIB; ANTINEOPLASTIC AGENT; N (4 BROMO 2 FLUOROPHENYL) 6 METHOXY 7 ((1 METHYLPIPERIDIN 4 YL)METHOXY)QUINAZOLIN 4 AMINE; N-(4-BROMO-2-FLUOROPHENYL)-6-METHOXY-7-((1-METHYLPIPERIDIN-4-YL)METHOXY)QUINAZOLIN-4-AMINE; PIPERIDINE DERIVATIVE; PROTEIN KINASE INHIBITOR; PTEN PROTEIN, HUMAN; QUINAZOLINE DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER RESISTANCE; CHEMOSENSITIVITY; CONTROLLED STUDY; DRUG EFFICACY; DRUG INHIBITION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; GENE SILENCING; HUMAN; HUMAN CELL; IN VITRO STUDY; LUNG NON SMALL CELL CANCER; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS INHIBITION; ANIMAL; DRUG SCREENING; FEMALE; GENETICS; LUNG TUMOR; MUTATION; NUDE MOUSE; PATHOLOGY; PHYSIOLOGY; PROTO ONCOGENE; TREATMENT OUTCOME; TUMOR CELL LINE;

ANIMALS; ANTINEOPLASTIC AGENTS; CARCINOMA, NON-SMALL-CELL LUNG; CELL LINE, TUMOR; FEMALE; GENES, ERBB-1; HUMANS; LUNG NEOPLASMS; MICE; MICE, NUDE; MUTATION; PIPERIDINES; PROTEIN KINASE INHIBITORS; PTEN PHOSPHOHYDROLASE; QUINAZOLINES; TREATMENT OUTCOME; XENOGRAFT MODEL ANTITUMOR ASSAYS;

MLCS; MLOWN;

EID: 84875518717     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2012.12.018     Document Type: Article

References (39)

1. Mitsudomi T., Yatabe Y. Mutations of the epidermal growth factor receptor gene and related genes as determinants of epidermal growth factor receptor tyrosine kinase inhibitors sensitivity in lung cancer. Cancer Sci. 2007, 98:1817-1824.
2. Gazdar A.F., Shigematsu H., Herz J., Minna J.D. Mutations and addiction to EGFR: the Achilles 'heal' of lung cancers?. Trends. Mol. Med. 2004, 10:481-486.
3. Lynch T.J., Bell D.W., Sordella R., Gurubhagavatula S., Okimoto R.A., Brannigan B.W., Harris P.L., Haserlat S.M., Supko J.G., Haluska F.G., Louis D.N., Christiani D.C., Settleman J., Haber D.A. Activating mutations in the epidermal growth factor receptor underlying responsiveness of non-small-cell lung cancer to gefitinib. N. Engl. J. Med. 2004, 350:2019-2029.
4. Pao W., Miller V., Zakowski M., Doherty J., Politi K., Sarkaria I., Singh B., Heelan R., Rusch V., Fulton L., Mardis E., Kupfer D., Wilson R., Kris M., Varmus H. EGF receptor gene mutations are common in lung cancers from never smokers and are associated with sensitivity of tumors to gefitinib and erlotinib. Proc. Natl. Acad. Sci. U.S.A 2004, 101:13306-13311.
5. Mok T.S., Wu Y.-L., Thongprasert S., Yang C.-H., Chu D.-T., Saijo N., Sunpaweravong P., Han B., Margono B., Ichinose Y., Nishiwaki Y., Ohe Y., Yang J.-J., Chewaskulyong B., Jiang H., Duffield E.L., Watkins C.L., Armour A.A., Fukuoka M. Gefitinib or carboplatin-paclitaxel in pulmonary adenocarcinoma. N. Engl. J. Med. 2009, 361:947-957.
6. Inoue A., Suzuki T., Fukuhara T., Maemondo M., Kimura Y., Morikawa N., Watanabe H., Saijo Y., Nukiwa T. Prospective phase II study of gefitinib for chemotherapy-naive patients with advanced non-small-cell lung cancer with epidermal growth factor receptor gene mutations. J. Clin. Oncol. 2006, 24:3340-3346.
7. Pao W., Miller V.A., Politi K.A., Riely G.J., Somwar R., Zakowski M.F., Kris M.G., Varmus H. Acquired resistance of lung adenocarcinomas to gefitinib or erlotinib is associated with a second mutation in the EGFR kinase domain. PLos Med. 2005, 2:e73.
8. Kobayashi S., Boggon T.J., Dayaram T., Jänne P.A., Kocher O., Meyerson M., Johnson B.E., Eck M.J., Tenen D.G., Halmos B. EGFR mutation and resistance of non-small-cell lung cancer to gefitinib. N. Engl. J. Med. 2005, 24:768-792.
9. Ogino A., Kitao H., Hirano S., Uchida A., Ishiai M., Kozuki T., Takigawa N., Takata M., Kiura K., Tanimoto M. Emergence of epidermal growth factor receptor T790M mutation during chronic exposure to gefitinib in a non small cell lung cancer cell line. Cancer Res. 2007, 67:7807-7814.
10. Ichihara E., Ohashi K., Takigawa N., Osawa M., Ogino A., Tanimoto M., Kiura K. Effects of vandetanib on lung adenocarcinoma cells harboring epidermal growth factor receptor T790M mutation in vivo. Cancer Res. 2009, 69:5091-5098.
11. Engelman J.A., Zejnullahu K., Mitsudomi T., Song Y., Hyland C., Park J.O., Lindeman N., Gale C.M., Zhao X., Christensen J., Kosaka T., Holmes A.J., Rogers A.M., Cappuzzo F., Mok T., Lee C., Johnson B.E., Cantley L.C., Janne P.A. MET amplification leads to gefitinib resistance in lung cancer by activating ERBB3 signaling. Science 2007, 316:1039-1043.
12. Yano S., Wang W., Li Q., Matsumoto K., Sakurama H., Nakamura T., Ogino H., Kakiuchi S., Hanibuchi M., Nishioka Y., Uehara H., Mitsudomi T., Yatabe Y., Nakamura T., Sone S. Hepatocyte growth factor induces gefitinib resistance of lung adenocarcinoma with epidermal growth factor receptor-activating mutations. Cancer Res. 2008, 68:9479-9487.
13. Sequist V., Waltman B.A., Dias-Santagata D., Digumarthy S., Turke A.B., Fidias P., Bergethon K., Shaw A.T., Gettinger S., Cosper A.K., Akhavanfard S., Heist R.S., Temel J., Christensen J.G., Wain J.C., Lynch T.J., Vernovsky K., Mark E.J., Lanuti M., Iafrate A.J., Mino-Kenudson M., Engelman J.A. Genotypic and histological evolution of lung cancers acquiring resistance to EGFR inhibitors. Sci. Transl. Med. 2011, 3:75ra26.
14. Thomson S., Buck E., Petti F., Griffin G., Brown E., Ramnarine N., Iwata K.K., Gibson N., Haley J.D. Epithelial to mesenchymal transition is a determinant of sensitivity of non-small-cell lung carcinoma cell lines and xenografts to epidermal growth factor receptor inhibition. Cancer Res. 2005, 65:9455-9462.
15. Salmena L., Carracedo A., Pandolfi P.P. Tenets of PTEN tumor suppression. Cell 2008, 133:403-414.
16. Soria J.-C., Lee J.I., Lee H.-Y., Wang L., Issa J.-P., Kemp B.L., Liu D.D., Kurie J.M., Mao L., Khuri F.R. Lack of PTEN Expression in non-small cell lung cancer could be related to promoter methylation. Clin. Cancer Res. 2002, 8:1178-1184.
17. Forgacs E., Biesterveld E.J., Sekido Y., Fong K., Muneer S., Wistuba I.I., Milchgrub S., Gazdar A.F., Minna J.D. Mutation analysis of the PTEN/MMAC1 gene in lung cancer. Oncogene 1998, 24:1557-1565.
18. Jin G., Kim M.J., Jeon H.S., Choi J.E., Kim D.S., Lee E.B., Cha S.I., Yoon G.S., Kim C.H., Jung T.H., Park J.Y. PTEN mutations and relationship to EGFR, ERBB2, KRAS, and TP53 mutations in non-small cell lung cancers. Lung Cancer 2010, 69:279-283.
19. Sos M.L., Koker M., Weir B.A., Heynck S., Rabinovsky R., Zander T., Seeger J.M., Weiss J., Fischer F., Frommolt P., Michel K., Peifer M., Mermel C., Girard L., Peyton M., Gazdar A.F., Minna J.D., Garraway L.A., Kashkar H., Pao W., Meyerson M., Thomas R.K. PTEN loss contributes to erlotinib resistance in EGFR-mutant lung cancer by activation of Akt and EGFR. Cancer Res. 2009, 69:3256-3261.
20. Kokubo Y., Gemma A., Noro R., Seike M., Kataoka K., Matsuda K., Okano T., Minegishi Y., Yoshimura A., Shibuya M., Kudoh S. Reduction of PTEN protein and loss of epidermal growth factor receptor gene mutation in lung cancer with natural resistance to gefitinib (IRESSA). Br. J. Cancer 2005, 92:1711-1719.
21. Yamamoto C., Basaki Y., Kawahara A., Nakashima K., Kage M., Izumi H., Kohno K., Uramoto H., Yasumoto K., Kuwano M., Ono M. Loss of PTEN expression by blocking nuclear translocation of EGR1 in gefitinib-resistant lung cancer cells harboring epidermal growth factor receptor-activating mutations. Cancer Res. 2010, 70:8715-8725.
22. She Q.-B., Solit D., Basso A., Moasser M.M. Resistance to gefitinib in PTEN-Null HER-overexpressing tumor cells can be overcome through restoration of PTEN function or pharmacologic modulation of constitutive phosphatidylinositol 3-kinase/Akt pathway signaling, Clin. Cancer Res. 2003, 9:4340-4346.
23. Yamasaki F., Johansen M.J., Zhang D., Krishnamurthy S., Felix E., Bartholomeusz C., Aguilar R.J., Kurisu K., Mills G.B., Hortobagyi G.N., Ueno N.T. Acquired resistance to erlotinib in A-431 epidermoid cancer cells requires down-regulation of MMAC1/PTEN and up-regulation of phosphorylated Akt. Cancer Res. 2007, 67:5779-5788.
24. Mellinghoff I.K., Wang M.Y., Vivanco I., Haas-Kogan D.A., Zhu S., Dia E.Q., Mischel P.S. Molecular determinants of the response of glioblastomas to EGFR kinase inhibitors. N. Engl. J. Med. 2005, 353:2012-2024.
25. Wedge S.R., Ogilvie D.J., Dukes M., Kendrew J., Chester R., Jackson J.A., Boffey S.J., Valentine P.J., Curwen J.O., Musgrove H.L., Graham G.A., Hughes G.D., Thomas A.P., Stokes E.S., Curry B., Richmond G.H., Wadsworth P.F., Bigley AL H.L. ZD6474 inhibits vascular endothelial growth factor signaling, angiogenesis, and tumor growth following oral administration. Cancer Res. 2002, 15:4645-4655.
26. Ryan A.J., Wedge S.R. ZD6474 - a novel inhibitor of VEGFR and EGFR tyrosine kinase activity. Br. J. Cancer 2005, 92(Suppl 1):S6-13.
27. Naumov G.N., Nilsson M.B., Cascone T., Briggs A., Straume O., Akslen L.A., Lifshits E., Byers L.A., Xu L., Wu H.K., Janne P., Kobayashi S., Halmos B., Tenen D., Tang X.M., Engelman J., Yeap B., Folkman J., Johnson B.E., Heymach J.V. Combined vascular endothelial growth factor receptor and epidermal growth factor receptor (EGFR) blockade inhibits tumor growth in xenograft models of EGFR inhibitor resistance. Clin. Cancer Res. 2009, 15:3484-3494.
28. Lee J.S., Hirsh V., Park K., Qin S., Blajman C.R., Perng R.P., Chen Y.M., Emerson L., Langmuir P., Manegold C. Vandetanib versus placebo in patients with advanced non-small-cell lung cancer after prior therapy with an epidermal growth factor receptor tyrosine kinase inhibitor: a randomized, double-blind phase III trial (ZEPHYR). J. Clin. Oncol. 2012, 30:1114-1121.
29. Natale R.B., Thongprasert S., Greco F.A., Thomas M., Tsai C.M., Sunpaweravong P., Ferry D., Mulatero C., Whorf R., Thompson J., Barlesi F., Langmuir P., Gogov S., Rowbottom J.A., Goss G.D. Phase III trial of vandetanib compared with erlotinib in patients with previously treated advanced non-small-cell lung cancer. J. Clin. Oncol. 2011, 29:1059-1066.
30. Herbst R.S., Sun Y., Eberhardt W.E.E., Germonpré P., Saijo N., Zhou C., Wang J., Li L., Kabbinavar F., Ichinose Y., Qin S., Zhang L., Biesma B., Heymach J.V., Langmuir P., Kennedy S.J., Tada H., Johnson B.E. Vandetanib plus docetaxel versus docetaxel as second-line treatment for patients with advanced non-small-cell lung cancer (ZODIAC): a double-blind, randomised, phase 3 trial. Lancet. Oncol. 2010, 11:619-626.
31. de Boer R.H., Arrieta O., Yang C.H., Gottfried M., Chan V., Raats J., de Marinis F., Abratt R.P., Wolf J., Blackhall F.H., Langmuir P., Milenkova T., Read J., Vansteenkiste J.F. Vandetanib plus pemetrexed for the second-line treatment of advanced non-small-cell lung cancer: a randomized, double-blind phase III trial. J. Clin. Oncol. 2011, 29:1067-1074.
32. Kim E.S., Herbst R.S., Wistuba I.I., Lee J.J., Blumenschein G.R., Tsao A., Stewart D.J., Hicks M.E., Erasmus J., Gupta S., Alden C.M., Liu S., Tang X., Khuri F.R., Tran H.T., Johnson B.E., Heymach J.V., Mao L., Fossella F., Kies M.S., Papadimitrakopoulou V., Davis S.E., Lippman S.M., Hong W.K. The BATTLE trial: personalizing therapy for lung cancer. Cancer Discov. 2011, 1:44-53.
33. Holden S.N., Eckhardt S.G., Basser R., de Boer R., Rischin D., Green M., Rosenthal M.A., Wheeler C., Barge A., Hurwitz H.I. Clinical evaluation of ZD6474, an orally active inhibitor of VEGF and EGF receptor signaling, in patients with solid, malignant tumors. Ann. Oncol. 2005, 16:1391-1397.
34. Hanrahan E.O., Ryan A.J., Mann H., Kennedy S.J., Langmuir P., Natale R.B., Herbst R.S., Johnson B.E., Heymach J.V. Baseline vascular endothelial growth factor concentration as a potential predictive marker of benefit from vandetanib in non-small cell lung cancer. Clin. Cancer Res. 2009, 15:3600-3609.
35. Milton D.T., Riely G.J., Azzoli C.G., Gomez J.E., Kris R.T.H.M.G., Krug L.M., Pao W., Pizzo B., Rizvi N.A., Miller V.A. Phase 1 trial of everolimus and gefitinib in patients with advanced nonsmall-cell lung cancer. Cancer 2007, 110:599-605.
36. Janmaat M.L., Rodriguez J.A., Gallegos-Ruiz M., Kruyt F.A.E., Giaccone G. Enhanced cytotoxicity induced by gefitinib and specific inhibitors of the Ras or phosphatidyl inositol-3 kinase pathways in non-small cell lung cancer cells. Int. J. Cancer 2006, 118:209-214.
37. Bivona T.G., Hieronymus H., Parker J., Chang K., Taron M., Rosell R., Moonsamy P., Dahlman K., Miller V.A., Costa C., Hannon G., Sawyers C.L., NF-kappaB F.A.S. signalling modulate dependence of lung cancers on mutant EGFR. Nature 2011, 471:523-526.
38. Kim S., Domon-Dell C., Kang J., Chung D.H., Freund J.N., Evers B.M. Down-regulation of the tumor suppressor PTEN by the tumor necrosis factor-alpha/nuclear factor-kappaB (NF-kappaB)-inducing kinase/NF-kappaB pathway is linked to a default IkappaB-alpha autoregulatory loop. J. Biol. Chem. 2004, 279:4285-4291.
39. Takeuchi K., Soda M., Togashi Y., Suzuki R., Sakata S., Hatano S., Asaka R., Hamanaka W., Ninomiya H., Uehara H., Lim Choi Y., Satoh Y., Okumura S., Nakagawa K., Mano H., Ishikawa Y. RET, ROS1 and ALK fusions in lung cancer. Nat. Med. 2012, 18:378-381.